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Spruce-living spiders and forest decline; the importance of needle-loss
Biological Conservation 43 (1988) 309-319
Spruce-living Spiders and Forest Decline; the Importance of Needle-loss
Bengt Gunnarsson Department of Zoology, University of GSteborg, Box 25059, S-400 31 G6teborg, Sweden (Received 11 June 1987; revised version received 8 July 1987; accepted 21 July 1987)
ABSTRACT Air pollution is presumed to cause needles-loss in spruce Picea abies in S W Sweden, with a consequent change in habitat structure for spruce-living spiders and other arthropods. The abundance and taxonomic composition of autumn spider populations were assessed in two close stands of spruce, having relatively high ( H) and low ( L ) percentages of needle-loss, respectively. A difference in abundance was observedfor large spiders (length > 2"5 ram), the density in the L-stand being about twice that in the H-stand. Taxonomic data suggest that needle-loss in spruce may have an impact on the composition of the spider community. Sheetweb spiders ( Linyphiidae) seemed to benefit from the more open structure caused by needle-loss, whereas raptorial spiders (mostly Thomisidae) were associated with needle-dense branches. The density reduction of large spiders in the H-stand is discussed in relation to their importance as prey for overwintering passerine birds.
INTRODUCTION Forest decline in several parts .of central and northern Europe is widely considered to be an effect of air pollution (Lichtenthaler, 1984; Blank, 1985; Nihlghrd, 1985). For instance, large amounts of pollutants, including particles and vapour, may be deposited directly on the vegetation (Lindberg et al., 1986). Needle-loss in coniferous trees in SW Sweden is an example of forest damage which is in part induced by air pollution (Andersson, 1986). This means that branches of spruce Picea abies (L.) Karst. become less 309 Biol. Conserv. 0006-3207/88/$03"50 © Elsevier Applied Science Publishers Ltd, England, 1988. Printed in Great Britain
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'needle-dense' and the proportion of needle-free twigs increases, i.e. the structural composition in the trees changes. The effects of air pollution thus change the habitat for animals living in coniferous trees and the aim of the present study was to investigate whether needle-loss affects the population of spiders, an important arthropod group living on spruce branches (Jansson & v o n Brrmssen, 1981). Indirect air pollution effects are known among other arthropods, e.g. aphids, which increase their growth rate in polluted areas (Dohmen et al., 1984; Dohmen, 1985). I report on the abundance and taxonomic composition of spruce-living spiders in SW Sweden, comparing two spruce stands with relatively high and low percentages of needle-loss, respectively. The results of this study have implications for wintering passerine birds, especially goldcrest Regulus regulus L. and tits Parus spp., which prey upon spruce-living spiders (Thaler, 1973; Jansson, 1982; Hogstad, 1984).
M A T E R I A L AND M E T H O D S The study site, which is part of a vast coniferous forest, is situated about 20 km SE of Kungsbacka in SW Sweden, with spruce the dominant tree, in different stages of succession. Spiders were collected from spruce branches in October 1985. I selected two groups of trees, situated about 75 m apart, for comparison. The weightpercentage of needles in each branch was calculated and the assumptions described below were tested. In the first group (H) a high percentage of needleloss was expected since the trees are exposed to winds from the west and southwest and are thus exposed to air pollutants. The second group (L) was situated in a sheltered position about 50 m from the forest edge and thus a lower percentage of needle-loss was expected. Each branch was dried at + 85°C for 24 h and was then divided into two fractions, needles and twigs, which were weighed to the nearest gramme. There are two advantages associated with the use of two close groups of trees for sampling: (1) effect on the spider density and species composition caused by geographical factors is minimised; (2) differences between the two spider populations compared in the present study are underestimated since all trees in the area should be more or less affected by air pollution but the severity of the damage varies. A statistically significant difference between the two stands should therefore be considered as strong evidence. A disadvantage of choosing one exposed and one sheltered group of trees is that there may be microclimate differences but this (see Discussion) should not interfere with the interpretation of the results in the present study.
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In each stand eight spruces were randomly selected, and two branches cut from each tree (Gunnarsson, 1983). The branches were taken at random up to a height of about 3 m above the ground. The branches were cut directly into, or carefully transferred to, plastic sacks, which were sealed and stored at + 4°C until examination. The spiders were obtained by cutting the branches into small pieces; each piece was shaken and carefully examined over a white bowl. The spiders were stored in 70% alcohol and identified to species or genus level. The length of each specimen was measured with a measuring ocular on a stereo microscope. The specimens were then categorised into 'small' (length < 2.5 mm) and 'large' (>2.5 mm) spiders (Askenmo et al., 1977; Norberg, 1978). The spider families were combined into four guilds depending on their hunting strategy. The 'raptorial spiders' guild used here included Thomisidae, Clubionidae, Anyphaenidae and Salticidae, with the common characteristic of not producing any hunting webs. The term 'raptorial' has been used in a more restricted sense by Turner & Polis (1979), who confined the guild to Thomisidae. Numerically, in the present case, Thomisidae made up over 80% of the guild (data from Table 3). The majority of families were web-builders, and were categorised into three guilds, following Rypstra (1982): 'orbweb spiders' including Araneidae, Tetragnathidae, Metidae, Uloboridae; 'tangleweb spiders', including Theridiidae, Dictynidae; and 'sheetweb spiders', including Linyphiidae.
RESULTS
Spruce branches The average mass for a spruce branch in the H-stand (high percentages of needle-loss expected) was 1.630kg fresh weight compared with 1.158 kg in the L-stand (low percentages of needle-loss expected). This difference is statistically significant (Table 1). When comparing the dry weights of branch-mass and twig-mass (i.e. branch-mass minus needles), the L-stand sample had significantly lower averages than the H-sample (Table 1). However, the needle-mass did not differ between the two stands. This means that the percentage of needles in relation to the total branch-mass is significantly lower (mean 32-7%) in the H-stand sample that in the L-stand (mean 39.9%) (Table 1). Hence, the branches are smaller in the L-stand than in the H-stand, but those in the L-stand are relatively needle-dense, i.e. they have low percentages of needle-loss. This is consistent with the prediction made about neddle-loss (Material and Methods).
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TABLE 1 Data on Spruce Branches in Stands with Relatively High (H-stand) and Low (L-stand) Percentages of Needle Loss, respectively
Branch-mass, fresh weight (kg) Branch-mass, dry weight (kg) Twig-mass, dry weight (kg) Needle-mass, dry weight (kg) Percentage of needles per branch
H-stand (SD)
L-stand ~ (SD)
Mann- Whitney U-test (2-tailed)
1.630 (0.730) 0.857 (0.362) 0.569 (0-232) 0.288 (0-147) 32-7 (6.7)
1.158 (0.539) 0.577 (0.263) 0.344 (0.152) 0.234 (0.117) 39.9 (5-0)
U=75-5; U = 63; U = 53; U = 103; U = 49;
Pro0.05 P < 0.02 P < 0-02 P>> 0-05 P < if01 °
° 1-tailed test, see the prediction in the text.
Spider densities The total density of spiders, and the densities for 'large' (length >_2-5 mm) and 'small' ( < 2.5 mm) specimens, were calculated in the two spruce stands, respectively. The number of spiders on each branch was related to (1) the fresh branch-mass, (2) the dry branch-mass, and (3) the dry needle-mass (all in kg). I then compared the spider categories for each set of density values. In all cases the density of large spiders was significantly lower in the Hstand than in the L-stand samples (Table 2), and that of small spiders was significantly higher in the H-stand when considering numbers per kg dry needle-mass (Table 2). No other significant differences were found. TABLE 2 Abundance of Three Spider Categories--Large and Small Specimens (delimination length 2.5 mm), and Total (large + small)--in Two Spruce Stands, of Trees with Relatively High Percentages of Needle Loss (H-stand), and Trees with Low Percentages of Needle Loss (L-stand) Spider category
Numbers/kg fresh branch-mass H-stand (SD)
Large Small Total
L-stand ~ (SD)
Numbers/kg dry branch-mass H-stand ~ (SD)
H-stand ~ (SD)
L-stand ~ (SD)
2"8 (2.1) ~-~ 5"3 (2.7) 5-2 (3'8)~b 1(~5 (5"1) 17"0 (13'4) *-% 26"3 (12"1) 26"9 (13.2) 19.0(6'2) 49-9(22"7) 38.1 (13"8) 163.1 (97.3) ~ 95"3 (31"0) 29.7 (14"6) 24.3 (7.2) 55.1 (25-2) 48.6 (15"5) 180-1(107-2) 121"5(33"9)
Mann-Whitney U-test, 2-tailed; U = 53, P < 0"02. b U = 49, P < 0-02. ' U = 73, P < 0"05. U=67, P < 0.05. °
L-stand £ (SD)
Numbers/kg dry needle-mass
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There were no correlations between the spider densities and (1) the dry branch-mass, (2) the dry needle-mass, or (3) the weight percentage of needles in each branch. I tested each spruce stand separately and considered the densities of large and small specimens, and the total spider density (Spearman rank correlation tests, two-tailed, P > 0.10 in all cases). Taxonomy and guilds The percentage distribution at the family level was similar in the two spruce stands. In an average branch in the H-stand Linyphiidae made up 61-3% of the specimens in number, compared with 56.5% in the L-stand (Table 3). Thomisidae came second with 15.5% (H-stand) compared with 15.8% (Lstand). Four families occurred only in one of the stands. Uloboridae was absent from the H-stand, but scored 6.3% (the fourth family by number) in the L-stand. I calculated the spider guild densities as described above. Since no predictions about guild differences between the stands could be made (Table 3), I used two-tailed statistics in the tests. The 'orbweb spiders' was the only guild density which differed significantly between the H- and L-stands, this group being more common in the L-stand (Table 4), due to the high densities of the Uloboridae (Table 3). TABLE 3 Taxonomic Composition as Percentage Distribution in Spruce Stands with High (H-stand) and Low (L-stand) Percentages of Needle Loss, respectively Family
Clubionidae Anyphaenidae Thomisidae Salticidae Dictynidae Theridiidae Uloboridae Tetragnathidae Metidae Araneidae Linyphiidae Unidentified
Guild
"~ t ~, f "~ I
Raptorial Tangleweb Orbweb Sheetweb
H-stand % (SO)
L-stand % ~ (SD)
0.7 (1.1) 1.3 (2.6) 15.5 (10.4) 0-4 (1-4) 1-5 (2-0) 12.3 (8.6) 0 0-2 (0.7) 0 4.3 (5"9) 61-3 (12.7) 2.4 (5"1)
3-7 (4-5) 0 15.8 (10-4) 0 1.4 (2-2) 10.3 (6.8) 6.3 (9-0) 1.1 (2.3) 0-6 (1.8) 3-5 (3"5) 56-5 (16-6) 0"7 (2"2)
99-9 (n = 725) 99"9 (n = 456)
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TABLE 4 A b u n d a n c e o f F o u r Spider G u i l d s (see text) in Spruce Stands with High (H-stand), a n d L o w (L-stand) Percentages o f Needle Loss, respectively
Guild
Numbers/kg fresh branch-mass H-stand Yc(SO)
Raptorial spiders Orbweb spiders Tangleweb spiders Sheetweb spiders
L-stand ~ (SD)
5"6 (4.2) 4.6 (2.4) 1"2 (1.5) ~ ° ~3.2 (3.5) 4"0 (3"2) 2'8 (1'9) 18-1 (9.7) 13.3 (4.4)
Numbers/kg dry branch-mass H-stand .~ (SD)
L-stand .f (SD)
10-5 (7.8) 9-1 (4'6) 2-2 (2-9) ~ b ~ 6'5 (6.9) 7.4 (5-5) 5'7 (4"1) 33.4 (16.8) 26.7 (9-5)
Numbers/kg dry needle-mass
H-stand .~ (SD)
L-stand ~ (SO)
32"6 (24.3) 22.7 (lff7) 6-3 (7"9)~-L-~15"5(15"6) 25'8 (28"0) 13"8 (9'7) 110.5 (66.8) 68.3 (27.4)
° Mann-Whitney U-test, 2-tailed; U = 71.5, P < 0.05. b U = 70, P < 0"05. c U = 7 2 , P <0-05.
Two related hypotheses were tested. First, I assumed that the high relative abundance of raptorial spiders is associated with branches with high weight percentages of needles, since such branches should offer good hiding-places for the spiders between the needles. The proportion of raptorial spiders was calculated in relation to the total number of identified specimens, and a positive correlation was found in the H-stand (Fig. 1 (a); Spearman rank correlation test, one-tailed; r s = 0.450, P < 0.05). In the L-stand no such correlation was found (Fig. l(b)). Second, the needle-loss on spruce branches might provide web-builders with better possibilities for attaching their webs to the twigs and if the first hypothesis is valid may thus increase their relative abundance. I tested this hypothesis on the sheetweb spiders since they were the most abundant of the web-builders (Table 4). Correlations were found between increasing percentage of twig-mass and the relative abundance of sheetweb spiders in the two spruce stands (Fig. l(c), (d); H-stand: rs = 0.607, P < 0.01; L-stand: r s = 0.426, P ,.~ 0"05). When considering the relative abundance of the three web-building guilds together I found a significant correlation in the H-stand (r~ = 0"450, P < 0"05), but not in the L-stand (r~ = 0-085, P > 0"25).
DISCUSSION The abundance of large spiders was considerably higher in the L-stand compared with the H-stand. The spruce branches in the L-stand differed from the H-stand branches by, on average, being lighter and having higher percentages by weight of needles. This might suggest a relation between the size distribution of the spiders and the structural differences between the
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Fig. 1. The relative abundances of raptorial and sheetweb spiders in each branch in relation to the percentages of the mass of needles and twigs, respectively. Raptorial spiders in (a) the H-stand (trees with relatively high percentages of needle-loss), and (b) the L-stand (low percentages of needle-loss). Sheetweb spiders in (c) the H-stand, (d) the L-stand. N.B.: Different scales on abscissa in (c) and (d). branches in the two stands. However, this hypothesis has to be examined in m o r e detail by further studies. A tentative explanation o f the density differences o f the large spiders in the two stands m a y be bird predation, which is k n o w n to cause high mortality a m o n g spruce-living spiders (Askenmo et al., 1977; Gunnarsson, 1983). Large spiders might be more vulnerable to bird predation in the H-stand than in the L-stand since they should be easier to detect on branches with few needles. A n alternative explanation for the differences in the spider size
316
Bengt Gunnarsson
distribution is that the microclimate may have favoured large spiders in the sheltered L-stand, which is probably wetter and colder than the exposed Hstand. This hypothesis cannot be ruled out completely, but experimental results on dune-living spiders (including Philodromus aureolus (Clerck) which is common on spruce branches (Norberg, 1978; Gunnarsson, 1985)) show that there is no general correlation between the size of spiders and their resistance to desiccation, or thermal tolerance (Almquist, 1970, 1971). The reason for the higher density of small spiders in the H-stand than in the L-stand is uncertain since it was found only when relating numbers to the needle-mass. There are two possible explanations: (1) a low predation rate on small specimens in the H-stand since there are few large spiders (Gunnarsson, 1985), and (2) aeronautic spiders, i.e. mostly small specimens (Duffey, 1956), may be 'caught' by the forest edge. The approximate 50% reduction in the density of large spiders in the trees with high needle-loss may have serious effects on overwintering passerine birds. Spiders are important winter food for these birds (Jansson, 1982; Hogstad, 1984) and there are few alternative prey items in spruce (Jansson & von Br6mssen, 1981), In October spiders thus made up 45% of the total number of prey items for goldcrests foraging in spruce, but as winter progressed, they became more important, and in January and February formed about 80% of the prey (Hogstad, 1984). Index data from Denmark for the latest 10-year period show decreasing trends in population size for the goldcrest, crested tit and coal tit (P. ater L.) (Nohr et al., 1986) in coniferous forests. It is not known what caused this decrease but reduced winter food supply is a possible explanation. The autumn density of large spiders was on average 2.8 specimens kg- 1 fresh branch mass in the H-stand in contrast to 5-3 in the L-stand. In previous quantitative samples from spruce branches, taken between 1972 and 1978 about 30 km NE of the study site used here, the average autumn density of large spiders was 6.8 specimens kg- 1 fresh branch mass (mean value for six autumns, range 4.4-10.8) (Jansson & v o n Br6mssen, 1981). This may suggest a reduction of large spiders due to temporal factors, but since the samples were taken in different areas spatial differences may also be involved. The difference in orbweb spider density between the spruce stands was caused by the presence of Hyptiotesparadoxus (C. L. Koch)(Uloboridae), in the L-stand but not in the H-stand. In this case it cannot be ruled out that the microclimate, i.e. presumably wetter and colder in the L-stand than in the Hstand, caused the difference. Three more families occurred in only one of the two stands (Table 3). Their abundance was, however, very low, so they do not affect the densities of the guilds to any great extent. The absence of major differences in taxonomic composition and guild
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density between the stands may be an effect of the close location of the spruce stands. When the results in the present study are compared with quantitative samples taken in the study site of Jansson & von Brrmssen (1981) in 1975 and 1976, Thomisidae was the most abundant family with 37-45% by number (Norberg, 1978), versus 16% in my samples (Table 3). Linyphiidae made up 27% in the 75/76-samples (Norberg, 1978) versus 57--61% in the present study. These differences may be due to both spatial and temporal factors. It should, however, be noted that the forest decline has accelerated during these ten years (Blank, 1985). The hypothesis that the microhabitat change in spruce branches, caused by needle loss, may affect the taxonomic composition is supported by my results. In the H-stand high relative abundances of the raptorial spiders, consisting of Thomisidae (80%), were associated with needle-densebranches. No such correlation was found in the L-stand (Fig. l(b)). This may be due to the low variation in the percentage of needles (range 31.3-46-5%) in the L-stand samples. In the H-stand the range was 18.0-46.3% and the probability of detecting a correlation thus increased. Also, sheetweb spiders (Linyphiidae) increased their relative abundance when the percentage of twigs (i.e. branch-mass minus needles) increased. Consequently, the needleloss in coniferous trees seems to favour sheetweb spiders over raptorial species. Thus, the results seem to be in accordance with several other studies which have shown that habitat structure is an important determinant of the spider community (e.g. Duffey, 1962; Robinson, 1981; Rypstra, 1983; Greenstone, 1984). So far only a few investigations have focused on spiders in relation to air pollution. For instance, a negative correlation between the number of spider species and SO2-concentrations was found by Andr6 (1977) and Clausen (1984, 1986), but not by Gilbert (1971). The data from Andr6 (1977) also showed a negative correlation between spider density and SO2. These results could be attributed to structural differences, for example, the frequency of epiphytes, between the habitats (Clausen, 1986). In conclusion, large spiders were scarce in spruce branches with a relatively high percentage of needle-loss. Also, the taxonomic composition, as indicated by the relative abundance of different spider guilds, was correlated with the percentage of needles, or twigs, on the branches. Hence, the results support the hypothesis that the spider populations were affected by the forest decline and accompanying alteration of the spruce microhabitat. ACKNOWLEDGEMENTS I thank Mikael Hake for excellent assistance in the field and in the laboratory, Conny Askenmo and Jan Ekman for discussions, and Mats
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Eriksson for reading this manuscript. The study site was suggested by Bengt Hasselroth and Folke Andersson. This study was supported by grants from the National Swedish Environmental Protection Board.
REFERENCES Almquist, S. (1970). Thermal tolerances and preferences of some dune-liv.ing spiders. Oikos, 21, 230-6. Almquist, S. (1971). Resistance to desiccation in some dune-living spiders. Oikos, 22, 225-9. Andersson, F. (1986). Acidic deposition and its effects on the forests of Nordic Europe. Water, Air & Soil Pollut., 30, 17-29. Andr6, H. (1977). Introduction ~ l'6tude 6cologique des communant6s de microarthropodes corticoles soumises ~ la pollution atmosph6rique, II. Recherche de bioindicateurs et d'indices biologiques de pollution. Ann. Soc. r. Zool. Belg., 106, 211-24. Askenmo, C., von Br6mssen, A., Ekman, J. & Jansson, C. (1977). Impact of some wintering birds on spider abundance in spruce. Oikos, 28, 90-4. Blank, L. W. (1985). A new type of forest decline in Germany. Nature, Lond., 314, 311-14. Clausen, I. H. S. (1984). Notes on the impact of air pollution (SO2 & Pb) on spider (Araneae) populations in North Zealand, Denmark. Ent. Meddr., 52, 33-9. Clausen, I. H. S. (1986). The use of spiders (Araneae) as ecological indicators. Bull. Br. arachnol. Soc., 7, 83-6. Dohmen, G. P. (1985). Secondary effects of air pollution: enhanced aphid growth. Environ. Pollut. Ser. A., 39, 227-34. Dohmen, G. P., McNeill, S. & Bell, J. N. B. (1984). Air pollution increases Aphis fabae pest potential. Nature, Lond., 3117, 52-3. Duffey, E. (1956). Aerial dispersal in a known spider population. J. Anim. Ecol., 25, 85-111. Duffey, E. (1962). A population study of spiders in limestone grassland. The field layer fauna. Oikos, 13, 15-34. Gilbert, O. L. (1971). Some indirect effects of air pollution on bark-living invertebrates. J. appl. EcoL, 8, 77-84. Greenstone, M. H. (1984). Determinants of web spider species diversity: Vegetation structural diversity vs. prey availability. Oecologia (Berl.), 62, 299-304. Gunnarsson, B. (1983). Winter mortality of spruce-living spiders: Effects of spider interactions and bird predation. Oikos, 40, 226-33. Gunnarsson, B. (1985). Interspecific predation as a mortality factor among overwintering spiders. Oecologia (Berl.), 65, 498-502. Hogstad, O. (1984). Variation in numbers, territoriality and flock size ofa goldcrest Regulus regulus population in winter. Ibis, 126, 296-306. Jansson, C. (1982). Food supply, foraging, diet and winter mortality in two coniferous forest tit species. PhD thesis, University of G/Steborg. Jansson, C. & v o n Br6mssen, A. (1981). Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds. Holarct. EcoL, 4, 82-93.
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Lichtenthaler, H. K. (1984). Luftschadstoffe als Ausl6ser des Baumsterbens. Naturw. Rdsch., 37, 271-7. Lindberg, S. E., Lovett, G. M., Richter, D. D. & Johnson, D. W. (1986). Atmospheric deposition and canopy interactions of major ions in a forest. Science, N. Y., 231, 141-5. Nihlg~rd, B. (1985). The ammonium hypothesis--an additional explanation to the forest dieback in Europe. Ambio, 14, 2-8. Nohr, H., Hansen, K. & Braae, L. (1986). Fuglene sore indikator for skovdod? Fugle, 6, 25. (In Danish.) Norberg, R./~. (1978). Energy content of some spiders and insects on branches of spruce (Picea abies) in winter; prey of certain passerine birds. Oikos, 31,222-9. Robinson, J. V. (1981). The effect of architectural variation in habitat on a spider community: An experimental field study. Ecology, 62, 73-80. Rypstra, A. L. (1982). Building a better insect trap; An experimental investigation of prey capture in a variety of spider webs. Oecologia (BerL), 52, 31-6. Rypstra, A. L. (1983). The importance of food and space in limiting web-spider densities; a test using field enclosures. Oecologia (BerL), 59, 312-16. Thaler, E. (1973). Zum Verhalten iiberwinternder Goldh~ihnchen (Regulus r. regulus (L.)) in der Umgebung Innsbrucks (Nordtirol: Osterreich). Ber. nat.-med. Vet. Innsbruck, 60, 167-82. Turner, M. & Polis, G. A. (1979). Patterns of co-existence in guild of raptorial spiders. J. Anita. EcoL, 48, 509-20.
Spruce-living Spiders and Forest Decline; the Importance of Needle-loss
Bengt Gunnarsson Department of Zoology, University of GSteborg, Box 25059, S-400 31 G6teborg, Sweden (Received 11 June 1987; revised version received 8 July 1987; accepted 21 July 1987)
ABSTRACT Air pollution is presumed to cause needles-loss in spruce Picea abies in S W Sweden, with a consequent change in habitat structure for spruce-living spiders and other arthropods. The abundance and taxonomic composition of autumn spider populations were assessed in two close stands of spruce, having relatively high ( H) and low ( L ) percentages of needle-loss, respectively. A difference in abundance was observedfor large spiders (length > 2"5 ram), the density in the L-stand being about twice that in the H-stand. Taxonomic data suggest that needle-loss in spruce may have an impact on the composition of the spider community. Sheetweb spiders ( Linyphiidae) seemed to benefit from the more open structure caused by needle-loss, whereas raptorial spiders (mostly Thomisidae) were associated with needle-dense branches. The density reduction of large spiders in the H-stand is discussed in relation to their importance as prey for overwintering passerine birds.
INTRODUCTION Forest decline in several parts .of central and northern Europe is widely considered to be an effect of air pollution (Lichtenthaler, 1984; Blank, 1985; Nihlghrd, 1985). For instance, large amounts of pollutants, including particles and vapour, may be deposited directly on the vegetation (Lindberg et al., 1986). Needle-loss in coniferous trees in SW Sweden is an example of forest damage which is in part induced by air pollution (Andersson, 1986). This means that branches of spruce Picea abies (L.) Karst. become less 309 Biol. Conserv. 0006-3207/88/$03"50 © Elsevier Applied Science Publishers Ltd, England, 1988. Printed in Great Britain
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'needle-dense' and the proportion of needle-free twigs increases, i.e. the structural composition in the trees changes. The effects of air pollution thus change the habitat for animals living in coniferous trees and the aim of the present study was to investigate whether needle-loss affects the population of spiders, an important arthropod group living on spruce branches (Jansson & v o n Brrmssen, 1981). Indirect air pollution effects are known among other arthropods, e.g. aphids, which increase their growth rate in polluted areas (Dohmen et al., 1984; Dohmen, 1985). I report on the abundance and taxonomic composition of spruce-living spiders in SW Sweden, comparing two spruce stands with relatively high and low percentages of needle-loss, respectively. The results of this study have implications for wintering passerine birds, especially goldcrest Regulus regulus L. and tits Parus spp., which prey upon spruce-living spiders (Thaler, 1973; Jansson, 1982; Hogstad, 1984).
M A T E R I A L AND M E T H O D S The study site, which is part of a vast coniferous forest, is situated about 20 km SE of Kungsbacka in SW Sweden, with spruce the dominant tree, in different stages of succession. Spiders were collected from spruce branches in October 1985. I selected two groups of trees, situated about 75 m apart, for comparison. The weightpercentage of needles in each branch was calculated and the assumptions described below were tested. In the first group (H) a high percentage of needleloss was expected since the trees are exposed to winds from the west and southwest and are thus exposed to air pollutants. The second group (L) was situated in a sheltered position about 50 m from the forest edge and thus a lower percentage of needle-loss was expected. Each branch was dried at + 85°C for 24 h and was then divided into two fractions, needles and twigs, which were weighed to the nearest gramme. There are two advantages associated with the use of two close groups of trees for sampling: (1) effect on the spider density and species composition caused by geographical factors is minimised; (2) differences between the two spider populations compared in the present study are underestimated since all trees in the area should be more or less affected by air pollution but the severity of the damage varies. A statistically significant difference between the two stands should therefore be considered as strong evidence. A disadvantage of choosing one exposed and one sheltered group of trees is that there may be microclimate differences but this (see Discussion) should not interfere with the interpretation of the results in the present study.
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In each stand eight spruces were randomly selected, and two branches cut from each tree (Gunnarsson, 1983). The branches were taken at random up to a height of about 3 m above the ground. The branches were cut directly into, or carefully transferred to, plastic sacks, which were sealed and stored at + 4°C until examination. The spiders were obtained by cutting the branches into small pieces; each piece was shaken and carefully examined over a white bowl. The spiders were stored in 70% alcohol and identified to species or genus level. The length of each specimen was measured with a measuring ocular on a stereo microscope. The specimens were then categorised into 'small' (length < 2.5 mm) and 'large' (>2.5 mm) spiders (Askenmo et al., 1977; Norberg, 1978). The spider families were combined into four guilds depending on their hunting strategy. The 'raptorial spiders' guild used here included Thomisidae, Clubionidae, Anyphaenidae and Salticidae, with the common characteristic of not producing any hunting webs. The term 'raptorial' has been used in a more restricted sense by Turner & Polis (1979), who confined the guild to Thomisidae. Numerically, in the present case, Thomisidae made up over 80% of the guild (data from Table 3). The majority of families were web-builders, and were categorised into three guilds, following Rypstra (1982): 'orbweb spiders' including Araneidae, Tetragnathidae, Metidae, Uloboridae; 'tangleweb spiders', including Theridiidae, Dictynidae; and 'sheetweb spiders', including Linyphiidae.
RESULTS
Spruce branches The average mass for a spruce branch in the H-stand (high percentages of needle-loss expected) was 1.630kg fresh weight compared with 1.158 kg in the L-stand (low percentages of needle-loss expected). This difference is statistically significant (Table 1). When comparing the dry weights of branch-mass and twig-mass (i.e. branch-mass minus needles), the L-stand sample had significantly lower averages than the H-sample (Table 1). However, the needle-mass did not differ between the two stands. This means that the percentage of needles in relation to the total branch-mass is significantly lower (mean 32-7%) in the H-stand sample that in the L-stand (mean 39.9%) (Table 1). Hence, the branches are smaller in the L-stand than in the H-stand, but those in the L-stand are relatively needle-dense, i.e. they have low percentages of needle-loss. This is consistent with the prediction made about neddle-loss (Material and Methods).
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Bengt Gunnarsson
TABLE 1 Data on Spruce Branches in Stands with Relatively High (H-stand) and Low (L-stand) Percentages of Needle Loss, respectively
Branch-mass, fresh weight (kg) Branch-mass, dry weight (kg) Twig-mass, dry weight (kg) Needle-mass, dry weight (kg) Percentage of needles per branch
H-stand (SD)
L-stand ~ (SD)
Mann- Whitney U-test (2-tailed)
1.630 (0.730) 0.857 (0.362) 0.569 (0-232) 0.288 (0-147) 32-7 (6.7)
1.158 (0.539) 0.577 (0.263) 0.344 (0.152) 0.234 (0.117) 39.9 (5-0)
U=75-5; U = 63; U = 53; U = 103; U = 49;
Pro0.05 P < 0.02 P < 0-02 P>> 0-05 P < if01 °
° 1-tailed test, see the prediction in the text.
Spider densities The total density of spiders, and the densities for 'large' (length >_2-5 mm) and 'small' ( < 2.5 mm) specimens, were calculated in the two spruce stands, respectively. The number of spiders on each branch was related to (1) the fresh branch-mass, (2) the dry branch-mass, and (3) the dry needle-mass (all in kg). I then compared the spider categories for each set of density values. In all cases the density of large spiders was significantly lower in the Hstand than in the L-stand samples (Table 2), and that of small spiders was significantly higher in the H-stand when considering numbers per kg dry needle-mass (Table 2). No other significant differences were found. TABLE 2 Abundance of Three Spider Categories--Large and Small Specimens (delimination length 2.5 mm), and Total (large + small)--in Two Spruce Stands, of Trees with Relatively High Percentages of Needle Loss (H-stand), and Trees with Low Percentages of Needle Loss (L-stand) Spider category
Numbers/kg fresh branch-mass H-stand (SD)
Large Small Total
L-stand ~ (SD)
Numbers/kg dry branch-mass H-stand ~ (SD)
H-stand ~ (SD)
L-stand ~ (SD)
2"8 (2.1) ~-~ 5"3 (2.7) 5-2 (3'8)~b 1(~5 (5"1) 17"0 (13'4) *-% 26"3 (12"1) 26"9 (13.2) 19.0(6'2) 49-9(22"7) 38.1 (13"8) 163.1 (97.3) ~ 95"3 (31"0) 29.7 (14"6) 24.3 (7.2) 55.1 (25-2) 48.6 (15"5) 180-1(107-2) 121"5(33"9)
Mann-Whitney U-test, 2-tailed; U = 53, P < 0"02. b U = 49, P < 0-02. ' U = 73, P < 0"05. U=67, P < 0.05. °
L-stand £ (SD)
Numbers/kg dry needle-mass
313
Forest decline and spiders
There were no correlations between the spider densities and (1) the dry branch-mass, (2) the dry needle-mass, or (3) the weight percentage of needles in each branch. I tested each spruce stand separately and considered the densities of large and small specimens, and the total spider density (Spearman rank correlation tests, two-tailed, P > 0.10 in all cases). Taxonomy and guilds The percentage distribution at the family level was similar in the two spruce stands. In an average branch in the H-stand Linyphiidae made up 61-3% of the specimens in number, compared with 56.5% in the L-stand (Table 3). Thomisidae came second with 15.5% (H-stand) compared with 15.8% (Lstand). Four families occurred only in one of the stands. Uloboridae was absent from the H-stand, but scored 6.3% (the fourth family by number) in the L-stand. I calculated the spider guild densities as described above. Since no predictions about guild differences between the stands could be made (Table 3), I used two-tailed statistics in the tests. The 'orbweb spiders' was the only guild density which differed significantly between the H- and L-stands, this group being more common in the L-stand (Table 4), due to the high densities of the Uloboridae (Table 3). TABLE 3 Taxonomic Composition as Percentage Distribution in Spruce Stands with High (H-stand) and Low (L-stand) Percentages of Needle Loss, respectively Family
Clubionidae Anyphaenidae Thomisidae Salticidae Dictynidae Theridiidae Uloboridae Tetragnathidae Metidae Araneidae Linyphiidae Unidentified
Guild
"~ t ~, f "~ I
Raptorial Tangleweb Orbweb Sheetweb
H-stand % (SO)
L-stand % ~ (SD)
0.7 (1.1) 1.3 (2.6) 15.5 (10.4) 0-4 (1-4) 1-5 (2-0) 12.3 (8.6) 0 0-2 (0.7) 0 4.3 (5"9) 61-3 (12.7) 2.4 (5"1)
3-7 (4-5) 0 15.8 (10-4) 0 1.4 (2-2) 10.3 (6.8) 6.3 (9-0) 1.1 (2.3) 0-6 (1.8) 3-5 (3"5) 56-5 (16-6) 0"7 (2"2)
99-9 (n = 725) 99"9 (n = 456)
Bengt Gunnarsson
314
TABLE 4 A b u n d a n c e o f F o u r Spider G u i l d s (see text) in Spruce Stands with High (H-stand), a n d L o w (L-stand) Percentages o f Needle Loss, respectively
Guild
Numbers/kg fresh branch-mass H-stand Yc(SO)
Raptorial spiders Orbweb spiders Tangleweb spiders Sheetweb spiders
L-stand ~ (SD)
5"6 (4.2) 4.6 (2.4) 1"2 (1.5) ~ ° ~3.2 (3.5) 4"0 (3"2) 2'8 (1'9) 18-1 (9.7) 13.3 (4.4)
Numbers/kg dry branch-mass H-stand .~ (SD)
L-stand .f (SD)
10-5 (7.8) 9-1 (4'6) 2-2 (2-9) ~ b ~ 6'5 (6.9) 7.4 (5-5) 5'7 (4"1) 33.4 (16.8) 26.7 (9-5)
Numbers/kg dry needle-mass
H-stand .~ (SD)
L-stand ~ (SO)
32"6 (24.3) 22.7 (lff7) 6-3 (7"9)~-L-~15"5(15"6) 25'8 (28"0) 13"8 (9'7) 110.5 (66.8) 68.3 (27.4)
° Mann-Whitney U-test, 2-tailed; U = 71.5, P < 0.05. b U = 70, P < 0"05. c U = 7 2 , P <0-05.
Two related hypotheses were tested. First, I assumed that the high relative abundance of raptorial spiders is associated with branches with high weight percentages of needles, since such branches should offer good hiding-places for the spiders between the needles. The proportion of raptorial spiders was calculated in relation to the total number of identified specimens, and a positive correlation was found in the H-stand (Fig. 1 (a); Spearman rank correlation test, one-tailed; r s = 0.450, P < 0.05). In the L-stand no such correlation was found (Fig. l(b)). Second, the needle-loss on spruce branches might provide web-builders with better possibilities for attaching their webs to the twigs and if the first hypothesis is valid may thus increase their relative abundance. I tested this hypothesis on the sheetweb spiders since they were the most abundant of the web-builders (Table 4). Correlations were found between increasing percentage of twig-mass and the relative abundance of sheetweb spiders in the two spruce stands (Fig. l(c), (d); H-stand: rs = 0.607, P < 0.01; L-stand: r s = 0.426, P ,.~ 0"05). When considering the relative abundance of the three web-building guilds together I found a significant correlation in the H-stand (r~ = 0"450, P < 0"05), but not in the L-stand (r~ = 0-085, P > 0"25).
DISCUSSION The abundance of large spiders was considerably higher in the L-stand compared with the H-stand. The spruce branches in the L-stand differed from the H-stand branches by, on average, being lighter and having higher percentages by weight of needles. This might suggest a relation between the size distribution of the spiders and the structural differences between the
Forest decline and spiders
W t.
315
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Fig. 1. The relative abundances of raptorial and sheetweb spiders in each branch in relation to the percentages of the mass of needles and twigs, respectively. Raptorial spiders in (a) the H-stand (trees with relatively high percentages of needle-loss), and (b) the L-stand (low percentages of needle-loss). Sheetweb spiders in (c) the H-stand, (d) the L-stand. N.B.: Different scales on abscissa in (c) and (d). branches in the two stands. However, this hypothesis has to be examined in m o r e detail by further studies. A tentative explanation o f the density differences o f the large spiders in the two stands m a y be bird predation, which is k n o w n to cause high mortality a m o n g spruce-living spiders (Askenmo et al., 1977; Gunnarsson, 1983). Large spiders might be more vulnerable to bird predation in the H-stand than in the L-stand since they should be easier to detect on branches with few needles. A n alternative explanation for the differences in the spider size
316
Bengt Gunnarsson
distribution is that the microclimate may have favoured large spiders in the sheltered L-stand, which is probably wetter and colder than the exposed Hstand. This hypothesis cannot be ruled out completely, but experimental results on dune-living spiders (including Philodromus aureolus (Clerck) which is common on spruce branches (Norberg, 1978; Gunnarsson, 1985)) show that there is no general correlation between the size of spiders and their resistance to desiccation, or thermal tolerance (Almquist, 1970, 1971). The reason for the higher density of small spiders in the H-stand than in the L-stand is uncertain since it was found only when relating numbers to the needle-mass. There are two possible explanations: (1) a low predation rate on small specimens in the H-stand since there are few large spiders (Gunnarsson, 1985), and (2) aeronautic spiders, i.e. mostly small specimens (Duffey, 1956), may be 'caught' by the forest edge. The approximate 50% reduction in the density of large spiders in the trees with high needle-loss may have serious effects on overwintering passerine birds. Spiders are important winter food for these birds (Jansson, 1982; Hogstad, 1984) and there are few alternative prey items in spruce (Jansson & von Br6mssen, 1981), In October spiders thus made up 45% of the total number of prey items for goldcrests foraging in spruce, but as winter progressed, they became more important, and in January and February formed about 80% of the prey (Hogstad, 1984). Index data from Denmark for the latest 10-year period show decreasing trends in population size for the goldcrest, crested tit and coal tit (P. ater L.) (Nohr et al., 1986) in coniferous forests. It is not known what caused this decrease but reduced winter food supply is a possible explanation. The autumn density of large spiders was on average 2.8 specimens kg- 1 fresh branch mass in the H-stand in contrast to 5-3 in the L-stand. In previous quantitative samples from spruce branches, taken between 1972 and 1978 about 30 km NE of the study site used here, the average autumn density of large spiders was 6.8 specimens kg- 1 fresh branch mass (mean value for six autumns, range 4.4-10.8) (Jansson & v o n Br6mssen, 1981). This may suggest a reduction of large spiders due to temporal factors, but since the samples were taken in different areas spatial differences may also be involved. The difference in orbweb spider density between the spruce stands was caused by the presence of Hyptiotesparadoxus (C. L. Koch)(Uloboridae), in the L-stand but not in the H-stand. In this case it cannot be ruled out that the microclimate, i.e. presumably wetter and colder in the L-stand than in the Hstand, caused the difference. Three more families occurred in only one of the two stands (Table 3). Their abundance was, however, very low, so they do not affect the densities of the guilds to any great extent. The absence of major differences in taxonomic composition and guild
Forest decline and spiders
317
density between the stands may be an effect of the close location of the spruce stands. When the results in the present study are compared with quantitative samples taken in the study site of Jansson & von Brrmssen (1981) in 1975 and 1976, Thomisidae was the most abundant family with 37-45% by number (Norberg, 1978), versus 16% in my samples (Table 3). Linyphiidae made up 27% in the 75/76-samples (Norberg, 1978) versus 57--61% in the present study. These differences may be due to both spatial and temporal factors. It should, however, be noted that the forest decline has accelerated during these ten years (Blank, 1985). The hypothesis that the microhabitat change in spruce branches, caused by needle loss, may affect the taxonomic composition is supported by my results. In the H-stand high relative abundances of the raptorial spiders, consisting of Thomisidae (80%), were associated with needle-densebranches. No such correlation was found in the L-stand (Fig. l(b)). This may be due to the low variation in the percentage of needles (range 31.3-46-5%) in the L-stand samples. In the H-stand the range was 18.0-46.3% and the probability of detecting a correlation thus increased. Also, sheetweb spiders (Linyphiidae) increased their relative abundance when the percentage of twigs (i.e. branch-mass minus needles) increased. Consequently, the needleloss in coniferous trees seems to favour sheetweb spiders over raptorial species. Thus, the results seem to be in accordance with several other studies which have shown that habitat structure is an important determinant of the spider community (e.g. Duffey, 1962; Robinson, 1981; Rypstra, 1983; Greenstone, 1984). So far only a few investigations have focused on spiders in relation to air pollution. For instance, a negative correlation between the number of spider species and SO2-concentrations was found by Andr6 (1977) and Clausen (1984, 1986), but not by Gilbert (1971). The data from Andr6 (1977) also showed a negative correlation between spider density and SO2. These results could be attributed to structural differences, for example, the frequency of epiphytes, between the habitats (Clausen, 1986). In conclusion, large spiders were scarce in spruce branches with a relatively high percentage of needle-loss. Also, the taxonomic composition, as indicated by the relative abundance of different spider guilds, was correlated with the percentage of needles, or twigs, on the branches. Hence, the results support the hypothesis that the spider populations were affected by the forest decline and accompanying alteration of the spruce microhabitat. ACKNOWLEDGEMENTS I thank Mikael Hake for excellent assistance in the field and in the laboratory, Conny Askenmo and Jan Ekman for discussions, and Mats
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Eriksson for reading this manuscript. The study site was suggested by Bengt Hasselroth and Folke Andersson. This study was supported by grants from the National Swedish Environmental Protection Board.
REFERENCES Almquist, S. (1970). Thermal tolerances and preferences of some dune-liv.ing spiders. Oikos, 21, 230-6. Almquist, S. (1971). Resistance to desiccation in some dune-living spiders. Oikos, 22, 225-9. Andersson, F. (1986). Acidic deposition and its effects on the forests of Nordic Europe. Water, Air & Soil Pollut., 30, 17-29. Andr6, H. (1977). Introduction ~ l'6tude 6cologique des communant6s de microarthropodes corticoles soumises ~ la pollution atmosph6rique, II. Recherche de bioindicateurs et d'indices biologiques de pollution. Ann. Soc. r. Zool. Belg., 106, 211-24. Askenmo, C., von Br6mssen, A., Ekman, J. & Jansson, C. (1977). Impact of some wintering birds on spider abundance in spruce. Oikos, 28, 90-4. Blank, L. W. (1985). A new type of forest decline in Germany. Nature, Lond., 314, 311-14. Clausen, I. H. S. (1984). Notes on the impact of air pollution (SO2 & Pb) on spider (Araneae) populations in North Zealand, Denmark. Ent. Meddr., 52, 33-9. Clausen, I. H. S. (1986). The use of spiders (Araneae) as ecological indicators. Bull. Br. arachnol. Soc., 7, 83-6. Dohmen, G. P. (1985). Secondary effects of air pollution: enhanced aphid growth. Environ. Pollut. Ser. A., 39, 227-34. Dohmen, G. P., McNeill, S. & Bell, J. N. B. (1984). Air pollution increases Aphis fabae pest potential. Nature, Lond., 3117, 52-3. Duffey, E. (1956). Aerial dispersal in a known spider population. J. Anim. Ecol., 25, 85-111. Duffey, E. (1962). A population study of spiders in limestone grassland. The field layer fauna. Oikos, 13, 15-34. Gilbert, O. L. (1971). Some indirect effects of air pollution on bark-living invertebrates. J. appl. EcoL, 8, 77-84. Greenstone, M. H. (1984). Determinants of web spider species diversity: Vegetation structural diversity vs. prey availability. Oecologia (Berl.), 62, 299-304. Gunnarsson, B. (1983). Winter mortality of spruce-living spiders: Effects of spider interactions and bird predation. Oikos, 40, 226-33. Gunnarsson, B. (1985). Interspecific predation as a mortality factor among overwintering spiders. Oecologia (Berl.), 65, 498-502. Hogstad, O. (1984). Variation in numbers, territoriality and flock size ofa goldcrest Regulus regulus population in winter. Ibis, 126, 296-306. Jansson, C. (1982). Food supply, foraging, diet and winter mortality in two coniferous forest tit species. PhD thesis, University of G/Steborg. Jansson, C. & v o n Br6mssen, A. (1981). Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds. Holarct. EcoL, 4, 82-93.
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Lichtenthaler, H. K. (1984). Luftschadstoffe als Ausl6ser des Baumsterbens. Naturw. Rdsch., 37, 271-7. Lindberg, S. E., Lovett, G. M., Richter, D. D. & Johnson, D. W. (1986). Atmospheric deposition and canopy interactions of major ions in a forest. Science, N. Y., 231, 141-5. Nihlg~rd, B. (1985). The ammonium hypothesis--an additional explanation to the forest dieback in Europe. Ambio, 14, 2-8. Nohr, H., Hansen, K. & Braae, L. (1986). Fuglene sore indikator for skovdod? Fugle, 6, 25. (In Danish.) Norberg, R./~. (1978). Energy content of some spiders and insects on branches of spruce (Picea abies) in winter; prey of certain passerine birds. Oikos, 31,222-9. Robinson, J. V. (1981). The effect of architectural variation in habitat on a spider community: An experimental field study. Ecology, 62, 73-80. Rypstra, A. L. (1982). Building a better insect trap; An experimental investigation of prey capture in a variety of spider webs. Oecologia (BerL), 52, 31-6. Rypstra, A. L. (1983). The importance of food and space in limiting web-spider densities; a test using field enclosures. Oecologia (BerL), 59, 312-16. Thaler, E. (1973). Zum Verhalten iiberwinternder Goldh~ihnchen (Regulus r. regulus (L.)) in der Umgebung Innsbrucks (Nordtirol: Osterreich). Ber. nat.-med. Vet. Innsbruck, 60, 167-82. Turner, M. & Polis, G. A. (1979). Patterns of co-existence in guild of raptorial spiders. J. Anita. EcoL, 48, 509-20.