Forest Ecology and Management 277 (2012) 38–45

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Forest Ecology and Management

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Effects of repeated fertilization of young Norway spruce on foliar phenolicsand arthropods: Implications for insectivorous birds’ food resources

Lars Edenius a,⇑, Grzegorz Mikusinski b,c, Johanna Witzell d, Johan Bergh d

a Department of Wildlife, Fish, and Environmental Sciences, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Swedenb Grimsö Wildlife Research Station, Department of Ecology, Swedish University of Agricultural Sciences, SE-7310 91 Riddarhyttan, Swedenc School for Forest Management, Swedish University of Agricultural Sciences, Box 43, SE-739 21 Skinnskatteberg, Swedend Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, Box 49, SE-230 53 Alnarp, Sweden

a r t i c l e i n f o a b s t r a c t

Article history:Received 29 February 2012Received in revised form 16 April 2012Accepted 17 April 2012

Keywords:Intensive forestryFertilizationBirdsFoliar chemistryPhenolicsArthropods

0378-1127/$ - see front matter � 2012 Elsevier B.V. Ahttp://dx.doi.org/10.1016/j.foreco.2012.04.021

⇑ Corresponding author. Tel.: +46 90 786 8341; faxE-mail address: lars.edenius@slu.se (L. Edenius).

Repeated fertilization of young forests is a promising concept to increase the production of wood fiber,but the consequences of intense fertilization regimes on forest birds and their food resources, mediatedthrough changes in the foliar chemistry are inadequately known. We assessed the effects of repeated fer-tilization in stands of young Norway spruce (Picea abies) on foliar phenolics and arthropods in an inten-sively managed forest area in southern Sweden in relation to the abundance of arboreal feeding birdsbreeding in the same stands. We anticipated leaf-sucking arthropods (viz. Hemiptera (aphids)) to reactmore strongly to changes in foliar phenolics than other invertebrate groups. Overall, we found smalleffects of fertilization on abundance and composition of different groups of foliar arthropods. However,the abundance of Hemiptera was much higher in early spring in fertilized stands than in unfertilizedstands, whereas mites (Anactinotrichida and Actinotrichida) were more abundant in late spring in thefertilized stands. On the contrary, springtails (Collembola) were more abundant in unfertilized standsthan in fertilized stands the late spring. The concentrations of two of the most abundant phenolics(hydroxycinnamic acid derivatives) as well as the sum concentration of HPLC-phenolics, were consis-tently lower in the fertilized stands. Positive effects on arthropod abundance mediated trough changesin the foliar chemistry following fertilization could help to explain why resident Goldcrest (Regulusregulus), which feeds on folivorous arthropods (i.e. aphids) during winter, was found to be more commonin the fertilized stands (Edenius et al., 2011). Our results suggest that in intensively managed forest areasrepeated fertilization of young spruce has the potential to enhance the suitability of these stands as win-ter feeding habitat for coniferous foliage-gleaning insectivorous birds compared to unfertilized stands inthe same developmental stage. However, intensification of forest management further impedes habitatquality for more specialized species and generally reduces the diversity of forest birds by simplifyingstructure and composition of forest stands and shortening the rotation period. Therefore, careful planningof spatial arrangement of treatment units with different management, retention of natural forest and/orstructures and legacies such as dead wood and deciduous trees are necessary to promote avian diversityin intensified forest management schemes.

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1. Introduction

The productivity of high-latitude forests is to a large extent lim-ited by the availability of nitrogen (Tamm, 1991). It has been dem-onstrated that supplementary nitrogen provided throughfertilizers can largely increase the production of wood fiber bio-mass in these forests in comparison with traditional silviculturalmanagement (e.g. Kenk and Fischer, 1988). In Scandinavia, it hasbeen suggested that the repeated applications of fertilizers toyoung stands of Norway spruce (Picea abies) can increase produc-

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tion of stem wood up to 300% (Bergh et al., 2005, 2008). Sincethe demands for wood fiber and biofuels are expected to grow sig-nificantly in the near future (Raunikar et al., 2010), the interest ofincreasing biomass production in existing forests is growing (e.g.Nabuurs et al., 2007). Therefore, the perspective of intensificationof biomass production in high-latitude forests through supplemen-tary nitrogenous fertilizer application becomes very attractivefrom an economical point of view. However, intensification offorestry may cause undesirable changes in forest ecosystems,including biodiversity loss (Hartmann et al., 2010; Strengbom etal., 2011).

Among different groups of forest organisms, avian communitiesare often negatively affected by intensification of silviculture

L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45 39

(Imbeau et al., 2001; Järvinen et al., 1977; Vanderwel et al., 2009;Virkkala, 2004). These effects are linked to the structural simplifi-cation of forest stands (fewer tree species, less dead wood, youngerstands with lack of big and old trees), fragmentation of formerlycontiguous forest landscapes through clear-cutting, and finally vir-tual lack of most important disturbance agent, i.e. fire (Edenius andElmberg, 1996; Imbeau et al., 2001; Söderström, 2009). Hole-nest-ing birds including woodpeckers, sedentary, highly specialized andarea demanding species are most negatively affected by such alter-ation of forest ecosystems (Angelstam and Mikusinski, 1994; Im-beau et al., 2001; Schmiegelow and Mönkkönen, 2002). All thesespecies are generally rare or absent in intensively managed forestlandscapes. However, also among the relatively common forestbird species one may expect differences in community structuredepending on the type of silviculture (e.g. Lance and Phinney,2001). One mechanism behind such variation at the stand andlandscape levels may be linked to the main food basis for a largeshare of the forest birds, namely foliar arthropods.

Site productivity and diversity and abundance of canopy arthro-pods have been shown to be positively correlated. Recher et al.(1996) for example, demonstrated that in eucalypt forests, therichest and most abundant arthropod faunas occurred on sites withthe greatest soil fertility and in the tree species with highest levelsof foliage nutrients (i.e. nitrogen and phosphorous). Furthermore,the authors attributed the higher diversity of birds in these sitesto the above pattern. The change of site productivity by additionof fertilizer may also affect the structure and functioning of arbo-real communities by increasing abundance of organisms in severaltrophic levels as experimentally shown in oak stands (Forkner andHunter, 2000). In extreme cases, fertilization may even, at leasttemporally, increase the overall biodiversity as demonstrated byRowe et al. (2006) in primary succession.

Edenius et al. (2011) found that three arboreal insectivorousbird species had higher abundance in young spruce stands sub-jected to repeated fertilization than in unfertilized stands in thesame development stage. This result raises the question whetherresource-based bottom-up forces regulate food resources for arbo-real birds. A specific group of plant chemicals, phenolic com-pounds, have frequently been pointed out as important factorsdetermining the preferences and performance of phytophagousarthropods (Lindroth et al., 1988; Simmonds, 2003), and the effectsof fertilization on concentrations of phenolics have been investi-gated in numerous studies. Several of these investigations have fo-cused on the basic concept that fertilization reduces theconcentration of defensive phenolics in plants while the vegetativegrowth is increased (see Glynn et al., 2003; Herms and Mattson,1992; Rowe et al., 2006), in parallel the abundance and perfor-mance of arthropods on fertilized plants is expected to increase(Kytö et al., 1996; Wait et al., 1998). However, the experimentalevidence has not always provided unequivocal support for thesenotions (Dudt and Shure, 1994; Hamilton et al., 2001). Some ofthe factors that seem to complicate the issue are the different re-sponses by individual phenolic compounds or groups of phenolicsto treatments, the large temporal and spatial variation in plantchemical quality, the often non-linear effect of experimental fertil-ization treatments and versatile role of phenolics in plants (Closeand McArthur, 2002; Gripenberg et al., 2007; Riipi et al., 2002).To be able to understand the effects of intensive fertilization onforest biodiversity, it is important to study if bottom-up regulatoryforces can be activated by this silvicultural practice, and if it causeschanges in structure of arboreal communities.

In this study, conducted in the same stands as work by Edeniuset al. (2011), we address the above question by investigating theeffect of fertilization on foliar phenolics and abundance of foliararthropod groups in young Norway spruce forest. We hypothesizedthat any effect of fertilization conveyed on arthropods and further

onto birds could operate through the dynamics of the chemicalquality of foliage. More specifically, we expected that (1) the effectof fertilization on the pool of phenolic metabolites would be highlycompound-specific, leading to altered phenolic pattern rather thanto a general reduction in their concentration in foliage. Moreover,we expected that (2) fertilization might alter (most likely reduce)the temporal dynamics in phenolic concentrations during thegrowth season. Finally, we anticipated that (3) different types of fo-liar arthropods would respond to fertilization-induced alterationsin plant quality differently. Thus, we expected that the abundanceof arthropods belonging to the groups that are direct herbivores onthe needles, i.e. sucking arthropods such as Hemiptera (aphids),would be readily altered by the changed quality of needles as feed-ing substrate (Kytö et al., 1996), while omnivorous or predatoryspecies might show less obvious changes. We also discuss whetherthe observed changes in phenolics and abundance of arthropodscould explain the previously (Edenius et al., 2011) reported pat-terns in avian fauna in the same experimental treatment units.

2. Materials and methods

2.1. Study area

The study area is located in Toftaholm in the hemi-boreal zonein southern Sweden (57�00’ N/14�09’ E) (Ahti et al., 1968). The basi-cally flat (145–170 m asl) terrain is dominated by Norway spruceforest intermixed with patches of deciduous forest and lakes. Themean annual temperature, based on 1961–1990 data, is 6.5 �C,(15 �C in July, �1.5 �C in January). The mean annual precipitationis ca. 800 mm, with highest amount in July–August and Novem-ber–December (Raab and Vedin, 1994). The number of days withprecipitation is about 200 per year, i.e. the climate is characterizedas humid. The mean site productivity, expressed in the H100-indexsystem (tree height at 100 years of age), varies between 30 and34 m, which is relative high for the region. Toftaholm was severelyaffected by the Gudrun storm in January 2005, which felled >50% ofthe standing tree volume. Young forest stands thus abound in thearea.

Since 2003, approximately 35 ha of young Norway spruce havebeen fertilized repeatedly every second year in Toftaholm. On eachoccasion, 100–125 kg ha�1 of nitrogen was distributed by machin-ery from the ground along skid roads transecting the fertilizedstands at 40–50 m regular distance. We compared fertilized andunfertilized young spruce stands distributed over a c. 15 km2 largearea. Four fertilized stands and 12 unfertilized stands, i.e. 16 standsin total were used. All available fertilized stands were used andmany more unfertilized stands were included to cover as large gra-dient as possible in stand characteristics among young intensivelymanaged spruce stands in the area. The investigated stands spans6–27 years in age (Table 1). Stands were subjected to intensive sil-viculture including mechanical cleaning and pre-commercial thin-ning of deciduous trees (birch, Betula spp.). We did not use standsthat had been recently cleaned or thinned to avoid the confoundingeffects of these treatments in the analyses.

2.2. Foliar phenolics and arthropod surveys

The sampling of foliar chemistry and arthropods was done atlocations directly linked to bird survey points (Edenius et al.,2011). Thirty survey points were located in the 16 stands, with be-tween one and four points per stand depending on the size of thestand such that each survey point represented approximately 3–4 ha of forest. In larger stands survey points were located randomlywithin 50 m from stand borders whereas in smaller stands the

Table 1Characteristics of fertilized and unfertilized Norway spruce stands surveyed. Means (range; standard error).

Category No. ofstands

Area (ha) Age (years) Height (m) Stem volumeof spruce(m3 ha�1)

Branch weight(50 cm length)

Volume birch(m3 ha�1)

Variation instem density(CV%)

Canopyclosure (%)

Fertilized 4 7.3 (4.6–13.4; 2.0) 12 (11–13; 0.6) 9.6 (9.3–9.9; 0.2) 58 (45–90; 11) 71 (60–83; 8) 2.5 (0–5; 1.4) 45 (24–72; 12) 41 (11–13; 0.6)Unfertilized 12 7.1 (3–18.6; 1.3) 14.5 (6–27; 1.9) 10 (5.6–12.9; 0.6) 89 (5–280; 24) 69 (44–116; 18) 5.8 (0–20; 2.3) 37 (21–69; 4) 41 (6–27; 1.9)

40 L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45

survey point was located at the center of the stand. Multiple surveypoints in stands were at least 100 m apart.

The two spruce trees closest to the center of the survey pointwere chosen for arthropod and chemical surveys. At each tree,two 50 cm branches were clipped at 1.5–2.5 m height at the north-ern (shaded) side of the tree. Branches for arthropod surveys wereimmediately put in bags and stored in a �18 �C freezer. Needlesamples were extracted from the branches and allowed to dry inpaper bags at room temperature for chemical analysis. Branchsamples were collected from the same spruce trees at two occa-sions, April 8 and May 29, 2010, in order to account for temporalaspects in foliar chemistry and arthropod occurrence. In total 24050 cm branch samples were collected for analysis of arthropodoccurrence and phenolics. In the lab the frozen branches were firstweighted and then vigorously shaken and storage bags meticu-lously cleaned to standardize extraction of arthropods. The col-lected specimen were classified to order (sub-order) but in caseof springtails (Collembola) to class only.

For extraction of phenolic chemicals, the dried needles weremilled into a homogenous powder. The samples harvested on April8 contained only previous year’s needles, whereas the samples har-vested on May 29 contained both current and previous year’s nee-dles. We could not observe any differences in leaf flush phenologybetween fertilized and unfertilized stands. Thus, composite sam-ples of needles were used in phenolic analyses, presuming thatthe foliage that was analyzed represented the available habitatfor the studied arthropods at the time point of harvest. Ten mgof each sample was extracted with HPLC grade methanol followingthe protocol of Witzell et al. (2003). The phenolics were separatedon coupled into a Merck Hitachi LaChrom HPLC system consistingof a D-7100 pump, D-7200 autosampler, D-7300 column oven (setat 35 �C) and a D-7455 DAD detector scanning the absorbance be-tween 220 and 400 nm. Separation on an Aquasil C18 column(Thermo Scientific, Waltham, MA, USA) was achieved using a gra-dient of water (acidified with o-phosphoric acid to pH 3; A) andmethanol (B) as follows: 0% B (0–1 min); 5–45% B (1–15 min);45–85% B (15–20 min); 85% B (20–23 min) and 85–100% B (23–25 min), 100% B (25–27 min), followed by equilibration to initialconditions. The flow rate was 0.8 ml/min and the injection volumewas 10 ll. The peak area data for eight individual compounds andthe sum area of all detected compounds were collected at 320 nm,allowing quantification of mainly phenolic acids and flavonoids,and expressed as peak area (AU) �10�5 (Nagle et al., 2011) normal-ized against sample weight per each injection (hereafter referred toas concentration). UV-spectrum collected at 200–400 nm were

Table 2Mean abundance per 50 cm branch of folivorous arthropods in fertilized and unfertilized

Order (class) Suborder

AraneaeAnactinotrichida and ActinotrichidaCollembolaHemiptera Sternorrhyncha and AuchenorrhyncColeopteraHymenoptera ApocritaDiptera

compared to spectral data in a standard compound library andthe compounds were tentatively identified if their spectrumexhibited a match of 99% or better against that of a known withauthentic standard analyzed under same or similar conditions (p-coumaric acid and ferulic acid derivatives, (+)-catechin), or basedon published spectra (resveratrol derivative; Watts et al., 2006).The tannic fraction was not analyzed in this study, instead we fo-cused on individual phenolics because the compound-specificmetabolism has been pointed out as an important factor in tree-herbivores (Ikonen, 2001; Salminen et al., 2004a; Ingersoll et al.,2010), and because individual phenolics are known to vary in theirreactivity to fertilization treatments (e.g. Hakulinen et al., 1995).

2.3. Data analysis

Stem volume of spruce was extracted from the stand recorddata. Besides spruce and birch there were almost no other tree spe-cies in the stands. The arthropod and chemical data were averagedper stand (N = 16) and analyzed separately with respect to order(class) in case of arthropods. Generalized linear modeling (GLM)was employed to analyze the data. Fertilization was added as a bin-ary (1, 0) effect variable in the analyses, and volume of spruce,branch weight and sampling period were used as ancillary explan-atory variables. The spruce volume data were log-transformed be-fore analysis in order to homogenize the variance. The coefficientof variation (CV, i.e. standard deviation divided by mean, (Zar,1999) was calculated for individual and total sum of phenolics tocompare the relative variability in concentrations between treeswithin fertilized and control stands. Differences were consideredsignificant at the p < 0.05-level.

3. Results

In terms of arthropod abundance per 50 cm branch, springtails(Collembola) were the dominant group, followed by Anactinotrich-ida and Actinotrichida (mites), Araneae (spiders) and Hemiptera(aphids) (Table 2, Fig. 1). Other groups of arthropods (Plecoptera,Psocoptera, Lepidoptera) were much less common and thereforenot analyzed further. The total sample size of the more abundantarthropod groups amounted to 1863 specimens. Among analyzedarthropods, there were a higher number of taxonomic groups rep-resented in late spring in comparison to early spring. In both typesof stands Hymenoptera and Coleopterans were virtually absent inthe earlier sampling period. The abundance of mites in fertilizedstands was 60 times lower in early spring in comparison to late

young Norway spruce stands in Toftaholm.

Fertilized stands (N = 4) Unfertilized stands (N = 12)

0.5 0.72.1 1.23.0 4.2

ha 0.8 0.30.1 0.10.3 0.20.1 0.2

Fig. 1. Abundance of arboreal arthropods per 50 cm branch in fertilized and unfertilized spruce stands in Toftaholm in early spring and late spring. Means ± 1 SE.

L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45 41

spring, making this group quantitatively dominant in the lattersampling period (54% of all individuals). In unfertilized stands in-stead, springtails were the most abundant group in both periods(79% and 49% of all individuals in early and late spring, respec-tively). On average, abundance of the more numerous arthropodsamounted to 7.0 per branch, being lowest (5.2) in unfertilizedstands (early spring) and highest (8.5) in unfertilized stand in latespring. We found significant effect of sampling period on the abun-dance pattern of Araneae, Collembola and Hemiptera (Table 3).Hemiptera were more common in early spring in fertilized standsthan in unfertilized stands (0.9 vs. 0.02 specimens per branch,Fig. 1, Table 3). On the contrary, springtails (Collembola) weremore abundant in unfertilized stand than in fertilized stands inthe late spring. Additionally, Anactinotrichida and Actinotrichida(mites) were more abundant in fertilized stands compared tounfertilized stands in late spring. However, except for Hemipteraour GLM-model did not detect any fertilization induced effect onthe abundance of arthropods (Table 3). The effect of branch weightand volume of spruce on Hemiptera abundance was positive andnegative, respectively.

The GLM-analysis revealed a clear temporal aspect in concen-tration of two individual phenolics, tentatively identified as (+)-catechin and isoferulic acid and the sum concentration of HPLCphenolics, which all were higher in early than in late spring,regardless of the fertilization regime (Table 3, Fig. 2). The concen-tration of the same individual phenolics and the sum concentrationof HPLC phenolics were significantly lower in the fertilized standsthan in the unfertilized stands (Table 3, Fig. 2).). In fertilized trees,the sum concentration of HPLC phenolics was reduced by 31% be-tween early and late spring measurements, while for the unfertil-ized trees the corresponding reduction was slightly higher (44%,Fig. 2). With one exception (a putative resveratrol derivative in latespring), the coefficient of variation for the individual phenolics andthe sum of phenolics was lower for the samples collected fromtrees in fertilized stands, as compared to the samples collectedfrom trees in the unfertilized stands (Table 4).

To take the analysis of the effect of fertilization on abundanceof Hemiptera one step further, we combined the arthropodanalysis and the phenolic compound analysis. More specifically,we included sampling period, treatment, branch weight and the

Table 3P-Values from the GLM-analysis of the effects of treatment (fertilization), branch weight, spruce volume and time on arthropod abundance and foliar phenolics in fertilized andunfertilized young Norway spruce stands.

Treatment Branch weight Spruce volume Time

(a) ArthropodsAraneae 0.601 0.416 0.196 <0.001Anactinotrichida and Actinotrichida 0.120 0.209 0.087 0.214Collembola 0.601 0.416 0.196 <0.001Hemiptera 0.033 0.038 0.048 <0.001

(b) Phenolics(+)-Catechin 0.013 0.067 0.645 0.004Isoferulic acid 0.038 0.775 0.201 0.005p-Coumaric acid 0.221 0.011 0.189 0.414Resveratrol derivative 0.808 0.643 0.248 0.386Caffeic acid derivative 0.366 0.044 0.056 0.554Ferulic acid derivative 0.320 0.371 0.488 0.257Unknown 0.073 0.196 0.310 0.341Unknown 0.563 0.399 0.433 0.769Sum of HPLC phenolics 0.007 0.232 0.754 0.001

42 L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45

interaction between branch weight and treatment, and each of thephenolic compounds for which fertilization had a significant effect((+)-catechin, isoferulic acid, sum of HPLC phenolics; Table 3). Withthe interaction between treatment and branch weight in the mod-el, none of the effect variables were significant except samplingperiod; removing the interaction term resulted in a significant ef-fect of fertilization and isoferulic acid on Hemiptera abundance(p = 0.023 and 0.038, respectively).

4. Discussion

Our results indicate a clear distinction in the occurrence ofarthropods and chemical quality of Norway spruce foliage betweenthe early and late sampling period. This is in agreement with theresults of several earlier studies that have shown temporal fluctu-ations in arthropod distribution patterns in woody plants, as wellas temporal heterogeneity in plant quality (Gripenberg et al.,2007; Riipi et al., 2002; Salminen et al., 2004b). Decreasing concen-trations of some methanol extractable foliar phenolics have beenreported also in other studies (Covelo and Gallardo, 2001; Nurmiet al., 1996; Witzell et al., 2003). Whether or how the frequencyor diversity of invertebrates on the studied trees was affected bythe within-seasonal variation in secondary chemistry is difficultto assess, and may be highly dependent on the feeding mode. How-ever, by rendering the plant quality temporally unpredictable, sea-sonal fluctuations in secondary chemicals may protect the plantsagainst the invertebrates that react to secondary chemicals as feed-ing deterrents or cues (Gripenberg et al., 2007). If fertilization mit-igates this variation in young Norway spruce forests, as our dataimplies (the difference in sum concentration of phenolics betweenearly and late spring measurements was slightly smaller in fertil-ized trees than in unfertilized trees), herbivores may encounter aqualitatively more uniform and thus less risky habitat in these for-est stands. The lower CV values for phenolics measured in needlesof the fertilized trees also suggest that fertilization reduced thevariability in phenolic concentrations. This in turn can reduce var-iation in distribution, abundance and performance of invertebrateherbivores and increase the likelihood of locally adapted inverte-brate demes to arise at the level of individual trees (cf. Gripenberget al., 2007).

The observed reduction in concentration of two of the mostabundant individual foliar phenolics (that largely dictated the re-sponse of the total sum of HPLC phenolics), but not in others, in fer-tilized young Norway spruce trees is in agreement with severalearlier studies on fertilized woody plants (Hakulinen et al., 1995;Stolter et al., 2010; Witzell and Shevtsova, 2004) . The fertilization

effect on these two compounds and the sum amount of phenolicswas significant and consistent at both time points, indicating thatthe effect was not transient. Catechins and ferulic acids have beenpointed out as important compounds in plant defense againstinvertebrate herbivores (Leiss et al., 2009; Stenberg et al., 2006),and their relevance for herbivore defense could be related to theirfunctions as precursors for biopolymers that are hard to digest, i.e.condensed tannins, built up of catechin units (Khanbabaee and vanRee, 2001) and lignin, for which ferulic acid is a metabolic interme-diate (Boerjan et al., 2003), The reduced concentrations of thesecompounds in the foliage of intensively fertilized young Norwayspruce trees may thus exert bottom-up force on certain inverte-brate foliar invertebrates. In our study this might have been thecase for Hemiptera, i.e. leaf-sucking arthropods that were mostabundant in fertilized trees in April. Hemiptera have been foundto readily respond to nutrient additions also in other studies(Kytö et al., 1996; Rowe et al., 2006). In addition, aphids are linkedto arboreal habitat throughout the year while other arthropods areoften dependent on other environments in different stages of theirlife. Besides the positive effect of fertilization on Hemiptera abun-dance, there was a positive effect of branch weight and a negativeeffect of spruce volume. In other words, small trees with heavybranches were more likely to host higher abundance of aphids thanbig trees with light branches irrespective of fertilization treatment.This pattern may possibly be related to a higher needle density ofheavier branches, providing more habitat for arthropods. Needledensity may also promote aphid abundance indirectly by relaxingpredation risk by insectivorous birds, although the evidence forthis hypothesis is inconclusive (Gunnarssson, 1996). One groupof arthropods that was quite abundant on spruce in mature standin other study in Sweden (Pettersson et al., 1995) but almost ab-sent in the present study was Psocoptera. However, these herbi-vores are mostly feeding on lichens that are generally uncommonin young forests.

The abundance of several groups of arthropods in this studyincreased between sampling periods i.e. early and late spring.This difference was particularly distinct in the case of mites. Ithas been observed that arboreal community of arthropods hasmuch higher abundance and biomass in summer in comparisonto winter (e.g. Hijii, 1989). This pattern is explained by increasingavailability of food after winter for all different guilds of arthro-pods that occur in the canopy, i.e. ranging from detritivores andphytophages to parasitoids and predatory species. The arborealmicrohabitats that become suitable may be colonized in springby individuals originating from the soil stratum (e.g. Bowden etal., 1976).

Fig. 2. Peak areas at 320 nm for eight individual foliar phenolics and their sum amount in fertilized and unfertilized spruce stands in early spring (April 8, 2010) and latespring (May 29, 2010). Means ± 1 SE.

L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45 43

Simultaneously collected data on the avian fauna on the samesurvey points (Edenius et al., 2011) allow us to make inferencesabout the ecological significance of our findings with respect forthe role of the arthropods as food for foliage-gleaning insectivorousbirds. After controlling for forest structure and composition, Ede-nius et al. (2011) found three bird species to be more common inthe fertilized stands: Lesser Whitethroat (Sylvia curruca), GardenWarbler (Sylvia borin) and Goldcrest (Regulus regulus). The firsttwo species are migratory, whereas the Goldcrest is primarily res-ident. In contrast to the two other species, the Goldcrest is innorthern latitudes highly associated with coniferous trees (Tiainen

et al., 1983; Ulfstrand, 1976). Moreover, Norway spruce appears tobe especially important for Goldcrest as foraging substrate (seeCramp, 1992). It has been demonstrated in other studies performedin coniferous plantations in southern Sweden that spruce trees arethe most common feeding substrate for Goldcrest during breedingseason (Ulfstrand, 1976). The Goldcrest was the most numerousresident species in both types of surveyed stands (Edenius et al.,2011). Studies on diet of Goldcrest indicate that Hemiptera, Col-lembola and spiders are important food items for the species(Cramp, 1992). Hemiptera appears to be important through theyear including breeding period, spiders in late winter while

Table 4Coefficient of variation for concentrations of eight individual phenolics and sum of HPLC phenolics in Norway spruce needles from unfertilized and fertilized stands in early spring(April 8) and late spring (May 29) of 2010.

Time (+)-Catechin

Isoferulicacid

p-Coumaricacid

Resveratrolderivative

Caffeic acidderivative

Ferulic acidderivative

Unknown Unknown Sum of HPLCphenolics

Control Earlyspring

0.53 0.32 0.60 0.58 0.74 0.52 0.34 0.33 0.24Fertilized 0.17 0.18 0.42 0.24 0.40 0.32 0.28 0.24 0.07Control Late

spring0.54 0.42 1.68 0.55 0.74 0.56 0.64 0.33 0.25

Fertilized 0.52 0.08 0.30 0.90 0.41 0.27 0.12 0.24 0.06

44 L. Edenius et al. / Forest Ecology and Management 277 (2012) 38–45

Collembola were found crucial as a food of newly-hatched young(Cramp, 1992). These taxonomic groups dominated among the fo-liar arthropod assembly in the surveyed stands. The higher abun-dance of Goldcrests in fertilized stands coincides with a higherabundance of Hemiptera in the late winter period, i.e. before theonset of spring. A study performed in Moscow region by Inozemt-sev (1964) showed great dominance of Homoptera (suborder ofHemiptera) in winter diet of the Goldcrest. The late winter periodhas been suggested as critical for the survival of resident birdsdependent on foliar arthropods (Pettersson et al., 1995). The pop-ulation dynamics of Goldcrests are characterized by strong annualfluctuations correlated to the harshness of the winter (Lindström etal., 2010). As the Goldcrest is intimately connected to coniferoustrees during winter, fertilization may therefore potentially increasesuitability of such stands as winter habitat and contribute to ahigher survival during harsh winters.

Our analysis does not offer any direct explanation why the Les-ser Whitethroat and Garden Warbler were more numerous in fer-tilized stands. Both species are ecologically more connected todeciduous trees than coniferous trees, but their occurrence wasnot correlated to the abundance of birch per se (Edenius et al.,2011). However, we cannot rule out an effect of fertilization onthe abundance of arthropods living on birch and subsequently onthese deciduous foliage-gleaning birds. Rowe et al. (2006) demon-strated clearly that fertilization may increase the abundance ofarthropods on birch. Moreover, as pointed out by Edenius et al.(2011), the by-effect of increased habitat heterogeneity imposedby the skid road system in the fertilized stands may be ofimportance.

In conclusion, our results confirm the compound-specific re-sponses of individual phenolic compounds to fertilization, and pro-vide some support for our hypotheses about the effect offertilization on the within-seasonal variation in phenolics. We alsofound an expected increase in the abundance of Hemiptera speciesin fertilized trees, but none of the other taxonomic groups exhib-ited any significant changes associated with fertilization per se.We attribute this pattern to the fact that among all groups ofarthropods in our study, the aphids as a group are directly depen-dent on the amount and quality of needles in terms of food re-source. This link appears to be much weaker and indirect in thecase of other arboreal arthropods. The combined results of the cur-rent study and investigation by Edenius et al. (2011) thus indicatethat the effect of fertilization on young Norway spruce stands maymodify food resources for arboreal birds mediated by changes inthe abundance of arthropod groups (mainly Hemiptera), and thatthese alterations may partly be driven by bottom-up regulation,i.e. altered chemical quality of the foliage. Furthermore, we mayexpect certain improvement of habitat quality through fertilizationfor some common bird species that are predators on folivorousarthropods. The feed-backs between trophic levels (e.g. throughpredation) may override the impacts of these alterations (Garibaldiet al., 2010; Marquis and Whelan, 1994; Strong et al., 2000). Be-cause such ecological feedbacks depend on complex trophic inter-actions and multiple environmental factors, they are likely to betemporally pending and spatially changeable. Therefore, it is

difficult to predict the effects of fertilization on the entire biologi-cal community, especially in long-term perspective.

5. Management recommendations

At the landscape level, the spatial and temporal patterns of for-est fertilization rather than its intensity per se, may be more crucialfor the conservation of arthropod and avian fauna. Thus, the impor-tance of careful spatial planning and inclusion of mitigation such astree retention and set-aside areas when employing intensified fer-tilization regimes in managed forests becomes obvious (Strengbomet al., 2011). Nevertheless, our current knowledge-base may still betoo limited to allow us to accurately predict the extent to whatintensive forest fertilization schemes should be applied to opti-mally meet the society’s goals of conservation, amount and timingof future timber supplies and carbon sequestration. In order to im-prove this knowledge-base, it is warranted to monitor the arthro-pod and avian fauna at both stand and landscape level during theintroduction of more intensive fertilization regimes and to conductmore detailed studies regarding the possible regulating or modify-ing effect of co-occurring deciduous forests.

Acknowledgements

We gratefully acknowledge the Swedish Energy Agency forfunding this study. Thanks to Johan Frisk, Södra, for help in plan-ning the fieldwork and Åke Nordström and Iryna Semashko forfield and lab work. The manuscript benefitted from the commentsby Raimo Virkkala, Knut Kielland and one anonymous reviewer.

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