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New Forest 4: 13-25, 1900. 0 1990 Kluwer Academic Publishers. Printed in the Netherlunds. Abundance and control of Lygzts rugulipennis (Heteroptera: Miridae) on Scats pine (Pinus sylvestrisL.) nursery stock JARMO K. HOLOPAINEN’ and RISTO RIKALA* ‘Ecological Laboratory Department of Environmental Sciences, University of Kuopio, P.O. Box 6, SF-7021 1, Kuopio, Finland; ?Finnish Forest Research Institute, Suonenjoki Research Station, SF- 77600 Suonenioki, Finland Received 29 April 1989; accepted 17 January 1990 Key words: pint seedlings, bud abnormality, insects, cypermethrin Application. A positive relationship was observed between the peak numbers of ovcr- wintered European tarnished plant bug, Lygus rugulipennis Popp. adults and nymphs and the occurrence of bud abnormalities in 2- and 3-year-old Scats pine nursery seedlings in central Finland. The numbers of bugs and damaged seedlings were reduced with insecticide sprayings. However, the correct timing of insecticide application is important for significant reduction of bud abnormalities. Abstract. Population fluctuations of the European tarnished plant bug (Lygus rugulipennis Popp.) on nursery-grown Scats pine, Pinus sylvestris L. were monitored with sweep net samples over five growing seasons. The effects of cypermethrin, lindane and oxydemeton- methyl insecticide sprayings on the occurrence of Lygus adults and nymphs and prevalence of bud disorders of pine seedlings were studied. The number of Lygus bugs was highest in 1984, the first year of the study, and thereafter the annual levels of the bug declined, reaching a low in 1988. On 2- and 3-year-old Scats pine seedlings the numbers of over- wintered L. rugufipennis adults and nymphs correlated positively with the occurrence of abnormal buds. Cypermethrin sprayings significantly reduced the numbers of Lygus nymphs in 1985 and 1987. In 1986 significantly fewer damaged seedlings and L. rugulipennis adults were found in pine transplants treated with cypermethrin. Introduction Lygus bugs are common pests of many agricultural crops in Europe (Beth 1966; Varis 1972; Bournoville et al. 1984) and North America (Strong 1970; Fye 1984), including nursery-grown deciduous trees (Haseman 19 18; Koehler 1963; Wilson and Moore 1985). Recently Lygus bugs have also been shown to injure the apical shoots of nursery grown conifers (Shrimpton 1985; Holopainen 1986; Schowalter et al. 1986; South 1986; Poteri et al. 1987; Schowalter and Stein 1987).

Abundance and control of Lygus rugulipennis (Heteroptera: Miridae) on Scots pine (Pinus sylvestris L.) nursery stock

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New Forest 4: 13-25, 1900. 0 1990 Kluwer Academic Publishers. Printed in the Netherlunds.

Abundance and control of Lygzts rugulipennis (Heteroptera: Miridae) on Scats pine (Pinus sylvestris L.) nursery stock

JARMO K. HOLOPAINEN’ and RISTO RIKALA* ‘Ecological Laboratory Department of Environmental Sciences, University of Kuopio, P.O. Box 6, SF-7021 1, Kuopio, Finland; ?Finnish Forest Research Institute, Suonenjoki Research Station, SF- 77600 Suonenioki, Finland

Received 29 April 1989; accepted 17 January 1990

Key words: pint seedlings, bud abnormality, insects, cypermethrin

Application. A positive relationship was observed between the peak numbers of ovcr- wintered European tarnished plant bug, Lygus rugulipennis Popp. adults and nymphs and the occurrence of bud abnormalities in 2- and 3-year-old Scats pine nursery seedlings in central Finland. The numbers of bugs and damaged seedlings were reduced with insecticide sprayings. However, the correct timing of insecticide application is important for significant reduction of bud abnormalities.

Abstract. Population fluctuations of the European tarnished plant bug (Lygus rugulipennis Popp.) on nursery-grown Scats pine, Pinus sylvestris L. were monitored with sweep net samples over five growing seasons. The effects of cypermethrin, lindane and oxydemeton- methyl insecticide sprayings on the occurrence of Lygus adults and nymphs and prevalence of bud disorders of pine seedlings were studied. The number of Lygus bugs was highest in 1984, the first year of the study, and thereafter the annual levels of the bug declined, reaching a low in 1988. On 2- and 3-year-old Scats pine seedlings the numbers of over- wintered L. rugufipennis adults and nymphs correlated positively with the occurrence of abnormal buds. Cypermethrin sprayings significantly reduced the numbers of Lygus nymphs in 1985 and 1987. In 1986 significantly fewer damaged seedlings and L. rugulipennis adults were found in pine transplants treated with cypermethrin.

Introduction

Lygus bugs are common pests of many agricultural crops in Europe (Beth 1966; Varis 1972; Bournoville et al. 1984) and North America (Strong 1970; Fye 1984), including nursery-grown deciduous trees (Haseman 19 18; Koehler 1963; Wilson and Moore 1985). Recently Lygus bugs have also been shown to injure the apical shoots of nursery grown conifers (Shrimpton 1985; Holopainen 1986; Schowalter et al. 1986; South 1986; Poteri et al. 1987; Schowalter and Stein 1987).

14

Very severe growth distortion in young Scats pine (Pinus sylvestris L.) seedlings have been recorded in many Finnish forest nurseries (Raitio 1983; 1985), and regulations from the Ministry of Agriculture and Forestry forbid the sale of pine seedlings with multiple leaders or abnormal apical buds. On young (cotyledon stage) Scats pine Lygus feeding causes wither- ing of the growing shoot tip and new primary needles, followed by the development of multiple leaders (Holopainen 1986; Poteri et al. 1987) In older seedlings damage occurs mostly on the apical buds which either die or form a group of buds (Poteri et al. 1987) resulting in seedlings with multiple leaders in the summer following seeding.

In this paper annual (1984-1988) and seasonal fluctuations in num- bers of the European tarnished plant bug (Lygus rugulipennis Popp.) on Scats pine seedlings in a Finnish forest nursery are described. A second objective was to evaluate the effects of insecticide sprayings on Lygus abundance and occurrence of apical bud disorders.

Materials and methods

Site description

The study was carried out in a forest nursery at Suonenjoki, central Finland (62”38’ N, 27” 04’ E, 142 m above sea level). The nursery contains 12 ha of fields and 0.7 ha of greenhouses. It is surrounded by a dry pine forest of Culluna and Vuccinium forest site types (Cajander 1949). Understory vegetation consists mostly of Culluna vulguris L., Vaccinium vitis-idae L., I/. myrtillus L. and Empetrum rzigrum L. The nearest agricultural field, growing strawberries, is about 1000 m from the nursery.

The nursery soil was a mixture of native fine sand with added Sphagnum peat. Organic soil content varied between 4-7%. Total amount of added nitrogen applied as NPK + micronutrient fertilizer varied between 5-10 g m-l year- ‘. Fields were irrigated daily during the first 2-3 weeks after sowing, 3-4 days after transplanting and thereafter according to need.

Weeds in the nursery fields were controlled with the herbicides hexazinon and atrazin but occasionally weeds occurred at the ends of seedbeds, in the field boundaries and in fallow fields. The most abundant weed species Poa annua L. and Senecio vulgaris L. were present in areas not treated with the herbicides. Other weeds that grew in the fields were Equisetum arvense L., Capsella bursa-pastoris (L.) Medicus, Elymys repens (L.) Gould., Gnaphalium uliginosum L., Chamerion angustifolium

15

(L.) J. Holub, Cirsium arvense (L.) Stop., Rumex acetosellu L. and Sonchus arvensis L.

Fungicides (maneb, chlorothalonil) for control of pine needle cast (Lophodermium sp.) and pine dieback (Ascocalyx ubietinu (Lagerb.)), were normally applied as a spray at 2-week intervals beginning in June and were continued until October. Quintozene (PCNB) was sprayed for control of snow blight (I’hucidium infestuns Karst.) in the autumn before the arrival of permanent snow cover.

Insecticide treatments

Over the 1984-87 period experiments with different insecticides were conducted on the growing seedlings. Both the occurrence of Lygus bugs and growth abnormalities of the pine seedlings were monitored. The Scats pine seedlings used in the experiments and the insecticides applied are given in Table 1.

In 1984, the objective was to detect possible insect pests which were causing damage to the seedlings, especially to young first-year pine seedl- ings in the nursery beds. Insecticide (oxydemeton-methyl, lindane) and control treatments were arranged in three separate areas of the seedbeds. The same insecticide-treated areas were sprayed with cypermethrin during the second growing season in 1985. Between 1985-87, cypermethrin was also applied to the transplant beds. Similar adjacent beds were elected as treated and control areas. The transplant bed contained five seedling rows with 22 cm between rows and 5 cm between seedlings in the rows. Normally both treated and control areas consisted of 5 to 10 beds, each 100 to 200 m long. For practical reasons the insecticide treatments in seedbeds and transplant beds could not be replicated.

Insect monitoring

Lygcls bug occurrence on seedlings was monitored by sweepnet sampling. Each sample consisted of 30 sweeps. Four replicate samples were col- lected from both insecticide-treated and control areas at each sampling over the whole growing season. However, from l+O pine the first sweepnet samples were collected after mid-July in 1984 because the seedlings were small. Following the 1984 growing season no monitoring of insects was done in l+O pine seedbeds as the use of propylene fiber gauze had effectively reduced Lygus bug damage (Poteri et al. 1987).

Collected bugs were kept in transparent plastic cylinders for determin- ing their species and sex. Nymphs were identified only to genus. In 1984

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and 1985 the samples were taken at 7 days intervals and the collected bugs were used in laboratory experiments. In 1986-1988, samples were collected at 3-5 day intervals during the peak period of bug occurrence. After identification insects were released at their original collection sites to minimize the effect of reduction in numbers of bugs caused by sampl- ing.

Flying insects were also monitored in the seedbeds in 1984 using yellow water-traps (Pioneer Container Ltd, Feltham, England, no. 40 A, diam. 17 cm) from June 12 to September 11. Traps were filled with water (about a third of the total volume) containing a few drops of detergent. The insects were removed every 2 to 3 days.

Damage phenology

Growth abnormalities on seedlings shoots and buds were recorded at the end of each growing season. In 1984 and 1985 multiple-leadered and stunted (Raitio 1983, 1985; Poteri et al. 1987) l+O and 2+0 seedlings were counted from 18 systematically located, 500 cm2 sample plots, in four 12 m X 6.5 m replicate plots, in each treatment.

In 1984 affected 2+1 transplants with many bud disorders and some multiple-leaders, were counted in systematically sampled plots covering 2.5% of the transplant area. From 1985-1988 very few multiple-leadered seedlings occurred in the transplant beds because the affected l+O or 2+0 stock was culled before transplanting. Various kinds of bud dis- orders, however, appeared in seedlings after transplanting. In the most severely affected seedlings the apical bud comprised clusters of small buds, or the bud was killed resulting in fascicles of buds. Sometimes no dominant apical bud was evident as all the buds were about the same size. Needles below apical buds were often deformed, thick and sickle-shaped. In 1985, abnormal buds were recorded for 60, 2+1 seedlings in six systematically-located, 5 ml plots. In 1986 (l+l, 2+1) and 1987 (2+0) seedlings bud disorders were monitored in systematically sampled plots which contained 2.5% of the seedlings in the control and treated areas.

Analysis of data

The results of 1984 seedling counts in seedbeds were analysed using one-way analysis of variance (SPSS/PC+ system, SPSS Inc., Chicago, Illinois). The data were arcsin transformed prior to analysis. Means were tested with Duncan’s Multiple Range Test (Duncan 1955). All Lygus counts and 1985 seedling counts in seedbeds and seedling counts in transplant beds were analysed by t-tests. Regression analyses were con-

18

ducted to estimate relationships between numbers of bugs and proportion of damaged seedlings.

Results

Abundance of Lygus bugs

Lygus rugulipennis was the dominant Lygus species in the nursery. In 1984 12% of the Lygus adults were L. punctatus (Zett.) but later this species accounted for up to 1% of the total populations.

May, 1984, was exceptionally warm and early migration of Lygus bugs from the forest into the nursery occurred. The first bugs were recorded on transplants on 15 May (Fig. 1). The peak occurrence of overwintered adults was attained by the end of May and the first nymphs appeared on 12 June. The greatest numbers of Lygus nymphs were collected in the sweepnet samples of 10 July when 45 nymphs were found per sample. The first teneral adults were also found on that date.

In pine seedbeds, sown on 7 June in 1984, germinants emerged in mid-June when overwintered Lygus adults were no longer detected. No Lygus adults and nymphs were seen on l+O seedlings in sweepnet samples during July and August and only 12 individuals were caught in the yellow traps during the early June - late August monitoring period.

May and early June 1985 were cold, thus peak numbers of overwin- tered adults occurred about 3 weeks later than in 1984. Cypermethrin spraying of 2+0 seedbed seedlings and 2+1 transplants kept the numbers of Lygus nymphs at a significantly lower level than in control plots in July (Fig. 1).

In 1986 Lygus numbers were very low, but in l+l transplant stock significantly fewer overwintered adult bugs were observed after the first cypermethrin spray. Although numbers of Lygus nymphs did not differ significantly, they caused less damage in the insecticide-treated plots (Fig. 4). Numbers of Lygus adults and nymphs on 2+1 transplants were very low and no differences were found between the treatments (Fig. 2).

In 1987, seasonal fluctuations in numbers of L. rugulipennis were very similar to 1986. The first overwintered adults were detected in the nursery at the beginning of June and the mean number of adults per sample did not exceed four individuals (Fig. 2). Cypermethrin was applied after significantly more of Lygus nymphs were observed in the control plots than in the planned spraying plots. After insecticide treatment no Lygus nymphs were detected.

The number of overwintered L. rugulipennis adults was extremely low

19

45 9 45 :

40 - l wwp 0

- adults 35- ~-- nymphs

25

J ‘4 Ol, 1 I I I I x -0

15 1 15 1 15 1 15 1 May June July August

Fig. 1. Numbers of Lygus rugulipennis adults and Lygus nymphs on Scats pint seedlings in unsprayed and cypermethrin sprayed plots in 1984 and 1985. The arrows indicate the date of spraying. Significant differences between treatments arc indicated with asterisks (* = p < 0.05, +* = p < 0.01, *** = p < 0.001). Numbers arc means of four samples (30 sweeps per sample).

in 1988. Only one adult was found on 2+1 pine stock at the end of May so no insecticides were applied. Peak numbers of Lygus nymphs preceded the peak in populations of teneral adults in mid-July (Fig. 2). Compared to other study years, numbers of tenerals were remarkably large.

Seedling condition

In 1984, incidence of bud abnormalities of l+O pine seedlings was low and not significantly reduced by insecticide treatments (Table 2). Figure 3 shows the proportion of 2- and 3-year-old seedlings with abnormal buds in 1984-1988. In 1984, when the bugs were not controlled and the bug population was large in the transplant field, the bud damage was highest.

20

15 15

10 10

5 5

2

f 10 0 0 10 In

t 0 0

p’ 15 15

B 10 10

z “E 5 5

2 0 0

10 10

5 5

0 0 15 1 15 1 15 i 15 1

May June July August

Fig. 2. Numbers of Lygus rugulipennis adults and Lygus nymphs on Scats pint seedlings in unsprayed and cypermcthrin sprayed plots in 1984 and 1985. The arrows indicate the date of spraying. Significant differences between treatments are indicated with an asterisk (p < 0.05). Numbers are means of four samples (30 sweeps per sample).

In 1985 five cypermethrin sprayings did not significantly affect the number of 2+0 or 2+1 seedlings with bud disorders, although 8% fewer seedlings were damaged in the cypermethrin-treated 2+1 transplants. Two sprayings with cypermethrin significantly reduced numbers of seedlings with deformed buds in 1986. In 2+1 stock 46% fewer seedlings were damaged and in l+ 1 stock a 41% reduction in the proportion of damaged

Table 2. Mean numbers of 1+0 Scats pine with multiple leaders from insecticide-treated and untreated seedbeds in 1984.

Treatment Seedlings per m? Seedlings with multiple leaders %

Control 862 Oxydcmeton-methyl 998 Lindanc 690

3.10a 3.94 a 3.55 a

Values within column are means of 72 observations; means followed by the same letter are not significantly different (p < 0.05).

21

0 Control

q Cypermethrin

treated

2+1 1984 2+1 1985 2+0 1985 l+l 1986 2+1 1986 2+0 1987 2+1 1988

Seedling type and year

Fig. 3. Pcrccntagcs of cypermethrin-treated and untreated Scats pine seedlings with bud deformations in studied plots. The vertical bar is the SD. * and *+* over the bars indicate that adjacent means arc significantly different at the p = 0.05 and 0.001 levels, respectively.

seedlings after cypermethrin treatments was observed. One spraying in 1987 did not reduce insect damage.

A positive and significant (p = 0.003) relationship was found between the peak numbers of Lygus nymphs and the proportion of pine seedlings with bud disorders (Fig. 4). For the analysis, only data from untreated plots were used. The peak numbers of overwintered L. rugulipennis adults were also significantly (p = 0.022) related to seedlings suffering bud damage in the plots.

Discussion

The abundance of L. rugdipennis on Scats pine seedlings varied greatly over the study period. In 1984 the insects were exceptionally abundant and affected agricultural crops in Finland, e.g., sugarbeet (Markkula 1985). During the same year both the numbers of L. rugulipennis in the pine nursery and seedling damage were considerable higher than in following years. However, the proportion of multiple-leadered l+O pine seedlings in the seedbeds decreased in comparison to the previous year (1983) when 42% of pine seedlings growing in seedbeds suffered growth disturbances (Raitio 1985). This might be due to the early migration of the

22

50 H - Nymphs y=O.41x+6.04, r2=0.848, n=7

y=O.O6x+1.93, r2=0.676, n=7 '

Cl ______------- ____---- -n ____-----

0 10 20 30 40 50 60 70 80 90

Damaged seedlings %

Fig. 4. Relationship between the peak numbers of Lygus rugulipennis adults in early summer and peak numbers of Lygus nymphs in July and the percentage of seedlings with bud disorders in untreated pint plots (n = 7).

bugs in 1984 which meant that populations had declined before the seedlings emerged.

Numbers of adult bugs were higher in June than in August. The low numbers of teneral adults on Scats pine is partly explained by the rapid migration to weeds after emergence (Holopainen 1989a).

Our study did not provide any information on the efficiency of lindane and oxydemeton-methyl against Lygus bugs on pine seedlings as no bugs occurred on l+O pine in 1984. In the laboratory oxydemeton-methyl killed more Lygus nymphs and adults on pine seedlings than cypermeth- rin. Nevertheless, Lygus damage was greater on oxydemeton-methyl treated than on cypermethrin-treated seedlings (Holopainen 1989b).

Doses of 50-200 g a.i./ha cypermethrin did not sufficiently control Lygus bugs in alfalfa fields (Isenhour 1985) and seven sprayings (15 g active ingredient/ha) were needed against L. lineolaris on Coronilla varia (Martel and others 1986). In the present study significantly fewer Lygus bugs were found after a single spray using 50 g a.i./ha. The rather good efficiency of cypermethrin against Lygus bugs may be due to the relatively

23

low temperatures in central Finland in June (average temperature in June is 14 “C in Kuopio, Anon. 1988). Pyrethroids are more toxic at low than at high temperatures (Plapp 198 1).

The number of bugs clearly decreased following cypermethrin spray- ings and the proportion of bud abnormalities was generally lower on sprayed than on control seedlings. However, a significant decrease in numbers of deformed buds was only recorded in 1986. In 1985 slight damage to 2+0 seedlings in control plots was perhaps due to the higher seedling density as compared to the 2+1 transplant stock where 40% of the seedlings were damaged since the numbers of bugs per seedling would be much higher on these transplants. Also in 1985, the decrease of Lygus nymphs was highly significant in sprayed plots of 2+1 transplants, but no clear decrease in abundance of adult bugs was seen. Only a slight decrease in the numbers of deformed buds were recorded in the insecticide treated plots. The significant reduction of bud abnormalities on cypermethrin- treated l+l seedlings in 1986 suggest that feeding injury by overwintered adults is more detrimental to buds than feeding by nymphs.

The migration of Lygus bugs starts during the first warm and sunny days in late May or early June but the sweepnet sampling in our study was at periods of 3 to 7 days. It is possible that 1 to 2 day periods of bug activity on sunny days in early summer were not recorded. This may explain why no differences in bug activity were observed between treat- ments on 2-l-l pine in 1986, although seedling damage was significantly reduced in the cypermethrin treated plots.

Deformation was classified according to appearance, but all types of deformation could not be related to bug feeding and some were perhaps caused by other factors. For example, pine bud disorders can be caused by frost at the time of shoot elongation (Rikala and Repo 1987; Raitio 1987). In 1984, when highest incidence of bud disorder also occurred, temperatures fell to as low as -6.8 “C in mid-June. However, in 1985 bud disorder in pine transplants was still relatively common, although frost did not occur in June. Bud abnormalities have been observed to increase also with intense nitrogen fertilization of seedlings (Rikala unpubl.) which may cause disturbances in apical dominance (Will 1971). Nitrogen fertilization also increases the numbers of sucking insects (Heliovaara et al. 1983; Strauss 1987) and may have interaction with insect injuries.

Although bugs have been shown to induce growth disturbances on l+O pine seedlings (Holopainen 1986; Poteri et al. 1987) more research is needed to establish their role in bud disorders of transplanted Scats pine. Nevertheless, our results suggest the importance of Lygus control in years when these bugs occur in high numbers.

24

Acknowledgments

This study was supported by the Academy of Finland, the Foundation for Research of Natural Resources in Finland, and the Finnish Forest Research Institute. We thank Professor Anna-Liisa Varis, Dr. Heikki Hokkanen, Mr. Hannu Raitio (Lit. Phil.) and Mr. Hannu Kukkonen (M.Sc. For.) for comments on the manuscript. We are grateful to Mr. Robin Sen who corrected the English, and to Ritva Pitkanen, Anja Aaltonen, Eila Kainulainen, Tarja Kananen, Ilkka Rasanen, Jari Spoof, Juha Kaitera, Heikki Ronkko and the staff of Suonenjoki nursery for technical assistance.

References

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Nachr. blatt. Deuts. Pflschutzd. 20: 178-l 8 1. Bournoville, R., Dontchev, K. and Sedivy, J. 1984. Pests of the seed production of lucerne

in Europe. Proceedings of the Medicago sativu group of Eucarpia, 27-30, August 1984 Brno, Czechoslovakia, 359-364.

Cajander, A. K. 1949. Forest types and their significance. Acta. For. Fenn. 56: 1-7 1. Duncan, D. B. 1955. Multiple range and multiple F tests. Biometrics 11: l-42. Fye, R. E. 1984. Damage to vegetable and forage seedlings by overwintcring Lyg74s hesperus

(Heteroptcra: Miridae) adults. J. Econ. Entomol. 77: 1141-I 143. Haseman, L. 1918. The tarnished plant-bug and its injury to nursery stock. Missouri. Agr.

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Holopainen, J. K. 1986. Damage caused by LJJgus r!*gulipennis Popp. (Hcteroptera, Miridac), to Pinus sylvestris seedlings. Stand. J. For. Rcs. 1: 343-349.

Holopaincn. J. K. 1989a. Host plant prefcrcncc of the tarnished plant bug Lygzrs ncg7t/ipe77- nis Popp. J. Appl. Ent. 107: 78-82.

Holopaincn, J. K. 1989b. The influence of cypcrmethrin and oxydemcton-mctyl treatment on Lygtcs damage in young Scats pint seedlings. Ann. Appl. Biol. I 14: 209-2 13.

Iscnhour. D. J. 1985. Efficacy of insccticidcs against Spissistiltrs fksti7747.s (Say), En7poos47cw jirbae (Harris), and Lygus lineolaris (Palisot de Bcauvois) in alfalfa in Georgia. J. Entomol. Sci. 20: I 2 I - 128.

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Markkula, M. 1985. Pest of cultivated plants in Finland in 1984. Ann. Agr. Fcnn. 24: 97- 100.

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Raitio, H. 1987. Site clcvation differences in frost damage to Scats pint (I’inus sylvestris). For. Ecol. Manag. 20: 299-306.

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