Hydra vulgaris assay as environmental assessment tool for ecotoxicology in freshwaters: a review
A. Cera A 1 , G. Cesarini A 1 , F. Spani A B and M. Scalici AA Department of Sciences, University of Rome ‘Roma Tre’, Viale Guglielmo Marconi 446, I-00146 Roma, Italy.
B Corresponding author. Present address: Departmental Faculty of Medicine and Surgery, Università Campus Bio-Medico di Roma, Unit of Diagnostic Imaging, Via Alvaro del Portillo 21, I-00128 Roma, Italy. Email: federica.spani@uniroma3.it
Marine and Freshwater Research 72(6) 745-753 https://doi.org/10.1071/MF20115
Submitted: 19 April 2020 Accepted: 17 September 2020 Published: 17 December 2020
Abstract
Freshwaters are vulnerable ecosystems owing to several anthropogenic impacts, including chemical pollution. Among existing model organisms, the cnidarian Hydra vulgaris is widely used for toxicological tests, with the aim of detecting either toxicity or teratogenicity of different dissolved chemicals. Given the widespread range of applications and developed assays, the aim of this review was to show and discuss the actual use of this model for ecotoxicological assessments in freshwaters as an ‘early warning system’. To achieve this goal, a thorough review was conducted by consulting several search engines for peer-reviewed international articles. Among all resulting articles from literature search, those focusing on H. vulgaris assay applied to environmental pollution were first selected (n = 19). Then, only articles that specifically tested freshwater samples collected directly in the field were considered (n = 4). The literature search highlighted that Hydra assays are suitable monitoring tools for freshwater ecotoxicity assessment. In addition, H. vulgaris allows testing diverse biomarkers (e.g. molecular, histological, morphological and behavioural) and exploring innovative research fields. So as to be able to assess the impact of emerging contaminants on both habitat and human health, the Hydra assays are demonstrating that they have an increasing potential that must be exploited.
Keywords: biological monitoring, early warning system, emergent contaminants, Hydra vulgaris, regeneration, teratogens.
References
Ambrosone, A., Mattera, L., Marchesano, V., Quarta, A., Susha, A. S., Tino, A., Rogach, A. L., and Tortiglione, C. (2012). Mechanisms underlying toxicity induced by CdTe quantum dots determined in an invertebrate model organism. Biomaterials 33, 1991–2000.| Mechanisms underlying toxicity induced by CdTe quantum dots determined in an invertebrate model organism.Crossref | GoogleScholarGoogle Scholar | 22169823PubMed |
Ambrosone, A., Scotto di Vettimo, M. R., Malvindi, M. A., Roopin, M., Levy, O., Marchesano, V., Pompa, P. P., Tortiglione, C., and Tino, A. (2014). Impact of amorphous SiO2 nanoparticles on a living organism: morphological, behavioral, and molecular biology implications. Frontiers in Bioengineering and Biotechnology 2, 37.
| Impact of amorphous SiO2 nanoparticles on a living organism: morphological, behavioral, and molecular biology implications.Crossref | GoogleScholarGoogle Scholar | 25325055PubMed |
Arkhipchuk, V. V., Romanenko, V. D., Malinovskaya, M. V., Kipnis, L. S., Solomatina, V. D., and Krot, Y. G. (2000). Toxicity assessment of water samples with a set of animal and plant bioassays: experience of the Ukrainian participation in the WaterTox program. Environmental Toxicology 15, 277–286.
| Toxicity assessment of water samples with a set of animal and plant bioassays: experience of the Ukrainian participation in the WaterTox program.Crossref | GoogleScholarGoogle Scholar |
Arkhipchuk, V. V., Blaise, C., and Malinovskaya, M. V. (2006). Use of hydra for chronic toxicity assessment of waters intended for human consumption. Environmental Pollution 142, 200–211.
| Use of hydra for chronic toxicity assessment of waters intended for human consumption.Crossref | GoogleScholarGoogle Scholar | 16324774PubMed |
Auclair, J., Quinn, B., Peyrot, C., Wilkinson, K. J., and Gagné, F. (2020). Detection, biophysical effects, and toxicity of polystyrene nanoparticles to the cnidarian Hydra attenuata. Environmental Science and Pollution Research International 27, 11772–11781.
| Detection, biophysical effects, and toxicity of polystyrene nanoparticles to the cnidarian Hydra attenuata.Crossref | GoogleScholarGoogle Scholar | 31975008PubMed |
Beach, M. J., and Pascoe, D. (1998). The role of Hydra vulgaris (Pallas) in assessing the toxicity of freshwater pollutants. Water Research 32, 101–106.
| The role of Hydra vulgaris (Pallas) in assessing the toxicity of freshwater pollutants.Crossref | GoogleScholarGoogle Scholar |
Blaise, C., and Kusui, T. (1997). Acute toxicity assessment of industrial effluents with a microplate-based Hydra attenuata assay. Environmental Toxicology and Water Quality 12, 53–60.
| Acute toxicity assessment of industrial effluents with a microplate-based Hydra attenuata assay.Crossref | GoogleScholarGoogle Scholar |
Blaise, C., Gagné, F., Harwood, M., Quinn, B., and Hanana, H. (2018). Ecotoxicity responses of the freshwater cnidarian Hydra attenuata to 11 rare earth elements. Ecotoxicology and Environmental Safety 163, 486–491.
| Ecotoxicity responses of the freshwater cnidarian Hydra attenuata to 11 rare earth elements.Crossref | GoogleScholarGoogle Scholar | 30075452PubMed |
Bohórquez-Echeverry, P., Duarte-Castañeda, M., León-López, N., Caicedo-Carrascal, F., Vásquez-Vásquez, M., and Campos-Pinilla, C. (2012). Selection of a bioassay battery to assess toxicity in the affluents and effluents of three water-treatment plants. Universitas Scientiarum 17, 152–166.
| Selection of a bioassay battery to assess toxicity in the affluents and effluents of three water-treatment plants.Crossref | GoogleScholarGoogle Scholar |
Bowden, H. C., Wilby, O. K., Botham, C. A., Adam, P. J., and Ross, F. W. (1995). Assessment of the toxic and potential teratogenic effects of four glycol ethers and two derivatives using the hydra regeneration assay and rat whole embryo culture. Toxicology in vitro 9, 773–781.
| Assessment of the toxic and potential teratogenic effects of four glycol ethers and two derivatives using the hydra regeneration assay and rat whole embryo culture.Crossref | GoogleScholarGoogle Scholar | 20650156PubMed |
Brooun, M., Manoukian, A., Shimizu, H., Bode, H. R., and McNeill, H. (2013). Organizer formation in Hydra is disrupted by thalidomide treatment. Developmental Biology 378, 51–63.
| Organizer formation in Hydra is disrupted by thalidomide treatment.Crossref | GoogleScholarGoogle Scholar | 23531412PubMed |
Brown, K. A., Mays, T., Romoser, A., Marroquin-Cardona, A., Mitchell, N. J., Elmore, S. E., and Phillips, T. D. (2014). Modified hydra bioassay to evaluate the toxicity of multiple mycotoxins and predict the detoxification efficacy of a clay-based sorbent: detoxification efficacy of a clay-based mycotoxin sorbent in hydra. Journal of Applied Toxicology 34, 40–48.
| Modified hydra bioassay to evaluate the toxicity of multiple mycotoxins and predict the detoxification efficacy of a clay-based sorbent: detoxification efficacy of a clay-based mycotoxin sorbent in hydra.Crossref | GoogleScholarGoogle Scholar | 23047854PubMed |
Campbell, R. D. (1989). Taxonomy of the European Hydra (Cnidaria: Hydrozoa): a re-examination of its history with emphasis on the species H. vulgaris Pallas, H. attenuata Pallas and H. circumcincta Schulze. Zoological Journal of the Linnean Society 95, 219–244.
| Taxonomy of the European Hydra (Cnidaria: Hydrozoa): a re-examination of its history with emphasis on the species H. vulgaris Pallas, H. attenuata Pallas and H. circumcincta Schulze.Crossref | GoogleScholarGoogle Scholar |
Castro, S., Espinola, J., Migues, D., and Viana, F. (2002) Los bioensayos como herramienta de evaluación de la toxicidad de los efluentes industriales en Uruguay (File 04464). Informe final, International Development Research Centre (IDRC), Montevideo, Uruguay.
Cera, A., Ceschin, S., Del Grosso, F., Traversetti, L., and Scalici, M. (2020). Correlating ecotoxicological early-warning systems to biotic indices to assess riverine teratogenic contamination. Marine and Freshwater Research 71, 1033–1039.
| Correlating ecotoxicological early-warning systems to biotic indices to assess riverine teratogenic contamination.Crossref | GoogleScholarGoogle Scholar |
Fu, L., Staples, R., and Stahl, R. (1991). Application of the Hydra attenuata assay for identifying developmental hazards among natural waters and wastewaters. Ecotoxicology and Environmental Safety 22, 309–319.
| Application of the Hydra attenuata assay for identifying developmental hazards among natural waters and wastewaters.Crossref | GoogleScholarGoogle Scholar | 1778117PubMed |
Gagné, F., Auclair, J., and Quinn, B. (2019). Detection of polystyrene nanoplastics in biological samples based on the solvatochromic properties of Nile red: application in Hydra attenuata exposed to nanoplastics. Environmental Science and Pollution Research International 26, 33524–33531.
| Detection of polystyrene nanoplastics in biological samples based on the solvatochromic properties of Nile red: application in Hydra attenuata exposed to nanoplastics.Crossref | GoogleScholarGoogle Scholar | 31578681PubMed |
Holdway, D. A. (2005). Hydra population reproduction toxicity test method. In ‘Small-scale Freshwater Toxicity Investigations’. (Eds C. Blaise and J.-F. Férard.) Vol. 1, pp. 395–411. (Springer Netherlands.)
Huarachi, R., and Gonzalez, R. (2012). Hydra vulgaris Pallas, 1766 (Hydrozoa: Hydridae) as bioindicator of the water quality of the River Chili, Arequipa, Peru. The Biologist 10, 13.
Hyne, R. V., Rippon, G. D., White, J., and Ellender, G. (1992). Accumulation of uranium by freshwater Hydra into discharged nematocysts. Aquatic Toxicology 23, 231–245.
| Accumulation of uranium by freshwater Hydra into discharged nematocysts.Crossref | GoogleScholarGoogle Scholar |
Johnson, E. M., and Gabel, B. E. G. (1992). Applications of the Hydra assay for rapid detection of developmental hazards. Journal of the American College of Toxicology 1, 57–71.
| Applications of the Hydra assay for rapid detection of developmental hazards.Crossref | GoogleScholarGoogle Scholar |
Johnson, E. M., Gabel, B. E. G., Christian, M., and Sica, E. (1986). The developmental toxicity of xylene and xylene isomers in the Hydra assay. Toxicology and Applied Pharmacology 82, 323–328.
| The developmental toxicity of xylene and xylene isomers in the Hydra assay.Crossref | GoogleScholarGoogle Scholar | 3945957PubMed |
Johnson, E. M., Newman, L. M., Gabel, B. E. G., Boerner, T. F., and Dansky, L. A. (1988). An analysis of the Hydra assay’s applicability and reliability as a developmental toxicity prescreen. Journal of the American College of Toxicology 7, 111–126.
| An analysis of the Hydra assay’s applicability and reliability as a developmental toxicity prescreen.Crossref | GoogleScholarGoogle Scholar |
Kar, S., and Aditya, A. K. (2007). Evaluation of freshwater toxicity with Hydra as a test animal. Philippine Journal of Science 136, 173–179.
Karntanut, W., and Pascoe, D. (2002). The toxicity of copper, cadmium and zinc to four different Hydra (Cnidaria: Hydrozoa). Chemosphere 47, 1059–1064.
| The toxicity of copper, cadmium and zinc to four different Hydra (Cnidaria: Hydrozoa).Crossref | GoogleScholarGoogle Scholar | 12137038PubMed |
Lasker, H. R., Syron, J. A., and Clayton, W. S. (1982). The feeding response in Hydra verdis: effects of prey density on capture rates. The Biological Bulletin 162, 290–298.
| The feeding response in Hydra verdis: effects of prey density on capture rates.Crossref | GoogleScholarGoogle Scholar |
Lekamge, S., Miranda, A. F., Abraham, A., Li, V., Shukla, R., Bansal, V., and Nugegoda, D. (2018). The toxicity of silver nanoparticles (AgNPs) to three freshwater invertebrates with different life strategies: Hydra vulgaris, Daphnia carinata, and Paratya australiensis. Frontiers in Environmental Science 6, 152.
| The toxicity of silver nanoparticles (AgNPs) to three freshwater invertebrates with different life strategies: Hydra vulgaris, Daphnia carinata, and Paratya australiensis.Crossref | GoogleScholarGoogle Scholar |
Manfrin, A., Larsen, S., Scalici, M., Wuertz, S., and Monaghan, M. T. (2018). Stress response of Chironomus riparius to changes in water temperature and oxygen concentration in a lowland stream. Ecological Indicators 95, 720–725.
| Stress response of Chironomus riparius to changes in water temperature and oxygen concentration in a lowland stream.Crossref | GoogleScholarGoogle Scholar |
Marchesano, V., Ambrosone, A., Bartelmess, J., Strisciante, F., Tino, A., Echegoyen, L., Tortiglione, C., and Giordani, S. (2015). Impact of carbon nano-onions on Hydra vulgaris as a model organism for nanoecotoxicology. Nanomaterials 5, 1331–1350.
| Impact of carbon nano-onions on Hydra vulgaris as a model organism for nanoecotoxicology.Crossref | GoogleScholarGoogle Scholar | 28347067PubMed |
McKinley, K., McLellan, I., Gagné, F., and Quinn, B. (2019). The toxicity of potentially toxic elements (Cu, Fe, Mn, Zn and Ni) to the cnidarian Hydra attenuata at environmentally relevant concentrations. The Science of the Total Environment 665, 848–854.
| The toxicity of potentially toxic elements (Cu, Fe, Mn, Zn and Ni) to the cnidarian Hydra attenuata at environmentally relevant concentrations.Crossref | GoogleScholarGoogle Scholar | 30790757PubMed |
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., PRISMA Group (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6, e1000097.
| Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.Crossref | GoogleScholarGoogle Scholar | 19753108PubMed |
Moore, M. N., Depledge, M. H., Readman, J. W., and Leonard, D. R. P. (2004). An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutation Research. Fundamental and Molecular Mechanisms of Mutagenesis 552, 247–268.
| An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management.Crossref | GoogleScholarGoogle Scholar | 15288556PubMed |
Murphy, F., and Quinn, B. (2018). The effects of microplastic on freshwater Hydra attenuata feeding, morphology & reproduction. Environmental Pollution 234, 487–494.
| The effects of microplastic on freshwater Hydra attenuata feeding, morphology & reproduction.Crossref | GoogleScholarGoogle Scholar | 29216486PubMed |
Murugadas, A., Zeeshan, M., Thamaraiselvi, K., Ghaskadbi, S., and Akbarsha, M. A. (2016). Hydra as a model organism to decipher the toxic effects of copper oxide nanorod: eco-toxicogenomics approach. Scientific Reports 6, 29663.
| Hydra as a model organism to decipher the toxic effects of copper oxide nanorod: eco-toxicogenomics approach.Crossref | GoogleScholarGoogle Scholar | 27417574PubMed |
Murugadas, A., Mahamuni, D., Nirmaladevi, S. D., Thamaraiselvi, K., Thirumurugan, R., and Akbarsha, M. A. (2019). Hydra as an alternative model organism for toxicity testing: study using the endocrine disrupting chemical Bisphenol A. Biocatalysis and Agricultural Biotechnology 17, 680–684.
| Hydra as an alternative model organism for toxicity testing: study using the endocrine disrupting chemical Bisphenol A.Crossref | GoogleScholarGoogle Scholar |
Napiórkowski, P., Ślebioda, K., and Kentzer, A. (2010). Evaluation of the quality of waters flowing into the Vistula River at the longitude of the city of Toruń by means of biotests with the use of Artemia salina and Hydra attenuata. Limnological Papers 5, 17–25.
| Evaluation of the quality of waters flowing into the Vistula River at the longitude of the city of Toruń by means of biotests with the use of Artemia salina and Hydra attenuata.Crossref | GoogleScholarGoogle Scholar |
Pachura-Bouchet, S., Blaise, C., and Vasseur, P. (2006). Toxicity of nonylphenol on the cnidarian Hydra attenuata and environmental risk assessment. Environmental Toxicology 21, 388–394.
| Toxicity of nonylphenol on the cnidarian Hydra attenuata and environmental risk assessment.Crossref | GoogleScholarGoogle Scholar | 16841324PubMed |
Pascoe, D., Karntanut, W., and Müller, C. T. (2003). Do pharmaceuticals affect freshwater invertebrates? A study with the cnidarian Hydra vulgaris. Chemosphere 51, 521–528.
| Do pharmaceuticals affect freshwater invertebrates? A study with the cnidarian Hydra vulgaris.Crossref | GoogleScholarGoogle Scholar | 12615105PubMed |
Persoone, G., Marsalek, B., Blinova, I., Torokne, A., Zarina, D., Manusadzianas, L., Nalecz-Jawecki, G., Tofan, L., Stepanova, N., Tothova, L., and Kolar, B. (2003). A practical and user-friendly toxicity classification system with microbiotests for natural and wastewaters. Environmental Toxicology 18, 395–402.
| A practical and user-friendly toxicity classification system with microbiotests for natural and wastewaters.Crossref | GoogleScholarGoogle Scholar | 14608609PubMed |
Pollino, C. A., and Holdway, D. A. (1999). Potential of two Hydra species as standard toxicity test animals. Ecotoxicology and Environmental Safety 43, 309–316.
| Potential of two Hydra species as standard toxicity test animals.Crossref | GoogleScholarGoogle Scholar | 10381310PubMed |
Quinn, B., Gagné, F., and Blaise, C. (2009). Evaluation of the acute, chronic and teratogenic effects of a mixture of eleven pharmaceuticals on the cnidarian, Hydra attenuata. The Science of the Total Environment 407, 1072–1079.
| Evaluation of the acute, chronic and teratogenic effects of a mixture of eleven pharmaceuticals on the cnidarian, Hydra attenuata.Crossref | GoogleScholarGoogle Scholar | 19013635PubMed |
Quinn, B., Gagné, F., and Blaise, C. (2012). Hydra, a model system for environmental studies. The International Journal of Developmental Biology 56, 613–625.
| Hydra, a model system for environmental studies.Crossref | GoogleScholarGoogle Scholar | 22689364PubMed |
Singh, P., and Nel, A. (2017). A comparison between Daphnia pulex and Hydra vulgaris as possible test organisms for agricultural run-off and acid mine drainage toxicity assessments. Water S.A. 43, 323–332.
| A comparison between Daphnia pulex and Hydra vulgaris as possible test organisms for agricultural run-off and acid mine drainage toxicity assessments.Crossref | GoogleScholarGoogle Scholar |
Terracciano, M., De Stefano, L., Santos, H. A., Martucci, N. M., Tino, A., Ruggiero, I., Rendina, I., Migliaccio, N., Tortiglione, C., Lamberti, A., and Rea, I. (2016). Silica-based nanovectors: from mother nature to biomedical applications. In ‘Algae: Organisms for Imminent Biotechnology’. (Eds N. Thajuddin, and D. Dhanasekaran.) pp. 211–235. (IntechOpen.)
Terracciano, M., De Stefano, L., Tortiglione, C., Tino, A., and Rea, I. (2019). In vivo toxicity assessment of hybrid diatomite nanovectors using Hydra vulgaris as a model system. Advanced Biosystems 3, 1800247.
| In vivo toxicity assessment of hybrid diatomite nanovectors using Hydra vulgaris as a model system.Crossref | GoogleScholarGoogle Scholar | 32627433PubMed |
Traversetti, L., Del Grosso, F., Malafoglia, V., Colasanti, M., Ceschin, S., Larsen, S., and 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.
| The Hydra regeneration assay reveals ecological risks in running waters: a new proposal to detect environmental teratogenic threats.Crossref | GoogleScholarGoogle Scholar | 27995409PubMed |
Trottier, S., Blaise, C., Kusui, T., and Johnson, E. M. (1997). Acute toxicity assessment of aqueous samples using a microplate-based Hydra attenuata assay. Environmental Toxicology and Water Quality 12, 265–271.
| Acute toxicity assessment of aqueous samples using a microplate-based Hydra attenuata assay.Crossref | GoogleScholarGoogle Scholar |
van Dam, R., Hogan, A., Harford, A., and Markich, S. (2008). Toxicity and metal speciation characterisation of waste water from an abandoned gold mine in tropical northern Australia. Chemosphere 73, 305–313.
| Toxicity and metal speciation characterisation of waste water from an abandoned gold mine in tropical northern Australia.Crossref | GoogleScholarGoogle Scholar |
Wang, M., Maki, C. R., Deng, Y., Tian, Y., and Phillips, T. D. (2017). Development of high capacity enterosorbents for Aflatoxin B1 and other hazardous chemicals. Chemical Research in Toxicology 30, 1694–1701.
| Development of high capacity enterosorbents for Aflatoxin B1 and other hazardous chemicals.Crossref | GoogleScholarGoogle Scholar | 28768106PubMed |
Wang, X., Bai, Y., Huang, H., Tu, T., Wang, Y., Wang, Y., Luo, H., Yao, B., and Su, X. (2019). Degradation of aflatoxin B1 and zearalenone by bacterial and fungal laccases in presence of structurally defined chemicals and complex natural mediators. Toxins 11, 609.
| Degradation of aflatoxin B1 and zearalenone by bacterial and fungal laccases in presence of structurally defined chemicals and complex natural mediators.Crossref | GoogleScholarGoogle Scholar |
Wilby, O. K. (1988). The Hydra regeneration assay. In ‘Proceedings of Workshop Organized by Association Francaise de Teratologie’, 3 June 1988, Royaumont, France. pp. 108–124. (Association Francaise de Teratologie.)
Wilby, O. K., and Tesh, J. M. (1987). Letters to the editor: a Hydra assay as a pre-screen for teratogenic potential. Food and Chemical Toxicology 25, 637–638.
| Letters to the editor: a Hydra assay as a pre-screen for teratogenic potential.Crossref | GoogleScholarGoogle Scholar |
Wilby, O. K., and Tesh, J. M. (1990). The Hydra assay as an early screen for teratogenic potential. Toxicology in vitro 4, 582–583.
| The Hydra assay as an early screen for teratogenic potential.Crossref | GoogleScholarGoogle Scholar | 20702233PubMed |
Wilby, O. K., Newall, D. R., and Tesh, J. M. (1986). A Hydra assay as a pre-screen for teratogenic potential. Food and Chemical Toxicology 24, 651–652.
| A Hydra assay as a pre-screen for teratogenic potential.Crossref | GoogleScholarGoogle Scholar |
Wilby, O. K., Tesh, J. M., and Shore, P. R. (1990). Application of the Hydra regeneration assay: assessment of the potential teratogenic activity of engine exhaust emissions. Toxicology in vitro 4, 612–613.
| Application of the Hydra regeneration assay: assessment of the potential teratogenic activity of engine exhaust emissions.Crossref | GoogleScholarGoogle Scholar | 20702240PubMed |
Yamindago, A., Lee, N., Woo, S., Choi, H., Mun, J. Y., Jang, S.-W., Yang, S. I., Anton-Erxleben, F., Bosch, T. C. G., and Yum, S. (2018). Acute toxic effects of zinc oxide nanoparticles on Hydra magnipapillata. Aquatic Toxicology 205, 130–139.
| Acute toxic effects of zinc oxide nanoparticles on Hydra magnipapillata.Crossref | GoogleScholarGoogle Scholar | 30384194PubMed |
Zeeshan, M., Murugadas, A., Ghaskadbi, S., Ramaswamy, B. R., and Akbarsha, M. A. (2017). Ecotoxicological assessment of cobalt using Hydra model: ROS, oxidative stress, DNA damage, cell cycle arrest, and apoptosis as mechanisms of toxicity. Environmental Pollution 224, 54–69.
| Ecotoxicological assessment of cobalt using Hydra model: ROS, oxidative stress, DNA damage, cell cycle arrest, and apoptosis as mechanisms of toxicity.Crossref | GoogleScholarGoogle Scholar | 28222982PubMed |