Preliminary data on the biology of brown marmorated stink …...stink bug adults from the...

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Turkish Journal of Zoology Turk J Zool(2018) 42: 617-624© TÜBİTAKdoi:10.3906/zoo-1802-34

Preliminary data on the biology of brown marmorated stink bug Halyomorpha halys (Hemiptera, Pentatomidae) in Georgia

Maka MURVANIDZE1,*, Greg KRAWCZYK2, Nino INASARIDZE3, Lika DEKANOIDZE3, Natia SAMSONADZE3, Mariam MACHARASHVILI3, Sopho KHUTSISHVILI3, Salome SHENGELAIA3

1Institute of Entomology, Agricultural University of Georgia, Tbilisi, Georgia2Department of Entomology, Fruit Research and Extension Center, Pennsylvania State University, Biglerville, PA, USA3Department of Biology, Faculty of Exact and Natural Sciences, I. Javakhishvili Tbilisi State University, Tbilisi, Georgia

* Correspondence: [email protected]

1. IntroductionBrown marmorated stink bug (BMSB) Halyomorpha halys (Stäl) is an invasive insect pest species naturally occurring in Japan, southern China, and Korea (Hoebeke and Carter, 2003; Lee et al., 2013).The predictive model of BMSB distribution shows suitable areas for its distribution stretching between latitudes 30° and 50° and including parts of Europe, North America, Australia, the North Island of New Zealand, Angola, and Uruguay (Zhu et al., 2012). Since the late 1990s BMSB populations have become established in North America and since the mid-2000s in Europe (Wermelinger et al., 2008; Leskey et al., 2012; Callot and Brua, 2013). In the Republic of Georgia, BMSB individuals were first observed during the 2015 season with significant injuries to hazelnut first reported during the 2016 season. The estimated 2016 economic impact for Georgian hazelnut farmers and exporters/processors totals approximately 52.7–68.6 million US dollars (National Food Agency, Ministry of Agriculture of Georgia report presented on 20 November 2016; http://www.moa.gov.ge/En/). During the 2016 season, damaging infestation levels in hazelnuts were observed in the Samegrelo Region while moderate nut injuries were also reported in the Guria and Imereti regions of Georgia. In addition to hazelnuts, BMSB also has the potential to cause severe economic injuries

to other crops, such as pome and stone fruit, vegetables (tomato and pepper), and field crops (maize or various grains). Based on published reports from North America, BMSB can potentially be responsible for up to 70% loss in crop value in fruit and vegetables (Leskey et al., 2012).

BMSB monitoring studies documented the viability of commercially available BMSB traps and lures to assess the population levels of BMSB adults and nymphs (Leskey et al., 2015). Employing BMSB monitoring traps in an orchard provides a very reliable indicator of stink bugs’ presence in the area. Understanding stink bug biology and behavior is a key precondition for effective planning and implementation of best integrated pest management practices directed against this pest. The BMSB seems to be univoltine in the upper mid-Atlantic region (Nielsen and Hamilton, 2009a) and bivoltine in areas of southern Pennsylvania, Virginia, West Virginia, and North Carolina (Leskey et al., 2012, Bakken et al., 2015), while in southern China the BMSB populations are reported to have 4 to 6 generations (Hoffman, 1931; Lee et al., 2013). The specific aspects of BMSB biology or behavior in Georgia and the Caucasus region need to be investigated.

The Republic of Georgia is located in the Caucasus, a biodiversity hotspot that shelters the most diverse flora and fauna of the temperate region (Zazanashvili et al.,

Abstract: During the 2017 season we investigated the occurrence and biology of the brown marmorated stink bug (BMSB), Halyomorpha halys, a new invasive insect pest in two commercial hazelnut orchards located in the Samegrelo Region, Republic of Georgia. The first stink bug adults from the overwintering generation appeared on sticky traps at the end of May, while all instar nymphs and adults were observed at the end of July and through August. The peak occurrence of adults and nymphs in the field was observed at 896–1061 DD13.9. The wooded areas around orchards supported the development of two BMSB generations. The forested areas and wild vegetation provided the source of continuous influx of the pest into the orchards, while the BMSB influx from a neighboring meadow and abandoned buildings was less important.

Key words: Halyomorpha halys, hazelnut orchard, sticky traps, migration, Zugdidi, Georgia

Received: 22.02.2018 Accepted/Published Online: 01.11.2018 Final Version: 12.11.2018

Research Article

This work is licensed under a Creative Commons Attribution 4.0 International License.

https://orcid.org/0000-0001-8579-4011https://orcid.org/0000-0002-5396-0967https://orcid.org/0000-0003-0753-6118https://orcid.org/0000-0002-1437-6338https://orcid.org/0000-0003-1224-3029https://orcid.org/0000-0003-1758-3882https://orcid.org/0000-0003-3939-6615https://orcid.org/0000-0003-3246-5593

MURVANIDZE et al. / Turk J Zool

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2004). The western part of the country, where the BMSB outbreak was recorded, harbors unique Colchic forests and can be classified as temperate rainforest due to the barrier mountains located along coastlines that trap a large portion of the humidity from oceanic air masses (Zazanashvili, 2009).

This report provides the first documentation of the distribution, biology, and behavior of the BMSB in two Georgian hazelnut orchards located in the Samegrelo Region conducted by utilizing commercially available BMSB monitoring tools. The main objectives of this project included observations of BMSB biology in commercial Georgian hazelnut orchards and investigations of potential BMSB migration routes during the growing season.

2. Materials and methods2.1. Site descriptionField works were conducted in two commercial hazelnut orchards located in the village of Rike, Zugdidi District, Samegrelo Region, Georgia. The first orchard (Orchard

A) used for observations was about 750 m2 in size and was located adjacent to a farmer’s house (42.583509°N, 41.893866°E). From the southern and western sides the orchard was surrounded by road, while from the northern and eastern sides by a house and a yard with ornamental and fruit trees such as grape (Vitis sp.), apple (Malus sp.), pear (Pyrus sp.), and feijoa (Feijoa sp.) (Figure 1).

The second hazelnut orchard (Orchard B) was 1.2 ha in size and located about 200 m away from the first one (42.585183°N, 41.896607°E). The orchard from the north was surrounded by wild vegetation including Populus gracilis Grossh., Acacia sp., Alnus sp., and Eriobotrya japonica Thnb. From the south side it was bordered by road, from the west by a corn field, and from the east by ruins of an old building; wild vegetation including Acacia sp., Rubus sp., Thea sp., and Dryopteris sp.; and a commercial corn field (Figure 2).2.2. Trap placement and monitoringField observations were conducted by utilization of sticky traps baited with pheromone lures. BMSB surveillance

Figure 1. Placement of sticky traps in Orchard A and cumulative number of individuals of H. halys on each trap.

Figure 2. Placement of sticky traps in Orchard B and cumulative number of individuals of H. halys on each trap.


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activity utilizing pheromone-baited traps is documented to provide reliable information about the presence of various BMSB developmental forms in the monitored area (Josef et al., 2014; Leskey et al., 2015)

Commercially available BMSB monitoring lure Pherocon BMSB and clear sticky Stink Bug STKY dual panel adhesive traps (Trece, Inc., Adair, OK, USA) were used for BMSB monitoring at both sites. In the first orchard (Orchard A), eight BMSB monitoring traps were distributed at the edges of the orchard. The distances between individual traps varied with the pairs 1–4 and 2–3 placed at a distance of about 50 m apart; traps 1–2, 3–4, 8–9, and 7–10 with about 10 m distance between traps; and 40 m between traps 7–8 and 9–10. A single trap was also placed on the pear tree in the center of the house’s front yard and one additional trap on the fig tree in the backyard. A total of ten traps were placed in this orchard (Table 1; Figure 1). To describe the location of traps, the traps numbered 1, 5, 6, and 7 are marked as ‘house in’, while the traps numbered 2, 3, 4, 8, 9, and 10 are labeled as ‘house out’.

In the second orchard (Orchard B), 13 monitoring traps were placed at the perimeter of the orchard at about 40 m distance from each other, while eight additional traps were placed inside of the orchard, for a total of 21 traps (Table 1; Figure 2). Traps were placed within the tree canopies at about 1.70 m above the ground. Traps in Orchard A were placed on 6 May while traps in the Orchard B were placed on 20 May 2017. The clear sticky parts of the traps were replaced every 6 weeks while pheromone lures were replaced every 12 weeks, according to the instructions for the products.

All traps were checked weekly for the presence of stink bugs. The numbers of collected BMSB adults and nymphs were recorded individually for each trap. The captures of each nymphal stage were recorded separately, except for the first instar nymphs, which were absent on the sticky traps but were observed on egg masses.

The degree-day accumulations were calculated as DD = (t°min + t°max)/2 – 13.9 (13.9 °C was used as the lower developmental threshold (Nielsen and Hamilton, 2009b)).

2.3. Data analysesThe BMSB capture data were analyzed using one-way ANOVA procedures (Statistix 9, 2008). Before the mean separation analyses, to normalize the results of the weekly observations, all data were transformed using square root transformation. The differences among means were analyzed using the Fisher LSD protected mean separation test at P < 0.05 (Statistix 9, 2008). The same procedures were applied to compare the differences in BMSB captures for both orchards individually by individual trap, by date, and by trap location (e.g., house in, house out, inside the orchard, adjacent to the meadow, and adjacent to the woodland area).

3. Results3.1. Phenology of H. halys in hazelnut orchardsThe first BMSB adults in both orchards were observed by 20 May. Only BMSB adults were captured on sticky traps until 8 July. The second instar BMSB nymphs were first captured on 8 July. After the first capture of nymphs, the immature stages became the most abundant part of the BMSB population observed in traps. At the end of July and throughout August all BMSB instars and adults were observed at the same time. In September, the numbers of nymphal stages started to decrease, and by the end of September, only adults and fifth instar nymphs were observed. In October, the number of BMSB individuals found on sticky traps decreased significantly, and by the end of the month, only two adults were found in the first orchard near the household area (Table 2; Figures 3A and 3B). Comparison of numbers of observed BMSB adults and nymphs present in both orchards utilizing all traps and all observation dates shows significant differences between numbers of adults (df = 1, F = 10.83, P < 0.05) and 2nd and 3rd instar nymphs (df = 1, F = 25.28, P < 0.05), but no significant differences were observed between the 4th and 5th instar nymphs (df = 1, F = 1.55, P > 0.05). 3.2. Effect of temperature on biology of H. halysThe accumulation of degree days using the lower threshold of 13.9 °C was calculated starting from 6 May, the first

Table 1. Location of sticky traps in two commercial hazelnut orchards.

Orchard # Trap # House in House out Perimeter, close to the wild vegetationPerimeter, close to the meadow and corn field Inside the orchard

A1, 5, 6, 7 + - - - -2, 3, 4, 8, 9, 10 - + - - -

B

11–14 - - + - -15–17 - - - + -18–20 - - + - -21–23 - - - + -24–31 - - - - +


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day the traps were placed in orchards. Adults from the overwintering BMSB population started to appear in orchards when average daily temperature was at or above 13–15 °C (31.25 DD13.9). The second instar nymphs on sticky traps were first found when the temperature reached above 23°C at DD accumulation of 359.45 DD13.9. All instar nymphs and BMSB adults were simultaneously present in traps as long as the average temperature was above 23–26 °C (DD accumulation 896–1061 DD13.9). At about 1200 DD13.9 only BMSB adults and fifth instar nymphs were found in traps. After the DD accumulation reached 1266 DD13.9 only individual BMSB adults were still observed on traps (Figure 4). 3.3. Distribution of BMSB individuals in orchardsThe average weekly captures of BMSB adults and nymphs

per trap were similar in both evaluated orchards (P > 0.05), suggesting relatively uniform distribution of BMSB adults and nymphs within both orchards (Tables 3 and 4).

In Orchard A no differences were observed in the distribution pattern of stink bug stages in traps located close to the house. Cumulative numbers of nymphs were higher than numbers of adults, with the exception of trap number 5, which was located on the pear tree in front of the house and recorded the highest number of adults. A low cumulative number of both adults and nymphs was recorded from trap number 6, which was placed on the fig tree in the back yard (Figure 1).

In Orchard B the number of adults and nymphs was always higher around the perimeter (trap numbers 11–23) than inside the orchard (trap numbers 24–31), but the

Table 2. The average weekly captures of brown marmorated stink bug adults and nymphs in two commercial hazelnut orchards with indication of DD13.9 .The BMSB capture data are presented from n = 10 traps in Orchard A and n = 21 traps in Orchard B, Samegrelo, Georgia, 2017.

Date DD13.9Adults 2nd and 3rd instars 4th and 5th instars

A B A B A B20-May 31.25 0.1 l 0.0 h 0.0 e 0.0 g 0.0 f 0.0 g26-May 39.9 0.5 ghi 0.4 fgh 0.0 e 0.0 g 0.0 f 0.0 g03-Jun 76.5 2.9 def 0.7 f 0.0 e 0.0 g 0.0 f 0.0 g10-Jun 136.3 3.0 def 1.3 e 0.3 de 0.0 g 0.0 f 0.0 g17-Jun 172.1 1.6 f–i 0.4 fgh 0.0 e 0.0 g 0.0 f 0.0 g24-Jun 221.4 0.6 ghi 0.5 fg 0.0 e 0.0 g 0.0 f 0.0 g01-Jul 286.3 0.4 hi 0.2 fgh 0.0 e 0.0 g 0.0 f 0.0 g08-Jul 359.4 0.2 hi 0.0 gh 3.1 d 0.0 g 0.0 f 0.0 g15-Jul 422.7 1.1 f–i 0.2 fgh 14.3 c 0.9 f 0.2 f 0.0 g22-Jul 504.8 1.2 e–h 0.1 gh 73.8 a 4.0 de 0.4 ef 0.1 fg29-Jul 587.7 1.0 f–i 0.4 fgh 62.7 a 5.7 d 2.3 cd 0.5 ef05-Aug 668.1 1.0 ghi 0.4 fgh 36.0 b 16.0 b 3.4 c 1.9 cd12-Aug 767.3 3.9 de 1.7 e 36.8 b 23.8 a 9.8 b 4.2 c27-Aug 948.1 8.4 c 6.4 c 7.9 c 16.6 ab 1.2 de 4.3 b03-Sep 1013.9 13.9 bc 9.6 b 2.7 de 9.2 c 1.5 de 4.1 b09-Sep 1061.6 34.0 a 20.1 a 0.3 de 3.3 e 1.1 def 3.6 b15-Sep 1117.5 28.1 a 21.6 a 0.2 de 0.7 f 0.2 ef 1.0 e23-Sep 1200.3 18.1 a 7.1 c 0.0 e 0.0 g 12.6 a 7.6 a30-Sep 1242.5 9.9 bc 9.1 b 0.0 e 0.0 g 2.4 c 0.8 e07-Oct 1252.8 3.9 c 3.9 d 0.0 e 0.0 g 0.9 de 0.3 fg14-Oct 1264 1.8 d–g 2.0 e 0.0 e 0.0 g 2.8 c 1.0 de21-Oct 1266.7 1.4 f–i 0.6 f 0.0 e 0.0 g 0.0 f 0.0 g28-Oct 1278.2 0.2 hi 0.1 gh 0.0 e 0.0 g 0.0 f 0.0 g

Means within a column followed by the same letters are not significantly different (ANOVA, Fisher’s LSD test, P > 0.05, data for analyses transformed using square root transformation).


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Figure 3. The dynamics of the various stages of H. halys in A) Orchard A and B) Orchard B, Samegrelo, Georgia, 2017.

Figure 4. Degree days (DD13.9) accumulation data for H. halys during the observation period. Solid lines indicate Orchard A, dashed lines Orchard B. BMSB traps were placed in Orchard A on 6 May 2017 and on 20 May 2017 in Orchard B.


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highest numbers were recorded on traps located adjacent to wild vegetation (trap numbers 11,12,13, and 14 and trap numbers 18,19, and 20) (Figure 2).

Distribution of adults and 2nd and 3rd instar nymphs significantly differed among trap locations (df = 4, P < 0.05, F = 3.4 for adults and F = 7.41 for 2nd and 3rd instars). For the 4th and 5th instars the differences were not significant (df = 4, F = 1.87, P > 0.05) (Table 5).

4. DiscussionThe emergence of adult stink bugs from overwintering sites in fruit orchards located in the Mid-Atlantic Region of the United States is known to start around mid-April and it is suggested there are overlapping BMSB generations present in orchards around mid-June (Nielsen et al., 2008; Bergh et al., 2017). In Asian countries, the emergence of BMSB from overwintering shelters is reported to start in mid-March, when temperatures are over 10 °C, and continue until mid-May (Lee et al., 2013). Utilizing BMSB monitoring traps, we observed the occurrence of the first BMSB adults in the end of May; however, no searches were conducted prior to the placement of the traps in orchards. During the 2017 season, the climate conditions in the Zugdidi region were quite abnormal, with average humidity ranging from 80% to 100% from May to the end of July and with average precipitation three times higher than normal. Continuous heavy rains could potentially impact the early season emergence of BMSB adults from their overwintering shelters. In our observations, the first adults were detected at the end of May when average temperature was about 13 °C, despite the start of observations on 6 May. The highest numbers of BMSB adults with potentially overlapping generations were observed from mid-July to August when the average high temperatures reached 23–26 °C (about 504 DD13.9). Highest numbers of adults and all instar nymphs in the field were recorded from 504 to 950 DD13.9. In laboratory studies described by Nielsen et al. (2008), the BMSB development from egg to adult stage was observed to occur at temperatures between 17 and 33 °C with eggs hatching even at 15 °C; however, an average of 535 DD13.9 was necessary to complete the development of eggs, and 830–1000 DD13.9 to find representatives of all juvenile stages (Nielsen et al., 2008; Nielsen and Hamilton, 2009b).

The results of our observations generally agree with the observations reported by Nielsen et al. (2008) and Nielsen and Hamilton (2009b). After the finding of first BMSB adults on traps, it took 677 DD13.9 to find the first second instar nymphs and 896–1061 DD13.9 were needed to find representatives of all developmental stages in the field. The development of BMSB from one instar to another takes about 3–6 days (Hoebeke and Carter, 2003; Leskey et al., 2012; Lee et al., 2013), depending on the temperature. The latest second instar nymphs were found in mid-September,

Table 4. The average captures of brown marmorated stink bug adults and nymphs from each of the traps located in Orchard B during the 2017 season. Trap # Adults Nymphs 2–3 Nymphs 4–5 Nymphs total11 5.3 a 2.0 ab 1.4 ab 3.4 abc12 4.2 a 8.6 a 3.4 a 12.0 a13 3.2 a 2.7 ab 0.9 ab 3.6 abc14 3.5 a 2.0 ab 0.9 ab 2.9 abc15 3.4 a 4.1 ab 0.9 ab 5.0 abc16 4.6 a 3.2 ab 1.1 ab 4.3 abc17 2.3 a 4.2 ab 1.2 ab 5.4 ab18 2.6 a 7.1 a 1.7 ab 8.8 ab19 4.3 a 7.7 a 2.0 a 9.7 a20 3.6 a 5.0 a 2.3 a 7.3 ab21 3.5 a 2.8 ab 1.5 ab 4.3 abc22 4.0 a 5.7 a 1.3 ab 7.0 ab23 5.1 a 6.2 a 1.1 ab 7.3 ab24 4.3 a 2.0 ab 0.8 ab 2.8 abc25 4.0 a 1.6 ab 1.4 ab 3.0 abc26 3.3 a 2.1 ab 1.0 ab 3.1 abc27 4.9 a 1.6 ab 1.0 ab 2.6 abc28 3.5 a 1.3 ab 0.7 ab 2.0 bc29 3.9 a 1.5 ab 0.9 ab 2.4 abc30 3.8 a 1.6 ab 1.0 ab 2.6 abc31 1.9 a 0.4 b 0.3 b 0.7 c


Table 3. The average captures of brown marmorated stink bug adults and nymphs from each of the traps located in Orchard A during the 2017 season. Trap # Adults Nymphs 2–3 Nymphs 4–5 Nymphs total1 2.7 b 8.8 a 1.0 a 9.9 a2 5.1 ab 12.7 a 1.1 a 13.8 a3 4.1 b 8.2 a 1.5 a 9.7 a4 5.7 ab 10.6 a 3.5 a 14.1 a5 12.7 ab 12.2 a 0.9 a 13.1 a6 5.5 ab 4.3 a 1.1 a 5.3 a7 7.4 ab 9.7 a 2.3 a 12.0 a8 4.9 b 12.9 a 1.6 a 14.6 a9 6.3 ab 11.7 a 1.9 a 13.6 a10 5.3 b 12.3 a 1.9 a 14.2 a



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suggesting that the last eggs were laid no later than in the beginning of September. Based on our field observations and accumulation of degree-days, we propose the presence of two full generations of BMSB for the subtropic climate zone of western Georgia.

Studies conducted in peach orchards showed clustering of BMSB on orchards at late sampling dates (mid- to late August) when fruit was ripe or ripening (Hahn et al., 2017). The authors proposed that immigrants from neighboring areas (e.g., forested territories) were triggered by aggregating individuals in orchards, leading to the increased damage. Other investigations conducted in an apple orchard also demonstrated a high number of BMSB individuals on trees located close to the orchard borders and mostly in the upper part of the canopy (Josef et al., 2014). During the late season, stink bugs are known to develop on both native and nonnative host plants surrounding orchards and constantly invade crop areas (Nielsen et al., 2011; Josef et al., 2014). We also observed considerably high proportions of BMSB adults and nymphs on traps located close to the forested areas in Orchard B. This observation suggests that wild vegetation surrounding hazelnut orchards is possibly the

main source of the continuous influx of new stink bugs into the orchards. The lower numbers of BMSB observed on traps located next to the meadow and abandoned buildings suggest lower BMSB pressure coming from these directions (Figure 2). This was true at least until late in the season, when the numbers increased as the BMSB adults initiated movement in search for diapausing shelters. Buildings and other structures harboring overwintering BMSB populations are known to serve as an important source of overwintering adults invading orchards in the spring.

Our observations documented the presence of high numbers of BMSB adults and nymphs in hazelnut orchards located in the Samegrelo Region of Georgia. The changes in the seasonal distribution of the stink bugs within the orchards suggested a continuous influx of BMSB adults from surrounding vegetation into managed habitats. Multiseason observations are needed to better understand the biology of BMSB in Georgia and the Caucasus. The presence of BMSB adults and nymphs in orchards implies very high potential for the occurrence of economic injuries to nuts, consequently suggesting the necessity of the development of effective pest management strategies to mitigate the impact of this pest.

AcknowledgmentsThe authors would like to express gratitude to local farmer Gela Vekua for allowing them to conduct investigations in his orchards, to Demetre Lipartia from the Georgian Hazelnut Growers’ Association for providing meteorological data and for overall help during field works, and to the National Food Agency for technical support. Special thanks to USAID/REAP and its COP Dr. Louisa Namicheishvili for providing overall support. The investigation was conducted in the framework of a students’ project financed by Tbilisi State University and the USAID/REAP Georgia internship program.

Table 5. Comparison of the average numbers of BMSB adults and nymphs collected in traps at various traps locations. Data include captures from both orchards and all trap locations. Location Adults Nymphs 2–3 Nymphs 4–5 Nymphs totalHouse in 7.1 a 8.8 ab 1.3 ab 10.1 abHouse out 5.2 ab 11.4 a 1.9 a 13.3 aInside 3.7 b 1.5 c 0.9 b 2.4 cMeadow 3.8 b 4.4 bc 1.2 ab 5.6 bWoods 3.8 b 5.0 b 1.8 a 6.8 b


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