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Observations on the reproductive biology of Unio terminalis (Bivalvia: Unionidae)

Year 2017, Volume 34, Issue 3, 303 - 309, 26.09.2017
https://doi.org/10.12714/egejfas.2017.34.3.09

Abstract

In the present study some observations were made on the reproductive biology of Unio terminalis (Bourguignat, 1852; Bivalvia: Unionidae) from River Çine (Aydın, Turkey). Egg packages that are typically seen in the breeding process of freshwater mussels were laid by the adults in May and November at 21–25 Cº water temperature under the laboratory conditions. The egg packages were contained eggs or/and glochidia. The mean egg diameter was ~226 μm and no correlation was found with the broodstck size (R2<0.01). At the same time larvae size did not differ with the broodstck size (p>0.1); the mean height of the glochidia were ~186 μm. Density of the glochidia were 30±6 mm-2. The openning closing movement of the glochidial valves was observed; the fastest frequency was recorded as 1.2 sec-1 and larvae were able to keep this frequency up to 15 seconds. But this frequency was recorded as less than 1 movement per minute for many cases with live glochidia. After releasing, glochidia were found only at the gills of Andinoacara sp. among 3 different fish species.

References

  • Aldridge, D. C., & McIvor, A. L. (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, no. (1): 55-59. doi: 10.1093/mollus/69.1.55
  • Bauer, G. (1994). The Adaptive Value of Offspring Size among Freshwater Mussels (Bivalvia; Unionidae). Journal of Animal Ecology, 63: 933–944. doi: 10.2307/5270
  • Bogan, A.E. (2008). Global diversity of freshwater mussels (Mollusca: Bivalvia) in freshwater. Hydrobiologia, 595: 139–147. doi: 10.1007/s10750-007-9011-7
  • Chester, C.M. (1996). The effect of adult nutrition on the reproduction and development of the estuarine nudibranch, Tenellia adspersa (Nordmann, 1845). Journal of Experimental Marine Biology and Ecology,198: 113-130. doi: 10.1016/0022-0981(95)00197-2
  • Çek, Ş., & Şereflişan, H. (2006). Certain reproductive characteristics of the freshwater mussel Unio terminalis delicates (lea, 1863) in Gölbaşı lake, Turkey. Aquaculture Research, 37(13), 1305-1315. doi:10.1111/j.1365-2109.2006.01563.x
  • Engel, H. (1990). Untersuchungen zur Autökologie von Unio crassus in Nord deutschland. Dissertation, Universität Hanhover. Thesis (doctoral)-Universität Hannover, 1990.
  • Ercan, E., Gaygusuz, Ö., Tarkan, A. S., Reichard, M., & Smith, C. (2013). The ecology of freshwater bivalves in the lake sapanca basin, Turkey. Turkish Journal of Zoology, 37(6): 730-738. doi:10.3906/zoo-1212-23
  • Ercan, E., & Tarkan, A.S. (2014). Effect of Salinity on the Growth and Survival of the Freshwater Mussel, Unio crassus, in an Environmentally Disturbed River. Pakistan Journal of Zoology, vol. 46(5): 1399-1406.
  • Geist, J. (2010). Strategies for the conservation of endangered freshwater pearl mussel (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia, 664: 69–88. doi: 10.1007/s10750-010-0190-2
  • Graf, D. L. (2013). Patterns of Freshwater Bivalve Global Diversity and the State of Phylogenetic Studies on the Unionoida, Sphaeriidae, and Cyrenidae. American Malacological Bulletin, 31: 135-153. doi: 10.4003/006.031.0106
  • Güler, M., & Lök, A. (2014). Embryonic development and intracapsular feeding in Hexaplex trunculus (Gastropoda: Muricidae). Marine Ecology, 35: 193 – 203. doi:10.1111/maec.12066
  • Heard, W. L. (1975). Sexuality and other aspects of reproduction in Anodonta (Pelecypoda: Unionidae). Malacologia, 15 (1):81–103.
  • Hendry, A., & Day T. (2003). Revisiting the positive correlation between female size and egg size. Evolutionary Ecology Research, 5: 421–429.
  • Henley, W. F., & Neves, R. J. (2001). Behavioral responses of glochidia of freshwater mussels (bivalvia: Unionidae) to chemical cues of fish. American Malacological Bulletin, 16(1-2), 131-135.
  • Hochwald, S. & Bauer, G. (1990). Untersuchungen zur Populations ökologie und Fortpflanzungs biologie der Bachmuschel Unio crassus (PHIL.) 1788. Schriftenreihe Bayerisches Landesamt für Umweltschutz Heft 97: 31–49; München.
  • Korniushin, A. V., & Glaubrecht, M. (2003). Novel reproductive modes in freshwater clams: brooding and larval morphology in Southeast Asian taxa of Corbicula (Mollusca, Bivalvia, Corbiculidae). Acta Zoologica, 84: 291–315. doi: 10.1046/j.1463-6395.2003.00150.x
  • Krug, P.J. (1998). Poecilogony in an estuarine opisthobranch: planktotrophy, lecithotrophy, and mixed clutches in a population of the ascoglossan Alderia modesta. Marine Biology, 132: 483-494. doi: 10.1007/s002270050414
  • Lamand, F., Roche, K., & Beisel, J. N. (2016). Glochidial infestation by the endangered mollusc Unio crassus in rivers of north-eastern France: Phoxinus phoxinus and Cottus gobio as primary fish hosts. Aquatic Conservation: Marine and Freshwater Ecosystems, 26: 445–455. doi: 10.1002/aqc.2603
  • Lopes-Lima, M. & Seddon, M.B. (2014). Unio terminalis. The IUCN Red List of Threatened Species 2014: e.T164866A42466771. doi: 10.2305/IUCN.UK.2014-1.RLTS.T164866A42466771.en
  • Lundberg, S. & Österling, M. (2016). Return of the Thick-shelled River Mussel – Restoring floodplains, habitats and connectivity by using mussels and brains. Handbook, UC4LIFE Project, Skåne County Administrative Board.
  • Lydeard, C., Cowie, R. H., Ponder, W. F., Bogan, A. E., Bouchet, P., Clark, S. A., Cummings, K.S., Frest, T.J., Gargominy, O., Herbert, D.G., Hershler, R., Perez, K.E., Roth, B., Seddon, M., Strong, E.E. &Thompson, F. G. (2004). The global decline of nonmarine mollusks. Bioscience, 54(4) :321-330. doi: 10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2
  • Ostrovsky, I., Gophen, M., & Kalikhman, I. (1993). Distribution, growth, production, and ecological significance of the clam Unio terminalis in Lake Kinneret, Israel. Hydrobiologia, 271: 49–63. doi: 10.1007/BF00005695
  • Pechenik, J.A. (1979). Role of encapsulation in invertebrate life histories. American Naturalist, 114:859–870
  • Reichard, M. Polačik, M., Tarkan, A.S., Spence, R., Gaygusuz, Ö., Ercan, E., Ondračková, M. & Smith, C. (2010). The bitterling-mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution, 64(10): 3047-3056. doi: 10.1111/j.1558-5646.2010.01032.x
  • Smith, C., & Fretwell, S. (1974). The optimal balance between size and number of offspring. American Naturalist, 108:499–506.
  • Soto, D. & Mena, G. (1999). Filter feeding by the freshwater mussel, Diplodon chilensis, as a biocontrol of salmon farming eutrophication. Aquaculture, 171: 65–81. doi: 10.1016/S0044-8486(98)00420-7
  • Strayer, D. L., Hunter, D. C., Smith, L. C., & Borg, C. K. (1994). Distribution, abundance, and roles of freshwater clams (Bivalvia, Unionidae) in the freshwater tidal Hudson River. Freshwater Biology, 31: 239–248. doi: 10.1111/j.1365-2427.1994.tb00858.x
  • Strayer, D.L., Downing, J.A., Haag, W.R., King, T.L., Layzer, J.B., Newton, T.J., & Nichols, S.J. (2004). Changing Perspectives on Pearly Mussels, North America's Most Imperiled Animals. BioScience, 54: 429–439. doi: 10.1641/0006-3568(2004)054[0429:CPOPMN]2.0.CO;2
  • Şereflişan, H., Menderes, S., & Soylu, S. (2009). Description of glochidia of three species of freshwater mussels (unionidae) from southeastern Turkey. Malacologia, 51 doi:10.4002/040.051.0112
  • Şereflişan, H. (2014). Investigation on Economical Characteristics of Freshwater Mussels in Gölbaşi Lake (Hatay). Yunus Araştırma Bülteni, 2014 (3), 43-49. doi: 10.17693/yunusae.v2014i21953.235714
  • Taeubert, J., Martinez, A. M. P., Gum, B., & Geist, J. (2012). The relationship between endangered thick-shelled river mussel (Unio crassus) and its host fishes. Biological Conservation, 155, 94-103. doi:10.1016/j.biocon.2012.06.005
  • Vaughn, C. C. (2012). Life history traits and abundance can predict local colonization and extinction rates of freshwater mussels. Freshwater Biology, 57: 982–992. doi: 10.1111/j.1365-2427.2012.02759.x
  • Vaughn, C. C., & Hakenkamp, C. C. (2001). The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology, 46: 1431–1446. doi: 10.1046/j.1365-2427.2001.00771.x
  • Wachtler, K., Dreher-Mansur, M. C. & Richter, T. (2001). Larval types and early postlarval biology in naiads (Unionoida). In Bauer, G. & K. Wachtler (eds), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin, Heidelberg: 93–125.
  • Watters, G. (2001). The Evolution of the Unionacea in North America, and Its Implications for the Worldwide Fauna - In: Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin, pp. 281–307.
  • Weber, E. (2005). Population size and structure of three mussel species (Bivalvia: Unionidae) in a northeastern German river with special regard to influences of environmental factors. Hydrobiologia, 537, 169–183. doi: 10.1007/s10750-004-2839-1
  • Welker, M., & Walz, N. (1998). Can mussels control the plankton in rivers? A planktological approach applying a Lagrangian sampling strategy. Limnology and Oceanography, 43: 753–762. doi: 10.4319/lo.1998.43.5.0753
  • Wood, E. M. (1974). Some mechanisms involved in host recognition and attachment of the glochidium larva of Anodonta cygnea (Mollusca: Bivalvia). Journal of Zoology, 173: 15–30. doi: 10.1111/j.1469-7998.1974.tb01744.x
  • Zettler, M. L., & Jueg, U. (2007). The situation of the freshwater mussel Unio crassus (Philipsson 1788) in north-east Germany and its monitoring in terms of the EC Habitats Directive. Mollusca, 25: 165–174.
  • Zimmerman, L., & Neves, R. J. (2002). Effects of temperature on duration of viability for glochidia of freshwater mussels (Bivalvia: Unionidae). American Malacological Bulletin, 17: 31–35.

Unio terminalis (Bivalvia: Unionidae)' in üreme biyolojisi üzerine gözlemler

Year 2017, Volume 34, Issue 3, 303 - 309, 26.09.2017
https://doi.org/10.12714/egejfas.2017.34.3.09

Abstract

Çalışmamızda Çine Çayından toplanan tatlı su midyesi Unio terminalis (Bourguignat, 1852; Bivalvia: Unionidae)’ in üreme biyolojisi ile ilgili gözlemler yapılmıştır. Tatlı su midyelerinin kendilerine has üreme şekillerinde görülen yumurta paketleri, laboratuvar şartları altında yaklaşık 21–25 Cº su sıcaklığında Mayıs ve Kasım aylarında elde edilmiştir. Yumurta paketlerinin yumurta ve/veya özelleşmiş bir larva tipi olan glochidia ihtiva ettiği gözlenmiştir. Yumurtaların çapı ~225 μm olarak tespit edilmiştir; yumurtaları bırakan dişi boyu ve yumurta çapı arasında bir ilişki bulunmamıştır (R2<0,01). Elde edilen glochidia ortalama büyüklüğü ~185 μm ve bırakıldığı yapıdaki yoğunluğu 30±6 adet mm-2 olarak kaydedilmiştir. Farklı boylardaki dişilerden elde edilen glochidia boyları arasında anlamlı bir büyüklük farkı bulunmamıştır (p>0,1). Larvalarının kapak hareketlerinin gözlenmesi sonucu en hızlı 1,2 sn-1frekansında kapaklarını açıp kapattıkları ve bu hızı 15 sn boyunca koruyabildikleri gözlenmiştir. Bununla beraber, birçok larvanın 1 dk-1 frekansından daha düşük sıklıkta kapak açma kapama hareketi yaptığı tespit edilmiştir. Farklı balık türleri ile birlikte yürütülen larva tutunma çalışmasında glochidia sadece Andinoacara cinsi balıkların solungaçlarında tespit edilmiştir.

References

  • Aldridge, D. C., & McIvor, A. L. (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, no. (1): 55-59. doi: 10.1093/mollus/69.1.55
  • Bauer, G. (1994). The Adaptive Value of Offspring Size among Freshwater Mussels (Bivalvia; Unionidae). Journal of Animal Ecology, 63: 933–944. doi: 10.2307/5270
  • Bogan, A.E. (2008). Global diversity of freshwater mussels (Mollusca: Bivalvia) in freshwater. Hydrobiologia, 595: 139–147. doi: 10.1007/s10750-007-9011-7
  • Chester, C.M. (1996). The effect of adult nutrition on the reproduction and development of the estuarine nudibranch, Tenellia adspersa (Nordmann, 1845). Journal of Experimental Marine Biology and Ecology,198: 113-130. doi: 10.1016/0022-0981(95)00197-2
  • Çek, Ş., & Şereflişan, H. (2006). Certain reproductive characteristics of the freshwater mussel Unio terminalis delicates (lea, 1863) in Gölbaşı lake, Turkey. Aquaculture Research, 37(13), 1305-1315. doi:10.1111/j.1365-2109.2006.01563.x
  • Engel, H. (1990). Untersuchungen zur Autökologie von Unio crassus in Nord deutschland. Dissertation, Universität Hanhover. Thesis (doctoral)-Universität Hannover, 1990.
  • Ercan, E., Gaygusuz, Ö., Tarkan, A. S., Reichard, M., & Smith, C. (2013). The ecology of freshwater bivalves in the lake sapanca basin, Turkey. Turkish Journal of Zoology, 37(6): 730-738. doi:10.3906/zoo-1212-23
  • Ercan, E., & Tarkan, A.S. (2014). Effect of Salinity on the Growth and Survival of the Freshwater Mussel, Unio crassus, in an Environmentally Disturbed River. Pakistan Journal of Zoology, vol. 46(5): 1399-1406.
  • Geist, J. (2010). Strategies for the conservation of endangered freshwater pearl mussel (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia, 664: 69–88. doi: 10.1007/s10750-010-0190-2
  • Graf, D. L. (2013). Patterns of Freshwater Bivalve Global Diversity and the State of Phylogenetic Studies on the Unionoida, Sphaeriidae, and Cyrenidae. American Malacological Bulletin, 31: 135-153. doi: 10.4003/006.031.0106
  • Güler, M., & Lök, A. (2014). Embryonic development and intracapsular feeding in Hexaplex trunculus (Gastropoda: Muricidae). Marine Ecology, 35: 193 – 203. doi:10.1111/maec.12066
  • Heard, W. L. (1975). Sexuality and other aspects of reproduction in Anodonta (Pelecypoda: Unionidae). Malacologia, 15 (1):81–103.
  • Hendry, A., & Day T. (2003). Revisiting the positive correlation between female size and egg size. Evolutionary Ecology Research, 5: 421–429.
  • Henley, W. F., & Neves, R. J. (2001). Behavioral responses of glochidia of freshwater mussels (bivalvia: Unionidae) to chemical cues of fish. American Malacological Bulletin, 16(1-2), 131-135.
  • Hochwald, S. & Bauer, G. (1990). Untersuchungen zur Populations ökologie und Fortpflanzungs biologie der Bachmuschel Unio crassus (PHIL.) 1788. Schriftenreihe Bayerisches Landesamt für Umweltschutz Heft 97: 31–49; München.
  • Korniushin, A. V., & Glaubrecht, M. (2003). Novel reproductive modes in freshwater clams: brooding and larval morphology in Southeast Asian taxa of Corbicula (Mollusca, Bivalvia, Corbiculidae). Acta Zoologica, 84: 291–315. doi: 10.1046/j.1463-6395.2003.00150.x
  • Krug, P.J. (1998). Poecilogony in an estuarine opisthobranch: planktotrophy, lecithotrophy, and mixed clutches in a population of the ascoglossan Alderia modesta. Marine Biology, 132: 483-494. doi: 10.1007/s002270050414
  • Lamand, F., Roche, K., & Beisel, J. N. (2016). Glochidial infestation by the endangered mollusc Unio crassus in rivers of north-eastern France: Phoxinus phoxinus and Cottus gobio as primary fish hosts. Aquatic Conservation: Marine and Freshwater Ecosystems, 26: 445–455. doi: 10.1002/aqc.2603
  • Lopes-Lima, M. & Seddon, M.B. (2014). Unio terminalis. The IUCN Red List of Threatened Species 2014: e.T164866A42466771. doi: 10.2305/IUCN.UK.2014-1.RLTS.T164866A42466771.en
  • Lundberg, S. & Österling, M. (2016). Return of the Thick-shelled River Mussel – Restoring floodplains, habitats and connectivity by using mussels and brains. Handbook, UC4LIFE Project, Skåne County Administrative Board.
  • Lydeard, C., Cowie, R. H., Ponder, W. F., Bogan, A. E., Bouchet, P., Clark, S. A., Cummings, K.S., Frest, T.J., Gargominy, O., Herbert, D.G., Hershler, R., Perez, K.E., Roth, B., Seddon, M., Strong, E.E. &Thompson, F. G. (2004). The global decline of nonmarine mollusks. Bioscience, 54(4) :321-330. doi: 10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2
  • Ostrovsky, I., Gophen, M., & Kalikhman, I. (1993). Distribution, growth, production, and ecological significance of the clam Unio terminalis in Lake Kinneret, Israel. Hydrobiologia, 271: 49–63. doi: 10.1007/BF00005695
  • Pechenik, J.A. (1979). Role of encapsulation in invertebrate life histories. American Naturalist, 114:859–870
  • Reichard, M. Polačik, M., Tarkan, A.S., Spence, R., Gaygusuz, Ö., Ercan, E., Ondračková, M. & Smith, C. (2010). The bitterling-mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution, 64(10): 3047-3056. doi: 10.1111/j.1558-5646.2010.01032.x
  • Smith, C., & Fretwell, S. (1974). The optimal balance between size and number of offspring. American Naturalist, 108:499–506.
  • Soto, D. & Mena, G. (1999). Filter feeding by the freshwater mussel, Diplodon chilensis, as a biocontrol of salmon farming eutrophication. Aquaculture, 171: 65–81. doi: 10.1016/S0044-8486(98)00420-7
  • Strayer, D. L., Hunter, D. C., Smith, L. C., & Borg, C. K. (1994). Distribution, abundance, and roles of freshwater clams (Bivalvia, Unionidae) in the freshwater tidal Hudson River. Freshwater Biology, 31: 239–248. doi: 10.1111/j.1365-2427.1994.tb00858.x
  • Strayer, D.L., Downing, J.A., Haag, W.R., King, T.L., Layzer, J.B., Newton, T.J., & Nichols, S.J. (2004). Changing Perspectives on Pearly Mussels, North America's Most Imperiled Animals. BioScience, 54: 429–439. doi: 10.1641/0006-3568(2004)054[0429:CPOPMN]2.0.CO;2
  • Şereflişan, H., Menderes, S., & Soylu, S. (2009). Description of glochidia of three species of freshwater mussels (unionidae) from southeastern Turkey. Malacologia, 51 doi:10.4002/040.051.0112
  • Şereflişan, H. (2014). Investigation on Economical Characteristics of Freshwater Mussels in Gölbaşi Lake (Hatay). Yunus Araştırma Bülteni, 2014 (3), 43-49. doi: 10.17693/yunusae.v2014i21953.235714
  • Taeubert, J., Martinez, A. M. P., Gum, B., & Geist, J. (2012). The relationship between endangered thick-shelled river mussel (Unio crassus) and its host fishes. Biological Conservation, 155, 94-103. doi:10.1016/j.biocon.2012.06.005
  • Vaughn, C. C. (2012). Life history traits and abundance can predict local colonization and extinction rates of freshwater mussels. Freshwater Biology, 57: 982–992. doi: 10.1111/j.1365-2427.2012.02759.x
  • Vaughn, C. C., & Hakenkamp, C. C. (2001). The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology, 46: 1431–1446. doi: 10.1046/j.1365-2427.2001.00771.x
  • Wachtler, K., Dreher-Mansur, M. C. & Richter, T. (2001). Larval types and early postlarval biology in naiads (Unionoida). In Bauer, G. & K. Wachtler (eds), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin, Heidelberg: 93–125.
  • Watters, G. (2001). The Evolution of the Unionacea in North America, and Its Implications for the Worldwide Fauna - In: Bauer, G. and Wächtler K. (eds.), Ecology and Evolution of the Freshwater Mussels Unionoida. Springer-Verlag, Berlin, pp. 281–307.
  • Weber, E. (2005). Population size and structure of three mussel species (Bivalvia: Unionidae) in a northeastern German river with special regard to influences of environmental factors. Hydrobiologia, 537, 169–183. doi: 10.1007/s10750-004-2839-1
  • Welker, M., & Walz, N. (1998). Can mussels control the plankton in rivers? A planktological approach applying a Lagrangian sampling strategy. Limnology and Oceanography, 43: 753–762. doi: 10.4319/lo.1998.43.5.0753
  • Wood, E. M. (1974). Some mechanisms involved in host recognition and attachment of the glochidium larva of Anodonta cygnea (Mollusca: Bivalvia). Journal of Zoology, 173: 15–30. doi: 10.1111/j.1469-7998.1974.tb01744.x
  • Zettler, M. L., & Jueg, U. (2007). The situation of the freshwater mussel Unio crassus (Philipsson 1788) in north-east Germany and its monitoring in terms of the EC Habitats Directive. Mollusca, 25: 165–174.
  • Zimmerman, L., & Neves, R. J. (2002). Effects of temperature on duration of viability for glochidia of freshwater mussels (Bivalvia: Unionidae). American Malacological Bulletin, 17: 31–35.

Details

Subjects Science
Journal Section Articles
Authors

Mehmet GÜLER
ADNAN MENDERES UNIV
orcid.org/0000-0001-8257-1138
Türkiye


Deniz ÇOBAN
ADNAN MENDERES UNIV


Birsen KIRIM This is me
ADNAN MENDERES UNIV

Publication Date September 26, 2017
Application Date February 21, 2017
Acceptance Date June 8, 2017
Published in Issue Year 2017, Volume 34, Issue 3

Cite

APA Güler, M. , Çoban, D. & Kırım, B. (2017). Observations on the reproductive biology of Unio terminalis (Bivalvia: Unionidae) . Ege Journal of Fisheries and Aquatic Sciences , 34 (3) , 303-309 . DOI: 10.12714/egejfas.2017.34.3.09