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Variations in hemocyte profile induced by Beauveria bassiana (Bals.) Vuill. in Periplaneta americana (L.) (Blattodea: Ectobiidae)

  • Abhilisa Mudoi
  • Purnima Das
  • Lakshmi Kanta Hazarika
  • Karishma Das
  • Somnath RoyEmail author
Original Research Article

Abstract

Hemocytes of healthy (untreated) and Beauveria bassiana (Bals.-Criv.) Vuill.-treated nymphs and adults Periplaneta americana (L.) (Blattodea: Ectobiidae) were examined with phase contrast microscopy. The total hemocyte counts (THCs) and differential hemocyte counts (DHCs) were estimated and compared between the untreated and treated nymphs and adults; significant augmentation of THC was observed in the treated 3rd, 4th, 5th instars and adults at 6 h after treatment (HAT), compared to the untreated individuals, followed by its suppression. In addition to changes in the population dynamics of prohemocytes (PRs), plasmatocytes (PLs), granulocytes (GRs) and spherulocytes (SPs), their morphology was also affected. GRs, predominant hemocytes involved in cell-mediated defense, responded to the infection differently including the formation of fine pseudopodia–like cytoplasmic extensions and, they clumped together.

Keywords

American cockroach Cell-mediated defense Hemocyte Insect immunocytes Total hemocyte count 

Notes

Acknowledgements

We are very much grateful to Assam Agricultural University, Jorhat for providing financial assistance to carry out this investigation. We are also thankful to Dr. Coby Schal, Blanton J. Whitmire, Distinguished Professor, Department of Entomology and Plant Pathology, North Carolina State University, Raleigh and Professor Michael L. May, Department of Entomology, School of Environmental and Biological Sciences, Rutgers, The State University of New Jersey, 96 Lipman Drive, New Brunswick for critically reviewing the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Arnold JW (1970) Haemocytes of the Pacific beetle cockroach, Diploptera punctata. Canad Ento 102:830–835CrossRefGoogle Scholar
  2. Arnold JW, Hinks CF (1976) Haemopoiesis in Lepidoptera. The multiplication of circulating haemocytes. Can J Zool 54:1003–1012CrossRefGoogle Scholar
  3. Barson GN, Renn N, Bywater AF (1994) Laboratory evaluation of six species of entomopathogenic fungi for the control of the house fly (Musca domestica L.), a pest of intensive animal units. J Invertebr Pathol 64:107–113PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bell WJ, Adiyodi KG (1982) Circulatory system. In: Bell WJ (ed) The American cockroach. Kluwer Academic publishers, London, New York, pp 7–13Google Scholar
  5. Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore, pp 1–2Google Scholar
  6. Boucias DG, Pendland JC, Latge JP (1988) Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol 54:1795–1805PubMedPubMedCentralGoogle Scholar
  7. Bracke JW, Cruden DL, Markovetz AJ (1979) Intestinal microbial flora of the of the American cockroach, Periplaneta americana L. Appl Environ Microbiol 38:945–955PubMedPubMedCentralGoogle Scholar
  8. Cen K, Li B, Lu Y, Zhang SC, Wang C (2017) Divergent LysM effectors contribute to the virulence of Beauveria bassiana by evasion of insect immune defenses. PLoS Pathog 13:e1006604PubMedPubMedCentralCrossRefGoogle Scholar
  9. Chaurasia AY, Lone Y, Wani O, Gupta US (2016) Effect of certain entomopathogenic fungi on oxidative stress and mortality of Periplaneta americana. Pestic Biochem Physiol 127:28–37PubMedCrossRefPubMedCentralGoogle Scholar
  10. Cornwell PB (1968) The cockroach. Hutchinson and Co., Ltd, London, p 391Google Scholar
  11. Dun PE (1986) Biochemical aspects of insect immunology. Annu Rev Entomol 31:321–339CrossRefGoogle Scholar
  12. Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Sci Tech 4:3–34CrossRefGoogle Scholar
  13. Ferron P (1978) Biological control of insect pests by entomogenous fungi. Annu Rev Entomol 23:409–442CrossRefGoogle Scholar
  14. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643PubMedCrossRefPubMedCentralGoogle Scholar
  15. Gillespie JP, Burnett C, Charnle AK (2000) The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum. J Insect Physiol 4:429–437CrossRefGoogle Scholar
  16. Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, Butt TM, Belvin M, Hoffmann JA, Ferrandon D (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127:1425–1437PubMedPubMedCentralCrossRefGoogle Scholar
  17. Gupta AP (1979a) Hemocytes types: their structures, synonymies, interrelationships and taxonomic significance. In: Gupta AP (ed) Insect Hemocytes: development, forms, functions and techniques. Cambridge University Press, Cambridge, pp 85–127CrossRefGoogle Scholar
  18. Gupta AP (1979b) Identification key for hemocyte types in hanging drop preparation. In: Gupta AP (ed) Insect Hemocytes: development, forms, functions and techniques. Cambridge University Press, Cambridge, pp 527–529CrossRefGoogle Scholar
  19. Gupta AP (1985) Cellular elements in the haemolymph. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, Biochemistry and Pharmacology. Pergamon Press, Oxford, pp 401–451Google Scholar
  20. Gupta AP, Sutherland DJ (1968) Effect of sublethal doses of chlordane on the hemocytes and midgut epithelium of Periplaneta americana. Ann Entomol Soc Am 61:910–918CrossRefGoogle Scholar
  21. Guthrie DM, Tindall AR (1968) The biology of the cockroach. London 1968: Edward Arnold (Publ.) LtdGoogle Scholar
  22. Hajek AE, St. Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322CrossRefGoogle Scholar
  23. Hazarika LK, Gupta AP (1987) Variation in hemocyte populations during various developmental stages of Blatella germanica (L.) (Dictyoptera, Blattellidae). Zool Sci 4:307–313Google Scholar
  24. Hazarika LK, Puzari KC (1990) Beauveria bassiana (Bals.) Vuill. For biological control of rice hispa in Assam, India. Int Rice Res Newsl 11:31Google Scholar
  25. Hazarika LK, Kalita S, Das P, Borah BK (2019) Insect immunology and Pest management. Diamond creation, Delhi printer and lamination, New Delhi, pp 1–112Google Scholar
  26. Hubner-Campos RF, Leles RN, Rodrigues J, Luz C (2013) Efficacy of entomopathogenic hypocrealean fungi against Periplaneta americana. Parasitol Int 62:517–521PubMedCrossRefGoogle Scholar
  27. Jones JC (1962) Current concepts concerning insect haemocytes. Am Zool 2:209–246CrossRefGoogle Scholar
  28. Kaakeh W, Reid BL, Bohnert TJ, Bennett GW (1997) Toxicity of imidacloprid in the German cockroach (Dictyoptera: Blattellidae), and the synergism between imidacloprid and Metarhizium anisopliae (imperfect Fungi: Hyphomycetes). J Econ Entomol 90:473–482CrossRefGoogle Scholar
  29. Kolundžić E, Kovacević G, Špoljar M, Sirovina D (2018) A comparison of Hemocytes in Phasmatodea and Blattodea species. Ento News 127:471–477CrossRefGoogle Scholar
  30. Kulshrestha V, Pathak SC (1997) Aspergillosis in German cockroach Blattella germanica (L.) (Blattoidea: Blattellidae) Vandana. Mycopathologia. 139:75–78PubMedCrossRefPubMedCentralGoogle Scholar
  31. Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309PubMedCrossRefPubMedCentralGoogle Scholar
  32. Lord JC (2005) Low humidity, moderate temperature, and desiccant dust favor efficacy of Beauveria bassiana (Hyphomycetes: Moniliales) for the lesser grain borer, Rhyzopertha dominica (Coleoptera: Bruchidae). Biol Control 34:180–186CrossRefGoogle Scholar
  33. Mudoi A, Das P, Hazarika LK (2017) Pathogenicity of Beauveria bassiana (Bals.) Vuill.(KR855715) against Periplaneta americana (L.). J Ento Zool Stud 5:1516–1519Google Scholar
  34. Mudoi A, Das P, Hazarika LK (2018) Beauveria bassiana (Bals.) Vuill. Strains pathogenic to Periplaneta americana (L.). J Ento Zool Stud 6:903–907Google Scholar
  35. Mullins DE, Cochran DG (1987) Nutritional ecology of cockroaches. In: Slansky F Jr, Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, New York, pp 885–902Google Scholar
  36. Pachamuthu P, Kamble ST (2000) In vivo study on combined toxicity of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) strain ESC-1 with sublethal doses of chlorpyrifos, propetamphos, and cyfluthrin against German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 93:60–70PubMedCrossRefPubMedCentralGoogle Scholar
  37. Pachamuthu P, Kamble ST, Yuen GY (1999) Virulence of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) strain ESC-1 to the German cockroach (Dictyoptera: Blattellidae) and its compatibility with insecticides. J Econ Entomol 92:340–346CrossRefGoogle Scholar
  38. Phukan M, Hazarika LK, Barooah M, Puzari KC, Kalita S (2008) Interaction of Dicladispa armigera (Coleoptera: Chrysomelidae) haemocytes with Beauveria bassiana. Int J Trop Ins Sci 28:88–97CrossRefGoogle Scholar
  39. Ragyalis AK (1982) Physiological and biochemical changes in Acantholyda posticalis hemolymph during ontogeny: 1. Cell morphology. Liet Tsr Mokslu Akad DarbSer C Biol Mokslai 4:69–78Google Scholar
  40. Ratcliffe NA, Rowley AF (1979) Roles of haemocytes in defence against biological agents. In: Gupta AP (ed) Insect Haemocytes. Cambridge University Press, Cambridge, pp 331–414CrossRefGoogle Scholar
  41. Ratner S, Vinson SB (1983) Encapsulation reactions in vitro by haemocytes of Heliothis virescens. J Insect Physiol 29:855–863CrossRefGoogle Scholar
  42. Rosenberger CR, Jones JC (1960) Studies on total blood cell counts of the southern armyworm larva, Prodenia eridania (Lepidoptera). Ann Entomol Soc Am 53:351–355CrossRefGoogle Scholar
  43. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357PubMedCrossRefGoogle Scholar
  44. Rust MK, Reierson DA, Hansgen KH (1991) Control of American cockroaches (Dictyoptera: Blattidae) in sewers. J Med Entomol 28:210–221PubMedCrossRefGoogle Scholar
  45. Rust MK, Owens JM, Rierson DA (1995) Understanding and controlling the German cockroach. Oxford University Press, New York, p 430Google Scholar
  46. Salt G (1970) The cellular defence reaction of insects. Cambridge monograph in experimental biology, no. 16. Cambridge University press, LondonGoogle Scholar
  47. Schal C, Hamilton RL (1990) Integrated suppression of synanthropic cockroaches. Annu Rev Entomol 35:521–551PubMedCrossRefGoogle Scholar
  48. St. Leger RJ, Wang C (2010) Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl Microbiol Biotechnol 85:901–907PubMedCrossRefGoogle Scholar
  49. Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14CrossRefGoogle Scholar
  50. Toledo J, Campos SE, Flores S, Liedo P, Barrera JF, Villasenor A, Montoya P (2007) Horizontal transmission of Beauveria bassiana in Anastrepha ludens (Diptera: Tephritidae) under laboratory and field cage conditions. J Econ Entomol 100:291–297PubMedCrossRefPubMedCentralGoogle Scholar
  51. Wang C, Wang S (2017) Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol 62:73–90PubMedCrossRefPubMedCentralGoogle Scholar
  52. Xiao G, Ying SH, Zheng P, Wang ZL, Zhang S, Xie XQ, Shang Y, Leger RJS, Zhao GP, Wang C, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483PubMedPubMedCentralCrossRefGoogle Scholar
  53. Zhang S, Xia YX, Kim B, Keyhani NO (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Mol Microbiol 80:811–826PubMedCrossRefPubMedCentralGoogle Scholar
  54. Zurek L, Watson DW, Schal C (2002) Synergism between Metarhizium anisopliae (Deuteromycota: Hyphomycetes) and boric acid against the German cockroach (Dictyoptera: Blattellidae). Biol Control 23:296–302CrossRefGoogle Scholar

Copyright information

© African Association of Insect Scientists 2019

Authors and Affiliations

  • Abhilisa Mudoi
    • 1
  • Purnima Das
    • 1
  • Lakshmi Kanta Hazarika
    • 2
  • Karishma Das
    • 1
  • Somnath Roy
    • 3
    Email author
  1. 1.Department of EntomologyAssam Agricultural UniversityJorhatIndia
  2. 2.Assam Women’s UniversityJorhatIndia
  3. 3.Tocklai Tea Research InstituteTea Research AssociationJorhatIndia

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