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Variations in circulating hemocytes are affected by age and caste in the stingless bee Melipona quadrifasciata

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Abstract

The insect immune system faces various challenges; particularly in social bees, caste system and age polyethism expose individuals to numerous environmental and working conditions. However, little is known about how cellular defenses in social bees may be organized to respond to a variety of immune challenges. Here, we describe the morphological features and the total and differential counts of hemocytes in different female classes (newly emerged workers, nurses, foragers, and virgin queens) of the eusocial stingless bee Melipona quadrifasciata. Granulocytes and prohemocytes were, respectively, the most and the least abundant cells among all classes of females. Furthermore, there were more prohemocytes in virgin queens than in foragers. The total number of hemocytes was smaller in foragers, whereas the largest number was observed in nurse workers. This reduced amount of hemocytes in foragers might allow energy savings to perform colony activities such as foraging and defense. Foragers also had the biggest hemocytes (either prohemocytes, granulocytes, or plasmatocytes) in comparison to the other classes of females, which might have arisen as a compensation for the reduction in number of these cells during aging. These results suggest that profiles of hemocytes of M. quadrifasciata vary according to the caste and age of this eusocial bee.

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References

  • 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

    Article  PubMed  Google Scholar 

  • Amdam GV, Simões ZLP, Hagen A, Norberg K, Schrøder K, Mikkelsen Ø, Kirkwood TBL, Omholt SW (2004) Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp Gerontol 39:767–773

    Article  PubMed  CAS  Google Scholar 

  • Araújo HC, Cavalcanti MG, Santos SS, Alves LC, Brayner FA (2008) Hemocytes ultrastructure of Aedes aegypti (Diptera: Culicidae). Micron 39:184–189

  • Arteaga Blanco LA, Crispim JS, Fernandes KM, de Oliveira LL, Pereira MF, Bazzolli DMS, Martins GF (2017) Differential cellular immune response of Galleria mellonella to Actinobacillus pleuropneumoniae. Cell Tissue Res 370:153–168

    Article  PubMed  CAS  Google Scholar 

  • Bedick JC, Tunaz H, Nor Aliza AR, Putnam SM, Ellis MD, Stanley DW (2001) Eicosanoids act in nodulation reactions to bacterial infections in newly emerged adult honey bees, Apis mellifera, but not in older foragers. Comp Biochem Physiol C Toxicol Pharmacol 130:107–117

    Article  PubMed  CAS  Google Scholar 

  • Brayner FA, Araujo HR, Cavalcanti MG, Alves LC, Peixoto CA (2005) Ultrastructural characterization of the hemocytes of Culex quinquefasciatus (Diptera: Culicidae). Micron 36:359–367

    Article  PubMed  CAS  Google Scholar 

  • Corona M, Velarde R a, Remolina S, Moran-Lauter A, Wang Y, Hughes K a, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A 104:7128–7133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cremer S, Sixt M (2009) Analogies in the evolution of individual and social immunity. Philos Trans R Soc Lond B Biol Sci 364:129 LP–129142

    Article  Google Scholar 

  • da Silva C, Dunphy GB, Rau ME (2000) Interaction of hemocytes and prophenoloxidase system of fifth instar nymphs of Acheta domesticus with bacteria. Dev Comp Immunol 24:367–379

    Article  PubMed  Google Scholar 

  • de Negreiro MCC, Carvalho RBR, de Andrade FG, Levy SM, Moscardi F, Falleiros ÂMF (2009) Caracterização citológica dos hemócitos de Anticarsia gemmatalis (Lepidoptera, Noctuidae) em larvas resistentes ao vírus AgMNPV. Iheringia Sér Zool 99:66–70

  • El-Aziz NMA, Awad HH (2010) Changes in the haemocytes of Agrotis ipsilon larvae (Lepidoptera: Noctuidae) in relation to dimilin and Bacillus thuringiensis infections. Micron 41:203–209

    Article  PubMed  CAS  Google Scholar 

  • El-Mohandes SS, Nafea AE, Fawzy AM (2010) Effect of different feeding diets on the haemolymph of the newly emerged honeybee workers Apis mellifera L. Egypt Acad J Biol Sci 3:213–220

  • Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert A d MP, Galetto L, Nates-Parra G, Quezada-Euán JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346

    Article  Google Scholar 

  • Gätschenberger H, Azzami K, Tautz J, Beier H (2013) Antibacterial immune competence of honey bees (Apis mellifera) is adapted to different life stages and environmental risks. PLoS One 8:e66415

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gerloff CU, Ottmer BK, Schmid-Hempel P (2003) Effects of inbreeeding on immune response and body size in a social insect, Bombus terrestris. Funct Ecol 17:582–589

    Article  Google Scholar 

  • Grigorian M, Hartenstein V (2013) Hematopoiesis and hematopoietic organs in arthropods. Dev Genes Evol 223:103–115

    Article  PubMed  CAS  Google Scholar 

  • Gupta AP (1979) Hemocyte types: their structures, synonymies, interrelationships, and taxonomic significance. In: Gupta AP (ed) Insect hemocytes: development, forms, functions and techniques. Cambridge University Press, Cambridge, pp 85–128

    Chapter  Google Scholar 

  • Hillyer JF (2016) Insect immunology and hematopoiesis. Dev Comp Immunol 58:102–118

    Article  PubMed  CAS  Google Scholar 

  • Hwang S, Bang K, Lee J, Cho S (2015) Circulating hemocytes from larvae of the Japanese rhinoceros beetle Allomyrina dichotoma (Linnaeus) (Coleoptera: Scarabaeidae) and the cellular immune response to microorganisms. PLoS One 10:e0128519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hystad EM, Salmela H, Amdam GV, Münch D (2017) Hemocyte-mediated phagocytosis differs between honey bee (Apis mellifera) worker castes. PLoS One 12:e0184108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Imperatriz-Fonseca VL, Saraiva AM, de Jong D (2006) Bees as pollinators in Brazil: assessing the status and suggesting best practices, 1st edn. Editora Holos, Ribeirão Preto

    Google Scholar 

  • Janzen DH (1980) Ecologia vegetal nos trópicos. Temas de Biologia, 1st edn. Editora Pedagógica e Universitária, São Paulo

  • Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236

    Article  PubMed  CAS  Google Scholar 

  • Kerr WE, Carvalho GA, Nascimento VA, Bego LR, de Alves RMO, Martins MAS, Souza IC (1996) Abelha urucu: biologia, manejo e conservação, 1st edn. Fundação Acangau, Belo Horizonte

  • Kwon H, Bang K, Cho S (2014) Characterization of the hemocytes in larvae of Protaetia brevitarsis seulensis: involvement of granulocyte-mediated phagocytosis. PLoS One 9:e103620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lanot R, Zachary D, Holder F, Meister M (2001) Postembryonic hematopoiesis in Drosophila. Dev Biol 230:243–257

    Article  PubMed  CAS  Google Scholar 

  • Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309

    Article  PubMed  CAS  Google Scholar 

  • League GP, Estévez-Lao TY, Yan Y, Garcia-Lopez VA, Hillyer JF (2017) Anopheles gambiae larvae mount stronger immune responses against bacterial infection than adults: evidence of adaptive decoupling in mosquitoes. Parasit Vectors 10:367

    Article  PubMed  PubMed Central  Google Scholar 

  • Lima MAP, Martins GF, Oliveira EE, Guedes RNC (2016) Agrochemical-induced stress in stingless bees: peculiarities, underlying basis, and challenges. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 202:733–747

    Article  PubMed  CAS  Google Scholar 

  • Pandey JP, Tiwari RK, Kumar D (2008) Reduction in haemocyte mediated immune response in Danais chrysippus following treatment with neem-based insecticides. J Entomol 5:200–206

    Article  Google Scholar 

  • Reavey CE, Warnock ND, Garbett AP, Cotter SC (2015) Aging in personal and social immunity: do immune traits senesce at the same rate? Ecol Evol 5:4365–4375

    Article  PubMed  PubMed Central  Google Scholar 

  • Ribeiro C, Brehélin M (2006) Insect haemocytes: what type of cell is that? J Insect Physiol 52:417–429

    Article  PubMed  CAS  Google Scholar 

  • Schmid MR, Brockmann A, Pirk CWW, Stanley DW, Tautz J (2008) Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J Insect Physiol 54:439–444

    Article  PubMed  CAS  Google Scholar 

  • Simone-Finstrom M (2017) Social immunity and the superorganism: behavioral defenses protecting honey bee colonies from pathogens and parasites. Bee World 94:21–29

    Article  Google Scholar 

  • Slaa EJ, Sánchez Chaves LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315

    Article  Google Scholar 

  • Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14

  • Yamashita M, Iwabuchi K (2001) Bombyx mori prohemocyte division and differentiation in individual microcultures. J Insect Physiol 47:325–331

    Article  PubMed  CAS  Google Scholar 

  • Youngjin P, Yonggyun K, David S (2011) Cellular immunosenescence in adult male crickets, Gryllus assimilis. Arch Insect Biochem Physiol 76:185–194

    Article  CAS  Google Scholar 

  • Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22

    Article  PubMed  Google Scholar 

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Funding

The authors thank the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG CBB-APQ-00247-14), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico for the financial support.

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Authors and Affiliations

  1. Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Samira Veiga Ravaiano & Wagner Faria Barbosa

  2. Departamento de Biologia Geral, Universidade Federal de Viçosa (UFV), Viçosa, MG, 36570-900, Brazil

    Lúcio Antônio Campos & Gustavo Ferreira Martins

Authors
  1. Samira Veiga Ravaiano
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  2. Wagner Faria Barbosa
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  3. Lúcio Antônio Campos
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  4. Gustavo Ferreira Martins
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Correspondence to Gustavo Ferreira Martins.

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Communicated by: Sven Thatje

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Ravaiano, S.V., Barbosa, W.F., Campos, L.A. et al. Variations in circulating hemocytes are affected by age and caste in the stingless bee Melipona quadrifasciata. Sci Nat 105, 48 (2018). https://doi.org/10.1007/s00114-018-1573-x

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  • DOI: https://doi.org/10.1007/s00114-018-1573-x

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