Skip to main content
Log in

Measure of environmental stress on Porcellio laevis Latreille, 1804 sampled near active Tunisian industrial areas

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This study aimed to observe the type of asymmetry exhibited by Porcellio laevis sampled from 15 sites belonging to Tunisian industrialized areas. Physicochemical parameters such as pH, organic matter and CaCO3 contents were measured in soils. Moreover, Cd, Pb, Zn, and Cu concentrations were determined in both soils and woodlice. Additionally, 10 metrical traits were measured to evaluate the type of asymmetry on individuals: the basis, the second and the third articles of the antenna, the first article of the flagellum of the antenna and the merus, the carpus, and the propodus of the sixth and the seventh pereopods. Among the 531 measured individuals, 432 exhibited fluctuating asymmetry (FA) while the remaining individuals exhibited antisymmetry or directional asymmetry. The data obtained were analyzed using a multivariate statistical analysis. Contrary to our hypothesis, the results showed that individuals from contaminated sites have a low FA level, whereas those from uncontaminated sites have a high FA level, particularly females but with some exceptions. Variations in FA level in the traits and populations studied and its usefulness as a stress indicator were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agodi A, Oliveri-Conti G, Barchitta M, Quattrocchi A, Lombardo BM, Montesanto G, Messina G, Fiore M, Ferrante M (2015) Validation of Armadillo officinalis Dumèril, 1816 (Crustacea, Isopoda, Oniscidea) as a bioindicator: in vivo study of air benzene exposure. Ecotoxicol Environ Saf 114:171–178

    Article  CAS  Google Scholar 

  • Alaya-Ltifi L, Chokri MA, Selmi S (2012) Breeding performance of passerines in a polluted oasis habitat in southern Tunisia. Ecotoxicol Environ Saf 79:170–175

    Article  CAS  Google Scholar 

  • Alaya-Ltifi L, Hayder-Benyahya N, Selmi S (2015) Condition and health of Rufous Bush Robin (Cercotrichas galactotes) nestlings in a polluted oasis habitat in Southern Tunisia. Bull Environ Contam Toxicol 94:732–737

    Article  CAS  Google Scholar 

  • Barhoumi S, Messoudi I, Deli T, Said K, Kerkn A (2009) Cadmium bioaccumulation in three benthic fish species, Salaria basilisca, Zosterisessor ophiocephalus and Solea vulgaris collected from the Gulf of Gabes in Tunisia. J Environ Sci 21:980–984

    Article  CAS  Google Scholar 

  • Băncilă R, van Gelder I, Rotteveel E, Loman J, Arntzen JW (2010) Fluctuating asymmetry is a function of population isolation in island lizards. J Zool 282:266–275

    Article  Google Scholar 

  • Beasley DE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indic 30:218–226

    Article  Google Scholar 

  • Ben Garali A, Ouakad M, Gueddari M (2009) Bilans hydrologiques de la lagune de Bizerte (Nord-Est de la Tunisie). J Water Sci 22:525–534

    Google Scholar 

  • Boldina-Cosqueric I, Amiard JC, Amiard-Triquet C, Dedourge-Geffard O, Metais I, Mouneyrac C, Moutela B, Berthet B (2010) Biochemical physiological and behavioural markers in the endobenthic bivalve Scrobicularia plana as tools for the assessment of estuarine sediment quality. Ecotoxicol Environ Saf 73(7):1733–1741

    Article  CAS  Google Scholar 

  • Bridle JR, Vines TH (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol Evol 22:140–147

    Article  Google Scholar 

  • Brown JH, Stevens GC, Kaufman DM (1996) The geographic range: size, shape, boundaries, and internal structure. Annu Rev Ecol Evol Syst 27:597–623

    Article  Google Scholar 

  • Chang X, Zhai B, XLiu X, Wang M (2007) Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (Selys) (Odonata: Zygoptera) larvae. Ecotoxicol Environ Saf 67:120–127

    Article  CAS  Google Scholar 

  • Costa M, Mateus RP, Moura MO (2015) Constant fluctuating asymmetry but not directional asymmetry along the geographic distribution of Drosophila antonietae (Diptera, Drosophilidae). Rev Brasi Entomol. https://doi.org/10.1016/j.rbe.2015.09.004

  • Couto-Mendoza María T, Servia María J, Cobo Fernando (2014) Regeneration interferes with fluctuating asymmetry analysis in odonate larvae. Limnetica 33(1):107–120

    Google Scholar 

  • Dailey Tm, Claussen DL, Ladd GB, Buckner ST (2009) The effects of temperature, desiccation, and body mass on the locomotion of the terrestrial isopod, Porcellio laevis. Comp Biochem Physiol, Part A 153:162–166

    Article  CAS  Google Scholar 

  • Dallinger R, Berger B, Birkel S (1992) Terrestrial isopods: useful biological indicators of metal pollution. Oecologia 89:32–41

    Article  Google Scholar 

  • Dauwe T, Janssens E, Eens M (2006) Effects of heavy metal exposure on the condition and health of adult great tits (Parus major). Environ Pollut 140:71–78

    Article  CAS  Google Scholar 

  • Dong JH, Yu M, Bian ZF, Wang Y, Di CL (2011) Geostatistical analyses of heavy metal distribution in reclaimed mine land in Xuzhou, China. Environ Earth Sci 62(1):127–137

    Article  CAS  Google Scholar 

  • Eeva T, Tanhuanpaa S, Rabergh C, Airaksinen S, Nikinmaa M, Lehikoinen E (2000) Biomarkers and fluctuating asymmetry as indicators of pollution-induced stress in two hole-nesting passerines. Funct Ecol 14:235–243

    Article  Google Scholar 

  • Forest J, Bacescu M, Bellan-Santini D, Boxshall GA, Cals Ph Casanova JP, Dalens H, Gutu M, Hessler RR, Lagardère JP, Monod Th Nouvel H, Petrescu I, Roman ML, Sieg J, Trilles JP, Watling L (1999) Traité de zoologie: anatomie, systématique, biologie: 7. Crustacés: 3A. Péracarides. Mémoires de l’Institut océanographique, Monaco, p 450

    Google Scholar 

  • Galeotti P, Sacchi R, Vicario V (2005) Fluctuating asymmetry in body traits increases predation risks: tawny owl selection against asymmetric woodmice. Evol Ecol 19:405–418

    Article  Google Scholar 

  • Gargouri D, Azri C, Serbaji MM, Jedoui Y, Montacer M (2010) Heavy metal concentrations in the surface marine sediments of Sfax Coast Tunisia. Environ Monit Assess. https://doi.org/10.1007/s10661-010-1548-7

  • Ghannem N, Azri C, Serbaji MM, Yaich C (2011) Spatial distribution of heavy metals in the coastal zone of “Sfax–Kerkennah” plateau, Tunisia. Environ Prog Sustain Ener 30(2):221–233

    Article  CAS  Google Scholar 

  • Ghemari C, Bouslama MF, Ayari A, Nasri-Ammar K (2016) Population structure and dynamics of Porcellio laevis (Latreille, 1804) in Northern Tunisia. Vie Milieu 66(2):209–218

    Google Scholar 

  • Ghemari C, Waterlot C, Ayari A, Leclerq J, Douay F, Nasri-Ammar K (2017) Assessment of heavy metals in soil and terrestrial isopod Porcellio laevis in Tunisian industrialized areas. Environ Earth Sci 76:223. https://doi.org/10.1007/s12665-017-6946-5

    Article  CAS  Google Scholar 

  • Godet JP, Demuynck S, Waterlot C, Lemiere S, Souty-Grosset C, Sheifler R, Douay F, Lepretre A, Pruvot C (2012) Fluctuating asymmetry analysis on Porcellio scaber (Crustacea, Isopoda) populations living under metals-contaminated woody habitats. Ecol Indic 23:130–139

    Article  CAS  Google Scholar 

  • Hammouda A, Selmi S, Pearce-Duvet J, Chokri MA, Arnal A, Gauthier-Clerc Michel, Boulinier T (2012) Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis. PLoS ONE 7(5):e34966. https://doi.org/10.1371/journal.pone.0034966

    Article  CAS  Google Scholar 

  • Heikens A, Peijnenburg WJGM, Hendriks AJ (2001) Bioaccumulation of heavy metals in terrestrial invertebrates. Environ Pollut 113:385–393

    Article  CAS  Google Scholar 

  • Hénin S (1983) Les éléments traces dans le sol. Sci du Sol 2:67–71

    Google Scholar 

  • Hoffmann AA, Shirriffs J (2002) Geographic variation for wing shape in Drosophila serrata. Evolution 50:1068–1073

    Article  Google Scholar 

  • Hoffmann AA, Woods RE, Collins E, Wallin K, White A, McKenzie JA (2005) Wing shape versus asymmetry as an indicator of changing environmental conditions in insects. Aust J Entomol 44:233–243

    Article  Google Scholar 

  • Hopkin SP, Hardisty GN, Martin MH (1986) The woodlouse Porcellio scaber as a biological indicator of zinc, cadmium, lead and copper pollution. Environ Pollut 11:271–290

    Article  CAS  Google Scholar 

  • Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier, London, p 366

    Google Scholar 

  • Hussein MA, Obuid-Allah AH, Mohammad AH, Scott-Fordsmand JJ, Abd El-Wakeil KF (2006) Seasonal variation in heavy metal accumulation in subtropical population of the terrestrial isopod Porcellio laevis. Ecotoxicol Environ Saf 63:168–174

    Article  CAS  Google Scholar 

  • Jelassi R, Zimmer M, Khemaissia H, Garbe-Schonberg D, Nasri-Ammar K (2013) Amphipod diversity at three Tunisian lagoon complexes in relation to environmental conditions. J Nat Hist 47:2849–2868

    Article  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, LLC, Boca Raton

    Google Scholar 

  • Kark S (2001) Shifts in bilateral asymmetry within a distribution range: the case of the chucar partridge. Evolution 55:2088–2096

    Article  CAS  Google Scholar 

  • Kark S, Lens L, Van Dongen S, Schmidt E (2004) Asymmetry patterns across the distribution range: does the species matter? Biol J Linn Soc 81:313–324

    Article  Google Scholar 

  • Khemaissia K (2014) Oniscidean diversity in Tunisian Wetlands. PhD thesis, University of Tunis El Manar, p 284

  • Köhler HR, Hüttenrauch K, Berkus M, Grǎff S, Alberti G (1996) Cellular hepatopancreatic reactions in Porcellio scaber (Isopoda) as biomarkers for the evaluation of heavy metal toxicity in soils. Appl Soil Ecol 3:1–15

    Article  Google Scholar 

  • Krásný J, Sharp JM (2007) Groundwater in fractured rocks: IAH- selected paper on hydrology, vol 9. pp 658. CRC Press, Boca Rato

  • Lazic MM, Kaliontzopoulou A, Carretero MA, Crnobrnja-Isailovic´ J (2013) Lizards from urban areas are more asymmetric: using fluctuating asymmetryto evaluate environmental disturbance. PLoS ONE 8(12):e84190. https://doi.org/10.1371/journal.pone.0084190

    Article  CAS  Google Scholar 

  • Leamy LJ, Klingenberg CP (2005) The genetics and evolution of fluctuating asymmetry. Ann Rev Ecol Evol Syst 36:1–21

    Article  Google Scholar 

  • Lefebvre F, Limousin M, Caubet Y (2000) Sexual dimorphism in the antennae of terrestrial isopods: a result of male contests or scramble competition? Can J Zool 78:1987–1993

    Article  Google Scholar 

  • Leistikow A, Wägale JW (1999) Checklist of the terrestrial isopods of the New World (Crustacea, Isopoda, Oniscoidea). Rev Bras Zool 16:1–72

    Article  Google Scholar 

  • Lens L, Van Dongen S, Kark S, Matthysen E (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77:27–38

    Article  Google Scholar 

  • Leung B, Knopper L, Mineau P (2003) A critical assessment of the utility of fluctuating asymmetry as a biomarker of anthropogenic stress. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, p 415–426

    Google Scholar 

  • Longo G, Trovato M, Mazzei V, Ferrante M, OliveriConti G (2013) Ligia italica (Isopoda, Oniscidea) as bioindicator of mercury pollution of marine rocky coasts. PLoS ONE 8(3):e58548. https://doi.org/10.1371/journal.pone.0058548

    Article  CAS  Google Scholar 

  • Mazzei V, Giannetto A, Brundo MV, Maisano M, Ferrante M, Copat C, Mauceri A, Longo G (2015) Metallothioneins and heat shock proteins 70 in Armadillidium vulgare (Isopoda, Oniscidea) exposed to cadmium and lead. Ecotoxicol Environ Saf 116:99–106

    Article  CAS  Google Scholar 

  • Møller AP (1997) Developmental stability and fitness: a review. Am Nat 149:916–932

    Article  Google Scholar 

  • Møller AP, Swaddle JP (1997) Developmental stability and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page AL, Miller RH, Oomen AG, Hack A, Minekus M, Zeijdner E, Cornelis C, Schoeters G, Verstraete W, Van de Wiele T, Wragg J, Romperberg CJM, Sips AJAM, Wijnen JHV (eds) Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environ Sci Technol 36: 3326−3334

  • Odendaal JP, Reinecke AJ (1999) The toxicity of sublethal lead concentrations for the woodlouse, Porcellio laevis (Crustacea, Isopoda). Biol Fertil Soils 29:146–151

    Article  CAS  Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications. Kluwer Academic Publishers, Dordrecht, The Netherlands, p 335–364

    Chapter  Google Scholar 

  • Palmer AR (1996) Fluctuating asymmetry analyses: a primer. In: Markow TA (Ed.) Developmental instability: its origins and evolutionary implications.. Kluwer, Netherlands, p 335–364

    Google Scholar 

  • Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement. Anal Patterns Annu Rev Ecol Evol Syst 17:391–421

    Article  Google Scholar 

  • Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:57–72

    Google Scholar 

  • Palmer AR, Strobeck C (2003) Fluctuating asymmetry analyses revisited. developmental instability (DI): causes and consequences. department of biological sciences. University of Alberta Edmonton, Alberta, Canada, p 77, 36

    Google Scholar 

  • Pils JRV, Karathanasis AD, Mueller TG (2004) Concentration and distribution of six trace metals in northern Kentucky soils. Soil Sedt Contam 13:37–51

    Article  CAS  Google Scholar 

  • Powers LW, Bliss DE (1983) Terrestrial adaptations. In: Vernberg FJ, Vernberg WB (eds) The biology of crustacea. Vol. 8 Environmental adaptations. Academic Press, New York, p 271–333

    Google Scholar 

  • Rabaoui L, Balti R, Zrelli R, Tlig-Zouari S (2014) Assessment of heavy metals pollution in the gulf of Gabes (Tunisia) using four mollusk species. Mediterr Mar Sci 15(1):45–58

    Article  Google Scholar 

  • Rasmuson M (2002) Fluctuating asymmetry indicator of what? Hereditas 136:177–183

    Article  Google Scholar 

  • Scalici M, Traversetti L, Spani F, Malafoglia V, Colamartino M, Persichini T, Cappello S, Mancini G, Guerriero G, Colasanti M (2017) Shell fluctuating asymmetry in the sea-dwelling benthic bivalve Mytilus galloprovincialis (Lamarck, 1819) as morphological markers to detect environmental chemical contamination. Ecotoxicology 26:396–404. https://doi.org/10.1007/s10646-017-1772-9

    Article  CAS  Google Scholar 

  • Schmalfuss H (2003) World catalog of terrestrial isopods (Isopoda: Oniscidea). Stuttg Beitr Natur Ser A654:341

    Google Scholar 

  • Sousa JP, Loureiro S, Pieper S, Frost M, Kratz W, Nogueira AJA, Soares AMVM (2000) Soil and plant diet exposure routes and toxicokinetics of lindane in a terrestrial isopod. Environ Toxicol Chem 19:2557–2563

    Article  CAS  Google Scholar 

  • Stamenkovic Radak M, Kalajdzic P, Savic T, Savic M, Kurbalija Z, Rasic G, Andjelkovic M (2008) The effect of lead on fitness components and developmental stability in Drosophila subobscura. Acta Biol Hung 59:47–56

    Article  Google Scholar 

  • Traversetti L, Del Grosso F, Malafoglia V, Colasanti M, Ceschin S, Larsen S, Scalici M (2017) The Hydra regeneration assay reveals ecological risks in running waters: a new proposal to detect environmental teratogenic threats. Ecotoxicology 26:184–195. https://doi.org/10.1007/s10646-016-1753-4

    Article  CAS  Google Scholar 

  • Trotta V, Calboli FCF, Garoia F, Grifoni D, Cavicchi S (2005) Fluctuating asymmetry as a measure of ecological stress in Drosophila melanogaster (Diptera: Drosophilidae). Eur J Entomol 102:195–200

    Article  Google Scholar 

  • Van valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142

    Article  Google Scholar 

  • Vilisics Ferenc, Sólymos Péter, Hornung Elisabeth (2005) Measuring fluctuating asymmetry of the terrestrial isopod Trachelipus rathkii (Crustacea: Isopoda, Oniscidea) Eur J Soil Biol 41:85–90

    Article  Google Scholar 

  • Vishalakshi C, Singh BN (2006) Fluctuating asymmetry in certain morphological traits in laboratory populations of Drosophila ananassae. Genome 49:777–785. https://doi.org/10.1139/G06-031

    Article  CAS  Google Scholar 

  • Waterlot C, Bidar G, Peldrêne A, Roussel H, Fourrier H, Douay F (2013) Contamination, fractionation and availability of metals in urban soils in the vicinity of former lead and zinc smelters, France. Pedosphere 23:143–159

    Article  CAS  Google Scholar 

  • Weller B, Ganzhorn JU (2004) Carabid beetle community composition, body size, and fluctuating asymmetry along an urban-rural gradient. Basic Appl Ecol 5:193–201

    Article  Google Scholar 

  • Zidar P, Bozic J, Strus J (2005) Behavioral response in the terrestrial isopod Porcellio scaber (Crustacea) offered a choice of uncontaminated and cadmium contaminated food Ecotoxicology 5:493–502

    Article  Google Scholar 

  • Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda: Oniscidea): an evolutionary-ecological approach. Biol Rev 77:455–493

    Article  Google Scholar 

Download references

Acknowledgements

The study was supported by the Research Unit of Bio-ecology and Evolutionary Systematic (RU11SE11), University of Tunis El Manar, Faculty of Science of Tunis. The authors are grateful to Mr. Ahmed Ouni for his statistical help and Mrs. Sonia Hamaïed for her contribution by drawing the different articles of the antenna and the pereopods. We gratefully acknowledge the support of all members of the LGCgE regarding their considerable assistance in the analysis. The authors thank Mrs. Linda Northup, PhD, ELS, English solutions (Voiron, France), and Dr. Ivanklin Soares Campos Filho for providing English correction to the manuscript. We also thank the two anonymous reviewers for providing constructive criticism on an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chedliya Ghemari.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present study did not involve human participants. All the applicable institutional guidelines for welfare, care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghemari, C., Ayari, A., Hamdi, N. et al. Measure of environmental stress on Porcellio laevis Latreille, 1804 sampled near active Tunisian industrial areas. Ecotoxicology 27, 729–741 (2018). https://doi.org/10.1007/s10646-018-1955-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1955-z

Keywords

Navigation