Variation in abundance and feeding impact of tarnished plant bug (Hemiptera: Miridae) for different cultivars of strawberry: role of flowering phenology and yield attributes

The current study evaluated whether flowering phenology and yield attributes of different strawberry cultivars affect the abundance and feeding impact of tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), as well as behavioral decisions made by feeding nymphs and ovipositing adults. The distribution of emerged nymphs in cage experiments involving nine different cultivars of June-bearing strawberry cultivars suggests that females lay more eggs on plants with numerous flower receptacles, while cultivar per se did not influence their oviposition behavior. A large number of nymphs emerged from receptacles of strawberry plants, while the distribution of emerged nymphs among receptacles, petioles, leaves, and stems varied for different cultivars. These results suggest that the relative intensity of damage caused by ovipositing females may vary for different cultivars. Foraging nymphs did not exhibit a preference for any strawberry cultivar per se, although the abundance of nymphs increased with the weight of receptacles, especially for late instars. Evaluating the density and feeding impact of L. lineolaris for different cultivars under field conditions revealed that some host plant attributes affect the abundance of plant bugs, such as early flowering season and high productivity. Decreasing number of emerged nymphs per flower per plant with increasing density of receptacles per plant suggests that females lay relatively more eggs per receptacle on plants with few receptacles; this pattern of oviposition may explain, in part, why patches with low density of plants typically have high incidence of damage. Planting a high yielding early season cultivar such as 'Cavendish' may contribute to reduce the incidence of damage by L. lineolaris.     

Testing the resource concentration hypothesis with tarnished plant bug on strawberry: density of hosts and patch size influence the interaction between abundance of nymphs and incidence of damage

Abstract. 1. Attributes of patches with strawberry plants were manipulated experimentally to assess the impact of patch size and host density on the abundance of tarnished plant bug (Hemiptera: Miridae) and incidence of fruit damage.
2. The density of nymphs per inflorescence increased with patch size and host density for some but not all generations of plant bug, providing partial support for the resource concentration hypothesis, while emphasising the importance of replicating experiments across several generations of herbivore.
3. Increasing density of nymphs with increasing patch size and host density did not translate into a high incidence of damage, which may be due to the relatively low feeding impact of nymphs in patches with numerous fruits and to the relatively high perimeter-to-area ratio in small patches resulting in a relatively high proportion of damaged fruits.
4. The decreasing proportion of damaged fruits with increasing density of fruits per patch suggests that nymphs exhibit a saturating functional response to density of strawberry fruits. Functional responses of herbivores may be a critical yet overlooked component that influences interactions between insects and their host plant. In particular, concentrated plant resources may result in increased numbers of herbivores yet sill have a negligible influence on plant damage and/or fitness.     

Evaluation of methods to control Phytonemus pallidus and Anthonomus rubi in organic strawberry production

Abstract:  Use of the predatory mite Neoseiulus cucumeris (Oudemans) (Acari, Phytoseiidae) and a fleece cover in combination with pyrethrum application showed potential for control of two important pests in organic production of strawberry ( Fragaria  ×  ananassa Duch.), although there were some unexpected interactions between pyrethrum and the release of N. cucumeris that need to be investigated further. Two cultivars, Honeoye and Cavendish, were treated with pyrethrum with or without fleece to control strawberry blossom weevils [ Anthonomus rubi Herbst. (Col., Curculionidae)] and N. cucumeris was released to control strawberry mites [ Phytonemus pallidus (Banks) (Acari, Tarsonemidae)]. Number of strawberry mites, number of flower buds damaged by the weevil, incidence of grey mould and powdery mildew, and fruit yield were measured in two consecutive fruiting seasons. In Honeoye, the fleece in combination with pyrethrum decreased the proportion of damaged buds by 11–23% and increased yield by 49–91 g per plant. When pyrethrum was used alone it did not influence the number of damaged buds or yield. This indicates that the combined treatment was more effective because of the fleece. In Cavendish, the fleece and pyrethrum treatments were not found to be effective. Almost no P. pallidus was found in Honeoye and the results were not analysable. In plots with Cavendish where N. cucumeris had been released, there were approximately 50% fewer P. pallidus from the end of August onwards in 2003. However, this response did not significantly influence the succeeding year's yield. The number of fruits infected with fungi was very low and no effects were observed for any of the treatments.     

Fragaria virginiana resists tarnished plant bug

An experiment that involved 79 named cultivars and advanced selections of Fragaria × ananassa L., 46 Fragaria virginiana Duch. clones, and 12 F. virginiana backcross selections, and eight Fragaria virginiana × Fragaria chiloensis (L.) Duch. (all Rosaceae) selections, was conducted to detect variation in strawberry genotypes for resistance to tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) (Heteroptera: Miridae). The F. virginiana genotypes were shown to be more resistant than the cultivars and advanced selections in both 2001 and 2002. Within the group of cultivars and advanced selections, several June‐bearing and dayneutral genotypes were more resistant than others. There were fewer plant bugs on F. virginiana than on the cultivars and hybrids. Insect numbers were consistently correlated with percentage of damaged fruits and damage severity, but total numbers of flowers and fruits were only correlated with insect numbers, percentage fruit damage, and damage severity in 1 of the 2 years. Our results suggest that strawberry cultivars, highly resistant to tarnished plant bug, can be bred, if the trait is introgressed from F. virginiana selections.     

Control of western tarnished plant bug Lygus hesperus Knight (Hemiptera: Miridae) in California organic strawberries using alfalfa trap crops and tractor-mounted vacuums

A key economic pest of strawberries in California is the western tarnished plant bug, Lygus hesperus Knight (Hemiptera:Miridae). Alfalfa (Medicago sativa L.) is a highly attractive plant host to western tarnished plant bug, and we hypothesized that it can be successfully managed as a trap crop for pest suppression in strawberries. Completely randomized design trap cropping experiments were established on an organic strawberry farm from 2002 to 2004. Western tarnished plant bug adults and nymphs were significantly more abundant in alfalfa trap crops than in comparable edge strawberry rows. Over 3 experimental yr, twice-weekly summer vacuuming of alfalfa trap crops with a tractor-mounted vacuuming device reduced adult and nymph abundance by 72 and 90%, respectively, in trap crops. This summer vacuuming of alfalfa trap crops also significantly reduced damage caused by western tarnished plant bug in associated unvacuumed organic strawberries (June and July 2002, June 2003, and June and July 2004) compared with either an untreated control (2003) or the organic strawberry grower's standard whole field vacuuming treatment. Vacuuming of alfalfa trap crops reduces an organic grower's costs (tractor, tractor fuel, and driver time) by 78% compared with current whole field vacuuming practices. An economic analysis of a whole hectare model indicates that a positive return from the use of vacuumed trap crops could be realized in 2004. The overall potential positive net return for the 3 mo of vacuumed alfalfa trap crop treatments in 2004 was calculated at +$1,829/ha.     

Circadian activity of Lygus lineolaris (Hemiptera: Miridae) and effectiveness of sampling techniques in strawberry fields

Mobility and distribution of adult tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), was studied on a day-neutral strawberry cultivar ('Selva') in 1991 and 1992 at L'Acadie, Quebec, Canada. On cage-covered plants, individuals were located mainly on reproductive parts. Study of the flight activity with sticky posts revealed that most captures were obtained < 1 m from ground level and that the time of the day at which the maximum counts occur varied among seasons. Three pest-sampling methods (white sticky trap, tapping of flower clusters, and D-Vac) were evaluated over continuous 24-h periods. Maximum captures of adults with white sticky traps were made at midday (1000-1400 hours), whereas the two other methods proved more effective at the beginning (0600-0800 hours) or the end of the day (2000-2200 hours) or during night time. For nymphs, maximum catches were obtained during the day with tapping and D-Vac; white sticky traps were ineffective. Because the D-Vac captures individuals present on all parts of the plant, these counts were used to monitor the effectiveness of the two other sampling techniques. The data suggest that tapping flower clusters throughout the day is a very effective sampling method to estimate nymphal tarnished plant bug populations in strawberries. However, sampling of populations with a high proportion of adults should take into account the bias caused by their flight activity, and sampling should be conducted early in the morning or at the end of the day.     

Oviposition and development of the tarnished plant bug (Heteroptera: Miridae) on field maize

Reduced insecticide use in cotton, Gossypium hirsutum L., as a consequence of the Boll Weevil Eradication Program and the broad adoption of Bt cotton, have helped make the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), a consistent pest of cotton each year in the mid-south. Maize, Zea mays L., has been implicated as having a role in the season-long dynamics of tarnished plant bug infestations in cotton. To date, no published information exists describing the quality of maize as a host for tarnished plant bug. No-choice field studies indicated that adult tarnished plant bug females oviposited into maize leaves, tassels, and ears. Laboratory studies showed that first-instar tarnished plant bugs could successfully develop to the adult stage when fed maize silks at the R1 growth stage, tassels before (VT) and during (R1) pollen shed, and milk stage (R3) kernels from the tip and base of the ear. The proportion of nymphs surviving to the adult stage on these tissues was often similar to that of broccoli, Brassica oleracea L. Nymphs did not develop to adults when fed V5 or R1 maize leaves. However, survival of first instars to the adult stage was improved when nymphs fed on tassels with pollen for 6 d and then moved to silks or leaves. Another field study showed that tarnished plant bugs reproduced in maize mainly during the tassel (VE and VT) and the R1-R3 ear growth stages, and a single new generation was produced in maize during these stages. The highest population recorded during the study (24 June 2005) consisted mostly of nymphs and was estimated to be 29,600/ha (12,000/acre). These studies showed that maize is a suitable host for tarnished plant bug reproduction and development, and its production plays a significant role in the population dynamics of the tarnished plant bug in the mid-south.     

Field evaluation of efficacy and persistence of an insect vacuum device against the tarnished plant bug (Hemiptera: Miridae) in a day-neutral strawberry field

The efficacy of a vacuuming device to reduce Lygus lineolaris (Palisot de Beauvois) populations was evaluated over 3 yr in a day-neutral strawberry field. Immediately after treatments, a significant reduction of population estimates (by tapping of flower clusters) was observed for adults (75% of the time) and nymphs (50% of the time). Under the same conditions, control (i.e., vacuum turbine off) treatments significantly reduced adult population estimates 25% of the time. Lygus lineolaris tapping samples taken from strawberry plants adjacent to the treated zone did not show significant variations over sampling time, suggesting that no escape behavior occurred. This was supported by adult catches on sticky traps located in zones adjacent to the treated one. Our results suggest that vacuuming had inconsistent effect on tarnished plant bug populations and that L. lineolaris mobility plays a marginal role in the use of this control method.     

Impact of Nosema (Microsporidia) infection and fumagillin treatment on Lygus lineolaris (Hemiptera: Miridae)

A consistent supply of healthy tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) (Hemiptera: Miridae), is necessary for the development of novel management strategies targeting this pest. After being in culture for several years, a substantial portion of a tarnished plant bug colony was found to be infected with a Nosema (Microsporidia) species. Studies were subsequently undertaken to evaluate the impact of Nosema infection on tarnished plant bug productivity and to test the efficacy of fumagillin to treat this infection. Using buffalo black stain, infections could not be reliably detected in adult tarnished plant bugs until adults were 6-8days post eclosion. Nosema infections reduced adult longevity and fecundity. Maximum fecundity was restored using a concentration of 16.8ppm fumagillin while maximum longevity for females was at a concentration of 33.6ppm fumagillin incorporated into the tarnished plant bug diet. Minimum infection scores were obtained at 67.2ppm, the highest concentration tested. A field survey of tarnished plant bugs in Mississippi found Nosema infections in 3% of wild tarnished plant bugs.     

The phenology of Lygus rugulipennis, the European tarnished plant bug, on late-season strawberries, and control with insecticides

The phenology of Lygus rugulipennis, the European tarnished plant bug, was studied in fields of strawberries producing late-season (July to September) crops. Adults invaded fields in small numbers, mainly in July. Large numbers of nymphs were found in late July and early August; these matured into adults from late August. Adults formed the overwintering population; some remained in strawberry fields but left in spring to feed on other host plants. All the insecticides tested, i.e. malathion, chlorpyrifos, heptenophos, cypermethrin, bifenthrin and trichlorfon, gave good short-term control of nymphs.     

Tactics for management of thrips (Thysanoptera: Thripidae) and tomato spotted wilt virus in tomato

Four studies were conducted in Georgia during spring 1999, 2000, 2001, and 2002 to evaluate various management tactics for reducing thrips and thrips-vectored tomato spotted wilt virus (TSWV) in tomato and their interactions relative to fruit yield. Populations of thrips vectors of TSWV, Frankliniella occidentalis (Pergande) and Frankliniella fusca (Hinds), were determined using flower and sticky trap samples. The management practices evaluated were host plant resistance, insecticide treatments, and silver or metallic reflective mulch. Averaged over all tests, the TSWV-resistant tomato 'BHN444' on silver mulch treatment had the largest effect in terms of reducing thrips and spotted wilt and increasing marketable yield. Of the insecticide treatments tested, the imidacloprid soil treatment followed by early applications of a thrips-effective foliar insecticide treatment provided significant increase in yield over other treatments. Tomato yield was negatively correlated with the number of F. fusca and percentage of TSWV incidence. F. occidentalis per blossom was positively correlated with percentage of TSWV incidence, but not with yield. No significant interactions were observed between cultivar reflective mulch main plot treatments and insecticide subplot treatments; thus, treatment seemed to be additive in reducing the economic impact of thrips-vectored TSWV. Control tactics that manage thrips early in the growing season significantly increased tomato yield in years when the incidence of TSWV was high (>17%).     

Relationships between the occurrence of misshapen fruit on late-season strawberry in the United Kingdom and infestation by insects, particularly the European tarnished plant bug, Lygus rugulipennis

In experiments in which the European tarnished plant bug, Lygus rugulipennis, was caged on the developing flowers or young fruits of strawberry, the insects caused malformation of the fruits. Another species of capsid, Plagiognathus chrysanthemi, caused similar damage; this species is less numerous than L. rugulipennis on late-season crops of strawberry in UK. Other insects which sometimes occur in large numbers in the flowers of late-season strawberry, i.e. various species of thrips and pollen beetles, did not cause fruit malformation in caging experiments, though thrips sometimes caused discoloration of the fruit. In field experiments where numbers of L. rugulipennis were reduced by the use of insecticides, the amount of misshapen fruit was reduced greatly compared to untreated plots. Correlations between the numbers of L. rugulipennis present at the early stages of fruit development and damage scores for fruit deformity were highly significant. This capsid is likely to be the major cause of fruit malformation in late-season crops of strawberry in the UK.     

Economic Thresholds of Western Flower Thrips (Thysanoptera: Thripidae) for Unripe Red Pepper in Greenhouse

This study was conducted to develop economic thresholds of western flower thrips (Frankliniella occidentalis Pergande) for unripe red pepper in greenhouses. To investigate the relationship between the density of thrips and resulting damages, experimental plots with five treatments (0, 4, 16, 48, 96 adults per plot) as initial release densities were established at the National Institute of Agricultural Science and Technology, Suwon, Korea, in 2004. Western flower thrips density was monitored using flower samplings and yellow sticky trap (8×13 cm) counts. Western flower thrips density was directly related to increased numbers of damaged fruits and reduced fruit yield. The number of marketable fruits produced decreased as the thrips densities increased. The major damage to pepper fruits caused by thrips was cosmetic scars that resulted from immature feeding. When flower samples or yellow trap caches were used to determine the density of thrips, which were collected on a previous sampling date, thrips densities were determined to be related to the percentage of fruits that were damaged, and a significant relationship was found for the flower samples (y = 0.3219x + 1.0792, r² = 0.8640 and for trap catches (y = 11.9209 log(x) −2.158, r² = 0.8306). The economically-tolerable ratio of damaged fruits based on control cost and market values under current greenhouse cultivation was estimated as 3.4 to 8.0%. Economic thresholds of western flower thrips ranged from 0.7 to 2.1 adults or nymphs per flower, and 2.3 to 5.7 adults per four-day sticky card count.     

Flower Volatiles,Crop Varieties and Bee Responses

Pollination contributes to an estimated one third of global food production, through both the improvement of the yield and the quality of crops. Volatile compounds emitted by crop flowers mediate plant-pollinator interactions, but differences between crop varieties are still little explored. We investigated whether the visitation of crop flowers is determined by variety-specific flower volatiles using strawberry varieties (Fragaria x ananassa Duchesne) and how this affects the pollination services of the wild bee Osmia bicornis L. Flower volatile compounds of three strawberry varieties were measured via headspace collection. Gas chromatography showed that the three strawberry varieties produced the same volatile compounds but with quantitative differences of the total amount of volatiles and between distinct compounds. Electroantennographic recordings showed that inexperienced females of Osmia bicornis had higher antennal responses to all volatile compounds than to controls of air and paraffin oil, however responses differed between compounds. The variety Sonata was found to emit a total higher level of volatiles and also higher levels of most of the compounds that evoked antennal responses compared with the other varieties Honeoye and Darselect. Sonata also received more flower visits from Osmia bicornis females under field conditions, compared with Honeoye. Our results suggest that differences in the emission of flower volatile compounds among strawberry varieties mediate their attractiveness to females of Osmia bicornis. Since quality and quantity of marketable fruits depend on optimal pollination, a better understanding of the role of flower volatiles in crop production is required and should be considered more closely in crop-variety breeding.     

Utilization of early soybeans for food and reproduction by the tarnished plant bug (Hemiptera: Miridae) in the delta of Mississippi

Commercially produced maturity group (MG) IV soybeans, Glycine max L., were sampled during bloom for tarnished plant bugs, Lygus lineolaris (Palisot de Beauvois), during May and June 1999 (3 fields) and 2001 (18 fields). The adults and nymphs were found primarily in single population peaks in both years, indicating a single new generation was produced during each year. The peak mean numbers of nymphs were 0.61 and 0.84 per drop cloth sample in 1999 and 2001, respectively. Adults peaked at 3.96 (1999) and 3.76 (2001) per sweep net sample (25 sweeps). Tests using laboratory-reared and field-collected tarnished plant bugs resulted in very poor survival of nymphs on 16 different soybean varieties (MG III, one; IV, four; V, nine; VI, two). A large cage (0.06 ha) field test found that the number of nymphs produced on eight soybean varieties after mated adults were released into the cages was lower than could be expected on a suitable host. These results indicated that soybean was a marginal host for tarnished plant bugs. However, the numbers of adults and nymphs found in the commercially produced fields sampled in the study may have been high enough to cause feeding damage to the flowering soybeans. The nature of the damage and its possible economic importance were not determined. Reproduction of tarnished plant bugs in the commercially produced early soybean fields showed that the early soybeans provided tarnished plant bugs with a very abundant host at a time when only wild hosts were previously available.     

Evaluation of damage to physic nut (Jatropha curcas) by true bugs

The type of injury and amount of damage to the fruits and seeds of physic nut (Jatropha curcas L., Euphorbiaceae) caused by two species of fruit feeding true bugs, Pachycoris klugii Burmeister (Heteroptera: Scutelleridae) and Leptoglossus zonatus (Dallas) (Heteroptera: Coreidae), and the flower feeding true bug, Hypselonotus intermedius Distant (Heteroptera: Coreidae), were assessed using field cages. The parameters analysed were infructescence, fruit, seed and seed kernel weight, seed length, fruit and seed abortion, seed malformation and oil and protein content of the seed kernels. All three species reduced overall yield. The two members of the fruit feeding guild led to premature fruit abortion and malformed seeds. Reduction of fruit, seed and seed kernel weight as well as seed length could be expressed as linear regressions of adult population densities. The oil content of the seeds was slightly reduced by the bugs, but protein content remained unchanged. Damage increased with the developmental stage of the larvae. Whereas adult L. zonatus of both sexes produced more damage than the nymphs, female P. klugii caused less damage than nymphs, and male P. klugii no significant damage at all. H. intermedius is a pollinator of this entomogamous plant. At high densities, however, it reduced the number of fruits maturing.     

Identification of Lygus hesperus by DNA barcoding reveals insignificant levels of genetic structure among distant and habitat diverse populations

Background

The western tarnished plant bug Lygus hesperus is an economically important pest that belongs to a complex of morphologically similar species that makes identification problematic. The present study provides evidence for the use of DNA barcodes from populations of L. hesperus from the western United States of America for accurate identification.

Methodology/Principal Findings

This study reports DNA barcodes for 134 individuals of the western tarnished plant bug from alfalfa and strawberry agricultural fields in the western United States of America. Sequence divergence estimates of <3% reveal that morphologically variable individuals presumed to be L. hesperus were accurately identified. Paired estimates of F_st and subsequent estimates of gene flow show that geographically distinct populations of L. hesperus are genetically similar. Therefore, our results support and reinforce the relatively recent (<100 years) migration of the western tarnished plant bug into agricultural habitats across the western United States.

Conclusions/Significance

This study reveals that despite wide host plant usage and phenotypically plastic morphological traits, the commonly recognized western tarnished plant bug belongs to a single species, Lygus hesperus. In addition, no significant genetic structure was found for the geographically diverse populations of western tarnished plant bug used in this study.     

Effects of cultivar, fruit number and reflected photosynthetically active radiation on Fragaria x ananassa productivity and fruit ellagic acid and ascorbic acid concentrations

BACKGROUND AND AIMS: A number of strawberry varieties were surveyed for their total ellagic acid concentration, and attempts were made to determine if ellagic acid and ascorbic acid concentrations of two strawberry cultivars could be increased by polythene reflective mulches. METHODS: After adjusting crop yields and cultivation using polythene mulches with two different PAR reflective capacities, field- and polytunnel-grown strawberries were analysed for ellagic acid and ascorbic acid concentrations by HPLC. Comparative measurements of yield and fruit quality were determined along with plant developmental changes. KEY RESULTS: Ellagic acid concentration varied widely with strawberry cultivar (60-341 microg g(-1) frozen weight), as did the ratio of conjugated ellagic acid : free ellagic acid. Also, there was significant year-to-year variation in total ellagic acid concentration with some cultivars. Mulches with different reflective capacities impacted on strawberry production; highly reflective mulches significantly increased growth and yield, the latter due to increases in fruit size and number. CONCLUSIONS: Highly reflective mulches significantly increased total concentrations of ellagic acid and ascorbic acid relative to control in fruit of different cultivars. The potential of agronomic practices to enhance the concentration and amounts of these important dietary bioactive compounds is discussed.     

Impact of twospotted spider mite (Acari: Tetranychidae) on growth and productivity of glasshouse cucumbers

Experiments were conducted to assess the damage of the glasshouse cucumber by twospotted spider mite, Tetranychus urticae Koch, and to investigate when the economic yield begins to decrease after T. urticae infestations. To assess the damage, dry matter partitioning in the cucumber plant was quantified and plant growth analyses were conducted at four different T. urticae infestation levels. T. urticae infestations decreased leaf productivity by reducing the total number of leaves per plant. Approximately 14% reductions of total leaf areas could result in significant yield loss. The decreased leaf productivity by T. urticae feeding caused biomass reductions and altered the pattern of dry matter partitioning in the plant; damaged plants accumulated more dry matter in the leaf, and partitioning of dry matter to fruits was hindered. The economic yield of cucumber began to significantly decrease as early as 4 wk after heavy mite infestations. This study also showed the seasonal differences in T. urticae-cucumber damage interactions among mite infestation levels.     

The invasive Leptoglossus seed bug,a threat for commercial seed crops,but for conifer diversity?

Among the recent introductions of alien insects in Europe, the polyphagous western conifer seed bug, Leptoglossus occidentalis Heidemann (Heteroptera; Coreidae) can seriously be regarded as a major threat for all the European conifer forests. In the current study combining laboratory and field experimentations, we characterized first bug damage by developing specific damage categories on seeds of different conifer species by the use of X-ray. Secondly, we investigated the impact of the invasive bug on key conifer species used for afforestation in Western and Central Europe. For this purpose, we performed germination tests on predated seeds which revealed that even light damage (consumption of <1/3 of the whole seed content) strongly reduced the germination capability of the seed. We also compared the impact of feeding on the proportion of filled seeds. Second year cones of Pinus sylvestris and Pinus nigra have been enclosed and offered to different life stages (nymphs and adults) and the results showed a significant reduction of filled seeds whatever the life stage. In field, we annually surveyed the bug seed damage for six different conifer species planted in southwestern French seed orchards. Taking into account the economic value of improved seeds in seed orchards, economic impact of bug damage was important although never exceeded 25 %. Two natural or semi-natural alpine pine stands were also surveyed and appeared to be highly affected by the bug (up to 70 % of damaged seeds). Therefore, bug damage could also be considered as a serious threat for seed production in natural stands.