Re-discovery and identification of Iphiseius degenerans (Acari: Phytoseiidae) in Turkey, based on morphological and molecular data

Öz

The monotypic genus Iphiseius is represented by only Iphiseius degenerans (Berlese) (Acari: Phytoseiidae). This species, which is one of the most common predatory mites in citrus orchards in Mediterranean countries, is an important biological control agent of various pests that include thrips, whiteflies and spider mites. This species was included in a brief report of the Turkish fauna some 50 years ago. However, there was no morphological information, illustrations or collection details of the examined specimens, except for its host plant, sour lemon, and an unknown locality in Mersin Province, Turkey. Since that time, extensive surveys conducted in citrus plantations in both Mersin and Adana Provinces have not confirmed its presence. However, in 2008, 2011 and 2013, a natural population of I. degenerans was encountered in Anıtlı town, near the border with Antalya Province, where it was associated with thrips on a non-cultivated host, Hedera helix L. (Araliaceae). In this study, we re-describe I. degenerans, based on both female and male specimens, and provide all morphological details. The DNAs of the specimens were successfully isolated and amplified using an internal transcribed spacer (ITS) gene marker by polymerase chain reaction (PCR). A phylogenetic tree was constructed using the DNA sequence of the amplified region, as well as other sequences deposited in the National Center for Biotechnology Information (NCBI). The phylogenetic tree and genetic divergence were constructed and estimated, respectively, using the Jukes and Cantor models, respectively. There were no morphological differences in comparison to other populations of I. degenerans. This result was confirmed by the molecular study as no genetic divergence with other populations was found. The results of this study will be useful for further systematic studies on theTurkish Phytoseiidae, and would also help non-expert, phytoseiid taxonomists to correctly identify I. degenerans. 

Anahtar Kelimeler

• Iphiseius degenerans
• ITS region
• genetic divergence
• phylogenetic tree
• Turkey

Türkiye’de Iphiseius degenerans (Acari: Phytoseiidae)’ın yeniden saptanması ve moleküler-morfolojik verilere bağlı olarak tanımlanması

Öz

Iphiseius cinsi sadece Iphiseius degenerans (Berlese) (Acari: Phytoseiidae) tarafından temsil edilen monotipik bir cinstir. Bu tür Akdeniz ülkeleri turunçgil bahçelerinde bulunan en yaygın avcı akarlardan biri olup, kırmızıörümcek, beyazsinek ve thrips gibi birçok zararlının biyolojik mücadelesinde kullanılan önemli bir doğal düşmandır. Bu türün Türkiye faunası için varlığı yaklaşık 50 yıl önce Mersin ilinde limon ağaçlarında saptanmış morfolojik özelliklere ve çizimlere yer verilmeden kısaca bildirilmiştir. Ancak daha sonra Adana ve Mersin illeri turunçgil bahçelerinde yapılan kapsamlı sörvey çalışmalarında bu türe rastlanılmamıştır. Iphiseius degenerans’ın doğal populasyonu Mersin ili Anıtlı köyünde thrips ile bulaşık Hedara helix (Araliaceae) bitkileri üzerinde 2008, 2011 ve 2013 yıllarında saptanmıştır. Bu çalışmada, I. degenerans’ın tanısı erkek ve dişi bireyler üzerinden yeniden yapılmış ve bütün morfolojik özellikleri modern tanımlamalara göre verilmiştir. Avcı akarın DNA’sı ITS gen bölgesine ait primer kullanılarak PZR (Polimeraz Zincir Reaksiyonu) ile elde edilmiş ve çoğaltılmıştır. Filogenetik ağaç, çalışmada elde edilen sekanslar ve NCBI gen bankasında depolanan sekanslar kullanılarak oluşturulmuştur. Filogenetik ağaç ve genetik uzaklık Jukes & Cantor modeline göre oluşturulmuş ve hesaplanmıştır. Sonuçlara göre I. degenerans’n Türkiye populasyonu ile diğer populasyonlar arasında herhangi bir morfolojik farklılık gözlemlenmemiştir. Morfolojik olarak saptanan bu sonuç moleküler yöntemler ile desteklenmiş ve yapılan filogenetik analizlerde tüm I. degenerans türleri aynı grup içerisinde yer almıştır. Bu çalışmanın sonuçları Türkiye’de klasik yöntemler ile yapılan phytoseiid teşhislerinin desteklenmesi açısından fayda sağlayacak, ayrıca uzman olmayan araştırıcıların teşhis yapabilmelerine yardımcı olacaktır. 

Anahtar Kelimeler

• Iphiseius degenerans
• ITS bölgesi
• genetik uzaklık
• filogenetik ağaç
• Türkiye

Kaynakça

1. Akyazı, R., E.A., Ueckermann & M. Soysal 2016. The new distribution of Amblyseius herbicolus in Turkey (Parasitiformes, Phytoseiidae) with a key of Amblyseius species found in Turkey. Acarologia, 56 (2): 237–244.
2. Athias–Henriot, C. 1975. Nouvelles notes sur la Amblyseiini. II. Le releve organotaxique de la face dorsale adulte (Gamasides Protoadenique, Phytoseiidae). Acarologia, 17: 20–29.
3. Athias–Henriot, C. 1977. Nouvelles notes sur la Amblyseiini. III. Sur la genre Cydnodromus: redefinition, composition (Parasitiformes, Phytoseiidae). Entomophaga, 22: 61–73.
4. Barbar, Z. 2013. Survey of phytoseiid mite species (Acari: Phytoseiidae) in citrus orchards in Lattakia governorate, Syria. Acarologia, 53: 247–261.
5. Chant D.A. & J.A. McMurtry 2005. A review of the subfamily Amblyseiinae Muma (Acari: Phytoseiidae) Part VI. The tribe Euseiini n. tribe, subtribes Typhlodromalina n. subtribe, Euseiina n. subtribe, and Ricoseiina n. subtribe. International Journal of Acarology, 31: 187–224.
6. Chant, D.A. & J.A. McMurtry 2007. Illustrated keys and diognoses for the genera and subgenera of the Phytoseiidae of the world (Acari: Mesostigmata). Indira Publishing House, West Bloomfield, 219 pp.
7. Chant, D.A. & E. Yoshida–Shaul 1989. Adult dorsal setal patterns of the family Phytoseiidae (Acari: Gamasina). International Journal of Acarology, 15: 219–233.
8. Chant, D.A. & E. Yoshida–Shaul 1991. Adult ventral setal patterns in the family Phytoseiidae (Acari: Gamasina). International Journal of Acarology, 17: 187–199.

9. Chant, D.A. & E. Yoshida–Shaul 1992. Adult idiosomal setal patterns in the family Phytoseiidae (Acari: Gamasina). International Journal of Acarology, 18: 177–193.
10. Çakmak, İ. & S. Çobanoğlu 2006. Amblyseius californicus (McGregor, 1954) (Acari: Phytoseiidae), a new record for the Turkish fauna. Turkish Journal of Zoology, 30: 55–58.
11. Denmark, H.A. & G.A. Evans 2011. Phytoseiidae of North America and Hawaii (Acari: Mesostigmata). Indira Publishing House, West Bloomfield, USA, 451 pp.
12. Döker, İ., & C. Kazak 2012. Detecting acaricide resistance in Turkish populations of Panonychus citri McGregor (Acari: Tetranychidae). Systematic and Applied Acarology, 17: 368–377.
13. Döker, İ., Th.I. Stathakis, C. Kazak, K. Karut & G.Th. Papadoulis 2014a. Four new records and two new species of Phytoseiidae (Acari: Mesostigmata) from Turkey, with a key to the Turkish species. Zootaxa, 3827: 331–342.
14. Döker, İ., J. Witters, J. Pijnakker, C. Kazak, M.-S. Tixier & S. Kreiter 2014b. Euseius gallicus Kreiter and Tixier (Acari: Phytoseiidae) is present in four more countries in Europe: Belgium, Germany, The Netherlands and Turkey. Acarologia, 54: 245–248.
15. Döker, İ., C. Kazak & K. Karut 2015. A new species and two new records of the family Phytoseiidae (Acari: Mesostigmata) from Turkey. Zootaxa, 3918: 439–445.
16. Döker, İ., C. Kazak & K. Karut 2016. Contributions to the Phytoseiidae (Acari: Mesostigmata) fauna of Turkey: morphological variations, twelve new records, re-description of some species and a revised key to the Turkish species. Systematic and Applied Acarology, 21: 505–527.
17. Döker, İ., C. Kazak, & K. Karut, 2017. Three new species of the family Phytoseiidae (Acari: Mesostigmata) from Turkey. Zootaxa, 4243: 565–576.
18. Döker, İ. 2018. Re-description of two new records and description of Neoseiulella kazaki sp. nov. (Acari: Phytoseiidae) from Turkey. Systematic and Applied Acarology, 23: 113–122.
19. Düzgüneş Z. 1963. Türkiyede yeni bulunan akarlar. Bitki Koruma Bülteni, 3: 237–246
20. Evans, G.O. & W.M. Till 1979. Mesostigmatic mites of Britain and Ireland (Chelicerata: Acari– Parasitiformes): An introduction to their external morphology and classification. Transactions of the Zoological Society of London, 35: 139–270.
21. Evans, G.O. 1963. Observations on the chaetotaxy of the legs in the free–living Gamasina (Acari: Mesostigmata). Bulletin of the British Museum National History, 10: 277–303.
22. Fantinou, A.A., A. Baxevani, F. Drizou, P. Labropoulos, D. Perdikis & G. Papadoulis 2012. Consumption rate, functional response and preference of the predaceous mite Iphiseius degenerans to Tetranychus urticae and Eutetranychus orientalis. Experimental & Applied Acarology, 58: 133–144.
23. Faraji, F., S. Çobanoğlu & I. Çakmak 2011. A checklist and a key for the Phytoseiidae species of Turkey with two new species records (Acari: Mesostigmata). International Journal of Acarology, 37: 221–243.
24. Ferragut, F., I. Pérez Moreno, V. Iraola, & A. Escudero 2010. Ácaros depredadores em las plantas cultivadas. Família Phytoseiidae. Ediciones Agrotécnicas, Madrid, 202 pp.
25. Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
26. Jukes T.H. & C.R. Cantor 1969. Evolution of protein molecules. In Munro HN, editor, Mammalian Protein Metabolism, pp. 21-132, Academic Press, New York.
27. Kasap, İ. 2001. Turunçgil kırmızıörümceği Panonychus citri (McGregor) ile avcı akar Typhlodromus athiasae Porath and Swirski (Acarina: Tetranychidae; Phytoseiidae) arasındaki ilişkiler ve gün derece modellerinin oluşturulması. Çukurova Üniversitesi, Fenbilimleri Enstitüsü, Bitki Koruma Anabilim Dalı, Doktora Tezi, Adana, 93 s.
28. Kazak, C., İ. Döker, K. Karut 2016. Abundance of the phytoseiid (Acari: Mesostigmata) mites in citrus ecosystems in Adana Province, Turkey. Book of Abstracts of 8th Symposium of the European Association of Acarologists, Valencia, Spain, sayfa 83.
29. Kolodochka, L.A. 2006. Phytoseiid mites of the Palaearctic Region (Parasitiformes, Phytoseiidae): faunistic, taxonomy, ecomorphology, evolution. Vestnik Zoologii, suppl. 21, 250pp. [in Russian].
30. Kumar S., G. Stecher, K. Tamura 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger data sets. Molecular Biology and Evolution. 33(7):1870–1874.
31. Lindquist, E.E. & G.O. Evans 1965. Taxonomic concepts in the Ascidae, with a modified setal nomenclature for the idiosoma of the Gamasina (Acarina: Mesostigmata). Memoirs of the Entomological Society of Canada, 47: 1–64. http://dx.doi.org/10.4039/entm9747fv
32. Moraes, G.J. de, I.D. Zannou, E.A. Ueckermann, A.R. Oliveira, J.S. Yaninek & R. Hanna 2007. Phytoseiid mites of the tribes Afroseiulini, Kampimodromini and Phytoseiulini, and complementary notes on mites of the tribes Euseiini and Neoseiulini (Acari: Phytoseiidae) from sub-Saharan Africa. Zootaxa, 1628: 1–22.
33. McMutry, J.A., G.J. de Moraes & N. Famah Sourassou 2013. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic & Applied Acarology, 18: 297–320.
34. Navajas, M., J. Lagnel, G. Fauvel, G.J. Moraes 1999. Sequence variation of Ribosomal Internal Transcribed Spacer (ITS) in commercially important Phytoseiidae mites. Experimental & Applied Acarology, 23: 851–859.
35. Papadoulis, G.Th., N.G. Emmanouel & E.V. Kapaxidi 2009. Phytoseiidae of Greece and Cyprus (Acari: Mesostigmata). Indira Publishing House. 200 pp.
36. Rowell, H.L., D.A. Chant & R.I.C. Hansell 1978. The determination of setal homologies and setal patterns on the dorsal shield in the family Phytoseiidae (Acarina: Mesostigmata). The Canadian Entomologist, 110: 859–876.
37. Sekeroglu, E. & C. Kazak 1993. First record of Phytoseiulus persimilis (Acari: Phytoseiidae) in Turkey. Entomophaga, 38: 343–345.
38. Şekeroğlu, E. 1984. Phytoseid mites (Acarina: Mesostigmata) of Southern Anatolia, their biology, and effectiveness as a biological control agent on strawberry plant. Doğa Bilim Dergisi, 8: 320–336 (in Turkish with English summary).
39. Tsolakis, H., M.-S. Tixier, S. Kreiter & S. Ragusa, 2012. The genus concept within the family Phytoseiidae (Acari: Parasitiformes). Historical review and phylogenetic analyses of the genus Neoseiulus Hughes. Zoological Journal of the Linnean Society, 165: 253–273.
40. Vicente dos Santos, V. & M.-S. Tixier 2016. Which molecular markers for assessing which taxonomic level? The case study of the mite family Phytoseiidae (Acari: Mesostigmata). Cladistics. Wainstein, B.A. & E.S. Arutunjan 1973. New species of predatory mites of the family Phytoseiidae (Parasitiformes) in Armenian SSR. Doklady Akademii Nauk Armyanskoy SSR, 56: 55–58 [in Russian].
41. Yıldız S. 1998. Doğu Akdeniz Bölgesi sebze alanlarında görülen Phytoseiidae familyası türlerinin saptanması. Çukurova Üniversitesi, Fenbilimleri Enstitüsü, Bitki Koruma Anabilim Dalı, Yüksek Lisans Tezi, Adana, 36s.