Life cycle of the Syrian bean-caper hawk moth, Hyles zygophylli (Lepidoptera: Sphingidae), and identification of its parasitoids in Urmia region, Iran

Document Type : Paper, Persian

Authors

1 Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia - Iran

2 Department of Plant Protection- Faculty of Agriculture- Urmia University- Urmia / Iran

3 Plant Protection Research Department, East-Azarbaijan Agricultural and Natural Resources Research & Education Center, AREEO, Tabriz, Iran.

Abstract

The Syrian bean-caper hawk moth, Hyles zygophylli L., is distributed in the eastern Palaearctic region and feeds on the leaves of the Syrian bean caper, Zygophyllum fabago L. In order to study the life history traits and its parasitoids, continuous rearing was conducted in field and laboratory conditions. The results showed that H. zygophylli completed four generations within the growing season and hibernate as pupal stage in the soil at a depth of 2 to 6 cm. The annual life cycle of the species begins in late April with the emergence of adults from overwintering pupae and ends in early October with the pupation of fourth-generation larvae. Adult hawk moths 2-3 days after emergence mates and begin laying eggs in irregular shape on the stems and underside of leaves. They are spherical shape, light green and 1.1 ± 0.1 mm in diameter. Depends on daily temperature, the incubation period takes 3-5days. The larval development time takes 18-25 days and pupal stage lasted 12-16 days. Laval development were completed in five larval instars. The maximum length (in rest position), head capsule, and weight of completely developed larvae were 6.6-6.9 mm, 4.9 mm, and 3.8-4.9 gr, respectively. The larvae and pupa of H. zygophylli were parasitized by two species of tachinid and chalcid flies namely, Masicera sphingivora (R.-D.), Tachina praeceps Meigen and Proconura barbara Masi in Urmia region. The association of parasitoids with H. zygophylli are reported for the first time.

Keywords


Abdurahmanov, A. G. (1999) Species and some biological features of hawk moths (Macrojugata. Metaheterocera. Sphingidae. Lepidoptera.) of Daghestan republic. Ecology of Daghestan. 1,132-142. [In Russian]
Agosta, S. J. & Janzen, D. H. (2005) Body size distributions of large Costa Rican dry forest moths & the underlying relationship between plant & pollinator morphology. Oikos 108, 183–193.
Akhyani, K. (1992) Flora of Iran, No.7: Zygophyllaceae. Tehran: Research Institute of Forests & Rangelands. 52 pp.
Akila, G. Djamil, K., Samira, Z. & Sadia, B. (2014) Zygophyllum gaetulum aqueous extract protects against diabetic dyslipidemia & attenuates liver & kidney oxidative damage in streptozotocin induced-diabetic rats. International Journal of Pharmaceutical Science & Research 5(11), 4709 - 4717.
Akkuzu, E. Ayberk, H. & Inac, S. (2007) Hawk moths (Lepidoptera: Sphingidae) of Turkey and their zoogeographical distribution. Journal of Environmental Biology 28(4), 723-30.
Amini-Chermahini, F. Ebrahimi, M. Farajpour, M. & Bordbar, Z. T. (2014) Karyotype analysis and new chromosome number reports in Zygophyllum species. Caryologia. 67(4), 321-324.
Barzegar, R. Safaei, H. R. Nemati. Z. Ketabchi, S. & Talebi, E. (2018) Green synthesis of silver nanoparticles using Zygophyllum oatarense Hadidileaf extract & evaluation of their antifungal activities. Journal of Applied Pharmaceutical Science 8(3), 168-171.
Batra, S. W. T. (1984) Establishment of Hyles euphorbiae (L.) (Lepidoptera; Sphingidae) in the United States for the control of weedy spurges Euphorbia esula L. & E. cyparissias L. Journal of the New York Entomological Society 91, 304–311.
Beck, J. Kitching, I. J. & Linsenmair, K. E. (2006b) Effects of habitat disturbance can be subtle yet significant: biodiversity of hawkmoth-assemblages (Lepidoptera: Sphingidae) in Southeast-Asia. Biodiversity & Conservation 15, 465–486.
Beck, J. Kitching, I. J. & Linsenmair, K., E. (2006a) Wallace's line revisited: has vicariance or dispersal shaped the distribution of Malesian hawkmoths (Lepidoptera: Sphingidae)? Biological Journal of the Linnaean Society 89, 455–468.
Beier, B. A. Chase, M. W. & Thulin, M. (2003) Phylogenetic relationships & taxonomy of subfamily Zygophylloideae (Zygophyllaceae) based on molecular & morphological data. Plant Systematics & Evolution 240(1–4), 11–39.
Belguidoum, M. Dendougui, H. Kendour, Z. Assia, B. Bensaci, C. & Hadjadj, M. (2015) Antioxidant activities, phenolic, flavonoid & tannin contents of endemic Zygophyllum Cornutum Coss. from Algerian Sahara. Der Pharma Chemica 7(11), 312 – 317.
Bellotti, A. C. Arias, V. B. & Guzman, O. L. (1992) Biological control of the cassava hornworm Erinnyis ello (Lepidoptera: Sphingidae). Florida Entomologist 75, 506–515.
Bourgou, S. Megdiche, W. & Ksouri, R. (2017) The Halophytic Genus Zygophyllum and Nitraria from North Africa: A Phytochemical and Pharmacological Overview. pp. 345-356 in Neffati, M. Najjaa H. & Máthé, Á. (Eds) Medicinal and Aromatic Plants of the World – Africa, Volume 3. 411pp. Springer, Dordrecht.
Cerretti, P. & Tschorsnig, H. P.  (2010) Annotated host catalogue for the Tachinidae (Diptera) of Italy. Stuttgarter Beiträge zur Naturkunde A, Neue Serie 3, 305–340.
Danner, F. Eitschberger, U. & Surholt, B. (1998) Die Schwärmer der westlichen Palaearktis. Bausteine zur einer Revision (Lepidoptera: Sphingidae) Textband. Herbipoliana, 4(1), 1-368. [in German]
Delvare, G. Talaee, L. & Goldansaz, S. H. (2011) New Chalcididae (Hymenoptera: Chalcidoidea) of economic importance from Iran. Annales Zoologici (Warszawa). 61(4), 789-801. 
Didmanidze, E. A., Petrov, V. A. & Zolotuhin, V. V. (2013) A list of the Sphingidae (Lepidoptera) of Georgia and neighboring countries with special attention to material from the Simon JANASHIA Museum of Georgia. Entomofauna, 34(21), 269-304.
Ebert, G. (1969) Afghanische Bombyces und Sphinges. 3. Sphingidae (Lepidoptera). Ergebnisse der 2. Deutschen Afganistan-Expedition (1966) der Landessammlungen für Naturkunde in Karlsruhe. Reichenbachia, 12: 37-53. [in German]
Eitschberger, U. & Lukhtanov, V. A. (1996) Neue Unterarten und Namen bei westpaläarktischen Sphingiden (Lepidoptera, Sphingidae). Atalanta Würzburg 27(3-4), 615-621. [in German]
El-Shora, H. M.  El-Amier, Y. A. & Awad, M. H. (2016) Antioxidant Activity of Leaf extracts from Zygophyllum coccineum L. collected from Desert & Coastal Habitats of Egypt. International Journal of Current Microbiology & Applied Sciences 5(4), 635-641.
Eversmann, E. (1844) Fauna Lepidopterologica Volgo-Uralensis, xiv, 633 pp. Kasani. [in Latin]
Ganbaatar, C. Gruner, M. Tunsag, J. Batsuren, D. Ganpurev, B. Chuluunnyam, L. Sodbayar, B. Schmidt, A. W. & Knölker, H. J. (2016) Chemical constituents isolated from Zygophyllum melongena Bunge growing in Mongolia. Natural Product Research 30(14), 1661-1664.
Gibbons, S. & Oriowo, M. A. (2001) Antihypertensive effect of an aqueous extract of Zygophyllum coccineum L. in rats. Phytotherapy Research 15(5), 452-455.
Hammad, I. & Qari, S. H. (2010) Genetic diversity among Zygophyllum (Zygophyllaceae) populations based on RAPD analysis. Genetic & Molecular Research 9(4), 2412-2420.
Jackson, D. M. (1990) Plant-insect behavioral studies: examples with Heliothis & Manduca species. Florida Entomologist 73, 378–391.
Jiangbo, H. Xiaoman, L. Yanfen, N. Jian, T. Bo, W. Jing, J. & Weiwei, C.  (2016) Four new compounds from Zygophyllum fabago L. Phytochemistry Letter 15, 116-120.
Jindra, M. Huang, J. Y. Malone, F. Asahina, M. & Riddiford, L. M. (1997) Identification & mRNA developmental profiles of two ultraspiracle isoforms in the epidermis & wings of Manduca sexta. Insect Molecular Biology 6, 41–53.
Jochova, J. Quaglino, D. Zakeri, Z. Woo, K. & Sikorska, M. (1997) Protein synthesis, DNA degradation, & morphological changes during programmed cell death in labial glands of Manduca sexta. Developmental Genetics 21, 249–257.
Kara, K. & Tschorsnig, H. P. (2003) Host catalogue for the Turkish Tachinidae (Diptera). Journal of Applied Entomology 127, 465-476. 
Karimpour, Y. (2018) Notes on life history, host plants and parasitoids of Malacosoma castrensis L. (Lepidoptera: Lasiocampidae) in Urmia region, Iran. Biharean Biologist 12 (2), 79-83.
Karimpour, Y. Fathipour, Y. Talebi, A. A. & Moharramipour, S. (2006) Biology of Hyles euphorbiae (Lep., Sphingidae) on weedy spurges and determination of its parasitoids in west Azerbaijan, Iran. Iranian Journal of Agricultural Sciences, 37(4), 727-735 [in Farsi]
Kelber, A. Balkenius, A. & Warrant, E. J. (2003) Colour vision in diurnal & nocturnal hawkmoths. Integrative & Comparative Biology 43, 571–579.
Kessler, A. & Baldwin, I. T. (2002) Manduca quinquemaculata's optimization of intra-plant oviposition to predation, food quality, & thermal constraints. Ecology 83, 2346–2354.
Khan, S. S. Khan, A. Khan, A. Wadood, A. Farooq, U. Ahmed, A. Zahoor, A. Ahmad, V. U. Sener, B.  & Erdemoglu, N. (2014)Urease inhibitory activity of ursane type sulfated saponins from the aerial parts of Zygophyllum fabago Linn. Phytomedicine 21(3), 379-82.
Kitching, I. J. & Cadiou, J. M. (2000) Hawkmoths of the world: annotated & illustrated revisionary checklist (Lepidoptera: Sphingidae) (Vol. 226). Ithaca: Cornell University Press.
Korb, S. K. (2018) Automatic autonomous light traps and their usage for the quantitative accounting on example of hawkmoths of Kyrgyzstan (Lepidoptera: Sphingidae). Nature Conservation Research 3(3), 80-85.
Lotfalizadeh, H. (2014) Preliminary faunistic study of Haltichellinae (Hym.: Chalcididae) in East-Azarbaijan province. Plant Pests Research 4(2), 19-30.
Medjdoub, H. & Boufeldja, T. (2012) Antidiabetic effect of the aerial part ethanolic extracts of Zygophyllum geslini Coss. in streptozotocin induced-diabetic rats. Metabolic Function Research 5, 7-20.
Mitroshina, L. A. (1989) Ecology of the Sphingidae (Lepidoptera) of northern Turkmenistan. Izvestiya Akademii Nauk Turkmenskoi. SSR, Seriya Biologicheskikh (6): 20-24. [In Russian with English summary]
Mouna, K. Hichem, B. S. Rania, M. & Noureddine, A. (2015) Anti-oxidant and anti-acetylcholinesterase activities of Zygophyllum album. Bangladesh Journal of Pharmacology 11 (1), 54-62.
Mückstein, P. Tschorsnig, H. P. Vaňhara, J. & Michalková, V. (2007) New host & country records for European Tachinidae (Diptera). Entomologica Fennica 18, 179-183.
Nikdel, M. Sadaghian, B. & Dordaei, A. A. (2004) Biology of brown-tail moth, Euproctis chrysorrhoea (L.) and identification of associated natural enemies in Arasbaran forests. Iranian Journal of Forest and Range Protection Research 1(2), 97-118. [in Persian with English summary]
Nilsson, L. A. (1998) Deep flowers for long tongues. Trends in Ecology & Evolution 13, 259–260.
Nilsson, L. A. Jonsson, L. Rason, L. & R&rianjohany, E. (1985) Monophily & pollination mechanisms in Angraecum arachnites Schltr (Orchidaceae) in a guild of long-tongued hawk-moths (Sphingidae) in Madagascar. Biological Journal of the Linnean Society 26, 1–19.
Noyes, J. S. (2021) Universal Chalcidoid Database. The Natural History Museum. London.
Osborne, K. H. (1995) Biology of Proserpinus clarkiae (Lep., Sphingidae). Journal of the Lepidopterists' Society 49(1), 72-79.
Osier, T. L. Traugott, M. S. & Stamp, N. E. (1996) Allelochemicals in tomato leaves affect a specialist herbivore Manduca sexta negatively but with no ill effects on a generalist insect predator, Podisus maculiventris. Oikos 77, 481–488.
Pittaway, A. R. & Kitching, I. J. (2000) Notes on selected species of hawkmoths (Lepidoptera: Sphingidae) from China, Mongolia and the Korean Peninsula. Tinea 16(3), 170-211.
Pittaway, A. R. (1993) The Hawkmoths of the Western Palaearctic. 240 pp. Harley Books & Natural History Museum, London. UK.
Raguso, R. A. & Willis, M. A. (2002) Synergy between visual & olfactory cues in nectar feeding by naive hawkmoths, Manduca sexta. Animal Behaviour 64, 685–695.
Richter, V. A. (2008) On the Tachinid fauna of southeastern part of European Russia (Diptera: Tachinidae). Entomological Review 88(1), 97-107.
Saleh, N. A. M. & El-Hadidi, M. N. (1977) An approach to the chemosystematics of the Zygophyllaceae. Biochemical Systematic & Ecology 5(2), 121-128.
Sheahan, D. F. & Cutler, F. L. S. (1993) Contribution of vegetative anatomy to the systematics of the Zygophyllaceae. Botanical Journal of the Linnean Society 113(3), 227-262.
Shovkoon, D. F. (2015) To hawkmoths (Lepidoptera, Sphingidae) distribution of the South Kazakhstan. Entomological and parasitological studies in the Volga region, 12, 50–55. [in Russian]
Tavakoli Roodi, T. Fallahzadeh, M. & Lotfalizadeh, H. (2016) Fauna of chalcid wasps (Hymenoptera: Chalcidoidea, Chalcididae) in Hormozgan province, southern Iran. Journal of Insect Biodiversity and Systematics 2(1), 155-166.
 
Wannenmacher, G. & Wasserthal, L. T. (2003) Contribution of the maxillary muscles to proboscis movement in hawkmoths (Lepidoptera: Sphingidae) an electrophysiological study. Journal of Insect Physiology 49, 765–776.
Wąsala, R. & Zamorski, R. (2015) New moth species Akbesia davidii OBERTHÜR, 1884 recorded in Armenia, and new records on the occurrence of hawk-moths (Lepidoptera: Sphingidae) in Armenia. Wiadomości Entomologiczne, 34(4), 48-53.
Wasserthal, L. T. (1997) The pollinators of the Malagasy star orchids Angraecum sesquipedaleA. sororium & A. compactum & the evolution of extremely long spurs by pollinator shift. Botanica Acta 110, 343–359.
Winder, J. A. (1976) Ecology & control of Erinnyis ello & E. alope, important insect pests in the New World. Proceedings of the National Academy of Sciences of the United States of America, 22, 449–466.
Zaki, A. A. Ali, Z. El-Amir, Y. A. & Khan, E. (2016). A new lignan from Zygophyllum aegyptium: Lignan sulfate from Zygophyllum aegyptium. Magnetic Resonance in Chemistry54(9), 771-774.
Zargari, A. (1995) Medicinal herbs. Vol. 2, 840 pp. Tehran University Press. [In Persian].