effects of elatobium abietinum on nutrient fluxes in sitka spruce canopies receiving elevated...

Effects of Elatobium abietinum on nutrient ¯uxes in Sitka sprucecanopies receiving elevated nitrogen and sulphur deposition

Bernhard Stadler*³, Thomas MuÈ ller², Lucy Sheppard³ and Alan Crossley³

*Bayreuth Institute for Terrestrial Ecosystem Research, University of Bayreuth, 95440 Bayreuth, Germany, ²Centre for Agricultural Landscape

and Land Use Research, MuÈncheberg, and Institute of Microbial Ecology and Soil Biology, Gutshof 7, 14641 Paulinenaue, Germany and

³Centre for Ecology and Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK

Abstract 1 In a ®eld acid mist simulation experiment, Sitka spruce (Picea sitchensis) was

sprayed with different pollutant treatments: N, NH4NO3; S, Na2SO4; NS Acid,

NH4NO3 + H2SO4 and control, no spray. Treatment effects on the abundance of

the green spruce aphid Elatobium abietinum and honeydew production were

assessed. In addition, needles were sampled for phyllosphere micro-organisms. In

a manipulative experiment, shoots were established and maintained as with or

without E. abietinum infestation in order to determine the effects of infestation

on needle loss and throughfall nutrient ¯uxes.

2 Aphid numbers were highest during the end of May and early June, with almost

twice as many needles infested in the NS Acid treatment compared with the

other treatments. Honeydew production was not affected by the treatments.

3 On infested shoots, increasing numbers of yellowing and dead needles were

recorded above the throughfall collectors as the season progressed. The numbers

of dead needles falling into the collectors were signi®cantly higher beneath

infested shoots. There were strong positive correlations between aphid numbers

above the throughfall collectors, the number of yellowing and dead needles on

the shoots and the number of needles in the funnels of the throughfall collectors.

Litter production was more affected by aphid number than by pollutant treat-

ment.

4 Bacteria, yeasts and ®lamentous fungi were more proli®c on infested needles and

treatment effects on colony forming units (CFUs) were most pronounced in the

NS Acid treatment.

5 Fluxes of inorganic nitrogen beneath infested shoots were generally lower than

beneath uninfested shoots. This effect was more pronounced in those treatments

that supplied N i.e. N, NS Acid. The combination of aphid infestation and N-

addition exerted the strongest in¯uence on nutrient ¯uxes. The ¯uxes of potas-

sium and of organic carbon (DOC) were higher beneath infested shoots in all

treatments, through most of the survey period.

Keywords Elatobium abietinum, epiphytic micro-organisms, forested ecosystems,

honeydew, nutrient cycling, pollutants, wet deposition.

Introduction

The response of forested ecosystems to the deposition of

pollutants has been of considerable interest during the last few

decades (Schulze et al., 1989; Field et al., 1992; MuÈller-

Dombois, 1992). Investigations on direct effects of pollutants

on plants have addressed changes in community structure

(Berendse & Elberse, 1990; Tilman, 1990) changes in

physiological processes such as gas exchange (Schulze, 1989;

Curtis & Wang, 1998), growth rates (Bloom et al., 1985;

Sheppard et al., 1999), allocation processes (Wilson, 1988;

Ingestad & AÊ gren, 1991) and effects on nutrient uptake and loss

(Lovett et al., 1985; Sayre & Fahey, 1999). Indirect effects of airCorrespondence: Bernhard Stadler. Tel.: + 49 (0)921 55 5622; fax:

+ 49 (0)921 55 5799; e-mail: [email protected]

ã 2001 Blackwell Science Ltd

Agricultural and Forest Entomology (2001) 3, 253±261Agricultural and Forest Entomology (2001) 3, 253±261

pollutants on plants may originate from increased growth rates of

forest insect populations, which may achieve pest status (Alstad

et al., 1982; Dohmen et al., 1984; Warrington & Whittaker,

1990; Brown et al., 1993; Fleming & Volney, 1995; Docherty

et al., 1997), resulting in detrimental effects on their host plants

(Schowalter et al., 1986; Holopainen et al., 1991). Less clear,

however, are the combined effects of these direct and indirect

stressors on ecosystem response, for example on trophic

interactions and nutrient cycling, resulting from plant±herbivore

interactions under changing environmental conditions.

The green spruce aphid, Elatobium abietinum (Walker), is a

major pest species of Sitka spruce, Picea sitchensis (Bong.)

Carr., and causes considerable economic damage to the forest

industry throughout the spruce growing regions of the UK

(Carter & Nichols, 1988; Straw et al., 1998). Feeding on the

needles results in needle yellowing within a week (Kloft &

Ehrhardt, 1959) and needle fall within 4±6 weeks (Parry, 1974)

eventually leading to a reduction in shoot and tree growth (Straw

et al., 1998). Litterfall studies have demonstrated a reduction in

needle N content on infested spruce (Pedersen & Bille-Hansen,

1999). Studies on trophic interactions induced by phytophagous

insects in the canopies of forest trees indicate a pronounced

effect of the biotic community on nutrient cycling. Herbivores

produce excreta (honeydew, frass) and physically damage the

foliage, improving conditions for microbial growth both in the

canopies and soil, leading to increased carbon availability and

decreased nitrogen ¯uxes (Lovett & Ruesink, 1995; Stadler

et al., 1998; Michalzik & Stadler, 2000; Stadler & MuÈller, 2000).

In this study we report on the effects of aphids on nutrient

¯uxes through the canopy of Sitka spruce under increased N and

S inputs to the forest ecosystem via wet deposition. In particular

we address the questions: (1) does wet deposition affect litter

production through changes in the infestation patterns of aphids;

(2) do pollutants affect trophic interactions between aphids and

epiphytic micro-organisms; (3) does the combination of

pollutant application and aphid infestation differentially affect

nutrient ¯uxes in throughfall of Sitka spruce.

Materials and methods

Experimental design

The experiment covers 1.5 ha, on a very acidic drained basin

peat (< pH 3.0 measured in CaCl2 1 : 5 SoilV : LiquidV),

290 m a.s.l., in the Scottish Borders. The trees, P. sitchensis,

were planted in 1986 at 2 m spacing on ridges of peat removed to

form the drainage ditches. Each plot contained 10 trees in two

lines, and was replicated four times for each treatment. When

treatment commenced in May 1996, the basal branches had

begun to interlock and the 10-year-old trees had a mean height of

3.8 m. The experimental design, site information and meth-

odologies are detailed in Sheppard et al. (1999). Treatments

were made up in rainwater, collected at the site, and applied to

the upper canopy as mist droplets (100±250 mm diameter) from

full cone sprayers (two per tree) supported by a framework of

galvanized steel poles. There were six treatments in the main

experiment, but only four were examined, for the period spring

and early summer 2000. The N treatment provided additional N

at 48 kg/ha/y, the S treatment provided additional S at 50 kg/ha/

y, and the NS Acid treatment at pH 2.5 provided the same

amounts of S and N, but together. The control treatment received

no spray. Treatments were supplied as NH4NO3 (N), Na2SO4

(S), H2SO4 + NH4NO3 (NS Acid). Ions were supplied at a

concentration of 1.6 mol/m3 (NH4+, NO3±, SO4

2±) and 3.2 mol/

m3 (H+, Na+). Background N-deposition at the site is

approximately 8 kg N/ha (wet + dry) and the treatment solution

provides the sprayed trees with an additional 10% of the annual

rainfall. The mean pH of the rainwater is about 4.5 (Sheppard

et al., 1999).

Aphid abundance and honeydew production

The overall abundance of E. abietinum in each treatment plot

was surveyed every 2 weeks from April until July on one-year-

old needles by turning them upside down and counting the

number of infested needles (needles with at least one aphid) per

10 cm of shoot length. These aphids attack one-year-old and

older needles but not growing needles, probably because of a

volatile substance present in the epicuticular wax (Jackson &

Dixon, 1996). Therefore, this method does not give the absolute

number of aphids on a tree during any point in time, especially if

aphids change their feeding places during the growing period or

in response to prevailing weather conditions (Dixon, 1998), but

it provides a relative measurement by which to compare aphid

abundance on trees subjected to different treatments. However,

because these aphids do not cluster in dense colonies, but tend to

spread over a shoot, the number of infested needles should give a

reasonable indication of the overall infestation pattern at the

study site. The survey was restricted to shoots growing at breast

height (c. 1.3 m) and at least 25 shoots were monitored in each

plot on each date. Shoots were chosen at random each time and

no distinction was made between main and side shoots.

The amount of honeydew produced by E. abietinum on trees

subjected to different treatments was measured on 16 June and 4

July. The honeydew was collected by mounting a pre-weighed

aluminium foil (diameter 8 cm) laid in a Petri dish underneath an

aphid colony feeding on one-year-old shoots. For each sampling

date, ®ve replicate foils were set up in each treatment replicate

plot. No effort was made to control the exposure of a branch

where the measurement was made. After 24 h the foils were

removed and the number of aphids above the foils counted. The

honeydew was dried at 30 °C for 2 days and the foil re-weighed

on a Mettler microbalance. The amount of honeydew produced

was calculated as the average of both sampling dates for a single

aphid irrespective of its developmental state. Mean temperatures

on the 2 days were 13.0 °C and 11.3 °C, respectively, with

temperatures recorded every 30 min.

Analysis of micro-organisms in the phyllosphere

On 19 June, current and one-year-old shoots were cut off using

sterile scissors and each shoot was placed immediately into

sterile stomacher polyethylene bags for transport to the

laboratory. Five shoots infested with aphids and ®ve uninfested

shoots were chosen randomly from trees in each treatment (N, S,

NS Acid, Control), but only one shoot per tree was collected. In

addition, the shoots came from trees growing in different

replicate plots. Shoots were sampled mainly from second order

ã 2001 Blackwell Science Ltd, Agricultural and Forest Entomology, 3, 253±261

254 Bernhard Stadler et al.254 Bernhard Stadler et al.

peripheral branches similar to those above the throughfall

collectors. Because of the density of the growing trees no effort

was made to collect shoots facing the same aspect. No rainfall

was recorded for 4 days prior to the sampling of the shoots.

For the microbial analyses, 5 g of needles from one-year-old

shoots were cut off with sterile scissors and blended with

145 mL water for 2 min. These sample solutions were then

logarithmically diluted with quarter-strength Ringer solution

and analysed by spread plating. A Standard II nutrient agar

(Merck, Darmstadt, Germany) medium (pH 7.0) was used to

grow aerobic heterotrophic bacteria, supplemented with 0.4 g/L

cycloheximide (Merck) to inhibit the growth of fungi. The yeasts

and ®lamentous fungi were grown on a Sabouraud-1% dextrose-

1% maltose agar (Merck) (pH 5.5) medium, to which 0.4 g/L

chloramphenicol (Berlin-Chemie, Berlin, Germany) was added

to suppress bacterial growth. All plates were incubated at 25 °C

for 5 days before the number of colony forming units (CFU) was

counted.

Manipulation experiment and throughfall collection

In each treatment (N, S, NS Acid, Control) three polyethylene

collectors (sample volume 5 L) were placed beneath shoots that

were arti®cially infested with 20 adult aphids, and another set of

collectors beneath uninfested shoots. This de®ned a common

infestation pattern above all the throughfall collectors at the start

of the study. Subsequently, aphid numbers above each through-

fall collector were only counted on the needles de®ned by a

vertical projection into the canopy of the collector sampling area

(diameter 20 cm). Again, shoots were turned upside down,

examined for aphids and their numbers on the needles were

counted between throughfall collection dates. On uninfested

control shoots, any aphids that happened to colonize the shoots

above the collectors were manually removed with a pair of ®ne

tweezers. No insecticides were used in case they interfered with

throughfall chemistry. In addition, the numbers of yellowing and

dead needles due to current or earlier aphid infestations on the

shoots of the previous year were counted. This was done by

selecting three or four shoots in the canopy above the collectors

(as previously de®ned) and counting the needles in a particular

category (yellowing, those which showed green and yellow

bands, or dead needles that were completely brown) out of a total

of 100 needles.

Each sampler was located beneath a different tree. The trees

were chosen at random in different replicate chambers and the

collectors were placed towards the periphery of the canopy to

collect throughfall from mainly the one-year-old shoots. No

more than ®ve or six shoots were located above each sampler.

Throughfall samples were collected every two weeks from 3

May to 5 July. Only the last sampling period was longer

(25 days), due to small amounts of rainfall. Previous experi-

ments have shown that the concentrations of organic and mineral

nitrogen are not signi®cantly in¯uenced by microbes washed

into the throughfall collectors, even when much longer sampling

intervals are used (Michalzik et al., 1997).

On each sampling date, the numbers of needles landing in the

funnel of the throughfall collectors were counted to determine

litter fall due to aphid infestation and treatment. Throughfall

collectors were cleaned with deionized water after each

sampling interval and a new coarse ®lter was inserted in the

funnel to prevent debris being washed into the collectors.

After transfer to the laboratory, samples were immediately

vacuum ®ltered (cellulose-acetate membrane, 0.45 mm) and

stored at 4 °C until the next day when the chemical analyses

were done.

Chemical analyses

Dissolved organic carbon (DOC) was measured by infrared

detection of CO2 after persulphate UV digestion using a DOC

analyser (Foss Heraeus, Liqui TOC, Hanau, Germany).

Ammonium-N (NH4-N), nitrate-N (NO3-N), Cl±, Mg2+, K+

and Ca2+ were measured by ion chromatography (Metrohn Ion

Analyser, Metrohn Ltd, U.K). Dissolved organic nitrogen

(DON) was calculated by difference, subtracting the sum of

NH4-N and NO3-N from the total dissolved nitrogen (Ntotal).

Total dissolved nitrogen was measured as NOx after thermo-

oxidation at 700 °C (Abimed: TN-05, Langenfeld, Germany).

Statistical analyses

Differences in the number of CFUs between aphid treatments

were tested with the Mann±Whitney U-test. Because of the high

variability in rainfall amounts during the experiment, through-

fall ¯uxes are presented as differences between infested and

uninfested trees from the different treatments (N, S, NS Acid,

Control). This approach precludes statistical treatment, but is

better suited to highlighting the effect of aphids and microbes on

throughfall chemistry during the course of the season. Fluxes

were expressed as either mg/m2/14 days (or per 25 days),

depending on the sampling frequency as determined by rainfall.

Multivariate analysis of variance (GLM) was used to determine

the effect of treatment and infestation level on ions not included

in the treatment spray. This analysis was restricted to the ®rst

three sampling dates when aphid numbers were increasing.

Figure 1 Seasonal change (mean 6 SE) in the numbers of infested

needles of Sitka spruce. Aphids were only counted on one-year-old

needles (grown in 1999) giving an estimate of the overall infestation

pattern in the treatment chambers. Treatments were: NS Acid, S, N,

Control.


Forest canopies and throughfall ¯uxes 255Forest canopies and throughfall ¯uxes 255

Omitting the period when aphid numbers were declining helps to

exclude possible artefacts associated with delayed effects. For

example, needles turn yellow and die even if the aphids have fed

for only a short period of time (Parry, 1974). Homogeneity of

variances was tested using Levine's test and normality using the

Shapiro±Wilk test. Except for the Cl-¯ux, all other ion ¯uxes

were log- and square-root-transformed to satisfy the assumption

of homogeneity of variances. When treatment effects were not

signi®cant, the data were pooled for correlation analyses with

aphid infestation. All data were analysed with the SPSS

statistical package (SPSS, 1999).

Results

Aphid infestation

On one-year-old shoots, spruce aphid numbers started to

increase in early May and peaked during the end of May/early

June (Fig. 1). Subsequently, the number of infested needles

declined to levels similar to those in early spring. During this

period, trees subjected to the NS Acid treatment had signi®cantly

more needles infested with aphids than those from the other

treatments (repeated measure ANOVA: F4,93 = 18.643,

P < 0.001). On a one-year-old shoot (10 cm in length), an

average of 12.7 needles were infested in the NS Acid treatment

compared to 6.9 in the N, S and control treatments.

Honeydew production was not affected by treatment (ANOVA:

F3,39 = 0.595, P = 0.622). On average a single aphid produced

0.0157 mg honeydew over 24 h.

Phyllosphere micro-organisms

On needles of infested shoots the average numbers of micro-

organisms were always higher when compared with uninfested

needles (Fig. 2). In the NS Acid treatment these differences were

most pronounced, leading to signi®cantly higher CFUs of

bacteria, yeasts and ®lamentous fungi on infested needles.

Bacteria and yeast in the NS Acid and S treatment showed the

highest relative increase in numbers when the shoots were

infested with aphids, whereas differences were generally smaller

in the N and control treatment. Pooling data from all uninfested

needles of the N, S and NS Acid treatments indicated that no

group of microorganism CFUs differed from the Control (t-test:

Figure 2 Number of colony forming units (CFUs) of (a) bacteria,

(b) yeasts and (c) ®lamentous fungi on needles of Sitka spruce infested

with E. abietinum (solid columns) or with no aphids (open columns).

Results were separated for different treatments. The asterisks indicate

signi®cant differences in the CFUs between infested and uninfested

needles (P < 0.05).

Figure 3 Number of aphids (mean 6 SE) above the throughfall

samplers, in different treatments, for each sampling date. Treatments

were: NS Acid, S, N, Control.



bacteria: t = 0.904, d.f. = 18, P(2-tailed) = 0.378; yeasts:

t = 1.564, d.f. = 17, P(2-tailed) = 0.136; fungi: t = 0.800,

d.f. = 18, P(2-tailed) = 0.434). This suggests the 10% increase

in water applied with the treatment solution had no effect on

epiphytic micro-organisms. In total, numbers of CFUs on

infested needles increased 13.9-fold for bacteria, 6.3-fold for

yeasts and 5.9-fold for fungi compared to those on uninfested

needles.

Manipulation experiment

The number of aphids above the throughfall collectors at the ®rst

sampling date after the manipulation was similar in the different

treatments, with an average of 14.2 aphids per shoot (Fig. 3).

Aphid densities increased until the end of May and tended to

decline from mid-June. The variability in aphid number above

the collectors was always rather high, which might re¯ect the

mobility of these aphids. Note that the overall infestation pattern

given in Fig. 1 does not exactly mirror the aphid densities above

the throughfall collectors (Fig. 3). This was because the aphids

kill the needles they feed on, forcing them to move to adjacent

needles/branches. As the throughfall collectors remained in the

same place throughout the experiment, the number of aphids

above a sampler might change quite substantially, which is

indicated by the large standard errors.

The feeding activities of E. abietinum signi®cantly increased

the number of yellowing and dead needles above the throughfall

collectors (Figs 4a,b), compared with uninfested shoots where

the proportion of yellowing and dead needles remained low at

1.2% and 1.1%, respectively. Needle numbers in the throughfall

Figure 4 Needle litter development on aphid infested (solid line) and uninfested (dashed line) shoots: (a) proportion of yellow needles (= needles with

yellow and green bands) above the collectors, (b) proportion of dead needles (= brown needles), (c) needles collected in the funnel of the rain

sampler and (d) needles collected in collectors separated for different treatments. Values are means 6 SE; in (a), (b) and (c) data from all treatments

were pooled.



collectors increased exponentially with the duration of the

infestation (Fig. 4c). Signi®cantly more needles were present in

the throughfall collectors beneath infested shoots (t-test:

t = 3.487, d.f. = 94, P < 0.001) leading to a 66% increase in

needle litter (Fig. 4d). Despite the short delay in the develop-

ment of yellowing of needles after the aphids start feeding, there

was a positive correlation between the number of aphids and

yellow needles above the collectors (rp = 0.809, P < 0.0001,

n = 71). A similar correlation was obtained between the number

of aphids and dead needles above the collectors (rp = 0.508, P

< 0.0001, n = 71).

Throughfall ¯uxes

The average throughfall pH values for each treatment were:

infested N: 4.21; S: 4.94; NS Acid: 3.20; Control: 5.30 and for

uninfested N: 4.26; S: 4.83; NS Acid: 3.22; Control: 5.13. There

was no effect of infestation on throughfall pH. However, there

appeared to be some neutralization of the original acidity in the

NS Acid (pH 2.5) treatment. In order to clarify the effects of the

trophic relationships between aphids, micro-organisms and the

N, S and NS Acid treatments on throughfall chemistry,

differences in nutrient ¯uxes between infested and uninfested

shoots were plotted for each sampling date (Fig. 5a±d).

Increasing aphid numbers were associated with lower inorganic

nitrogen ¯uxes underneath infested shoots but only where

additional N was provided by the treatment (Figs 5a,b). Over the

complete sampling period, the NH4-N-¯ux underneath infested

shoots was reduced in the N treatment by 28.2% and in the NS

Acid treatment by 17.6%. Potassium ¯uxes were also strongly

affected by the presence and activity of the aphids, with higher

¯uxes beneath infested shoots (Fig. 5c). Potassium ¯uxes tended

to increase towards the end of the experiment, indicating a

delayed leaching response to aphid infestation, which had

peaked over the ®rst few weeks in June (see Fig. 3). A similar

pattern but with smaller ¯uxes was found for chloride.

Irrespective of treatment, DOC ¯uxes were generally higher

beneath infested shoots and there was initially an exponential

increase in ¯uxes with time in all infested samples, especially in

the S and Control treatment (Fig. 5d). The infested NS Acid

samples showed an even greater increase in the DOC ¯uxes with

time (four times that of uninfested NS Acid). In contrast, the

infested S and Control DOCs peaked at the end of May and then

declined slowly over time.

Multivariate analyses of the effects of the mist treatments and

aphid infestation showed that Mg-, Cl-, Ca- and DON ¯uxes in

throughfall were primarily affected by the application of the

pollutants, whereas K- and DOC-¯uxes were signi®cantly

Figure 5 Differences in pH and throughfall ¯uxes between aphid infested and uninfested shoots separated for different compounds and sampling

dates. The unit of the difference for the ®rst three data points is: mg/m2/14 days; the last data point has a unit of mg/m2/25 days because of low

amounts of rainfall during that sampling period.



affected by the aphids (Table 1). No signi®cant interaction

effects were identi®ed, indicating the speci®city of both effects.

Discussion

Understanding to what extent insects contribute to the

disturbance and destabilization of forest ecosystems under

changing environmental conditions is dependent on our ability to

link life-history attributes, population and community dynamics

and their regulating mechanisms with biochemical ¯uxes. Forest

canopies provide a useful subsystem in which to study the

integration of some of these factors (Schowalter, 2000).

Early indicators of damage to Sitka spruce needles by the

green spruce aphid, E. abietinum, are yellow chlorotic bands that

develop at the sites of stylet insertion that can lead to needles

dying and turning brown. Infestations rarely kill the tree but can

result in reduced growth (Carter, 1977; Seaby & Mowat, 1993;

Straw et al., 1998). Aphids grown on trees exposed to a variety of

pollutants, including SO2 have been shown to exhibit enhanced

growth rates (Holopainen et al., 1991; Brown et al., 1993;

Docherty et al., 1997; Watt et al., 1998). For example, in an SO2

fumigation experiment aphid numbers on Sitka spruce increased

threefold but only on well watered trees (Warrington &

Whittaker, 1990). The overall aphid population densities in

this study were comparable with those recorded in other ®eld

studies with moderate to severe degrees of infestations (Day,

1984), with the highest abundance being observed in the NS

Acid. However, growth analyses showed no reduction in NS

Acid tree growth compared to the other treatments. On the

contrary, stem growth was enhanced by 15±20% (Sheppard

et al., 1999). The absence of enhanced aphid numbers when N

and S were supplied separately suggests that the aphids were

responding to the combined input of N and S and possibly

acidity.

There were positive correlations between aphid numbers

above the throughfall collectors and the number of yellowing or

dead needles. In addition, the numbers of needles that fell into

the collectors were signi®cantly higher beneath infested shoots,

as previously observed by Parry (1974), Day & McClean (1991)

and Watt et al. (1998). About 66% of the needles shed during the

experimental period could be attributed to aphids, rather than to

direct treatment effects or to the growth conditions. This

suggests that the impacts of aphids may mask pollutant effects

on litterfall. Interestingly, the highest litterfall has consistently,

for over 2 years, been recorded in the NS Acid treatments

(Sheppard & Crossley, 2000). There were also considerable

differences in precipitation and periods with strong winds during

the study period, which could affect the number of dead needles

dropping from the shoots and thus affect the strength of the

correlation with aphid abundance. Similarly, all biotic processes

in the canopy are likely to be dominated by the prevailing

weather conditions. Despite these confounding factors, trophic

links between aphids and micro-organisms were detectable in all

treatment chambers. For example, nitrogen ¯uxes declined more

underneath infested trees, whereas DOC-¯uxes increased

underneath infested trees. The decline of inorganic nitrogen

¯uxes underneath infested trees was more pronounced in the N

addition chambers (N, NS Acid). Therefore, both compounds

(honeydew, N) need to be available to signi®cantly affect

nutrient cycling in the canopy. The ¯ux of potassium in

throughfall is a good indicator of the feeding pressure, showing

a strong relationship with aphid abundance and thus, yellowing

and dead needles. Therefore, the results for E. abietinum were

similar to those for folivores in deciduous forests (Seastedt et al.,

1983) where the rate of cycling of K is enhanced in a similar way.

The leaching of potassium was not affected by the pollutants per

se, showing its sensitivity to herbivore stressors.

Under ®eld conditions, no differences in the amount of

honeydew produced by E. abietinum on trees subjected to

different treatments could be found. Although these aphids

produced only small quantities of honeydew, the mechanism

determining how the droplets are ¯icked off the anus are more

important than the absolute amount of honeydew produced.

Stadler & MuÈller (2000) showed that epiphytic micro-organisms

grew better when honeydew was scattered in tiny droplets across

leaves than when concentrated in a few spots. As a consequence,

the overall distribution of aphids within a tree might play an

important role in trophic cascades and the variability in

throughfall chemistry. Elatobium abietinum had strong positive

effects on the growth of epiphytic micro-organisms and these

were especially pronounced in the NS Acid treatment (Fig. 2),

which might explain the strong initial decline in NH4-N and

NO3-N-¯uxes underneath infested spruce (Figs 5a.b). This was a

surprising response, because at pH 2.5 we expected less

microbial activity on the needle surface. It is conceivable that

an acid-tolerant micro¯ora, which also uses honeydew as energy

source developed on the needle surface in the NS Acid treatment.

Currently, our data only re¯ect the situation in the peripheral

part of the canopy and it remains to be shown how biotic

interactions and throughfall dynamics are linked and vary

Table 1 Multivariate (Wilks' lambda) and univariate F-statistics from GLM-MANOVA of the effects of spraying treatment and the presence of aphids on

throughfall ¯uxes (mg/m2/14 days) during the ®rst 6 weeks of the experiment. Signi®cant effects are in italics

Wilks' lambda K-¯ux Mg-¯ux Cl-¯ux Ca-¯ux DOC-¯ux DON-¯ux

dfa F P dfb F P F P F P F P F P F P

Spraying treatment 3, 71 9.34 < 0.001 3, 63 0.90 0.444 44.55 < 0.001 7.14 < 0.001 37.55 < 0.001 0.70 0.556 10.24 < 0.001

Aphid Infestation 1, 71 14.28 < 0.001 1, 63 17.54 < 0.001 0.81 0.373 0.27 < 0.603 0.34 0.563 49.64 < 0.001 2.11 0.151

Spraying ¢ Infestation 3, 71 1.530 0.085 3, 63 0.81 0.490 0.62 0.602 0.48 0.701 0.92 0.439 1.58 0.203 1.47 0.231

aDegrees of freedom (treatment, error) for multivariate analysis.bDegrees of freedom (treatment, error) for univariate analysis.



horizontally and vertically within the canopy. Nevertheless,

even in the periphery of the Sitka spruce canopy E. abietinum

exerted a strong effect on litterfall, microbial communities and

throughfall chemistry. These effects were quite robust and in

terms of throughfall chemistry, were most pronounced in the

treatments that contained nitrogen (N, NS Acid). Therefore, if

aphid numbers are positively affected via pollutants (directly or

indirectly), signi®cantly higher rates of nutrient cycling might be

expected in the canopies of forest trees receiving elevated N

deposition.

Acknowledgements

We would like to thank Masaaki Chiwa for his generous help

with the ion chromatography. Petra Dietrich and Gunter Ilgen

helped with the DOC and DON analysis. Neil Cape and David

Fowler have contributed to the discussion. The European

Science foundation provided a travel grant to B.S. Financial

support came from the German Ministry for Research and

Technology (FoÈrdernummer: BMBF No. PT BEO 51-

0339476B). The UK Department of the Environment,

Transport and the Regions fund the experimental facility at

Deepsyke forest (Contract No. EPG1/3/52).

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Accepted 1 August 2001



effects of elatobium abietinum on nutrient fluxes in sitka spruce canopies receiving elevated...

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