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Canopy arthropods on Scots pine: influence of season and stand age on community structure and the position of sawflies (Diprionidae) in the community
Forest Ecology and Management, 62 (1993) 85-98
85
Elsevier Science Publishers B.V., Amsterdam
Canopy arthropods on Scots pine: influence of season and stand age on community structure and the position of sawflies (Diprionidae) in the community Jii-i Simandl Institute of Entomology, CzechAcademy of Sciences, Brani~ovskd 31, 3 70 05 ~eskk Bud~jovice, Czech Republic (Accepted 8 July 1993)
Abstract
The response of arthropods to season and age of stands was studied in the crowns of managed, pure Scots pine stands (Pinus sylvestris L. ) by insecticide fogging. Pine monocultures were characterised by a stable guild composition (defoliators being predominant) rather than by the composition of taxonomic groups (orders) which are subject to seasonality (mainly Hymenoptera, Coleoptera, Lepidoptera, Homoptera). The second variable (age) had more influence on the community composition than the first (season). In total, significant differences related to the age of the pines were found among most of the arthropod taxa, the medium-aged stands showing a higher density of arthropods in the crown strata. The evaluation of abundance of Hymenoptera (sawfly larvae being the majority in samples----eight species present) by canonical correspondence analysis, in relation to the two environmental variables examined, showed their shift towards the spring (June) in the ordination diagram, when the population density of pine sawfly larvae was higher in comparison with the late summer period. The age variable was not significant in diprionid response. Quantitative data on the most numerous arthropods are included.
Introduction
Using different methods, the species composition of arthropods associated with Scots pine (Pinus sylvestris L. ) tree crowns has been studied by several authors in Europe. There are data on species composition and succession or changes in the abundance of species during the growing season, but pine sawfly populations have received little attention. The group is briefly mentioned in some studies (Engel, 1941; Klomp and Teerink, 1973; Borkowski, 1986 ) but these data show a very low abundance and diversity of diprionids. Hrregot's ( 1960 ) study does not include the needle-eating hymenopterans living in pine crowns at all. © 1993 Elsevier Science Publishers B.V. All rights reserved 0378-1127/93/$06.00
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There have been a few attempts to study patterns that could be useful in identifying community responses to environmental conditions (e.g. Lawton, 1984) in coniferous trees because changes in the community structure may support or limit populations of economically important pine insects (Strong et al., 1984; Schowalter, 1986 ). Some detailed data are available on abundance and food (foliage) consumption by insects feeding on pine needles (Larsson and Tenow, 1980). Feeding dynamics in relation to stand age reported by Tenow and Larsson (1987) concern the main selected defoliators (including Diprionidae). The guilds within the community of pine defoliators have not been well studied. In this study we examined: (a) the effect of season and stand age on the structure of functional and taxonomical groups of arthropods; (b) the composition ofarthropods (higher taxa-orders) and quantitative contribution of guilds/orders to canopy arthropod community; (c) the proportion of pine sawfly larvae (non-outbreaking population) within a season/age class in comparison with other coexisting arboreal arthropods. This paper is also based on the results of several years monitoring of nonoutbreaking populations of pine sawflies and coexisting defoliators. Materials and methods
Study sites Field investigations were conducted in managed, pure Scots pine stands in southern Bohemia, Czechoslovakia (elevation 450-500 m) in 1988. Two stand groups (age classes) separated by a pine plantation were chosen (the wood complex of about 20 000 ha is situated in a region of original occurrence of Scots pine). One group of stands was aged up to 50 years (40-50 years; hereafter referred to as medium-aged stands ); the other group of stands was aged over 80 years (80-100 years; referred to as mature stands). Characteristics of the examined groups of stands are included in Table 1. Mean Table 1 Characteristics of the investigated Scots pine stands (Pinus sylvestris L. ) Stand age (years)
DBH l (mm)
Mean tree height
Tree density ( h a - l)
(m) 41 45 83 91 ~Diameter at breast height.
120 120 210 260
12.0 13.0 16.5 22.5
2600 2700 1400 1100
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annual temperature is 7.4 ° C , and mean annual precipitation in the region is 639-670 mm.
Methods Insecticide fogging was used for direct examination of the arthropod community. Within each stand site, which was a 100 m 2 unit (n = 32 ) situated on the stand diagonal transect (n = 6), one tree (n = 15 in the mature, n = 17 in the medium-aged stands) was treated. The distance between these randomly sampled sites was 200 m. Dead insects were collected on sheets of paper 1 m 2 in size (n = 11-21, their area depended on the crown projection size) spread under the crown projection of the treated tree. All arthropods were collected for 3 days after the treatment. Samples were taken by canopy fogging with a synthetic pyrethroid insecticide Cymbush 10 EC (ICI, U K ) applied with a Thermofog TF 30 (IGEBA, Germany). Insecticidal treatments were applied on 3-7 June and 18-20 September, early in the morning when weather conditions were suitable (04:30-06:00 h, air flow up to 0.4 m s -1). The treatments were timed for peaks of the seasonal abundance of the pine sawfly complex established in previous years (Simandl, 1989 ).
Guild separation The arthropods included in samples were sorted into higher taxa (orders) in the laboratory and assigned to the following seven guilds according to their relationships to the host plant. Defoliators: a group including needle-eating insects with trophic relations to the foliage or reproductive organs of Scots pine: it is represented by larvae of the orders Hymenoptera (Symphyta), Lepidoptera, and some adult beetles (Coleoptera). Predators: mainly Brachycera, Arachnoidea including Araneae plus Pseudoscorpiones, predacious Heteroptera and Coleoptera-Carabidae living in crown strata. Detritivores (saprophages): represented by the orders Psocoptera and Blattodea, or developing in the litter layer (some Diptera, Coleoptera, etc. ). Sap-suckers: sucking on bark, foliage or shoots, represented for example by Homoptera (Aphidoidea, Cicadoidea) and bugs (Heteroptera: Aradidae). Parasitoids: parasitic Hymenoptera (Ichneumonidae, Braconidae, etc. ) and Diptera (Tachinidae) associated with primary consumers. Xylophages: adults sampled; larvae living in woody and subcortical tissues of pines (mainly Coleoptera-Cerambycidae, Curculionidae, HymenopteraSyricidae ). Others ('tourists'): arthropods with no relation to pine as a host, or without direct relation to primary consumers of pines. This group includes migrating
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insects, such as aquatic species (Ephemeroptera, Plecoptera, Trichoptera) and individuals of other groups accidentally present, e.g. defoliating beetles living on deciduous trees, in the herbaceous stratum, etc.
Statistical methods The influence of environmental variables, i.e. age and season on arthropod (guild/taxa) densities and the significance of differences were evaluated by the analysis of variance (two-way ANOVA) followed by the Student-Newman-Keul test. Theoretically, all the canopy arthropods (guilds/taxa) had the same opportunity of reacting to the same composite gradients of environment, in this case the age of trees and the season. For the division of main macroarthropod taxa and guilds in relation to the age of the trees and season we used two canonical correspondence analyses (CANOCO) (CCA) which escape the assumption of linearity and can detect unimodal relationships between animals and external variables (cf. ter Braak, 1987). Differences among the treatments were evaluated by cluster analysis (Orl6ci, 1978) where dissimilarity measure is the non-standardised Euclidean distance and average linkage is used for hierarchical clustering. For this purpose, the individual trees (n = 32 ) were grouped according to annual period and stand age. Results
Guilds The total abundance distribution of the functional groups (guilds) of arthropods in the samples is shown in Fig. 1. In comparison with the results of Basset ( 1985 ), the prevalence of guilds more closely related to the host plant, i.e. primary consumers (defoliators and xylophages) indicated that the feeding pressure of phytophages was relatively high, which is a general trait of forest monocultures. Consequently, the higher abundance of primary consumers was reflected by the presence of numerous natural enemies (predacious and parasitic arthropods) in samples. The influence of season on the density of most guilds was low, being significant only in three (defoliators, predators and parasitoids ). However, the influence of stand age on numerical contributions of the guilds was distinct; there were significant differences in all the guilds related to the host plant (Table 2). The medium-aged stands exhibited significantly higher population densities of all arthropod guilds, the densities of both main guilds, i.e. defoliators and predators, being especially high ( P < 0.001 ). The main differences within the guild of defoliators were caused by increased population densities of Bupalus piniarius L. (Geometridae) larvae in the medium-aged stands during the second sampling period. The influence of both variables examined by CCA was found not to be signif-
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J. Simandl I Forest Ecology and Management 62 (1993) 85-98
n
1400
1200
-----7 1000
800
~ 7 600
400
200
Df
Pd
Dt
Se
Ps
Ot
Xy
Guilds Fig. 1. Frequency distribution of arthropod abundances according to guilds in the crown strata of managed Scots pine stands. Hatched area, proportion ofdiprionid larvae; Df, defoliators; Pd, predators; Dr, detritivores; Sc, sap-suckers; Ps, parasitoids; Ot, others ('tourists'); Xy, xylophages.
Table 2 Guild mean ( _+SD) densities (n per 100 m 2) in relation to season and age Guild
All arthropods Defoliators Predators Detritivores Sap-suckers Parasitoids Others Xylophages
Season
P
Spring
Autumn
2600 697(323) 724(361) 462(284) 346(220) 159(138) 79(77) 35(52)
2870 1135(495) 941(486) 562(287) 302(199) 81(75) 73(74) 24(23)
** * NS NS * NS NS
*P< 0.05; **P< 0.01 ; ***P< 0.001 ; NS, non-significant.
Stand age (years) < 50
> 80
2603 1135(418) 1134(325) 631(250) 414(228) 172(139) 93(92) 45(50)
1880 638(364) 476(211) 371(264) 225(127) 66(50) 58(44) 13(15)
P
*** *** ** ** ** NS *
16.6 10.4 38.0 7.6 2.7 0.7 12.3 7.0 0.8 1.6 10.3 2.4
453(230) 287(148) 927(494) 200(176) 81(54) 53(36) 369(263) 164(104) 51(29) 48(46) 230(169) 54(47)
66(13) 37(30) 171(125) 40(24)
312(146) 183(121) 537(313) 368(367) 911(402) 349(181) 219(197) 265(198)
Mean (SD)
Mean (SD)
D%
September
June
Season
0.3 0.7 4.4 0.4
9.0 6.2 15.4 11.7 31.4 10.1 8.7 7.7
D%
NS NS NS -
* NS *** NS ** ** NS NS
P
39(18) 55(47) 262(171) 45(44)
472(203) 267(133) 1022(424) 272(217) 582(573) 243(232) 422(274) 251(120)
< 50 Mean (SD)
Age (years)
69(26) 31(23) 135(88) 65(35)
290(165) 206(154) 428(236) 365(286) 387(343) 148(95) 213(124) 191(165)
> 80 Mean (SD)
1Family, included also in Hymenoptera. 2Class. 31ncluding Trichoptera (n = 17), Ephemeroptera (n = 5 ), Plecoptera (n = 21 ), Dermaptera (n = 9) and Orthoptera (n = 3). *P< 0.05; **P< 0.01 ; ***P< 0.001 ; NS, non-significant; n = 17, 15, 17, 15 for the four sampling events, respectively.
Hymenoptera Diprionidae ~ Coleoptera Diptera Lepidoptera Heteroptera Homoptera Psocoptera Neuroptera and Raphidioptera Blattodea Arachnoidea 2 Others 3
Order
NS * * -
** NS *** NS * *** * NS
P
29/7 91/6 571/70 -
593/220 407/31 1443/140 300/47 1473/27 373/6 482/147 327/76
M/m
Table 3 Average ( _+SD) density (n per 100 m 2 ), dominance (D%), and recorded maxima (M) and minima ( m ) of densities of arthropods sampled in Scots pine crowns as related to season and age of stand
5-,
~D O
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J. Simandl / Forest Ecology and Management 62 (1993) 85-98
X I)I
X NIl
X P!;
X L I'
o I: 4 × ItY
oCI ~HO XAR
xco
X tll X BI IIY [:[1 lit LP I1[ t10 P~; NR Bt
HYMENOPTERA [:OL[OPTERA OIt'TERA LEPIOOPTI.RA HETEROPTERA IIOBOPT ERA PSOCOPTERA NEIJROPT[RA : ;RAPtlIBIOPIERA Ill ATTODCA
Fig. 2. Results of CCA of the main taxa of arthropods sampled in Scots pine crowns. Centroids of environmental variables: C1, spring (June); C2, late summer (September); C3, less than 50 years of age; C4, more than 80 years of age; x, order locations. icant for changes in the distribution of arboreal guilds (P = 0.14, Monte Carlo permutation test) and there was no defined, distinct assemblage of guild members in pine crowns. The composition of guilds was more stable than that of taxonomic groups.
Taxa (orders) In total, 3622 arthropod specimens of 15 insect orders and the class Arachnoidea fell from the crown strata at canopy fogging (for survey see Table 3 ). Significant quantitative changes in the density of arthropods with season were found in four orders whose members are more (Coleoptera, Lepidoptera and Heteroptera) or less (Hymenoptera, mainly Diprionidae sampled) subject
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J. Simandl / Forest Ecology and Management 62 (1993) 85-98
ED
10
Im
I v
~
.
.
.
.
v
Fig. 3. Dendrogram of the cluster analysis of arthropod samples. Dissimilarity measure, nonstandardised Euclidean distance (ED). 1, Spring sampling period; 2, late summer sampling period; MEa, medium-agedstand; MTR, mature stand (age of stand in parentheses). to seasonality (Table 3 ). The first sampling period was dominated by Coleoptera and among them the herbivorous pine blossom weevil Anthonomus pubescens Payk. (Curculionidae) (up to 710 individuals per 100 m 2 in medium-aged stand) along with the predacious Halyzia 28-guttata L. (Coccinelidae) were the most numerous. However, the abundance of Lepidoptera and predaceous Heteroptera peaked during the second sampling period owing to increasing B. piniarius and Miridae populations. Greater differences were found between age classes. Seven arthropod orders exhibited significant preferences for the medium-aged stand habitat (Table 3 ) where the densities of some species (as mentioned above) were high. The results of correspondence analysis (Fig. 2 ) of the whole set of the most abundant arthropod orders show that most of them were allocated into two opposite groups along the first axis which corresponds to higher variation in the seasonal structure. The stand age mainly contributed to ordination along the second axis. The influence of both variables examined by CCA was signif-
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J. Simandl / Forest Ecology and Management 62 (1993) 85-98
icant ( P < 0.05 ) for taxonomic composition and as a result most of the orders were characterised by preference for medium-aged stands in the original pine ecosystems. The diagram also shows that the age variable contributed more to the community composition than the seasons. A comparison of treatment similarities (Fig. 3 ) shows three groups of samples separated according to the sampling period and stand age. The primary bifurcation among the sample clusters is between the seasons ( 1 vs. 2, see Fig. 3 ) followed by division according to the level of age variable.
The position of pine sawflies Diprionidae were represented by eight species in the samples. Their quantitative position (dominance) within the arthropod canopy community as related to season is shown in Fig. 4. Their bivoltinism (except for Neodiprion sertifer Geoff. ) was an assumption for their more abundant occurrence during the seasons, with larval density higher during the first (spring) wave 3 UNE
SEPTEMBER
YEAR
COLEOPTERA
~NEUROPTERA+ +RAPHIDIOPIERA BLATTODEA
DIPTERA
~HOMBPTERA
IIYMENOP]ERA ~
L.EPIDOPTERA
PSOCOPTERA
HEIEROPIERA
ARACHNDIDEA
DPR DIPRIONIDAE
~ ] ~ OIHERS
Fig. 4. Seasonal position (dominance) of diprionid larvae as related to coexisting groups of arthropods (taxa) in Scots pine crowns.
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J. Simandl / Forest Ecology and Management 62 (1993) 85-98
(presence of N. sertifer larvae). Several characteristic pine feeders contributed to the bimodal abundance pattern within the seasons, i.e. sawfly larvae along with herbivorous beetles (Anthonomus spp. and others) and Panolis flammea (D&S) larvae contributed to an increase in defoliator abundances during the first (spring) sampling period, unlike the second sampling period when another peak of defoliators included mainly B. piniarius larvae plus the second wave of diprionids. These herbivores were characteristic of the situation in pure pine forests when defoliators were the most stable and constant guild during the season. The annual population of sawfly larvae averaged onetwelfth (238.5 +_ 144.3 individuals per 100 m 2 ) of all arthropods in the crown strata (see Fig. 1 ). Differences in sawfly densities as related both to seasonal period and age were not significant (Table 3 ), the group being constant and having a relatively stable position (peaking at least twice during the season) in the pine canopy community. Discussion
Guilds A comparison of the results of this study with those existing for guilds in coniferous (Douglas fir) (cf. Schowalter et al., 1988 ) as well as North American deciduous (Schowalter and Crossley, 1987) forests indicated a functional similarity of arthropod guilds of the examined forest types, comparable data not being available for European coniferous forests. Basset ( 1985 ) found at most 6.0% of defoliators among arthropods on Pinus mugo Turra, and our results indicate that Scots pine monocultures support higher densities of primary consumers. The first successional stages of young coniferous forests are usually characterised by the dominance of sap-suckers (Mispagel and Rose, 1978; Schowalter et al., 1988) along with their higher biomass (Schowalter, 1989 ). In contrast, the old-growth conifer canopies (more than 400 years old) were dominated by defoliators with a lower herbivore biomass (Reichle et al., 1973; Schowalter et al., 1988). Relatively high consumption rate caused by defoliators in a mature Scots pine stand was demonstrated in the 1 year study of Larsson and Tenow (1980). The observed responses of the most important pine species (mainly of the defoliators guild) to the environmental variables examined seemed to be best explained by the age of stands; the denser stands supporting mainly higher densities of primary consumers and their enemies. Variation in the population density of some species each year are also reflected adequately at guild level (defoliators and predators).
Taxonomic composition and reliability of the method The direct, quantitative sampling method of insecticide fogging reveals a larger part of canopy-inhabiting free-living insects (see Noyes, 1989; Morse
J. Simandl / Forest Ecology and Management 62 (1993) 85- 98
95
et al., 1988 ), but its disadvantage is that it may underestimate some groups, e.g. sedentary arthropods, leaf and bud miners, fast flying insects, etc. (Majer and Recher, 1988 ). Among the fallen macroarthropods we also found larvae of Acantholyda nernoralis Thomson (Tenthredinidae) living solitarily in silk tents. Beetles are reliably sampled by this method (Stork, 1987), and probably also all free-living larvae of pine sawflies. However, winged and highly mobile adults of some insects react quickly to insecticide application and may escape from the treated tree space. To prevent most of these mobile insects from escaping, treatments were performed early in the morning when the air was cooler and the mobile insects were unable to react quickly. Even so, some adult moths and dipterans may have been underestimated in the samples. Some accidentally represented groups of aquatic insects classified as 'tourists' in pine crowns occurred there because of relatively short distances from water sources (ponds/streams). According to a preliminary estimate, it seems that the arthropod species composition and richness (except for Diprionidae) was similar (more than 100 species present) to data reported from other European pine regions (see Klomp and Teerink, 1973; Borkowski, 1986). Both qualitative and quantitative differences may have been due to the different methods used and geographic regions sampled. Although the arthropod densities were similar during both seasons, the spring seems to exhibit a greater suitability of environmental conditions resulting in a higher species diversity. Nevertheless, parallel investigations (frass-drop measurements, insect trapping) suggest that needle-eating insect species (larval stage) were usually dominant in the examined plots (unpublished data), especially in medium-aged managed monocultures.
Position of pine sawflies and other defoliators A long latency of insects depends on many factors (e.g. Hanski, 1987). During this phase, non-outbreaking sawfly populations fluctuate within certain limits among years (Simandl, 1989), but density amplitudes are usually relatively lower in comparison with outbreaking populations. The estimated density of sawflies in stands over 40 years old varied at endemic level from 2000 (seasonal minimum, Simandl, 1989 ) to 30 000 larvae ha-1 in a mature stand (seasonal maxima, central Sweden, Larsson and Tenow, 1980). Some maximal local densities of sawfly larvae in the investigated region were over 40 000 ha -1 (unpublished data); because there were eight species present, their feeding lasted 5.5-6 months in this geographical zone (Simandl, 1989 ). During the monitoring of pine defoliators the density of B. piniarius regularly increased in autumn each year (unpublished data). Our results suggested bimodal seasonal pattern of abundances of main defoliators in pine monocultures (Larsson and Tenow, 1980): the first peak
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J. Simand! /Forest Ecology and Management 62 (1993) 85-98
(June) was dominated by herbivorous Coleoptera+ first wave of diprionids +Panolisflammea, the second one (September) by B. piniarius+ second wave of diprionids + Geometridae in samples. Of the two seasonal peaks of insect defoliators, the second is more important because the loss of needles caused by their feeding pressure is the highest in late summer when the food consumption of B. piniarius and the complex of diprionid species culminates (Larsson and Tenow, 1980; Tenow and Larsson, 1987) along with the consumption of other defoliating insects. Presumably, the loss of foliage caused by the defoliator complex can affect, negatively, the growth of the trees, more during late season (Ericsson et al., 1980). The probability of development of outbreak foci is apparently higher in medium-aged stands owing to better trophic conditions (greater volume of foliage) with a greater abundance of pine defoliators to whose activity these stands are naturally susceptible. However, increased species diversity of arthropods, orders of which were distributed more frequently between centroids C 1 and C3 (Fig. 2, spring, mediumaged stands), may contribute to the ecosystem stability. Nevertheless, the repetition of peaking of typical pine insects (mainly defoliators) each year was distinct during both previous and subsequent investigations (unpublished data). These swings of the population densities support the opinion that pine monocultures are vulnerable to attack of insects at any other (abiotic) disturbance of their balance, e.g. poor soil conditions (White, 1984; Leather and Barbour, 1987; Mattson and Haack, 1987; Niemel~i et al., 1987 ) in connection with water stress (Wagner and Frantz, 1990) can create optimal trophic conditions for population growth of needle-eating insects.
Acknowledgements The author is indebted to anonymous referees for their helpful critical comments on the former version of this paper, and to Dr. J. Lep~ (Centre of Biomathematical Methods, Czech Academy of Sciences) for his kind assistance in the processing of statistics.
References Basset, Y., 1985. Aspectsde la r6partition des peuplementsd'arthropodes dans les coronnes de Pinus mugo Turra. Mitt. Schweiz.Entomol. Gessel., 58: 263-274. Borkowski, K., 1986. Contribution to the knowledgeof the insect fauna of the crown of Scots pine trees. Pol. Pismo Entomol., 56:667-676 (Englishsummary). Engel,H., 1941. Beitr~igezur Faunistikder Kiefernkronenin verschiedenenBestandstypen.Mitt. Forstw. Forstwis., 12:334-361. Ericsson, A., Larsson, S. and Tenow, O., 1980. Effects of early and late season defoliation on growth and carbohydratedynamics in Scotspine. J. Appl. Ecol., 17: 747-769. Hanski, I., 1987. Pine sawfly population dynamics: patterns, processes, problems. Oikos, 50: 327-335.
J. Simand! / Forest Ecology and Management 62 (1993) 85-98
97
H6regot, H., 1960. Untersuchungen iiber die qualitative und quantitative zusammensetsung der Arthropodenfauna in den Kiefernkronen. Beitr. Entomol., 10:891-916. Klomp, H. and Teerink, B.J., 1973. The density of the invertebrate summer fauna on the crowns of pine trees, Pinus sylvestris, in the central part of the Netherlands. Beitr. Entomol., 23: 325-340. Larsson, S. and Tenow, O., 1980. Needle-eating insects and grazing dynamics in a mature Scots pine forest in Central Sweden. In: T. Persson (Editor), Structure and Function of Northern Coniferous Forests--An Ecosystem Study. Ecol. Bull. (Stockholm), 32: 269-306. Lawton, J.N., 1984. Herbivore community organization: general models and specific tests with phytophagous insects. In: P.W. Price, C.N. Slobodchikoffand W.S. Gaud (Editors), A New Ecology. Wiley, New York, pp. 329-352. Leather, S.R. and Barbour, D.A., 1987. Associations between soil type, lodgepole pine (Pinus contorta) provenance, and the abundance of the Pine Beauty Moth, Panolis flarnmea. J. Appl. Ecol., 24: 945-951. Majer, J.D. and Recher, H.F., 1988. Invertebrate communities on Western Australian eucalypts: a comparison of branch clipping and chemical knockdown. Austr. J. Ecol., 13: 269278. Mattson, W.J. and Haack, R.A., 1987. The role of drought in outbreak of plant-eating insects. BioScience, 37:110-118. Mispagel, M.E. and Rose, S.D., 1978. Arthropods associated with various age stands of Douglas-fir from foliar, ground, and aerial strata. US/IBP Conif. For. Biome Bull. 13, University of Washington, Seattle, 55 pp. Morse, D.R., Stork, N.E. and Lawton, J.H., 1988. Species number, species abundance and body length relationships of arboreal beetles in Bornean lowland rain forest trees. Ecol. Entomol., 13: 25-37. NiemelL P., Rousi, M. and Saarenmaa, H., 1987. Topographical delimitation of Neodiprion sertifer (Hym., Diprionidae) outbreaks on Scots pine in relation to needle quality. J. Appl. Entomol., 103: 84-92. Noyes, J.S., 1989. A study of five methods of sampling Hymenoptera (Insecta) in a tropical rainforest, with special reference to the Parasitica. J. Nat. Hist., 23: 285-289. Orldci, L., 1978. Multivariate Analysis in Vegetation Research. Junk, The Hague/Boston, 451 PP. Reichle, D.E., Goldstein, R.A., van Hook, Jr., R.I. and Dodson, G.J., 1973. Analysis of insects consumption in a forest canopy. Ecology, 54: 1076-1084. Schowalter, T.D., 1986. Ecological strategies of forest insects: the need for a community-level approach to reforestation. New Forests, 1: 57-66. Schowalter, T.D., 1989. Canopy arthropod community structure and herbivory in old-growth and regenerating forests in western Oregon. Can. J. For. Res., 19:318-322. Schowalter, T.D. and Crossley, Jr., D.A., 1987. Canopy arthropods and their response to forest disturbance. In: W.T. Swank and D.A. Crossley, Jr. (Editors), Forest Hydrology and Ecology at Coweeta. Springer, New York, pp. 207-218. Schowalter, T.D., Stafford, S.G. and Stagle, R.L., 1988. Arboreal arthropod community structure in an early successional coniferous forest ecosystem in western Oregon. Great Basin Nat., 48: 324-327. Simandl, J., 1989. Seasonal changes in the synusia of pine sawflies (Hym., Diprionidae) during their latency. J. Appl. Entomol., 108:217-226. Stork, N.E., 1987. Guild structure of arthropods from Bornean rain forest trees. Ecol. Entomol., 12: 69-80. Strong, D.R., Lawton, J.H. and Southwood, T.R.E., 1984. Insects on plants: community patterns and mechanisms. Harvard University Press, Cambridge, MA, 313 pp.
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Tenow, O. and Larsson, S., 1987. Consumption by needle-eating insects on Scots pine in relation to season and stand age. Holarc. Ecol., 10:249-261. Ter Braak, J.F.C., 1987. CANOCO--a FORTRAN program for canonical community ordination by [ partial ] (detrended) (canonical) correspondence analysis (version 2.1 ). ITI-TNO, Wageningen, 95 pp. Wagner, M.R. and Frantz, D.P., 1990. Influence of induced water stress in ponderosa pine on pine sawflies. Oecologia (Berlin), 83: 452-457. White, T.C.R., 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia (Berlin), 63: 90-105.
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Elsevier Science Publishers B.V., Amsterdam
Canopy arthropods on Scots pine: influence of season and stand age on community structure and the position of sawflies (Diprionidae) in the community Jii-i Simandl Institute of Entomology, CzechAcademy of Sciences, Brani~ovskd 31, 3 70 05 ~eskk Bud~jovice, Czech Republic (Accepted 8 July 1993)
Abstract
The response of arthropods to season and age of stands was studied in the crowns of managed, pure Scots pine stands (Pinus sylvestris L. ) by insecticide fogging. Pine monocultures were characterised by a stable guild composition (defoliators being predominant) rather than by the composition of taxonomic groups (orders) which are subject to seasonality (mainly Hymenoptera, Coleoptera, Lepidoptera, Homoptera). The second variable (age) had more influence on the community composition than the first (season). In total, significant differences related to the age of the pines were found among most of the arthropod taxa, the medium-aged stands showing a higher density of arthropods in the crown strata. The evaluation of abundance of Hymenoptera (sawfly larvae being the majority in samples----eight species present) by canonical correspondence analysis, in relation to the two environmental variables examined, showed their shift towards the spring (June) in the ordination diagram, when the population density of pine sawfly larvae was higher in comparison with the late summer period. The age variable was not significant in diprionid response. Quantitative data on the most numerous arthropods are included.
Introduction
Using different methods, the species composition of arthropods associated with Scots pine (Pinus sylvestris L. ) tree crowns has been studied by several authors in Europe. There are data on species composition and succession or changes in the abundance of species during the growing season, but pine sawfly populations have received little attention. The group is briefly mentioned in some studies (Engel, 1941; Klomp and Teerink, 1973; Borkowski, 1986 ) but these data show a very low abundance and diversity of diprionids. Hrregot's ( 1960 ) study does not include the needle-eating hymenopterans living in pine crowns at all. © 1993 Elsevier Science Publishers B.V. All rights reserved 0378-1127/93/$06.00
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There have been a few attempts to study patterns that could be useful in identifying community responses to environmental conditions (e.g. Lawton, 1984) in coniferous trees because changes in the community structure may support or limit populations of economically important pine insects (Strong et al., 1984; Schowalter, 1986 ). Some detailed data are available on abundance and food (foliage) consumption by insects feeding on pine needles (Larsson and Tenow, 1980). Feeding dynamics in relation to stand age reported by Tenow and Larsson (1987) concern the main selected defoliators (including Diprionidae). The guilds within the community of pine defoliators have not been well studied. In this study we examined: (a) the effect of season and stand age on the structure of functional and taxonomical groups of arthropods; (b) the composition ofarthropods (higher taxa-orders) and quantitative contribution of guilds/orders to canopy arthropod community; (c) the proportion of pine sawfly larvae (non-outbreaking population) within a season/age class in comparison with other coexisting arboreal arthropods. This paper is also based on the results of several years monitoring of nonoutbreaking populations of pine sawflies and coexisting defoliators. Materials and methods
Study sites Field investigations were conducted in managed, pure Scots pine stands in southern Bohemia, Czechoslovakia (elevation 450-500 m) in 1988. Two stand groups (age classes) separated by a pine plantation were chosen (the wood complex of about 20 000 ha is situated in a region of original occurrence of Scots pine). One group of stands was aged up to 50 years (40-50 years; hereafter referred to as medium-aged stands ); the other group of stands was aged over 80 years (80-100 years; referred to as mature stands). Characteristics of the examined groups of stands are included in Table 1. Mean Table 1 Characteristics of the investigated Scots pine stands (Pinus sylvestris L. ) Stand age (years)
DBH l (mm)
Mean tree height
Tree density ( h a - l)
(m) 41 45 83 91 ~Diameter at breast height.
120 120 210 260
12.0 13.0 16.5 22.5
2600 2700 1400 1100
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87
annual temperature is 7.4 ° C , and mean annual precipitation in the region is 639-670 mm.
Methods Insecticide fogging was used for direct examination of the arthropod community. Within each stand site, which was a 100 m 2 unit (n = 32 ) situated on the stand diagonal transect (n = 6), one tree (n = 15 in the mature, n = 17 in the medium-aged stands) was treated. The distance between these randomly sampled sites was 200 m. Dead insects were collected on sheets of paper 1 m 2 in size (n = 11-21, their area depended on the crown projection size) spread under the crown projection of the treated tree. All arthropods were collected for 3 days after the treatment. Samples were taken by canopy fogging with a synthetic pyrethroid insecticide Cymbush 10 EC (ICI, U K ) applied with a Thermofog TF 30 (IGEBA, Germany). Insecticidal treatments were applied on 3-7 June and 18-20 September, early in the morning when weather conditions were suitable (04:30-06:00 h, air flow up to 0.4 m s -1). The treatments were timed for peaks of the seasonal abundance of the pine sawfly complex established in previous years (Simandl, 1989 ).
Guild separation The arthropods included in samples were sorted into higher taxa (orders) in the laboratory and assigned to the following seven guilds according to their relationships to the host plant. Defoliators: a group including needle-eating insects with trophic relations to the foliage or reproductive organs of Scots pine: it is represented by larvae of the orders Hymenoptera (Symphyta), Lepidoptera, and some adult beetles (Coleoptera). Predators: mainly Brachycera, Arachnoidea including Araneae plus Pseudoscorpiones, predacious Heteroptera and Coleoptera-Carabidae living in crown strata. Detritivores (saprophages): represented by the orders Psocoptera and Blattodea, or developing in the litter layer (some Diptera, Coleoptera, etc. ). Sap-suckers: sucking on bark, foliage or shoots, represented for example by Homoptera (Aphidoidea, Cicadoidea) and bugs (Heteroptera: Aradidae). Parasitoids: parasitic Hymenoptera (Ichneumonidae, Braconidae, etc. ) and Diptera (Tachinidae) associated with primary consumers. Xylophages: adults sampled; larvae living in woody and subcortical tissues of pines (mainly Coleoptera-Cerambycidae, Curculionidae, HymenopteraSyricidae ). Others ('tourists'): arthropods with no relation to pine as a host, or without direct relation to primary consumers of pines. This group includes migrating
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insects, such as aquatic species (Ephemeroptera, Plecoptera, Trichoptera) and individuals of other groups accidentally present, e.g. defoliating beetles living on deciduous trees, in the herbaceous stratum, etc.
Statistical methods The influence of environmental variables, i.e. age and season on arthropod (guild/taxa) densities and the significance of differences were evaluated by the analysis of variance (two-way ANOVA) followed by the Student-Newman-Keul test. Theoretically, all the canopy arthropods (guilds/taxa) had the same opportunity of reacting to the same composite gradients of environment, in this case the age of trees and the season. For the division of main macroarthropod taxa and guilds in relation to the age of the trees and season we used two canonical correspondence analyses (CANOCO) (CCA) which escape the assumption of linearity and can detect unimodal relationships between animals and external variables (cf. ter Braak, 1987). Differences among the treatments were evaluated by cluster analysis (Orl6ci, 1978) where dissimilarity measure is the non-standardised Euclidean distance and average linkage is used for hierarchical clustering. For this purpose, the individual trees (n = 32 ) were grouped according to annual period and stand age. Results
Guilds The total abundance distribution of the functional groups (guilds) of arthropods in the samples is shown in Fig. 1. In comparison with the results of Basset ( 1985 ), the prevalence of guilds more closely related to the host plant, i.e. primary consumers (defoliators and xylophages) indicated that the feeding pressure of phytophages was relatively high, which is a general trait of forest monocultures. Consequently, the higher abundance of primary consumers was reflected by the presence of numerous natural enemies (predacious and parasitic arthropods) in samples. The influence of season on the density of most guilds was low, being significant only in three (defoliators, predators and parasitoids ). However, the influence of stand age on numerical contributions of the guilds was distinct; there were significant differences in all the guilds related to the host plant (Table 2). The medium-aged stands exhibited significantly higher population densities of all arthropod guilds, the densities of both main guilds, i.e. defoliators and predators, being especially high ( P < 0.001 ). The main differences within the guild of defoliators were caused by increased population densities of Bupalus piniarius L. (Geometridae) larvae in the medium-aged stands during the second sampling period. The influence of both variables examined by CCA was found not to be signif-
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n
1400
1200
-----7 1000
800
~ 7 600
400
200
Df
Pd
Dt
Se
Ps
Ot
Xy
Guilds Fig. 1. Frequency distribution of arthropod abundances according to guilds in the crown strata of managed Scots pine stands. Hatched area, proportion ofdiprionid larvae; Df, defoliators; Pd, predators; Dr, detritivores; Sc, sap-suckers; Ps, parasitoids; Ot, others ('tourists'); Xy, xylophages.
Table 2 Guild mean ( _+SD) densities (n per 100 m 2) in relation to season and age Guild
All arthropods Defoliators Predators Detritivores Sap-suckers Parasitoids Others Xylophages
Season
P
Spring
Autumn
2600 697(323) 724(361) 462(284) 346(220) 159(138) 79(77) 35(52)
2870 1135(495) 941(486) 562(287) 302(199) 81(75) 73(74) 24(23)
** * NS NS * NS NS
*P< 0.05; **P< 0.01 ; ***P< 0.001 ; NS, non-significant.
Stand age (years) < 50
> 80
2603 1135(418) 1134(325) 631(250) 414(228) 172(139) 93(92) 45(50)
1880 638(364) 476(211) 371(264) 225(127) 66(50) 58(44) 13(15)
P
*** *** ** ** ** NS *
16.6 10.4 38.0 7.6 2.7 0.7 12.3 7.0 0.8 1.6 10.3 2.4
453(230) 287(148) 927(494) 200(176) 81(54) 53(36) 369(263) 164(104) 51(29) 48(46) 230(169) 54(47)
66(13) 37(30) 171(125) 40(24)
312(146) 183(121) 537(313) 368(367) 911(402) 349(181) 219(197) 265(198)
Mean (SD)
Mean (SD)
D%
September
June
Season
0.3 0.7 4.4 0.4
9.0 6.2 15.4 11.7 31.4 10.1 8.7 7.7
D%
NS NS NS -
* NS *** NS ** ** NS NS
P
39(18) 55(47) 262(171) 45(44)
472(203) 267(133) 1022(424) 272(217) 582(573) 243(232) 422(274) 251(120)
< 50 Mean (SD)
Age (years)
69(26) 31(23) 135(88) 65(35)
290(165) 206(154) 428(236) 365(286) 387(343) 148(95) 213(124) 191(165)
> 80 Mean (SD)
1Family, included also in Hymenoptera. 2Class. 31ncluding Trichoptera (n = 17), Ephemeroptera (n = 5 ), Plecoptera (n = 21 ), Dermaptera (n = 9) and Orthoptera (n = 3). *P< 0.05; **P< 0.01 ; ***P< 0.001 ; NS, non-significant; n = 17, 15, 17, 15 for the four sampling events, respectively.
Hymenoptera Diprionidae ~ Coleoptera Diptera Lepidoptera Heteroptera Homoptera Psocoptera Neuroptera and Raphidioptera Blattodea Arachnoidea 2 Others 3
Order
NS * * -
** NS *** NS * *** * NS
P
29/7 91/6 571/70 -
593/220 407/31 1443/140 300/47 1473/27 373/6 482/147 327/76
M/m
Table 3 Average ( _+SD) density (n per 100 m 2 ), dominance (D%), and recorded maxima (M) and minima ( m ) of densities of arthropods sampled in Scots pine crowns as related to season and age of stand
5-,
~D O
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X I)I
X NIl
X P!;
X L I'
o I: 4 × ItY
oCI ~HO XAR
xco
X tll X BI IIY [:[1 lit LP I1[ t10 P~; NR Bt
HYMENOPTERA [:OL[OPTERA OIt'TERA LEPIOOPTI.RA HETEROPTERA IIOBOPT ERA PSOCOPTERA NEIJROPT[RA : ;RAPtlIBIOPIERA Ill ATTODCA
Fig. 2. Results of CCA of the main taxa of arthropods sampled in Scots pine crowns. Centroids of environmental variables: C1, spring (June); C2, late summer (September); C3, less than 50 years of age; C4, more than 80 years of age; x, order locations. icant for changes in the distribution of arboreal guilds (P = 0.14, Monte Carlo permutation test) and there was no defined, distinct assemblage of guild members in pine crowns. The composition of guilds was more stable than that of taxonomic groups.
Taxa (orders) In total, 3622 arthropod specimens of 15 insect orders and the class Arachnoidea fell from the crown strata at canopy fogging (for survey see Table 3 ). Significant quantitative changes in the density of arthropods with season were found in four orders whose members are more (Coleoptera, Lepidoptera and Heteroptera) or less (Hymenoptera, mainly Diprionidae sampled) subject
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ED
10
Im
I v
~
.
.
.
.
v
Fig. 3. Dendrogram of the cluster analysis of arthropod samples. Dissimilarity measure, nonstandardised Euclidean distance (ED). 1, Spring sampling period; 2, late summer sampling period; MEa, medium-agedstand; MTR, mature stand (age of stand in parentheses). to seasonality (Table 3 ). The first sampling period was dominated by Coleoptera and among them the herbivorous pine blossom weevil Anthonomus pubescens Payk. (Curculionidae) (up to 710 individuals per 100 m 2 in medium-aged stand) along with the predacious Halyzia 28-guttata L. (Coccinelidae) were the most numerous. However, the abundance of Lepidoptera and predaceous Heteroptera peaked during the second sampling period owing to increasing B. piniarius and Miridae populations. Greater differences were found between age classes. Seven arthropod orders exhibited significant preferences for the medium-aged stand habitat (Table 3 ) where the densities of some species (as mentioned above) were high. The results of correspondence analysis (Fig. 2 ) of the whole set of the most abundant arthropod orders show that most of them were allocated into two opposite groups along the first axis which corresponds to higher variation in the seasonal structure. The stand age mainly contributed to ordination along the second axis. The influence of both variables examined by CCA was signif-
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icant ( P < 0.05 ) for taxonomic composition and as a result most of the orders were characterised by preference for medium-aged stands in the original pine ecosystems. The diagram also shows that the age variable contributed more to the community composition than the seasons. A comparison of treatment similarities (Fig. 3 ) shows three groups of samples separated according to the sampling period and stand age. The primary bifurcation among the sample clusters is between the seasons ( 1 vs. 2, see Fig. 3 ) followed by division according to the level of age variable.
The position of pine sawflies Diprionidae were represented by eight species in the samples. Their quantitative position (dominance) within the arthropod canopy community as related to season is shown in Fig. 4. Their bivoltinism (except for Neodiprion sertifer Geoff. ) was an assumption for their more abundant occurrence during the seasons, with larval density higher during the first (spring) wave 3 UNE
SEPTEMBER
YEAR
COLEOPTERA
~NEUROPTERA+ +RAPHIDIOPIERA BLATTODEA
DIPTERA
~HOMBPTERA
IIYMENOP]ERA ~
L.EPIDOPTERA
PSOCOPTERA
HEIEROPIERA
ARACHNDIDEA
DPR DIPRIONIDAE
~ ] ~ OIHERS
Fig. 4. Seasonal position (dominance) of diprionid larvae as related to coexisting groups of arthropods (taxa) in Scots pine crowns.
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(presence of N. sertifer larvae). Several characteristic pine feeders contributed to the bimodal abundance pattern within the seasons, i.e. sawfly larvae along with herbivorous beetles (Anthonomus spp. and others) and Panolis flammea (D&S) larvae contributed to an increase in defoliator abundances during the first (spring) sampling period, unlike the second sampling period when another peak of defoliators included mainly B. piniarius larvae plus the second wave of diprionids. These herbivores were characteristic of the situation in pure pine forests when defoliators were the most stable and constant guild during the season. The annual population of sawfly larvae averaged onetwelfth (238.5 +_ 144.3 individuals per 100 m 2 ) of all arthropods in the crown strata (see Fig. 1 ). Differences in sawfly densities as related both to seasonal period and age were not significant (Table 3 ), the group being constant and having a relatively stable position (peaking at least twice during the season) in the pine canopy community. Discussion
Guilds A comparison of the results of this study with those existing for guilds in coniferous (Douglas fir) (cf. Schowalter et al., 1988 ) as well as North American deciduous (Schowalter and Crossley, 1987) forests indicated a functional similarity of arthropod guilds of the examined forest types, comparable data not being available for European coniferous forests. Basset ( 1985 ) found at most 6.0% of defoliators among arthropods on Pinus mugo Turra, and our results indicate that Scots pine monocultures support higher densities of primary consumers. The first successional stages of young coniferous forests are usually characterised by the dominance of sap-suckers (Mispagel and Rose, 1978; Schowalter et al., 1988) along with their higher biomass (Schowalter, 1989 ). In contrast, the old-growth conifer canopies (more than 400 years old) were dominated by defoliators with a lower herbivore biomass (Reichle et al., 1973; Schowalter et al., 1988). Relatively high consumption rate caused by defoliators in a mature Scots pine stand was demonstrated in the 1 year study of Larsson and Tenow (1980). The observed responses of the most important pine species (mainly of the defoliators guild) to the environmental variables examined seemed to be best explained by the age of stands; the denser stands supporting mainly higher densities of primary consumers and their enemies. Variation in the population density of some species each year are also reflected adequately at guild level (defoliators and predators).
Taxonomic composition and reliability of the method The direct, quantitative sampling method of insecticide fogging reveals a larger part of canopy-inhabiting free-living insects (see Noyes, 1989; Morse
J. Simandl / Forest Ecology and Management 62 (1993) 85- 98
95
et al., 1988 ), but its disadvantage is that it may underestimate some groups, e.g. sedentary arthropods, leaf and bud miners, fast flying insects, etc. (Majer and Recher, 1988 ). Among the fallen macroarthropods we also found larvae of Acantholyda nernoralis Thomson (Tenthredinidae) living solitarily in silk tents. Beetles are reliably sampled by this method (Stork, 1987), and probably also all free-living larvae of pine sawflies. However, winged and highly mobile adults of some insects react quickly to insecticide application and may escape from the treated tree space. To prevent most of these mobile insects from escaping, treatments were performed early in the morning when the air was cooler and the mobile insects were unable to react quickly. Even so, some adult moths and dipterans may have been underestimated in the samples. Some accidentally represented groups of aquatic insects classified as 'tourists' in pine crowns occurred there because of relatively short distances from water sources (ponds/streams). According to a preliminary estimate, it seems that the arthropod species composition and richness (except for Diprionidae) was similar (more than 100 species present) to data reported from other European pine regions (see Klomp and Teerink, 1973; Borkowski, 1986). Both qualitative and quantitative differences may have been due to the different methods used and geographic regions sampled. Although the arthropod densities were similar during both seasons, the spring seems to exhibit a greater suitability of environmental conditions resulting in a higher species diversity. Nevertheless, parallel investigations (frass-drop measurements, insect trapping) suggest that needle-eating insect species (larval stage) were usually dominant in the examined plots (unpublished data), especially in medium-aged managed monocultures.
Position of pine sawflies and other defoliators A long latency of insects depends on many factors (e.g. Hanski, 1987). During this phase, non-outbreaking sawfly populations fluctuate within certain limits among years (Simandl, 1989), but density amplitudes are usually relatively lower in comparison with outbreaking populations. The estimated density of sawflies in stands over 40 years old varied at endemic level from 2000 (seasonal minimum, Simandl, 1989 ) to 30 000 larvae ha-1 in a mature stand (seasonal maxima, central Sweden, Larsson and Tenow, 1980). Some maximal local densities of sawfly larvae in the investigated region were over 40 000 ha -1 (unpublished data); because there were eight species present, their feeding lasted 5.5-6 months in this geographical zone (Simandl, 1989 ). During the monitoring of pine defoliators the density of B. piniarius regularly increased in autumn each year (unpublished data). Our results suggested bimodal seasonal pattern of abundances of main defoliators in pine monocultures (Larsson and Tenow, 1980): the first peak
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(June) was dominated by herbivorous Coleoptera+ first wave of diprionids +Panolisflammea, the second one (September) by B. piniarius+ second wave of diprionids + Geometridae in samples. Of the two seasonal peaks of insect defoliators, the second is more important because the loss of needles caused by their feeding pressure is the highest in late summer when the food consumption of B. piniarius and the complex of diprionid species culminates (Larsson and Tenow, 1980; Tenow and Larsson, 1987) along with the consumption of other defoliating insects. Presumably, the loss of foliage caused by the defoliator complex can affect, negatively, the growth of the trees, more during late season (Ericsson et al., 1980). The probability of development of outbreak foci is apparently higher in medium-aged stands owing to better trophic conditions (greater volume of foliage) with a greater abundance of pine defoliators to whose activity these stands are naturally susceptible. However, increased species diversity of arthropods, orders of which were distributed more frequently between centroids C 1 and C3 (Fig. 2, spring, mediumaged stands), may contribute to the ecosystem stability. Nevertheless, the repetition of peaking of typical pine insects (mainly defoliators) each year was distinct during both previous and subsequent investigations (unpublished data). These swings of the population densities support the opinion that pine monocultures are vulnerable to attack of insects at any other (abiotic) disturbance of their balance, e.g. poor soil conditions (White, 1984; Leather and Barbour, 1987; Mattson and Haack, 1987; Niemel~i et al., 1987 ) in connection with water stress (Wagner and Frantz, 1990) can create optimal trophic conditions for population growth of needle-eating insects.
Acknowledgements The author is indebted to anonymous referees for their helpful critical comments on the former version of this paper, and to Dr. J. Lep~ (Centre of Biomathematical Methods, Czech Academy of Sciences) for his kind assistance in the processing of statistics.
References Basset, Y., 1985. Aspectsde la r6partition des peuplementsd'arthropodes dans les coronnes de Pinus mugo Turra. Mitt. Schweiz.Entomol. Gessel., 58: 263-274. Borkowski, K., 1986. Contribution to the knowledgeof the insect fauna of the crown of Scots pine trees. Pol. Pismo Entomol., 56:667-676 (Englishsummary). Engel,H., 1941. Beitr~igezur Faunistikder Kiefernkronenin verschiedenenBestandstypen.Mitt. Forstw. Forstwis., 12:334-361. Ericsson, A., Larsson, S. and Tenow, O., 1980. Effects of early and late season defoliation on growth and carbohydratedynamics in Scotspine. J. Appl. Ecol., 17: 747-769. Hanski, I., 1987. Pine sawfly population dynamics: patterns, processes, problems. Oikos, 50: 327-335.
J. Simand! / Forest Ecology and Management 62 (1993) 85-98
97
H6regot, H., 1960. Untersuchungen iiber die qualitative und quantitative zusammensetsung der Arthropodenfauna in den Kiefernkronen. Beitr. Entomol., 10:891-916. Klomp, H. and Teerink, B.J., 1973. The density of the invertebrate summer fauna on the crowns of pine trees, Pinus sylvestris, in the central part of the Netherlands. Beitr. Entomol., 23: 325-340. Larsson, S. and Tenow, O., 1980. Needle-eating insects and grazing dynamics in a mature Scots pine forest in Central Sweden. In: T. Persson (Editor), Structure and Function of Northern Coniferous Forests--An Ecosystem Study. Ecol. Bull. (Stockholm), 32: 269-306. Lawton, J.N., 1984. Herbivore community organization: general models and specific tests with phytophagous insects. In: P.W. Price, C.N. Slobodchikoffand W.S. Gaud (Editors), A New Ecology. Wiley, New York, pp. 329-352. Leather, S.R. and Barbour, D.A., 1987. Associations between soil type, lodgepole pine (Pinus contorta) provenance, and the abundance of the Pine Beauty Moth, Panolis flarnmea. J. Appl. Ecol., 24: 945-951. Majer, J.D. and Recher, H.F., 1988. Invertebrate communities on Western Australian eucalypts: a comparison of branch clipping and chemical knockdown. Austr. J. Ecol., 13: 269278. Mattson, W.J. and Haack, R.A., 1987. The role of drought in outbreak of plant-eating insects. BioScience, 37:110-118. Mispagel, M.E. and Rose, S.D., 1978. Arthropods associated with various age stands of Douglas-fir from foliar, ground, and aerial strata. US/IBP Conif. For. Biome Bull. 13, University of Washington, Seattle, 55 pp. Morse, D.R., Stork, N.E. and Lawton, J.H., 1988. Species number, species abundance and body length relationships of arboreal beetles in Bornean lowland rain forest trees. Ecol. Entomol., 13: 25-37. NiemelL P., Rousi, M. and Saarenmaa, H., 1987. Topographical delimitation of Neodiprion sertifer (Hym., Diprionidae) outbreaks on Scots pine in relation to needle quality. J. Appl. Entomol., 103: 84-92. Noyes, J.S., 1989. A study of five methods of sampling Hymenoptera (Insecta) in a tropical rainforest, with special reference to the Parasitica. J. Nat. Hist., 23: 285-289. Orldci, L., 1978. Multivariate Analysis in Vegetation Research. Junk, The Hague/Boston, 451 PP. Reichle, D.E., Goldstein, R.A., van Hook, Jr., R.I. and Dodson, G.J., 1973. Analysis of insects consumption in a forest canopy. Ecology, 54: 1076-1084. Schowalter, T.D., 1986. Ecological strategies of forest insects: the need for a community-level approach to reforestation. New Forests, 1: 57-66. Schowalter, T.D., 1989. Canopy arthropod community structure and herbivory in old-growth and regenerating forests in western Oregon. Can. J. For. Res., 19:318-322. Schowalter, T.D. and Crossley, Jr., D.A., 1987. Canopy arthropods and their response to forest disturbance. In: W.T. Swank and D.A. Crossley, Jr. (Editors), Forest Hydrology and Ecology at Coweeta. Springer, New York, pp. 207-218. Schowalter, T.D., Stafford, S.G. and Stagle, R.L., 1988. Arboreal arthropod community structure in an early successional coniferous forest ecosystem in western Oregon. Great Basin Nat., 48: 324-327. Simandl, J., 1989. Seasonal changes in the synusia of pine sawflies (Hym., Diprionidae) during their latency. J. Appl. Entomol., 108:217-226. Stork, N.E., 1987. Guild structure of arthropods from Bornean rain forest trees. Ecol. Entomol., 12: 69-80. Strong, D.R., Lawton, J.H. and Southwood, T.R.E., 1984. Insects on plants: community patterns and mechanisms. Harvard University Press, Cambridge, MA, 313 pp.
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Tenow, O. and Larsson, S., 1987. Consumption by needle-eating insects on Scots pine in relation to season and stand age. Holarc. Ecol., 10:249-261. Ter Braak, J.F.C., 1987. CANOCO--a FORTRAN program for canonical community ordination by [ partial ] (detrended) (canonical) correspondence analysis (version 2.1 ). ITI-TNO, Wageningen, 95 pp. Wagner, M.R. and Frantz, D.P., 1990. Influence of induced water stress in ponderosa pine on pine sawflies. Oecologia (Berlin), 83: 452-457. White, T.C.R., 1984. The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia (Berlin), 63: 90-105.