Skip to main content
SpringerLink
Log in

Growth, reproductive traits and habitat patterns of Unio ravoisieri (Mollusca: Bivalvia) from Ichkeul Lake tributaries (Northern Tunisia)

  • Original Article
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Habitat patterns, growth and reproductive traits of the freshwater mussel Unio ravoisieri were investigated for the first time in two streams (Sejenane and Elmaleh) of the Ichkeul Lake basin (northern Tunisia) over the course of a year. A very similar profile was observed for the two studied populations. The median age class dominated in the age structure, indicating good recruitment and viability. The reproductive period lasted approximately 10 months (from September to June). Females at different gametogenesis stages were found during autumn, winter and spring. Gravid females were sampled during winter and spring, and larval release occurred from early spring to early summer. The number of embryos produced per female reached 84,000 per year. In Elmaleh stream, characterized by high salinity, reproduction of the mussel took place slightly earlier than in the other habitat (Sejenane). However, the variation in reproduction traits between the two populations was not significant (p > 0.05). Similar patterns, but with a difference in the timing of the breeding season, were recorded for Spanish populations. The results highlight a reproductive plasticity of U. ravoisieri and an ability to tolerate harsh abiotic conditions. Nevertheless, salinity and temperature seem to have a stressful effect on different reproductive stages, mainly during the brooding period; negative correlation was found between condition index and the two parameters: Pearson’s r = 0.4–0.8; p < 0.05. To avoid their adverse effects, U. ravoisieri appears to be able to adjust its reproductive cycle to the wet season when these parameters are moderate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aldridge D (1999) The morphology, growth and reproduction of Unionidae (Bivalvia) in a fenland waterway. J Molluscan Stud 65:47–60. https://doi.org/10.1093/mollus/65.1.47

    Article  Google Scholar 

  • Aldridge DW, McIvor AL (2003) Gill evacuation and release of glochidia by Unio pictorum and Unio tumidus (Bivalvia: Unionidae) under thermal and hypoxic stress. J Molluscan Stud 69:55–59. https://doi.org/10.1093/mollus/69.1.55

    Article  Google Scholar 

  • Amraoui I, Khalloufi N, Touaylia S (2018) Effects to perfluorooctane sulfonate (PFOS) on the mollusk Unio ravoisieri under laboratory exposure. Chem Ecol 38:324–339. https://doi.org/10.1080/02757540.2018.1433168

    Article  CAS  Google Scholar 

  • Anthony JL, Kesler DH, Downing WL, Downing JA (2001) Length-specific growth rates in freshwater mussels (Bivalvia: Unionidae): extreme longevity or generalized growth cessation? Freshw Biol 46:1349–1359. https://doi.org/10.1046/j.1365-2427.2001.00755.x

    Article  Google Scholar 

  • Araujo R, Reis J, Machordom A, Toledo C, Madeira MJ, Gomez I, Velasco JC, Morales J, Barea JM, Ondina P, Ayala I (2009) Las náyades de la peninsula Ibérica. Iberus 27(2):7–72 https://core.ac.uk/download/pdf/36055181.pdf

    Google Scholar 

  • Araujo R, Feo-Quer C, Pou-Rovira Q, Campos M (2015) Conservation of two endangered European freshwater mussels (Bivalvia: Unionidae): a three-year, semi-natural breeding experiment. Nautilus 129(3):126–135

    Google Scholar 

  • Bauer G (1987) Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J Anim Ecol 56:691–704. https://doi.org/10.2307/5077

    Article  Google Scholar 

  • Bauer G (1988) Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe. Biol Conserv 45:239–253. https://doi.org/10.1016/0006-3207(88)90056-0

    Article  Google Scholar 

  • Bauer G (1992) Variation in the life span and size of the freshwater pearl mussel. J Anim Ecol 61:425–436. https://doi.org/10.2307/5333

    Article  Google Scholar 

  • Bauer G (2001) Life-history variation on different taxonomic levels of naiads. In: Bauer G, Wächtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Ecological studies, vol 145. Springer, Heidelberg, pp 83–91. https://doi.org/10.1007/978-3-642-56869-5_5

    Chapter  Google Scholar 

  • Beasley CR, De Quadros Miranda L, STM A, Melo AG, Souza JO, Tagliaro CH (2005) Brood size and larval length of Paxyodon syrmatophorus (Bivalvia, Hyriidae) from the Tocantins River, Brazil. Amazoniana 18:173–184

    Google Scholar 

  • Blakeslee CJ, Galbraith HS, Robertson LS, John-White BS (2013) The effects of salinity exposure on multiple life stages of a common freshwater mussel, Elliptio complanata. Environ Toxicol Chem 32:2849–2854. https://doi.org/10.1002/etc.2381

    Article  CAS  PubMed  Google Scholar 

  • Christian AD, Davidson CL, Posey IIWR, Rust PJ, Farris JL, Harris JL, Harp GL (2000) Growth curves of four species of commercially valuable freshwater mussels (Bivalvia: Unionidae). J Ark Acad Sci 54:41–50

    Google Scholar 

  • Cope WG, Bringolf RB, Buchwalter DB, Newton TJ, Ingersoll C, Wang N, Augspurger T, Dwyer FJ, Barnhart MC, Neves RJ, Hammer E (2008) Differential exposure, duration, and sensitivity of Unionoidean bivalve life stages to environmental contaminants. J N Am Benthol Soc 27:451–462. https://doi.org/10.1899/07-094.1

    Article  Google Scholar 

  • Daget J (1998) Catalogue raisonné des Mollusques bivalves d'eau douce africains. Back-huys, Orstom, p 329. http://horizon.documentation.ird.fr/exl-doc/pleins_textes/divers14-12/010016420.pdf

  • Dame R, Bushek D, Allen D, Levitus A, Edward D, Koeppler E, Gregory L (2002) Ecosystem response to bivalve density reduction: management implications. Aquat Ecol 36:51–65 https://link.springer.com/article/10.1023/A:1013354807515

    Article  Google Scholar 

  • Ercan E, Tarkan AS (2014) Effect of salinity on the growth and survival of the freshwater mussel, Unio crassus, in an environmentally disturbed river. Pak J Zool 46(5):1399–1406

    Google Scholar 

  • Ercan E, Gaygusuz Ö, Tarkan AS, Reichard M, Smith C (2013) The ecology of freshwater bivalves in the Lake Sapanca basin, Turkey. Turk J Zool 37:730–738. https://doi.org/10.3906/zoo-1212-23

    Article  Google Scholar 

  • Evans JD (1996) Straightforward statistics for the behavioral sciences. Brooks/Cole (ed), Pacific Grove, p 600

    Google Scholar 

  • Fong PP, Kyozuka K, Duncan J, Rynkowski S, Mekasha D, Ram JL (1995) The effect of salinity and temperature on spawning and fertilization in the zebra mussel Dreissena polymorpha (Pallas) from North America. Biol Bull 189:320–329. https://doi.org/10.2307/1542149

    Article  CAS  PubMed  Google Scholar 

  • Gascho Landis AM, Mosley TL, Haag WR, Stoeckel JA (2012) Effects of temperature and photoperiod on lure display and glochidial release in a freshwater mussel. Freshwater Science 31:775–786 https://www.fs.usda.gov/treesearch/pubs/41726

    Article  Google Scholar 

  • Gillis PL (2011) Assessing the toxicity of sodium chloride to the glochidia of freshwater mussels: implications for salinization of surface waters. Environ Pollut 159:1702–2708. https://doi.org/10.1016/j.envpol.2011.02.032

    Article  CAS  PubMed  Google Scholar 

  • Graf DL (2007) Palearctic freshwater mussel (Mollusca: Bivalvia: Unionoida) diversity and the comparatory method as a species concept. Proc Acad Natl Sci Phila 156:71–88. https://doi.org/10.1635/0097-3157(2007)156[71:PFMMBU]2.0.CO;2

  • Graf DL, Ó Foighil D (2000) The evolution of brooding characters among the freshwater pearly mussels (Bivalvia: Unionoidea) of North America. J Molluscan Stud 66:157–170. https://doi.org/10.1093/mollus/66.2.157

    Article  Google Scholar 

  • Haag WR (2009) Extreme longevity in freshwater mussels revisited: sources of bias in age estimates derived from mark–recapture experiments. Freshw Biol 54:1474–1486. https://doi.org/10.1111/j.1365-2427.2009.02197.x

    Article  Google Scholar 

  • Haas F (1969) Superfamilia Unionacea. Das Tierreich, Berlin, p 663

    Google Scholar 

  • Hastie LC, Cosgrove PJ (2002) Intensive searching for mussels in a fast-flowing river: an estimation of sampling bias. J Conchol 37(4):309–316

    Google Scholar 

  • Hastie LC, Young MR (2003) Timing of spawning and glochidial release in Scottish freshwater pearl mussel (Margaritifera margaritifera) populations. Freshw Biol 48:2107–2117. https://doi.org/10.1046/j.1365-2427.2003.01153.x

    Article  Google Scholar 

  • Hastie LC, Tarr EC, al-Mousawi B, Young MR (2010) Medium-term recruitment patterns in Scottish freshwater pearl mussel Margaritifera margaritifera populations. Endanger Species Res 11:21–33. https://doi.org/10.3354/esr00262

    Article  Google Scholar 

  • Hinzmann M, Lopes-Lima M, Teixeira A, Varandas S, Sousa R, Lopes A, Froufe E, Machado J (2013) Reproductive cycle and strategy of Anodonta anatina (L., 1758): Notes on hermaphroditism. J Exp Zool 319(A):378–390 https://core.ac.uk/download/pdf/153410221.pdf

    Article  Google Scholar 

  • Hochwald S (2001) Plasticity of life-history traits in Unio crassus. In: Bauer G, Wächtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Ecological studies, vol 145. Springer, Heidelberg, pp 127–142. https://doi.org/10.1007/978-3-642-56869-5_7

    Chapter  Google Scholar 

  • Jirka KJ, Neves RJ (1992) Reproductive biology of four species of freshwater mussels (Mollusca: Unionidae) in the New River, Virginia and West Virginia. J Freshw Ecol 7(1):35–44. https://doi.org/10.1080/02705060.1992.9664668

    Article  Google Scholar 

  • Jones JW, Neves RJ, Ahlstedt SA, Hubbs D, Johnson M, Dan H, Ostby BJK (2010) Life history and demographics of the endangered birdwing pearly mussel (Lemiox rimosus) (Bivalvia: Unionidae). Am Midl Nat 163:335–350. https://doi.org/10.1674/0003-0031-163.2.335

    Article  Google Scholar 

  • Kang DH, Hyun CY, Limpanont Y, Choi KS (2007) Annual gametogenesis of the Chinese Anapella clam Coecella chinensis (Deshayes 1855) at an upper intertidal sandy beach on the east coast of Jeju, Korea. J Shellfish Res 26:433–441. https://doi.org/10.2983/0730-8000(2007)26[433:AGOTCA]2.0.CO;2

  • Karoui-Yaakoub N, Mtimet M, Béjaoui S, Amri L, Khalloufi N, Ben Aissa L, Martínez-Navarro B (2016) Middle to Late Pleistocene malacofauna from the archeopaleontological site of Oued Sarrat (Tajerouine area, NW Tunisia). Arab J Geosci 9:345. https://doi.org/10.1007/s12517-016-2310-4

    Article  CAS  Google Scholar 

  • Khalloufi N, Boumaiza M (2005) Première note sur la présence d’Anodonta cygnea (Linnaeus, 1758) (Mollusca, Bivalva, Unionidae) en Tunisie. Zool Baetica 16:21–29

    Google Scholar 

  • Khalloufi N, Boumaiza M (2009) First record and biology of Unio gibbus Spengler, 1793 in Tunisia. Biologia 64(6):1178–1183. https://doi.org/10.2478/s11756-009-0196-2

    Article  Google Scholar 

  • Khalloufi N, Toledo C, Machordom A, Boumaïza M, Araujo R (2011) The unionids of Tunisia: taxonomy and phylogenetic relationships, with redescription of Unio ravoisiseri Deshayes, 1847 and U. durieui Deshayes, 1847. J Molluscan Stud 77:1–13 http://www.fauna-iberica.mncn.csic.es/CV/rafa_PDF_2/JMS_Tunez.pdf

    Article  Google Scholar 

  • Labelle M, Hampton J, Bailey K, Murray T, Fournier DA, Sibert JR (1993) Determination of age and growth of South Pacific albacore (Thunnus alalunga) using three methodologies. Fish Bull 91(4):649–663

    Google Scholar 

  • Laruelle F, Molloy DP, Fokin S, Ovcharenko M (1999) Histological analysis of mantle-cavity ciliates in Dreissena polymorpha: their location, symbiotic relationship, and distinguishing morphological characteristics. J Shellfish Res 18(1):251–257

    Google Scholar 

  • Lima P, Monteiro SM, Sousa M, Machado J (2012) A histological study of oogenesis in the freshwater mussel Anodonta cygnea (Linnaeus, 1758) in Mira lagoon, Portugal. Malacologia 55(2):251–261. https://doi.org/10.4002/040.055.0206

    Article  Google Scholar 

  • Lopes-Lima M, Teixeira A, Froufe E, Lopes A, Varandas S, Sousa R (2014) Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia 735:1–13 https://link.springer.com/article/10.1007/s10750-014-1902-9

    Article  Google Scholar 

  • Lydeard CRH, Cowie W, Ponder F, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of non-marine mollusks. Bioscience 54:321–330. https://doi.org/10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2

  • Maaß S (1987) Untersuchungen zur Fortpflanzungsbiologie einheimischer Süßwassernuscheln der Gattung Unio. Dissertation, Tierärztliche Hochschule Hannover, Germany Zoologisches Institut

  • Mandahl-Barth G (1988) Studies on African freshwater bivalves. Danish bilharziasis laboratory, Charlottenlund

    Google Scholar 

  • Mcivor AL, Aldridge DC (2007) The reproductive biology of the depressed river mussel, Pseudanodonta complanata (Bivalvia: Unionidae), with implications for its conservation. J Molluscan Stud 73:259–266. https://doi.org/10.1093/mollus/eym023

    Article  Google Scholar 

  • Nagel KO, Castagnolo L, Cencetti L, Moro GA (2007) Notes on reproduction, growth and habitat of Microcondylaea bonellii (Mollusca: Bivalvia: Unionidae) in the Torrente versa (Italy). Mollusca 25(1):41–49 https://www.researchgate.net/publication/203413492

    Google Scholar 

  • Nagel KO, Dumpelmann C, Pfeiffer M (2015) Effective growth cessation in adult Unio crassus philipsson, 1788 (bivalvia: unionidae) from Germany. Folia Malacologica 23(4):309–313. https://doi.org/10.12657/folmal.023.027

    Article  Google Scholar 

  • National Meteorological Institute (NMI) (2011) Monthly climatic tables. INM archive for the period of 2009-2010, Sejenane Station

  • Neves RJ, Bogan AE, Williams JD, Ahlstedt SA, Hartfield PW (1998) Status of aquatic mollusks in the Southeastern United States: A downward spiral of diversity. In: Benz GW, Collins DE (eds) Aquatic fauna in Peril: the Southeastern perspective 3rd edn. Special publication 1. Southeast Aquatic Research Institute, Lenz Design and Communications, Decatur, pp 43–86 https://www.researchgate.net/publication/258304352

    Google Scholar 

  • 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. https://doi.org/10.1007/BF00005695

    Article  Google Scholar 

  • Pandolfo TJ (2008) Beating the heat: upper thermal tolerances of the early life stages of eight species of freshwater mussel (Unionidae). J N Am Benthol Soc 29(3):959–969. https://doi.org/10.1899/09-128.1

    Article  Google Scholar 

  • Piechocki A (1999) Reproductive biology of Unio pictorum (Linnaeus) and U. tumidus Philipsson in the Pilica River (Central Poland). Heldia 4(6):53–60

    Google Scholar 

  • Pou-Rovira Q, Campos M, Feo-Quer C, Camós I, Martí J, Angelats I, Cros C, Casadevall R, Dalmau G, Cruset E, Canal A, Hernández M, Rodríguez M, Puigvert T, Bassols E (2015) Age, growth and demography of several populations of Unio mancus and U. ravoisieri in northeast of Catalonia. (Poster) 2nd International Seminar Rearing of Unionoid mussels, Luxembourg 24–27 November 2015. http://www.heppi.com/seminar/Uc_Lux_2015_QPR.pdf

  • Ravera O, Frediani A, Riccardi N (2007) Seasonal variations in population dynamics and biomass of two Unio pictorum mancus (Mollusca, Unionidae) populations from two lakes of different trophic state. J Limnol 66(1):15–27. https://doi.org/10.4081/jlimnol.2007.15

    Article  Google Scholar 

  • Sansom BJ, Atkinson CL, Vaughn CC (2016) Growth and longevity estimates for mussel populations in three Ouachita mountain rivers. Freshwater Mollusk Biology and Conservation 19:19–26. https://doi.org/10.31931/fmbc.v19i2.2016.19-26

  • Southward GM, Chapman DG (1965) Utilization of Pacific halibut stocks: study of Bertalanffy’s growth equation. International Pacific Halibut Commission Report 39:1–33. http://docs.streamnetlibrary.org/IPHC/Report0039.pdf

  • Van Damme D (1984) The freshwater Mollusca of northern Africa: distribution, biogeography and Palaeoecology. Developments in Hydobiology 25, Junk W (ed). Dordrecht, p 164

  • Walford LA (1946) A new graphic method of describing the growth of animals. Biol Bull 90:141–147 https://www.jstor.org/stable/1538217

    Article  CAS  PubMed  Google Scholar 

  • Young MR, Williams JC (1984) The reproductive biology of the freshwater pearl mussel Margaritifera margaritifera (Linn.) in Scotland. I. Field studies. Arch Hydrobiol 99:405–422

    Google Scholar 

  • Zimmerman LL, Neves RJ (2002) Effect of temperature on duration of viability for glochidia of freshwater mussels (Bivalvia: Unionodaae). Am Malacol Bull 17(1/2):31–35

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to Manuel Lopes-Lima, Coordinator of the Red List Authority on Freshwater Bivalves Mollusk Specialist Group (IUCN/SSC), from the University of Porto (Portugal) for the scientific review of this paper, the English version, his valuable comments and advice. Thanks are also due to Dr. Rafael Araujo (Museum of Natural Sciences of Madrid) for his comments and data on the Unio ravoisieri populations from Spain. Thanks to Pr. David Reid for his helpful comments and for the English review.

Author information

Authors and Affiliations

  1. Faculty of Sciences of Bizerte, LR01ES14, Laboratory of Environment Biomonitoring, University of Carthage, 7021 Jarzouna, Bizerte, Tunisia

    Noureddine Khalloufi, Chrifa Aissaoui & Mustapha Béjaoui

Authors
  1. Noureddine Khalloufi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chrifa Aissaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mustapha Béjaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Noureddine Khalloufi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(PDF 445 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khalloufi, N., Aissaoui, C. & Béjaoui, M. Growth, reproductive traits and habitat patterns of Unio ravoisieri (Mollusca: Bivalvia) from Ichkeul Lake tributaries (Northern Tunisia). Biologia 74, 821–834 (2019). https://doi.org/10.2478/s11756-019-00213-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-019-00213-2

Keywords

Search

Navigation