Skip to main content

Fungal diversity and mycotoxin distribution in echinoderm aquaculture


Aquaculture has been a growing sector of food production worldwide in the last decades, and now starts to include new, unconventional species from the Phylum Echinodermata, such as sea urchin (Paracentrotus lividus) and sea cucumber (Holothuria tubulosa). However, little is known in this context with regard to food safety aspects arising from toxigenic fungi. In this study, samples of feed (n = 7) and water (n = 8) or water filters (n = 4) from experimental aquaculture systems, producing sea urchin and sea cucumber, were analyzed by culture-based microbiological methods to assess fungal associations. Additionally, a search using molecular techniques for toxigenic sections within the genus Aspergillus in these materials was done. Finally, samples were analyzed for 37 mycotoxins by LC-MS/MS. In feed samples, Fusarium verticillioides and F. culmorum were detected. In water and water filter samples, Aureobasidium spp., Penicillium spp., and Cladosporium spp. were found. No genes of species from toxigenic Aspergillus sections were detected. Some feed samples were contaminated by multiple mycotoxins, namely deoxynivalenol (DON), zearalenone (ZEN), fumonisins (FBs), T-2 toxin, ochratoxin A (OTA), and mycophenolic acid (MPA). This is the first one study dealing with toxigenic fungi and mycotoxins in echinoderm-producting aquaculture. Although no clear evidence for adverse effects on the production systems could be found, the confirmed environmental association of mycotoxins and echinoderms requires further consideration. Studies on the consequences of introducing cereal-based fungi and their mycotoxins via feeds into aquaculture systems for echinoderm production seem to be advisable, to assess possible adverse effects on production and to clarify the potential impact on public health.

This is a preview of subscription content, access via your institution.


  • Almeida LG (2014) Developing an integrated multi-trophic aquaculture as a solution to the sector’s challenges. Instituto Politécnico de Leiria, Escola Superior de Turismo e Tecnologia do Mar, Dissertação de Mestrado em Aquacultura, 101pp

  • Almeida IFM, Martins HML, Santos SMO, Freitas MS, Costa JMGN, Bernardo FMA (2011) Mycobiota and aflatoxin B1 in feed for farmed sea bass (Dicentrarchus labrax). Toxins 3:163–171.

  • Anater A, Manyes L, Meca G, Ferrer E, Luciano FB, Pimpão CT, Font G (2016) Mycotoxins and their consequences in aquaculture: a review. Aquaculture 451:1–10.

    Article  CAS  Google Scholar 

  • Arendrup MC, Rodriguez-Tudela JL, Lass-Flörl C, Cuenca-Estrella M, Donnelly JP, Hope W (2013) EUCAST technical note on anidulafungin. Clin. Microbiol Infect. 19(6):278–280.

  • Carboni S, Vignier J, Chiantore M, Tocher DR, Migaud H (2012) Effects of dietary microalgae on growth, survival and fatty acid composition of sea urchin Paracentrotus lividus throughout larval development. Aquaculture 324-325:250–258.

  • Cardoso C, Lourenço H, Costa S, Gonçalves S, Nunes ML (2015) Survey into the seafood consumption preferences and patterns in the Portuguese population: education, age, and health variability. J Food Prod Market 22:421–435.

    Article  Google Scholar 

  • Castilla-Gavilán M, Buzin F, Cognie B, Dumay J, Turpin V, Decottignies P (2018) Optimising microalgae diets in sea urchin Paracentrotus lividus larviculture to promote aquaculture diversification. Aquaculture 490:251–259.

  • Cruz-Perez P, Buttner MP, Stetzenbach LD (2001) Detection and quantitation of aspergillus fumigatus in pure culture using polymerase chain reaction. Mol Cell Probes 15:81–88.

    Article  CAS  PubMed  Google Scholar 

  • De Hoog GS, Guarro J, Gebé J, Figueras MJ (2000) Atlas of clinical fungi, 2nd edn. Centraalbureau voor Schimmelcultures, Utrecht

    Google Scholar 

  • Embaby EM, Ayaat NM, El-Galil MMA, Abdel-Hameid NA, Gouda MM (2015) Mycoflora and mycotoxin contaminated chicken and fish feeds. Middle East J Appl Sci 5:1044–1054.

    Article  Google Scholar 

  • EPA, United StatesEnvironmental Protection Agency (2017) About the National Exposure Research Laboratory (NERL). Avaiable from: URL: 〈〉 (Accessed 19 June 2017)

  • Fabbrocini A, Volpe MG, Di Stasio M, D’Adamo R, Maurizio D, Coccia E, Paolucci M (2012) Agar-based pellets as feed for sea urchins (Paracentrotus lividus): rheological behaviour, digestive enzymes and gonad growth. Aquac Res 43:321–331.

  • Fabbrocini A, Volpe MG, Coccia E, D’Adamo R, Paolucci M (2015) Agar-based biocomposites slow down progression in the reproductive cycle facilitating synchronization of the gonads of reared specimens of Paracentrotus lividus. Int J Aquac Fish Sci 1:35–41.

  • Fan J, Chen F, Diao Y, Cools HJ, Kelly SL, Liu X (2014) The Y123H substitution perturbs FvCYP51B function and confers prochloraz resistance in laboratory mutants of Fusarium verticillioides. Plant Pathol 63:952–960.

    Article  CAS  Google Scholar 

  • Fernandes CP (2017) The consumption of seafood in Portugal – preferences, knowledge and public perception. Universidade de Lisboa, Faculdade de Ciências, Departamento de Biologia Animal, Dissertação de Mestrado em Ecologia e Gestão Ambiental, pp60

  • Ferrigo D, Raiola A, Causin R (2016) Fusarium toxins in cereals: occurrence, legislation, factors promoting the appearance and their management. Molecules 21:E627.

    Article  CAS  PubMed  Google Scholar 

  • Hara-Kudo Y, Konuma H, Kamata Y, Miyahara M, Takatori K, Onoue Y, Sugita-Konishi Y, Ohnishi T (2013) Prevalence of the main food-borne pathogens in retail food under the national food surveillance system in Japan. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:1450–1458.

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Steele JC, Meng XZ (2017) Usage, residue, and human health risk of antibiotics in Chinese aquaculture: a review. Environ Pollut 223:161–169.

    Article  CAS  Google Scholar 

  • Lopes ASC (2016) From consumption to production – development of fisheries and aquaculture in Portugal. Universidade Nova de Lisboa, Faculdade de Ciências e Tecnologia, Dissertação de Mestrado em Engenharia e Gestão da Água, 123pp

  • Maciel ES, Sonati JG, Lima LKF, Savay-da-Silva LK, Galvão JA, Oetterer M (2016) Similarities and distinctions of fish consumption in Brazil and Portugal measured through electronic survey. I Food Res Int 23:395–402

    CAS  Google Scholar 

  • Martins HM, Marques M, Almeida I, Guerra MM, Bernardo F (2008) Mycotoxins in feedstuffs in Portugal: an overview. Mycotoxin Res 24:19–23.

    Article  CAS  PubMed  Google Scholar 

  • Matejova I, Svobodova Z, Vakula J, Mares J, Modra H (2016) Impact of mycotoxins on aquaculture fish species: a review. J World Aquacult Soc 48:186–200.

    Article  CAS  Google Scholar 

  • Mayer Z, Bagnara A, Färber P, Geisen R (2003) Quantification of the copy number of nor-1, a gene of the aflatoxin biosynthetic pathway by real-time PCR, and its correlation to the cfu of Aspergillus flavus in foods. Int J Food Microbiol 82:143–151.

    Article  CAS  PubMed  Google Scholar 

  • Olaya-Restrepo J, Erzini K, González-Wangüemert M (2018) Estimation of growth parameters for the exploited sea cucumber Holothuria arguinensis from South Portugal. Fish Bull 116:1–8.

    Article  Google Scholar 

  • Pietsch C, Kersten S, Burkhardt-Holm P, Valenta H, Dänicke S (2013) Occurrence of deoxynivalenol and zearalenone in commercial fish feed: an initial study. Toxins 5:184–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pietsch C, Katzenback BA, Garcia-Garcia E, Schulz C, Belosevic M, Burkhardt-Holm P (2015) Acute and subchronic effects on immune responses of carp (Cyprinus carpio L.) after exposure to deoxynivalenol (DON) in feed. Mycotoxin Res 31:151–164.

    Article  CAS  PubMed  Google Scholar 

  • Pillay TVR (1983) Fish feeds and feeding in developing countries, FAO Fisheries Technical Report ADCP/ REP/ 83/18: 97

  • Purcell SW, Samyn Y, Conand C (2012) Commercially important sea cucumbers of the world. Rome, FAO, Species Catalogue for Fishery Purposes, 6:150

  • Santos R, Dias S, Pinteus S, Silva J, Alves C, Tecelão C, Pombo A (2015a) Sea cucumber Holothuria forskali, a new resource for aquaculture? Reproductive biology and nutraceutical approach. Aquac Res 47:1–17.

  • Santos R, Dias S, Pinteus S, Silva J, Alves C, Tecelão C, Pombo A, Pedrosa R (2015b) The biotechnological and seafood potential of Stichopus regalis. Adv Biosci Biotechnol 6:194–204.

  • Sartori D, Scuderi A, Sansone G, Gaion A (2015) Echinoculture: the rearing of Paracentrotus lividus in a recirculating aquaculture system – experiments of artificial diets for the maintenance of sexual maturation. Aquacult 23:111–125.

  • Spirlet C, Grosjean P, Jangoux M (2001) Cultivation of Paracentrotus lividus (Echinodermata: Echinoidea) on extruded feeds: digestive efficiency, somatic and gonadal growth. Aquac Nutr 7:91–100.

  • Suckling CC, Symonds RC, Kelly MS, Young AJ (2011) The effect of artificial diets on gonad colour and biomass in the edible sea urchin Psammechinus miliaris. Aquaculture 318:335–342.

  • Tančić S, Stanković S, Lević J, Krnjaja V (2015) Correlation of deoxynivalenol and zearalenone production by Fusarium species originating from wheat and maize grain. Pestic Phytomed 30:99–105.

  • Tola S, Bureau DP, Hooft JM, Beamish FWH, Sulyok M, Krska R, Encarnação P, Petkam R (2015) Effects of wheat naturally contaminated with Fusarium mycotoxins on growth performance and selected health indices of red tilapia (Oreochromis niloticus × O. mossambicus). Toxins 7:1929–1944.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viegas C, Faria T, Carolino E, Sabino R, Quintal Gomes A, Viegas S (2016) Occupational exposure to fungi and particles in animal feed industry. Med Pr 67(2):143–154.

    Article  PubMed  Google Scholar 

  • Viegas C, Faria T, Cebola de Oliveira A, Aranha Caetano L, Carolino E, Quintal-Gomes A, Twarużek M, Kosicki R, Soszczyńska E, Viegas S (2017a) A new approach to assess fungal contamination and mycotoxins occupational exposure in forklifts drivers from waste sorting. Mycotoxin Res 33:285–295.

    Article  CAS  Google Scholar 

  • Viegas C, Faria T, Aranha L, Carolino E, Quintal Gomes A, Viegas S (2017b) Aspergillus prevalence in different occupational settings. J Occup Environ Hyg 14:771–785.

    Article  PubMed  Google Scholar 

  • Viegas C, Faria T, Monteiro A, Aranha Caetano L, Carolino E, Quintal Gomes A, Viegas S (2018) A novel multi-approach protocol for the characterization of occupational exposure to organic dust—swine production case study. Toxics 6(5). doi

Download references


This work was supported by Instituto Politécnico de Lisboa, Lisbon, Portugal, that funded the Project “Bioburden and mycotoxigenic burden from feed applied in aquaculture – Risk assessment and control” [IPL/2018/ BIO&MYCOAQUAINVEST_ESTeSL].

Author information

Authors and Affiliations


Corresponding author

Correspondence to Carla Viegas.

Ethics declarations

Conflict of interest


Additional information

Publisher’s note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Viegas, C., Esteves, L., Faria, T. et al. Fungal diversity and mycotoxin distribution in echinoderm aquaculture. Mycotoxin Res 35, 253–260 (2019).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Fungi
  • Mycotoxin
  • Aquaculture
  • Echinoderm
  • Sea urchin, Paracentrotus lividus
  • Sea cucumber, Holothuria tubulosa
  • Fusarium