Environmental Monitoring and Assessment

, Volume 177, Issue 1–4, pp 437–447 | Cite as

Hemocitical responses to environmental stress in invertebrates: a review

  • Danielli Giuliano Perez
  • Carmem Silvia Fontanetti


Although invertebrates are recognized by the great facility to accumulate pollutants present in their environment and many of them are used as sentinel species in biomonitoring studies, little is known about the impact of toxicants on the immune system of these animals. In this regard, hemocytes play a fundamental role: these cells circulate freely through the hemolymph of invertebrates and act on the recognition of foreign material to the organism, mediating and effecting the cellular defense, such as phagocytosis, nodulation, and encapsulation. Different morphological types can be recognized but still there is controversy among the researchers about the exact classification of the hemocytes due to the diversity of techniques for the preservation and observation of these cells. In the present study, a review on the main hemocyte responses to environmental stress in different invertebrate organisms is presented, emphasizing the contamination by heavy metals. It is discussed parameters such as: alteration in the number of cells involved in the defense reaction, phagocytic activity, lysosomal responses, and production of reactive oxygen species.


Hemocytes Immunity of invertebrates Cellular defense Environmental stress Heavy metals 


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  1. Ahearn, G. A., Mandal, P. K., & Mandal, A. (2004). Mechanisms of heavy-metal sequestration and detoxification in crustaceans: A review. Journal of Comparative Physiology B, 174, 439–452.CrossRefGoogle Scholar
  2. Andrade, F. G., Negreiro, M. C. C., & Falleiros, A. M. F. (2004). Aspectos dos mecanismos de defesa da lagarta da soja Anticarsia gemmatalis (Hübner 1818) relacionados ao controle biológico por Baculovirus anticarsia (AGMNPV). Arquivos do Instituto Biológico, 71(3), 391–398.Google Scholar
  3. Andrews, G. K. (2000). Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochemical Pharmacology, 59(1), 95–104.CrossRefGoogle Scholar
  4. Auffret, M., & Oubella, R. (1997). Hemocyte aggregation in the oyster Crassostrea gigas: In Vitro measurement and experimental modulation by xenobiotics. Comparative Biochemistry and Physiology, 118A(3), 705–712.Google Scholar
  5. Auffret, M., Mujdzic, N., Corporeau, C., & Moraga, D. (2002). Xenobiotic-induced immunomodulation in the European flat oyster, Ostrea edulis. Marine Environmental Research, 54, 585–589.CrossRefGoogle Scholar
  6. Barraco, M. A., & Amirante, G. A. (1992). Morphological and cytochemical studies of the hemocytes of Squilla mantis (Stomatopoda). Journal of Crustacean Biology, 12(3), 372–382.CrossRefGoogle Scholar
  7. Bogdan, C., Röllinghoff, M., & Diefenbach, A. (2000). Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology, 12, 64–76.CrossRefGoogle Scholar
  8. Bombonato, M. T., & Gregório, E. A. (1995). Estudo morfológico e quantitativo dos hemócitos em larvas de Diatraea sacharalis (Fabricius) (Lepidoptera, Pyralidae). Revista Brasileira de Zoologia, 12(4), 867–879.CrossRefGoogle Scholar
  9. Cajaraville, M. P., Olabarrieta, I., & Marigomez, I. (1996). In vitro activities in mussel hemocytes as biomarkers of environmental quality: A case study in the Abra Estuary (Biscay Bay). Ecotoxicology and Environmental Safety, 35, 253–260.CrossRefGoogle Scholar
  10. Carneiro, M. E., & Daemon, E. (1997). Caracterização dos tipos celulares presentes na hemolinfa de adultos de Rhipicephalus sanguineus (Latreille, 1806) (Ixodoidea: Ixodidae) em diferentes estados nutricionais. Revista Brasileira de Parasitologia Veterinária, 6(1), 1–9.Google Scholar
  11. Carneiro, M. E., & Daemon, E. (2001). Caracterização dos tipos celulares presentes na hemolinfa de adultos de Amblyomma cajennense (Fabricius) Koch, 1844 e de Haemaphysalis sp. Revista Brasileira de Zoociências, 3(2), 139–145.Google Scholar
  12. Coles, J. A., Farley, S. R., & Pipe, R. K. (1995). Alteration of the immune response of the common marine mussel Mytilus edulis resulting from exposure to cadmium. Diseases of Aquatic Organisms, 22, 59–65.CrossRefGoogle Scholar
  13. Correia, A. A. (2008). Histofisiologia do canal alimentar e hemócitos de Spodoptera frugiperda (J.E. Smith) (Lepdoptera: Noctuidae) tratadas com nim (Azadirachta indica A. Juss). Dissertation, Universidade Federal Rural de Pernambuco.Google Scholar
  14. Correia, A. A., Ferreira, A. V. S., Wanderley-Teixeira, V., & Teixeira, A. A. C. (2005). Descrição morfológica dos hemócitos do gafanhoto Tropidacris collaris (Stoll, 1813) (Orthoptera: Romaleidae). Arquivos do Instituto Biológico, 72(1), 57–61.Google Scholar
  15. Coutinho, H. D., & Barbosa, A. R. (2007). Fitorremediação: Considerações gerais e características de utilização. Silva Lusitana, 15(1), 103–117.Google Scholar
  16. David, J. A. O., Salaroli, R. B., & Fontanetti, C. S. (2008). The significance of changes in Mytella falcata (Orbigny, 1842) gill filaments chronically exposed to polluted environments. Micron 39, 1293–1299.CrossRefGoogle Scholar
  17. Erold-Erickson, M., Mishra, S., & Schneider, D. (2000). Interactions between the cellular and humoral immune responses in Drosophila. Current Biology, 10, 781–784.CrossRefGoogle Scholar
  18. Falleiros, A. M. F. (1995). Células sanguíneas de Diatraea saccharalis (Lepidóptera: Pyralidae): Estudo citoquímico ultraestrutural e à microscopia de varredura. Thesis, Universidade Estadual Paulista Júlio de Mesquita Filho.Google Scholar
  19. Falleiros, A. M. F., Bombonato, M. T. S., & Gregório, E. A. (2003). Ultrastructural and quantitative studies of hemocytes in sugarcane borer, Diatraea saccharalis (Lepidoptera: Pyralidae). Brazilian Archives of Biology and Technology, 46(2), 287–294.CrossRefGoogle Scholar
  20. Faraldo, A. C. (2000). Hemócitos de Diptera economicamente importantes: Análise qualitativa, quantitativa e funcional. Dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho.Google Scholar
  21. Fisher, W. S., Wishkovsky, A., & Chu, F.-L. E. (1990). Effects of tributyltin on defense-related activities of oyster hemocytes. Archives of Environmental Contamination and Toxicology, 19, 354–360.CrossRefGoogle Scholar
  22. Fisher, W. S., Oliver, L. M., Winstead, J. T., & Long, E. R. (2000). A survey of oysters Crassostrea virginica from Tampa Bay, Florida: Associations of internal defense measurements with contaminant burdens. Aquatic Toxicology, 51, 115–138.CrossRefGoogle Scholar
  23. Freire, M. M., Santos, V. G., Ginuino, I. S. F., & Arias, A. R. L. (2008). Biomarcadores na avaliação da saúde ambiental dos ecossistemas aquáticos. Oecologia Brasiliensis, 12(3), 347–354.CrossRefGoogle Scholar
  24. Giamberini, L., & Pihan, J. C. (1997). Lysosomal changes in the hemocytes of the freshwater mussel Dreissena polymorpha experimentally exposed to lead and zinc. Diseases of Aquatic Organisms, 28, 221–227.CrossRefGoogle Scholar
  25. Gillespie, J. P., Kanost, M. R., & Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology, 42, 611–643.CrossRefGoogle Scholar
  26. Gillespie, J. P., Burnett, C., & Charnley, A. K. (2000). The immune response of the desert locust Schistocerca gregaria during mycosis of the entomopathogenic fungus, Metarhizium anisopliae var acridum. Journal of Insect Physiology, 46(4), 429–437.CrossRefGoogle Scholar
  27. Godoy, J. A. P., & Fontanetti, C. S. (2009). Diplopods as bioindicators of soils: Analysis of midgut of individuals maintained in substract containing sewage sludge. Water, Air and Soil Pollution. doi: 10.1007/s11270-009-0261-z.Google Scholar
  28. Greig, R. A., Sawyer, T. K., Lewis, E. J., & Galasso, M. E. (1982). A study of metal concentrations in relation to gill color and pathology in the rock crab. Archives of Environmental Contamination and Toxicology, 11, 539–545.CrossRefGoogle Scholar
  29. Gupta, A. P. (1979). Insect hemocytes: Development, forms, functions and techniques. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  30. Gupta, A. P. (1985). Cellular elements in the hemolymph. In G. A. Kertutand & L. I. Gilbert (Eds.), Comprehensive insects physiology, biochemistry and pharmacology (pp. 402–444). Oxford: Pergamon Press.Google Scholar
  31. Hall, J. L. (2002). Cellular mechanisms for heavy metals detoxification and tolerance. Journal of Experimental Botany, 53(366), 1–11.CrossRefGoogle Scholar
  32. Jiravanichpaisal, P., Lee, B. L., & Söderhäll, K. (2006). Cell-mediated immunity en arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology, 211, 213–236.CrossRefGoogle Scholar
  33. Johansson, M. W., Keyser, P., Sritunyalucksana, K., & Söderhäll, K. (2000). Crustacean haemocytes and haematopoiesis. Aquaculture, 191, 45–52.CrossRefGoogle Scholar
  34. Klaassen, C. D., Liu, J., & Choudhuri, S. (1999). Metallothionein: An intracellular protein to protect against cadmiun toxicity. Annual Review of Pharmacology and Toxicology, 39(1), 267–294.CrossRefGoogle Scholar
  35. Lavine, M. D., & Strand, M. R. (2002). Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32, 1295–1309.CrossRefGoogle Scholar
  36. Lorenzon, S., Francese, M., Smith, V. J., & Ferrero, E. A. (2001). Heavy metals affect the circulating haemocyte number in the shrimp Palaemon elegans. Fish & Shellfish Immunology, 11, 459–472.CrossRefGoogle Scholar
  37. Lowe, D. M., & Pipe, R. K. (1994). Contaminant induced lysosomal membrane damage in marine mussel digestive cells: An in vitro study. Aquatic Toxicology, 30, 357–365.CrossRefGoogle Scholar
  38. Lowenberger, C. (2001). Innate immune response of Aedes aegypti. Insect Biochemistry and Molecular Biology, 31, 219–229.CrossRefGoogle Scholar
  39. Mandato, C. A. (1998). Modulators of the insect cellular immune response. Thesis, University of Waterloo.Google Scholar
  40. Matozzo, V., Ballarin, L., Pampanin, D. M., & Marin, M. G. (2001). Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Archives of Environmental Contamination and Toxicology, 41, 163–170.CrossRefGoogle Scholar
  41. Mayrand, E., ST-Jean, S. D., & Courtenay, S. C. (2005). Haemocytes responses of blue mussels (Mytilus edulis L.) transferred from a contaminated site to a reference site: Can the immune system recuperate? Aquaculture Research, 36, 962–971.CrossRefGoogle Scholar
  42. Muta, T., & Iwanaga, S. (1996). The role of hemolymph coagulation in innate immunity. Current Opinion in Immunology, 8, 41–47.CrossRefGoogle Scholar
  43. Negreiro, M. C. C., Andrade, F. G., & Falleiros, A. M. F. (2004). Sistema imunológico de defesa em insetos: Uma abordagem em lagartas da soja, Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), resistentes ao AgMNPV. Semina: Ciências Agrárias, 25(4), 293–308.Google Scholar
  44. Nogarol, L. R., & Fontanetti, C. S. (2010). Acute and subchronic exposure of diplopods to substrate containing sewage mud: Tissular responses of the midgut. Micron, 41(3), 239–246.CrossRefGoogle Scholar
  45. Olabarrieta, I., L’azou, B., Yuric, S., Cambar, J., & Cajaraville, M. P. (2001). In vitro effects of cadmium on two different animal cell models. Toxicology in Vitro, 15, 511–517.CrossRefGoogle Scholar
  46. Oliver, L. M., & Fisher, W. S. (1995). Comparative form and function of oyster Crassostrea virginica hemocytes from Chesapeake Bay (Virginia) and Apalachicola Bay (Florida). Diseases of Aquatic Organisms, 22, 217–225.CrossRefGoogle Scholar
  47. Oubella, R., Maes, P., Paillard, C., & Auffret, M. (1993). Experimentally induced variation in hemocyte density for Ruditapes philippinarum and R. decussatus (Mollusca, Bivalvia). Diseases of Aquatic Organisms, 15, 193–197.CrossRefGoogle Scholar
  48. Park, J. D., Liu, Y., & Klaassen, C. D. (2001). Protective effect of metallothionein against toxicity of cadmiun and other metals. Toxicology, 163(2–3), 93–100.CrossRefGoogle Scholar
  49. Pech, L. L., & Strand, M. R. (1996). Granular cells are required for encapsulation of foreign targets by insect haemocytes. Journal of Cell Science, 109, 2053–2060.Google Scholar
  50. Perez, D. G., & Fontanetti, C. S. (2008). Respostas tissulares do intestino médio do diplópodo Rhinocricus padbergi exposto a substrato contendo lodo de esgoto. Dissertation, Universidade Estadual Paulista.Google Scholar
  51. Pipe, R. K. (1992). Generation of reactive oxygen metabolites by the haemocytes of the mussel Mytilus edulis. Developmental and Comparative Immunology, 16, 111–122.CrossRefGoogle Scholar
  52. Pipe, R. K., & Coles, J. A. (1995). Environmental contaminants influencing immune function in marine bivalve molluscs. Fish and Shellfish Immunology, 5, 581–595.CrossRefGoogle Scholar
  53. Pipe, R. K., Coles, J. A., Carissan, F. M. M., & Ramanathan, K. (1999). Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquatic Toxicology, 46, 43–54.CrossRefGoogle Scholar
  54. Pirie, B. J. S., George, S. G., Lytton, D. G., & Thomson, J. D. (1984). Metal-containing blood cells of oysters: Ultrastructure histochemistry X-ray microanalysis. Journal of the Marine Biological Association of the United Kingdom, 64, 115–123.CrossRefGoogle Scholar
  55. Radford, J. L., Hutchinson, A. E., Burandt, M., & Raftos, D. A. (2000). Effects of metal-based environmental pollutants on tunicate hemocytes. Journal of Invertebrate Pathology, 76, 242–248.CrossRefGoogle Scholar
  56. Ratcliffe, N. A., Rowley, A. F., Fitzgeald, S. W., & Rhodes, C. P. (1985). Invertebrate immunity: Basic concepts and recents advances. International Review of Cytology, 97, 183–350.CrossRefGoogle Scholar
  57. Ribeiro, C., & Brehélin, M. (2006). Insect haemocytes: What type of cell is that? Journal of Insect Physiology, 52, 417–429.CrossRefGoogle Scholar
  58. Robinson, W. E., & Ryan, D. K. (1988). Transport of cadmium and other metals in the blood of the bivalve mollusc Mercenaria mercenaria. Marine Biology, 97, 101–109.CrossRefGoogle Scholar
  59. Roesijadi, G., Brubacher, L. L., Unger, M. E., & Anderson, R. S. (1997). Metallothionein mRNA induction and generation of reactive oxygen species in molluscan hemocytes exposed to cadmiun in vitro. Comparative Biochemistry and Physiology, 118C(2), 171–176.Google Scholar
  60. Russo, J., Brehélin, M., & Carton, Y. (2001). Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. Journal of Insect Physiology, 47, 167–172.CrossRefGoogle Scholar
  61. Sauvé, S., Brousseau, P., Pellerin, J., Morin, Y., Senécal, P., Goudreau, P., et al. (2002). Phagocytic activity of marine and freshwater bivalves: In vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquatic Toxicology, 58, 189–200.CrossRefGoogle Scholar
  62. Silva, J. E. B., Boleli, I. C., & Simões, Z. L. P. (2002). Hemocyte types and total and differential counts in unparasitized and parasitized Anastrepha obliqua (Diptera, Tephritidae) larvae. Brazilian Journal of Biology, 62(4a), 689–699.CrossRefGoogle Scholar
  63. Snyman, R. G., Reinecke, S. A., & Reinecke, A. J. (2000). Hemocytic lysosome response in the snail Helix aspersa after exposure to the fungicide cooper oxychloride. Archives of Environmental Contamination and Toxicology, 39, 480–485.CrossRefGoogle Scholar
  64. Sorvari, J., Rantala, L. M., Rantala, M. J., Hakkarainen, H., & Eeva, T. (2007). Heavy metal pollution disturbs immune response in wild ant populations. Environmental Pollution, 145, 324–328.CrossRefGoogle Scholar
  65. Truscott, R., & White, K. N. (1990). The influence of metal and temperature stress on the immune system of crabs. Functional Ecology, 4, 455–461.CrossRefGoogle Scholar
  66. Tzou, P., Gregorio, E., & Lemaitre, B. (2002). How Drosophila combats microbial infection: A model to study innate immunity and host–pathogen interactions. Current Opinion in Microbiology, 5, 102–110.CrossRefGoogle Scholar
  67. van de Braak, K. (2002). Haemocytic defence in black tiger shrimp (Penaeus monodon). Thesis, Wageningen University.Google Scholar
  68. Vasak, M. (2005). Advances in metallothionein structure and functions. Journal of Trace Elements in Medicine and Biology, 19(1), 13–17.CrossRefGoogle Scholar
  69. Viarengo, A., Lowe, D., Bolognesi, C., Fabbri, E., & Koehler, A. (2007). The use of biomarkers in biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative Biochemistry and Physiology part C: Toxicology and Pharmacology, 146(3), 281–300.CrossRefGoogle Scholar
  70. Victor, B. (1993). Responses of hemocytes and gill tissues to sublethal cadmium chloride poisoning in the crab Paratelphusa hydrodromous (Herbst). Archives of Environmental Contamination and Toxicology, 24, 432–439.CrossRefGoogle Scholar
  71. Winston, G. W., Moore, M. N., Kirchin, M. A., & Soverchia, C. (1996). Production of reactive oxygen species by hemocytes from the marine mussel, Mytilus edulis: Lysosomal localization and effect of xenobiotics. Comparative Biochemistry and Physiology, 113C(2), 221–229.Google Scholar
  72. Wong, S., Fournier, M., Coderre, D., Banska, W., & Krzystyniak, K. (1992). Environmental immunotoxicology. In D. Peakall (Ed.), Animal biomarkers as pollution indicators (pp. 167–189). London: Chapman and Hall.Google Scholar
  73. Xylander, W. E. R. (2009). Hemocytes in Myriapoda (Arthropoda): A review. Invertebrate Survival Journal, 6, 114–124.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Danielli Giuliano Perez
    • 1
  • Carmem Silvia Fontanetti
    • 1
  1. 1.Department of Biology—Institute of BiosciencesUNESPRio ClaroBrazil

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