151 Sarkaut Hussein Muhammed Bull. Iraq nat. Hist. Mus. (2020) 16 (2):151-160. https://doi.org/10.26842/binhm.7.2020.16.2.0151 SEASONAL FLUCTUATION OF STINK BUG MUSTHA SPINULOSA (LEFEBVRE, 1831) (HEMIPTERA, PENTATOMIDAE) ON SOME TREES IN ERBIL CITY Sarkaut Hussein Muhammed Department of Biology, College of Science, University of Salahaddein, Erbil, Iraq Corresponding author e-mail: sarkaut.muhammed@su.edu.krd Received Date: 19 July 2020, Accepted Date: 19 August 2020, Published Date: 21 December 2020 ABSTRACT Phytophagous stink bugs (Hemiptera, Pentatomidae) are economically important insect pests of fruit, vegetable, nut and field crops. This study was carried out during the season of 2013 in orchards within Erbil city, to follow the stink bug Mustha spinulosa (Lefebvre, 1831) seasonal fluctuation on some fruit trees: olive, plum, apricot, pear, apple and almond. The stink bug reaches its maximum abundance throughout the second week of August (38.2/tree) coinciding with mean temperature and relative humidity of 33.40C and 28.14% respectively, and the highest total mean of the number of the insect was recorded on the olive trees (181.8/tree). The study reveals that the stink bug attacked 22 trees (fruit and forest) while it has not attack any herbal plant. Key words: Fruit trees, Mustha spinulosa, Pentatomidae, Seasonal fluctuation, Stink bug. INTRODUCTION The stink bugs belong to the superfamily Pentatomoidea, family Pentatomidae of the order Hemiptera, and suborder Heteroptera (Borror et al, 1989). They have a single generation annually and in almost all species the adult is the overwintering stage (Dolling, 1991). The Family is very important from an agricultural point of view; they feed by inserting their stylets into the food source to suck up nutrients so they cause injury to plant tissue, and consequently the plant wilts (Panizzi et al., 2000). Because some of them feed on several plant species of economic importance they are regarded as major pests, (Panizzi and Grazia, 2001). In Erbil city, many kinds of fruit trees are grown due to the suitability of environmental conditions, such as trees of plum, apricot, apple, olive, almond and pear (RSO, 2008). These trees are infested with many sap-sucking insects, the stink bugs are one of the common insects. The tree gets damaged due to sucking juices by these insects, later it becomes weak and vulnerable to other diseases (Muhammed, 1994). 152 Seasonal fluctuation of stink bug Mustha spinulosa Review of literature shows poor information about the stink bug Mustha spinulosa (Lefebvre, 1831), in which most of the previous data focused only on host recording. Kirkaldy (1909) demonstrated in his catalogue that the genus Mustha Amyot & Serville, 1834 had six species almost all from Persia (Iran); it is also recorded from many other areas such as Iraq and Pakistan, while Stichel (1960) listed five species under Mustha from Palaearctic region. Puchkov (1965) in his revising Halyini, keyed five genera under tribe Halyini i.e. Mustha, Apodiphus, Iskenderia, Halys and Carcenoplistus from Russia. According to Ahmad and Kamaluddin (1984) Mustha apparently is a Palaearctic genus and has been reported from Yugoslavia, Albania, Bulgaria, Greece, Syria, Cyprus, Iraq, South Russia, Iran, and Turkey. Hoberlandt (1995) identified seven species of Mustha in Iran. Bolu et al. (2005) in his study revealed that M. longispinis Reuter, 1890 was the most important species among insects that attacks almond trees in Turkey while Ozgen et al. (2005) recorded that M. longispinis attacked pistachio trees, also they concluded that this species could be considered as one of the important pests among other pentatomid bugs species that should be considered in the future. In another study done in two provinces of Turkey, Tezcan and Onder (2003) found that M. spinulosa was one of the injurious phytophagous insects that attacked cherry trees, while Orçan and Kivan (2017) found only one specimen from this insect on apple trees. Linnavouri (2008) in his study in northern Iran found M. spinulosa in hilly forests on deciduous trees such as Quercus, Prunus, Crataegus and Cupressus. Muhammed and Al-Iraqi (2010) recorded numerous fruit and non-fruit trees as a host for this insect in Erbil city- Iraq. In this perspective, the present paper aims to clarify the seasonal fluctuation of M. spinulosa on some fruit trees in Erbil city during the growing season 2013, and so this represents the first study on this genus in our area. MATERIALS AND METHODS Survey Many orchards and parks which were planted with both forest and fruit trees within Erbil city have been visited weekly; whole trees (both fruit and forest) were examined by visual searches to determine the host plants of stink bug M. spinulosa. The insect was identified by Mr. Linnavouri (Personal contact) while the hosts were identified in Herbarium section at the College of Science, University of Salahaddein-Erbil. Seasonal fluctuation The population of M. spinulosa, on fruit trees was monitored in orchards planted within Erbil city, from January till December 2013; a weekly visiting through direct visual inspection of M. spinulosa on the infested trees under the study was done, from each orchard five trees similar in size and age were selected and the numbers of adults were recorded periodically, with calculating the mean number of bugs in specimen/week, for each type of olive, plum, apricot, pear, apple and almond taking into consideration the prevention the spraying of pesticides during the period of study. The daily average of temperature and relative humidity was obtained from the meteorological station of Erbil city. 153 Sarkaut Hussein Muhammed RESULTS AND DISCUSSION Survey of Host Plants The survey shows that the stink bug M. spinulosa feed on several host plants from forest and fruit trees. The stink bugs lay their eggs on the pine trees, after hatching the first nymph instar stays on the same tree. After 1st molting the nymph can crawl through branches to other trees which are planting near the pines such as Cupressus sp., Casuarina sp, and Eucalyptus sp.; when the adults appear they fly to other hosts which are mentioned in the Table (1), so as to start feeding on sap cells from the stems. The insect does not migrate to other places for hibernation like other stink bugs, but stay in the same environment. Table (1): Determination of fruit and forest trees attached by stink bug M. spinulosa during season 2013 in Erbil city orchards and parks. Host plants Family Feeding stage Fruit trees Mulberry Moraceae Adult Olive Oleaceae Adult Plum Rosaceae Adult Apricot Rosaceae Adult Apple Rosaceae Adult Almond Rosaceae Adult Pear Rosaceae Adult Fig Moraceae Adult Loquat Rosaceae Adult Walnut Juglandaceae Adult Sumac Anacardiaceae Adult Forest trees Cypress Cupressaceae Adult, nymph Pine Pinaceae Adult, nymph She-oaks Casuarinaceae Adult, nymph Blue gum Myrtaceae Adult, nymph Oak Fagaceae Adult Black locust Fabaceae Adult Arborvitae Cupressaceae Adult Neem Meliaceae Adult Poplar Salicaceae Adult Oriental plane Platanaceae Adult Princess tree Paulowniaceae Adult The seasonal fluctuation on fruit trees The data in Table (2) revealed that the stink bug M. Spinulosa began to appear on olive trees from the first week of May with a low number (4 individuals/trees) coinciding with the mean temperature and relative humidity of 24.36C and 42.71% respectively. Afterwards the maximum number of the insect was recorded during the first week of June (25.6 individuals/trees) under the average temperature 30.60C and relative humidity 38.86. Then variable numbers are found till they disappeared during the first week of October. 154 Seasonal fluctuation of stink bug Mustha spinulosa Table (2): Mean number of stink bug M. spinulosa population on the studied fruit trees during season 2013 in Erbil city orchard. Date Olive Plum Apricot Pear Apple Almond Total Mean 07/05/2013 04.0 2.2 01.6 0 0 0 07.8 14/05/2013 09.4 2.4 03.4 0 0 0 15.2 21/05/2013 11.0 2.8 03.2 0 0 0 17.0 28/05/2013 19.4 2.2 02.4 1.0 0.6 0 25.6 04/06/2013 25.6 1.6 01.0 0.6 0.8 0 29.6 11/06/2013 09.0 2.4 01.4 1.0 1.0 0 14.8 18/06/2013 08.2 2.8 01.0 0.6 0.8 0 13.4 25/06/2013 05.2 3.6 02.0 0.6 0.4 0 11.8 02/07/2013 04.4 2.4 01.8 0.8 0.6 0 10.0 09/07/2013 04.0 2.0 02.2 0.6 1.0 0 09.8 16/07/2013 07.0 2.0 05.8 1.0 1.0 0 16.8 23/07/2013 10.0 1.8 06.4 1.6 1.2 1.4 22.4 30/07/2013 08.6 6.2 07.8 2.6 2.0 2.4 29.6 06/08/2013 12.6 7.0 08.0 2.4 2.4 4.0 36.4 13/08/2013 14.2 7.4 09.0 2.2 2.4 3.0 38.2 20/08/2013 11.0 8.8 09.4 2.6 2.0 2.8 36.6 27/08/2013 06.6 8.4 09.6 2.2 2.0 3.4 32.2 03/09/2013 04.2 6.2 10.2 4.0 1.6 3.8 30.0 10/09/2013 04.0 8.0 07.0 5.0 2.6 5.8 32.4 17/09/2013 01.8 2.6 03.4 3.4 1 4.6 16.8 24/09/2013 01.6 0 05.6 3.0 0 4.0 14.2 01/10/2013 0 0 04.0 2.0 0 2.4 08.4 08/10/2013 0 0 04.0 1.8 0 2.0 07.8 15/10/2013 0 0 0 1.0 0 0 01.0 22/10/2013 0 0 0 0 0 0 0 Total 181.8 82.8 110.2 40 23.4 39.6 477.8 The individuals on the plum trees were represented by relatively low numbers during the first week of May (2.2 individuals/trees) coinciding with the mean temperature and relative humidity of 24.36C and 42.71% respectively. Thereafter the number increased to reach the maximum during the third week of August (8.8 individuals/trees) under the average 155 Sarkaut Hussein Muhammed temperature 34.39 C and relative humidity 28.00%. Then the number decreased gradually and disappeared completely through the fourth week of September. On the other hand, the results indicated that the insects presence on apricot trees started at the first week of May (1.6 individuals/trees) coinciding with the mean temperature and relative humidity of 23.36C and 42.71% respectively. Thereafter the numbers increased to reach the maximum during the first week of September (10.2 individuals/trees) under the average of temperature 35.06C and relative humidity 28.71%. Then the number which it decreased and ended completely through the second week of September. The results also showed that M. spinulosa began to appear on pear trees from the fourth week of May (1.0 individual/trees) coinciding with the mean temperature and relative humidity of 33.39C and 32.63% respectively. After that the numbers varied and reached the maximum during the second week of September (5.0 individuals/trees) under the average of temperature 33.20C and relative humidity 30.14%. Then the number which it decreased gradually and vanished completely through the third week of October. The results revealed that M. spinulosa began to appear on apple trees from the fourth week of the June (0.6 individual/trees) coinciding with the mean temperature and relative humidity of 33.39C and 32.63% respectively. After that the numbers fluctuated and reached the maximum during the second week of September (2.6 individuals/trees) under the average of temperature 33.20C and relative humidity 30.14%, and after one week, the insects completely disappeared the fourth week of September. The infestation of the almond trees was delayed, the stink bug appeared to attack trees at the third week of July (1.4 individuals/trees) coinciding with the mean temperature and relative humidity of 34.79C and 30.13% respectively. Later, the numbers increased to reach the maximum during the second week of September (5.8 individuals/trees), under the average of temperature 33.20C and relative humidity 30.14%. Then the number decreased gradually and went out of sight during the second week of October. Panizzi and Grazia (2001) found that the relationship between the pentatomids and their hosts depended on several factors involving: the life history of pentatomids, characteristics of the plant, and the abundant and their adaptation to the weather conditions. Additionally, Mouraa et al. (2017) mentioned that, phytophagous insects might choose host plants depending on the conditions that would enhance offspring performance. However, some insect species may also select plants based on attributes that enhance their performance regardless of the consequences for offspring survival. The host selection by phytophagous insects is often explained by the optimal oviposition theory. This hypothesis states that females should select host plants based on their capacity to provide suitable resources for offspring development, such as food and shelter (Gripenberg et al. 2010). Low densities of stink bug on apple trees suggest that it is an unsuitable developmental host (Nielsen and Hamilton, 2009). The obtained data in Table (1) showed that the highest total number of the insects during the growing season was noticed on the olive trees (181.8 individuals/trees), followed by the 156 Seasonal fluctuation of stink bug Mustha spinulosa apricot trees (110.2 individuals/trees), while apple trees showed lowest numbers of insects (23.2 individuals/trees), and the number of insects oscillated along with seasonal growth on the fruit trees in the orchard of Erbil city. The olive tree is a drought -tolerant species which can have an exceptionally long life-span. It is limited only by frost and high temperatures and to a lesser extent by soil fertility; additionally, olive trees have a huge branching which can used by the insect for hiding. Sap cells may have a role in attracting the insects (McGh ee, 1997). The highest number of the insects was recorded in the second week of August which was 38.2 individuals under the average of temperature 33.40C and relative humidity 28.14% and the lowest number was recorded in the second week of October which was (1.0 individuals/trees) under the average of temperature 27.39C and relative humidity 32.00%. Based on the total mean numbers of M. spinulosa, it was found that the insect appearance on the fruit trees start from the first week of May (7.8 individuals) and continues along with June, July, August and September, and it will end in the second week of October. On the other hand the results indicated that the insect population reached their maximum numbers during the second week of August (38.2 individuals), coinciding with the mean temperature and relative humidity of 33.40C and 28.14% respectively. Thereafter the stink bugs disappear and migrate to forest trees in the third week of October, coinciding with the mean temperature and relative humidity of 19.58C and 34.75% respectively (Diag. 1). According to Penn State ( 2006), the numbers of stink bugs present in trees at any given time during the season are greatly dependent on the weather, the surrounding vegetation (alternate host plants), the orchard history and chemical composition of sap cell which is changed according to the environmental condition and other factors. 157 Sarkaut Hussein Muhammed Diagram (1): Total mean number of M. spinulosa population on the studied fruit trees at Erbil city with temperature and relative humidity during season 2013. LITERATURE CITED Ahmad, I. and Kamaluddin, S. 1984. Re-description of Mustha spinosulus and M. spinosus (Hemiptera: Pentatominae: Halyini) from Pakistan and their zoogeography and relationships. Oriental Insects, 18 (1): 187-194. Bolu, H., Ozgen, Y. and Fent, M. 2005. The investigations on Almond Pentatomidae (Heteroptera) fauna in Diyarbakir, Elazyo and Mardin Province. Available at: www.tarimdrgrisi.yyu.edu.tr Borror, D. J., Triplehorn, C. A. and Johnson, N. F. 1989. An introduction to the study of insects. 6th ed. Philadelphia: Saunders College Publishing, 340 pp. Dolling, W. R. 1991. The Hemiptera. Oxford: Oxford University press, 274 pp. Gripenberg, S., Mayhew, P. J. Parnell, M. and Roslin, R. 2010. A meta-analysis of preference–performance relationships in phytophagous insects. Ecology Letters. 13:383–393. (Cited in Mouraa et al. (2017)) Hoberlandt, L. 1995. Results of the entomological expeditions to Iran (Heteroptera, Pentatomidae). Acta entomologica Musei Nationalis Pragae, 44: 216-233. (Cited in Memon (2002)). 158 Seasonal fluctuation of stink bug Mustha spinulosa Kirkaldy, G. W. 1909. Catalogue of the Hemiptera (Heteroptera) with biological and anatomical references, lists of food plants and parasites, etc. Prefaced by a discussion on nomenclature and an analytical table of families, p182-205. (Cited in Memon, (2002)). Linnavouri, E. R. 2008. Studies on the Acanthosomatidae, Scutelleridae and Pentatomidae (Heteroptera) of Gilan and the adjacent provinces in northern Iran. Acta Entomologica Musei Nationalis Pragae, 48 (1): 1-21. McGhee, P. S. 1997. Biology, ecology, and monitoring of the Pentatomidae (Heteroptera) species complex associated with tree fruit production in Washington. M.Sc. thesis. Washington State University, Department of Entomology, 70 pp. Memon, N. 2002. A revision of the berry bugs (Heteroptera: Pentatomoidea: Halyini) of Indo- Pakistan subcontinent with special reference to cladistic analysis of Halyine genera . Ph. D thesis. University of Karachi, 409 pp. Mouraa, R. R., Ribeiroa, P. V. A., Pereiraa, B. G., Queroa, A., Carvalhoa, R. L. and Oliveirab, D. C. 2017. Food, shelter or competitors? Overlapping of life stages and host plant selection in a Neotropical stink bug species. Journal of Plant Interactions, 12(1): 560-566. Muhammed, S. H. 1994. Study of population density of some sap sucking insects on some fruit trees in Erbil. M. Sc. thesis, College of Education, University of Salahaddein- Erbil. Muhammed, S. H. and Al-Iraqi, R. A. 2010. Occurrence and record of stink bug Apodiphus amygdali (Germar) (Hemiptera: Pentatomidae) on some fruit trees in certain localities of Erbil Governorate. Kurdistan 3rd conference on Biological Sciences, 4-6 May, Dohuk University. Nielsen, A. l. and Hamilton, G. C. 2009. Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. Journal of Economic Entomology, 102:1133-1140. Orçan, Ö. S. and Kivan, M. 2017. Pentatomidae (Hemiptera) species on fruit trees in Saray district of Tekirdag, Turkey. Global Journal of Advanced Research, 4(10): 293-300. Ozgen, I., Gozuacik, C., Karsavuran, Y. and Fent, M. 2005. Investigations on the pentatomidae (Heteroptera) fauna in apricot, cherry, olive and pistachio plantations in east and southeastern Anatolia region (Turkey). The Journal of Ege University, Faculty of Agriculture, 42 (2): 35-43. Panizzi, A. R. and Grazia, J. 2001. Stink bugs (Heteroptera, Pentatomidae) and an unique host plant in the Brazilian subtropics. Iheringia Série Zoologia, 90: 21-35. 159 Sarkaut Hussein Muhammed Panizzi, A. R., McPherson, J. E., James, D. G., Javahery, M. and McPherson, R. M. 2000. Stink bugs (Pentatomidae). P 421-474. In: Scheafer, C. W. and Pannizi, A. R., (eds) Heteroptera of Economic Importance. Boca Raton: CRC Press, 828 pp. Penn State. 2006. Fruit production for the home gardener: a comprehensive guide. College of Agricultural Science, the Pennsylvania State University, USA, 187 pp. Puchkov, V. G. 1965. Shield-bug of central Asia (Hemiptera, Pentatomidae). Inst. Biol. Frunze Acad. Sc. Kirgiskoi, SSR. (In Russian, cited in Memon, (2002)). RSO (Regional Statistics Organizing). 2008. A survey of different fruit trees in Kurdistan Region. Report prepared by Ministry of Planning (agricultural sector), Kurdistan region. Iraq. Stichel, W. 1960. Illustrierte Bestimmungstabellen der wanzen. II. Europa (Hemiptera- Heteroptera Europae). Vol.3. Berlin-Hermsdorf, 428 pp. Tezcan, S. and Önder, F. 2003. Faunistical studies in ecological cherry orchards in Izmir and Manisa provinces of Turkey: an evaluation on the species of Heteroptera. Anadolu Journal, 13 (1): 124-131. 160 Seasonal fluctuation of stink bug Mustha spinulosa Bull. Iraq nat. Hist. Mus. (2020) 16 (2): 151-160. التباين الموسمي لحشرة البق النتن Mustha spinulosa (Lefebvre, 1831) (Hemiptera, Pentatomidae) نة اربيلعلى بعض االشجار في مدي سركوت حسين محمد قسم علوم الحياة،كلية العلوم، جامعة صالح الدين، اربيل، العراق 21/12/2020، تأريخ النشر: 19/08/2020، تأريخ القبول: 19/07/2020تأريخ االستالم: صةالـخال مققن Hemipteraرتبققة Pentatomidaeالبققا النققلن الققد يعققوئ القق عا لققة غديققة اللققي تكققين كققل مققن اكققوار الوواكقق ال ققر ات الحشققرات اباتيققة الل المكسققرات افقققاىة القق محاصقققيل حتليققةا اجريقققي بققدي الدراسقققة ىققي بسقققاتين ذلك لدراسة اللباين الموسمي للبا النقلن 2013 حدا ا مدينة اربيل خالل عام M. spinulosa ااقققوان مقققن اكقققوار الواكوقققةا الصيلقققو ا جقققا 6علققق المشمش العرموط اللواح اللوزا بلغققي ذر ة اشققاط البققا النققلن خققالل تواجققدي علقق اكققوار الواكوققة ىققي الحتققل كورة( باللصامن مع معد ت ئرجقات /2ا38خالل ا سبون الثااي من كور اب ) علقق اللققوالي ، اعلقق اسققبة % 14ا28 40ا33الحققرارة الرطوبققة النسققبية كورة(ا/8ا181للحشرة تم تسويلوا عل اكوارالصيلو ) عا ل )اكقوار ىاكوقة بابقات( ، 22اظورت الدراسة ا الحشرة تلغدى عل اعشبي لم تسول تغدية الحشرة عل ا ابات تأريخ الاستلام: 19/07/2020، تأريخ القبول: 19/08/2020، تأريخ النشر: 21/12/2020