Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Incidence of morphometry variation, growth alteration, and reproduction performance of the annular sea bream (Diplodus annularis) as effective tools to assess marine contamination: how useful is a multi-biotimarkers approach?

  • 65 Accesses

Abstract

A wide variety of contaminants in the aquatic environment causes several deleterious effects on aquatic organism traits ranging from molecular to individual and population levels. This in situ study investigated morphometry, growth performance, and reproduction success of a teleost fish, Diplodus annularis, from a polluted site “Sayada” and a reference site “Salakta” in the eastern Tunisian coastline. Morphometric indexes, generalized Procruste analysis, thin plate, and otolith contour methods were used to assess the pollution effects on morphological traits. The growth performance of fish from contaminated and control sites were studied using the Von Bertalanffy equation. Gonadosomatic (GSI) and Hepatosomatic (HSI) Indexes and absolute and relative fecundity were used to assess the impact of pollution on the reproduction success of this species. The obtained results showed that the fish of the contaminated zone had significant alteration of the morphology, slower growth, significant increase in the HSI, significant decrease in female GSI, and a decrease in absolute and relative fecundity compared to specimens from the unpolluted zone. Based on these results, the biological traits of Diplodus annularis can be used as biological biomarkers in the monitoring and protection programs of the marine contamination in the Mediterranean Sea.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Abdelhady AA (2016) Phenotypic differentiation of the Red Sea gastropods in response to the environmental deterioration: geometric morphometric approach. J Afr Earth Sci 115:191–202

  2. Adeogun AO, Chukwuka AV (2011) Effect of textile factory effluent on otolith and somatic growth parameters in Clarias gariepinus. Zoologist 9:70–77

  3. Agbohessi PT, Imorou Toko I, Ouédraogo A, Jauniaux T, Mandiki SN, Kestemont P (2015) Assessment of the health status of wild fish inhabiting a cotton basin heavily impacted by pesticides in Benin (West Africa). Sci Total Enviran 506-507:567–584

  4. Amin MR, Mollah MF, Taslima K, Muhammadullah (2014) Morphological observation and length-weight relationship of critically endangered riverine catfish Rita rita (Hamilton). Pak J Biol Sci 17(2):234–240

  5. Bauchot ML (1987) Sparidae. In: Fischer W, Bauchot ML, Schneider M (Eds.), Fiches FAO d’Indentification des espèces pour les Besoins de la Pêche (Revison 1), Méditerranée et Mer Noire. Zones de pechê 37, vol. II (Vertébrés). FAO-CEE, Rome, pp. 761-1530

  6. Bell JD, Harmelin-Vivien ML (1983) Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. 2. Feeding habits. Tethys 11:1–14

  7. Ben-Khedher S, Jebali J, Kamel N, Banni M, Rameh M, Jrad A, Boussetta H (2013) Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta lagoon: an integrated approach in biomonitoring of marine complex pollution. Environ Sci Pollut Res 20(4):2616–2631

  8. Ben-Khedher S, Jamel J, Zohra H, Amel NHJ, Hamadi BMB (2014) Metals bioaccumulation and histopathological biomarkers in Carcinus maenas crab from Bizerta lagoon. Environ Sci Pollut Res 21(6):4343–4357

  9. Bervoets L, Knapen D, De Jonge M, Van Campenhout K, Blust R (2013) Differential hepatic metal and metallothionein levels in three feral fish species along a metal pollution gradient. PLoS One 8(3):e60805

  10. Bose APH, McCallum ES, Raymond K, Marentette JR, Balshine S (2018) Growth and otolith morphology vary with alternative reproductive tactics and contaminant exposure in the round goby Neogobius melanostomus. J Fish Biol 93:674–684

  11. Bradai MN, Jarboui O, Ghorbel M, Bouain A, El Abed A (2001) Age et croissance du sparaillon D. annularis (Teleosteens, Sparidae) du Golfe de Gabes. Rapp Comm Int Mer Medit. 36: 246

  12. Bugel SM, White LA, Cooper KR (2009) Impaired reproductive health of killifish (Fundulus heteroclitus) inhabiting Newark Bay NJ, a chronically contaminated estuary. Aquat Toxicol 96(3):182–193

  13. Chaouch, H.,Ben Abdallah, O.,Ghorbel, M., & Jarboui,O. (2013). Reproductive biology of the annular seabream,Diplodus annularis(Linnaeus, 1758), in the Gulf of Gabes( centel Mediterranean). Jour of App Ichthyol 29:796–800

  14. Damak M, Frontalini F, Elleuch B, Kallel M (2018) Benthic foraminiferal assemblages as pollution proxies along the coastal fringe of the Monastir Bay (Tunisia). J Afr Earth Sci. https://doi.org/10.1016/j.jafrearsci.2018.11.013

  15. Damak M, Fourati R, Ellech B, Kallel M (2019) Assessment of organic and metallic contamination in the surface sediment of Monastir Bay (eastern Tunisia): spatial distribution, potential sources, and ecological risk assessment. Mar Pollut Bull 149:110500

  16. Darilmaz E, Kucuksezgin F (2012) Distribution of aliphatic and aromatic hydrocarbons in red mullet (Mullus barbatus) and annular sea bream (Diplodus annularis) from the Izmir Bay (eastern Aegean). Bull Environ Contam Toxicol 88:283–289

  17. Deepa KPA, Kumar KV, Kottnis O, Nikkia R, Bineesh KK, Hashim M, Saravanane N, Sudhakar M (2019) Population variations of opal fish, Bembrops caudimacula Steindachner, 1876 from Arabian Sea and Andaman Sea: evidence from otolith morphometry. Reg Stud Mar Sci 25:100466

  18. Donnaloia M, Zupa W, Arnesano M, Neglia C, Facchini MT, Carbonara P (2017) Reproductive biology of Diplodus annularis (linnaeus, 1758) in the central-western mediterranean seas. Biol Mar Mediterr 24(1):182–183

  19. Dragun Z, Filipović Marijić V, Kapetanović D, Valić D, Vardić Smrzlić I, Krasnići N, Strižak Ž, Kurtović B, Teskeredžić E, Raspor B (2013) Assessment of general condition of fish inhabiting a moderately contaminated aquatic environment. Environ Sci Pollut Res Int 20(7):4954–4968

  20. Fontana A, Le Guen JC (1969) Étude de la maturité sexuelle et de la fécondité de Pseudotolithus (fonticulus) elongatus. ORSTOM, série Océanographique, 7(3):9–19.

  21. García-Rubies A, Macpherson E, (1995) Substrate use and temporal pattern of recruitment in juvenile fishes of the Mediterranean littoral. Mar Biol 124:35–42. https://doi.org/10.1007/BF00349144.

  22. Gerbron M, Geraudie P, Fernandes D, Rotchell JM, Porte C, Minier C (2014) Evidence of altered fertility in female roach (Rutilus rutilus) from the River Seine (France). Environ Pollut 191:85–61

  23. Gharred T, Helaoui A, Mannai R, Jebali J (2019) Effect of multiple pollution on the cholinesterase activity, morphometry and reproduction performance of Patella caerulea collected from eastern Tunisian coasts. Cah Biol Mar 60:11–20

  24. Ghedira J, Jebali J, Bouraoui Z, Banni M, Guerbej H, Boussetta H (2010) Metallothionein and metal levels in liver, gills and kidney of Sparus aurata exposed to sublethal doses of cadmium and copper. Fish Physiol Biochem 36:101–107

  25. Gonul LT, Kucuksezgin F (2007) Mercury accumulation and speciation in the muscle of red mullet (Mullus barbatus) and annular sea bream (Diplodus annularis) from Izmir Bay (eastern Aegean). Mar Pollut Bull 54:1962–1989

  26. Gordoa A, Molí B (1997) Age and growth of the sparids Diplodus vulgaris D. sargus and D. annularis in adult populations and the differences in their juvenile growth patterns in the north-western Mediterranean Sea. Fish Res 33(1–3):123–129

  27. Gulland JA (1969) Manual methods for fish stock assessment. Part I. Fish population analysis. FAO Fish sci 4:154

  28. Hauser-Davis RA, Lavandier RC, Bastos FF, Oliveira TF, Ribeiro CA, Ziolli RL, de Campos RC (2012) Alterations in morphometric and organosomatic indices and histopathological analyses indicative of environmental contamination in millet, Mugil liza, from southeastern. Bull Environ Contam Toxicol 89(6):1154–1160

  29. Hossain M, Nahiduzzaman MD, Saha D, Khanam H, Alam M (2010) Landmark-based morphometric and meristic variations of the endangered carp, Kalibaus Labeo calbasu, from stocks of two isolated Rivers, the Jamuna and Halda, and a hatchery. Zoological Stadies 49(4):556–563

  30. Iwata H, Ukai Y (2002) SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. J Hered 93:384–385

  31. Jebali J, Ben-Khedher S, Ghedira J, Kamel N, Boussetta H (2011) Integrated assessment of biochemical responses in Mediterranean crab (Carcinus maenas) collected from Monastir Bay Tunisia. J Environ Sci 23(10):1714–1720

  32. Jebali J, Banni M, Boussetta H (2012). Biochemical biomarkers in aquatic ecotoxicology: fundamental mechanisms, application, and perspectives. NOVA Science Publishers, Inc. advances in Environmental Research, 23: 359 pp.

  33. Jebali J, Chicano-Gálvez E, Banni M, Guerbej H, Boussetta H, López-Barea J, Alhama J (2013a) Biochemical responses in seabream (Sparus aurata) caged in-field or exposed to benzo(a)pyrene and paraquat. Characterization of glutathione S-transferases. Ecotoxicol Environ Saf 88:169–177

  34. Jebali J, Sabbagh M, Banni M, Kamel N, Ben-Khedher S, M'hamdi N, Boussetta H (2013b) Multiple biomarkers of pollution effects in Solea solea fish on the Tunisia coastline. Environ Sci Pollut Res 20(6):3812–3821

  35. Jebali J, Chicano-Gálvez E, Fernandez-Cinal R, Banni M, Chouba L, Boussetta H, López-Barea J, Alhama J (2014) Proteomic analysis in caged Mediterranean crab (Carcinus maenas) and chemical contaminant exposure in Téboulba harbour, Tunisia. Ecotoxicol Environ Saf 100:15–26

  36. Johnson LL, Lomax DP, Myers MS, Olson OP, Sol SY, O'Neill SM, West J, Collier TK (2008) Xenoestrogen exposure and effects in English sole (Parophrys vetulus) from Puget Sound, WA. Aquat Toxicol 88(1):29–38

  37. Kaouèche M, Bahri-Sfar L, Hammami I, Ben Hassine OK (2017) Morphometric variations in white seabream Diplodus sargus (Linneus, 1758) populations along the Tunisian coast. Oceanologia 59:129–138

  38. Khenfech NH, Boumaiza M (2011) Morphological abnormalities in the annular sea bream M Diplodus annularis (Osteichthyes: Sparidae) from the lagoon of Bizerte (Notheastern Tunisia, Central Mediterranean). Annales, Series Historia Naturalis 21:161–166

  39. Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

  40. Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Com G Ima Proc 18:236–258

  41. March D, Alós J, Grau A, Palmer M (2011) Short-term residence and movement patterns of the annular seabream Diplodus annularis in a temperate marine reserve. Estuar Coast Shelf Sci 92:581–587

  42. Matic-Skoko S, Kraljevisc M, Dulcic J, Jardas I (2007) Age, growth, mortality and yield-per-recruit for annular seabrean (Diplodus annularis L.) from the eastern middle Adriatic Sea. J Appel Ichthyol 23:152–157

  43. Mills LJ, Chichester C (2005) Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? Sci Total Environ 343(1–3):1–34

  44. Montaño-Campaz ML, Gomes-Dias L, Toro Restrepo BE, Garcıa-Merchan VH (2019) Incidence of deformities and variation in shape of mentum and wing of Chironomus columbiensis (Diptera, Chironomidae) as tools to assess aquatic contamination. PLoS One 14(1):e0210348

  45. Morat F, Betoulle S, Robert M, Thailly AF, Biagianti-Risbourg S, Lecomte-Finiger R (2008) What can otolith examination tell us about the level of perturbations of salmonid fish from the Kerguelen Islands? Ecol Freshw Fish 17:617–627

  46. Mouine N, Ktari M, Chakroun-Marzouk N (2012) Reproductive biology of four Diplodus species Diplodus vulgaris, D. annularis, D. sargus sargus and D.puntazzo (Sparidae) in the gulf of Tunis (Central Mediterranean). J Mar Biol Assoc UK 92(3):623–631

  47. Nouira T, Tagorti MA, Budzinski H, Etchebert H, Boussetta H (2012) Polycyclic aromatic hydrocarbons (PAHs) in surface sediments of Monastir Bay (Tunisia, Central Mediterranean): distribution, origin and seasonal variations. Int J Environ Anal Chem 93:1470–1483. https://doi.org/10.1080/03067319.2012.746325

  48. Nouira T, Risso C, Chouba L, Budzinski H, and Boussetta H (2013) Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in surface sediments from Monastir Bay (Tunisia, Central Mediterranean): occurrence, distribution and seasonal variations,” Chemosphere 93(3)487–493, 2013. https://doi.org/10.1016/j.chemosphere.2013.06.017

  49. Pajuello J, Lorenzo J (2001) Biology of the annular seabream, Diplodus annularis(Sparidae), in the coastal waters of the canary islands. J Appl Ichihyol 17:121–125

  50. Pajuelo JG, Lorenzo JM (2002) Growth and age estimation of Diplodus sargus cadenati (Sparidae) off the Canary Islands. Fish Res 59:93–100

  51. Prado PS, Pinheiro APB, Bazzoli N, Rizzo E (2014) Reproductive biomarkers responses induced by xenoestrogens in the characid fish Astyanax fasciatus inhabiting a South American reservoir: an integrated field and laboratory approach. Environ Res 131:165–173

  52. Sanchez W, Sremski W, Piccini B, Palluel O, Maillot-Maréchal E, Betoulle S, Jaffal A, Aït-Aïssa S, Brion F, Thybaud E, Hinfray N, Porcher JM (2011) Adverse effects in wild fish living downstream from pharmaceutical manufacture discharges. Environ Int 2011 37(8):1342–1348

  53. Sassi R, Souissi F, Soussi N, Boukaaba M, Belayouni H (1998) Organic matter geochemistry to analyse the degradation of the Monastir-Ksibet el Mediouni littoral (eastern Tunisia). Earth Planet Sci 327:303–308

  54. Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556

  55. Shinn C, Blanchet S, Loot G, Lek S, Grenouillet G (2015) Phenotypic variation as an indicator of pesticide stress in gudgeon: accounting for confounding factors in the wild. Sci Total Environ 538:733–742

  56. Silva A (2003) Morphometric variation among sardine (Sardina pilchardus) populations from the northeastern Atlantic and the western Mediterranean. ICES J Marine Sci 60:1352–1360

  57. Solé M, Raldua D, Piferrer F, Barceló D, Porte C (2003) Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. Comp Biochem Physiol Toxicol Pharmacol 136(2):145–156

  58. Straüss RE, Bookstein FL (1982) The truss: body from reconstructions in morphometrics. Syst Zool 31:113–135

  59. Toro B, Navarro JM, Palma-flemming H (2003) Relationship between bioenergetics responses and organic pollutants in the giant mussel, Chromitilus chorus (Molusca mytilidae). Aquat Toxicol 63:257–269

  60. Turki O, M’hetli M, Chriki A, Kraem MM (2009) Characterization and phenotypic and biological variation in the two sexes of pikeperch Sander lucioperca (L., 1758) (Teleostei, Percidae) in the Nebhana reservoir (Central Tunisia). Bull. Inst. Natn. Scien. Tech. Mer de Salammbô, Vol. 36:75–86

  61. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

  62. Van Poorten BT, Walters CJ, (2016) How can bioenergetics help us predict changes in fish growth patterns? Fish. Res. 180: 23–30. https://doi.org/10.1016/j.fishres.2015.07.031.

  63. Vasil’eva ED, Vasil’ev VP (2010) Genetic and environmental variations in quantitative characters in fishes: a comparative analysis of monoclonal triploid and bisexual tetraploid spined loaches (Cobitis, Cobitidae). J Ichthyol 50:960–968

  64. Zelditch ML, Swiderski DL, David Sheets H (2012) Geometric morphometrics for biologists: aprimer. Academic Press, 488p

  65. Zrafi I, Bakhrouf A, Rouabhia M, Saidane-Mosbahi D (2013) Aliphatic and aromatic biomarkers for petroleum hydrocarbon monitoring in Khniss Tunisian-coast, (Mediterranean Sea) Procedia Environmental Sciences, 18: 211–220

Download references

Funding

This work was supported by a fund from the Ministry of Higher Education and Scientific Research, University of Monastir, Tunisia (Research Laboratory Bioresources: Integrative Biology and Valorisation, High Institute of Biotechnology of Monastir, Tunisia).

Author information

Correspondence to Tahar Gharred.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gharred, T., Mannai, R., Belgacem, M. et al. Incidence of morphometry variation, growth alteration, and reproduction performance of the annular sea bream (Diplodus annularis) as effective tools to assess marine contamination: how useful is a multi-biotimarkers approach?. Environ Sci Pollut Res 27, 4075–4088 (2020). https://doi.org/10.1007/s11356-019-07014-9

Download citation

Keywords

  • Pollution
  • Diplodus annularis
  • Morphology
  • Growth
  • Reproduction
  • Fecundity