W O R K I N G P A P E R 4 2

Mineral Nutrition and Fertilization ofDeciduous Broadleaved Tree Species inBritish Columbia

Ministry of Forests Research Program

Mineral Nutrition and Fertilization ofDeciduous Broadleaved Tree Species inBritish Columbia

Ministry of Forests Research Program

Kevin R. Brown

Canadian Cataloguing in Publication DataBrown., Kevin R., Mineral nutrition and fertilization of deciduous broadleavedtree species in British Columbia. Res. Br., B.C. Min. For., Victoria, B.C. Work. Pap./

Prepared byKevin R. BrownB.C. Ministry of ForestsResearch BranchGlyn Road Research StationPO Box Stn Prov GovtVictoria, BC

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EXECUTIVE SUMMARY

There is increasing interest in the management and utilization of hybridpoplars and native deciduous broadleaved tree species (hardwoods) inBritish Columbia. This paper examines aspects of mineral nutritionand fertilization which are currently important or which may becomeimportant as management and utilization of the most importantspecies increases. Gaps in knowledge about hardwood nutrition are alsoidentified.

Maintaining nutrition to achieve the highest growth rates possible ismore critically important for the culture of hybrid poplars than of nativehardwoods. Hybrid poplars are grown under intensive managementregimes, mainly to produce pulp, with rotations of years or less. Planta-tions can be established where moisture is clearly sufficient. Under suchmanagement regimes, adequate nutrition and appropriate fertilization areessential for maximizing productivity and shortening rotations. The nutri-tion of native hardwoods is less important simply because native hard-wood species are not heavily used at present. However, much of thestanding volume of hardwood species in interior and coastal BritishColumbia is in near-mature, mature, or overmature stands. Therefore, itis prudent to assess how nutrient availability affects growth and whetherfertilization may be useful in the long-term management of hardwoodand mixed-wood stands.

Topics addressed in the review were: () the ecological roles and poten-tial growth responses of hardwood species to fertilization as comparedwith the species’ coniferous associates; () elements likely to be deficientin hardwoods; () growth responses of hardwoods to fertilization asaffected by site conditions; () effects of fertilization on stress toleranceand mycorrhizal associates; and () tactics for ameliorating elemental defi-

ciencies. Species-specific nutritional issues and operational contexts inwhich fertilization might be beneficial were also reviewed, and priorityareas for research identified.

There is a considerable body of literature on the responses to fertiliza-tion by conifers, but virtually no published field studies of hardwoodresponses to fertilization in British Columbia. While principles developedfrom studies of conifer nutrition apply to hardwoods, site-specific growthresponses to fertilization are likely much different in hardwoods than inconifers. The hardwood species of greatest importance generally predomi-nate earlier in succession on wetter and more fertile sites than do conifer-ous species. These hardwood species also typically have greater growthrates when young, shorter lifespans, and greater annual nutrient require-ments than do conifers of similar size. To achieve maximum growth rates,hardwoods may require greater quantities of nutrients than do conifersgrowing on sites of similar fertility.

Ongoing fertilization trials of hybrid poplar on Vancouver Island sug-gest that both N and P may limit growth. Growth responses may be con-siderable. A greater variety of options exist for delivery of nutrients thanexist for native hardwood stands. Intensive breeding is producing numer-ous clones that differ in their growth rates and may differ in their abilitiesto grow on nutrient- and moisture-limited sites. Important still to do are

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the following: () relating site characteristics and fertilization response; ()assessing the advantages and disadvantages of establishment-yearfertilization vs. later (rd-year) fertilization; () determining which formsof nutrients are most appropriate (e.g., organic vs. inorganic); and() predicting how clones vary in response to site fertility and to addednutrients.

Stands of native hardwoods are much less likely to be managed at thesame intensity as are hybrid poplar plantations. Virtually nothing isknown of native hardwood growth responses to fertilization in BritishColumbia, except with respect to black cottonwood in the southwesternpart of the province. It will be important to confirm what elements aredeficient, to predict how growth responses to fertilization will vary withsoil moisture and soil nutrient regimes, and to identify at what stand agesit is appropriate to fertilize in order to maximize tree value at harvest.Ongoing fertilization studies of red alder and trembling aspen may pro-vide some of this information. Studies of aspen, alder, and paper birchare of the highest priority because of their extent and potential productvalue, while studies of black cottonwood, balsam poplar, and bigleafmaple are of lower priority.

Red alder is unique among native hardwood trees in that it fixesatmospheric N2 in symbiotic association with the actinomycete Frankiasp. Fertilization trials and correlative studies of site:growth relations sug-gest that P may limit growth on some sites. Fertilization of young (- to-year-old) stands has significantly increased growth, but various studiesindicate the responses are sensitive to available soil P, soil moisture, andsoil pH. Operational contexts in which nutrition may be an importantfactor include: () plantation management on sites considered appropriatefor red alder; () management on Phellinus-infected sites that mightnormally be considered too dry and infertile for adequate growth ofalder; () management on deactivated roads and landings; and ()management of alder in repeated rotations on sites on which conifersare difficult to establish.

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ACKNOWLEDGEMENTS

For reviewing this paper, I thank Pasi Puttonen, Bob van den Driessche,Paul Courtin, Phil Comeau, Rob Brockley, Gordon Weetman, Reid Carter,Richard Kabzems, Paul Heilman, Reinhard Mueller, and Keith Thomas. Ialso thank Peter McAuliffe and Cees van Oosten for improving my under-standing of hybrid poplar culture in British Columbia. Many others gen-erously shared ideas, observations, and unpublished data that assisted mein preparing the review. Georgina Montgomery edited the manuscript.Funding for preparing and publishing the review was provided by ForestRenewal BC (projects -, -). This assistance is grate-fully acknowledged.

TABLE OF CONTENTS

Executive Summary ..................................................................................... iii

Acknowledgements....................................................................................... v

Introduction ...........................................................................................

Format of the Review ...........................................................................

Ecology of Deciduous Broadleaved Species: Site Associations,Successional Roles, and Coniferous Associates ..................................

Growth and Mineral Nutrition of Deciduous Broadleaved VS.Coniferous Species.................................................................................

Mineral Nutrients Limiting Growth....................................................

. Limiting Nutrients .........................................................................

. Deficiency Diagnosis: Critical Concentrations and ElementalRatios...............................................................................................

. Vector Analyses...............................................................................

. Elemental Form..............................................................................

. Non-Destructive Probes of Elemental Deficiencies ....................

Growth Responses to Fertilization as Affected by SiteConditions ..............................................................................................

. Regression Approaches ..................................................................

. Simulation Models .........................................................................

Tree Nutrition and the Tolerance of Moisture Stress, Frost,Herbivores, and Pathogens ...................................................................

. Mineral Nutrition and Plant Water Relations.............................

. Mineral Nutrition and Frost Damage..........................................

. Mineral Nutrition and Insect Herbivores ....................................

. Mineral Nutrition and Tree Pathogens ........................................

Fertilization and Mycorrhizae..............................................................

Amelioration of Mineral Nutrient Deficiencies .................................

. N Sources ........................................................................................

. P Sources.........................................................................................

. Frequency of Fertilization .............................................................

. Biosolids ..........................................................................................

Species-Specific Mineral Nutrition-Related Research Problems ......

. Red Alder ........................................................................................

. Black Cottonwood, Balsam Poplar, Trembling Aspen,Paper Birch, Bigleaf Maple............................................................

. Hybrid Poplars................................................................................

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Priorities for Research ..........................................................................

Conclusions ............................................................................................

Literature Cited......................................................................................

Predominant biogeoclimatic zones, soil moisture regimes (),and soil nutrient regimes () associated with the majordeciduous broadleaved tree species native to British Columbia(adapted from Klinka et al. and Massie et al. )..................

Adequate foliar macroelemental concentrations for deciduousbroadleaved species occurring in British Columbia and for relatedspecies (derived from DeBell and Radwan 1984; van den Burg1985; Fyles et al. 1994)..........................................................................

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1 INTRODUCTION

The hardwood or deciduous broadleaved1 trees considered to be of thegreatest potential economic importance in British Columbia are the nativeAlnus rubra (red alder), Acer macrophyllum (bigleaf maple), Populustrichocarpa (black cottonwood), Populus tremuloides (trembling aspen),Populus balsamifera (balsam poplar), Betula papyrifera (paper birch), andhybrid poplars, primarily clones of P. trichocarpa × P. deltoides. Red alder,bigleaf maple, and black cottonwood occur mainly in coastal BritishColumbia, while trembling aspen and balsam poplar occur primarily inthe Interior. Paper birch occurs in both regions. Hybrid poplars are beingincreasingly planted on the east side of Vancouver Island and in theFraser Valley and, to a lesser extent, in the Interior.

Historically, native hardwoods have been an insignificant componentof the British Columbia forest economy, though not of the forested land-scape. It has been estimated that the harvestable area with significant vol-umes of hardwood species is about . × 6 ha, most of which containstrembling aspen occurring in the northern interior of the province. Thepotential annual harvest is × 6 m3 (Massie et al. ), i.e., –% ofthe total annual forest harvest in British Columbia (B.C. Ministry ofForests ). Native hardwood species are therefore important for main-taining future fibre supplies from British Columbia forests. Species suchas maple, birch, and alder are also desirable for the manufacture of high-value products such as veneer and furniture (Massie et al. ; Raettig etal. ). Demand has increased for chips and sawn wood products fromnative British Columbia hardwoods in recent years, in conjunction withdecreases in the coniferous-dominated land base available for harvestingand with continued high world-wide demand for fibre.

A significant percentage of interior cottonwood, aspen, and birch isconsidered mature or overmature, while most of the volumes of red alderand bigleaf maple are near-mature or mature (Massie et al. ). Long-term supplies of native hardwoods may therefore be of concern. Similarly,concerns have been expressed over the diminishing quantity and qualityof alder logs in Oregon and Washington, as demands for products fromalder increase internationally (Raettig et al. ). In general, understand-ing how to maximize both productivity and log quality, while minimizingenvironmental impact, are important silvicultural research goals for nativehardwoods.

Hybrid poplars have been increasingly planted on private lands, mainlyin coastal British Columbia, as a fast-growing source of fibre for pulp.Rotations are expected to be less than years. Understanding how tomaximize juvenile productivity is a key to the economic viability ofhybrid poplar culture, but issues such as log quality are of little concern.

My objectives in this assessment were to review existing knowledge andto suggest research directions pertaining to the nutrition and fertilizationof native hardwoods and hybrid poplars. Growth responses to changes innutrient supply and nutrient status were emphasized. Other important

Throughout this document, “hardwood” and “deciduous broadleaved” are used interchangeably.

aspects of fertilization and hardwood nutrition, such as the economics offertilizing hardwoods, within-stand and within-tree nutrient cycling, andthe impacts of fertilization on ecosystem components other than targettrees, are not addressed in this review. Hardwood ecology and manage-ment in British Columbia have been recently reviewed (Peterson et al.; McLennan and Mamias ; Peterson and Peterson ; Simardand Vyse ; Enns et al. ; Massie et al. ; Comeau et al. ),but nutritional concerns have generally been ranked as a low priority(e.g., McLennan and Mamias ).

Understanding the role of nutrition in maintaining or increasing pro-ductivity and the value of forested stands is important for several reasons:

• The growth potential of vegetation in natural environments is oftenlimited by a low availability of one or more mineral nutrients (Ericssonet al. ) even when other factors, such as moisture, also limitgrowth. There are no conclusive data to suggest otherwise for BritishColumbian forests, although the responses to added nutrients areaffected by the moisture available (Carter et al. ).

• Nutrient deficiencies can be minimized in a cost-effective manner whenfertilization is used appropriately in combination with soil conservationand with the control of competing vegetation.

• An improvement in growth rates resulting from appropriate nutrientadditions may decrease the time until a new stand is free-to-grow andmay also reduce the age required for trees to reach minimum harvest-able sizes. These changes may increase short-term or mid-term timbersupplies (e.g., Pederson a, b) and increase allowable annual cuts() per unit of available land area. For instance, fertilizationincreased basal area of coastal Douglas-fir by % relative to controlsover years (Weetman et al. ). In that study, the site index(-year base) was increased from to m. Growth simulations pro-jected an additional m3 ha-1 over the rotation if the increasedgrowth rates could be maintained.

• Fertilization, properly timed and applied in conjunction with other sil-vicultural treatments, may increase product value in addition to growthrates. For example, an increase of cm diameter in loblolly pine follow-ing fertilization can increase the value by –% m-3 simply by increas-ing the proportion of wood suitable for higher-valued products (Bink-ley et al. ). This may be an important consideration for hardwoodsused in the production of veneers and other value-added products.

Before maximum growth responses to fertilization can be obtained:() the elements that limit productivity in a given species on a given sitemust be correctly diagnosed, () the relation between site and stand char-acteristics and growth response to the added elements must be under-stood, and () the limiting elements must be applied in an appropriateform and at an appropriate time. In recent years, much of that informa-tion has become available for commercially important coniferous speciesin British Columbia, particularly coastal Douglas-fir (Weetman et al. ;Carter et al. ). Such information is not easily applied to hardwoodspecies, however. In particular, the quantities of mineral nutrients

required for maximum growth may differ among hardwood species andtheir coniferous associates, as well as among hardwood species. In general,the dominant native hardwoods of British Columbia are early successionaland most prominent on moister, more fertile sites (Klinka et al. ),compared with their coniferous associates. Potential growth rates of nativehardwoods may be greater (and rotations shorter) than those of theirconiferous associates, but the greater growth rates may also require greaterirradiances and availabilities of moisture and mineral nutrients. Annualnutrient uptake requirements may also be greater in deciduous hardwoodsbecause the entire canopy is replaced annually and the percentage ofgrowth-enhancing elements supplied by retranslocation from senescingtissue is typically lower than in evergreen conifers (Cole and Gessel ).Thus, site fertility considered adequate for the growth of coniferousspecies may limit the growth of hardwoods naturally occurring on thesame site.

2 FORMAT OF THE REVIEW

In this paper, ecological roles, site associations, and coniferous associatesof the major hardwood species native to British Columbia are consideredfirst. This is followed by a discussion of general questions concerningmineral nutrition and fertilization that will likely be important in thefuture management of native hardwoods and hybrid poplar:

. How do the responses of native hardwoods to fertilization comparewith those of their coniferous associates?

. What, if any, mineral nutrients limit productivity on a given site? Howcan deficiencies be diagnosed?

. What growth responses can be expected from increased nutrientavailability? How will those responses be influenced by site and standcharacteristics?

. Will changes in the nutrient status of an individual tree affect theresistance to, or recovery from, abiotic stresses such as limited moistureavailability and low temperatures, or biotic stresses associated withpathogens or herbivorous insects?

. What are the most effective fertilization tactics for alleviating nutri-tional deficiencies?

Finally, relevant nutritional data and nutritional issues for each species,including hybrid poplars, are discussed.

An initial review of the literature revealed no published field studies ofthe relations between growth and mineral nutrition of red alder, paperbirch, trembling aspen, balsam poplar, bigleaf maple, or hybrid poplar inBritish Columbia. As appropriate, I have summarized recent unpublisheddata from studies conducted in British Columbia, reviewed studies of therelevant species or genera conducted elsewhere, and reviewed relevantnutrition and fertilization studies of native conifers conducted in or nearBritish Columbia.

3 ECOLOGY OF DECIDUOUS BROADLEAVED SPECIES:SITE ASSOCIATIONS, SUCCESSIONAL ROLES, AND CONIFEROUSASSOCIATES

The native hardwoods of British Columbia are mainly seral species,usually dominating stands early in succession and eventually being over-topped by slower-growing conifers. Each of the major hardwood speciesoccurs in one or more biogeoclimatic zones (Klinka et al. ). All of themajor species occur primarily on rich to very rich sites. Balsam poplar,black cottonwood, and bigleaf maple occur primarily on moist sites, whilepaper birch occurs primarily on fresh sites. Aspen occurs commonly onboth fresh and moist sites, while red alder may commonly occur in sitesranging from fresh to wet (Klinka et al. ) (Table ). In general, agiven deciduous broadleaved species is associated with richer sites thanare the coniferous species that occur frequently within that zone.

4 GROWTH AND MINERAL NUTRITION OF DECIDUOUSBROADLEAVED VS CONIFEROUS SPECIES

No published data exist comparing the effects of fertilization on decidu-ous broadleaved trees with the effects on their coniferous associates oncommon sites in British Columbia. However, deciduous broadleavedspecies are often more responsive to nutrient additions than are conifers,at least when young. Greater growth responses may result from greaterplasticity of biomass allocation to foliage (e.g., Chapin et al. ), andbecause photosynthetic rates increase more with nutrient availability(Reich et al. ; Brown et al. a). Although both broadleaved and

Predominant biogeoclimatic zones, soil moisture regimes (SMR), and soilnutrient regimes (SNR) associated with the major deciduous broadleaved treespecies native to British Columbia (adapted from Klinka et al. 1990 andMassie et al. 1994). Rankings of SMR and SNR are based on a total of 26species characterized: a ranking of 1 indicates an association with the driestor least fertile sites, while a ranking of 26 indicates species most commonlyassociated with the wettest or most fertile sites.

Soil moisture Soil nutrientSpecies BGC Zone regime regime

Red alder CDF, CWH fresh to wet () rich to very rich ()Bigleaf maple CDF, CWH moist () very rich ()Black CWH, CDF, ICH, moist () very rich ()

Cottonwood SBSBalsam poplar BWBS, SBS, SWB moist () very rich ()Birch SBS, BWBS, ICH, fresh () medium to rich ()Aspen BWBS, SBS, ESSF, fresh to moist () medium to rich ()

SBPS, IDF, ICH

coniferous species exhibit indeterminate patterns of shoot growth in theseedling stage (Kramer and Kozlowski ), species of many broadleavedgenera—including Populus (Critchfield ), Acer (Critchfield ), Alnus(Oliver and Larson ), and Betula (Kozlowski and Clausen )—continue to exhibit indeterminate shoot growth after the seedling stage.These genera may respond more rapidly to fertilization than do conifers(Linder and Rook ). Early successional forest habitats typically exhibita greater availability of resources, including nutrients, than do later-successional habitats. Plants associated with those early successional habi-tats exhibit greater maximum growth rates as nutrient availabilityincreases (Grime ; Chapin ). This response is more difficult togeneralize for trees than for herbaceous plants because tree species maydiffer in their patterns of age-related growth rates (data cited in Green-wood ). In comparative studies of responses to increasing N and Pavailability, maximum relative growth rates or whole-plant masses ofpoplar, birch, and alder seedlings were greater than those of pine orspruce seedlings as N or P availability increased (Ingestad ; Chapin etal. ; Jia and Ingestad ; Ingestad and Kahr ; Brown and Hig-ginbotham ). Thus, while growth rates may have been similar atlower nutrient availabilities, the deciduous broadleaved species requiredgreater nutrient availabilities for maximum growth.

5 MINERAL NUTRIENTS LIMITING GROWTH

Nutritional deficiencies are most conclusively identified through field fer-tilization studies (Binkley ). At present, black cottonwood (McLennan), trembling aspen,2 and red alder3 are the only native hardwood treespecies that have been, or are being, subjected to fertilization trials inBritish Columbia. Several field studies of N and P fertilization effects onhybrid poplar growth are underway or recently completed on eastern Van-couver Island, as discussed below.

Ongoing field fertilization trials on Vancouver Island indicate that Nand P deficiencies may limit the growth of hybrid poplar (data containedin van den Driessche ; van den Driessche []), while deficiencies ofP and other non-nitrogenous elements may limit the growth of red alder.4

Nitrogen availability commonly limits the growth of conifers in BritishColumbia. While N is often limiting, erratic responses to N fertilizationhave been attributed to deficiencies of P, S, B, Fe, and Cu either inherentin the particular site or induced by N fertilization (e.g., Weetman et al.a,b; Brockley , , , ; Carter and Brockley ; Majidand Ballard ; Brockley et al. ; Weetman et al. ; Green andCarter ; Brockley and Sheran ; Carter et al. ). Potassiumdeficiencies have not been reported in native trees in British Columbia;

Dave Coopersmith, poster presented at “Silviculture of Temperate and BorealBroadleaf-conifer Mixtures” Workshop, February –March , , Richmond, B.C.; pers.comm., November .

Kevin Brown, B.C. Min. For. EP ., . Brown, unpubl. data, EP ., EP ., EP ..

5.1 LimitingNutrients

however, deficiencies of K in Douglas-fir were induced by N fertilizationin northern Idaho and western Montana (Mika and Moore ). Thedeficiencies were more pronounced over granitic parent materials thanover basaltic parent materials (Moore and Mika ).

Optimal elemental balances in foliage are broadly similar in seedlingsof a broad range of tree species, although the optimal balances of K, Ca,and Mg may be higher in deciduous broadleaved species than in conifersunder optimal nutrition (Ingestad ). Why this is so is unclear, butdeciduous broadleaved trees have a greater capacity to assimilate NO3-Nin foliage than do conifers (Smirnoff and Stewart ; Knoepp et al.). The greater uptake rates of cations may be associated with uptakeand assimilation of NO3-N. Deciduous broadleaved species may bebroadly predisposed to deficiencies of the same elements that limit conifergrowth on a given site, but greater elemental requirements in hardwoodsindicate they may be more prone to deficiencies on a given site.

Diagnoses of nutrient deficiencies in trees typically rely on publishedfoliar concentrations associated with growth. Critical concentrations,defined variously as the lowest foliar elemental concentrations associatedwith maximum or near-maximum growth (see Timmer ), have notbeen developed specifically for hardwood species in British Columbia. Thedata that have been published (Table ) are much less complete than arethose compiled for native conifers (e.g., Ballard and Carter ) and theyare extremely variable. Nonetheless, foliar concentrations of macroele-ments considered “adequate” appear higher than for those in associatednative conifers (Ballard and Carter ). Toxic levels of essential elementsare largely unknown. However, one study reported that foliar damageascribed to boron toxicity occurred at lower foliar concentrations of B inbigleaf maple than in digger pine, California laurel, or madrone (Glaubigand Bingham ).

Applying critical concentrations is problematic. Critical foliar elementalconcentrations associated with growth reductions may: () vary within aspecies; () decrease with increasing age of the tree, at least in coniferousspecies (Miller et al. ); or () vary with the availability of otherresources such as moisture (Lambert ) or mineral nutrients otherthan the one of interest. It is assumed that if foliar elemental concentra-tions are less than previously published critical concentrations, the treesin question will respond to additions of those elements. However, an ele-ment thought to be deficient may be less deficient than other elements, inwhich case additions of the former will not increase growth. Conse-quently, foliar elemental concentrations may be combined with ratios ofelements, such as N/P, N/K (Mika and Moore ), or N/S (Ballard andCarter ).

A diagnostic approach that relies solely on elemental ratios is the Diag-nosis and Recommendation Integrated System (), which uses multi-ple two-way comparisons of foliar elemental ratios with establishednorms (Timmer ). Index values, based on elemental ratios, are calcu-lated for each element of interest in foliage. The indices are comparedwith indices developed for plants growing under optimal conditions, andthe relative deficiency of a given element is then estimated. The data setused for generation of the indices should be compiled under conditions

5.2 DeficiencyDiagnosis: Critical

Concentrations andElemental Ratios

(e.g., irradiance, humidity, soil moisture) representative of those to which will be applied. It is also important to know what elemental concen-trations are associated with maximum growth. The basic data require-ments are therefore as great as those required for determination of criticalconcentrations. has been applied to nutritional studies of hybridpoplars in Ontario (Leech and Kim ) and to field studies of black cot-tonwood in southwestern British Columbia (McLennan ), but thereare no records in the literature of its application to other deciduousbroadleaved trees in the province.

In contrast to the above approaches, foliar vector analysis combinesmeasures of elemental concentration and foliar mass responses to treat-ments. In its most common form, changes in the concentration of theelements of interest are plotted against changes in content (the product

Adequate foliar macroelemental concentrations for deciduous broadleavedspecies occurring in British Columbia and for related species (derived fromDeBell and Radwan 1984; van den Burg 1985; Fyles et al. 1994).

Species Element Concentration (%)

Acer macrophyllum ?Acer saccharum N 1.6 –2.6

P 0.13 –0.20K 0.6 –0.7Ca 0.7 –0.9Mg 1.0 –1.3

Alnus rubra N 1.79 –3.16P 0.15 –0.21K 0.89 –0.99

Betula papyrifera N 1.62 –1.79P 0.19 –0.32K 0.94 –1.45Ca 0.99 –1.07Mg 0.25 –0.30

Populus balsamifera N 2.5 –2.6P 0.19 –0.24K 1.15 –1.45Ca 0.43Mg 0.21 –0.29

Populus tremuloides N 2.1 –2.8P 0.15 –0.30K 0.77 –1.56Ca 1.25 –2.76Mg 0.14 –0.31

Populus trichocarpa N >2.5P 0.10 –0.44K 0.44 –1.76Ca 1.44 –2.14Mg 0.22 –0.37

5.3 Vector Analyses

of elemental concentration and mass of a standardized number of leavesduring the growing season following fertilization). Deficient elements arethose whose concentration and standardized leaf mass both increase inresponse to a treatment (i.e., leaf mass is limited by that element).Recently, it has been suggested that changes in elemental concentration beplotted against changes in leaf mass, with the responses of elements thathave been added plotted separately from those that have not been added(Valentine and Allen ; Brockley and Sheran ). The major advan-tages of the vector approach are that it facilitates tentative diagnosticinterpretations about the nutritional status of foliage with respect to bothadded and non-added nutrients and allows simultaneous comparisons ofseveral nutrients, sites, or treatments.

The vector analysis technique has most commonly been applied toconifers with determinate patterns of shoot elongation (i.e., those inwhich needle numbers on a shoot are predetermined the preceding fall).Increases in needle mass have been correlated with subsequent increasesin basal area increment (Weetman et al. ). The technique has alsobeen applied with variable success to species with indeterminate shootelongation. In studies of hybrid poplar responses to liming and P fertiliza-tion during the establishment year (Timmer ; Teng and Timmer), vectors were developed from foliar data collected from the entirestem. In another study, van den Driessche [] used newly expandedleaves along the stem. In western hemlock, Weetman et al. (b)assumed that fertilization did not affect needle numbers on the sampledlateral shoot5; in western redcedar, entire branchlets were sampled. Theproblem with the latter was that branchlet mass was not well correlatedwith height increment (Weetman et al. b). Likewise, McLennan ()found little correlation between foliar mass on the terminal shoot andeither height or basal area increment in fertilization studies of black cot-tonwood. In contrast, areas of newly-mature individual leaves were closelycorrelated with 1st- and 2nd-year stem growth in hybrid poplars (Harring-ton et al. ; van den Driessche []), as did whole-plant leaf area(Larson and Isebrands ; Hinckley et al. ; Brown et al.6). Populustrichocarpa (Critchfield ), P. tremuloides (Kozlowski and Clausen ;Pollard ), B. papyrifera (Kramer and Kozlowski ), and A. rubra(Oliver and Larson ) all exhibit indeterminate shoot elongation.Shoot elongation patterns of Acer spp. vary with the species (Critchfield), but those in A. macrophyllum have not been described. Further-more, the percentage of shoots exhibiting indeterminate growth on agiven tree may decrease with age (Kramer and Kozlowski ). The vec-tor analysis technique deserves further attention as a means of detectingelemental deficiencies in deciduous broadleaved species. Consideration ofthe type of growth exhibited by the shoot sampled should be taken intoaccount, and long-term measurements should be made to relate the mag-nitude of stemwood growth response to leaf size increases.

Note: Kramer and Kozlowski () cite data from Owens and Molder () indicatingthat western hemlock exhibits determinate growth.

K.R. Brown, F.D. Beall, and G.D. Hogan. Biomass accumulation in hybrid poplars duringthe establishment year. Unpubl. manuscript. Can. For. Serv., Sault Ste. Marie, Ont.

Alternatives to measuring total concentrations of elements in foliage havebeen suggested in the literature. One is to combine the elemental determi-nations with determinations of chlorophyll concentrations (Oren et al.). A second is to measure concentrations of specific forms of ele-ments, for example, inorganic P as a measure of P status (Sun et al. ),NO3-N or specific amino acids and amides as an indicator of relative Nstatus (Nasholm and McDonald ), SO4–S as a measure of S status(Turner et al. ), and active-Fe (that Fe extracted with dilute acids orchelators) as an indicator of Fe status (DeKock et al. ). A lack ofSO4–S has been related to a lack of growth response to N fertilization inseveral coniferous species (Ballard and Carter ). Active-Fe is thoughtto be of the form Fe(II), as opposed to Fe(III). Although neither the com-position nor the cellular location are conclusively known (Abadia ),active-Fe is often a better indicator of Fe deficiency, especially in plantsgrown in calcareous soils or subject to high availabilities of P (Marschner). In general, vacuolar concentrations of elements (or the elementalforms that accumulate in the vacuoles) may be the best indicator ofrelative status of elements because they represent an accumulation of anelement in excess of immediate needs for growth (Chapin and vanCleve ).

The difficulties in extraction and quantification of labile forms ofelements may negate their advantages as diagnostic tools, although theymay be easier to extract from deciduous hardwood foliage than fromconiferous foliage. In Douglas-fir, concentrations of soluble N com-pounds showed greater changes in response to increased N availabilitythan did total N. However, analytical precision was less for soluble Ncompounds than for total N, possibly because of a greater sensitivity totemperature and moisture stress (van den Driessche and Webber ). Inbirch seedlings, the ratio of amino acid-N (mainly citrulline, glutamine,y-aminobutyric acid, and arginine) to total N increased with N supply(Nasholm and McDonald ). However, soluble N compounds werenot a more sensitive predictor of growth response to N fertilization thanwas total foliar N in sycamore plantations (Tschaplinski and Norby ).At this time, including measures of SO4–S in routine foliar nutrient analy-ses for native broadleaved species, as recommended for conifers (Ballardand Carter ; Weetman and Wells ), seems reasonable. Active-Femight be a useful measure of Fe deficiency in those species occurring incalcareous soils.

Procedures for the collection of foliage and its analysis for total elementalconcentrations are well established for trees, including deciduous broad-leaved species (e.g., Weetman and Wells ). The preparation of tissuesamples to determine elemental concentrations is labour-intensive, timeconsuming, and expensive. It remains a major impediment to routinescreening of vegetation for elemental deficiencies. Alternative approachesfor this assessment are therefore of interest.

The spectral characteristics of tissue may have promise for indicatingnutrient stress (Powers ). In contrast to traditional wet chemistrytechniques, there is no need to determine sample masses, no reagentsare required, and the analytical time is relatively short. Near-infraredreflectance spectroscopy () has been used with some success for

5.4 Elemental Form

5.5 Non-DestructiveProbes of Elemental

Deficiencies

estimating foliar concentrations of Kjeldahl-N and organic constituentssuch as lignin and proteins, occurring in concentrations greater than .%(dry mass) (Westerhaus cited in Wessman et al. ) in tissues thatwere dried and ground. However, deficiencies of Ca and P were difficultto detect (data cited in Wessman et al. ). The technique may be mosteffective in assessing specific elemental deficiencies if one or very fewdeficiencies predominate. Measurements of other compounds may indi-cate whether a plant is under stress, for example, by showing a shift inthe ratios of N, lignin, carbohydrates, and protein (Waring et al. ).

Remote sensing of plant stress associated with elemental deficiencieswould be particularly useful in assessing limitations to productivity in thewidespread forested areas of British Columbia. There is some evidencethat nutritional changes in the canopy can be detected by remote sensingtechniques. For example, reflectance in the visible red spectrum decreasedand that in the near-infrared region () increased with increasing ratesof N application (Al-Abbas et al. ). Laser-induced fluorescence () isa non-destructive technique that may have some promise for use in iden-tifying elemental deficiencies as part of remote sensing surveys. In onestudy, deficiencies of N, P, and Fe decreased fluorescence at one wave-length, while a deficiency of K caused a three-fold increase at the samewavelength (Jackson ).

There are numerous problems in obtaining interpretable foliar nutri-tion data from airborne sensors, ranging from problems in analyzing freshintact leaves to problems in scaling from individual leaves to canopies.The analysis of fresh intact leaves may be more difficult than that ofdried, ground tissue because: () the waxy cuticle of leaves may causehigh specular reflectance, () the distribution within leaves of chloroplastsand of compounds associated with nutrient status (e.g., pigments, pro-teins) is not uniform, and () the high absorbance by water of infraredradiation and the presence of air and water interfaces with varied refrac-tive indices may obscure variation in absorption associated with bio-chemical changes (Yoder and Pettigrew-Crosby ). Problems in scalingfrom individual leaves to canopies include the difficulty in accounting forvarying leaf area index (), which alters the contribution of the back-ground to overall reflectance and affects the scattering of light (Yoder andPettigrew-Crosby ). In addition, other stresses (e.g., moisture stress)may influence canopy reflectances by affecting leaf reflectance, leaf orien-tation, and canopy architecture (Jackson ). While problems clearlyexist, it is worth noting that N concentrations of fresh tissue have beenpredicted from reflectance data, with the use of shortwave infraredbands (data cited in Yoder and Pettigrew-Crosby ). As well, canopyN concentrations have been predicted from Airborne Visible /InfraredImaging Spectrometer () data in forests in Massachusetts, Wiscon-sin, and Oregon (Martin and Aber and Johnson et al. , bothcited in Yoder and Pettigrew-Crosby ). Remote sensing techniquesmay have long-term applicability in assessing health and nutrition ofBritish Columbia forests, whether those forests are dominated by conifer-ous or deciduous broadleaved trees. The techniques deserve furtherattention.

Appropriate measurements of photosynthesis may provide an assess-ment of elemental deficiencies. Photosynthetic rates of trees have been

associated with foliar concentrations of numerous elements, including N(Field and Mooney ; Reich et al. ), P (Conroy et al. ;Raaimakers et al. ), and Mg, S, Fe, Mn, Cu, and Zn (see reviews byLinder and Rook ; Marschner ). Because photosynthetic rates arealso limited by factors such as moisture availability, CO2 fixation ratesalone appear to be of little use in indicating any elemental deficiencies, letalone specific deficiencies. However, patterns of chlorophyll fluorescencemay vary with changes in the concentration of those elements associatedwith specific components of the light harvesting and electron transportreactions—elements such as Mn, Mg, Fe, and Cu (Kriedemann et al. ;Baillon et al. ; Fodor et al. ; Gorge et al. ). Phosphorus defi-

ciencies may be inferred by fluorescence patterns and by the response ofphotosynthetic rates to increasing internal CO2 concentrations (Conroyet al. ). The utility of photosynthetic probes in identifying nutrientdeficiencies should be tested in well-designed experiments under fieldconditions.

6 GROWTH RESPONSES TO FERTILIZATION AS AFFECTEDBY SITE CONDITIONS

Some minimum level of irradiance, soil moisture, and temperature mustbe reached before fertilization can increase tree growth (e.g., Brockleyet al. ; Chappell et al. ), but fertilization may increase tree growtheven when factors other than nutrient availability are less than optimal(e.g., Brix ). Attempts to relate site conditions to fertilizer responsefor a given species have not always been successful because site conditionsare difficult to quantify in a manner meaningful for the understanding oftree growth. Characteristics of the site may affect nutrient availability ornutrient utilization. Nonetheless, the ability to select responsive standsand to predict the magnitude of the response to fertilization has impor-tant implications for the economic viability of fertilization programs. Todate, black cottonwood is the only deciduous broadleaved species nativeto British Columbia in which such relationships have been examined(McLennan ).

Most attempts to relate site conditions to fertilization response have usedregression approaches. In British Columbia, such attempts have beenconfined to studies of Douglas-fir (e.g., Carter and Klinka ; Carter etal. ). Site index was correlated with both continuous variables(mineralizable-N, site moisture balance) and categorical variables (soilmoisture regime and soil nutrient regime), as defined in the biogeo-climatic ecosystem classification. Carter and Klinka () concludedthat the continuous variable model was not as portable as the categoricalvariable model, primarily because of difficulties in applying the water bal-ance model used. Later analyses showed that rd- and th-year relativebasal area responses generally decreased with increasing mineralizable-N,with increasing moisture deficit, and with increasing site index. However,large increases occurred on sites of high site index with low soil mineral-izable N concentrations, low foliar N concentrations, adequate foliar P

6.1 RegressionApproaches

concentrations, and an absence of soil moisture deficits. These sites wereidentified as having the greatest potential economic gains fromfertilization.

In Washington and Oregon, the relative response of Douglas-fir to Nfertilization decreased linearly with increasing foliar N concentration ofunfertilized trees at a range of sites (Hopmans and Chappell ). FoliarN was a better predictor of response to N fertilization than was soil Nconcentration or C/N ratio. Miller et al. () attempted to predictperiodic annual increment in Douglas-fir stands in Oregon fertilized witheither or kg N ha-1, using a combination of stand variables(-year site index, age at breast height, relative density), site and climaticvariables (average annual precipitation, solar radiation, effective soildepth, available water-holding capacity), and soil variables (anaerobicallymineralized N, total N, organic matter). An initial core equation incorpo-rated stand variables known to be relevant predictors of growth andresponse; the stepwise procedure thereafter was based on ease and cost ofmeasurement (soil test variables went in last). Core equations predictedthe growth of unfertilized stands, but not fertilizer response. The bestadditional variable was surface soil C/N. The lack of effect from site vari-ables suggested that the effects of site were already incorporated intostand variables. In other studies, incorporation of S/N improved predic-tions of growth responses to fertilization in Douglas-fir (Blake et al.), and initial foliar concentrations of SO4–S improved predictions ofgrowth responses in lodgepole pine (Brockley ).

Findings from studies of Douglas-fir have suggested a number of vari-ables that might be used to identify which stands are likely to be respon-sive to fertilization. Other species have not been similarly examined.However, site factors have been related to site index in western hemlock(Kayahara et al. ), Sitka spruce (Kayahara and Pearson ), lodge-pole pine and interior spruce (Wang et al. ), and red alder (Courtin) in British Columbia, and in red alder in Washington and Oregon(Harrington and Curtis ).

The studies highlight the difficulties in using site classification schemessuch as soil nutrient regime () (Kabzems and Klinka a) to predictthe growth (and the growth response to fertilization) of different species.For example, the site index of western hemlock increased as increased from very poor to poor, but did not increase further in mediumand rich sites, even though mineralizable soil N increased (Kayahara andPearson ). Site index of Douglas-fir, in contrast, increased as sincreased from medium to rich to very rich (Kabzems and Klinka b).Site indices of interior spruce were lower than those of lodgepole pine insites classified as nutrient-poor, but higher than those of lodgepole pinein sites classified as nutrient-rich. The site index of red alder increasedwith site productivity class for Douglas-fir, but the highest site indices forred alder were on sites considered unsuitable for growing Douglas-fir(Harrington and Curtis ). The poor relationship between red aldersite index and Douglas-fir site productivity class was attributed to differ-ent requirements for mineral-N and differences in the growth of the twospecies on wetter and drier sites. Similar principles might apply to otherhardwood associates of Douglas-fir that also do not fix N2. If site classifi-

cation is associated primarily with nutrient supply rate, a species with

greater requirements for nutrient uptake would be nutrient-limited(hence, more responsive to fertilization) in a more productive site classthan would a species with lesser requirements (Binkley ).

If improving the productivity of hardwoods is important, then there isa pressing need to understand species-specific responses to fertilization, torelate these responses to site classification systems, and to refine soil fertil-ity classifications. For operations, it is important to be able to identify ele-ments that are deficient and to predict growth responses to fertilizationacross the range of soil moisture regime and soil nutrient regime combi-nations occupied by a given species. To this end, a well-replicated set offertilization trials should be established in a range of site series or siteassociations within a given biogeoclimatic zone, since these provide theecological framework for silvicultural prescriptions. Additional measure-ments relating to site characteristics (e.g., pH, nutrient and moistureavailability) would be required, because the native hardwoods may exhibita wide range of productivities over sites classified as rich to very rich(e.g., Courtin ). In addition, appropriate detailed growth and physio-logical measurements (e.g., plant moisture status) may be necessary if weare to understand why responses to nutrient addition vary with site series,as discussed below.

Moisture availability and nutrient uptake and utilization are linked.Low soil moisture contents may reduce the effective diffusion coefficientof elements in the soil solution, and plant moisture stress may reducetranspiration rates and the permeability of roots, thereby reducing themass flow and uptake of elements. Water stress reduces the uptake of Caand Mg less than that of N, P, and K (Sands and Mulligan ), and theuptake of B is sharply reduced under moisture stress (Marschner ).Although N uptake may be reduced by drought, in one study, moisture-stressed individuals of six clones of Populus deltoides had higher foliarN concentrations than did control plants (Broadfoot and Farmer ),possibly indicating that N uptake was less affected by water stress thanwas plant growth.

Fertilization with P increased the growth of red alder more in water-logged or relatively dry soils than in well-drained soils with optimalmoisture contents (Radwan and DeBell ). Likewise, fertilization withP had a greater effect on the growth of hybrid poplars under mild waterstress than on those trees that were well irrigated (DeBell et al. ).Greater responses to P fertilization by water-stressed trees may indicatethat () higher P supply rates are needed to maintain P uptake andadequate tissue concentrations of P when moisture is not at optimallevels, () increasing P supply is associated with increased rooting andmoisture availability, or () increasing tissue P concentrations are associ-ated with greater water use efficiency.

The effects of stand and site conditions on yield responses to nutrientadditions may eventually be best understood through the use ofphysiologically based growth models, such as (McMurtrie et al.; McMurtrie ) and (Host et al. ).

simulates the carbon and water balance of trees in relation totheir mineral nutrition, and therefore requires the collection of meteoro-logical, stand, and site data (e.g., soil moisture characteristics) and the

6.2 SimulationModels

determination of photosynthetic responses to light and CO2 as affected byfoliar elemental concentrations. Canopy net photosynthesis is calculated asa function of: () the proportion of foliage in each of three canopy layersexposed to direct and diffuse radiation, and () the quantum yield andlight-saturated rates of photosynthesis in each of the canopy layers.Stomatal conductance is estimated as a function of photosynthetic rate,humidity, and atmospheric CO2, and is assumed to decline when soilwater content declines to a threshold value. Values of photosynthetic para-meters and partitioning coefficients are considered to be a function offoliar elemental concentrations. To apply the models, the relationships offoliar elemental concentration to biomass allocation and photosyntheticcharacteristics will likely have to be determined for a given species (e.g.,Brown et al. a,b). Such data do not currently exist for deciduousbroadleaved species occurring in British Columbia.

, developed for hybrid poplars, estimates growth during theestablishment year. Growth is simulated as a function of photosynthateproduction, based on light interception and photosynthetic responses tolight by individual leaves, photosynthetic and respiratory responses totemperature, and the partitioning of photosynthate as a function of leafdevelopment. The initial versions of the model could not simulatebranching and did not incorporate the effects of moisture or nutrientstress on photosynthesis or partitioning of photosynthate. Submodels ofroot growth and stomatal responses to moisture and nutrient stress andsubroutines to incorporate branching were planned as the next majordevelopment in the model.7

Light interception, which is strongly influenced by leaf and branch dis-tribution and growth, is recognized as a major determinant of tree pro-ductivity. In hybrid poplars, the amount of sylleptic branching maycorrelate with tree biomass (Ceulemans et al. ), presumably throughits effects on light interception. Sylleptic branching may vary with clone(Ceulemans et al. ) and with nutrient availability.8 Chen et al. ()presented a fractal-based canopy structure model for estimating lightinterception in hybrid poplar plantations. Such an approach might beuseful in assessing the effects of nutrition on growth of different clones ofpoplar after the establishment year.

Use of the above models requires the collection of considerable data. Todetermine site characteristics, appropriate measurements must be made ofphoton flux densities, temperatures, and moisture and nutrient availabil-ity; determining plant characteristics requires the gathering of biomassand appropriate morphological (e.g., leaf and branch growth patterns)and physiological (gas exchange, water relations, photosynthate allocation)data. However, as the relationships between plant nutrition and physio-logical processes underlying growth responses become better understood,this process-based approach may ultimately provide the best way of pre-dicting growth responses to fertilization. With respect to hybrid poplarmanagement, the use of models such as may be valuable inmatching specific clones with specific sites. To make these approaches

George Host, University of Minnesota-Duluth, pers. comm., May . Brown, unpubl. data, .

usable operationally, it will be necessary to accumulate key physiologicaldata for the variety of clones likely to be used in operational plantings.It will also be necessary to minimize the amount of site data required tosimulate growth.

7 TREE NUTRITION AND THE TOLERANCE OF MOISTURE STRESS,FROST, HERBIVORES, AND PATHOGENS

While the availability of water may affect nutrient uptake and tree growthresponses to fertilization, tree water relations and tolerance of moisturestress may, in turn, be affected by tree nutrient status. Radiata pine fertil-ized with N had less negative shoot water potentials (implying less waterstress) than did unfertilized trees (Carlysle ). A similar response,though less pronounced, was observed in Douglas-fir (Brix and Mitchell). Roots in nutrient-deficient soil may be less effective at water uptakebecause of reduced root conductivity (Sands and Mulligan ). Higherfoliar N concentrations may increase tissue elasticity (Tan and Hogan) and increase photosynthetic rates and water use efficiency (Mitchelland Hinckley ; Brown et al. a). However, increases in leaf arearelative to root area could predispose the plant to increased water stressand offset an increase in leaf-level water use efficiency.

In studies of four clones of hybrid poplar, high rates of P additiondecreased vessel pit pore diameters and cavitation when drought stresswas imposed, whereas high rates of N addition increased vessel diameterand cavitation (Harvey ; Harvey and van den Driessche ). Highrates of N addition also increased water use efficiency prior to droughtingand increased osmotic adjustment after droughting (Harvey ).

The severity of frost damage to trees may be associated with the nutri-tional status of the tree and hence be affected by fertilization. The rela-tionship, however, has not been studied in deciduous broadleaved treesin British Columbia and is poorly understood in other species. In general,high tissue concentrations of N and P may be associated with delays inthe onset of dormancy, leading to greater damage from late-season frosts,but fertilization after active growth has ceased may reduce frost damage(van den Driessche ). Nitrogen fertilization increased needle frost har-diness of red spruce seedlings, but decreased frost hardiness of the bud(L’Hirondelle et al. ). Greater frost damage to N-fertilized birch wasassociated with N-induced deficiencies of B (Brakke cited in van denDriessche ). A late spring frost resulted in a greater frequency ofsevere damage to red alder seedlings fertilized with triple super phosphatethan was experienced by unfertilized seedlings (Peeler and DeBell ).The researchers did not present foliar nutrient concentrations as part ofthe study. Fertilization with K, after the cessation of growth, reduced frostdamage to Picea sitchensis and Tsuga heterophylla seedlings in the nursery,and K fertilization at planting reduced winter frost damage to -year-oldPinus sylvestris and Picea abies (data cited in van den Driessche ).Conversely, K-deficient Picea abies were hardy to -ºC weeks beforewell-nourished trees and ºC hardier than well-nourished trees prior to

7.1 MineralNutrition and Plant

Water Relations

7.2 MineralNutrition and Frost

Damage

budburst (Jalkanen et al. ). Van den Driessche () suggested thatthe apparent cold hardiness sometimes associated with K fertilization mayinstead reflect an improved drought resistance, at least under conditionswhere water stress and cold temperatures occur concurrently.

An understanding of relations between nutrition and frost damage maybe important for managing red alder and hybrid poplar plantations.Newly planted red alder deharden quickly after thawing and planting andare especially prone to frost damage if located in cold air drainages(Dobkowski et al. ). Such damage may greatly reduce eventual sawlogquality and value. The rapid growth of the poplar hybrids most oftenplanted in coastal British Columbia (crosses of the native P. trichocarpawith P. deltoides from the southern United States) is largely the result of alonger leaf area duration (Ceulemans et al. ). That extended leaf areaduration, combined with intensive fertilization, may make hybrid poplarplantations particularly susceptible to frost damage if they are located onfrost-prone sites.

The nutritional status of broadleaved trees may influence their resistanceto, and tolerance of, insect herbivores or pathogens. Outbreaks of tentcaterpillars (Malacosoma disstria) may cause significant growth reductionsin red alder, birch, and aspen (Gara and Jaeck ; Peterson and Peterson), while the large aspen tortrix is primarily a defoliator of balsampoplar (Peterson and Peterson ). Sawfly (Trichiocampus spp., Nematusspp.) larvae may also be significant defoliators of red alder (Gara andJaeck ). Nitrogen fertilization increased the nutritional value of aspenleaves for larvae of the large aspen tortrix, by increasing foliar N concen-trations (from – mg g-1) and by decreasing the concentrations oftoxic or digestion-inhibiting metabolites (tannins and phenolic glycosides)(Bryant et al. ). The concentrations of secondary metabolites eitherbefore or following defoliation may vary with clone (Mattson and Palmer; Robison and Raffa ). As well, nitrogen fertilization may affectthe insect-induced production of defensive compounds (e.g., condensedtannins, proanthocyanidins) in paper birch (Bryant et al. ) and oaks(Hunter and Schultz ). Such differences in phytochemical inductionbetween clones or species may be due in part to differences in nutrientavailability to the particular trees.

Fertilization may also increase the ability of trees to recover after defo-liation. Nitrogen fertilization of stands infested with spruce budwormsreduced defoliation and increased growth of infested trees (Wickman etal. ). Fertilization increased the numbers of larvae, but presumablyincreased the growth of foliage even more. Weetman et al. (a)observed greater incidence of spruce weevil damage after N and P fertil-ization of Sitka spruce. Although gains in height growth more than com-pensated for growth reductions from weevil damage, stem form was stilladversely affected. It is unknown what effect fertilization might have onthe ability of deciduous broadleaved trees to tolerate insect infestation.

How nutrition might affect the susceptibility of deciduous broadleavedtrees to pathogens in British Columbia has not been determined. Thesetree species are susceptible to a variety of diseases. Poplars, for example,are particularly susceptible to damage from leaf rust (Melampsora spp.)

7.3 MineralNutrition and Insect

Herbivores

7.4 MineralNutrition and Tree

Pathogens

(Wang and van der Kamp ; Newcome et al. ) and a variety offungi causing heartwood decay, cankers and galls, stem and butt rotscaused by Phellinus spp., and root rots caused by Armillaria spp., in addi-tion to others (Peterson and Peterson ; Simard and Vyse ). Paperbirch is susceptible to Phellinus spp., Armillaria, and Fomes spp. in olderstands, as well as a variety of sap rots, leaf rust and “dieback,” which is aprogressive dying of twigs and branches from the treetop outward(Simard and Vyse ). However, birch may be resistant to Armillariaostoyae and the Douglas-fir variety of P. weirii (Massie et al. ). Redalder may be susceptible to F. annosus, but is known to be resistant tolaminated root rot caused by P. weirii (Nelson et al. ).

There is evidence that the resistance to some pathogens may be infl-

uenced by plant nutritional status. Obligate parasites such as rusts may bepromoted either by deficiencies of K (Suzuki and Chiba cited in vanden Driessche ) or excesses of N. The increase in infection severitywith deficiencies of K or excesses of N may be mediated throughincreased accumulations of low-molecular-weight substances (Marschner); it was not associated with decreased foliar concentrations of pheno-lic compounds (Hakulinen ). Sulphur-deficient Pinus radiata weresubject to more severe infections by the needle cast fungus, Dothistromaspp. (Lambert ), in association with increased foliar concentrations ofarginine. Thinning and fertilization with urea increased the infection byArmillaria spp. of Rocky Mountain Douglas-fir, compared with control orthinned, unfertilized trees (Entry et al. ). The greater incidence ofinfection may have been associated with higher concentrations of sugarsin roots and decreased concentrations of lignin and tannins. Fertilizationwith N alone may also have predisposed the trees to infection by increas-ing leaf:root ratios and increasing water stress (Belanger et al. ; Milleret al. ). The susceptibility of aspen to stem cankers caused by Hypoxy-lon spp. increased with N fertilization, but decreased with P and K addi-tion (Teachman et al. ). Clonal interactions with nutrient additionwere also noted. Fertilization may affect the interactions between decidu-ous broadleaved trees and pathogens and insects. However, it is unknownhow tissue elemental concentrations, productivity, and susceptibility toinsects and pathogens are related.

8 FERTILIZATION AND MYCORRHIZAE

Root systems of temperate forest trees are commonly infected by mycor-rhizae. The most consistently reported beneficial effect of mycorrhizalinfection for trees is enhanced uptake of mineral nutrients. It is unclearhow fertilization may affect mycorrhizal presence and function and therelationships among fertilization, mycorrhizae, tree nutrition, and growth.

There are two primary types of mycorrhizae found on deciduousbroadleaved trees: endomycorrhizae, dominated by the vesicular-arbuscularmycorrhizae () and ectomycorrhizae (). The native hardwoodtrees of British Columbia may host either, but one type or the other typi-cally dominates, depending on the host species. In red alder (Molina et al.), paper birch (Perala and Alm ; Jones et al. ), and trembling

aspen (Cripps and Miller cited in Pregitzer and Friend ), dominate. Hybrids of Populus deltoides, which should include theP. trichocarpa × P. deltoides hybrids typically planted in coastal BritishColumbia, may have either mycorrhizal type, but are usually dominatedby (Godbout and Fortin ). Both may also occur simultaneouslyon the same root system (Lodge ).

Mycorrhizae are commonly reported to enhance the uptake of P, butthey also increase the uptake of K, Ca, S, Cu, Zn, NH4-N, and organic N(Bowen ; Marschner ). The enhanced uptake of immobile ele-ments may be associated with the extensive surface areas of hyphalstrands, but may also be able to utilize Al and Fe phosphates nototherwise assimilated by the host tree (Bowen ).

The effects of fertilization on mycorrhizal development are unclear. Fer-tilization with P did not affect development in red alder seedlings(Koo cited in Molina et al. ). Elsewhere, the numbers of mycor-rhizal root tips per unit volume of soil in an -year-old Pinus taedaplantation were reduced in plots fertilized with N only, compared withunfertilized plots or plots fertilized with P only or N+P+K (Menge et al.). Fertilization with B well in excess of host plant demand enhancedroot infection (Mitchell et al. ). Marschner () suggested thatinfection was low at low availability of P, increased to an optimum, thendecreased as P availability further increased. Rate of decline in infectionwith increasing P appeared to vary with the fungal species. It is unknownhow fertilization might impact mycorrhizal development in hardwoods inBritish Columbia and how this, in turn, might relate to tree growth andnutrition. Presumably, fertilization would offset any declines in nutrientuptake associated with decrease mycorrhizal infection and vigour.

9 AMELIORATION OF MINERAL NUTRIENT DEFICIENCIES

Fertilization is the primary approach for correcting mineral nutrientdeficiencies in forest stands. The efficiency of fertilization (i.e., the per-centage of the applied element assimilated by the target trees) may varywith the form of the element and its frequency of application. The effectsof elemental form on fertilization efficiency have been examined only inconiferous species in British Columbia, although the effects of P form arecurrently being examined in hybrid poplars (see below). Of the deciduousbroadleaved species significant to forestry in British Columbia, the effectsof fertilization frequency have been examined only in hybrid poplars(Zabek ).

Typically, only –% of applied N is assimilated by the target trees,compared with efficiencies exceeding % in crop species (Nason andMyrold ). Nitrogen is generally applied in coastal forests as urea andin the Interior as a blend of urea and ammonium sulphate. The mostappropriate form of N to add is not always obvious. Application ofammonium nitrate resulted in greater growth responses by Douglas-fir onVancouver Island, but was no more effective than urea in trials in north-ern Idaho and western Montana (Mika et al. ) and the interior of

9.1 N Sources

British Columbia (Brockley ). Ammonium nitrate may be generallymore effective in cooler climates and on soils with low native fertility orrestricted moisture (Bengtson cited in Ballard ). Although ureacontains a greater percentage of N (% vs % in ammonium nitrate),hydrolysis of urea produces NH3, which may volatilize under conditionsof restricted moisture availability. As much as –% of N applied asurea may be volatilized and lost from the soil-plant system (Marshall andDeBell ). The losses may be reduced when the fertilizer is applied inconjunction with cool, wet conditions (e.g., fall-early winter) or when theurea is coated with S. Ammoniacal fertilizers (ammonium nitrate, ammo-nium sulphate) are mildly acidifying. Thus, NH4 remains protonated anddissolved in the soil solution and is not prone to volatilization (Nasonand Myrold ). The disadvantage of ammoniacal fertilizers is thatsignificant percentages (e.g., %) of the added N may be immobilized.

Nitrate-based fertilizers are not used in fertilization of coniferousforests in the Pacific Northwest. Concentrations of N in nitrate fertilizerare lower than in ammonium- or urea-based N fertilizers and the addednitrate may be readily leached. However, less N is immobilized (e.g., %)when added as nitrate than when added as ammonium. Nitrogen fertiliz-ers containing a significant portion of N as nitrate may be more appro-priate as a source for N fertilization for fast-growing hardwood species(except for red alder) than for associated conifers. In intensively managedstands, greater uptake rates of N may minimize leaching losses. As previ-ously mentioned, deciduous broadleaved species may have a greatercapacity for assimilating NO3 than do conifers, particularly in foliage(Smirnoff and Stewart ).

Controlled-release fertilizers (s) have received increasing attention asa way of increasing efficiency of nutrient uptake, especially by young trees.In studies conducted in British Columbia to date, s have not beenmore effective in increasing growth than soluble fertilizers. In studies con-ducted with two clones of hybrid poplar on Vancouver Island, four s(Osmocote --- MgO, Agroblen ff --+trace elements, Agroblen--- MgO, and Osmocote Poly-S --) and two readily soluble fertil-izers (Growers Standard -- and diammonium phosphate) were dib-bled into holes cm from newly planted cuttings at rates supplying ,., or g N per tree.9 Stem growth increased linearly with N supplythrough two growing seasons, but there was no difference among fertilizersafter one or two growing seasons.10 Studies with coniferous seedlings haveshown a similar lack of effect from release rate (van den Driessche ;Sandford and Andersen cited in van den Driessche ).

Phosphorus fertilizers generally occur as either water-soluble forms (e.g.,triple superphosphate, ) or water-insoluble (e.g., ground rock phos-phate, ) forms. Fertilization of coniferous forests in British Columbiaor surrounding regions has rarely included additions of P (Weetman et al.) and the efficacy of the different sources has not been comparedsystematically. Studies of growth responses of red alder, black cottonwood,

9.2 P Sources

R. van den Driessche and K. Brown, BC Min. For., EP ., . K. Brown and R. van den Driessche, unpubl. data, .

and hybrid poplars have also used (DeBell et al. ). Triple superphosphate may be superior on soils of moderate acidity and P-retentioncapacity, whereas may be more effective on acid soils of lowP-retention capacity and basic soils of high P-retention capacity (Ballard). The advantage of is its longer duration of effectiveness, whichpresumably occurs because of lesser leaching losses on soils of lowP-retention capacity and slower rates of transformation to unavailableforms of P on high P-retention capacity soils (Ballard ). However, may not supply adequate amounts of P to fast-growing, intensivelymanaged hardwood species such as hybrid poplars.

The effects of P sources, rate of P addition, method of application, andrate of N addition on hybrid poplar growth and nutrition are currentlybeing examined in a factorial experiment on eastern Vancouver Island.11

Through three growing seasons, mean stem volumes were about %greater in trees fertilized with diammonium phosphate or than intrees fertilized with .12 It appears that readily-soluble forms of P aremore effective in the short-term, although it is unclear if the advantagespersist longer into a rotation.

Operational fertilization of coniferous stands in British Columbia and thePacific Northwest states typically consists of about kg N ha-1 appliedevery – years (Diggle ; Olson ). The low fertilization efficiencyof N by forest stands may lead to increased nutrient runoff and waterpollution in situations requiring intensive rates of nutrient addition (e.g.,in short-rotation intensive culture). Fertilizer efficiency may be increasedby dividing the fertilizer application over several applications (i.e., fertiliz-ing more frequently and in smaller amounts per application) whileincreasing added amounts over time to match plant growth (Tamm ;Ingestad ). Annual applications of fertilizer have increased the pro-ductivity of Scots pine and Norway spruce by –%, compared withincreases of –% relative to that achieved by fertilization at intervalsof – years (Axelsson cited in Binkley ). A potential problem isthat nitrification may be promoted by small repeated applications of N.When short-rotation sycamore plantations were fertilized with kg Nha-1 as urea, additions at constant rates at the beginning of each growingseason (i.e., kg N ha-1) resulted in the greatest amounts of NO3 leach-ing; applications three times per year ( kg N ha-1 per application)decreased the amount of NO3 leaching, but increasing the amount of Nadded at the start of each growing season (e.g., , , kg N ha-1)resulted in the greatest growth, a - to -fold increase in N fertilizerefficiency and the smallest amounts of NO3 leached (van Miegroet et al.). Conversely, the growth of hybrid poplars at a site on VancouverIsland was not improved when fertilizer applications were split over agrowing season, compared with a single application at the beginning ofthe growing season (Zabek ). Moisture deficits late in the growingseason probably limited elemental uptake and growth responses to thelate-season applications.

9.3 Frequency ofFertilization

R. van den Driessche, BC Min.For., EP., Brown and van den Driessche, unpubl. data, .

Alternatives to fertilizing with chemical fertilizers include applying sewageeffluent or biosolids and interplanting with N2-fixing species. Interest inbiosolids applications has increased partly because of its potential value asa soil conditioner (adding mineral nutrients and organic matter), andpartly because of problems with disposal following completion of sec-ondary sewage treatment facilities in Vancouver. Concerns centre aroundsalt accumulation, groundwater contamination, and the possible inductionof secondary deficiencies of elements such as Mg (Harrison et al. ).Consequently, the effects of sludge on nutrition and growth of cotton-wood and hybrid poplars have been examined in several studies in BritishColumbia and Washington.

The city of Vernon, B.C., in conjunction with the B.C. Ministry ofForests and the University of British Columbia, has irrigated hybrid poplarplantations with municipal sewage effluent since (Carlson ). TheGreater Vancouver Regional District (), in conjunction with ScottPaper and the University of British Columbia, applied sludge in tohybrid poplars at rates intended to supply up to kg N ha-1. Sludgewas operationally applied to ha in and ha in at rates sup-plying about kg N ha-1.13 In eastern Washington, sludge has beenapplied to hybrid poplars in combination with irrigation in a study thatbegan in . Approximately % of the N initially added was lost tovolatilization, probably as a result of alkaline soils and warm, windy condi-tions at the site. Losses from volatilization appeared to be partially com-pensated by increased mineralization rates under sludge application.14

Biosolids may be an appropriate means of fertilizing intensively man-aged cottonwood and hybrid poplar stands. It is unclear, however,whether biosolids are more effective in supplying nutrients to fast-growing tree species than are synthetic fertilizers, although other factors(soil conditioning, cost) may make their use advantageous.

10 SPECIES-SPECIFIC MINERAL NUTRITION-RELATEDRESEARCH PROBLEMS

Several factors make red alder an appealing species to manage for incoastal British Columbia. It is the fastest-growing native tree species afterblack cottonwood and may be a source of relatively valuable wood forfurniture, cabinets, and turned-wood novelties (Plank and Willits ).Red alder is unique among the major hardwood species of the provincein its ability to fix atmospheric N2 symbiotically, in association with theactinomycete Frankia spp. Consequently, the presence of red alder maysignificantly improve the nitrogen capital of a site over time and improvethe growth of coniferous associates such as Douglas-fir that ultimatelydominate the site. The combination of fast growth and an ability to fixatmospheric N2 make red alder an appropriate species to plant for

9.4 Biosolids

10.1 Red Alder

Nutrifor Newsletter, July . Notes from presentation by Chuck Henry, University of Washington, at Poplar Field Day ,

Prosser, WA, August , .

revegetating deactivated forest roads and landings and for stabilizingslides. Finally, red alder is resistant to laminated root rot (Phellinusweirii), which infects many Douglas-fir stands on Vancouver Island.

Despite the apparent desirable characteristics of red alder, there hasbeen little interest until recently in managing for red alder in coastalBritish Columbia. One company, Coast Mountain Hardwoods Inc., wasawarded forest licences in , permitting the harvest of specified vol-umes of alder in four timber supply areas. In late , the four districtsin the Vancouver Forest Region (Port McNeill, Campbell River, SouthIsland, and Sunshine Coast) in which Coast Mountain Hardwoods heldforest licences agreed to plant a total of ha yr-1 in red alder for years. This is a test program to evaluate growth on a range of biogeocli-matic units and site series considered to be of medium-good quality.15

Operational contexts in which nutrition and fertilization studies may beparticularly appropriate for red alder include where there is: () plantationmanagement either on sites generally considered as appropriate for redalder (e.g., Green and Klinka ) or on Phellinus-infected sites thatwould normally be considered too dry and infertile for alder growth; ()management on deactivated roads and landings; () management ofrepeated rotations of red alder; and () management to improve site fer-tility for later rotations of coniferous associates.

A long-term issue is to determine what mineral nutrients limit thegrowth of red alder in British Columbia and what responses might beexpected on a variety of sites. Site indices (-year base) of red alder incoastal British Columbia ranged from – m on sites classified as richor very rich. These indices were also correlated with foliar P concentra-tions in acidic soils (pH .–.), indicating that some red alder standsmight be responsive to fertilization with P or other elements. In oneglasshouse study, the growth of seedlings in pots containing soils collectedfrom – cm depth in mature alluvial alder stands on Vancouver Islandincreased with the addition of . The effect of was greater in soilsof lower initial pH (.±.(sd)) than in higher pH soils (.±.), butthere was no effect in soils with high extractable-P concentrations. Theaddition of dolomite increased foliar Mg concentrations, but did notaffect growth.16 Single-tree plot fertilization studies in young (age –)alder plantations on Vancouver Island have produced mixed results. Inone trial, stem volume after one growing season decreased with increasingP supply, but the negative effect was offset by the addition of elementsother than N and P. In a second study, there was no effect of P or otherelements, and in a third study, volume increased by % with the addi-tion of P and other elements.17 In field fertilization trials conducted withplantation-grown alder in western Washington, P increased (Radwan andDeBell ) or had no effect (Harrington and DeBell ) on growth. Inthe former study, optimal P application rates increased with available

Minutes, Red Alder Management Committee Meeting, Vancouver Forest Region, November, .

Brown, unpubl. data, .. Brown, unpubl. data, ., .

moisture. Seedlings grown in pots containing native soils from Washing-ton and Vancouver Island responded to addition of P, S, and trace ele-ments (Binkley ; Radwan ; Compton ). Grey alder seedlingswere reported to require higher concentrations of P, relative to N, thandid birch seedlings (Ingestad ). Red alder may respond to fertilization,but the potential growth response and its relation to site characteristicsare unknown.

Nitrogen fixation rates depend on a continuous supply of newly fixedcarbohydrates to the root nodules (Marschner ), suggesting that theavailability of any essential element that is low enough to reduce plantvigour will also reduce N2-fixation rates. However, N2 fixation and noduledevelopment may be affected differently than is whole-plant growth as theavailability of a given element increases. Nodule initiation, but not laternodule growth, was sensitive to Ca supply in clover (Lowther andLongeran cited in Marschner ). An increasing P supply to soy-beans caused greater increases in nodule mass than in whole-plant mass(Israel ) and the ratio of nodule mass:root mass in red alder seedlingsmay have also increased with addition rates of triple superphosphate.18 Alow availability of P to legumes may be associated with N deficiencies(Marschner ). Among trace elements, supplies of Mo and Fe maydirectly affect N2-fixation rates. In peanuts, the addition of Mo increasednodule mass by .-fold, nitrogenase activity (per unit mass) by .-fold,shoot+pod mass by .-fold, and N uptake (per hectare) by .-fold(Hafner et al. ).

Because red alder is immune to laminated root rot caused by Phellinusweirii, it may be planted in disease centres of infected stands, typically ofDouglas-fir, and often in conjunction with commercial thinning of theinfected stand (Thies and Sturrock ). Such stands may be on sitesconsidered too dry and infertile to sustain adequate growth rates of redalder. In these situations, appropriate fertilization may have a strategicrole in maintaining adequate growth rates and in improving site N capitalfor a subsequent stand of Douglas-fir.

Fertilization may also have an important role in enhancing the growthof alder on slides or deactivated forest roads and landings in coastalBritish Columbia. Growth and N2 fixation may be limited by inadequatenutrition associated with removal of upper soil horizons and with soilcompaction. A commercial fertilizer blend called Alder-pak (ReforestationTechnologies Inc.), designed for adding at the time of planting, has beenapplied to seedlings planted on deactivated roads and landings and slidesin the South Island Forest District.19 Small-scale screening trials quantify-ing the effect of such fertilizers and their effectiveness in the different soilenvironments of slides, roads, and landings would provide a useful assess-ment of this practice.

Finally, an understanding of red alder nutrition may be important formanagement of the species in repeated rotations on sites on whichconifers may be difficult to establish. During the course of an alder rota-tion, N2 fixation may decrease soil pH over time and the growth of alder

Brown, unpubl. data, . P. Ducharme, B.C. Min. For., pers. comm., May .

seedlings planted on sites previously containing red alder may be reducedrelative to seedlings planted on similar sites that previously containedDouglas-fir (van Miegroet et al. ). After years, above-ground biomassof alder planted on an alder site in the Cedar River watershed of westernWashington was % less than that of alder planted on a Douglas-fir site.The lower growth rates were associated with lower Bray-extractable Pconcentrations in the soil, decreased foliar concentrations of P, Ca, andMg, and decreased leaf litter concentrations of N, P, K, Mg, and Fe(Compton et al. ). The observed declines in productivity and elemen-tal concentrations of second-rotation alder may have been associated withnitrification-enhanced reductions in soil pH and enhanced leaching of Caand Mg from the original alder stand (Binkley and Sollins ; vanMiegroet et al. ). The soil in the Cedar River site was a gravelly sandyloam and it is unclear whether such dramatic decreases in growth andnutrient availability would be seen in second-rotation alder stands grow-ing on better-buffered soils. Elsewhere, the presence of alder increasedthe availability of P, compared with that in adjacent coniferous stands(Giardina et al. ), although the availability of P may still have limitedalder growth.

Repeated rotations of red alder may be a preferred managementoption on sites in which establishment of Douglas-fir is difficult (e.g., wetalluvial sites). Because of this, it is important to determine to what extentthe results of the Cedar River studies apply to other sites. The followingquestions may be important to answer: () What elements limit aldergrowth in soils of different pH and buffering capacity? () Does the pres-ence of red alder necessarily result in site acidification and, if not, onwhich sites does it not? () What effect might site acidification have onthe nutrition and productivity of second-rotation alder seedlings andsaplings? () Can appropriate fertilization allow site management forconsecutive rotations of alder without resulting in appreciable losses inproductivity? () Can the problems alluded to above be minimized byappropriate mixtures of red alder and Douglas-fir, rather than managingfor pure stands?

As indicated previously, the effectiveness of different P fertilizer sourcesmay vary with soil acidity. Liming of acidic alder soils is one possibleapproach to minimize multiple elemental deficiencies (Seiler andMcCormick ; Ljungstrom and Nihlgard ). However, liming ofacidic soils may increase, decrease, or have no effect on P availability,depending on the soil and timing of lime and P applications (Haynes). Reviews of long-term liming trials in European forests suggest thatwhile some soil characteristics are improved by liming (decreased acidity,increased cation exchange capacity), growth and foliar K concentrationsmay be reduced, acidification may be promoted in deeper horizons, leach-ing of NO3-N may increase, and fine root growth may be concentrated inthe uppermost soil horizons (Huettl and Zoettl ). If so, liming maynot be an appropriate substitute for the readily soluble forms of specificelements.

Finally, improved nutrition of red alder in mixed stands may improverates of N accretion and N availability to coniferous associates that laterdominate the stand. Reported rates of accretion range from to kgN ha-1 yr-1 in pure stands and to kg N ha-1 yr-1 in mixed stands

(Binkley et al. ). Many factors other than nutrition, including differ-ences in sampling technique, stand age, moisture availability, and standdensity could contribute to this variation. Given the direct and indirectroles of various nutrients in enhancing N2 fixation, as demonstrated incontrolled studies (discussed above), it seems that fertilization with appro-priate elements other than N could enhance N availability to coniferousassociates during stand development. Currently, studies are underway incoastal British Columbia to assess the effects of various mixtures of alderand conifers on stand development and N accretion (Comeau et al. ).Fertilization, however, is not part of the study design.

The diagnosis of elemental deficiencies in relation to site associations ofthe biogeoclimatic ecosystem classification, and the prediction of growthresponses to nutritional amendments, are both important nutritionaltopics pertaining to the operational silviculture of black cottonwood,balsam poplar, trembling aspen, paper birch, and bigleaf maple. Eachspecies may occur in a variety of sites, but it is unknown how nutrientsupply affects growth in relation to quantifiable measures of site fertility(e.g., mineralizable-N, foliar elemental concentrations), soil moisture andstand characteristics (e.g., stand density, leaf area index) or categorical soilmoisture and nutrient regimes used in the provincial biogeoclimaticecosystem classification. To date in British Columbia, growth responses tonutrient additions have been examined only in black cottonwood(McLennan ) and are currently being examined in trembling aspen,as indicated previously.

Black cottonwood is the lead species on approximately ha ofcoastal forest land in British Columbia and slightly less in the southernInterior (Peterson et al. ). Balsam poplar is the lead species onapproximately ha in northern British Columbia, primarily in thenortheast. Both are most commonly associated with alluvial sites, but mayalso occur on moist upland sites. McLennan () observed that siteindex (-year base; SI15) of black cottonwood in alluvial stands increasedfrom . m to . m as soil nutrient regimes increased from medium tovery rich and was more strongly related to foliar concentrations of N andP than to those of other elements. was applied to identify elementsthat limited growth in different site associations. On low alluvial benches(cottonwood-willow association, mean SI15=. m), N was more limitingthan P and K. On middle benches (cottonwood-red osier dogwood associ-ation, mean SI15=. m), P and K were more limiting than N, and onhigh benches (Sitka spruce-salmonberry association, mean SI15=. m),K was more limiting than P. Nitrogen was not considered limiting on thehigh benches. Short-term fertilization screening trials were employed totest the accuracy of the conclusions. In general, fertilization hasnot been considered an issue of strategic importance in the intensivemanagement of native black cottonwood or balsam poplar stands, butMcLennan’s findings may be important in developing fertilization regimesfor hybrid poplar plantations located on alluvial sites.

It is important to understand where and how mineral nutrition limitsthe growth of aspen. Aspen is the most widely distributed hardwood treespecies in British Columbia and is the species harvested in the greatestquantities. Aspen stands may be responsive to fertilization at least to ages

10.2 BlackCottonwood, Balsam

Poplar, TremblingAspen, Paper Birch,

Bigleaf Maple

of years (Coyne and van Cleve ; van Cleve and Oliver ; Nilssonand Wasielewski ; Yang ). For example, stem volume of a -year-old aspen stand (initial volume m3) increased by . m3 ha-1 (.%)relative to the control stand when fertilized with kg N ha-1 and kgha-1 of P and K (Yang ). In contrast, fertilization with up to kg Nha-1 + micronutrients did not increase the growth of aspen on fertilesites.20 There is some concern that the capturing of added nutrients bythe abundant understorey vegetation associated with aspen stands willminimize any response to fertilization (Peterson and Peterson ).

Many of the aspen stands in northeastern British Columbia are –

years old and are considered overmature (Peterson and Peterson ). Ifthe harvesting of older stands is accelerated, factors affecting vegetativereproduction (i.e., suckering) and early growth must be understood. Pooraspen regeneration is often associated with herbivory and with soil com-paction following harvesting, possibly because of poor drainage or pooraeration.21 Soil temperature is felt to be a major influence on the initia-tion and development of suckers (Peterson and Peterson ). Animproved mineral nutrient status of the parent stand could increase thepost-harvest initiation of adventitious shoots on lateral roots by increasingcytokinin production, and might further affect the subsequent rate ofsucker growth by affecting concentrations of soluble carbohydrates in theroots (Tew ; Schier and Zasada ). With respect to nutritionalresearch, fertilization trials on a variety of sites are of high prioritybecause of the obvious operational implications. At the same time, therelation of fertilization and tree nutrient status to vegetative reproductionmay be of some importance. The effects of fertilization on tree growthand susceptibility to herbivores and diseases are of interest, but of lowerpriority.

Paper birch occurs throughout the Interior and, to a lesser extent, incoastal British Columbia. The highest concentrations occur in the north-eastern part of the province on sites considered to be of low productivity(Massie et al. ). Lower concentrations occur in the central and south-central parts of the province on sites of medium productivity. In theKamloops region, site index is strongly related to available moisture; siteindex at years ranged from . m in subxeric sites in the mw bio-geoclimatic variant to . m in subhygric sites (Simard and Vyse ).

The response of birches to fertilization have not been examined inBritish Columbia, though it has been studied elsewhere. The growth ofpaper birch on medium- or coarse-textured soils in the northeastern U.S.is often limited by deficiencies of N and P. If fertilized after thinning,growth responses to fertilization last – years (Safford ; Hoyle ).Hoyle () grew paper birch from seed for years under plantationconditions in New Hampshire. Seedlings fertilized with N, P, and limehad basal areas % greater than did controls, whereas the basal area ofyellow birch (Betula alleghensis) did not increase with fertilization. Protec-tion of the plantation from deer was essential for successful plantationculture of paper birch. Viro () studied the growth responses of

Dave Coopersmith, B.C. Min. For., pers. comm., November . Richard Kabzems, BC Min. For., pers. comm., January .

seedlings and near-mature (ages –) stands of warty and hairy birch(Betula verrucosa and B. pubescens, respectively) to fertilization in Finland.Fertilization the year after planting with ammonium sulphate increasedheights –% over controls; in older stands, fertilization with N+Pincreased stem diameters up to % over years in one study and %in a second. In a study conducted on a site considered to be fertile, noresponse to fertilization was observed. Fertilization was determined not tobe economically feasible even where growth responses were observed,because of the small tree size. However, the responses of pole-sized, well-stocked stands were not examined. In mixed stands, birch required greaterapplication rates of N to achieve a given relative increase in yield than didthe associated spruce (Picea abies), an interesting observation consideringthat hardwood species often respond more rapidly to fertilization (Linderand Rook ).

Clearly, and not surprisingly, the growth of birch may respond to theaddition of limiting nutrients. It is therefore important, as with otherspecies, to identify on which sites fertilization will evoke a growthresponse. Site moisture availability is likely to be important in determin-ing the response of birch to fertilization, at least in the southern interiorof the province. Safford () suggested that a site index of m at

years (equivalent to site indices observed in mesic-subhygric sites in the and zones of southern British Columbia) was the minimum toconsider for intensive culture, which would include fertilization.

The most valuable birch logs are those that are both large and withfew defects. While fertilization may be important for enhancing growthearly in stand development, fertilizing well-stocked, productive, and near-mature stands may be desirable economically. It is important to identifythe appropriate age and size of stands at which fertilization would bemost beneficial.

Increasing interest in the planting of bigleaf maple has revealed somedifficulties in the consistent production of high-quality nursery stock and inthe growth attainable after outplanting.22 Outplanted seedlings may exhibitlittle or no above-ground growth during the first growing season after out-planting; field observations suggested that seedlings planted in moistswordferm-dominated depressions outgrew those planted in coarse-texturedsoils derived from glacial till.23 This suggests that either nutrient or mois-ture availability, or both, may affect biomass allocation and growth ofbigleaf maple seedlings. However, the effects of plant nutrition and mois-ture status on biomass allocation and growth have not been studied. Rank-ings compiled by Klinka et al. () suggest that bigleaf maple is relativelyundemanding of moisture, compared with other coastal hardwoods. Theserankings, however, may not apply to seedling requirements. The relation-ships between seedling growth, nutrition, and moisture availability shouldbe examined. As with paper birch, the value of bigleaf maple logs increasewith size, as long as defects do not also increase (Massie et al. ).Hence, fertilization trials with near-mature stands might be appropriate.

A. Luckett . Big-leaf maple regeneration study. Progress report, Hardwood SilvicultureCooperative Meeting, January –, .

Phil Comeau, B.C. Min. For., pers. comm., January .

The specific nutritional concerns associated with hybrid poplars differfrom those of the native broadleaved species occurring in BritishColumbia forests. Site conditions, while variable, are likely much less sothan are those associated with widespread species such as tremblingaspen, black cottonwood, balsam poplar, or red alder. Intensive breedingprograms are producing numerous clones that may differ in growth ratesand their abilities to grow on nutrient- and moisture-limited sites. Thegreater growth potential of poplar hybrids, combined with their shortrotations (e.g., less than years) means that nutrient addition ratesrequired to achieve maximum growth will be greater than those ratesrequired by native broadleaved species. However, the plantation sites typi-cally have shallow water tables, and the over-application of fertilizers earlyin the life of the stand (within years following planting) could result ingreater leaching of added fertilizer to subsurface waters. At the same time,a greater variety of viable options exists for the delivery of nutrients.These include the application of biosolids, varied frequencies in the appli-cation of inorganic fertilizers, and irrigation with municipal effluent(Carlson ), as discussed previously. Research on these different meth-ods of nutrient delivery should be continued.

Clonal variation in response to site fertility and added nutrients is amajor area of uncertainty. Optimum soil pH for growth varies amongspecies and hybrids. For example, optimum pH tends to be lower inTacmahaca, Tacmahaca × Aigeiros, and Aigeiros cultivars and hybrids withbalsam poplar parentage than in Euramerican (deltoides × nigra) crosses(Heilman ). Clones sensitive to high pH may be prone to iron-chlorosis (Heilman ).

Clones of cottonwood and hybrid poplars may vary in their growthresponses to N (Curlin ; Heilman ; Heilman and Xie ) and Pfertilization24 and therefore may differ in their ability to capture and useavailable nutrients. An understanding of those differences may be impor-tant for matching clones to sites and for developing new clones. Differ-ences in growth responses to a given availability of nutrients may be dueto differences in: () the amount of root growth; () acquisition efficiency,the amount of a given nutrient assimilated per unit of root; and () uti-lization efficiency—the amount of biomass produced per unit of nutrientacquired. Clonal or varietal differences in early root growth may be asso-ciated with later differences in biomass accumulation (Bloomberg ;Tschaplinski and Blake ; Brown et al.25), implying that the rate andtotal amount of early root growth is important for providing the plantwith access to sufficient moisture and nutrients for establishment. Studiesof herbaceous species suggest that the uptake of P, a relatively immobileelement, is greater in varieties with larger or more fibrous root systems(Vose ). The distribution of root growth in relation to nutrient-richpatches may vary with clone (Friend et al. ). If so, clones may differin the amount of photosynthate they must allocate toward nutrient acqui-sition versus the capture of light and CO2.

10.3 Hybrid Poplars

R. van den Driessche, K.R. Brown, ., unpubl. data K.R. Brown, F.D. Beall, and G.D. Hogan. Biomass accumulation in hybrid poplars during

the establishment year. Can. For. Serv., Sault Ste. Marie, Ont., Unpubl. manuscript.

While clonal differences in root growth have been studied in hybridpoplars, it is unknown whether clones might also vary in their ability tosolubilize and assimilate nutrients existing in forms that are not readilyavailable. For example, some plants can hydrolyze organic phosphatesthrough secretions of phosphatases (e.g., Li et al. ). Likewise, it isunknown if uptake capacity (i.e., uptake per unit root mass or surfacearea) varies with clone or if it is even important compared with differ-ences in the amount of root growth. Variation of uptake capacity for NO3might be important, because NO3 is likely to be the predominant form ofavailable N in sites considered suitable for Populus, and because increaseduptake capacity is likely more important for mobile elements such asNO3 and K (Chapin et al. ; Garnier et al. ). Nitrate reductaseactivity was correlated with growth rate in clones of Populus deltoides(Gordon and Promnitz ), but it is unknown if NO3 reductase activityand NO3 uptake capacity are linked.

It is also unknown whether clones of hybrid poplar differ in theefficiency with which they utilize different elements. During a growingseason, N utilization efficiency may vary with N partitioning betweenphotosynthetic and other functions in the leaf, and with allocationbetween roots and foliage. Growth rates might be greater at a givenwhole-plant concentration of N if more assimilated N was allocated tofoliage, and a further increase could occur if a greater proportion of foliarN was partitioned to photosynthetic functions (Hirose ; Evans ;Brown et al. a,b). However, the highest whole-plant nutrient useefficiency should result when processes underlying growth (Bloom et al.) are limited equally by a given limiting nutrient. Whole-plant N useefficiency could be increased if less foliar N needed to be partitioned tophotosynthetic functions, thus allowing more N to be reallocated to sup-port growth in other parts of the plant. Differences in P utilizationefficiency have been attributed to differences in the utilization of stored Pi(e.g., in vacuoles) (Marschner ). Low apparent utilization efficienciesof elements may also result from deficiencies of other elements, moisture,or light (e.g., Brand ).

The relative importance of the components of nutrient use efficiencyhas rarely been assessed. In one study, family differences in N useefficiency of loblolly pine were due to different characteristics, dependingon the availability of N (Li et al. ). At low N, uptake efficiency wasmore important than was utilization efficiency. Rooting efficiency was themost important component of uptake efficiency. At high N, utilizationefficiency was more important. Conversion efficiency was the most impor-tant component of utilization efficiency.

Studies of nutrient efficiency have largely focused on short-term stud-ies, typically during a single growing season. However, whole-plant nutri-ent use efficiency may also be affected by the efficiency of retranslocationof elements prior to leaf senescence. Retranslocation efficiency may varywith the species. For example, one study found that the percentage offoliar P removed before senescence was % in Betula papyrifera and %in Alnus crispa, and the percentage of foliar N removed was % and%, respectively (Chapin and Kedrowski ). In addition, retransloca-tion efficiency may increase with the “sink strength” in the plant (Pug-naire and Chapin ), suggesting that an improved nutritional status

might improve retranslocation efficiency. However, retranslocationefficiency of P in barley decreased with increasing N and P availabilityand decreased with water stress (Pugnaire and Chapin ), whereas theretranslocation efficiency of N and K in Pinus radiata increased with Nfertilization (Nambiar and Fife ). Clearly, retranslocation efficiencymay vary with several factors.

In broadleaved stands, the extent to which a high retranslocationefficiency is desirable depends on what happens to elements lost from thetree via litterfall. If nutrients contained in litterfall were rapidly cycled backinto the crop trees, a greater retranslocation efficiency may be undesirable,in that more nutrients would be removed from the site at each harvest(assuming woody above-ground tissues only are removed). Such increasedremovals may be detrimental to the maintenance of site productivity. Theproblem would be exacerbated under the short-rotations typically used forproducing wood chips. The problem would be minimized if the trees wereharvested with the leaves attached and the leaves were then stripped andreturned to the site (as is commonly practiced in western Oregon andWashington). If the poplars are being grown in riparian zones as a bufferto adjacent agricultural lands, an increased retention of assimilated nutri-ents may be desired. Some Populus trichocarpa × P. deltoides (T × D)hybrids may return % of N in litterfall annually, whereas P. trichocarpamay return as much as %. If nutrients in runoff are a concern (e.g.,with agricultural runoff) the T × D hybrids may be desired.26

The identification and interpretation of differences in nutrient useefficiency is complicated by the number of underlying plant processesinvolved. When pot-based trials are used to elucidate clonal differences,interpretations may be further complicated by time-dependent declines intissue nutrient concentrations associated with insufficient nutrient sup-plies (Ingestad ; Brown ). Thus, reports of greater N-use efficiencyin fast-growing clones of Populus deltoides (Curlin ) may merely indi-cate that N supplies were insufficient to maintain constant tissue nutrientconcentrations over time. Nonetheless, a better understanding of theprocesses underlying nutrient-use efficiency could provide a useful direc-tion in poplar breeding and assist in the development of appropriatefertilization practices.

As indicated above, clonal differences in root growth may affect nutri-tion and growth. Conversely, the mineral nutrition of stool beds may beimportant in determining the rooting capability of poplar cuttings. Nitro-gen deficiencies may enhance the rooting of cuttings, whereas deficienciesof K, P, Mg and Ca may decrease rooting (Haissig ). It is not clearwhether mineral nutrition primarily affects root initiation (Lovell andWhite ) or subsequent root growth, and the underlying mechanismsare not yet understood.

Determining the most effective time to fertilize during a rotation is anarea of considerable uncertainty. Fertilization, at least with N, is notrecommended during the establishment year (Dickmann and Stuart; Hansen ). The most conservative approach advocates delaying

P. Heilman and J. Braatne. . Ecological concerns in poplar conservation. Paper pre-sented at International Poplar Symposium, Seattle WA, August –, .

fertilization until nutrient supply clearly limits growth (Heilman ).Root systems of the planted cuttings are more extensive during the ndand rd years following planting, and absolute growth rates (and nutrientdemand) are greater as the stand approaches canopy closure. Thus,demands are greater and losses of N to leaching and denitrification areless likely. However, fertilization with N and P during the establishmentyear increased height growth by up to % during the establishmentyear.27 It is unclear whether the advantages of increased growth duringthe establishment year are offset by a decreased fertilizer use efficiencyand by increased losses of added nutrients off-site.

Finally, understanding the effects of hybrid poplar plantation establish-ment on long-term site productivity is important. The site preparationconducted in association with establishment of hybrid poplar plantationson previously forested land is intensive and commonly involves windrow-ing and forest floor displacement. There is some concern that site degra-dation may occur over time under such intensive management, althoughinputs of senescing leaves and fine roots during the life of a plantationmay improve the productivity of the site. Conversely, the establishment ofplantations on sites formerly used for pasture might well improve sitequality. Long-term monitoring of relevant soil properties influencing siteproductivity, including nutritional aspects, should be initiated to quantifychanges in both situations.

11 PRIORITIES FOR RESEARCH

Although fertilization clearly has the potential to increase the productivityand value of hardwood species, the relationships between mineral nutri-tion and the productivity of deciduous broadleaved tree species in BritishColumbia are largely unknown. There is information available fromWashington concerning the nutrition and fertilization of poplar hybridscurrently grown in coastal British Columbia, but few data exist on theresponses of those hybrids to fertilization in the site conditions beingused for poplar culture in the province. It is not yet clear how clones ofhybrid poplar may vary in their growth responses to nutrient availabilityor what fertilization tactics are most appropriate to achieve maximumproductivity, although such studies are under way.

Native species are even less well understood. It is unknown, for exam-ple, how foliar elemental concentrations relate to growth in bigleaf maple,how growth and nutrient uptake responses to fertilization differ betweennative hardwood species and their coniferous associates, and how fertiliza-tion responses in red alder, bigleaf maple, trembling aspen, paper birch,or balsam poplar vary with stand and site characteristics. There is noinformation on the soil-based or physiological mechanisms underlyingresponses to fertilization, or on how tissue nutrient concentrations affectplant responses to other abiotic stresses (such as drought or frost) orbiotic stresses (pathogens, herbivores). Such information is essential for

van den Driessche and Brown, unpubl. data .

properly evaluating the potential productivity of hardwood trees in BritishColumbia.

Fortunately, some information from conifer fertilization studies inBritish Columbia can, with caution, be applied to hardwoods. Thisincludes data suggesting which elements are most likely to be deficient incertain sites and soils, and data indicating which types of N fertilizer maybe most effective as a source of N. Principles inferred from studies of therelationships among nutrient status, drought and cold stress, herbivoresand pathogens, and productivity are applicable, even if the threshold con-centrations of foliar nutrients associated with maximum growth rates andstress tolerance are not known for each species.

From an operations perspective, being able to predict growth responsesof the predominant hardwood species to fertilization on a variety of sitesand stand conditions is of the greatest strategic importance, as it is withconifers. Having the ability to predict responses implies understanding theprocesses affecting response. Which should be emphasized: intensively cul-tured hybrid poplars or less intensively managed (and presumably lessdesirable) native hardwoods? Both are important. The objective of hybridpoplar culture is to produce fibre. Fertilization has an immediate andobvious role in enhancing the growth of hybrid poplar plantations, withthe clear likelihood of resulting in positive net economic returns. Con-versely, the objectives of native hardwood management are much morevariable and may not include fibre production. However, the potentialarea available for native hardwood management is much greater than thatfor hybrid poplar plantations, and the relationships between site, produc-tivity, and potential responses to fertilization are more complicated. Hence,it is prudent to begin the appropriate research on nutrition of native hard-woods before demands increase substantially and supplies become limiting.That work should be largely extensive in nature (i.e., establishing fertiliza-tion trials on a variety of sites while measuring a minimal number of treeand site processes), with the intent being to examine soil and plant pro-cesses affecting nutrient uptake and utilization in more detail as fieldresults become available. In this regard, information gained from process-oriented studies on fertilized hybrid poplar plantations should be useful inguiding more intensive studies of native hardwoods.

Several areas of research should be emphasized for intensively culturedhardwoods, such as hybrid poplars. These include:

. Developing a better understanding of the constraints that nutrientlimitations place on productivity, and of how best to alleviate thoseconstraints.

This focus would be part of studies designed to identify clones suit-able for growing on marginal sites (e.g., less fertile, with shorter grow-ing season, or moisture-stressed), such as those found on VancouverIsland. Some emphasis should be placed on determining the mostefficient means of delivering mineral nutrients, including the use ofcontrolled-release fertilizers, and on understanding how soil moistureand fertilization interact in affecting elemental availability and uptake.Also important to examine is how plant nutrient status affects waterconsumption. In the longer-term, assessments should be made as tothe sustainability of repeated rotations of hybrid poplars.

. Determining whether clones likely to be used operationally vary intheir nutrient use efficiency to a degree sufficient to warrant consid-eration in planting decisions.

This focus will require extensive collaboration with tree breeders.Several long-term opportunities for such collaboration exist in theregion. The B.C. Ministry of Forests has committed to a hardwoodbreeding program, which will lead to the development of clones appro-priate to British Columbian climates and soils. As well, researchers atthe University of Washington have identified quantitative trait lociassociated with rapid stem and root growth and stress resistance (Brad-shaw and Stettler ), but factors contributing to clonal differences inthe efficiency of elemental use are not understood. Identification ofsuch traits could lead to the development of clones with greater growthpotential at lower rates of fertilization.

. As part of the two areas above, adapting appropriate simulation modelsand developing the required data base.

Such work should be continued. Use of the models and data mayprovide managers with mechanistically based tools for matching clonesto sites.

. Better defining the relationships between clone, nutrient status, andsusceptibility to abiotic (drought, frost) and biotic stresses (insect her-bivores and pathogens).

Research in this area is especially important, given the variety ofinsects and pathogens that attack hybrid poplars and the reportedeffects of nutrition on, and clonal susceptibility to, different pathogensand herbivores.

. Developing improved protocols, using the above information, for theearly (years and ) screening of new poplar clones.

The above studies will be much more intensive with respect to datacollection and instrumental needs than are those suggested for nativespecies. However, a better understanding of the processes limiting produc-tivity of hybrid poplars should help researchers answer similar questionsthat arise in the course of more extensive studies conducted on nativehardwood species.

Which native species are of the highest priority to study? Aspen is themost widespread species and is harvested in the greatest quantities. Sev-eral studies from outside British Columbia have related foliar elementalconcentrations to aspen growth, but only two trials to date have beenconducted in the province. Alder is less widespread than aspen, but is ofconsiderable value. Management problems perceived to be of someimportance (e.g., productivity in repeated rotations) almost certainly havesome nutritional basis. Therefore, experiments addressing relevant aspectsof nutrition and growth might have a larger impact on alder managementpractices than they would on aspen management.

Black cottonwood is of a lower priority to study. Growth has beenstudied in relation to site classification and fertilization on alluvial sites in

Peter McAuliffe, Scott Paper, pers. comm., August .

southwestern British Columbia. Basic fertilization guidelines have beendeveloped and are currently in use by Scott Paper28 and other studies areexamining responses to biosolid applications. Less is known of growthand nutrient relations of black cottonwood in more northerly sites, suchas those in the Prince Rupert region. Balsam poplar is of some interest.Although less widespread than aspen, it is a potentially fast-growingspecies that can occur on alluvial or upland sites in the interior of theprovince. Relationships between growth and mineral nutrition have notbeen studied. Although balsam poplar is closely related to black cotton-wood, the information available about site classification, productivity, andresponses to fertilization for black cottonwood may be of little directvalue to those interested in managing balsam poplar, simply because ofthe differences in their ranges and associated climates and soils. If newhybrids are developed for the Interior that incorporate a balsam poplarparent, it would be useful to have information on nutritional require-ments for the balsam poplar parent as a guide in breeding.

Paper birch is relatively widespread and potentially of considerablevalue. It can also be a desirable species to grow in areas prone to root rot.Studies outside British Columbia suggest that paper birch can be respon-sive to fertilization on appropriate sites. It would be prudent to undertakefertilization studies on appropriate sites as part of refining silviculturalpractices for birch.

Bigleaf maple is relatively restricted geographically and is of lessoverall economic importance than are the more widespread black cotton-wood or red alder. However, maple seedlings are increasingly beingplanted. The relationships between growth after planting and site qualityare not well understood and it is unknown how growth varies with tissueelemental concentrations. Research should be initiated to define theserelationships. As with paper birch, bigleaf maple may be most valuable(from a forest products perspective) as a source of sawn lumber. However,it is unclear how fertilization at different stages of stand developmentwill affect the quality and value of such products (e.g., Cahill andBriggs ).

12 CONCLUSIONS

Intelligent management of the native hardwoods of British Columbia,combined with the increased culture of hybrid poplars on appropriatesites, can contribute significantly to future supplies of fibre and to thedevelopment of a value-added hardwood forest products industry in theprovince. Compared with their coniferous associates, the hardwoodspecies may grow faster and have shorter rotations, but their growthrates may also be more sensitive to the availability of moisture and nutri-ents. Despite this, the responses of hardwoods to fertilization in BritishColumbia are unknown. Understanding the relations between growthand nutrition of hardwood species should provide a better basis for iden-tifying what sites are best suited to being managed as hardwood ormixedwood stands and what silvicultural treatments can best increasegrowth.

LITERATURE CITED

Abadia, J. . Leaf responses to Fe deficiency: a review. J. Plant Nutr.:–.

Al-Abbas, A.H., R. Barr, J.D. Hall, F.L. Crane, and M.F. Baumgardner. .Spectra of normal and nutrient-deficient maize leaves. Agron. J. :–.

Baillon, F., X. Dalschaert, S. Grassi, and F. Geiss. . Spruce photosyn-thesis: possibility of early damage diagnosis due to exposure to mag-nesium or potassium deficiency. Trees :–.

Ballard, R. . Fertilization of plantations. In Nutrition of plantationforests. G.D. Bowen and E.K.S. Nambiar (editors). Academic Press,Orlando, FL., pp. –.

Ballard, T.M. and R.E. Carter. . Evaluating forest stand nutrient status.B.C. Min. For., Victoria, B.C. Land Manage. Rep. .

Belanger, R.R., P.D. Manion, and D.H. Griffin. . Amino acid contentof water-stressed plantlets of Populus tremuloides clones in relationto clonal susceptibility to Hypoxylon mammatum in vitro. Can. J.Bot. :–.

Binkley, D. . Forest nutrition management. Wiley-Interscience, NewYork, N.Y.

Binkley, D., R. Carter, and H.L. Allen. . Nitrogen fertilization practicesin forestry. In Nitrogen fertilization in the environment. P.E. Bacon(editor). Marcel Dekker, Inc., New York, N.Y., pp. –.

Binkley, D., K. Cromack, Jr., and D.D. Baker. . Nitrogen fixation byred alder: biology, rates and controls. In The biology and manage-ment of red alder. D.E. Hibbs, D.S. DeBell and R.F. Tarrant (editors).Oreg. State Univ. Press, Corvallis, OR., pp. –.

Binkley, D. and P. Sollins. . Factors determining differences in soil pHin adjacent conifer and alder-conifer stands. Soil Sci. Soc. Am. J.:–.

Blake, J.I., H.N. Chappell, W.S. Bennett, S.R. Webster, and S.P. Gessel.. Douglas-fir growth and foliar nutrient responses to nitrogenand sulfur fertilization. Soil Sci. Soc. Am. J. :–.

Bloom, A.J., F.S. Chapin III, and H.A. Mooney. . Resource limitationin plants-an economic analogy. Ann. Rev. Ecol. Syst. :–.

Bloomberg, W.J. . The significance of initial adventitious roots inpoplar cuttings and the effect of certain factors on their develop-ment. For. Chron. :–.

Bowen, G.D. . Tree roots and the use of soil nutrients. In Nutrition ofplantation forests. G.D. Bowen and E.K.S. Nambiar (editors). Acade-mic Press, Orlando, FL., pp. –.

Bradshaw, H.D., Jr. and R.F. Stettler. . Molecular genetics of growthand development in Populus. IV. Mapping s with large effects ongrowth, form and phenology traits in a forest tree. Genetics:–.

Brand, D.G. . The establishment of boreal and sub-boreal coniferplantations: an integrated analysis of environmental conditions andseedling growth. For. Sci. :–.

B.C. Ministry of Forests. . Forest, range and recreation resource analy-sis, . Victoria, B.C.

Brix, H. . Fertilization and thinning effect on a Douglas-fir ecosystemat Shawnigan Lake: a synthesis of project results. For. Can. / B.C.Min. For., Victoria, B.C. Rep. .

Brix, H. and A.K. Mitchell. . Thinning and nitrogen fertilizationeffects on soil and tree water stress in a Douglas-fir stand. Can. J.For. Res. :–.

Broadfoot, W.M. and R.E. Farmer, Jr. . Genotype and moisture supplyinfluence nutrient content of eastern cottonwood foliage. For. Sci.:–.

Brockley, R.P. . Response of thinned immature lodgepole pine tonitrogen and boron fertilization. Can. J. For. Res. :–.

_____. . Response of thinned, immature lodgepole pine to nitrogenfertilization. For. Can. / B.C. Min. For., Victoria, B.C. Rep. .

_____. . Effects of fertilization on the nutrition and growth of a slow-growing Engelmann spruce plantation in south-central BritishColumbia. Can. J. For. Res. :–.

_____. . Effects of nitrogen source and season of application on thenutrition and growth of lodgepole pine. Can. J. For. Res.:–.

Brockley, R.P. and F.J. Sheran. . Foliar nutrient status and fascicleweight of lodgepole pine after nitrogen and sulphur fertilization inthe interior of British Columbia. Can. J. For. Res. :–.

Brockley, R.P., R.L. Trowbridge, T.M. Ballard, and A.M. Macadam. .Nutrient management in interior forest types. In Forest fertilization:sustaining and improving nutrition and growth of western forests.H.N. Chappell, G.F. Weetman and R.E. Miller (editors). Univ. Wash.Inst. For. Resources Contrib. , pp. –.

Brown, K. and K.O. Higginbotham. . Effects of carbon dioxide enrich-ment and nitrogen supply on growth of boreal tree seedlings. TreePhysiol. :–.

Brown, K.R. . Carbon dioxide enrichment accelerates the decline innutrient status and relative growth rate of Populus tremuloidesMichx. seedlings. Tree Physiol. :–.

Brown, K.R., W.A. Thompson, E.L. Camm, B.J. Hawkins, and R.D. Guy.a. Effects of N addition rates on the productivity of Piceasitchensis, Thuja plicata, and Tsuga heterophylla seedlings. II. Photo-synthesis, 13C discrimination and N partitioning in foliage. Trees:–.

Brown, K.R., W.A Thompson, and G.F. Weetman. b. Effects of Naddition rates on the productivity of Picea sitchensis, Thuja plicata,and Tsuga heterophylla seedlings I. Growth rates, biomass allocationand macroelement nutrition. Trees :–.

Bryant, J.P., T.P. Clausen, P.B. Reichardt, M.C. McCarthy, and R.A. Werner.. Effect of nitrogen fertilization upon the secondary chemistryand nutritional value of quaking aspen (Populus tremuloides Michx.)leaves for the large aspen tortrix (Choristoneura conflictana(Walker)). Oecologia :–.

Bryant, J.P., P.B. Reichardt, T.P. Clausen, and R.A. Werner. . Effects ofmineral nutrition on delayed inducible resistance in Alaska paperbirch. Ecology :–.

Cahill, J.M. and D.G. Briggs. . Effects of fertilization on wood qualityand tree value. In Forest fertilization: sustaining and improvingnutrition and growth of western forests. H.N. Chappell, G.F. Weet-man and R.E. Miller (editors). Univ. Wash. Inst. For. Resources,Contrib. , pp. –.

Carlson, M. . Municipal effluent irrigation of fast-growing hybridpoplar plantations near Vernon, British Columbia. For. Chron.:–.

Carlysle, J.C. . Relationships between nitrogen uptake, leaf area, waterstatus and growth in an -year-old Pinus radiata plantation inresponse to thinning, thinning residue, and nitrogen fertiliser. For.Ecol. Manage. :–.

Carter, R.E. and R.P. Brockley. . Boron deficiencies in British Colum-bia: diagnosis and treatment evaluation. For. Ecol. Manage. :–.

Carter, R.E and K. Klinka . Use of ecological site classification in theprediction of forest productivity and response to forest fertilization.S. Afr. For. J. :–.

Carter, R.E., E.R. McWilliams, and K. Klinka. . Predicting response ofcoastal Douglas-fir to fertilizer treatments. For. Ecol. Manage.:–.

Ceulemans, R., G.E. Scarascia-Mugnozza, B.M. Wiard, J.H. Braatne, T.M.Hinckley, R.F. Stettler, J.G. Isebrands, and P.E. Heilman. . Pro-duction physiology and morphology of Populus species and theirhybrids grown under short rotation. Can. J. For. Res. :–.

Ceulemans, R., R.F. Stettler, T.M. Hinckley, J.G. Isebrands, and P.E. Heil-man. . Crown architecture of Populus clones as determined by

branch orientation and branch characteristics. Tree Physiol.:–.

Chapin, F.S. III. . The mineral nutrition of wild plants. Ann. Rev.Ecol. Syst. :–.

Chapin, F.S. III and R.A. Kedrowski. . Seasonal changes in nitrogenand phosphorus fractions and autumn retranslocation in evergreenand deciduous taiga trees. Ecology :–.

Chapin, F.S. III, P.R. Tryon, and K. van Cleve. . Influence of phospho-rus supply on growth and biomass allocation of Alaskan taiga treeseedlings. Can. J. For. Res. :–.

Chapin, F.S. III and K. van Cleve. . Approaches to studying nutrientuptake, use and loss in plants. In Plant physiological ecology. Fieldmethods and instrumentation. R.W. Pearcy, J. Ehleringer, H.A.Mooney and P.W. Rundel (editors). Chapman and Hall, New York,N.Y., pp. –

Chapin, F.S. III, K. van Cleve, and P.R. Tryon. . Relationship of ionabsorption to growth rate in taiga trees. Oecologia :–.

Chappell, H.N., S.A.Y Omule, and S.P. Gessel. . Fertilization in coastalnorthwest forests: using response information in developing stand-level tactics. In Forest fertilization: sustaining and improving nutri-tion and growth of western forests. H.N. Chappell, G.F. Weetmanand R.E. Miller (editors). Univ. Wash. Inst. For. Resources, Contrib., pp. –.

Chen, S.G., R. Ceulemans, and I. Impens. . A fractal-based Populuscanopy structure model for the calculation of light interception. For.Ecol. Manage. :–.

Cole, D.W. and S.P. Gessel. . Fundamentals of tree nutrition. In Forestfertilization: sustaining and improving nutrition and growth ofwestern forests. H.N. Chappell, G.F. Weetman and R.E. Miller (edi-tors). Univ. Wash. Inst. For. Resources, Contrib. , pp. –.

Comeau, P., G. Harper, B. Biring, P. Fielder, and B. Reid. . Effects ofred alder on stand dynamics and nitrogen availability project-RE ( .). B.C. Min. For. Research Program.Extension Note .

Comeau, P.G., G.J. Harper, M.E. Blache, J.O. Boateng, and K.D. Thomas(editors). . Ecology and management of B.C. hardwoods. For.Canada / B.C. Min. For., Victoria, B.C. Report No. .

Compton, J.E. . Phosphorus distribution and cycling under redalder:implications for second-rotation alder growth and nutrition.MS thesis, Univ. Wash., Seattle, WA.

Compton, J.E., P.S. Homann, and D.W. Cole. . Leaf element concen-trations and soil properties in successive rotations of red alder. Can.J. For. Res. :–.

Conroy, J.P., R.M. Smillie, M. Kuppers, D.I. Bevege, and E.W. Barlow. .Chlorophyll a fluorescence and photosynthetic and growth responsesof Pinus radiata to phosphorous deficiency, drought stress and highCO2. Plant Physiol. :–.

Courtin, P.J. . The relationships between ecological site quality andthe site index and stem form of red alder in southwestern B.C. MFthesis, Univ. B.C., Vancouver, BC.

Coyne, P.I. and K. van Cleve. . Fertilizer-induced morphological andchemical responses of a quaking aspen stand in interior Alaska. For.Sci. :–.

Critchfield, W.B. . Leaf dimorphism in Populus trichocarpa. Am. J.Bot. :–.

_____. . Shoot growth and heterophylly in Acer. J. Arnold Arboretum:–.

Curlin, J. . Clonal differences in yield response of Populus deltoides tonitrogen fertilization. Proc. Soil Sci. Soc. Am. :–.

DeBell, D.S. and M.A. Radwan. . Foliar chemical concentrations inred alder stands of various ages. Plant Soil :–.

DeBell, D.S., M.A. Radwan, C.A. Harrington, G. Clendenen, J.C. Zasada,W.R. Harms, and M. McKevlin. . Increasing the productivity ofbiomass plantations of cottonwood and alder in the Pacific North-west. Ann. Tech. Rep. //–//, U.S. Dep. Energy Contract--.

DeKock, P.C., A. Hall, and R.H.E. Inkson. . Active iron in plant leaves.Ann. Bot. :–.

Dickmann, D.I. and K.W. Stuart. . The culture of poplars in easternNorth America. Hickory Hollow Associates, Dansville, MI.

Diggle, P.K. . Forest fertilization in interior British Columbia: the For-est Service approach. In Forest fertilization: sustaining and improv-ing nutrition and growth of western forests. H.N. Chappell, G.F.Weetman and R.E. Miller (editors). Univ. Wash. Inst. For. Resources,Contrib. , pp.–.

Dobkowski, A., P.F. Figueroa, and Y. Tanaka. . Red alder plantationestablishment. In The biology and management of red alder. D.E.Hibbs, D.S. DeBell and R.F. Tarrant (editors). Oreg. State Univ.Press, Corvallis, OR., pp. –.

Enns, K.A., E.B. Peterson, and D. McLennan. . Impacts of hardwoodmanagement on British Columbia wildlife: problem analysis. For.Canada / B.C. Min. For., Victoria, B.C. Rep. .

Entry, J.A., K. Cromack, R.G. Kelsey, and N.E. Martin. . Response ofDouglas-fir to infection by Armillaria ostoyae after thinning or thin-ning plus fertilization. Phytopathology :–.

Ericsson, T., L. Rytter, and S. Linder. . Nutritional dynamics andrequirements of short rotation forests. In Ecophysiology of short-rotation forest crops. C.P. Mitchell, J.B. Ford-Robertson, T. Hinckley,and L. Sennerby-Forse (editors). Elsevier Science Publishers, London,UK, pp. –.

Evans, J.R. . Photosynthesis and nitrogen relationships in leaves of C

plants. Oecologia :–.

Field, C. and H.A. Mooney. . The photosynthesis-nitrogen relationshipin wild plants. In On the economy of plant form and function.T. Givnish (editor). Cambridge University Press, Cambridge, UK,pp. –.

Fodor, F., B. Boddi, E. Sarvari, G. Zaray, E. Cseh, and F. Lang. . Corre-lation of iron content, spectral forms of chlorophyll andchlorophyll-proteins in iron-deficient cucumber (Cucumis sativus).Physiol. Plant. :–.

Friend, A.L., J.A. Mobley, E.A. Ryan, and H.D. Bradshaw. . Root plas-ticity of hybrid poplar in response to soil nutrient gradients. InFrontiers of forest biology. Joint Meeting Nor. Am. For. Biol.Workshop and West. For. Gen. Assoc. Victoria, BC. Abstr. No. .

Fyles, J.W., B. Cote, F. Courchesne, W.H. Hendershot, and S. Savoie. .Effects of base cation fertilization on soil and foliage nutrient con-centrations, litterfall and throughfall nutrient fluxes in a sugar mapleforest. Can J For Res :–.

Gara, R.I. and L.L. Jaeck. . Insect pests of red alder: potential prob-lems. In Utilization and management of red alder. D.G. Briggs, D.S.DeBell, and W.A. Atkinson (compilers). For. Serv. Gen. Tech.Rep. -, pp. –.

Garnier, E., G.W. Koch, J. Roy, and H.A. Mooney. . Responses of wildplants to nitrate availability. Relationships between growth rate andnitrate uptake parameters, a case study with two Bromus species,and a survey. Oecologia :–.

Giardina, C.P., S. Huffman, D. Binkley, and B.A. Caldwell. . Aldersincrease soil phosphorus availability in a Douglas-fir plantation.Can. J. For. Res. :–.

Glaubig, B.A. and F.T. Bingham. . Boron toxicity characteristics offour northern California endemic tree species. J. Env. Qual. :–.

Godbout, C. and J.A. Fortin. . Synthesized ectomycorrhizae of aspen:fungus genus level of structural characterization. Can. J. Bot.:–.

Gordon, J.C. and L.C. Promnitz. . Photosynthetic and enzymatic crite-ria for the early selection of fast-growing Populus clones. In Treephysiology and yield improvement. M.G.R. Cannell and J.T. Last(editors). Academic Press, New York, NY., pp. –.

Gorge, J. Lopez, O. Lastra, A. Chueca and M. Lachica. . Use of photo-synthetic parameters for the diagnosis of copper deficiency in Pinusradiata seedlings. Physiol. Plant. :–.

Green, R.N. and R.E. Carter. . Boron and magnesium fertilization of acoastal Douglas-fir plantation. West. J. Appl. For. :–.

Green, R.N. and K. Klinka. . A field guide for site identification andinterpretation for the Vancouver Forest Region. B.C. Min. For., Vic-toria, B.C. Land Manage. Handb. No. .

Greenwood, M. . The effect of phase change on annual growth incre-ment in eastern larch (Larix laricina (Du Roi) K.Koch). Ann. Sci.For. (suppl): s–s.

Grime, J.P. . Plant strategies and vegetation processes. John Wiley &Sons, New York, NY.

Hafner, H., B.J. Ndunguru, A. Bationo, and H. Marschner. . Effect ofnitrogen, phosphorus and molybdenum application on growth andsymbiotic N2-fixation of groundnut in an acid sandy soil in Niger.Fert. Res. :–.

Haissig, B.E. . Metabolic processes in adventitious rooting ofcuttings. In New root formation in plants and cuttings. M.B. Jackson(editor). Martinus Nijhoff, Zoetermeer, The Netherlands,pp. –.

Hakulinen, J. . Nitrogen-induced reduction in leaf phenolic level isnot accompanied by increased rust frequency in a compatible willow(Salix myrsinifolia)-Melampsora rust interaction. Physiol. Plant.:–.

Hansen, E.A. . A guide for determining when to fertilize hybridpoplar plantations. For. Serv. Res. Pap. NC-.

Harrington, C.A. and R.O. Curtis. . Height growth and site indexcurves for red alder. For. Serv. Res. Pap. -.

Harrington, C.A. and D.S. DeBell. . Effects of irrigation, spacing andfertilization on flowering and growth in young Alnus rubra. TreePhysiol. :–.

Harrington, C.A., M.A. Radwan, and D.S. DeBell. . Leaf characteristicsreflect growth rates of -year-old Populus trees. Can. J. For. Res.:–.

Harrison, R., D. Xue, and C.L. Henry. . Sludge fertilization on coarse-textured, nutrient-deficient soils: the potential for secondary nutrientdeficiency. In Forest fertilization: sustaining and improving nutritionand growth of western forests. H.N. Chappell, G.F. Weetman andR.E. Miller (editors). Univ. Wash., Inst. For. Resources, Contrib. ,pp. – (poster abstract).

Harvey, H.P. . Relationships between mineral nutrition, drought

resistance and clone in Populus. PhD dissertation, University of Vic-toria, Victoria, BC.

Harvey, H.P. and R. van den Driessche. . Nutrition, xylem cavitationand drought resistance in hybrid poplar. Tree Physiol. :–.

Haynes, R.J. . Effects of liming on phosphate availability in acid soils.Plant Soil :–.

Heilman, P.E. . Sampling and genetic variation of foliar nitrogen inblack cottonwood and its hybrids in short rotation. Can. J. For. Res.:–.

_____. . Sustaining production : nutrient dynamics and soils. In Eco-physiology of short-rotation forest crops. C.P. Mitchell, J.B. Ford-Robertson, T. Hinckley, and L. Sennerby-Forse (editors). ElsevierScience Publishers, London, UK, pp. –.

Heilman, P.E. and R.F. Stettler. . Nutritional concerns in selection ofblack cottonwood and hybrid clones for short rotation. Can. J. For.Res. :–.

Heilman, P.E. and Xie, F-G. . Influence of nitrogen on growth andproductivity of short-rotation Populus trichocarpa × Populus deltoideshybrids. Can. J. For. Res. :–.

Hinckley, T.M., R. Ceulemans, J.M. Dunlap, A. Figiola, P.E. Heilman, J.G.Isebrands, G. Scarascia-Mugnozza, P.J. Schulte, B. Smit, R.F. Stettler,E. van Volkenburgh, and B.M. Wiard. . Physiological, morpho-logical and anatomical components of hybrid vigor in Populus. InStructural and functional responses to environmental stresses. K.R.Kreeb, H. Richter, and T.M. Hinckley (editors). SPB Publishing, TheHague, pp.–.

Hirose, T. . Modelling the relative growth rate as a function of plantnitrogen concentration. Physiol. Plant. :–.

Hopmans, P. and H.N. Chappell. . Growth response of young,thinned Douglas-fir stands to nitrogen fertilizer in relation to soilproperties and tree nutrition. Can. J. For. Res. :–.

Host, G.E., H.M. Rauscher, J.G. Isebrands, D.I. Dickmann, R.E. Dickson,T.R. Crow, and D.A. Michael. . Microcomputer scientific soft-ware series . The user’s manual. For. Serv. Gen.Tech. Rep. NC-.

Hoyle, M.C. . Plantation birch: what works, what doesn’t. J. Forestry:–.

Huettl, R.F. and H.W. Zoettl. . Liming as a mitigation tool inGermany’s declining forests-reviewing results from former andrecent trials. For Ecol. Manage. :–.

Hunter, M.D. and J.C. Schultz. . Fertilization mitigates chemicalinduction and herbivore responses within damaged oak trees. Ecol-ogy :–.

Ingestad, T. . Mineral nutrient requirements of Pinus sylvestris andPicea abies seedlings. Physiol. Plant. :–.

_____. . Growth, nutrition and nitrogen fixation in grey alder at var-ied rate of nitrogen addition. Physiol. Plant. :–.

_____. . Relative addition rate and external concentration: drivingvariables used in plant nutrient research. Plant Cell Env. :–.

_____. . New concepts on soil fertility and plant nutrition as illus-trated by research on forest trees and stands. Geoderma:–.

_____. . A fertilization model based on the concepts of nutrient fluxdensity and nutrient productivity. Scand. J. For. Res. :–.

Ingestad, T. and M. Kahr. . Nutrition and growth of coniferousseedlings at varied relative nitrogen addition rate. Physiol. Plant.:–.

Israel, D.W. . Investigation of the role of phosphorus in symbioticdinitrogen fixation. Plant Physiol. :–.

Jackson, R.D. . Remote sensing of biotic and abiotic plant stress. Ann.Rev. Phytopath. :–

Jalkanen, R.E., D.B. Redfern, and L.J. Sheppard. . Nutrient deficitsincrease frost hardiness in Sitka spruce (Picea sitchensis) needles. For.Ecol. Manage. :–.

Jia, H. and T. Ingestad. . Nutrient requirements and stress response ofPopulus simonii and Paulownia tomentosa. Physiol. Plant. :–.

Jones, M.D., D.M. Durall, S.M.K. Harniman, D.C. Classen, and S.W.Simard. . Ectomycorrhizal diversity on Betula papyrifera andPseudotsuga menziesii seedlings grown in the greenhouse or out-planted in single-species and mixed plots in southern BritishColumbia. Can. J. For. Res. :–.

Kabzems, R.D. and K. Klinka. a. Initial quantitative characterization ofsoil nutrient regimes. I. Soil properties. Can. J. For. Res. :–.

Kabzems, R.D. and K. Klinka. b. Initial quantitative characterization ofsoil nutrient regimes. II. Relationships among soils, vegetation, andsite index. Can. J. For. Res. :–.

Kayahara, G.J., R.E. Carter, and K. Klinka. . Site index of westernhemlock (Tsuga heterophylla) in relation to soil nutrient and foliarchemical measures. For. Ecol. Manage. :–.

Kayahara, G.J. and A.F. Pearson. . Relationships between site index,and soil moisture and nutrient regimes for western hemlock andSitka spruce. B.C. Min. For., Victoria, BC. Working Pap. .

Klinka, K., M.C. Feller, R.N. Green, D.V. Meidinger, J. Pojar, and J.Worrall. . Ecological principles: applications. In RegeneratingBritish Columbia’s forests. D.P. Lavender, R. Parish, C.M. Johnson,

G. Montgomery, A. Vyse, R.A. Willis, and D. Winston (editors). UBCPress, Vancouver, BC, pp. –.

Knoepp, J.D., D.P. Turner, and D.T. Tingey. . Effects of ammoniumand nitrate on nutrient uptake and activity of nitrogen assimilatingenzymes in western hemlock. For. Ecol. Manage. :–.

Kramer, P.J. and T.T. Kozlowski. . Physiology of woody plants. Acade-mic Press, New York, NY.

Kozlowski, T.T. and J.J. Clausen. . Shoot growth characteristics of het-erophyllous woody plants. Can. J. Bot. :–.

Kriedemann, P.E., R.D. Graham, and J.T. Wiskich. . Photosyntheticdysfunction and in vivo changes in chlorophyll a fluorescence frommanganese-deficient wheat leaves. Aust. J. Agric. Res. :–.

Lambert. M.J. . Sulphur and nitrogen nutrition and their interactiveeffects on Dothistroma infection in Pinus radiata. Can. J. For. Res.:–.

Larson, P.R. and J.G. Isebrands. . The relation between leaf productionand wood weight in first-year root sprouts of two Populus clones.Can. J. For. Res. :–.

Leech, R.H. and Y.T. Kim. . Foliar analysis and as a guide to fer-tilizer amendments in poplar plantations. For. Chron. :–.

L’Hirondelle, S.J., J.S. Jacobson, and J.P. Lassoie. . Acidic mist andnitrogen fertilization effects on growth, nitrate reductase activity, gasexchange and frost hardiness of red spruce seedlings. New Phytol.:–.

Li, B., S.E. McKeand, and H.L. Allen. . Genetic variation in nitrogenuse efficiency of loblolly pine seedlings. For. Sci. :–.

Li, M., M. Osaki, I.M. Rao, and T. Tadano. . Secretion of phytase fromthe roots of several plant species under phosphorus-deficient condi-tions. Plant Soil :–.

Linder, S. and D.A. Rook. . Effects of mineral nutrition on carbondioxide exchange and partitioning of carbon in trees. In Nutrition ofplantation forests. G.D. Bowen and E.K.S. Nambiar (editors). Acade-mic Press, Orlando, FL., pp. –.

Ljungstrom, M. and B. Nihlgard. . Effects of lime and phosphate addi-tions on nutrient status and growth of beech (Fagus sylvaticus L.)seedlings. For. Ecol. Manage. :–.

Lodge, D.J. . The influence of soil moisture and flooding on forma-tion of VA-endo- and ectomycorrhizae in Populus and Salix. PlantSoil :–.

Lovell, P.H. and J. White. . Anatomical changes during adventitiousroot formation. In New root formation in plants and cuttings. M.B.

Jackson (editor). Martinus Nijhoff, Zoetermeer, The Netherlands,pp. –.

McLennan, D.L. . Growth and nutrient relations in black cottonwoodin south coastal British Columbia. PhD dissertation, University ofBritish Columbia, Vancouver, BC.

McLennan, D.L. . The nature of nutrient limitation in black cotton-wood stands in south coastal British Columbia. In Ecology andmanagement of B.C. hardwoods. P.G. Comeau, G.J. Harper, M.E.Blache, J.O. Boateng, and K.D. Thomas (editors) For. Canada / B.C.Min. For., Victoria, BC. Report No. ., pp. –.

McLennan, D.L. and A-M. Mamias. . Cottonwoods in British Colum-bia: problem analysis. For. Canada / B.C. Min. For., Victoria, BC. Rep. .

McMurtrie, R.E. . Modelling of canopy carbon and water balance. InPhotosynthesis and production in a changing environment. D.O.Hall, J.M.O. Scurlock, H.R. Bolhar-Nordenkampf, R.C. Leegood, andS.P. Long (editors). Chapman and Hall, New York, NY, pp. –.

McMurtrie, R., D.A. Rook, and F.M. Kelliher. . Modelling of yield ofPinus radiata on a site limited by water and nitrogen. For. Ecol.Manage. :–.

Majid, N.M. and T.M. Ballard. . Effects of foliar application of coppersulphate and urea on the growth of lodgepole pine. For. Ecol. Man-age. :–.

Marshall, V.G. and D.S. DeBell. . Comparison of four methods ofmeasuring volatilization losses of nitrogen following urea fertiliza-tion of forest soils. Can. J. Soil Sci. :–

Marschner, H. . Mineral nutrition in higher plants. nd ed. AcademicPress, New York, NY.

Massie, M.R.C., E.B. Peterson, N.M. Peterson, and K.A. Enns. . Anassessment of the strategic importance of the hardwood resource inBritish Columbia. For. Canada / B.C. Min. For., Victoria, BC. Rep. .

Mattson, W.J. and S.R. Palmer. . Changes in levels of foliar mineralsand phenolics in trembling aspen, Populus tremuloides, in responseto artificial defoliation. In Mechanisms of woody plant defensesagainst insects: search for pattern. W.J. Mattson, J. Levieux, and C.Bernard-Dagan (editors). Springer-Verlag, New York, NY, pp. –.

Menge, J.A., L.F. Grand and L.W. Haines. . The effect of fertilizationand mycorrhizae numbers in -year-old loblolly pine plantations.For. Sci. :–.

Mika, P.G. and J.A. Moore. . Foliar potassium status explainsDouglas-fir response to nitrogen fertilization in the Inland North-west. Water, Air, and Soil Pollution :–.

Mika, P.G., J.A. Moore, R.P. Brockley, and R.F. Powers. . Fertilizationresponse by interior forests: when, where and how much? InForest fertilization:sustaining and improving nutrition and growthof western forests. H.N. Chappell, G.F. Weetman, and R.E. Miller(editors). Univ. Wash. Inst. For. Resources, Contrib. , pp. –.

Miller, H.G., J.D. Miller, and J.M. Cooper. . Optimum foliar nitrogenconcentration in pine and its change with stand age. Can. J. For.Res. :–.

Miller, R.E., J.R. Boyle, A.E. Harvey, T.M. Ballard, L.M. Palazzi, and R.F.Powers. . Fertilizers and other means to maintain long-termproductivity of western forests. In Forest fertilization: sustaining andimproving nutrition and growth of western forests. H.N. Chappell,G.F. Weetman, and R.E. Miller (editors). Univ. Wash. Inst. For.Resources, Contrib. , pp. –.

Miller, R.E., D.H. McNabb, and J. Hazard. . Predicting Douglas-firgrowth and response to nitrogen fertilization in western Oregon.Soil. Sci. Soc. Amer. J. :–.

Mitchell, A.K. and T.M. Hinckley. . Effects of foliar nitrogen concen-tration on photosynthesis and water use efficiency in Douglas-fir.Tree Physiol. :–.

Mitchell, R.J., H.E. Garrett, G.S. Cox, and A. Atalay. . Boron and ecto-mycorrhizal influences on mineral nutrition of container-grownPinus echinata Mill. J. Plant Nutrition :–.

Molina, R., D. Myrold, and C.Y. Li. . Root symbioses of red alder:technological opportunities for enhanced regeneration and soilimprovement. In The biology and management of red alder. D.E.Hibbs, D.S. DeBell, and R.F. Tarrant (editors). Oreg. State Univ.Press, Corvallis, OR., pp. –.

Moore, J.A. and P.G. Mika. . Influence of soil parent material on thenutrition and health of established conifer stands in the inlandnorthwest. In Symposium proceedings on Forest Seedling Nutritionfrom the Nursery to the field. D.L. Haase and R. Rose (editors).Nursery Tech. Coop., Oregon State Univ., Corvallis, OR., pp. –.

Nambiar, E.K.S. and D.N. Fife. . Growth and nutrient retranslocationin needles of radiata pine in relation to nitrogen supply. Ann. Bot.:–.

Nasholm, T. and A.J.S. McDonald. . Dependence of amino acidcomposition upon nitrogen availability in birch (Betula pendula).Physiol. Plant. :–.

Nason, G.E. and D.D. Myrold. . Nitrogen fertilizers: fates and environ-mental effects in forests. In Forest fertilization: sustaining andimproving nutrition and growth of western forests. H.N. Chappell,G.F. Weetman, and R.E. Miller (editors). Univ. Wash. Inst. For.Resources, Contrib. , pp. –.

Nelson, E.E., E.M. Hansen, C.Y. Li, and J.M. Trappe. . The role of redalder in reducing losses from laminated root rot. In Utilization andmanagement of red alder. D.G. Briggs, D.S. DeBell, and W.A. Atkin-son (compilers). USDA For. Serv. Gen. Tech. Rep. -,pp. –.

Newcome, G., G.A. Chastagner, W. Schuette, and B.J. Stanton. . Mor-tality among hybrid poplar clones in a stool bed following leaf rustcaused by Melampsora medusae f.sp. deltoidae. Can. J. For. Res.:–.

Nilsson, L.O. and D. Wasielewski. . Influence of fertilization in a nat-ural Populus tremula stand. Scand. J. For. Res. :–.

Oliver, C.D. and B.C. Larson. . Forest stand dynamics. McGraw-Hill,New York, NY.

Olson, J.R. . Experience with nitrogen fertilization in northern Idaho.In Forest fertilization: sustaining and improving nutrition andgrowth of western forests. In H.N. Chappell, G.F. Weetman, and R.E.Miller (editors). Univ. Wash. Inst. For. Resources, Contrib. , pp.–.

Oren, R., K.S. Werk, N. Buchmann, and R. Zimmerman. .Chlorophyll-nutrient relationships identify nutritionally causeddecline in Picea abies stands. Can. J. For. Res. :–.

Owens, J.N. and M. Molder. . Bud development in western hemlock. I.Annual growth cycle of vegetative buds. Can. J. Bot. :–.

Pederson, L. a. Queen Charlotte Timber supply area. Rationale forAAC determination effective May , . B.C. Min. For., Victoria,BC.

_____. b. Strathcona Timber supply area. Rationale for determi-nation effective May , . B.C. Min. For., Victoria, BC.

Peeler, R. and D.S. DeBell. . Variation in damage from growing-seasonfrosts among open-pollinated families of red alder. For. Serv.Res. Note --.

Perala, D.A. and A.L. Alm. . Reproductive ecology of birch: a review.For. Ecol. Manage. :–.

Peterson, E.B., R.D. Kabzems, and N.M. Peterson. . Hardwood man-agement problems in northeastern British Columbia: an informationreview. For. Can. / B.C. Min. For., Victoria, BC. Rep .

Peterson, E.B. and N.M. Peterson. . Ecology, management and use ofaspen and balsam poplar in the prarie provinces. For. Can. NWRegion Spec. Rep. .

Peterson, E.B. and N.M. Peterson, . Aspen managers’ handbook forBritish Columbia. For. Canada / B.C. Min. For., Victoria, BC. Rep. .

Peterson, E.B., N.M. Peterson, and D.S. McLennan. . Blackcottonwood and balsam poplar managers’ handbook for BritishColumbia. For. Canada / B.C. Min. For., Victoria, BC. Rep. .

Plank, M.E. and S. Willits. . Wood quality, product yield and eco-nomic potential. In The biology and management of red alder.D.E. Hibbs, D.S. DeBell, and R.F. Tarrant (editors). Oreg. State Univ.Press, Corvallis, OR., pp. –.

Pollard, D. . Leaf area development on different shoot types in ayoung aspen stand and its effect upon production. Can. J. Bot.:–.

Powers, R.F. . Fertilization response of Abies subalpine forests in Cali-fornia. In Forest fertilization: sustaining and improving nutritionand growth of western forests. H.N. Chappell, G.F. Weetman, andR.E. Miller (editors). Univ. Wash. Inst. For. Resources, Contrib., pp. –

Pregitzer, K.S. and A.L. Friend. . The structure and function of Popu-lus root systems. In Biology of Populus. R.F. Stettler, H.D. Bradshaw,Jr., P.E. Heilman, and T.M. Hinckley (editors). NRC Research Press,Ottawa, ON., pp. –.

Pugnaire, F.I. and F.S. Chapin III. . Environmental and physiologicalfactors governing nutrient resorption efficiency in barley. Oecologia:–.

Radwan, M.A. . Effects of fertilization on growth and foliar nutrientsof red alder seedlings. For. Serv. Res. Pap. --.

Radwan, M.A. and D.S. DeBell. . Fertilization and nutrition of redalder. In The biology and management of red alder. D.E. Hibbs, D.S.DeBell, and R.F. Tarrant (editors). Oreg. State Univ. Press, Corvallis,OR., pp. –.

Raettig, T.L., K.P. Connaughton, and G.R. Ahrens. . Hardwood supplyin the Pacific Northwest: a policy perspective. For. Serv. Res.Pap. --.

Raiimakers, D., R.G.A. Boot, P. Dijkstra, S. Pot, and T. Pons. . Photo-synthetic rates in relation to leaf phosphorus content in pioneer ver-sus climax tropical rainforest trees. Oecologia :–.

Reich, P.B., M.B. Walters, D.S. Ellsworth, and C. Uhl. . Photosynthesis-nitrogen relations in Amazonian tree species. I. Patterns amongspecies and communities. Oecologia :–.

Robison, D. and K.F. Raffa. . Characterization of hybrid poplar clonesfor resistance to the forest tent caterpillar. For. Sci. :–.

Safford, L.O. . Silvicultural guide for paper birch in the Northeast. For. Serv. Res. Pap. -. Revised.

Sands, R. and D.R. Mulligan. . Water and nutrient dynamics and treegrowth. For. Ecol. Manage. :–.

Schier, G.A. and J.C. Zasada. . Role of carbohydrate reserves in thedevelopment of root suckers in Populus tremuloides. Can. J. For. Res.:–.

Seiler, J.R. and L.H. McCormick. . Effects of soil acidity and phospho-rus on the growth and nodule development of black alder. Can. J.For. Res. :–.

Simard, S. and A. Vyse. . Ecology and management of paper birch andblack cottonwood in southern British Columbia. B.C. Min. For., Vic-toria, BC. Land Manage. Rep. No. .

Smirnoff, N. and G.R. Stewart. . Nitrate assimilation and translocationby higher plants: comparative physiology and ecological conse-quences. Physiol. Plant. :–.

Sun, J.S., R.J. Simpson, and R. Sands. . A leaf phosphorus assay forseedlings of Acacia mangium. Tree Physiol. :–.

Tamm, C-O. . An attempt to assess the optimum nitrogen level inNorway spruce under field conditions. Stud. For. Suec. :–.

Tan, W. and G.D. Hogan. . Effects of nitrogen limitation on waterrelations of jack pine (Pinus banksiana Lamb.) seedlings. Plant CellEnv. :–.

Teachman, G.E., D.J. Frederick, W.E. Perkis, and M.F. Jurgensen. .Effects of fertilization on Hypoxylon canker of trembling aspen.Plant Disease :–.

Teng, Y. and V.R. Timmer. . Phosphorous-induced micronutrient dis-orders in hybrid poplar. I. Preliminary diagnosis. Plant Soil:–.

Tew, R.K. . Root carbohydrate reserves in vegetative reproduction ofaspen. For. Sci. :–.

Thies, W.G. and R.N. Sturrock. . Laminated root rot in North Amer-ica. For. Serv. Res. Bull. --.

Timmer, V.R. . Response of a hybrid poplar clone to soil acidificationand liming. Can. J. Soil Sci. :–.

Timmer, V. R. . Interpretation of seedling analysis and visual symp-toms. In Mineral nutrition of conifer seedlings. R. van den Driessche(editor). CRC Press, Boca Raton, FL., pp. –.

Tisdale, S.L., W.L. Nelson and J.D. Beaton . Soil fertility and fertilizers.th ed. MacMillan, New York, NY.

Tschaplinski, T.J. and T.J. Blake. . Correlation between early root pro-duction, carbohydrate metabolism and subsequent biomass produc-tion in hybrid poplar. Can. J. Bot. :–.

Tschaplinski, T.J. and R.J. Norby. . Physiological indicators of nitrogenresponse in a short-rotation sycamore plantation. II. Nitrogenmetabolism. Can. J. Bot. :–.

Turner, J., M.J. Lambert, and S.P. Gessel. . Use of foliage sulphate con-centrations to predict response to urea application by Douglas-fir.Can. J. For. Res. :–.

Valentine, D.W. and H.L. Allen. . Foliar responses to fertilizationidentify nutrient limitation in loblolly pine. Can. J. For. Res.:–.

van Cleve, K. and L. Oliver. . Growth response of post-fire quakingaspen (Populus tremuloides Michx.) to N, P, and K fertilization. Can.J. For. Res. :–.

van den Burg, J. . Foliar nutrient analysis for determination of treenutrient status: a compilation of literature data. Rijksinstitut voorOnderzoek in the Bos-en Landschapboniv “De Dorsch Kamp”.Wageningen, The Netherlands.

van den Driessche, R. . Nutrient storage, retranslocation and relation-ship of stress to nutrition. In Nutrition of plantation forests. G.D.Bowen and E.K.S. Nambiar (editors). Academic Press, Orlando, FL.,pp. –

_____. . Response of Douglas-fir (Pseudotsuga menziesii (Mirb.)Franco) to some different fertilizers applied at planting. New For.:–.

_____. . Are differences in formulations of fertilizers important? InSymposium proceedings on Forest Seedling Nutrition from theNursery to the field. D.L. Haase and R. Rose (editors). Nursery Tech.Cooperative, Oreg. State Univ., Corvallis, OR., pp. –.

_____.[]. Comparison of banding and placement fertilization of fourPopulus trichocarpa × P. deltoides clones after planting. Can. J. For.Res. In press.

van den Driessche, R. and J.E. Webber. . Total and soluble nitrogen inDouglas-fir in relation to plant nitrogen status. Can. J. For. Res.:–.

van Miegroet. H.M., D.W. Cole, and P.S. Homann. . The effect ofalder forest cover and alder forest conversion on site fertility andproductivity. In Sustained productivity of forest soils. S.P. Gessel,D.S. Lacate, G.F. Weetman, and R.F. Powers (editors). Proc. th N. A.For. Soils Conf., pp. –.

van Miegroet, H.M., R.J. Norby, and T.J. Tschaplinski. . Nitrogen fer-tilization strategies in a short-rotation sycamore plantation. For.Ecol. Manage. :–.

Viro, P.J. . Fertilization of birch. Commun. Inst. For. Fenn. ().

Vose, P.B. . Genetical aspects of mineral nutrition-progress to date.In Proc. Second International Symp. on Genetic Aspects of PlantMineral Nutrition. W.H. Gabelman and BC Loughman (editors).Dev. in Plant and Soil Sciences :–.

Wang, J. and B.J. van der Kamp. . Resistance, tolerance and yield ofwestern black cottonwood infected by Melamspora rust. Can. J. For.Res. :–.

Wang, Q., G.C. Wang, K.D. Coates, and K. Klinka. . Use of sitefactors to predict lodgepole pine and interior spruce site index inthe sub-boreal spruce zone. B.C. Min. For., Victoria, B.C. Res. NoteNo. .

Waring, R.H., A.J.S. McDonald, S. Larsson, T. Ericsson, A. Wiren, E.Arwidsson, A. Ericsson, and T. Lohammar. . Differences inchemical composition of plants grown at constant relative growthrates with stable mineral nutrition,. Oecologia :–.

Weetman, G.F., R. Fournier, J. Barker and E. Schnorbus-Panozzo. b.Foliar analysis and response of fertilized chlorotic western hemlockand western red cedar reproduction on salal-dominated cedar-hemlock cutovers on Vancouver Island. Can. J. For. Res.:–.

Weetman, G.F., R. Fournier, J. Barker, E. Schnorbus-Panozzo, and A. Ger-main. a. Foliar analysis and response of fertilized chlorotic Sitkaspruce plantations on salal-dominated cedar-hemlock cutovers onVancouver Island. Can. J. For. Res. :–.

Weetman, G.F., R.M. Fournier, and E. Schnorbus. . Lodgepole pinefertilization screening trials: four year growth response following ini-tial predictions. Soil Sci. Soc. Amer. J. :–.

Weetman, G.F., C.E. Prescott, F.L. Kohlberger, and R.M. Fournier. .Ten-year growth response of coastal Douglas-fir on Vancouver Islandto N and S fertilization in an optimum nutrition trial. Can. J. For.Res. :–.

Weetman, G.F., E.R.G. McWilliams, and W.A. Thompson . Nutrientmanagement of coastal Douglas-fir and western hemlock stands: theissues. In Forest fertilization: sustaining and improving nutritionand growth of western forests. H.N. Chappell, G.F. Weetman, andR.E. Miller (editors). Univ. Wash. Inst. For. Resources, Contrib. ,pp. –

Weetman, G.F. and C.G. Wells. . Plant analyses as an aid in fertilizingforests. In Soil testing and plant analysis. rd ed. R.L. Westerman(editor). Book Series. Soil Sci. Soc. Am., Madison, WI.,pp. –.

Wessman, C.A., J.D. Aber, D.L. Peterson, and J.M. Melillo. . Foliaranalysis using near-infrared reflectance spectroscopy. Can. J. For. Res.:–.

Wickman, B.E., R.R. Mason, and H.G. Paul. . Thinning and nitrogenfertilization in a grand fir stand infested with western spruce bud-worm. Part II. Tree growth response. For. Sci. :–.

Yang, R.C. . Fertilization: a tool for managing aspen in westernCanada. For. Can. NW Region, For. Manage. Note .

Yoder, B.J. and R.E. Pettigrew-Crosby. . Predicting nitrogen andchlorophyll content and concentrations from reflectance spectra(– nm) at leaf and canopy scales. Remote Sens. Environ.:–.

Zabek, L.M. . Optimum fertilization of hybrid poplar plantations incoastal British Columbia. MS thesis, Univ. B.C., Vancouver, BC.