Minia J. of Agric. Res. & Develop. Vol. (36), No. 4, pp. 673-681, 2016
FACULTY OF AGRICULTURE
PRESENCE AND INFESTATION OF THE PARASITOID FLY, SENOTAINIA TRICUSPIS (MEIGEN) (DIPTERA, SARCOPHAGIDAE) OF HONEY BEES IN SULTANATE OF OMAN
Eshbah, H. M.(1), A. A. Mohamed(1) and Q. R. Al Shmmaki(2)
(1)Plant Prot. Dept., Fac. of Agric. Minia Univ. Egypt (2)Res. Stat. of honeybees at Rostq, Oman
Received: 4 December (2016) Accepted: 18 Jan. (2017)
ABSTRACT Survey was conducted in all governorates of Oman Sultanate to indicate the existence of the endoparasitoid fly (Senotainia tricuspis) of the honeybee Apis mellifera in Oman. Samples were taken from all provinces of the eleven governorates of the country and examined in Agriculture Research of honey bee Institute of Oman. The study showed that the S. tricuspis was found in five governorates out of the eleven governorates examined.This endoparasitoid was recorded in AL Batinah south, AL Batinah north, Al Dakhiliyah, Muscat and Ad Dhahirah. Samples from Dhofar, Al Wasta, Ashariqiya north, Ashariqiya south, Musandam and Al Buraimi were negative for infestation. We confirmed the presence of S. tricuspis in the mountain areas of Oman and diagnosed its existence for the first time in Oman, ) GBIF Global Biodiversity Information Facility, 2016). The presence of infestation in different provinces in each governorate was varied. The highest presence (100%) was recorded in Ad Dhahirah in the three provinces followed with Ad Dakhiliyah 87.5% from eight provinces, Al Batinah south, 66.7% from six provinces, Al Batinah north 66.7% from six provinces and the least presence was in Muscut governorate 16.7% from six provinces where the infestation was appeared in one province (Qurayyat). The first appearance of infestation was recorded in February and the last observation of infestation was recorded in June for all governorates. The highest peak of infestation was recorded in March. Therefore, awareness program will be very helpful for the beekeeper sector in these governorates. H. M. Eshbah, et al., 2016
Key words: Honey bee, Parasitoid, Oman
INTRODUCTION a first instar larva on the thorax of the The presence of parasitoid honey bee. Thereafter, the larva enters dipterans in the honey bee (Apis the body of the honey bee and mellifera L.) has long been recognized. develops, feeding on hemolymph and The first fly reported to cause wing muscles, until it kills its host in apimyiasis was Rondaniooestrus 2–4 days (Bedini, et al. 2006). At the apivorus (Villeneuve, 1916), that third instar, the last larval stadium, the diagnosed on the African continent larva exits from the body of the dead (Knutson, 1978). In Europe, the most host. Sometimes, it can also feed on well-known parasitoid dipterans that the body of the dead host as a attack the bee are belong to the scavenger. Then the larva enters the Borophaga incrassata species (Paillot soil for pupation. During the late et al., 1944) of which the most spring or summer, the adult fly commonly identified is Senotainia emerges 7–12 days after pupation and tricuspis (Meigen) whose biology has the new generation can go forward been studied by Simintzis (1949), with its own parasitic behavior. Those Giordani (1955), and Boiko (1958). S. larvae that pupate in late summer will tricuspis was distributed throughout undergo diapause until next spring central and southern Europe, and has when the adults emerge (Bailey & been reported in Tunisia, Northern Ball, 1991). Attacks can be repeated Africa (Mathis, 1957). In addition, it every 10 sec. during the sunset hours recorded in Portugal (Rocha and of the day. Each female has 600–700 Delgado, 1986), In Spain, high larvae in its uterus and thus has the infestation levels by Dipteran potential to kill hundreds of honey bee throughout 1940-1949 are well known (Bedini, et al., 2006). It causes in the island of Mallorca (Ramírez apimyiasis which can sometimes be Gómez, 1949). quite serious. This parasitoid is more Recently it is recognized that S. frequent in sunny and warm regions. tricuspis (Meigen) is an endoparasitoid Recently, Haddad et al. (2015) showed of the adult honeybee (Felicioli et al., that S. tricuspis was present in four out 2000); Morse and Flottum, (1997). S. of the seven countries sampled i.e. tricuspis has a length of 5–8 mm and Jordan, Algeria, Italy and was gray-black color. Morphologically it is recorded in Egypt for the first time. similar to a domestic fly; it is Whereas, samples from Iraq, Lebanon, characterized by a light strip between and Palestine were negative. They the reddish compound eyes (Bedini, et concluded the presence of S. tricuspis al., 2006). Females of S. tricuspis are in the southern and western areas of larviparous and attack forager honey the Mediterranean regions. Also, it is bees flying in front of the hive. When recorded in Mediterranean countries S. tricuspis reaches its host, it deposits (Spain, Rumania, Italy, Tunisia, etc.) - 674 -
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(Orantes and Fernández, 1996). This Removal of S. tricuspis larvae is pest has not been recorded before in necessary to avoid the behavior of Oman (Gbif, 2016). The aim of this cannibalism, which is known with S. work was to survey the prevalence and tricuspis larvae (Pinzauti and Santini, existence of S. tricuspis. (Diptera, 1995). The infestation rate among Sarcophagidae) and to estimate its samples was calculated according to infestation percent and potential the formula: (number of positive danger peaks in apiaries in Al Batinah samples/ total number of samples in south governorate through two each provinces) x100. Samples were successive years. taken from all provinces of all governorates and examined in the MATERIALS AND METHODS laboratory where the samples that Larvae of the honeybee parasitoid contained larvae of the fly were were reared and the adults were considered as positive samples. From identified in the Lander Institute fur the province Al Rustaq and from Al Bienkune Hoben Neuendorf (Prof. Dr. Batinah south, samples were taken Kaspar Bienfeld) as Senotainia weekly from January 2015 until tricuspis (Meigen). However, for the December 2016 to determine the monitoring of S. tricuspis, 732 samples percent of infestations and the peaks of were collected from 61 provinces that infestation through the year. The belong to eleven governorates in percent of infestation were determined February, March, April and June in eight apiaries. Samples of honey bee during 2015 season. Honeybee worker workers were collected from each samples were collected from three apiary from three randomly chosen randomly chosen hives of each apiary. hives. Each sample represented one Each sample represented one apiary apiary and contained 30 foraging bees and contained at least 30 foraging and transferred to laboratory. Bees bees. Also the same number was taken were examined individually in search from the house bees. Three hives / of dipteran larvae. The thorax of each province were selected according to bee was cut and pressing on the thorax the beekeepers complaints of area and the haemolymph was unexplained colony depopulation. The examined (Astolfi, 2001). The percent bees were kept in a closed glass jar of of infestation from each bee sample 500 ml volume. The jar was closed was then calculated according to the with a net to allow air exchange for the formula: (number of infested bees breathing of the bees and each Jar was which contain S. tricuspis larvae / furnished with a small amount of wet number of collected bees) x100. sandy soil. Then, the collected honey (Pinzauti and Santini, 1995). Statistical bees were observed for 72hr and analysis, L.S.D. between means eventual specimens of S. tricuspis (Keppel, 1991). larvae were counted and removed.
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RESULTS AND DISCUSSION temperature (40-55Cº), therefor, the The survey conducted in 61 biology of this parasite in Oman provinces during 2015 season should be studied in the future. indicated that infestations with the fly Statistical analysis as shown in were distributed throughout five Tables (2 and 3) showed that there regions in Oman out of the eleven were highly significant differences governorates examined. This between months infestation thus the endoparasite was recorded in Al infestation percent of this parasite Batinah south (in the provinces affected with weather factors in Oman. Nakhal, Wadi Al Maawil, AL Awabi No infestations were observed in all and AL Rustaq) , Al Batinah north (in samples taken from house bees as the provinces Sohar, Saham, Al shown in Table (1). This parasite was Kahaburah, As Suwayq), Al recorded in different countries Dakhiliyah (in the provinces Nizwa, worldwide (Pires et al. 2011) where Samail, Bahla, Adam, Al Hamra, Izki, the flies were distributed throughout and Bidbid), Muscat (in only one all Portuguese regions, Azores region province Qurayyat) and Ad Dhahirah presented the lowest rate of prevalence (in provinces Ibri, Yanqul and Dhank). (2.1%) and the higher prevalence was Samples from governorates Dhofar, Al found in July (30%) and in September Wusta, Ashariqiyah north, Ashariqiyah (31%). The same author indicated that south, Musandam and Al Buraimi increase of the fertilized females were negative for infestation in the two coinciding with the height of summer years of study, In Table (1) the highest (last ten days of July -The end of infestation rate (100%) was observed August) our results in March and in Ad Dhahirah Governorate where April. (Piazza, and Marinelli, 2000) infestation appeared in all samples, investigated the presence of the whereas, the Muscut governorate endoparasitoid fly (S. tricuspis) of presented the lowest rate of prevalence honey bees in Latium, Italy, during (16.7%) where infestation was 1997-99 in 5 provinces with 28 recorded in only one province through stations distributed in littoral and the two successive years. Considering inland zones. Their study showed that the month effect, the higher prevalence the presence of S. tricuspis was was found in March (90.27 and observed in all the apiaries situated in 86.35%) and in April (85.28 and littoral areas with significantly higher 80.81% of the positive samples) in percentage than the inland ones. In 2015 and 2016 seasons, respectively. addition, they indicated that S. The least infestation percentages were tricuspis prefers sunny places with appeared in May and February while sandy soil wet which are more suitable the infestation was disappeared in all for pupation and overwintering of the apiaries from June until January. This larvae. This parasitoid also appeared disappearance in months of summer on the African countries (Knutson, and autumn may be due to the high 1978). In Europe, the most commonly - 676 -
H. M. Eshbah, et al., 2016 flies identified was tricuspis (Meigen), 1986), where it appeared during 1841, whose biology has been studied September, in contrast to France, by Simintzis (1949), Giordani (1955), where the highest levels of and Boiko (1958). Also, S. tricuspis is parasitization occur during August distributed throughout central and (Simintzis and Fiasson, 1951). The southern Europe, and had been appearance of the fly differed from one reported in Tunisia, Northern Africa country to other thus it should be study (Mathis, 1957). It was also recorded in the effect of weather factors on the Portugal (Rocha and Mira Delgado, infestation percent. Table (1): Survey of the parasitoid fly Senotainia tricuspis (Meigen) infesting honeybee (Apis mellifera yemenitica) in Sultanate of Oman during 2015 season. Infestation in Infested Governorate Provinces House bees Foraging bees provinces % Nakhal - + 66.7 Al Batinah Wadi Al Maawil - + South Al Awabi - + Al Musaanaah - - Barka - - Al Rustaq - + Dhofar Salalah - - 0 Taqah - - Mirbat - - Thumarit - - Sadha - - Rakhyut - - Dhalkut - - Muqshin - - Shaalim an the - - Halaniyat Al Mazyona - - Al Wusta Haima - - 0 Duqim - - Mahout - - Aljazar - - Ashariqiyah Ibra - - 0 north Al Mudhaibi - - Bidiyah - - Wadi Bani Khled - - Dema WaThaieen - - AlQabil - -
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Table (1): Continue Infestation in Infested provinces Governorate Provinces House Foraging % bees bees Ashariqiyah Masirah - - 0 South Sur - - JalanBani Bu Ali - - AlKamil Wal - - Wafi Musandam Khassab - - 0 Bukha - - Daba AlBayah - - Madha - - Muscat Muscat - - 16.7 Muttrah - - Bawshar - - Seeb - - AlAmerat - - Qurayyat - + Ad Dakhiliyah Nizwa - + 87.5 Samail - + Bahla - + Adam - + Al Hamra - + Manah - - Izki - + Bidbid - + Ad Dhahirah Ibri - + 100 Yanqul - + Dhank - + Al Bhatinah Sohar - + 66.7 North Shinas - - Liwa - - Saham - + Al Kahaburah - + As Suwayq - + AlBuraimi Al Buraimi - - 0 Mahdah - - Al Sinaina - -
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Table (2): Infestation percentages of parasitoid fly (Senotainia tricuspis) in south Al Batinah governorate, Sultanate of Oman during 2015 season. Apiary Infestation % *LSD No Jan. Feb. Mar. Apr. May Jun. 1 0 74.03 93.98 88.96 76.08 0 9.97 2 0 79.23 87.68 85.83 62.96 0 9.97 3 0 66.55 95.77 89.21 73.39 0 9.97 4 0 59.19 93.33 90.57 64.93 0 9.97 5 0 59.99 96.66 78.61 61.35 0 9.97 6 0 62.94 91.26 88.40 72.08 0 9.97 7 0 61.54 86.87 82.15 52.29 0 9.97 8 0 79.04 76.66 78.55 56.26 0 9.97 Mean 67.81 + 90.27 + 85.28 + 64.91 + 8.41 6.53 4.87 8.44 *L.S.D. Least significant differences between means.
Table (3): Infestation percentages of parasitoid fly (Senotainia tricuspis) in south Al Batinah governorate, Sultanate of Oman during 2016 season. Apiary Infestation % *LSD No Jan. Feb. Mar. Apr. May Jun. 1 0 77.94 85.69 75.63 82.64 0 24.68 2 0 88.33 97.5 90.5 33.39 0 24.68 3 0 63.60 94.16 70.11 75 0 24.68 4 0 18.26 60.41 66.74 20.83 0 24.68 5 0 64.49 95.83 88.33 31.66 0 24.68 6 0 44.91 84.01 86.90 62.42 0 24.68 7 0 78.90 85.83 81.66 73.30 0 24.68 8 0 64.49 87.44 86.66 74.04 0 24.68 Mean 62.61 + 86.35 + 80.81 + 56.66 + 22.2 11.4 8.95 24.12 *L.S.D. Least significant differences between means.
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Boiko, A.K. (1958). Senotaniosis Predators, and Diseases (Roger (apimyiasis) of bees. Proc. XVII A, Morse, ed.). Cornell Int. Beekeeping Congr. 24-25. University Press, Ithaca, NY, Felicioli, A.; Franceschini, S. and USA and London, UK, 128-137. Pinzauti, M. (2000). The agony Mathis, M. (1957). Un diptère parasite of a honey bee colony parasitized des abeilles adultes. Senotainia by the Sarcophagid fly Senotainia tricuspis (Meigen) identifié pour tricuspis: Temperature and la première fois en Tunisie. humidity variations. In Archiv Instit Pasteur Tunis 34, Proceedings of the XXI 107-113. International Congress of Morse, R. A. and Flottum, K. (1997). Entomology, Foz de Iguassu`, Honey bee pests, predators and Brasil, (20–26 August). vol. 1, p. diseases (3rd ed.). Medina, OH: 244. The A.I. Root Company. Gbif (2016). Global Biodiversity Orantes B. and Fernández, P. (1996). Information Facility. Data about Prevalence of parasitization by Oman. Diptera in Apis mellifera L. in http://www.gbif.org/country/ southern Spain. Apidology 27, Giordani, G. (1955). Contributo alla 467-471 conoscenza della „„Senotainia Paillot, A.; Kirkor, S. and tricuspis‟‟ (Meigan)., Dittero Granger, A.M. (1944). Sarcofagide, endoparassita L‟abeilleanatomie-maladies- dell‟Ape domestica. Boll. Inst. enemis. 2nd edn, G Patissier, Ent. Bologna, 21, 61-84. Trevoux, France. Haddad, N.; Adjlane, N.; Loucif-Ayad, Piazza, M. G. and Marinelli, E. (2000). W., Shebl, M. A.; Saba, M.; Investigation on the presence in Albaba, I.; Givsti, M. and Latium of Senotainia Felicioli, A. (2015). Presence and tricuspis (Meigen) (Diptera infestation rate of Senotainia Sarcophagidae), endoparasitoid tricuspis (Meigen) (Diptera, of Apis mellifera L. Redia, Sarcophagidae) on honey bees in 83:111-122. the Mediterranean Pinzauti, M. and Santini, L. (1995). On Region. Journal of Apicultural the “apymiasis” caused by Research, 54(2), 121-122. Senotainia tricuspis (Meigen) Keppel, G. (1991). Design and (Diptera, Sarcophagidae) in analysis: A researcher's handbook central Italy. In Proceedings of 3rd ed. Englewood CLIFB, NJ, XXXIVth International MS. Prentice. Hall Inc. Design Apicultural Congress, Lousanne, and analysis handbook 3rd ed. Switzerland. (Reprinted from xiii: 594 pp. L‟Apicoltore Moderno, 86, 179– Knutson, L. (1978). Insects: Diptera 183). (Flies). In: Honey bee Pests, - 680 -
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Pires, S., Cadavez, V. and Valério, M. Simintzis, G. (1949). Les larves de J. (2011). Prevalence and dipteres du genre Senotainia geographical distribution of tricuspis, parasites thoraciques Senotainia tricuspis internes de l‟abeille adulte. Revue (Meigen). Diagnosis and Control Française d „Apiculture, 12, 13- of Bee Diseases, pp. 11-11. 16. Ramírez Gómez, C. (1949). Nota sobre Simintzis, G. and Fiasson, S. (1951). el hallazgo de Acarapis woodi en Les myases des abeilles en la isla de Mallorca. Boletín de la France. Rev Med Veter, 102, Real Sociedad Española de 351-361. Historia Natural. Sección Villeneuve, J. (1916). A new species Geológica, (47), 611-618. of Tachino-Oestrid from South Rocha, M.T. and Delgado, L.M. Africa (Diptera). (1986) Senotainia tricuspis em Ann. South Afr. Mus. 15, 465-468. (in Portugal. Rep Trab LNIV, 18, 69- Knutson, 1978). 70.
تواجد وإصابة نحل العسل بالذبابة المتطفلة Senotainia tricuspis (Meigen) (Diptera, Sarcophagidae) في سلطنه عمان
حصافٙ دمحم عشبة )1(, عبذ انضالو إَٔس دمحم)1(, قاصى بٍ ساشذ بٍ حًٛذ انشًاخٙ)2(
)1( قضى ٔقاٚة انُبات, كهٛة انزساعة, جايعة انًُٛأ يصش )2( يحطة بحٕخ انُحم, صهطُة عًاٌ
جى عًم حصش نهزبابة انًحطفهة (Senotainia tricusp) عهٗ َحلم انعضلم فلٙ يُاحلم يحاف لات صهطُة عًاٌ. جى اخز انعُٛات يٍ جًٛع انٕالٚات نكم يحاف ة يٍ انًحاف ات اإلحذٖ عشش ٔفحصث انعُٛات فٙ يخحبش بحٕخ انُحم بضهطُة عًاٌ ٔبفحص انعُٛات اصحخشجث ٚشقات انزبابة يلٍ اجضلاو انُحلم انًصلا حٛد جى جشبٛحٓا نهٕصٕل نهطٕس انكايم ٔانز٘ جى اسصانة نألصحار انذكحٕس كاصبش بُٛفٛهذ فٙ يعٓذ Bienkune Hoben Neuendorf ٔانز٘ قشس االصى انعهSenotainia tricuspis (Meigen)ًٙ. ٔضحث انذساصة جٕاجذ ْزِ انزبابة فٙ خًش يحاف ات يٍ اإلحذٖ عشش يحاف ة انحٙ جى فحصلٓا ْٙٔ جُٕ انباطُة – شًال انباطُة – انذاخهّٛ– يضقط –ان اْشِ. ٔنقذ أضحث انذساصة ٔجٕد ْلزِ انزبابلة انًحطفهة فٙ انًُاطق انحجشٚة فٙ عًاٌ حٛد جلى جضلجٛهٓا لٔل يلشو. ٔنقلذ جباُٚلث اإلصلابة بلٍٛ ٔالٚلات كلم يحاف للة حٛللد كاَللث أعهللٗ َضللبة صللابة )111%( فللٙ انٕالٚللات انرالذللة نًحاف للة ان للاْشِ ٔجبعٓللا ٔالٚللات انذاخهّٛ بُضبة 8..5% ٔقذ صجهث فٛٓا صابة فٙ ذالخ ٔالٚات يٍ أسبع ٔالٚات يٍ انًحاف ة. أيا يحاف حٙ جُٕ انباطُة ٔشًال انباطُة قذ صجهث اإلصابة فٙ أسبع ٔالٚات يٍ صحة ٔالٚات نكم يحاف ة بُضلبة صلابة ....%.ٔكاَث اقم َضبة صابة فٙ ٔالٚات يحاف ة يضقط حٛلد بهتلث ...1% ٔكاَلث اإلصلابة فلٙ ٔالٚلّ ٔاحللذ فقللط يللٍ صللث ٔالٚللات ْٔللٕ ٔالٚللة قشٚللات. ٔنقللذ صللجهث بذاٚللة اإلصللابة انفعهٛللّ فللٙ انٕالٚللات انحابعللّ نهًحاف ات انًزكٕسِ اعالِ ابحذءا يٍ شٓش فبشاٚلش ٔاصلحًشت ححلٗ َٓاٚلة َٕٛٚلٕ ٔرنلم فلٙ جًٛلع انًحاف لات ٔكاَث أعهٗ صابة فٙ شٓش ياسس. ٔبانحانٙ جٕعٛة انُحانٍٛ فٙ ْزِ انٕالٚات ضشٔس٘ جذا. انكهًات انًفحاحٛة: َحم انعضم - طفٛم – صهطُّ عًاٌ
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