Abstract
In order to be a relevant indicator of exposure towards teratogenic stressors, morphological defects should not be passed on to the next generation. In this study, we compare morphological variations in Chironomids collected from a contaminated river stretch with those of their progeny, reared in uncontaminated sediment under laboratory conditions. We focused on mentum defects (deformities, fluctuating asymmetry and mean shape change), measured by geometric morphometrics. We observed no significant variation in deformity rate between the parental generation and its progeny. On the contrary, we observed a significant increase in fluctuating asymmetry and a significant decrease in mentum centroid size in the offspring. Our results suggest that shape defects are not caused by direct exposure to teratogenic stressors alone. We propose four hypotheses to explain this: (a) teratogenic contaminants are present in egg-clutches, (b) contaminants at the sampling site have mutagenic effects, (c) costs of tolerance, and (d) contamination-induced genetic impoverishment.
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References
Agra AR, Soares AMVM, Barata C (2011) Life-history consequences of adptation to pollution. “Daphnia longispina clones historically exposed to copper”. Ecotoxicology 20:552–562
Alibert P, Auffray JC (2003) Genomic coadaptation, outbreeding depression, and developmental instability. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 116–134
Allen D, Leamy L (2001) 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects size and shape, but not asymmetry, of mandibles in mice. Ecotoxicology 10:167–176
Arambourou H, Beisel JN, Branchu P, Debat V (2012) Patterns of fluctuating asymmetry and shape variation in Chironomus riparius (Diptera, Chironomidae) exposed to nonylphenol or lead. PLoS One 7:e48844
Arambourou H, Beisel JN, Branchu P, Debat V (2014) Exposure to sediments from polluted rivers has limited phenotypic effects on larvae and adults of Chironomus riparius. Sci Total Environ 484:92–101
Arimoro FO, Ikomi RB, Iwegbue CMA (2007) Water quality changes in relation to Diptera community patterns and diversity measured at an organic effluent impacted stream in the Niger Delta, Nigeria. Ecol Indic 7:541–552
Bird GA (1994) Use of chironomid deformities to assess environmental degradation in the Yamaska River, Quebec. Environ Monit Assess 30:164–175
Bird GA (1995) The effect of 210Pb and stable lead on the induction of menta deformities in Chironomus tentans larvae and on their growth and survival. Environ Toxicol Chem 14:2125–2130
Bleeker EA, Leslie HA, Groenendijk D et al (1999) Effect of exposure to azaarenes on emergence and mouthpart development in the midge Chironomus riparius (Diptera: Chironomidae). Environ Toxicol Chem 18:1829–1834
Boerger HJ, Clifford HF, Davies RW (1982) Density and microdistribution of chironomid larvae in an Alberta brown-water stream. Revue Canadienne de Zoologie 60:913–920
Bonada N, Williams DD (2002) Exploration of the utility of fluctuating asymmetry as an indicator of river condition using larvae of the caddisfly Hydropsyche morosa (Trichoptera: Hydropsychidae). Hydrobiologia 481:147–156
Bookstein F (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge
Chen G, White PA (2004) The mutagenic hazards of aquatic sediments: a review. Mutat Res Rev Mutat Res 567:151–225
Clarke GM (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ Pollut 82:207–211
Coustau C, Chevillon C, Ffrench-Constant R (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15:378–383
Coutellec MA, Barata C (2013) Special issue on long-term ecotoxicological effects: an introduction. Ecotoxicology 22:763–766
Dickman M, Brindle I, Benson M (1992) Evidence of teratogens in sediments of the Niagara river watershed as reflected by Chironomid (Dipera: Chironomidae) deformities. J Great Lakes Res 18:467–480
Drover S, Leung B, Forbes MR et al (1999) Lake pH and aluminium concentration: consequences for developmental stability of water strider Rheumatobates rileyi (Hemiptera: Gerridae). Can J Zool 77:157–161
Epler J (2001) Identification manual for the larval Chironomidae (Diptera) of North and South Carolina. North Carolina Department of Environment and Natural Resources. St. Johns River Water Management District, Raleigh
Franz ED, Wiramanaden CI, Janz DM, Pickering IJ, Liber K (2011) Selenium bioaccumulation and speciation in Chironomus dilutus exposed to water-borne selenate, selenite, or seleno-DL-methionine. Environ Toxicol Chem 30:2292–2299
Gower AM, Buckland PJ (1978) Water quality and the occurrence of Chironomus riparius Meigen (Diptera: Chironomidae) in a stream receiving sewage effluent. Freshw Biol 8:153–164
Graham J, Emlen J, Freeman D (1993) Developmental stability and its applications in ecotoxicology. Ecotoxicology 2:175–184
Groenendijk D, Zeinstra L, Postma J (1998) Fluctuating asymmetry and mentum gaps in populations of midge Chironomus riparius (Diptera: Chironomidae) from a metal contaminated river. Environ Toxicol Chem 17:1999–2005
Hoffmann A, Woods R, Collins E et al (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Aust J Entomol 44:233–243
Hwang H, Fisher SW, Landrum PF (2001) Identifying body residues of HCBP associated with 10-d mortality and partial life cycle effects in the midge, Chironomus riparius. Aquat Toxicol 52:251–267
Janssens de Bisthoven L, Postma J, Parren P et al (1998a) Relations between heavy metals in aquatic sediments and in Chironomus larvae of Belgian lowland rivers and their morphological deformities. J Can Sci Halieut Aquat 55:688–703
Janssens de Bisthoven L, Vermeulen A, Ollevier F (1998b) Experimental induction of morphological deformities in Chironomus riparius larvae by chronic exposure to copper and lead. Arch Environ Contam Toxicol 35:249–256
Jeyasingham K, Ling N (1997) Head capsule deformities in Chironomus zealandicus (Diptera: Chironomidae): Influence of site and substrate. N Z J Mar Freshw Res 31:175–184
Klingenberg C (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol 11:353–357
Klingenberg C, McIntyre G (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52:1363–1375
Klingenberg CP, Barluenga M, Mayer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920
Leamy L, Klingenberg C (2005) The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol Syst 36:1–21
Lee SD, Choi J (2006) Multilevel evaluation of nonylphenol toxicity in fourth-instar larvae of Chironomus riparius (Diptera, Chironomidae). Environ Toxicol Chem 25:3006–3014
Leung B, Mineau P, Knopper L (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 415–426
Madden CP, Suter PJ, Nicholson BC, Austin AD (1992) Deformities in chironomid larvae as indicators of pollution (pesticide) stress. Neth J Aquat Ecol 26:551–557
Martinez EA, Barry CM, Schaumloffel J, Dasgupta N (2001) Induction of morphological deformities in Chironomus tentans exposed to zinc and lead spiked sediment. Environ Toxicol Chem 20:2475–2481
Martinez EA, Moore BC, Schaumloffel J, Dasgupta N (2002) The potential association between menta deformities and trace elements in Chironomidae (Diptera) taken from a heavy metal contaminated river. Arch Environ Contam Toxicol 42:286–291
Martinez EA, Moore B, Schaumloffel J, Dasgupta N (2003) Morphological abnormalities in Chironomus tentans exposed to cadmium—and copper-spiked sediments. Ecotoxicol Environ Saf 55:204–212
Martinez EA, Moore B, Schaumloffel J, Dasgupta N (2004) Teratogenic versus mutagenic abnormalities in Chironomid larvae exposed to zinc and lead. Arch Environ Contam Toxicol 47:193–198
Michailova P, Petrova N, Sella G, Bovero B, Ramella L, Regoli F, Zelano V (2001) Genotoxic effects of chromium on polytene chromosomes of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Caryologia 54:59–71
Michailova P, Petrova N, Ilkova J, Bovero S, Brunetti S, White K, Sella G (2006) Genotoxic effect of copper on salivary gland polytene chromosomes of Chironomus riparius Meigen 1804 (Diptera, Chironomidae). Environ Pollut 144:647–654
Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36:235–247
Mogren CL, von Kiparski GR, Guntram R, Parker DR, Trumble JT (2012) Survival, reproduction, and arsenic body burdens in Chironomus riparius exposed to arsenate and phosphate. Sci Total Environ 425:60–65
Mogren CL, Webb SM, Walton WE, Trumble JT (2013) Micro X-ray absorption spectroscopic analysis of arsenic localization and biotransformation in Chironomus riparius Meigen (Diptera: Chironomidae) and Culex tarsalis Coquillett (Culicidae). Environ Pollut 180:78–83
Nowak C, Jost D, Vogt C, Oetken M, Schwenk K, Oehlmann J (2007a) Consequences of inbreeding and reduced genetic variation on tolerance to cadmium stress in the midge Chironomus riparius. Aquat Toxicol 85:278–284
Nowak C, Vogt C, Diogo B, Schwenk K (2007b) Genetic impoverishment in laboratory cultures of the test organism Chironomus riparius. Environ Toxicol Chem 26:1018–1022
Nowak C, Vogt C, Pfenninger M, Schwenk K, Oehlmann J, Streit B, Oetken M (2009) Rapid genetic erosion in pollutant-exposed experimental chironomid populations. Environ Pollut 157:881–886
OECD (2004) Test No. 218: Sediment-water chironomid toxicity using spiked sediment, OECD guidelines for the testing of chemicals, section 2. OECD publishing, Paris
Oliveira EE, Guedes RNC, Totóla MR, De Marco P Jr (2007) Competition between insecticide-susceptible and -resistant populations of the maize weevil, Sitophilus zeamais. Chemosphere 69:17–24
Palmer A, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, Oxford, pp 279–319
Pelabon C, Hanssen T (2008) On the adaptative accuracy of directional asymmetry in insect wing size. Evolution 62:2855–2867
Posthuma L, Van Straalen NM (1993) Heavy-metal adaptation in terrestrial invertebrates: a review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 106:11–38
Postma JF, van Kleunen A, Admiraal W (1995a) Alterations in life-history traits of Chironomus riparius (Diptera) obtained from metal contaminated rivers. Arch Environ Contam Toxicol 29:469–475
Postma JF, Kyed M, Admiraal W (1995b) Site specific differenciation in metal tolerance in the midge Chironomus riparius (Diptera, Chironomidae). Hydrobiologia 315:159–165
Reynolds SK, Ferrington LC (2001) Temporal and taxonomic patterns of mouthpart deformities in larval midges (Diptera: Chironomidae) in relation to sediment chemistry. J Freshw Ecol 16:14–28
Rohlf F (2010) TPS DIG, SUNY Stony Brook. http://life.bio.sunysb.edu/morph. Accessed 9 Sept 2010
R Development Core Team (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org. Accessed 30 May 2012
Servia M, Cobo F, González M (2000) Incidence and causes of deformities in recently hatched larvae of Chironomus riparius MEIGEN, 1804 (Diptera, Chironomidae). Arch Hydrobiol 149:387–401
Servia MJ, Cobo F, González MA (2004) Multiple-trait analysis of fluctuating asymmetry levels in anthropogenically and naturally stressed sites: a case study using Chironomus Riparius Meigen, 1804 larvae. Environ Monit Assess 90:101–112
Sharley DJ, Pettigrove V, Parsons YM (2004) Molecular identification of Chironomus spp (Diptera) for biomonitoring of aquatic ecosystems. Aust J Entomol 43:359–365
Sibly RM, Calow P (1989) A life-cycle theory of responses to stress. Biol J Linn Soc 37:101–116
van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142
Vogt C, Langer-Jaesrich M, Elsässer O, Schmitt C, Van Dongen S, Köhler HR, Oehlmann J, Nowak C (2013) Effects of inbreeding on mouthpart deformities of Chironomus riparius under sublethal pesticide exposure. Environ Toxicol Chem 32:423–425
Warwick WF (1990) Morphological deformities in Chironomidae (Diptera) larvae from the lac St. Louis and Laprairie bassins of the St. Lawrence river. J Great Lakes Res 16:185–208
Wene G (1940) The soil as an ecological factor in the abundance of aquatic chironomid larvae. Ohio J Sci 40:193–199
Wiederholm T (1984) Incidence of deformed chironomid larvae (Diptera: Chironomidae) in Swedish lakes. Hydrobiologia 109:243–249
Acknowledgments
Financial support for this study came from the French Ministry of Ecology, Sustainable Development and Energy, and from the French Institute of Science and Technology for Transport, Development and Networks. Comments by anonymous reviewers considerably improved the manuscript.
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Arambourou, H., Branchu, P. & Beisel, JN. Increase in Developmental Instability in a Field-Collected Chironomus Population Maintained Under Laboratory Conditions. Bull Environ Contam Toxicol 94, 681–687 (2015). https://doi.org/10.1007/s00128-015-1497-5
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DOI: https://doi.org/10.1007/s00128-015-1497-5