Skip to main content
Log in

Long-term cultivation of the groundwater amphipod Niphargus aquilex (Crustacea)

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

A lack of knowledge about the long-term cultivation requirements of groundwater fauna is hampering the establishment of biological criteria to identify chemical threats to groundwater. As a contribution to solving this problem, we have carried out comprehensive laboratory studies on the diet and survival rates of the groundwater amphipod Niphargus aquilex. Preference tests indicated higher consumption of common ash (Fraxinus excelsior) than black alder (Alnus glutinosa) foliage. Compared to detritus from the sampling site, however, survival rates of N. aquilex significantly increased when living oligochaetes were added to ash foliage as an additional food source. Our results indicate that N. aquilex has evolved an omnivorous feeding strategy as an adaptation to the limited availability of nutrient-rich food sources in aquifers. The high acceptance of animal food sources and the predatory behaviour of N. aquilex underline the importance of and requirement for protein in its diet and suggest a high trophic position in groundwater food webs. Based on our results, we provide an optimized culturing protocol that opens up new perspectives for using N. aquilex as an organism for testing the biological quality of groundwater.

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
Fig. 5

Similar content being viewed by others

Data availability

The datasets are available from the corresponding author on a reasonable request.

References

  • Arnscheidt, J., J. Dooley, K. Eriksson, C. Hack, H. J. Hahn, T. Higgins, T. K. McCarthy, C. McInerney & P. Wood, 2012. Biogeography and ecology of Irish groundwater fauna: assessment of the distribution, structure and functioning of subterranean fauna within Irish groundwater systems. (2007-W-MS-1-SI) STRIVE report. Environmental Protection Agency, Ireland.

  • Avramov, M., S. I. Schmidt, C. Griebler, H. J. Hahn & S. Berkhoff, 2010. Dienstleistungen der Grundwasserökosysteme. Korrespondenz Wasserwirtschaft 3: 74–81.

    Google Scholar 

  • Avramov, M., S. I. Schmidt & C. Griebler, 2013. A new bioassay for the ecotoxicological testing of VOCs on groundwater invertebrates and the effects of toluene on Niphargus inopinatus. Aquatic Toxicology 130–131: 1–8.

    Article  Google Scholar 

  • Bärlocher, F., 1982. The contribution of fungal enzymes to the digestion of leaves by Gammarus fossarum Koch (Amphipoda). Oecologia 52: 1–4.

    Article  Google Scholar 

  • Bärlocher, F. & B. Kendrick, 1975. Leaf-conditioning by microorganisms. Oecologia 20: 359–362.

    Article  Google Scholar 

  • Bewick, V., L. Cheek & J. Ball, 2004. Statistics review 12: survival analyses. Critical Care 8: 389–394.

    Article  Google Scholar 

  • Borowsky, B., 2011. Responses to light in two eyeless cave dwelling amphipods (Niphargus ictus and Niphargus frasassianus). Journal of Crustacean Biology 31: 613–616.

    Article  Google Scholar 

  • Boulton, A. J., G. D. Fenwick, P. J. Hancock & M. S. Harvey, 2008. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebrate Systematics 22: 103–116.

    Article  Google Scholar 

  • Danielopol, D. L., C. Griebler, A. Gunatilaka & J. Notenboom, 2003. Present state and future prospects for groundwater ecosystems. Environmental Conservation 30: 104–130.

    Article  CAS  Google Scholar 

  • Danielopol, D. L., J. Gibert, C. Griebler, A. Gunatilaka, H. J. Hahn, G. Messana, J. Notenboom & B. Sket, 2004. Incorporating ecological perspectives in European groundwater management policy. Environmental Conservation 31: 185–189.

    Article  CAS  Google Scholar 

  • De Pauw, N., P. Laureys & J. Morales, 1981. Mass cultivation of Daphnia magna Straus on ricebran. Aquaculture 25: 141–152.

    Article  Google Scholar 

  • Deharveng, L., F. Stoch, J. Gibert, A. Bedos, D. Galassi, M. Zagmajster, A. Brancelj, A. Camacho, F. Fiers, P. Martin, N. Giani, G. Magniez & P. Marmonier, 2009. Groundwater biodiversity in Europe. Freshwater Biology 54: 709–726.

    Article  Google Scholar 

  • Di Lorenzo, T., W. D. Di Marzio, B. Fiasca, D. M. P. Galassi, K. Korbel, S. Iepure, J. L. Pereira, A. S. S. P. Raboleira, S. I. Schmidt & G. C. Hose, 2019. Recommendations for ecotoxicity testing with stygiobiotic species in the framework of groundwater environmental risk assessment. Science of the Total Environment 681: 292–304.

    Article  Google Scholar 

  • Dickson, G. W., 1979. The importance of cave mud sediments in food preference, growth and mortality of the troglobitic amphipod crustacean Crangonyx antennatus Packard (Crangonyctidae). Crustaceana 36: 129–140.

    Article  Google Scholar 

  • Fišer, C., Ž Kovačec, M. Pustovrh & P. Trontelj, 2010. The role of predation in the diet of Niphargus (Amphipoda: Niphargidae). Speleobiology Notes 2: 4–6.

    Google Scholar 

  • Fišer, Ž, R. Luštrik & C. Fišer, 2016. Light triggers habitat choice of eyeless subterranean but not of eyed surface amphipods. The Science of Nature 103: 7.

    Article  Google Scholar 

  • Gibert, J., J. A. Stanford, M.-J. Dole-Olivier & J. V. Ward, 1994. Basic attributes of groundwater ecosystems and prospects for research. In Gibert, J., D. L. Danielopol & J. A. Stanford (eds), Groundwater Ecology Academic Press, London: 7–40.

    Chapter  Google Scholar 

  • Graça, M. A. S., L. Maltby & P. Calow, 1993. Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus. II. Effects on growth, reproduction and physiology. Oecologia 96: 304–309.

    Article  Google Scholar 

  • Griebler, C. & F. Mösslacher, 2003. Grundwasser-Ökologie, Facultas UTB, Stuttgart:

    Google Scholar 

  • Griebler, C., H. Stein, C. Kellermann, S. Berkhoff, H. Brielmann, S. I. Schmidt, S. Drazenka, C. Steube, A. Fuchs & H. J. Hahn, 2010. Ecological assessment of groundwater ecosystems – vision or illusion? Ecological Engineering 36: 1174–1190.

    Article  Google Scholar 

  • Grimm, C. & A. Gerhardt, 2018. Sensitivity towards copper: comparison of stygal and surface water species’ biomonitoring performance in water quality surveillance. International Journal of Scientific Research in Environmental Science and Toxicology 3: 1–15.

    Article  Google Scholar 

  • Hahn, H. J., C. Schweer & C. Griebler, 2018. Grundwasserökosysteme im Recht? Eine kritische Betrachtung zur rechtlichen Stellung von Grundwasserökosystemen. Grundwasser 23: 209–218.

    Article  Google Scholar 

  • Hancock, P. J., A. J. Boulton & W. F. Humphreys, 2005. Aquifers and hyporheic zones: towards an ecological understanding of groundwater. Hydrogeology Journal 13: 98–111.

    Article  CAS  Google Scholar 

  • Hargrave, B. T., 1970. The utilization of benthic microflora by Hyalella azteca (Amphipoda). Journal of Animal Ecology 39: 427–437.

    Article  Google Scholar 

  • Hargrave, B. T., 1972. Prediction of egestion by the deposit-feeding amphipod Hyalella azteca. Oikos 23: 116–124.

    Article  Google Scholar 

  • Herman, J. S., D. C. Culver & J. Salzman, 2001. Groundwater ecosystems and the service of water purification. Stanford Environmental Law Journal 20: 479–495.

    Google Scholar 

  • Hervant, F. & D. Renault, 2002. Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms. The Journal of Experimental Biology 205: 2079–2087.

    Article  CAS  Google Scholar 

  • Hervant, F., J. Mathieu, H. Barré, K. Simon & C. Pinon, 1997. Comparative study on the bahavioural, ventialatory and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comparative Biochemistry and Physiology Part A: Physiology 118: 1277–1283.

    Article  Google Scholar 

  • Hervant, F., J. Mathieu & H. Barré, 1999. Comparative study on the metabolic responses of subterranean and surface-dwelling amphipods to long-term starvation and subsequent refeeding. The Journal of Experimental Biology 202: 3587–3595.

    Article  Google Scholar 

  • Humphreys, W. F., 2007. Comment on assessing the need for groundwater quality guidelines for pesticides using the species sensitivity distribution approach by Hose, 2005. Human and Ecological Risk Assessment 13: 236–240.

    Article  Google Scholar 

  • Humphreys, W. F., 2009. Hydrogeology and groundwater ecology: does each inform the other? Hydrogeology Journal 17: 5–21.

    Article  CAS  Google Scholar 

  • Hüppop, K., 1985. The role of metabolism in the evolution of cave animals. Bulletin of the National Speleological Society 47: 136–146.

    Google Scholar 

  • Issartel, J., F. Hervant, Y. Voituron, D. Renault & P. Vernon, 2005. Behavioural, ventilatory and respiratory of epigean and hypogean crustaceans to different temperatures. Comparative Biochemistry and Physiology Part A: Physiology 141: 1–7.

    Article  Google Scholar 

  • Jenio, F., 1980. The life cycle and ecology of Gammarus troglophilus Hubricht & Mackins. Crustaceana, Supplements 6: 204–215.

    Google Scholar 

  • Johns, T., J. I. Jones, L. Knight, L. Maurice, P. Wood & A. Robertson, 2015. Regional-scale drivers of groundwater faunal distributions. Freshwater Science 34: 316–328.

    Article  Google Scholar 

  • Kinsey, J., T. J. Cooney & K. S. Simon, 2007. A comparison of the leaf shredding ability and influence on microbial films of surface and cave forms of Gammarus minus Say. Hydrobiologia 589: 199–205.

    Article  Google Scholar 

  • Knight, L. R. F. D. & T. Johns, 2015. Auto-ecological studies on Niphargus aquilex (Schiödte, 1855) and Niphargus glenniei (Spooner, 1952) (Crustacea: Amphipoda: Niphargidae). Cave and Karst Science 42: 63–77.

    Google Scholar 

  • Kosnicki, E. & E. Julius, 2019. Life-history aspects of Stygobromus pecki. Final report. Texas Edwards Aquifer Authority, San Antonio, TX, USA.

  • Kunz, P. Y., C. Kienle & A. Gerhardt, 2010. Gammarus ssp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests. Reviews of Environmental Contamination and Toxicology 205: 1–76.

    CAS  Google Scholar 

  • Kureck, A., 1964. Light sensitivity in the amphipode, Niphargus aquilex schellenbergi Karaman. Experientia 20: 523–524.

    Article  CAS  Google Scholar 

  • Kureck, A., 1967. Über die tagesperiodische Ausdrift von Niphargus aquilex schellenbergi Karaman aus Quellen. Zeitschrift für Morphologie und Ökologie der Tiere 58: 247–262.

    Article  Google Scholar 

  • Lawniczak, M., C. Romestaing, D. Roussel, C. Maazouzi, D. Renault & F. Hervant, 2013. Preventive antioxidant responses to extreme oxygen level fluctuation in a subterranean crustacean. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 165: 299–303.

    Article  CAS  Google Scholar 

  • Lindemann, R. L., 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399–417.

    Article  Google Scholar 

  • Little, S., T. Haslehurst & P. J. Wood, 2006. Intra-specific predation and survivourship of Gammarus pulex (Crustacea: Amphipoda) within aquatic karstic habitats. Cave and Karst Science 33: 73–76.

    Google Scholar 

  • Ludwig, F., 2011. Regional variation of chemical groundwater composition in Hessen, Germany, and its relation to the aquifer geology. Dissertation, Albert-Ludwigs-Universität Freiburg im Breisgau.

  • Luštrik, R., M. Turjak, S. Kralj-Fišer & C. Fišer, 2011. Coexistence of surface and cave amphipods in an ecotone environment. Contributions to Zoology 80: 133–141.

    Article  Google Scholar 

  • Malard, F. & F. Hervant, 1999. Oxygen supply and the adaptations of animals in groundwater. Freshwater Biology 41: 1–30.

    Article  Google Scholar 

  • Maltby, L., S. A. Clayton, R. M. Wood & N. McLoughlin, 2002. Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: robustness, responsiveness, and relevance. Environmental Toxicology and Chemistry 21: 361–368.

    Article  CAS  Google Scholar 

  • Marmonier, P., C. Maazouzi, A. Foulquier, S. Navel, C. François, F. Hervant, F. Mermillod-Blondin, A. Vieney, S. Barraud, A. Togola & C. Piscart, 2013. The use of crustaceans as sentinel organisms to evaluate groundwater ecological quality. Ecological Engineering 57: 118–132.

    Article  Google Scholar 

  • McCahon, C. P. & D. Pascoe, 1988. Culture techniques for three freshwater macroinvertebrate species and their use in toxicity tests. Chemosphere 17: 2471–2480.

    Article  CAS  Google Scholar 

  • Mezek, T., T. Simčič, M. T. Arts & A. Brancelj, 2010. Effect of fasting on hypogean (Niphargus stygius) and epigean (Gammarus fossarum) amphipods: a laboratory study. Aquatic Ecology 44: 397–408.

    Article  CAS  Google Scholar 

  • Navel, S., L. Simon, C. Lecuyer, F. Fourel & F. Mermillod-Blondin, 2011. The shredding activity of gammarids facilitates the processing of organic matter by the subterranean amphipod Niphargus rhenorhodanensis. Freshwater Biology 56: 481–490.

    Article  CAS  Google Scholar 

  • Nelson, D. & F. M. Wilhelm, 2011. Survival and growth of the stygophilic amphipod Gammarus troglophilus under laboratory conditions. Journal of Crustacean Biology 31: 424–433.

    Article  Google Scholar 

  • Nowlin, W. H., B. F. Schwartz, McL. Worsham & R. Gibson, 2016. Refugia research: development of husbandry and captive propagation techniques for invertebrates covered under the Edwards aquifer habitat conservation plan. Final report. Hg. v. Texas Edwards Aquifer Authority.

  • Pyke, D. A. & J. N. Thompson, 1986. Statistical analysis of survival and removal rate experiments. Ecology 67: 240–245.

    Article  Google Scholar 

  • Rumm, P., 1999. Untersuchungen zum Abbau partikulärer organischer Substanzen in einem Langsamsandfilter durch Metazoen am Beispiel von Niphargus fontanus. Dissertation, Carl von Ossietzky Universität Oldenburg.

  • Simčič, T. & A. Brancelj, 2007. The effect of oxygen consumption in two amphipod crustaceans – the hypogean Niphargus stygius and the epigean Gammarus fossarum. Marine and Freshwater Behaviour and Physiology 40: 141–150.

    Article  Google Scholar 

  • Simčič, T., S. Lukancic & A. Brancelj, 2005. Comparative study of electron transport system activity and oxygen consumption of amphipods from caves and surface habitats. Freshwater Biology 50: 494–501.

    Article  Google Scholar 

  • Sket, B., 1999. The nature of biodiversity in hypogean waters and how it is endangered. Biodiversity and Conservation 8: 1319–1338.

    Article  Google Scholar 

  • Stein, H., C. Kellermann, S. I. Schmidt, H. Brielmann, C. Steube, S. E. Berkhoff, A. Fuchs, H. J. Hahn, B. Thulin & C. Griebler, 2010. The potential use of fauna and bacteria as ecological indicators for the assessment of groundwater quality. Journal of Environmental Monitoring 12: 242–254.

    Article  CAS  Google Scholar 

  • Steube, C., S. Richter & C. Griebler, 2009. First attempt towards an integrative concept for the ecological assessment of groundwater ecosystems. Hydrogeology Journal 17: 23–35.

    Article  Google Scholar 

  • Thulin, B. & H. J. Hahn, 2008. Ecology and living conditions of groundwater fauna. Technical Report TR-08-06.

  • Tomlinson, M., A. J. Boulton, P. J. Hancock & P. G. Cook, 2007. Deliberate omission or unfortunate oversight: should stygofaunal surveys be included in routine groundwater monitoring programs? Hydrogeology Journal 15: 1317–1320.

    Article  Google Scholar 

  • Väinölä, R., J. D. S. Witt, M. Grabowski, J. H. Bradbury, K. Jazdzewski & B. Sket, 2008. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595: 241–255.

    Article  Google Scholar 

  • Weitowitz, D. C., A. L. Robertson, J. P. Bloomfield, L. Maurice & J. Reiss, 2019. Obligate groundwater crustaceans mediate biofilm interactions in a subsurface food web. Freshwater Science 38: 491–502.

    Article  Google Scholar 

  • Worrall, T. P. & P. J. Wood, 2007. Cannibalism within freshwater shrimp populations (Gammarus duebeni - Crustacea: Amphipoda) from spring, riverine and subterranean habitats, Marble Arch Cave System (Northern Ireland). Cave and Karst Science 34: 33–36.

    Google Scholar 

  • Wotton, R. S., 2007. Do benthic biologists pay enough attention to aggregates formed in the water column of streams and rivers? Journal of the North American Benthological Society 26: 1–11.

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Maria Wille for conducting the leaf preference test. We also thank Susanne Isabel Schmidt (UFZ Centre for Environmental Research, Magdeburg, Germany) and Elisabeth Pohlon (Justus Liebig University Gießen, Germany) for proofreading the manuscript. The study was part of the joint research project GroundCare that was funded by the German Federal Ministry of Education and Research (BMBF) through the project consortium ‘GroundCare’ (033W037E) via the call ‘Regional Water Resources Management for a Sustainable Protection of Waters in Germany’ (ReWaM) and the funding scheme ‘Sustainable Water Management’ (NaWaM).

Funding

This study was financially supported by the German Federal Ministry of Education and Research (BMBF) through the project consortium ‘GroundCare’ (Grant No. 033W037E) via the call ‘Regional Water Resources Management for a Sustainable Protection of Waters in Germany’ (ReWaM) and the funding scheme ‘Sustainable Water Management’ (NaWaM).

Author information

Authors and Affiliations

Authors

Contributions

NKR and JM designed the study; NKR performed the field and lab work under supervision of JM; NKR analyzed the data with assistance of JM; NKR wrote the first draft of the manuscript; NKR, JM and VW contributed to writing-revisions and editing substantially; VW procured funding and supervised the study; all authors read and approved the final manuscript.

Corresponding author

Correspondence to Nora K. Rütz.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Handling editor: Stuart Halse

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rütz, N.K., Marxsen, J. & Wolters, V. Long-term cultivation of the groundwater amphipod Niphargus aquilex (Crustacea). Hydrobiologia 850, 269–281 (2023). https://doi.org/10.1007/s10750-022-05058-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-022-05058-6

Keywords

Navigation