Hostname: page-component-6b989bf9dc-wj8jn Total loading time: 0 Render date: 2024-04-14T16:06:22.300Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructural Alterations of Midgut Epithelium, But Not Greater Wing Fluctuating Asymmetry, in Paper Wasps (Polistes dominula) from Urban Environments

Part of: Micrographia Collection

Published online by Cambridge University Press:  21 March 2018

Carlo Polidori ,
Agustín Pastor ,
Alberto Jorge  and
José Pertusa
Carlo Polidori*
Affiliation:
Instituto de Ciencias Ambientales (ICAM), Universidad de Castilla-La Mancha, Avenida Carlos III, s/n, 45071 Toledo, Spain
Agustín Pastor
Affiliation:
Departament de Química Analítica, Universitat de València, C/ Dr Moliner 50, ES-46100, Burjassot, Valencia, Spain
Alberto Jorge
Affiliation:
Laboratorio de Microscopia, Museo Nacional de Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, ES-28006, Madrid, Spain
José Pertusa
Affiliation:
Departament de Biologia Funcional i Antropologia Física, Universitat de València, C/ Dr Moliner 50, ES-46100, Burjassot, Valencia, Spain
*
Author for correspondence: Carlo Polidori, E-mail: carlo.polidori@uclm.es
Get access

Abstract

Polistes paper wasps can be used to monitor trace metal contaminants, but the effects of pollution on the health of these insects are still unknown. We evaluated, in a south-eastern area of Spain, whether workers of Polistes dominula collected at urban and rural sites differ in health of midgut tissue and in fluctuating asymmetry, an estimate of developmental noise. We found that wasps collected at the urban sites had abundant lead (Pb)-containing spherites, which were less visible in wasps from the rural sites. Evident ultrastructural alterations in the epithelium of the midgut of the wasps collected at the urban sites included broken and disorganized microvilli, a high amount and density of heterochromatin in the nucleus of epithelial cells, cytoplasmic vacuolization and mitochondrial disruptions. Altogether, these findings suggest a negative effect on the transmembrane transport and a less efficient transcription. On the contrary, a healthy epithelium was observed in wasps from the rural sites. These differences may be preliminarily linked with levels of lead pollution, given that wasps from urban sites had double the Pb concentrations of wasps from rural sites. Level of fluctuating asymmetry was unrelated to wasp origin, thus suggesting no link between developmental noise and Pb-driven pollution.

Keywords

urbanizationmidguttissue damagesfluctuating asymmetrywasp
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 24 , Issue 2 , April 2018 , pp. 183 - 192
Copyright
© Microscopy Society of America 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ballan-Dufrançais, CN (2002) Localization of metals in cells of pterygote insects. Microsc Res Tech 56, 403–420.Google Scholar
Beani, L, Dallai, R, Mercati, D, Cappa, F, Giusti, F and Manfredini, F (2011) When a parasite breaks all the rules of a colony: Morphology and fate of wasps infected by a strepsiptera endoparasite. Anim Behav 82, 1305–1312.Google Scholar
Beasley, DAE, Bonisoli-Alquati, A and Mousseau, TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecol Indic 30, 218–226.CrossRefGoogle Scholar
Braeckman, BP (2011) Heavy metal toxicity in an insect cell line (methyl-HgCl, HgCl2, CdCl2 and CuSO4). In Cellular Effects of Heavy Metals, Banfalvi, G (Ed.), pp. 115–144. New York: Springer.Google Scholar
Connell, DW and Miller, GJ (1984) Chemistry and Ecotoxicology of Pollution. New York: Wiley-Interscience.Google Scholar
Dauwe, T, Janssens, E and Eens, M (2006) Effects of heavy metal exposure on the condition and health of adult great tits (Parus major). Environ Pollut 40, 71–78.Google Scholar
Depledge, MH, Weeks, JM and Bjerregaard, P (1994) Heavy metals. In: Handbook of Ecotoxicology, vol. 2, Calow, P (Ed.), pp. 79–105. Oxford: Blackwell.Google Scholar
Eeva, T, Tanhuanpää, S, Rabergh, C, Airaksinen, S, Nikinmaa, M and Lehikoinen, M (2000) Biomarkers and fluctuating asymmetry as indicators of pollution-induced stress in two hole-nesting passerines. Funct Ecol 14, 235–243.Google Scholar
Eeva, T, Sorvari, J and Kolvunen, V (2004) Effects of heavy metal pollution on red wood ant (Formica s. str.) populations. Environ Pollut 132, 533–539.CrossRefGoogle Scholar
Evans, JE, Hetherington, C, Kirkland, AI, Chang, LY, Stahlberg, H and Browning, ND (2008) Low-dose aberration corrected cryo-electronmicroscopy of organic specimens. Ultramicroscopy 108, 1636–1644.Google Scholar
Glaeser, RM (1971) Limitations to significant information in biological electron microscopy as a result of radiation damage. J Ultrastruct Res 36, 466–482.Google Scholar
Goulson, D, Whitehorn, P and Fowley, M (2012) Influence of urbanisation on the prevalence of protozoan parasites of bumblebees. Ecol Entomol 37, 83–89.Google Scholar
Gramigni, E, Calusi, S, Gelli, G, Giuntini, L, Massi, M, Delfino, G, Chelazzi, G, Baracchi, D, Frizzi, F and Santini, G (2013) Ants as bioaccumulators of metals from soils: Body content and tissue-specific distribution of metals in the ant Crematogaster scutellaris . Eur J Soil Biol 58, 24–31.Google Scholar
Gregory, MA, Marshall, DJ, George, RC, Anandraj, A and McClurg, TP (2002) Correlations between metal uptake in the soft tissue of Perna perna and gill filament pathology after exposure to mercury. Mar Pollut Bull 45, 114–125.Google Scholar
Grewal, SI and Jia, S (2007) Heterochromatin revisited. Nat Rev Genet 8, 35–46.Google Scholar
Grześ, IM (2010) Ants and heavy metal pollution – a review. Eur J Soil Biol 46, 350–355.Google Scholar
Görür, G (2006) Developmental instability in cabbage aphid (Brevicoryne brassicae) populations exposed to heavy metal accumulated host plants. Ecol Indic 6, 743–748.Google Scholar
Hay, BA, Huh, JR and Guo, M (2004) The genetics of cell death: approaches, insights and opportunities in Drosophila . Nat Rev 5, 911–922.Google Scholar
Hopkin, SP (1989) Ecophysiology of Metals in Terrestrial Invertebrates. New York: Elsevier Applied Science.Google Scholar
Klumpp, A, Klumpp, G and Domingos, M (1994) Plants as bioindicators of air pollution at the Serra do Mar near the industrial complex of Cubatão. Brazil Environ Pollut 85, 109–116.Google Scholar
Köhler, H-R (2002) Localization of metals in cells of saprophagous soil arthropods (Isopoda, Diplopoda, Collembola). Microsc Res Tech 56, 393–401.Google Scholar
Köhler, H-R and Triebskorn, R (1998) Assessment of the cytotoxic impact of heavy metals on soil invertebrates using a protocol integrating qualitative and quantitative components. Biomarkers 3, 109–127.Google Scholar
Koponen, S and Niemelä, P (1995) Ground-living arthropods along pollution gradient in boreal pine forest. Entomol Fennica 6, 127–131.Google Scholar
Kowalczyk, JK and Watala, C (1989) Content of some heavy metal ions in various developmental stages of the social wasp Dolichovespula saxonica (Fabr.) (Hymenoptera, Vespidae). Bull Environ Contam Toxicol 43, 415–420.Google Scholar
Kozlov, MV, Wilsey, BJ, Koricheva, J and Haukioja, E (1996) Fluctuating asymmetry of birch leaves increases under pollution impact. J Appl Ecol 33, 1489–1495.Google Scholar
Lipovsek, S, Letofsy-Papst, I, Hofer, F and Pabst, MA (2002) Seasonal and age-dependent changes of the structure and chemical composition of the spherites in the midgut gland of the harvestmen Gyas annulatus (Opiliones). Micron 33, 647–654.Google Scholar
Loeb, MJ, Hakim, RS, Martin, P, Narang, N, Goto, S and Takeda, M (2000) Apoptosis in cultured midgut cells from Heliothis virescens larvae exposed to various conditions. Arch Insect Biochem Physiol 45, 12–23.Google Scholar
Markert, B (2007) Definitions and principles for bioindication and biomonitoring of trace metals in the environment. J Trace Elem Med Biol 21, 77–82.Google Scholar
Markert, B and Wünschmann, S (2011) Bioindicators and biomonitors: Use of organisms to observe the influence of chemicals on the environment. In: Organic Xenobiotics and Plants: Action and Ecophysiology, Schroeder, P and Collins, C (Eds.), pp. 217–236. New York: Springer.Google Scholar
Martinez-Haro, M, Green, AJ and Mateo, R (2011) Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environ Res 111, 530–538.Google Scholar
Markow, TA (1995) Evolutionary ecology and developmental instability. Annu Rev Entomol 40, 105–120.Google Scholar
Müller, SA and Engel, A (2006) Biological scanning transmission electron microscopy: Imaging and single molecule mass determination. Chimia 60, 749–753.Google Scholar
Nunes, LA, de Araújo, ED and Marchini, LC (2015) Fluctuating asymmetry in Apis mellifera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments. Rev Biol Trop 63, 673–682.Google Scholar
Nursita, AI, Singh, B and Lees, E (2004) Evaluation of cadmium toxicity to Collembola (Proisotoma minuta) using electron microscopy. In SuperSoil 2004. Proceedings 3rd Australian New Zealand Soils Conference’, Singh B (Ed.), pp. 1–8. Gosford, NSW: The Regional Institute Ltd. Available at: www.regional.org.au/au/asssi/supersoil2004/.Google Scholar
Osman, W and Shonouda, M (2017) X-ray metal assessment and ovarian ultrastructure alterations of the beetle, Blaps polycresta (Coleoptera, Tenebrionidae), inhabiting polluted soil. Environ Sci Pollut Res 24, 14867–14876.Google Scholar
Ozkaya, D, Zhou, W, Thomas, JM, Midgley, PA, Keast, VJ and Hermans, S (1999) High-resolution imaging of nanoparticle bimetallic catalysts supported on mesoporous silica. Catal Lett 60, 113–120.Google Scholar
Palmer, AR (1994) Fluctuating asymmetry analyses: A primer. In Developmental Instability: Its Origins and Evolutionary Implications, Markow TA (Ed.), pp. 335–364. Dordrecht, The Netherlands: Kluwer.Google Scholar
Parsons, PA (1990) Fluctuating asymmetry: An epigenetic measure of stress. Biol Rev 65, 131–145.Google Scholar
Perugini, M, Manera, M, Grotta, L, Abete, MC and Tarasco, R (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: Honeybees as bioindicators. Biol Trace Elem Res 140, 170–176.Google Scholar
Pigino, G, Migliorini, M, Paccagnini, E, Bernini, F and Leonzio, C (2005) Fine structure of the midgut and Malpighian papillae in Campodea (Monocampa) quilisi Silvestri, 1932 (Hexapoda, Diplura) with special reference to the metal composition and physiological significance of midgut intracellular electron-dense granules. Tissue Cell 37, 223–232.Google Scholar
Pigino, G, Migliorini, M, Paccagnini, E and Bernini, F (2006) Localization of heavy metals in the midgut epithelial cells of Xenillus tegeocranus (Hermann, 1804) (Acari: Oribatida). Ecotoxic Environ Safety 64, 257–263.Google Scholar
Rabitsch, WB (1997) Tissue-specific accumulation patterns of Pb, Cd, Cu, Zn, Fe, and Mn in workers of three ant species (Formicidae, Hymenoptera) from a metal-polluted site. Arch Environ Contam Toxicol 32, 172–177.Google Scholar
RaesH,R H,R, Cornelis, R and Rzeznik, U (1992) Distribution, accumulation and depuration of administered lead in adult honeybees. Sci Total Environ 113, 269–279.Google Scholar
Rainbow, PS (2006) Biomonitoring of trace metals in estuarine and marine environments. Australas J Ecotoxicol 12, 107–122.Google Scholar
Rainbow, PS (2007) Trace metal bioaccumulation: Models, metabolic availability and toxicity. Environ Int 33, 576–582.Google Scholar
Rodrigues, A, Cunha, L, Amaral, A, Medeiros, J and Garcia, P (2008) Bioavailability of heavy metals and their effects on the midgut cells of a phytopaghous insect inhabiting volcanic environments. Sci Total Environ 406, 116–122.Google Scholar
Rost-Roszkowska, MM, Poprawa, I, Klag, J, Migula, P, Mesjasz-Przybyłowicz, J and Przybyłowicz, W (2008) Degeneration of the midgut epithelium in Epilachna cf nylanderi (Insecta, Coccinellidae): Apoptosis, autophagy and necrosis. Can J Zool 86, 1179–1188.Google Scholar
Scheifler, R, Coeurdassier, M, Morilhat, C, Bernard, N, Faivre, B, Flicoteaux, P, Giraudoux, P, Noël, M, Piotte, P, Rieffel, D, de Vaufleury, A and Badot, PM (2006) Lead concentrations in feathers and blood of common blackbirds (Turdus merula) and in earthworms inhabiting unpolluted and moderately polluted urban areas. Sci Total Environ 371, 197–205.Google Scholar
Schilling, J and Lehman, M (2002) Bioindication of atmospheric heavy metal deposition in the Southeastern US using the moss Thuidium delicatulum . Atmos Environ 36, 1611–1681.Google Scholar
Scheiner, SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24, 35–68.Google Scholar
Sohal, RS, Peters, PD and Hall, TA (1977) Origin, ultrastructure, composition and age dependence of mineralized dense bodies (concretions) in the midgut epithelium of the adult housefly, Musca domestica . Tissue Cell 9, 87–102.Google Scholar
Szentgyörgyi, H, Moroń, D, Nawrocka, A, Tofilski, A and Woyciechowski, M (2017) Forewing structure of the solitary bee Osmia bicornis developing on heavy metal pollution gradient. Ecotoxicology 26, 1031–1040.Google Scholar
Takeda, M, Sakai, T, Fujisawa, Y, Narita, M, Iwabuchi, K and Loeb, MJ (2001) Cockroach midgut peptides that regulate cell proliferation, differentiation and death in vitro . In Vitro Cell Develop Biol Anim 37, 343–347.Google ScholarPubMed
Treacy, MMJ and Howie, A (1980) Contrast effects in the transmission electron microscopy of supported crystalline catalyst particles. J Catal 63, 265–269.Google Scholar
Triebskorn, R and Köhler, H-R (1996) The impact of heavy metals on the grey garden slug Deroceras reticulatum (Müller): Metal storage, cellular effects and semi-quantitative evaluation of metal toxicity. Environ Pollut 93, 327–343.Google Scholar
Turillazzi, S and West-Eberhard, MJ (Eds.) 1996) Natural History and Evolution of Paper Wasps. Oxford: Oxford University Press.CrossRefGoogle Scholar
Urbini, A, Sparvoli, E and Turillazzi, S (2006) Social paper wasps as bioindicators: A preliminary research with Polistes dominulus (Hymenoptera Vespidae) as a trace metal accumulator. Chemosphere 64, 697–703.Google Scholar
Uwo, MF, Vi-Tei, K, Park, P and Takeda, M (2002) Replacement of midgut epithelium in the greater wax moth Galleria mellonela during larval-pupal moult. Cell Tissue Res 308, 319–331.Google Scholar
Vaidyanathan, R and Scott, TW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11, 1643–1651.Google Scholar
Valkama, J and Kozlov, MV (2001) Impact of climatic factors on the developmental stability of mountain birch growing in a contaminated area. J Appl Ecol 38, 665–673.Google Scholar
Van Straalen, N and Roelofs, D (2005) Cadmium tolerance in a soil arthropod. A model of real-time microevolution. Entomol Ber (Amst) 65, 105–111.Google Scholar
Xia, Q, Sun, H, Hu, X, Shu, Y, Gu, D and Zhang, G (2005) Apoptosis of Spodoptera litura larval hemocytes induced by heavy metal zinc. Chin Sci Bull 50, 2856–2860.Google Scholar
Zhang, Y, Lambiase, L, Fasola, M, Gandini, C, Grigolo, A and Laudani, U (2001) Mortality and tissue damage by heavy metal contamination in the German cockroach, Blattella germanica (Blattaria, Blattellidae). It J Zool 68, 137–145.Google Scholar