Gall-Inducing Aphids of Populus spp. in Razavi Khorasan Province, with Introducing Two New Species for Iranian Fauna

Document Type : Research Article


Ferdowsi university of mashhad


Introduction: Poplar trees in Iran are hosts to a number of aphid species, some of which cause excrescences on leaves and other growing parts. These abnormal growths are classified as either galls or pseudogalls but innumerable gradations between the apparently normal and abnormal plant structures have made differentiation difficult. Galls are vegetable excrescences resulting from insect activities and usually sheltering the immature stages of the producers. The aphid genus Pemphigus Hartig, 1839 (Hemiptera: Sternorrhyncha) contains over 70 species widely distributed in the Holarctic, of which, 46 are known to form galls on leaves or twigs of Populus L. Aphids of the genus Pemphigus are usually holocyclic and heteroecious between a primary host, and several herbaceous secondary hosts. The majority of the family representatives are dioecious or heteroecious. Such species migrate from primary hosts (tree species) where they form galls characteristic in their size and shape to roots of secondary hosts (herbs or tree species). Only few species are monoecious, i.e. with life cycle occurring on one host species. Reviewing taxonomic related literature showed that the knowledge of Iranian galling aphids is still limited. So far 7 species e.g. P. borealis Tullgren, 1909, P. bursarius Linnaeus, 1758, P. immunis Buckton, 1896, P. populi Courchet, 1879, P. protospirae Lichtenstein, 1884, P. spyrothecae Passerini, 1856 and P. vesicarius Passerini, 1861 have been reported from Iran.
Materials and Methods: This study was conducted during the growing season of 2017. The study area, Razavi Khorasan province (35.1020° N, 59.1042° E) is located in the North eastern Iran, where no study has previously been carried out. The galls were collected from the leaves, petioles and branches of poplars, according to their location, and taken from them. Also some galls with aphids were put into vials filled with 75% alcohol for morphological studies. Sampling, preparation and identification of specimens were done according to the Blackman and Eastop (2000)). Specimens was approved by Dr. Roman Hałaj in Entomological Laboratory of the Upper Silesian Nature Society of Poland. Systematic knowledge, host plants, and synonyms of determined species were taken from Blackman and Eastop (2000) and Rezvani (2001).
Results and Discussion: Nine gall-inducing aphid species belonging to genus Pemphigus, Tribe Pemphigini and subfamily Eriosomatinae were found on four host plants. The occurrence of Pemphigus passeki (Börner), 1952 (Hem.: Aphididae) and Pemphigus populinigrae (Schrank), 1801 (Hem.: Aphididae) on Populus nigra in Iran are reported for the first time. The other recorded gall aphids are: 1-Pemphigus borealis which its galls are more or less oval in shape with a rather smooth surface galls, often merged into groups of 4-6 at the base (even up to 10). 2-Pemphigus bursarius with galls of more or less spherical, pear-shaped or pouch-like, green, yellow-green, sometimes red-brown in color. 3- Pemphigus immunis which its galls are walnut shape (c.a 4 cm in diameter), with think walls and uneven, wrinkled and often cracked surface, usually occurring individually, less often in small groups but always separated from one another. 4- Pemphigus passeki with galls at the base of the lamina, this gall was collected only from Neyshabour city. 5- Pemphigus populi with gall of more or less spherical or oval, more or less irregularly blobbed, almost always narrower at the base than at the top, pear-shaped or even slenderer, placed on the upper side of the lamina on the main nerve usually close to its base, size of a hazelnut, most often green in color. 6- Pemphigus populinigrae Schrank, 1801 with elongated galls and running along the main nerve, rather smooth, in their majority bright reddish and rather without yellowish tint, only partly open from the bottom side of the lamina. 7- Pemphigus protospirae with flattened and strongly spirally twisted galls, the twists are smaller and more numerous (more than 5) than those formed by P.spyrothecae. Galls very often on all the petiole and the base of lamina, shiny, green or green with red spot. 8- Pemphigus spirothecae with galls in the form of flattened and spirally twisted petiole, with the number of twists not exceeding 5 (usually 3-5). Galls are green, yellow-green to red-brown. 9- Pemphigus vesicarius with galls of combe-like, crown like or club-shaped, always with very distinct processes.
Conclusions: This preliminary research on gall-inducing aphids and their host plants in NE Iran added two new records of species to Iranian aphid fauna and 5 new records to Razavi Khorasan province. Previously about 485 aphid species were known for Iran. By the present study, the Iranian aphid fauna has at least 487 species. However, the number of insects especially aphids recorded from Iran is far from complete. Most probably due to the fact that the Iranian fauna has been poorly investigated and many areas have been sampled only sporadically.


1- Abrahamson W. G., and Weis A. E. 1987. Nutritional ecology of arthropod gall makers. p. 235-258. In F. Slansky, Jr. & Rodriquez, J. G.(ed.) Nutritional ecology of insects, mites, spiders & related invertebrates. John Wiley & Sons Press, New York.
2- Alleyne E. H., and Morrison F. O. 1977. Some Canadian poplar aphid galls. The Canadian Entomologist, 109(3): 321-328
3- Blackman R.L., and Eastop V.F. 1989. Aphids on the World's Crops: an Identification Guide. A Wiley. New York.
4- Blackman R.L., and Eastop V.F. 2000. Aphids on the World's Crops: an Identification and Information Guide, Second ed., Wiley Publication, New York.
5- Blackman R.L., and Eastop V.F. 2011. Aphids on the World’s Plants. Visited: 2017/11/25.
6- Buga S. V., Zhorov D. G., Leshchinskaya N. V., and Stekolshchikov A. V. 2016. Aphids of the family Eriosomatidae (Insecta: Homoptera) in Belarus, Zoosystematica Rossica, 25(2): 226–232
7- Chang G., and Zhong T. 1979. Five new species of Pemphigus H. from China. Acta entomologica sinica 22: 324-332.
8- Foster W.A. 1975. A new species of Pemphigus Hartig from Western Europe. Journal of Entomology, 44: 255-263.
9- Ghafouri-Moghaddam M., Lotfalizadeh H., and Rakhshani E. 2014. A survey on hyperparasitoids of the poplar spiral gall aphid, Pemphigus spyrothecae Passerini (Hemiptera: Aphididae) in Northwest Iran. Journal Crop Protection, 3(3): 369-376
10- Hałaj R., and Osiadacz B. 2013. European gall-forming Pemphigus (Aphidoidea: Eriosomatidae), Zoologischer Anzeiger, 252: 417-423.
11- Harris K.F., and Maramorosch K. 1980. Vectors of Plant Pathogens. Academic Press, New York-London.
12- Hasanshahi G. H., Jahan F., Abbasipoor H., and Japoshvili G. 2013. The first report of Protaphelinus nikolskajae (Yasnosh, 1963) (Chalcidoidea: Aphelinidae) parasitoid of Pemphigus immunis popular aphid from Iran. Journal of Plant Protection, 28(2): 274-276. (In Persian).
13- Ignoffo C.M., and Granovsky A.A. 1961. Life history and development of Mordwilkoja vagabonda (Homoptera: Alphididae) on Populus delfiodes. Annals of the Entomological Society of America, 54:486-499.
14- Meyer J. 1987. Plant galls and gall inducers. Berlin & Stuttgart: Borntraeger.
15- Mortazavi Z. S., Sadeghi H., Aktac N., Depa Ł., and Fekrat L. 2015. Ants (Hymenoptera: Formicidae) and their aphid partners (Homoptera: Aphididae) in Mashhad region, Razavi Khorasan Province, with new records of aphids and ant species for Fauna of Iran. HALTERES, 6: 4-12.
16- Osiadacz B., and Hałaj R. 2014. First records of gall-inducing aphid Pemphigus populi (Hemiptera: Aphidoidea, Eriosomatidae) in Poland with gall-based key to Central and North European species of the genus. Entomologica Fennica, 25: 16-25.
17- Pashchenko N.F. 1988. Suborder Aphidinea – aphids. In: Lehr, P.A. (ed.) Keys to the Identification of Insects of the Soviet Far East Vol. 2, Hemiptera and Heteroptera. 'Nauka', Leningrad, pp.546-686.
18- Redfern M. 1992. What are galls? Cecidology 7: 81-83.
19- Rezwani A. 2004. Aphids on Trees & Shrubs in Iran. Plant pests & diseases research Institute. Tehran.
20- Sadeghi S. E., Assareh M. H., and Tavakoli M. 2009. Oak gall wasps of Iran. Research Institute of forest and rangelands. Tehran.
21- Tarasi J., Sadeghi S. E., and Moradi P. 2007. Study and comparing of density of spiral gall aphid, Pemphigus spirothecae (Hom. Pemphigidae) on ten clones of black poplar, Populus nigra and its natural enemies in Zanjan province. Pajouhesh & sazandegi No77 pp: 130-134. (In Persian with English abstract)
22- Tseng S., and Tao C.C. 1936. New Chaitophorus spp. Entomology Phytopathology, 4: 120-176.
23- Urban J. 2002. Occurrence, development and natural enemies of Pemphigus spyrothecae (Homoptera, Pemphigidae), Journal of Forest Science, 48(6): 248–270.
24- Wool D. 1984. Gall-forming aphids. In T.N Ananthakrishnan (ed.), Biology of gall Insect. pp. 11-58. Oxford & IHB Publ. Co., India.