Abstract
Larvae (glochidia) of the freshwater mussel order Unionida undergo a brief parasitic phase by attaching to and metamorphosing on suitable host fish. Here, novel observations of complex glochidia release strategies and glochidia morphometry are reported and compared in two sympatric New Zealand hyriid species, Echyridella menziesii (Gray, 1843) and Echyridella aucklandica (Gray, 1843). Echyridella menziesii produced glochidia averaging 277 ± 0.7 (SE) µm in diameter which were broadcast individually and bound to mucus threads into the water column. In contrast, the sympatric E. aucklandica produced miniature glochidia (99 ± 0.3 µm SE) embedded in functional conglutinates, thought to facilitate host fish attraction. To our knowledge, this is the first Unionida species, outside of North America, reported to be using functional conglutinates to mimic host diet as an infection strategy. The production of miniature glochidia that were morphologically distinguishable from those of E. menziesii, coupled with contrasting release strategies, highlights the potential for partitioning of host resources through contrasting attachment strategies and infection times. Additionally, these findings provide the basis for distinguishing glochidia of the two Echyridella species in field studies of host fish infection and highlight the need to develop novel methods for captive propagation of E. aucklandica to support restoration of declining populations.
This is a preview of subscription content, access via your institution.




References
Aldridge, D. C. & A. L. Mcivor, 2003. Gill evacuation and release of glochidia by Unio pictorum and Unio tumidus (Bivalvia: Unionidae) under thermal and hypoxic stress. Journal of Molluscan Studies 69: 55–59.
Atkins, L. G., 1979. Observations of the glochidial stage of the freshwater mussel Hyridella (Hyridella) drapeta (Iredale) (Mollusca: Pelecypoda). Australian Journal of Marine and Freshwater Research 30: 411–416.
Bauer, G., 1988. Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biological Conservation 45: 239–253.
Bauer, G., 1994. The adaptive value of offspring size among freshwater mussels (Bivalvia; Unionoidea). Journal of Animal Ecology 63: 933–944.
Bauer, G. & K. Wächtler, 2001. Ecology and evolution of the naiads. In Wächtler, K. (ed), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer, Berlin: 383–388.
Barnhart, M. C., W. R. Haag & W. N. Roston, 2008. Adaptations to host infection and larval parasitism in Unionoida. Journal of the North American Benthological Society 27: 370–394.
Brown, R. L., S. J. Clearwater, K. J. Thompson, M. L. Martin & P. G. Jellyman, 2017. Comparison of host fish suitability for larvae (glochidia) of the native freshwater mussel, Echyridella menziesii. Poster presentation to the Integrating Multiple Aquatic Values, 5th Biennial Symposium of the International Society for River Science, Hamilton, New Zealand 19–24 November 2017.
Byrne, M., 1998. Reproduction of river and lake populations of Hyridella depressa (Unionacea: Hyriidae) in New South Wales: implications for their conservation. Hydrobiologia 389: 29–43.
Clearwater, S. J., K. J. Thompson & C. W. Hickey, 2014. Acute toxicity of copper, zinc, and ammonia to larvae (Glochidia) of a native freshwater mussel Echyridella menziesii in New Zealand. Archives of environmental contamination and toxicology 66: 213–226.
Ferguson, C. D., M. J. Blum, M. L. Raymer, M. S. Eackles & D. E. Krane, 2013. Population structure, multiple paternity, and long-distance transport of spermatozoa in the freshwater mussel Lampsilis cardium (Bivalvia: Unionidae). Freshwater Science 32: 267–282.
Ganser, A. M., T. J. Newton & R. J. Haro, 2015. Effects of elevated water temperature on physiological responses in adult freshwater mussels. Freshwater Biology 60: 1705–1716.
Geist, J. & K. Auerswald, 2007. Physicochemical stream bed characteristics and recruitment of the freshwater pearl mussel (Margaritifera margaritifera). Freshwater Biology 52: 2299–2316.
Grainger, N., J. S. Harding, T. Drinan, K. J. Collier, B. Smith, R. Death, T. Makan & J. Rolfe, 2018. Conservation Status of New Zealand Freshwater Invertebrates, New Zealand Threat Classification Series 28. Department of Conservation, Wellington: 1–28.
Haag, W. R., 2012. North American Freshwater Mussels: Natural History, Ecology, and Conservation. Cambridge University Press, Cambridge.
Haag, W. R., 2013. The role of fecundity and reproductive effort in defining life-history strategies of North American freshwater mussels. Biological Reviews. 88: 745–766.
Haag, W. R. & J. L. Staton, 2003. Variation in fecundity and other reproductive traits in freshwater mussels. Freshwater Biology 48: 2118–2130.
Haag, W. R. & M. L. Warren Jr., 1998. Role of ecological factors and reproductive strategies in structuring freshwater mussel communities. Canadian Journal of Fisheries and Aquatic Sciences 55: 297–306.
Haag, W. R. & M. L. Warren Jr., 2003. Host fishes and infection strategies of freshwater mussels in large Mobile Basin streams, USA. Journal of the North American Benthological Society 22: 78–91.
Haag, W. R., R. S. Butler & P. D. Hartfield, 1995. An extraordinary reproductive strategy in freshwater bivalves: prey mimicry to facilitate larval dispersal. Freshwater Biology 34: 471–476.
Hartfield, P. & E. Hartfield, 1996. Observations on the conglutinates of Ptychobranchus greeni (Conrad, 1834) (Mollusca: Bivalvia: Unionidae). American Midland Naturalist 135: 370–375.
Hastie, L. C. & M. R. Young, 2003. Timing of spawning and glochidial release in Scottish freshwater pearl mussel (Margaritifera margaritifera) populations. Freshwater biology 48: 2107–2117.
Hine, P. M., 1978. Distribution of some parasites of freshwater eels in New Zealand. New Zealand Journal of Marine and Freshwater Research 12: 179–187.
Hoggarth, M. A., 1987. Determination of anterior-posterior orientation of glochidia by the examination of glochidial valves present within the umbos of juvenile unionid clams (Mollusca: Bivalvia). The Ohio Journal of Science 87: 93–95.
Hoggarth, M. A. & A. S. Gaunt, 1988. Mechanics of glochidial attachment (Mollusca: Bivalvia: Unionidae). Journal of morphology 198: 71–81.
Jones, J. W., R. J. Neves, S. A. Ahlstedt & R. A. Mair, 2004. Life history and propagation of the endangered dromedary pearly mussel (Dromus dromas). Journal of the North American Benthological Society 23: 515–525.
Jupiter, S. D. & M. Byrne, 1997. Light and scanning electron microscopy of the embryos and glochidia larvae of the Australian freshwater bivalve Hyridella depressa (Hyriidae). Invertebrate Reproduction & Development 32: 177–186.
Kat, P. W., 1984. Parasitism and the unionacea (bivalvia). Biological Reviews 59: 189–207.
Kennedy, T. & W. R. Haag, 2005. Using morphometrics to identify glochidia from a diverse freshwater mussel community. Journal of the North American Benthological Society 24: 880–889.
Klunzinger, M. W., G. J. Thomson, S. J. Beatty, D. L. Morgan & A. J. Lymbery, 2013. Morphological and morphometrical description of the glochidia of Westralunio carteri Iredale, 1934 (Bivalvia: Unionoida: Hyriidae). Molluscan Research 33: 104–109.
Lopes-Lima, M., R. Sousa, J. Geist, D. C. Aldridge, R. Araujo, J. Bergengren & K. Douda, 2017. Conservation status of freshwater mussels in Europe: state of the art and future challenges. Biological Reviews 92: 572–607.
Marshall, B. A., M. C. Fenwick & P. A. Ritchie, 2014. New Zealand recent Hyriidae (Mollusca: Bivalvia: Unionida). Molluscan Research 34: 181–200.
McMichael, D. F. & I. D. Hiscock, 1958. A monograph of the freshwater mussels (Mollusca: Pelecypoda) of the Australian region. Marine and Freshwater Research 9: 372.
Melchior, M., 2017. Effects of water temperature on the release and viability of glochidia of the freshwater mussel, Echyridella menziesii. (Unpublished Dissertation), University of Waikato.
Nezlin, L. P., R. A. Cunjak, A. A. Zotin & V. V. Ziuganov, 1994. Glochidium morphology of the freshwater pearl mussel (Margaritifera margaritifera) and glochidiosis of Atlantic salmon (Salmo salar): a study by scanning electron microscopy. Canadian Journal of Zoology 72: 15–21.
Pasteur, G., 1982. A classificatory review of mimicry systems. Annual Review of Ecology and Systematics 13: 169–199.
Patterson, M., R. Mair, N. Eckert, C. Gatenby, T. Brady, J. Jones, R. Simmons & J. Devers, 2018. Freshwater Mussel Propagation for Restoration. Cambridge University Press, Cambridge.
Percival, E., 1931. A note on the life history of Diplodon lutulentus Gould. Transactions and Proceedings of the New Zealand Institute 62: 86–91.
Roper, D. S. & C. W. Hickey, 1994. Population structure, shell morphology, age and condition of the freshwater mussel Hyridella menziesii (Unionacea: Hyriidae) from seven lake and river sites in the Waikato River system. Hydrobiologia 284: 205–217.
Watters, G. T., 2002. The kinetic conglutinate of the creeper freshwater mussel, Strophitus undulatus (Say, 1817). Journal of Molluscan Studies 68: 155–158.
Watters, G. T., 2008. The morphology of conglutinates and conglutinate-like structures in North American freshwater mussels: a scanning-electron microscopy survey. Novapex 9: 1–2.
Zimmerman, L. L. & R. J. Neves, 2001. Effects of temperature on duration of viability for glochidia of freshwater mussels (Bivalvia: Unionidae). American Malacological Bulletin 17: 31–36.
Ziuganov, V. V., A. A. Zotin, L. P. Nezlin & V. Tretiakov, 1994. The Freshwater Pearl Mussels and Their Relationships with Salmonid Fish. VNIRO Publishing House, Moscow.
Acknowledgements
This research was funded by the New Zealand Ministry of Innovation and Employment (MBIE) grant to NIWA for the “Cultural Keystone Species: Co-management and restoration of our freshwater taonga species” Programme (Grant No. C01X1616). The authors thank Thomas Allen and Elmie Senekal for field assistance, Karen Thompson for advice on Echyridella menziesii brood pouch analyses and Wendell Haag for advice on North American conglutinates. We thank Manuel Lopes-Lima who provided helpful comments on an earlier manuscript draft and sincerely thank two anonymous reviewers for their valuable feedback.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Guest editors: Manuel P. M. Lopes-Lima, Nicoletta Riccardi, Maria Urbanska & Ronaldo G. Sousa / Biology and Conservation of Freshwater Molluscs
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 1 (MP4 22261 kb)
Online Resource 1. Echyridella menziesii female releasing glochidia as individuals and attached to mucus strings
Supplementary material 2 (MP4 5434 kb)
Online Resource 2. Echyridella aucklandica conglutinates released in the aquarium
Supplementary material 3 (MP4 14051 kb)
Online Resource 3. Echyridella aucklandica conglutinates attached temporarily to adhesive mucus strand protruding from between the extended tissues of the mantle margin
Rights and permissions
About this article
Cite this article
Melchior, M., Collier, K.J. & Clearwater, S.J. First record of complex release strategies and morphometry of glochidia in sympatric Echyridella species (Bivalvia: Unionida: Hyriidae). Hydrobiologia 848, 3115–3126 (2021). https://doi.org/10.1007/s10750-019-03995-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-019-03995-3