Conifer aphids in an air-polluted environment. I. Aphid density, growth and accumulation of sulphur and nitrogen by scots pine and Norway spruce seedlings

Environmental Pollution 80 (1993) 185-191

CONIFER APHIDS IN A N AIR-POLLUTED E N V I R O N M E N T . I. APHID DENSITY, GROWTH A N D A C C U M U L A T I O N OF S U L P H U R A N D N I T R O G E N BY SCOTS PINE A N D N O R W A Y SPRUCE SEEDLINGS J. K. Holopainen, A. Mustaniemi, P. Kainulainen, H. Satka & J. Oksanen Ecological Laboratory, Department of Environmental Sciences, University of Kuopio, PO Box 1627, SF-70211 Kuopio, Finland

(Received 31 October 1991; accepted 29 February 1992) Abstract The population dynamics of conifer aphids on pine and spruce seedlings growing in plastic pots were studied along a gradient from a pulp mill emitting mainly S02. At five locations, two apterous females of the grey pine aphid (Schizolachnus pineti L.) feeding on needles, and two apterous females of the spruce shoot aphid (Cinara pilicornis Hartig) feeding on the stem, were transferred to the leader shoot of 10 pine and spruce seedlings, respectively. The sulphur concentrations of the transplanted lichen Hypogymnia physodes (L.) Nyl. and needles of conifer seedlings were significantly increased in the close vicinity of the pulp mill. On pine seedlings, the numbers of S. pineti developed similarly at all study sites. However, in mid-July, the numbers of aphids started to decline near the emission source. In June, C. pilicornis reproduction on spruce was significantly faster at 0.2 and 0.5 km from the pollution source than at the more distant sites, but there was a rapid decline in aphid numbers in July. A negative correlation was observed between the numbers of C. pilicornis during the population peak in late June and the final length of the current year's leader shoot of spruce seedlings. Leader shoot growth of spruce seedlings infested by aphids was positively correlated with the distance from the pulp mill. There were no clear responses to pollution level in parasitization or predation rates of the aphids. The results suggest that all conifer aphids are not good indicators of pollution impact on conifers around a pollution source. There is a general agreement with the earlier reports that Cinara spp. numbers have a positive response to air pollution, especially to SO 2. This is probably due to promoted growth of nymphal aphids on the host plants suffering from pollution. However, high levels of air pollution may also cause rapid collapse of aphid populations. S. pineti, which lives on foliage, did not have a positive response to increased SO 2 levels.

ments with elevated levels of atmospheric pollutants. These environments are often near to industrial pollution sources (Wenzell, 1965; Thalenhorst, 1974; Villemant, 1981; Sierpinski, 1984; Helirvaara & Vais~inen, 1988; Przybylski, 1990; Rao et al., 1990), densely inhabited areas (Dohmen et al., 1984; Dohmen, 1985; Houlden et al., 1991) and roadsides (Przybylski, 1979; Braun & Fliickiger, 1984; Bolsinger & Fltickiger, 1987; Spencer & Port, 1988). Experimental exposures of host plants to different air pollutants have also been found to be beneficial to aphids (e.g. Warrington, 1987, 1989; Houlden et al., 1990; Kidd, 1990; Warrington & Whittaker, 1990; Holopainen et al., 1991). The purpose of the present study was to follow the population dynamics of conifer aphids on pine and spruce seedlings along a gradient from a pollution source emitting mainly sulphur dioxide. We also gathered information on the accumulation of sulphur and nitrogen in plants, as well as on the growth responses of spruce and pine seedlings to pollutants. The other part of the study (Kainulainen et al., 1993) investigated the effects of air pollution on the concentrations of several primary and secondary metabolites relevant to aphids on the pine and spruce seedlings. MATERIALS AND METHODS Site description The research area was located in the vicinity of a pulp mill (Mets~serla Oy), in Kuopio (62054' N, 27040' E), 7 km north of the town centre. The mill produced semichemical pulp by the ammonium sulphite method and its emissions in 1989 were 10 000 t of SO2, 400 t of NO2 and 8 t of ammonia (Nerg & Holopainen, 1991). In 1990, visible damage to the lichen flora was observed up to 8 km downwind of the pulp mill (Nerg & Holopainen, 1991). Five locations (0-2-4-5 km) on a gradient northeast of the factory were selected for investigation (Fig. 1). The modelled daily and hourly maximums of gaseous sulphur dioxide (Table 1) were highest at the site 0.5 km from the pulp mill (Rantala et al., 1991). However, the nearest site was considered to be the most severely

INTRODUCTION There is a growing body of observations of increased aphid growth rates or population densities in environEnviron. Pollut. 0269-7491/93/$06.00 © 1993 Elsevier Science Publishers Ltd, England. Printed in Great Britain

185

186

J. K. Holopainen, A. MustaniemL P. Kainulainen, H. Satka, J. Oksanen

~JJunQ ~Ju{y ~August

Table 2. Basal area of dominant tree species and mean cover of plant growth forms in the study sites

Species 0.2

0.5

1.0

2.0

4.5

6 1 0 0 4 11

4 7 0 0 1 12

0 3 3 4 0 10

0 12 5 3 0 20

0 1 3 5 0 8

Total mean cover (%) Forbs and subshrubs 81 Graminoids 2 Dwarf shrubs +a Bryophytes 4

15 36 +~ 5

7 33 28 30

22 24 37 52

4 19 21 73

Species number of vascular plants

18

12

18

11

Basal area (m2 h a 1) Alnus incana Betula pendula Picea abies Pinus sylvestris Sorbus aucuparia Total

Fig. 1. The location of study sites (A--E) in the vicinity of

the pulp mill (Metsiiserla Oy) in Kuopio. Reversed wind roses show the wind direction during the study, and the insert shows the location of the study area in Finland. polluted due to dry and wet deposition of sulphur and nitrogen. The lack of living conifers (Table 2) and the fact that dead spruce and pine saplings and old spruce stumps were seen at the two nearest sites indicated strong pollution effects. The study sites were located in forests which belong to the mesic site types of the Finnish forest classification (Kuusipalo, 1985b). However, near to the pollution source (0.2-1.0 km) the typical conifers were replaced by hardwood species (Table 2). Consequently, the sites near to the pollution source were more shaded (Kuusipalo, 1985a) than the more distant sites dominated by the conifers. In the more distant sites, bryophytes and dwarf shrubs were dominant, as is typical in the mesic forest vegetation (Kuusipalo, 1985b), but in the two closest sites they were very scarce, and instead forbs (e.g. Epilobium angustifolium L.) and the subshrub Rubus idaeus L. were abundant. However, there were no consistent trends in the total species number of vascular plants (Table 2). Seedling material Three-year-old Scots pine (Pinus sylvestris L.) seedlings (seed origin: Lepp~ivirta, T10-84-2) and 4-year-old Norway spruce (Picea abies (Karst.) L.) seedlings (Kerim/iki, T3-83-95) were obtained from a forest nursery at Suonenjoki (62038 ' N, 27004 ' E). The seedlings were planted in a mixture (1 : 1) of vermiculite and fertilized Table 1. Estimated daily and hourly maximum concentrations of SO 2 according to distribution models (Rantala et al., 1991) at study sites around the pulp mill

Site

A B C D E

Distance from the pulp mill (km) 0.2 0.5 1.0 2.0 4-5

SO2 concentration /zg m 3 h-i

/~g m-3 day l

400 500 400 300 <300

150 200 150 100 <100

Distance (km)

16

a Indicates cover of < 1%. and limed Sphagnum peat (Vapo peat PP6, basic fertilization 1 kg m-3: N - P - K (12:9: 18), with micronutrients, basic liming 3 kg m 3) in 7-5 litre plastic pots. There were four holes of 17 mm diameter in the bottom of each pot, which prevented flooding by rain water and allowed root tips of the seedlings to grow into the underlying soil. On 15 May, 1990, before the elongation of young shoots, 20 pots with pine and 20 pots with spruce seedlings were transported into the forest to each of five sites (0.2---4.5 km) at different distances in a northeast direction away from the factory (Fig. 1). The seedlings received ambient rain, and during dry periods they were watered weekly. The seedlings were randomly allocated in the experiment, and the initial height of the seedlings did not differ between the study sites. Therefore, the final length of the current year's leader shoot was used as an indicator of seedling growth. Measurements were made, and the needles for fresh and dry weight determination were collected on 29 August, except for the seedlings, which were taken for chemical analyses (Kainulainen et al., 1993) earlier in the summer. However, the current year's leader of most of the pine seedlings at the site 0.2 km were destroyed a few days before sampling by capercaillie (Tetrao urogallus) and these seedlings were not measured. Sulphur and nitrogen analyses

To estimate the rate of accumulation of sulphur, the epiphytic lichen Hypogymnia physodes (L.) Nyl. was collected from spruce in an unpolluted area and transplanted with branches on to tree branches near to the studied seedlings for 16 weeks on 15 May and left until 4 September. At the end of the growing season, total sulphur and nitrogen was measured from the needles of seedlings which had been sucked by aphids, because there was not any discoloration in the needles indicating aphid damage. For sulphur analysis, the previous year's needles and lichen material was separately dried at

Conifer aphids in an air-polluted environment. 1 65°C, milled, pelleted and combusted in an oxygen bomb (Parr 1241 (Parr, Moline, Illinois, USA)). Samples were analysed by ion chromatography (Dionex 2010i; Sunnyvale, CA, USA), using the method described by Mulik & Sawicki (1979). Total nitrogen concentration of the current year's needles was analysed by the standard Kjeldahl technique (Allen et al., 1986). The concentration of nitrate-N was determined for soil samples by using a saturated C a S O 4 extract with an ion-selective nitrate electrode (Orion 90-02; Cambridge, MA, USA), and soil ammonium-N was determined from 2 M KCI extracts with an ion-selective ammonium electrode (Orion 95-12). Aphid monitoring

Two newly moulted apterous females of the grey pine aphid (Schizolachnus pineti L.) and two apterous females of the spruce shoot aphid (Cinara pilicornis Hartig) were transferred to the leader shoot of 10 pine and spruce seedlings, respectively, at each location on 5 June 1990. S. pineti prefers feeding on current year needles after shoot elongation, and C. pilicornis feeds mainly on the stem of current year shoot, but it is found even on the main trunk at the end of the growing season. Before the aphids were transferred, the seedlings were searched and predatory arthropods were removed. S. pineti was collected from Pinus mugo L. near the main building of the University of Kuopio and C. pilicornis was collected from 10-year-old Norway spruce saplings growing in the botanical gardens of the University. Neither of the aphid species was attended by ants. The total aphid population on the seedlings was monitored at weekly intervals until 20 August. The numbers of nymphs and apterous and alate viviparae were not separated. To allow free access of pollutants to the whole foliage of the seedlings and to the aphids, the plants were not covered. Therefore, the aphids were also exposed to their natural enemies. Numbers of mummified aphids occurring on seedlings were counted as an indicator of parasitization on 23 July and 20 August. The numbers of spiders and predatory insects associated with the aphids were counted weekly. Table 3. Soil pH and the concentrations of ammonium- and nitrate-nitrogen at different distances from the pulp mill. (Means (SD) within the same column followed by the same letter are not significantly different (p < 0.05) according to Tukey's method)

Distance n from the pulp mill (km) 0-2 0.5 1.0 2.0 4.5 F p *n=4.

5 5 5 5 5

pH (CaCI2)

4.9 (0-55)a 5.4 (0.54)a 3.3 (0.07)b 3.9 (0.36)b 3.5 (0.20)b 22.71 <0.001

NH4+ (/xg g ])

46.01 (5.08)ab 79.81 (33.70)b 35.14(22-15)a 38.18(14.12)a 54.83(6.23)ab 4.25 0.012

NO3 (/~g g-l)

34-1 (6.52)a 3.2 (1.8)b* 3.0 (0.44)b 3.1 (0.52)b 2-8 (0.31b 99-60 0-001

187

RESULTS Accumulation of sulphur and nitrogen

The soil characteristics at the study sites were significantly affected by the distance from the emission source (Table 3). At the two nearest sites, soil pH was higher than at the other sites. This was caused by the liming of these forest sites a few years earlier (T. Holopainen, 1991, pers. comm.). The highest level of ammonium-N was at a distance of 0.5 km and nitrate-N at a distance of 0.2 km. Thus, the total detectable N concentration in the soil was clearly elevated in the close vicinity of the pulp mill. The sulphur concentration of the transplanted lichen H. physodes was significantly higher at a distance of 0-2 km compared to the other sites (Fig. 2). After 16 weeks, the sulphur concentration of the lichens was significantly increased relative to its spring levels (p < 0.001, t-test) at the 0.2 km site, but was significantly decreased (p < 0.001) at the 4.5 km site. This indicated that at the most remote site, leaching of sulphur from lichens was greater than the accumulation during the growing season. Both N and S concentrations in pine needles were significantly elevated at the 0.2 km site (Table 4). The S content of spruce needles was also significantly higher at a distance of 0.2 km than at the other sites, but the N concentration in spruce needles was not significantly influenced by distance (Table 4). Seedling growth The length of the current year's leader shoot in pine seedlings was not significantly correlated with logarithmic distance from the pollutant source for either infested (r = 0.103, p -- 0.504) or uninfested (r -- -0.004, p -0.985) seedlings. Only 17.9% of the variation in leader length of spruce seedlings infested by aphids was explained by distance from the pulp mill, but the trend was increasing, as shown by the positive correlation (r = 0.423, p = 0.002). In uninfested spruce seedlings 2400

I

F~.18 = 35.272 p < 0.001

22OO

o~ 2 0 0 0 o)

18oo

.o~"

1600

•" o o c o o r.~

1200

~ 1400

b

...............

1000

b

800

..........i

g:

0.2

0.5

1.0

2.0

4.5

Distance from the pulp mill (kin] Fig. 2. Mean concentration (_+SD) of sulphur on the transplanted epiphytic lichen (H. physodes) between 15 May and 4 September 1990. The dotted line shows the initial level at transplantation.

J. K. Holopainen, A. Mustaniemi, P. Kainulainen, H. Satka, J. Oksanen

188

Table 4. Concentration of total nitrogen in current year's needles and sulphur in previous years' needles in pine and spruce, respectively, at the study sites. (Means (SD) within the same column of each tree species followed by the same letter are not significantly different (p < 0.05) according to Tukey's method)

Distance from the pulp mill

Total nitrogen n

160 140

[ ] = Uninfested spruce seedlings • = Infested spruce seedlings

T

,..120

Sulphur

%

n

8o

/zg g 1

T

T

(kin) 8o

Scots pine 0.2 0.5 1.0 2.0 4.5

8 9 10 10 10

1.91 (0.20)a 1.54 (0-31)b 1.15 (0.16)c 1.26 (0-20)be 1.22 (0.22)c

F p

9 10 9 10 10

17.74 <0.001 10 10 10 10 10

1.66 (0.19)a 1.57 (0.20)a 1.66 (0.27)a 1.63 (0.21)a 1.76 (0-26)a

F p

10 10 10 10 10

1212.6(171.5)a 940.3 (94.0)b 940.5 (193.0)b 903.2 (179.9)b 911.1 (146-3)b

0-97 0.433

6.54 <0.001

there was no significant correlation (r = -0.026, p = 0.901) with distance from the pollution source. The length of the current year's leader shoot did not differ significantly between aphid-infested and uninfested pine seedlings at any site (Fig. 3). However, uninfested spruce seedlings had significantly longer current year's leaders (t = 3.64, p = 0.014) than aphid-infested spruce seedlings at a distance of 2 km from the mill (Fig. 4). Population growth of aphids

On pine seedlings, the numbers of S. pineti that developed were nearly equal at different study sites until the end of June. In mid-July, the numbers of aphids started to decline at the distances of 0.2 and 0.5 km from the emission source, while at the other 180 t ~ 160

2O 0

i

0.5

1.0

2.0

4.5

Distance from the pulp mill (kin) Fig. 4. Mean length (_+ SE) of the current year's leader shoot of spruce seedlings at various distances from the pulp mill. sites, aphid densities did not decrease until late July (Fig. 5). In June, C. pilicornis reproduction was significantly faster at 0-2 and 0.5 km from the pollution source than at the other sites (Table 5), but in July there was a rapid decline in aphid numbers at these sites. At the distance of 2 km, where the leader growth of aphidinfested spruce seedlings was reduced, C. pilicornis populations remained at a relatively high level until the end of the growing season (Fig. 6). Neither the foliar S nor N concentrations, nor the length of the current year's leader of pine or spruce were correlated with the log-transformed maximum number of aphids per seedlings. However, a significant (r -- -0.337, p -- 0.017) negative correlation was observed between the log-transformed numbers of C. pilicornis on spruce during the peak populations (25 June) and the final length of the current year's leader shoot. The observed numbers of natural enemies of aphids were very small. Spiders and their webs were occasionally observed in June, and some Coccinellid and Syrphid

= Uninfested pine seedlings Infested pine seedlings

2.4

140

;

0.2

14.67 <0.001

Norway spruce 0.2 0.5 1.0 2.0 4.5

4O

1430.7(272.7)a 958.7 (170.0)b 808.1 (142.0)b 998-1 (246.1)b 839.0 (109.8)b

• 2.0

Schizolachnus pineti

0.2 kmkm-o.s ___

.

i

":'-.

" - ' - . . " .......

°

1.o km . . . . . . . " =. 1.6 2.0 km. . . . . . . . . . . .. , 4.5 km . . . . . ..J'~-~------~~ o~ _ .z . °

"~120 EIO0

,,

'. •

"

e-

~ eo C

o

..i 60 4O

+

0

/

= 0.4

2O ~

~

0.2

0.5

1.0

2.0

4.5

Distance from the pulp mill (kin) Fig. 3. Mean length (+SE) of the current year's leader shoot of pine seedlings at various distances from the pulp mill.

0

|

5

i

i

i

i

12 18 25 2 JUNE

I

9

i

I

i

i

i

16 23 30 7 JULY

i

14 20

AUGUST

Fig. 5. Population dynamics of S. pineti on pine seedlings at study sites. The lines show cubic curve-fit of the data.

Conifer aphids in an air-polluted environment. I

189

Table 5. Significance of the effect of distance from the pollution source on the log (n+l)-transformed numbers of S. pineti and C. pilieornis on each observation date according to one-way analysis of variance (dr= 4, 45) (The letters indicate the sites (A = 0-2 km E = 4"5 km from the pollution source) which significantly (p < 0.05) differ from each other according to Tukey's method)

S. pineti

Date

12 June 18 June 25 June 2 July 9 July 16 July 23 July 30 July 7 August 20 August

C. pilicornis

F

p

F

p

0.986 0.746 0.763 0.688 0.679 1.393 5.451 5.480 7.757 5.978

0.425 0.566 0.555 0.604 0.610 0.252 0.001 (B < DE) 0.001 (B < CDE) <0.001 (B < ACDE) <0.001 (BC < D)

5.762 5.297 11.716 8-783 5.107 3.089 1.552 3-320 3-491 3.396

<0.001 (AB > E) 0.001 (AB > E) <0.001 (AB > CE) <0.001 (AB > CE) 0.002 (A > CE) 0.025 (D > AC) 0.204 0.018 (D > AC) 0.015 (D > A) 0.017 (D > AB)

larvae were seen in July. It was not possible to estimate the total rate of predation (e.g. by nocturnal enemies) using direct observations once a week. The mean number of mummified S. pineti individuals per 100 living aphids (Table 6) was highest at the distance of 0-5 km, but there was no clear response to the distance in the parasitization rate. Mummified C. pilicornis individuals were not found. DISCUSSION This study indicates that aphid species show diverse responses to air-pollutant emissions from a paper mill, and, therefore, it is very difficult to generalize about the effect of air pollution on aphid populations on conifers. Similarly, Villemant (1981) found that Cinara spp. and Eulachnus agilis (Kalt.) Guerc. o n pine were significantly more abundant in a polluted area, but an opposite trend was observed in S. pineti and Pineus pini L. An increased population density of Cinara spp. in the vicinity of industrial sources emitting SO2 was also reported by Sierpinski (1980) and Heli6vaara & V~iis~inen (1988). Experimental exposures of conifers and aphids to air pollutants have revealed various differences in the 1.9

Cinara pilicornis

•" ',.~ "0 1.6 ® •

0.2 km 0.5 k m - - - - - -

1.0 km . . . . . 2.0 km .......... 4.5 km . . . . .

~~ x x \

~ 1.3 o"-

x

'~ O.

\

'...

\\\

m

-'÷

¢!:' ....... . . . 7::: . . .

.~= 0.3

o

"'........ ....

\

0.6

I

5

I

I

I

12 18 25 JUNE

I

I

2

9

\'.

-..

,

I

I

16 23 JULY

I

30

!

I

I

7 14 2 0 AUGUST

Fig. 6. Population dynamics of C. pilicomis on spruce seedlings

at study sites. The lines show cubic curve-fit of the data.

response of individual aphid species to various pollutants and to the duration of exposure. In a field exposure to aqueous fluoride and nitrogen compounds and SO2, all of the treatments and their combinations increased the natural population density of C. pilicornis, while in an artificial infestation, exposure to SO2 alone did not affect aphid density (Holopainen et al., 1991). The mean relative growth rate (MRGR) of C. pilicornis on new shoots of Picea sitchensis (Bong.) Carr. was increased in a chamber experiment after 4 to 96 h continuous exposure to NO2 and ozone, but was reduced by episodic (8 h day t) exposure to ozone (McNeil & Whittaker, 1990). Similarly, the M R G R of S. pineti was increased after exposure to NO2, but was not affected after episodic exposure to ozone, and decreased after a few days of continuous exposure to ozone (McNeill & Whittaker, 1990). Kidd (1990) reported a 12% higher M R G R and a 34% higher population growth rate of S. pineti on pine trees exposed to simulated acid mist compared to the trees sprayed with deionized water. The evidence from the studies on the effects of air pollutants on insect-plant relationships suggests that the effects of gaseous pollutants are mostly mediated via the plants and, therefore, pollution is less likely to affect predators and parasitoids than herbivores. The rate of parasitism of the pine resin moth (Retinia resinella L.) did not depend on the distance from an industrial pollution source emitting SO2 and heavy metals (Heli6vaara & V~is~inen, 1986). Further investigations in the same locality (HeliOvaara & V~tis~inen, 1991) indicated that the parasitism of pine sawflies did not depend on the distance from the pollution source, Table 6. Number of mummified aphids (S. p/hen) per 100 living aphids (the absolute numbers of mummified aphids in parentheses) on pine seedlings at different distances from the pollution source

Site

23 July

20 August

0.2 0.5 1.0 2.0 4.5

0.43 (2) 16.16 (48) 0.06 (1) 0.45 (9) 0.60 (12)

0.80 (2) 52.46 (32) 16.13 (25) 1.48 (12) 7.27 (20)

190

J.K. Holopainen, A. MustaniemL P. Kainulainen, H. Satka, J. Oksanen

although the proportion of parasitized cocoons of Neodiprion sertifer (Geoffroy) was lowest and larval mortality caused by the polyhedrosis virus was elevated near the factories. In an open-air fumigation experiment, Aminu-Kano et al. (1991) observed that populations of parasitoids and most of the predators of the grain aphid (Sitobion avenae F.) were not affected by elevated SO2 levels (21-57 ppb). Braun & Fltickiger (1984) found more parasitoids and predatory Coccinellids and Syrphid larvae on a motorway verge and central area than at a less-polluted control site. However, the density of natural enemies relative to aphid numbers was similar to the control site. The present results are consistent with these earlier studies, indicating that the distance from the pollution source does not affect the rate of parasitism of aphids. However, the collapse of S. pineti populations at the 0.5 km distance from the pulp mill in July was partly caused by a high rate of parasitism. Fumigation experiments with high concentrations of gaseous SO2 have shown that SO2 does not have direct deleterious effects on sucking insects (Feir & Hale, 1983; Dohmen et al., 1984). However, fumigation with SO2 at concentrations above c. 260 /xg m 3 (100 ppb) had a harmful effect on aphids themselves feeding on pea plants (Whittaker & Warrington, 1990), while at lower fumigation concentrations there was a positive linear correlation between SO2 concentration and aphid growth rates (Warrington, 1987). The estimated hourly maximum concentrations from 400 to 500 /zg m 3 o f SO2 at the distances 0.2, 0-5 and 1.0 km in the present study suggest that these concentrations could be directly harmful to aphids. This also could be an explanation for the rather rapid collapse of C. pilicornis and S. pineti populations at 0-2 and 0.5 km from the emission source. Normally, C. pilicornis and S. pineti did not occur at the nearest site, because living conifers were not found close to the pulp mill. The elevated foliar concentration of nitrogen in pine seedlings at a distance of 0.2 km was associated with the higher sulphur concentration. This might be explained partly by NO2 and NH3 emission and partly by the enhancement of NH3 deposition at needle surfaces due to high SO2 levels (McLeod et al., 1990). Partly, the increased concentration of nitrogen in pine needles could be due to the better uptake of nitrogen from the soil by the main root, while diffuse spruce roots did not spread effectively to the soil. The more rapid population increase in C. pilicornis compared to S. pineti at the distances of 0.2 and 0.5 km in June, may indicate that C. pilicornis, which occurs on stems, can better use the increased available nitrogen in the host plant. Chemical analysis of uninfested pine and spruce seedlings (Kainulainen et al., 1993) along the pollution gradient indicated that the typical biochemical reactions near the pollution source were due to elevated levels of the amino acids ornithine, lysine and histidine, an increased proportion of arginine in early July, and elevated levels of the reducing sugars glucose and fructose in late August, in both conifers species. An increase in the concentration of reducing sugars

(Fltickiger et al., 1978) as well as in the levels of amino acids (Fliackiger et al., 1978; Braun & Fltickiger, 1985; Bolsinger & Flt~ckiger, 1987) have been found to be associated with increased aphid numbers on deciduous trees along motorways, where NO2 is an important air pollutant. In the present study, the relatively low population level of S. pineti on pine at the distances 0.2 and 0.5 km could be explained by the direct negative effects of SO2 and sulphur deposition on the needles. Our previous observations (Holopainen et al., 1991) suggest that C. pilicornis does not reproduce well if arginine concentration is high in spruce. The present results are not entirely consistent with this, since in late June the density of C. pilicornis was highest at sites 0.2, 0.5 and 2 km, where the relative proportion of arginine to total amino acids was highest in early July. However, just after the sampling date, aphid populations in the close vicinity of the pulp mill collapsed dramatically. Both of the studied aphid species damage conifer seedlings (Carter & Maslen, 1982). The negative correlation that was observed between the density of C. pilicornis in June and the final length of current year's leader shoot indicate that this aphid species can be harmful to spruce seedlings, when its rate of reproduction is increased due to air pollutants. In conclusion, the present results suggest that some conifer aphids are not good indicators of pollution impact on conifers. However, Cinara spp. seem to have a rapid positive response to elevated pollution levels. This is probably caused by promoted growth of nymphal aphids (Kidd, 1991) on the host plants. The rapid decline of C. pilicornis populations later in the summer may be due to a reduction in the nutritive value of the host plant or to a direct negative effect of pollutants. ACKNOWLEDGEMENTS This investigation was conducted with the financial support of the Academy of Finland and of the Maj and Tor Nessling Foundation. REFERENCES

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