Skip to main content
SpringerLink
Log in

Characteristic Light and Electron Microscopic Features of Adelina melolonthae, a Coccidian Pathogen of the European Cockchafer, Melolontha melolontha (Coleoptera/Scarabaeidae)

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

This article has been updated

Abstract

Purpose

The aim of this study was to investigate and document the characteristic electron microscopic features of the oocyst of Adelina melolonthae, a coccidian pathogen of the European cockchafer, Melolontha melolontha (Coleoptera: Scarabaeidae).

Methods

Larvae of M. melolontha were collected at Ordu, Turkey. Each larva was dissected in insect Ringer solution. Adeleid oocysts from the tissue that is suspected to Contain coccidian infections were examined under a light microscope (Zeiss), a scanning electron microscope (FEI Quanta 200) and transmission electron Microscope (Philips EM 208).

Results

Spherical to ellipsoidal oocysts measure ca. 24–44.5 µm (mean 35.6 µm) in diameter (n = 50) and include up to twelve sporocysts. The oocyst wall has double layers; the outer layer measured 400–500 nm in thickness and the inner one 10–25 nm. Sporocysts including two sporozoites are rounded ca. 11–12.5 µm (mean 11.7 µm) in diameter. The sporocyst wall consisted of only one 70–80-nm-thick layer. The sporozoites are ellipsoidal and measured 9–11 µm length and 3–4 µm in width. Sporocysts include residual bodies.

Conclusion

In the present paper, the morphology and ultrastructure of the oocyst of A. melolonthae is documented for the first time and compared with other Adelina and coccidian species infecting insects. The results in this study confirm his identification and justify the classification as a separate species A. melolonthae, which differs from other Adelina species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1–6
Fig. 7–11
Figs. 12–14

Similar content being viewed by others

Change history

  • 08 April 2021

    Table 1 contained a spelling error. This has been corrected."

References

  1. Lodos N (1995) Türkiye Entomolojisi IV. Ege Üniversitesi Ziraat Fakültesi Yayınları, Yayın No: 493, İzmir

  2. Hurpin B, Robert PH (1972) Comparison of the activity of certain pathogens of the cockchafer Melolontha melolontha in plots of natural meadowland. J Invertebr Pathol 19:291–298. https://doi.org/10.1016/0022-2011(72)90225-X

    Article  Google Scholar 

  3. Hurpin B, Robert PH (1977) Effects on a natural population of Melolontha melolontha (Col.: Scarabaeidae) of the introduction of Rickettsiella melolonthae and Entomopoxvirus melolonthae. Entomophaga 22:85–91. https://doi.org/10.1007/BF02372993

    Article  Google Scholar 

  4. Schweigkofler W (2004) Microbial pathogens of the cockchafer (Melolontha spp.). Laimburg J 2:186–192

    Google Scholar 

  5. Malinowski H (2011) Possibility of forest protection against insects damaging root systems with the use of biological method based on entomopathogenic nematodes and bacteria. Polskie Towarzystwo Lésne, Sylwan 155:104–111

    Google Scholar 

  6. Laznik Z, Vidrih M, Trdan S (2012) The effect of different entomopathogens on white grubs (Coleoptera: Scarabaeidae) in an organic hay-producing grassland. Arch Biol Sci Belgrade 64:1235–1246. https://doi.org/10.2298/ABS1204235L

    Article  Google Scholar 

  7. Yaman M, Algı G, Güner BG, Ertürk Ö, Ünal S, Radek R (2016) First record, occurrence and distribution of entomopathogens in populations of the European cockchafer, Melolontha melolontha (Coleoptera: Scarabaeidae) in Turkey. North West J Zool 12:192–195

    Google Scholar 

  8. Tuzet O, Vago C, Ormieres R, Robert P (1965) Adelina melolonthae n. sp, coccidie parasite des larves de Melolontha melolontha. Arch Zool Exp Gén 106:513–521

    Google Scholar 

  9. Lange CE, Wittenstein E (2001) An Adelina sp. (Apicomplexa: Coccidia) found in Anurogryllus muticus (De Geer) (Orthoptera: Gryllidae). J Invertebr Pathol 77:83–84. https://doi.org/10.1006/jipa.2000.4999

    Article  CAS  PubMed  Google Scholar 

  10. Kharazi-Pakdel A, Amargier A (1973) Pathogenesis of simultaneous infections by Adelina melolonthae and Nosema melolonthae for Melolontha melolonthae (in French). Entomophaga 18:229–235

    Article  Google Scholar 

  11. Yaman M, Algı G, Radek R (2019) Morphological, ultrastructural and molecular identification of a new microsporidian pathogen isolated from Crepidodera aurata (Coleoptera, Chrysomelidae). Turk J Zool 43:407–415. https://doi.org/10.3906/zoo-1902-4

    Article  CAS  Google Scholar 

  12. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Clin Microbiol Res 3:197–218. https://doi.org/10.1016/s0022-5320(69)90033-1

    Article  Google Scholar 

  13. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212. https://doi.org/10.1083/jcb.17.1.208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Malone LA, Dhana S (1988) Life cycle and ultrastructure of Adelina tenebrionis (Sporozoea: Adeleidae) from Heteronychus arator (Coleoptera: Scarabaeidae). Parasitol Res 74:201–207. https://doi.org/10.1007/BF00539566

    Article  Google Scholar 

  15. Butaeva FG (1996) Adelina grylli sp. nov. (Apicomplexa: Coccidia: Adeleidae) from Gryllus bimaculatus. Parazitologiya 30:64–69 (UDC: 576.893.192)

    Google Scholar 

  16. Ghosh C, Choudhury A, Misra KK (2000) Life histories of three new coccidian parasites from three coleopteran stored-grain pests of India. Acta Protozool 39:233–240

    Google Scholar 

  17. Petty BM, Johnson DT, Steinkraus DC (2012) Survey of pathogens and parasitoids of Popillia japonica (Coleoptera: Scarabaeidae) in northwest Arkansas. J Invertebr Pathol 111:56–59. https://doi.org/10.1016/j.jip.2012.06.004

    Article  CAS  PubMed  Google Scholar 

  18. Undeen AH, Vávra J (1997) Research methods for entomopathogenic protozoa. In: Lacey L (ed) Manual of techniques in insect pathology, Biological Techniques Series. Academic Press, London, pp 117–151

    Chapter  Google Scholar 

  19. Lange CE, Lord JC (2012) Protistan entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology. Academic Press, London, pp 367–394

    Chapter  Google Scholar 

  20. Malone LA, McIvor CA (1995) DNA probes for two microsporidia, Nosema bombycis and Nosema costelytrae. J Invertebr Pathol 65:269–273. https://doi.org/10.1006/jipa.1995.1041

    Article  CAS  PubMed  Google Scholar 

  21. Žižka Z (1985) Ultrastructure of the sporozoite and the sporocyst wall of the coccidian species Adelina tribolii Bhatia, 1937 within the course of an autoinfection. Arch Protistenkd 129:119–126 (PMID: 9645847)

    Article  Google Scholar 

  22. Sokolova YY (1999) Light and electron microscopic observation on life cycle stages of Adelina grylli Butaeva 1996 (Sporozoa, Adeleidae) from the fat body of the cricket Gryllus bimaculatus. Protistol 1:34–42 (Corpus ID: 85910754)

    Google Scholar 

  23. Nyberg PA, Knapp SE (1970) Scanning electron microscopy of Eimeria tenella oocysts. Proc Helm Soc Wash 37:32–36

    CAS  Google Scholar 

  24. Speer CA, Hammond DM, Mahrt JL, Roberts WL (1973) Structure of the oocyst and sporocyst walls and excystation of sporozoites of Isospora canis. J Parasitol 59:35–40

    Article  CAS  Google Scholar 

  25. Marchiondo AA, Duszynski DW, Speer CA (1978) Fine structure of the oocyst wall of Eimeria nieschulzi. J Protozool 25:434–437. https://doi.org/10.1111/j.1550-7408.1978.tb04165.x

    Article  CAS  PubMed  Google Scholar 

  26. Duszynski DW, Solangi MA, Overstreet RM (1979) A new and unusual eimerian (Protozoa: Eimeriidae) from the liver of the gulf killifish, Fundulus grandis. J Wildl Dis 15:543–552

    Article  CAS  Google Scholar 

  27. Christie E, Pappas PW, Dubey JP (1978) Ultrastructure of excystment of Toxoplasma gondii oocysts. J Protozool 25(438):443

    Google Scholar 

  28. Takov DI, Ostoich PV, Tchorbanov AI, Pilarska DK (2020) Order Diptera as a model in the studies of insect immunity: a review. Turk J Zool 44:481–489. https://doi.org/10.3906/zoo-2006-11

    Article  CAS  Google Scholar 

  29. Demirözer O, Pekbey G, Hayat R, Herdoğan A, Acanski J, Milicic M, Uzun A (2020) First contribution on distribution, abundance, and species richness of blowfly species (Diptera) of Isparta province with five new records for the Turkish fauna. Turk J Zool 44:69–79

    Article  Google Scholar 

  30. Kuyulu A, Genç H (2020) Genetic diversity of codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) populations in Turkey. Turk J Zool 44:462–471. https://doi.org/10.3906/zoo-2006-4

    Article  CAS  Google Scholar 

  31. İnal B, Kandemir İ (2020) DNA barcoding of black cherry aphid Myzus cerasi (Fabricus, 1775) (Hemiptera: Aphididae) populations collected from Prunus avium and Prunus cerasus. Turk J Zool 44:146–155. https://doi.org/10.3906/zoo-1908-9

    Article  CAS  Google Scholar 

  32. Arıkan TK, Turan SL (2020) Organochlorine pesticide residues in feathers of four bird species from western part of Turkey. Turk J Zool 44:401–407. https://doi.org/10.3906/zoo-2005-52

    Article  CAS  Google Scholar 

  33. Freitas ACO, Gigliolli AAS, Caleffe RTC, Conte H (2020) Insecticidal effect of diatomaceous earth and dolomite powder against Corn weevil Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae). Turk J Zool 44:490–497. https://doi.org/10.3906/zoo-2005-34

    Article  CAS  Google Scholar 

  34. Yaman M (2020) Transmission of Microsporidium sp. between different generations of Crepidopdera aurata (Coleoptera: Chrysomelidae). Turk J Zool 44:248–253. https://doi.org/10.3906/zoo-2003-32

    Article  Google Scholar 

  35. Léger L (1900) Sur la presence d’une Coccidie coelomique chez Olocrates abbreviatus O1. Arch Zool Exp Gén Sér 3(8):1–3

    Google Scholar 

  36. Purrini K (1984) Two new coccidian parasites of the genus Adelina (Adeleidae, Coccidia) parasitizing oribatid mite Nothrus silvestris (Oribatei, Acarina) and springtail Neanura muscorum (Collembola, Apterygota). Arch Protistenkd 128:99–107. https://doi.org/10.1016/S0003-9365(84)80032-9

    Article  Google Scholar 

  37. Léger L (1904) Sporozoaires parasites de l’Embia solieri Rambur. Arch Protistenkd 3:356–366

    Google Scholar 

  38. Levine ND (1988) The protozoan phylum Apicomplexa, vol 1 and 2. CRC Press, Boca Raton, FL, p 357

    Google Scholar 

  39. Yarwood EA (1937) The life cycle of Adelina cryptocerci sp. nov., a coccidian parasite of the roach Cryptocercus punctulatus. Parasitology 29:370–390. https://doi.org/10.1017/S0031182000024872

    Article  Google Scholar 

  40. Parez C (1899) Sur une coccidie nouvelle, Adelea mesnili n. sp., parasite coelomique d’un Lepidoptaire. C R Soc Biol (Paris) 51:694–696

    Google Scholar 

  41. Weiser J, Beard RL (1959) Adelina sericesthis n. sp., a new coccidian parasite of scarabaeid larvae. J Invertebr Pathol 1:99–106

    Google Scholar 

  42. Schneider A (1875) Contribution à l’histoire des Grégarines des Invertébrés de Paris et de Roscoff. Arch Zool Exp Gen 4:493–604

    Google Scholar 

  43. Sautet J (1930) A propos d’Adelina tenebrionis, coccidie coelomique de Tenebrio molitor. Ann Parasitol Hum Comp 8:582–589

    Article  Google Scholar 

  44. Moroff T (1907) Untersuchungen über Coccidien: I Adelea zonula n sp. Arch Protistenkd 8:17–51

    Google Scholar 

Download references

Acknowledgement

The study was financially supported as a research project by the Scientific and Technical Council of Turkey (112O807).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Arts and Science, Bolu Abant İzzet Baysal University, 14030, Bolu, Turkey

    Mustafa Yaman

  2. Institute of Biology/Zoology, Freie Universität Berlin, Königin-Luise-Str. 1–3, 14195, Berlin, Germany

    Renate Radek

Authors
  1. Mustafa Yaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Renate Radek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mustafa Yaman.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest. We certify that this manuscript is original and has not been published and will not be submitted elsewhere for publication while being considered by Acta Parasitologica.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yaman, M., Radek, R. Characteristic Light and Electron Microscopic Features of Adelina melolonthae, a Coccidian Pathogen of the European Cockchafer, Melolontha melolontha (Coleoptera/Scarabaeidae). Acta Parasit. 66, 925–931 (2021). https://doi.org/10.1007/s11686-021-00363-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-021-00363-x

Keywords

Search

Navigation