Abstract
We characterized individual morphological types of the rose sawfly, Arge ochropus (Gmelin) (Hymenoptera: Argidae), hemocytes for the first time by means of light and differential interference contrast microscopy and scanning and transmission electron microscopy. Four types of hemocytes were identified in the hemolymph of larvae and pupae of A. ochropus: prohemocytes, plasmatocytes, granulocytes, and oenocytoids. Prohemocytes are the smallest type of hemocytes, rounded to ovoid cells with large nuclei. Plasmatocytes are polymorphic and variable in size. Granulocytes are oval and spherical cells variable in size, with variable number of rough endoplasmic reticulum, mitochondria, and microtubules in the cytoplasm. Oenocytoids contain eccentric nucleus and cytoplasm with small mitochondria and few rough endoplasmic reticula. Differential hemocyte counts indicated that plasmatocytes are the most abundant hemocyte type during early instars while granulocytes are the most abundant hemocyte type in the last instar. The pattern of total hemocyte count changed during rose sawfly development and reached its peak in prepupae and then declined slowly in the pupal stage.
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Amaral IMR, Neto JFM, Pereira GB, Franco MB, Beletti ME, Kerr WE, Bonetti AM, Ueira-Vieira C (2010) Circulating hemocytes from larvae of Melipona scutellaris (Hymenoptera, Apidae, Meliponini): cell types and their role in phagocytosis. Micron 41:123–129
Battistella S, Amirante GA (1999) Prime indagini sui meccanismi immunitari di larve e adulti di Cetonischema aeruginosa Drury (1770). Boll Soci Adr Sci 78:27–34
Beaulaton J (1979) Hemocytes and hemocytopoiesis in silkworms. Biochem Mol Biol 61:157–164
Beckage NE (2008) Insect immunology. Academic Press Elsevier, San Diego
Berger J (2009) Preclinical testing on insects predicts human haematotoxic potentials. Lab Anim 43:328–332. doi:10.1258/la.2008.007162
Chain B, Leyshon-Sorland K, Siva-Jothy MT (1992) Haemocyte heterogeneity in the cockroach Periplaneta americana as revealed by monoclonal antibodies. J Cell Sci 103:1261–1267
Chiang AS, Gupta AP, Han SS (1988) Arthropod immune system: I. Comparative light and electron microscopy accounts of immunocytes and other hemocytes of Blattella germanica (Dictyoptera: Blattellidae). J Morphol 198:257–267
Falleiros AMF, Bombonato MTS, Gregorio EA (2003) Ultrastructural and quantitative studies of hemocytes in the sugarcane borer, Diatraea saccharalis (Lepidoptera: Pyralidae). Braz Arch Biol Technol 46:287–294
Gardiner EMM, Strand MR (2000) Hematopoiesis in larval Pseudoplusia includes and Spodoptera frugiperda. Arch Insect Biochem Physiol 43:147–164
Giglio A, Battistella S, Talarico FF, Brandmayr TZ, Giulianini PG (2008) Circulating hemocytes from larvae and adults of Carabus (Chaetocarabus) lefebvrei Dejean 1826 (Coleoptera: Carabidae): cell types and their role in phagocytosis after in vivo artificial non-self-challenge. Micron 39:552–558
Giulianini PG, Bertolo F, Battistella S, Amirante GA (2003) Ultrastructure of the hemocytes of Cetonischema aeruginosa larvae (Coleoptera, Scarabaeidae): involvement of both granulocytes and oenocytoids in in vivo phagocytosis. Tissue Cell 35:243–251
Gupta AP (1979) Insect hemocytes: development, forms, functions, and techniques. Cambridge University Press, Cambridge
Gupta AP (1985) Cellular elements in the hemolymph. In: Kerkut GA,Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon Press, Oxford, p 402–444
Hoffmann JA (1995) Innate immunity of insects. Curr Opin Immunol 7:4–10
Hoffmann JA (2003) The immune response of Drosophila. Nature 426:33–38
Hypša V, Grubhoffer L (1997) Two hemocyte populations in Triatoma infestans: ultrastructural and lectin-binding characterization. Folia Parasitol 44:62–70
Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, Zachary D (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol 7:335–350
Jones JC (1959) A phase contrast study of the blood cells in Prodenia larvae (Lepidoptera). J Microb Sci 100:17–23
Jones JC (1962) Current concepts concerning insect haemocytes. Am Zool 2:209–246
Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309
Manachini B, Arizza V, Parrinello D, Parrinello N (2011) Hemocytes of Rhynchophoru ferrugineus (Olivier) (Coleoptera: Curculionidae) and their response to Saccharomyces cerevisiae and Bacillus thuringiensis. J Invertebr Pathol 106:360–365
Meister M, Lagueux M (2003) Drosophila blood cells. Cell Microbiol 5:573–580
Okazaki T, Okudaira N, Iwabuchi K, Fugo H, Nagai T (2006) Apoptosis and adhesion of hemocytes during molting stage of silkworm, Bombyx mori. Zool Sci 23:299–304
Pathak J (1986) Haemograms and in endocrine control in insects. In: Brehelin (ed) Immunity in invertebrates. Springer, Berlin, pp 49–59
Pech LL, Strand MR (2000) Plasmatocytes from the moth Pseudoplusia includes induce apoptosis of granular cells. J Insect Physiol 46:1565–1573
Ratcliffe NA, Rowley AF, Fitzgerald SW, Rhodes CP (1985) Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol 97:186–350
Ribeiro C, Brehelin M (2006) Insect haemocytes: what type of cell is that? J Insect Physiol 52:417–429
Saito T, Iwabuchi K (2003) Effect of bombyxin-II, an insulin-related peptide of insects, on Bombyx mori hemocyte division in single-cell culture. Appl Entomol Zool 39:583–588
Sanjayan KP, Ravikumar T, Albert S (1996) Changes in the haemocyte profile of Spilostethus hospes (Fab) (Heteroptera: Lygaeidae) in relation to eclosion, sex and mating. J Biosci 21:781–788
SAS Institute (1997) SAS/STAT user’s guide for personal computers. SAS Institute, Cary
Shapiro L (1979) Changes in haemocyte population. In: Gupta AP (ed) Insect haemocytes. Cambridge University Press, Cambridge, pp 475–525
Siddiqui MI, Al-Khalifa MS (2013) Review of haemocyte count, response to chemicals, phagocytosis, encapsulation and metamorphosis in insects. Ital J Zool 1–14
Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14
Wheeler R (1963) Studies on the total haemocyte count and haemolymph volume in Periplaneta americana. Fed Pract 21:123
Wigglesworth VB (1959) Insect blood cells. Ann Rev Entomol 4:1–16
Yamashita M, Iwabuchi K (2001) Bombyx mori prohemocyte division and differentiation in individual microcultures. J Insect Physiol 47:325–331
Yeager JF (1945) The blood picture of the Southern armyworm Prodenia eridamin. J Agric Res 71:1–40
Acknowledgments
The corresponding author expresses his deep gratitude to Iran National Science Foundation (INSF) for the financial support (research grant 91003789). The authors are grateful to the University of Guilan for providing laboratory facility. We thank Núcleo de Plataformas Tecnológicas-CPqAM/FIOCRUZ for technical assistance for transmission electron microscopy.
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Edited by Guilherme D Rossi – UNESP
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Khosravi, R., Sendi, J.J., Brayner, F.A. et al. Hemocytes of the Rose Sawfly Arge ochropus (Gmelin) (Hymenoptera: Argidae). Neotrop Entomol 45, 58–65 (2016). https://doi.org/10.1007/s13744-015-0339-9
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DOI: https://doi.org/10.1007/s13744-015-0339-9