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Inverse relationship between understory light and foliar nitrogen along productivity gradients of boreal forests J.M. Kranabetter and S.W. Simard
Abstract: The constraints of light and N on sapling growth in forest understories can covary with site productivity, but this reciprocal relationship is not always recognized when describing stand dynamics. To facilitate this, we examined light availability and foliar N status of understory subalpine fir (Abies lasiocarpa (Hook.) Nutt.) along natural productivity gradients of old-growth boreal forests in British Columbia, Canada. Understory light declined with soil fertility, from a high of 30% of full sun on poor sites to as low as 15% on very rich sites. In contrast, understory foliar N concentration (N%) of subalpine fir increased with soil fertility (ranging from 9.3 to 14.2 gkg–1) and paralleled asymptotic stand height, despite growing in the shade. Trends in foliar N% of the understory were comparable with overstory subalpine fir, and both increased in foliar N% with soil fertility more so than lodgepole pine (Pinus contorta Dougl. ex Loud.). Foliar N per unit leaf area of the suppressed understory was fairly consistent and relatively low (approximately 2.0 g Nm–2), suggesting no net change in the resource constraints to growth along the productivity gradient. The inherent linkages between soil fertility, light attenuation, and species N nutrition provides a useful framework for understanding regeneration dynamics over a full range of site potential. Re´sume´ : Les effets limitatifs de la lumie`re et N sur la croissance des gaules en sous-e´tage des foreˆts peuvent interagir avec la productivite´ de la station mais cette relation re´ciproque n’est pas toujours prise en compte dans la description de la dynamique des peuplements. Afin de pallier cette lacune, nous avons e´tudie´ la disponibilite´ de la lumie`re et le statut de N foliaire chez le sapin subalpin (Abies lasiocarpa (Hook.) Nutt.) en sous-e´tage le long de gradients de productivite´ dans de vieilles foreˆts bore´ales de la Colombie-Britannique, Canada. La lumie`re en sous-e´tage diminuait avec l’augmentation de la fertilite´ du sol, allant d’un maximum de 30 % du plein soleil dans les stations pauvres a` aussi peu que 15 % dans les sta` l’inverse, la concentration de N foliaire (N%) du sapin subalpin en sous-e´tage augmentait avec la fertiltions tre`s riches. A ite´ du sol, variant de 9,3 a` 14,2 gkg–1 paralle`lement au comportement asymptotique de la hauteur du peuplement, malgre´ qu’il croisse a` l’ombre. Les tendances de N% foliaire en sous-e´tage e´taient comparables a` celles du sapin subalpin dominant et N foliaire augmentait avec la fertilite´ du sol dans les deux cas, davantage que chez le pin tordu (Pinus contorta Dougl. ex Loud.). L’azote foliaire par unite´ de surface foliaire en sous-e´tage, ou` les arbres sont supprime´s, e´tait assez consistent et relativement faible (environ 2,0 g Nm–2), indiquant qu’il n’y avait pas de changements nets dans les effets limitatifs des ressources sur la croissance le long du gradient de productivite´. Le lien inhe´rent entre la fertilite´ du sol, l’atte´nuation de la lumie`re et la nutrition en N d’une espe`ce procure un cadre utile pour comprendre la dynamique de la re´ge´ne´ration pour toute la gamme de capacite´ de production des stations. [Traduit par la Re´daction]
Introduction Forest understory plants face multiple limitations to growth, primarily light, nutrients (especially N), and water (Chapin et al. 1987). Determining the response of tree species to combinations of resource limitations has been a central theme in forest ecology research, often through controlled greenhouse studies (e.g., Canham et al. 1996). Extrapolating results to forests requires quantifying limiting resources and species’ responses across biophysical graReceived 8 November 2007. Accepted 4 July 2008. Published on the NRC Research Press Web site at cjfr.nrc.ca on 26 August 2008. J.M. Kranabetter.1 British Columbia Ministry of Forests and Range, Bag 6000, Smithers, BC V0J 2N0, Canada. S.W. Simard. The University of British Columbia, 3601 – 2424 Main Mall, Vancouver, BC V6T 1Z4, Canada. 1Corresponding
author (e-mail:
[email protected]).
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dients of landscapes, as well as through time following cycles of disturbance. Continuous monitoring of site conditions and leaf photosynthetic rates can be difficult, however, and assessments through foliar attributes, especially N concentration (N%) and leaf morphology, can more simply quantify and integrate the multiple resource limitations affecting growth (Reich et al. 1997). Such simple indicators may become increasingly useful for assessing species’ responses to rapid shifts in growing environments from anthropogenic influences such as CO2 emissions and climate change (Norby and Iverson 2006). With respect to biophysical gradients, Coomes and Grubb (2000) described how limiting resources in mature forest understories can covary in a predictable manner with soil fertility. They reviewed studies showing that nutrient-poor or droughty sites typically have higher levels of light in the understory than richer sites because of more open canopies of less productive overstory trees. Conversely, light is likely more limiting to growth than deficiencies in N and water in
doi:10.1139/X08-096
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the darker understories of more productive stands on richer sites. Understory resource interactions in boreal or temperate forests have been evaluated primarily by sapling growth rates among different forest types (Carter and Klinka 1992; Walters and Reich 1997; Drever and Lertzman 2001; Kobe 2006), but few studies have extended the analysis to relationships among light, soil resources, and foliar attributes of understory trees across a wide edaphic range in unmanaged mature forests. One of the more fundamental yet poorly documented patterns is the relationship between soil fertility and foliar N status of understory trees. Under full light, foliar N% and leaf size generally parallel the supply of N from soil (van den Driessche 1974; Ingestad 1982), and N% correlates strongly with leaf photosynthetic capacity and productivity (Reich et al. 1995). These gradations in foliar N% have been widely applied in the diagnosis of site N deficiencies for even-aged stands (Walker and Gessel 1991; Carter 1992; Brockley 2001). With shading, however, foliar N% of saplings could be reduced irrespective of soil because of biomass allocation to shoots rather than roots, by losses in the potential of roots to absorb nutrients, or by reductions in N demand under low growth rates (Chapin 1991a, 1991b). Little consensus on foliar interpretation has been provided from experiments in partially-cut forests, where neutral, positive, or negative effects of light availability on foliar N% of understory saplings have been reported (e.g., Niinemets 1997; Lusk and Reich 2000; Kaelke et al. 2001; Kazda et al. 2004). Very few of these studies include measures of soil resources, however, which may be problematic if large fluctuations in soil N availability and foliar N% occur after overstory trees are removed (Titus et al. 2006; Walters et al. 2006). A second uncertainty in understory tree response is the interpretation of leaf morphology under dual resource gradients of soil fertility and light availability. There are large potential ranges in leaf mass and surface area owing to the phenotypic plasticity of sun- and shade-adapted leaves for most tree species (Givnish 1988). In addition, foliar response to soil N availability, especially after fertilization, often includes a change in leaf size (Binkley 1986), and foliar N status may be more relevant when interpreted on the basis of leaf content (such as N per unit leaf area (Na)) rather than concentration. With this index, however, it becomes potentially difficult to separate the effects of soils on foliar N status from the concurrent influence of shading on leaf morphology (Niinemets et al. 2001; Fownes and Harrington 2004; Portsmuth and Niinemets 2007). Consequently, the influence of soil fertility on understory saplings may be best isolated and quantified using foliar N% values (Kobe 2006), but ideally this relationship should be validated for each species of interest. In this study, we report on the relationships between natural gradients in soil productivity and understory light availability in the southern boreal forests of British Columbia and the corresponding patterns in understory foliar attributes (N% and Na) of subalpine fir (Abies lasiocarpa (Hook.) Nutt.). We tested the hypothesis that an inverse relationship exists between light attenuation and soil N availability along productivity gradients and explored the effects of shading and suppressed growth on foliar N status by comparing understory
Can. J. For. Res. Vol. 38, 2008
subalpine fir trees with codominant overstory trees (both subalpine fir and lodgepole pine (Pinus contorta Dougl. ex Loud.)). The results of this study will contribute to our understanding of the relationships among growth-constraining resources inherent to climax forests and provide insights into the interpretation of foliar N status.
Materials and methods Site description The southern boreal forest of British Columbia is designated as the Sub-boreal spruce biogeoclimatic zone (SBS) and is located in the montane landscape of the central interior, within the closed forest portion of the Cordilleran boreal region (Pojar 1996). SBS has a continental climate characterized by severe, snowy winters and relatively short, warm, moist summers. Upland coniferous forests comprise lodgepole pine (Pl), hybrid white spruce (Sx) (Picea glauca (Moench) Voss Picea englemanii Parry ex Engelm.), and subalpine fir (Bl). Soils are free of permafrost and are predominantly deep blankets of lacustrine sediments, glacialfluvial deposits, or glacial tills with coarse fragments of mixed lithology. The study sites were located in the moist cold subzone of SBS near Smithers, British Columbia, Canada (54849’N, 127810’W, 522 m a.s.l.). Smithers has a mean annual air temperature of 3.9 8C and mean annual precipitation of 513 mm (354 mm as rainfall; Environment Canada 2006). Four site series (represented by climax plant communities corresponding to different soil moisture and nutrient regimes; Pojar et al. 1987) were sampled to provide a wide range of upland edaphic conditions: xeric and poor Pl–Cladonia (02); mesic and medium Sx–Huckleberry (01); subhygric and rich Sx–Oak fern (06); and subhygric and very rich Sx– Devil’s club (09) (Banner et al. 1993). Site series are hereinafter referred to by their nutrient regime and plant association name (e.g., poor–Cladonia). Five transects, each containing one replicate of each site series, were located along a 25 km portion of the McDonnell Forest Service Road (54840’–47’N and 127816’–36’W) at approximately 900 m a.s.l. We were unable to find a suitable very rich–Devil’s club plot on the fourth transect, however, so the study was limited to 19 plots. Each plot was 50 m 30 m (0.15 ha) in size. Plots were separate and generally F
9.7a (0.1) 10.5ab (0.4) 10.7bc (0.4) 11.5c (0.5) 0.020
2.24ab (0.09) 1.92a (0.16) 1.91a (0.14) 2.52b (0.15) 0.036
68.7 (1.8) 63.9 (5.3) 58.9 (4.0) 76.3 (4.9) 0.090
3.16 (0.09) 3.15 (0.17) 3.48 (0.15) 3.68 (0.12) 0.057
Note: Values within columns followed by different letters are significantly different (p < 0.05).Values in parentheses are SEs. *Soil nutrient regimes: P, poor; M, medium; R, rich; VR, very rich.
shifting needle size resulted in no difference in foliar Na among poor, medium, and rich plant associations (Table 2). In keeping with this trend, understory Na increased only slightly with soil N availability (Fig. 4a) or stand height (p = 0.039, r2 = 0.26). Overstory foliar attributes Foliar N% values of the overstory subalpine fir and lodgepole pine also increased from poor to very rich plant associations, although more so for subalpine fir than lodgepole pine (Table 3). Other nutrients did not vary as strongly as N%; foliar P and K concentrations were constant across plant associations, while foliar S and Mg increased slightly from poor to very rich sites for subalpine fir and lodgepole pine, respectively (Table 4). For both species of overstory trees, foliar N% was linearly correlated with soil N availability, but the slope for subalpine fir was steeper than lodgepole pine (Fig. 5a). Foliar mass of overstory subalpine fir also increased significantly with soil fertility, but that of lodgepole pine did not (Table 3). Foliar Na of subalpine fir increased with soil fertility, more so than that of lodgepole pine (Table 3), and the positive linear relationship between Na and soil N availability was slightly steeper for subalpine fir than lodgepole pine (Fig. 4b). Foliar N% of the overstory was more variable than that of the understory, perhaps because of the smaller sample size, but the correlation with soil N availability was similar (Fig. 5b). In contrast, foliar Na of the illuminated overstory was generally higher and was more closely correlated with soil N availability than that of the shaded understory (Fig. 4).
Discussion The inverse relationship between soil fertility and light attenuation to the understory that we described was consistent with many forest ecosystems in the absence of large-scale disturbance (Coomes and Grubb 2000). Understory light
availability declined predictably with soil N supply, owing to the observed increase in crown size with taller trees and the increased cover of subalpine fir and hybrid spruce, which both cast more shade than lodgepole pine (Messier et al. 1998). The shift in tree species composition was most significant on medium–Huckleberry sites, accentuating the decline in light from poor–Cladonia to very rich–Devil’s club sites, as indicated by the curvilinear correlation with stand height. A minor amount of tree mortality resulting from bark beetles, root pathogens, and windthrow had occurred, and these small gaps contributed to microsite variability and perhaps limited the degree of shading on the most productive sites. In general, light limitation in these oldgrowth boreal stands was not as severe as in some temperate and coastal forests (e.g.,
