When invasive species are included in a new ecosystem, they cause heavy economic losses throughout the world by negatively affecting the services provided by natural and agricultural ecosystems, as well as biological diversity. In addition, invasive species can act as disease vectors that adversely affect ecosystem function and human health. The infestation potential of invasive species is increasing through international trade and shipping. Generally, these species can form high populations in a short time due to the absence of natural enemies in the countries they come from, finding new hosts and high adaptability.
Halyomorpha halys (Hemiptera: Pentatomidae) , named The brown marmorated stink bug (BMSB) , is an invasive species originating from East Asia (China, Japan, Taiwan, Korea). It is stated that the introduction of the species into the USA was accidental in 1998 and in 2001 it was officially defined as a new invasive species. After this date, it was recorded that it was seen in 42 states, it formed the highest population in the Mid-Atlantic Region, and spread in Colombia, Canada and New Zealand.
This species has been detected in countries such as Germany, Austria, Bulgaria, Georgia, France, Netherlands, England, Spain, Switzerland, Italy, Liechtenstein, Hungary, Romania, Russia, Serbia, Slovakia, Chile, Turkey and Greece in recent years.
Its first detection in Turkey was given as Istanbul in 2017. In 2016, in the coastal areas of Artvin province (Kemalpaşa district), in Hopa and Arhavi districts in October and November 2017, in Artvin Borcka, Rize Fındıklı and Ardeşen in 2018, in Artvin Center in February 2019, and in Trabzon Center on April 22, 2019. and Esiroğlu, on April 26 in Akçaabat and finally in April (29 April 2019) in Giresun (Tirebolu) and it was observed that it continues to spread rapidly. It is also called "Brown Skunk Beetle", "Smelly brown bug" or "Brown stink bug" in Turkey.
The importance of this rapidly spreading species should be emphasized urgently, and public opinion should be formed in order to start the efforts to combat it as soon as possible. Because, it is of great importance for other regions of our country to start detailed studies on the bioecology and natural enemies of the species in this region where it entered Turkey, and to take measures to prevent its spread.
Adult, dark brown and 12-17 mm long, antennae are partially pale white, except for the 4th and 5th segments, the rest are black, and the legs are reddish yellow. The eggs are about 1.6 mm long and 1.3 mm in diameter, elliptical and light green, deposited in clusters of 20-30 on the underside of the leaves. The insect has 5 nymphal stages. In the later stages of nymphs, there are spines on their pronotum, dark red eyes are their most characteristic feature.
a) dorsal (top) view,
b) ventral (bottom) view,
c) eggs and 1st instar nymphs,
d) nymphs in the corn plant,
e) adult in hazelnut,
f) adults seen on the walls of the houses
It is stated that BMSB (Brown Marmorated Stink Bug) gives 1-2 offspring per year, it has been recorded that the annual number of offspring is up to 5 in tropical regions, and 1 generation per year in most parts of the USA.
They state that adults overwinter especially in buildings used by humans.
After the end of April, insects leave their wintering areas and are seen in feeding and breeding areas at the end of May/June. After a long period of mating and preoviposition, females lay their eggs from about June to August. Depending on the host plant species, females lay egg clusters (50-150 eggs in total) each containing 20-30 eggs. Egg clusters are in the middle of the lower part of the leaves. Egg laying peaks in July and ends at the end of August. In Europe (Switzerland), it has been found that up to 70% of eggs are laid between June and July. Different nymphal stages can be seen on the same host plant.
It is recorded that approximately 538 days/degrees are required for the insect to complete its development (from egg to adult). An additional 68-148 days/degrees are required for ovulation to begin. The first period nymphs, which emerge from the eggs in 4-5 days, stay in the place where the egg cluster is for a few days before they disperse. Early nymphs feed on egg chorion and obtain useful intestinal symbionts to increase their viability. They go through five nymphal stages. Adults are mainly seen feeding on fruits, especially in August.
Late-stage nymphs and adults pass from the soft and stone fruits they suck to woody ornamental plants. In addition, this host change continues throughout the growing season and the most nutritious host is sought. Adults do not mate before wintering. Beginning from September, insects move towards places where they can spend the winter (buildings, barns, building roofs, natural cracks, tree hollows, etc.).
It was determined that the species gave 2 offspring in the coastal parts of Artvin province and 1 generation in higher areas. It was determined that the most important factor determining the number of offspring was temperature. Depending on the temperature; While the first of these progeny appears from the second half of April, the second one appears to be at the end of July-early August. After mating (second or third week of May, depending on the temperature), adult females lay a total of about 100-220 eggs in groups of 20-28 on the lower surface of the leaves.
The first nymphs are seen after about a week, and they become adults after completing 5 nymphal stages (end of June-early July). In these areas where polyphagous species are seen, they form dense populations on kiwi, hazelnut, apple, date, pear, peach, bean, tomato, pepper, corn, ornamental plants and weeds. It has been noted that adults and nymphs cause significant damage as a result of inserting and sucking the plant sap. It has been observed that the adults are fed with many plants as they seek more juicy foods throughout the season. The insect completes its second generation at the end of September and spends the winter in the adult period. In addition, it was determined that the adults entered the houses, warehouses, roofs, barns and woodsheds to winter in December.
Known natural enemies for most pentatomid species are typical of H. halys. Predator spiders (spiders), ants (ants) and neuropters (lacewings) have been recorded. The number of parasitoid species seems to be less. In the USA, Telenomuspodisi, Trissolcus sp. and T. halyomorphae (Hymenoptera:Scelionidae) have been reported to parasitize H. halys, although they have also been noted to have little effect on population levels of the species. Also in the USA, a Scelionid (Telenomus sp.) and some Eupelmid (Anastatus spp.) egg parasitoids have been found. Tachinids parasitize adult beetles and then emerge from the host after overwintering. These Tachidids are attracted by the H. halys pheromone. In our country, studies on the natural enemies of the insect and determining the species that can be effective are among the issues that should be given priority.
Considering that it has newly entered our country and multiplied and spread very quickly, it is possible to see its natural enemies in our country in the future.
H. halys is a very important polyphagous species that causes damage to many garden and ornamental plants belonging to different genera. According to studies in the USA and literature studies originating from East Asian countries, more than 170 plant species have been listed as hosts by different researchers. The most important hosts are apricot, cherry, peach, plum, apple, pear, citrus, mulberry, persimmon, raspberry, grape, soybean, broad bean, pea, sugar beet, corn, maple, willow, butterfly bush, fire thistle, honeysuckle, vegetables such as lilac, Hibiscus spp., Japanese cedar, cypress, shrubs, tomatoes, peppers; Tropaeolum majus and Asparagus sp.
In addition, H. halys also feeds on some weeds. They noted that H. halys is a key pest in many crops in North West Italy. They also stated that hazelnut, which is the most important product in these areas, can suffer serious damage due to this type.
This species, which is polyphagous in Artvin, was found on kiwi, hazelnut, apple, pear, persimmon, peach, beans, tomato, pepper, corn, ornamental plants and weeds, and it was observed that it formed dense populations especially in Arhavi and Borcka.
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The fact that the species has reached as far as the Tirebolu district of Giresun province in the last period shows how dangerous the hazelnut, which has commercial importance in the region, is.
Due to its mobility, H. halys is a pest that spreads over large areas in a short time and has a wide host environment, which is difficult to control. When an agro enters the ecosystem, H. halys becomes the dominant pentatomid species. Traces of injury, pits, deformities and color changes occur as a result of H.halys feeding on fruits. As a result, these products cannot be marketed. Adults and nymphs are harmful by absorbing the plant sap of their hosts. In addition to all these, at the same time, the populations they form as a result of gathering for wintering in buildings (houses, schools, offices, commercial buildings) cause fear and anxiety in people. In addition to all these, H. Halys also carries some plant diseases. It has been noted that more than 25,000 insects invade some houses, insects gravitating towards the light strike people, and pollute these houses with their unpleasant odors and feces. Researchers mention that if a house is occupied by 25,000 H. halys, these individuals can create a summer population of about three million near this house during the summer period. It has been reported that the most effective method to stop the pest from entering buildings is the use of nets on doors and windows.
Similarly, in Artvin, it has been determined that adults enter the houses, warehouses, roofs, barns and woodsheds to winter in December, and it has been determined that people feel uncomfortable with this situation. In this sense, it will be inevitable for people to take some measures to prevent the entry of insects into these structures.
Both nymphs and adults of H.halys are fed with plant sap. Adults cause more damage to fruits than nymphs. The reason for this is thought to be due to the long stinging mouth tube in adults. Various enzymes secreted by the insect during feeding also cause bitterness in fruits.
Especially considering that it will be fed with the hazelnut fruit, the bitterness it will make on the fruits will cause great economic losses. The thin-shelled Giresun hazelnut will further increase the level of damage.
It was stated that the insect spread rapidly in the USA, the crop was completely lost two years in a row due to the damage in the infested peach field, and although insecticide was applied regularly in April and August, no results could be obtained.
It is reported that the estimated loss of hazelnuts caused by the pest in Georgia in 2016 is approximately 52.7-68.6 million dollars (National Food Agency Report of the Georgian Ministry of Agriculture, presented on 20 November 2016, http://www.moa.gov.ge/en/ ). Based on reports published in North America, it has been reported that BMSB could potentially be responsible for up to 70% loss in product value in fruits and vegetables. It is reported that it caused a loss of approximately 37 million USD in apples and peaches in New Jersey and its surrounding region in 2010, and also very serious losses in sweet corn, peppers, tomatoes, corn, soybeans, grapes and ornamental plants grown in nurseries.
They also noted that the species is spreading rapidly in Abkhazia and causing serious damage to many crops, and that the decrease in yield of peach, tangerine, persimmon and other crops in 2016 (13.2-87.4%) was most likely due to feeding of H. halys. As a result of the damage done in Georgia Anaklia hazelnut fields in 2018, hazelnuts in all hazelnut fields became rancid, so no hazelnut purchases were made.
Of course, it is very difficult to estimate the economic extent of the damage caused by such an important invasive species. This estimation can only be achieved as a result of combining the data to be obtained as a result of highly detailed studies. However, in 2018, the value of kiwi decreased due to the damage caused by the impacts it made on kiwi fruits, especially in Arhavi district.
IPM programs for this pest are under development. Pyrethroid and neonicotinoid insecticides are considered effective against the species, but adverse effects on beneficial arthropods and pollinators are noted. Again, these insecticides have very short-term effects and there is also evidence that H. halys develops resistance to them.
It has been suggested that pyramidal pheromone trap can be used as a useful tool to provide information about population density and movement of H. halys. The use of selective pesticides in accordance with IPM in agricultural areas for chemical control seems to be quite essential in terms of sustainability. Recently, strategies to lure the pest to a location and then kill it with limited chemical use in that location show great promise.
Researchers noted that, in general, pyramid traps prepared with light + pheromone proved to be successful in catching adults. They also stated that if the effect of biotic and abiotic factors on H. halys population dynamics can be revealed in more detail, the data of trapping can be interpreted better. The late season attractant for H.halys is the aggregation pheromone of Plautiastali (Hemiptera: Pentatomidae). This pheromone consists of methyl (E, E, Z) and 2,4,6 decatrienoate (MDT). It is stated that at the end of the season, it is considered beneficial in terms of monitoring the species and catching it in mass. The pheromone is also noted to attract other pentatomids, the insect's natural enemies tachinids and wasps, by acting as a kairomone.
The P. stali pheromone (MDT) is used in the commercial pyramid trap sold by AgBio. It is reported that the USDA has recently isolated the aggregation pheromone secreted by adult males of H.halys. The main component is (3S, 6S, 7R, 10S)-10-11-epoxy-1-bisabolen-3-ol (SSRS), which is 1,10-bisaboladien-3-ol ( He also notes that it is related to zingiberenol). This minor component is (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (RSRS). The SSRS/RSRS ratio in the natural pheromone is 1 in 3.5. Donald Weber from the USDA tested the H. halys pheromone and stated that mixtures of these two components attract the adults and nymphs of the insect.
Again, the same researchers found that the addition of H. halys pheromone to MDT was synergistic and the attractiveness of the combined mixture (COMB) continued throughout the year, that the combined mixture caught 3-4 times more adults and 2-4 times more nymphs than MDT alone. reported that the first H. halys adults emerged in April in their field tests, and the highest adult and nymph levels were reached in August. These studies suggest that the mixture (COMB) will play an important role in monitoring early-season populations, determining economic thresholds for IPM, and providing ensemble lure and kill opportunities. In addition, attracting the BMSB in all seasons is considered a very important step. It is very important to closely follow such studies carried out in the world. It is also important to take samples of the methods applied in studies with successful results for the control of the insect, which is an extremely important species.
Recently, survey studies on pheromone traps and species have been carried out under the leadership of the Ministry of Agriculture and Forestry in our country. For example, in this context, the Black Sea Agricultural Research Institute was established on 20.04.2018 with a technical team consisting of 72 people from the Central and Eastern Black Sea Region provinces of Samsun, Ordu, Giresun, Trabzon, Rize and Artvin Provincial Directorate of Food, Agriculture and Livestock and 49 districts of these provinces. personnel were given training on the "Survey of Halyomorphahalys (Stål) (Hemiptera: Pentatomidae) with Pheromone Traps in the Central and Eastern Black Sea Region" project. In the region, especially the Chambers of Agricultural Engineers support the studies based on the importance of the situation and warn the farmers about this issue. E.g; In April 2019, Artvin Borcka Agriculture District Directorate recommended the application of Decis 2.5 EC against this species to be applied in hazelnut orchards. In addition, experts are provided to give seminars to the relevant technical personnel. In 2019, seminars on this pest were given in the provinces of Trabzon and Rize. In 2018, TAGEM carried out a survey by hanging pheromone traps in the districts located on the coastline of Samsun, Ordu, Giresun, Trabzon, Rize and Artvin provinces in order to determine its distribution in the Eastern Black Sea Region.
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