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Mattesia cf. geminata, an ant-pathogenic neogregarine (Apicomplexa: Lipotrophidae) in two Temnothorax species (Hymenoptera: Formicidae)

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Abstract

An ant-pathogenic neogregarine in Temnothorax affinis and T. parvulus (Hymenoptera: Formicidae) is described based on morphological and ultrastructural characteristics. The pathogen infects the hypodermis of the ants. The infection was mainly synchronous so that only gametocysts and oocysts could be observed simultaneously in the host body. Gametogamy resulted in the formation of two oocysts within a gametocyst. The lemon-shaped oocysts measured 11–13 μm in length and 8–10 μm in width. The surface of the oocysts is not smooth but contains many buds. A ring-shaped line containing rosary-arrayed buds line up in the equatorial plane of the oocyst. These specific characteristics were observed for the first time in neogregarine oocysts from ants. Polar plugs were recognizable clearly by light and electron microscopy. The oocyst wall was quite thick, measuring 775 to 1000 nm. Each oocyst contained eight sporozoites. The neogregarines in the two Temnothorax species show many similarities such as the size and shape of the oocysts, a relatively fragile gametocyst membrane, host affinity, and tissue preference. We identified these neogregarines as Mattesia cf. geminata, which is here recorded from natural ant populations in the Old World for the first time. All neogregarine pathogens infecting ants in nature so far have been recorded from the New World. We present the two ant species, Temnothorax affinis and T. parvulus, as new natural hosts for M. cf. geminata. Furthermore, the morphological and ultrastructural characteristics of the oocyst of M. cf. geminata are documented by scanning and transmission electron microscopy for the first time.

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References

  • Baki D, Tosun HŞ, Erler F (2021) Indigenous entomopathogenic fungi as potential biological control agents of rose sawfly, Arge rosae L. (Hymenoptera: Argidae). Turk J Zool 45:517–525. https://doi.org/10.3906/zoo-2105-15

    Article  CAS  Google Scholar 

  • Bolton B (2003) Synopsis and classification of Formicidae. Mem Am Entomol Inst 71:1–370

    Google Scholar 

  • Buschinger A, Kleespies RG (1999) Host range and host specificity of ant-pathogenic gregarine parasite, Mattesia geminata (Neogregarinida: Lipotrophidae). Entomol Gen 24:93–104

    Article  Google Scholar 

  • Buschinger A, Kleespies RG, Schumann RD (1995) A gregarine parasite of Leptothorax ants from North America. Ins Soc 42:219–222

    Article  Google Scholar 

  • Crosland MWJ (1998) Effect of a gregarine parasite on the color of Myrmecia pilosula (Hymenoptera: Formicidae). Ann Entomol Soc Am 81:481–484. https://doi.org/10.1093/aesa/81.3.481

    Article  Google Scholar 

  • Jouvenaz DP, Anthony DW (1979) Mattesia geminata sp. n. (Neogregarinida: Ophrocystidae) a parasite of the tropical fire ant, Solenopsis geminata (Fabricus). J Protozool 26:354–356

    Article  Google Scholar 

  • Kiran K, Karaman C (2021) Ant fauna (Hymenoptera: Formicidae) of central Anatolian region of Turkey. Turk J Zool 45:161–196. https://doi.org/10.3906/zoo-2008-6

    Article  Google Scholar 

  • Kleespies RG, Huger AM, Buschinger A, Nähring S, Schumann RD (1997) Studies on the life history of a neogregarine parasite found in Leptothorax ants from North America. Biocontrol Sci Technol 7:117–129

    Article  Google Scholar 

  • Lange CE, Lord JC (2012) Chapter 10 – protistan entomopathogens. In: Vega FE, Kaya KK (eds) Insect pathology, 2nd edn. Academic Press, pp 367–394. https://doi.org/10.1016/B978-0-12-384984-7.00010-5

    Chapter  Google Scholar 

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

    Google Scholar 

  • Lord JC (2003) Mattesia oryzaephili (Neogregarinorida: Lipotrophidae), a pathogen of stored-grain insects: virulence, host range and comparison with Mattesia dispora. Biocontrol Sci Technol 13:589–598. https://doi.org/10.1080/0958315031000151800

    Article  Google Scholar 

  • Pereira RM, Williams DV, Becnel JJ, Oi HD (2002) Yellow-head disease caused by a newly discovered Mattesia sp. in populations of the red imported fire ant. Solenopsis Invicta J Invertebr Pathol 81:45–48

    Article  PubMed  Google Scholar 

  • Perkins FO, Barta JR, Clopton R, Peirce MA, Upton SJ (2000) Phylum Apicomplexa. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the protozoa, 2nd edn. Society of Protozoologists, Lawrence USA, pp 190–369

    Google Scholar 

  • Radchenko A (2004) A review of the ant genera Leptothorax Mayr and Temnothorax Mayr (Hymenoptera, Formicidae) of the Eastern Palaearctic. Acta Zool Acad Sci Hung 50:109–137

    Google Scholar 

  • Rasheed MT, Bodlah I, Magomedovıch YZ, Fareen AGE, Bodlah MA, Prebus M, Wachkoo AA (2020) Preliminary contributions toward a revision of the ant genus Temnothorax Mayr Hymenoptera: Formicidae from Pakistan. Turk J Zool 44:375–381. https://doi.org/10.3906/zoo-2003-54

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Clin Microbiol Res 3:197–218

    Google Scholar 

  • Stukalyuk S, Radchenko Y, Netsvetov M, Gilev A (2020) Effect of mound size on intranest thermoregulation in the red wood ants Formica rufa and F. polyctena (Hymenoptera, Formicidae). Turk J Zool 44:266–280. https://doi.org/10.3906/zoo-1912-26

    Article  Google Scholar 

  • Stukalyuk S, Gilev A, Antonov I, Netsvetov M (2021) Size of nest complexes, the size of anthills, and infrastructure development in 4 species of red wood ants (Formica rufa, F. polyctena, F. aquilonia, F. lugubris) (Hymenoptera; Formicidae). Turk J Zool 45:464–478. https://doi.org/10.3906/zoo-2105-39

    Article  Google Scholar 

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

    Chapter  Google Scholar 

  • Valles SM, Pereira RM (2003) Use of ribosomal DNA sequence data to characterize and detect a neogregarine pathogen of Solenopsis invicta (Hymenoptera: Formicidae). J Invertebr Pathol 84:114–118. https://doi.org/10.1016/j.jip.2003.09.001

    Article  CAS  PubMed  Google Scholar 

  • Yaman M (2017) Distribution and occurrence of the neogregarine pathogen, Ophryocystis anatoliensis (Apicomplexa) in populations of Chrysomela populi L. (Coleoptera: Chrysomelidae). Acta Protozool 56:283–288

    Google Scholar 

  • Yaman M, Radek R (2015) Mattesia weiseri sp. nov., a new neogregarine (Apicomplexa: Lipotrophidae) pathogen of the great spruce bark beetle, Dendroctonus micans (Coleoptera: Curculionidae, Scolytinae). Parasitol Res 114:2951–2958

    Article  PubMed  Google Scholar 

  • Yaman M, Radek R (2017) Ophryocystis anatoliensis sp. nov., a new neogregarine pathogen of the chrysomelid beetle Chrysomela populi. Eur J Protistol 59:26–33

    Article  PubMed  Google Scholar 

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Acknowledgements

Temnothorax samples in this study were provided by one (K.K.) of authors from his collections. The author wants to mention that he received TUBITAK support while collecting these samples for another faunistic study.

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Mustafa Yaman conducted experiments, identified the neogregarine pathogen, and wrote the manuscript. Kadri Kıran provided ant samples. Renate Radek conducted experiments and improved the manuscript.

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Correspondence to Mustafa Yaman.

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Yaman, M., Kıran, K. & Radek, R. Mattesia cf. geminata, an ant-pathogenic neogregarine (Apicomplexa: Lipotrophidae) in two Temnothorax species (Hymenoptera: Formicidae). Parasitol Res 122, 1573–1579 (2023). https://doi.org/10.1007/s00436-023-07860-0

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