期刊论文详细信息
BMC Developmental Biology
Mantle margin morphogenesis in Nodipecten nodosus (Mollusca: Bivalvia): new insights into the development and the roles of bivalve pallial folds
Sônia G. B. C. Lopes2  Andreas Wanninger1  José Eduardo A. R. Marian2  Jorge A. Audino2 
[1]Department of Integrative Zoology, University of Vienna, UZA1 Althanstraße 14, Vienna, 1090, Austria
[2]Department of Zoology, University of São Paulo, Rua do Matão, Travessa 14, n. 101, São Paulo, 05508-090, SP, Brazil
关键词: Periostracal groove;    Pectinidae;    Ontogeny;    Larvae;    Integrative microscopy;   
Others  :  1209035
DOI  :  10.1186/s12861-015-0074-9
 received in 2015-01-12, accepted in 2015-05-20,  发布年份 2015
PDF
【 摘 要 】

Background

Despite extensive knowledge on bivalve anatomy and development, the formation and differentiation of the mantle margin and its associated organs remain largely unclear. Bivalves from the family Pectinidae (scallops) are particularly promising to cast some light on these issues, because they exhibit a complex mantle margin and their developmental stages are easily obtained from scallop farms. We investigated the mantle margin of the scallop Nodipecten nodosus (L. 1758) during larval and postmetamorphic development.

Methods

A thorough analysis of the mantle margin development in Nodipecten nodosus, from veliger larvae to mature adults, was conducted by means of integrative microscopy techniques, i.e., light, electron, and confocal microscopy.

Results

Initially unfolded, the pallial margin is divided into distal and proximal regions by the periostracum-forming zone. The emergence of the pallial musculature and its neural innervation are crucial steps during bivalve larval development. By the late pediveliger stage, the margin becomes folded, resulting in a bilobed condition (i.e., outer and inner folds), a periostracal groove, and the development of different types of cilia. After metamorphosis, a second outgrowth process is responsible for emergence of the middle mantle fold from the outer surface of the inner fold. Once the three-folded condition is established, the general adult features are rapidly formed.

Conclusions

Our data show that the middle mantle fold forms from the outer surface of the inner fold after metamorphosis and that the initial unfolded mantle margin may represent a common condition among bivalves. The first outgrowth process, which gives rise to the outer and inner folds, and the emergence of the pallial musculature and innervation occur during larval stages, highlighting the importance of the larval period for mantle margin morphogenesis in Bivalvia.

【 授权许可】

   
2015 Audino et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150602015425111.pdf 6309KB PDF download
Fig. 17. 45KB Image download
Fig. 16. 128KB Image download
Fig. 15. 190KB Image download
Figure 6. 59KB Image download
Fig. 13. 127KB Image download
Fig. 12. 215KB Image download
Fig. 11. 23KB Image download
Fig. 10. 80KB Image download
Fig. 9. 110KB Image download
20150309024323776.pdf 592KB PDF download
Fig. 7. 185KB Image download
Fig. 6. 131KB Image download
Fig. 5. 96KB Image download
Fig. 4. 123KB Image download
Fig. 3. 90KB Image download
Fig. 2. 17KB Image download
Fig. 1. 141KB Image download
【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

Fig. 9.

Fig. 10.

Fig. 11.

Fig. 12.

Fig. 13.

Figure 6.

Fig. 15.

Fig. 16.

Fig. 17.

【 参考文献 】
  • [1]Carter JG, Harries PJ, Malchus N, Sartori AF, Anderson LC, Bieler R et al.. Illustrated Glossry of the Bivalvia. Treatise Online. 2012; 48:1-209.
  • [2]Stasek CR, Mcwilliams WR. The comparative morphology and evolution of the Molluscan Mande Edge. Veliger. 1973; 16:1-19.
  • [3]Steiner G. Observations on the anatomy of the scaphopod mantle, and the description of a new family, the Fustiariidae. Am Malacol Bull. 1991; 9:1-20.
  • [4]Lemche H, Wingstrand K. The anatomy of Neopilina galatheae, 1957 (Molllusca, Tryblidiacea). Galathea Rep. 1959; 3:9-71.
  • [5]Westermann B, Schmidtberg H, Beuerlein K. Functional morphology of the mantle of Nautilus pompilius (Mollusca, Cephalopoda). J Morphol. 2005; 264(March):277-85.
  • [6]Yonge CM. Mantle fusion in the Lamellibranchia. Pubbl Stn Zool di Napoli. 1957; 29:151-71.
  • [7]Yonge CM. Symmetries and the role of the mantle margins in the Bivalve Mollusca. Natl Widl. 1983; 16:1-10.
  • [8]Taylor JD. The structural evolution of the bivalve shell. Paleontology. 1973; 16:519-34.
  • [9]Wilbur K, Saleuddin A. Shell formation. In: The Mollusca, v. 4. Wilbur KM, editor. Academic, New York; 1983: p.235-87.
  • [10]Ansell AD. The functional morphology of the British species of Veneracea (Eulamellibranchis). J Mar Biol Assoc United Kingdom. 1961; 41:489-515.
  • [11]Hillman RE, Shuster CNJ. A comment on the origin of the fourth fold in the Mantle of the Quahog, Mercenaria mercenaria. Chesap Sci. 1966; 7:112-3.
  • [12]Sartori AF, Mikkelsen PM: Siphonal Structure in the Veneridae (Bivalvia : Heterodonta) with an assessment of its phylogenetic application and a review of venerids of the gulf of Thailand. Raffles Bull Zool. 2008:103–25.
  • [13]Passos FD, Domaneschi O. Biologia e anatomia funcional de Donax gemmula Morrison 674 (Bivalvia, Donacidae) do litoral de São Paulo, Brasil. Rev Bras Zool. 2004; 21:1017-32.
  • [14]Waller TR. Scanning electron microscopy of shell and mantle in the order Arcoida (Mollusca: Bivalvia). Smithson Contrib Zool. 1980:1–58.
  • [15]Morton B, Peharda M. The biology and functional morphology of Arca noae (Bivalvia: Arcidae) from the Adriatic Sea, Croatia, with a discussion on the evolution of the bivalve mantle margin. Acta Zool. 2008; 89(January):19-28.
  • [16]Yonge CM. Formation of Siphons in Lamellibranchia. Nature. 1948; 161:198-9.
  • [17]Yonge CM. Mantle margins with a revision of siphonal types in the Bivalvia. J Molluscan Stud. 1982; 48:102-3.
  • [18]Beedham GE, Owen G. The mantle and shell of Solemya parkinsoni (Protobranchia: Bivalvia). Proc Zool Soc London. 1965; 145:405-30.
  • [19]Morton B, Scott PJB. Morphological and functional specializations of the shell, musculature and pallial glands in the Lithophaginae (Mollusca: Bivalvia). J Zool. 1980; 192:179-203.
  • [20]Morton B. The mantle margin and radial mantle glands of Entodesma saxicola and E. inflata (Bivalvia: Anomalodesmata: Lyonsiidae). J Molluscan Stud. 1987; 53:139-51.
  • [21]Gilmour T. The defensive adaptations of Lima hians (Mollusca, Bivalvia). J Mar Biol Assoc United Kingdom. 1967; 47:209-21.
  • [22]Morton B. Dymantic display in Galeomma polita Deshayes (Bivalvia: Leptonacea). J Conchol. 1973; 28:365-9.
  • [23]Moir AJ. Ultrastructural studies on the ciliated receptors of the long tentacles of the giant scallop, Placopecten magellanicus (gmelin). Cell Tissue Res. 1977; 184:367-80.
  • [24]Morton B. The evolution of eyes in the Bivalvia: New Insights*. Am Malacol Bull. 2008; 26(July 2007):35-45.
  • [25]Serb JM, Eernisse DJ. Charting evolution’s trajectory: using molluscan eye diversity to understand parallel and convergent evolution. Evol Educ Outreach. 2008; 1:439-47.
  • [26]Cragg SM. Chapter 2 development, physiology, behaviour and ecology of scallop larvae. Dev Aquac Fish Sci. 2006; 35:45-122.
  • [27]Wanninger A, Koop D, Moshel-Lynch S, Degnan BM. Molluscan evolutionary development. In: Phylogeny and evolution of the Mollusca. Ponder W, Lindberg D, editors. University of California Press, California; 2008: p.427-46.
  • [28]Cole H a. The fate of the larval organs in the metamorphosis of Ostrea edulis. J Mar Biol Assoc United Kingdom. 1938; 22:469-84.
  • [29]Ansell AD. The functional morphology of the larva, and the post-larval development of Venus striatula (da Costa). J Mar Biol Assoc United Kingdom. 1962; 42:419-43.
  • [30]Hodgson C, Burke RD. Development and larval morphology of the spiny scallop, Chlamys hastata. Biol Bull (Woods Hole, MA). 1988; 174:303-18.
  • [31]Mouëza M, Gros O, Frenkiel L. Embryonic, larval and post larval development of the tropical clam, Anomalo Cardiabrasiliana (Bivalvia, Veneridae). J Nolluscan Stud. 1999:73–88.
  • [32]Carriker M. Embryogenesis and organogenesis of veligers and early juveniles. In: Biology of the hard clam. Kraeuter J, Castagna M, editors. Elsevier Ltd, Amsterdam; 2001: p.77-116.
  • [33]Weiss IM, Tuross N, Addadi L, Weiner S. Mollusc larval shell formation: Amorphous calcium carbonate is a precursor phase for aragonite. J Exp Zool. 2002; 293(May):478-91.
  • [34]Cannuel R, Beninger PG, McCombie H, Boudry P. Gill Development and its functional and evolutionary implications in the blue mussel Mytilus edulis (Bivalvia: Mytilidae). Biol Bull. 2009; 217(October):173-88.
  • [35]Cranfield HJ. Observations on the morphology of the mantle folds of the pediveliger of Ostrea edulis L. and their function during settlement. Marine Biological Association of the United Kingdom, Journal 54(1):1–12, 2 pls. J Mar Biol Assoc United Kingdom. 1974; 54:1-12.
  • [36]Raven C. Morphogenesis: the analysis of molluscan development. Pergamon Press, New York; 1958.
  • [37]Waller TR. Functional morphology and development of Veliger Larvae of the European Oyster, Ostrea edulis Linne. Smithson Contrib Zool. 1981; 328:1-80.
  • [38]Moor B. Organogenesis. In: The Mollusca, v. 3. Wilbur K, editor. Academic, New York; 1983: p.123-77.
  • [39]Carriker M. Functional significance of the pediveliger in bivalve development. In: The Bivalvia: Proceedings of a Memorial Symposium in honour of Sir Charles Maurice Yonge (1899–1986) at the 9th International Malacological Congress, 1986, Edinburgh, Scotland, UK. Morton B, editor. Hong Kong University Press, Hong Kong; 1990: p.267-82.
  • [40]Cragg SM. The phylogenetic significance of some anatomical features of bivalve veliger larvae. In: Origin and evolutionary radiation of the Mollusca. Taylor JD, editor. Oxford University Press, Oxford; 1996: p.371-80.
  • [41]Alejandrino A, Puslednik L, Serb JM. Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae). BMC Evol Biol. 2011; 11:164. BioMed Central Full Text
  • [42]Beninger PG, Pennec M Le. Structure and Function in Scallops. In: Shumway SE, Parsons GJ, editors. Scallops: biology, ecology and aquaculture. Amsterdam: Elsevier B.V.; 2006. p. 123–227.
  • [43]Waller TR. New Phylogenies of the Pectinidae (MoUusca : Bivalvia): reconciling morphological and molecular approaches. Scallops: biology, ecology and aquaculture. 2008.1991-1.
  • [44]Wilkens LA. Neurobiology and behavior of the scallop. In: Shumway SE, Parsons GJ, editors. Scallops: biology, ecology and aquaculture. Elsevier B.V.; 2006. p. 317–56.
  • [45]Dakin WJ. The Eye of Pecten. Q J Microsc Sci. 1910; 55:49-112.
  • [46]Land MF. Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J Physiol. 1965; 179:138-53.
  • [47]Morton B. The function of pallial eyes within the Pectinidae, with a description of those present in Patinopecten yessoensis. Geol Soc London Spec Publ. 2001; 177:247-55.
  • [48]Malkowsky Y, Jochum A. Three-dimensional reconstructions of pallial eyes in Pectinidae (Mollusca: Bivalvia). Acta Zool. 1871; 2014:1-7.
  • [49]Audino JA, Marian JEAR, Wanninger A, Lopes SGBC: Development of the pallial eye in Nodipecten nodosus (Mollusca : Bivalvia): insights into early visual performance in scallops. Zoomorphology. 2015. doi:10.1007/s00435-015-0265-8.
  • [50]Buddenbrock W. Untersuchungen über die Schwimmbewegungen und die Statocysten der Gattung Pecten. Sitz Heidelb Akad Wiss. 1911; 28:1-24.
  • [51]Yonge CM. The evolution of the swimming habit in the Lamellibranchia. Mem Mus R Hist Nato Belg. 1936; 3:77-100.
  • [52]Moore JD, Trueman’ ER. Swimming of the Scallop, Chlamys Opercularzs (L.). J Exp Mar Biol Ecol. 1971; 6:179-85.
  • [53]Elston R. Functional anatomy, histology and ultrastructure of the soft tissues of the larval American oyster, Crassostrea virginica. Proc Natl Shellfish Assoc. 1980; 70:65-93.
  • [54]Creek GA. The development of the lamellibranch Cardium edule L. Proc Zool Soc London. 1960; 135:243-60.
  • [55]Drew GA. The life history of Nucula delphinodonta (Mighels). Q J Microsc Sci. 1901; 44:313-91.
  • [56]Altnöder A, Haszprunar G. Larval morphology of the brooding clam Lasaea adansonii (Gmelin, 1791) (Bivalvia, Heterodonta, Galeommatoidea). J Morphol. 2008; 269(April):762-74.
  • [57]Bellolio G, Lohrmman K, Dupré E. Larval morphology of the scallop Argopecten purpuratus as revealed by scanning electron microscopy. Veliger. 1993; 36:322-42.
  • [58]Silberfeld T, Gros O. Embryonic development of the tropical bivalve Tivela mactroides (Born, 1778) (Veneridae: Subfamily Meretricinae): A SEM study. Cah Biol Mar. 2006; 47(October 2005):243-51.
  • [59]Smith KK. Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc. 2001; 73:169-86.
  • [60]Mcnamara KJ. Heterochrony: the evolution of development. Evol Educ Outreach. 2012; 5:203-18.
  • [61]Yonge CM. On the primitive significance of the byssus in the Bivalvia and its effects in evolution. J Mar Biol Assoc United Kingdom. 1962; 42:113-25.
  • [62]Stanley SM. Functional morphology and evolution of byssally attached bivalve mollusks. J Paleontol. 1972; 46:165-212.
  • [63]Morton B. Functional morphology of Bathyarca pectunculoides (Bivalvia: Arcacea) from a deep Norwegian fjord with a discussion of the mantle margin in the Arcoida. Sarsia. 1982; 67:269-82.
  • [64]Sastry AN. The development and external post-larval stages of the bay scallop, aequipecten irradians concentricus say, reared in the laboratory. Bull Mar Sci. 1965; 15:417-35.
  • [65]Bayne BL. Some morphological changes that occur at the metamorphosis of the larvae of Mytilus edulis. In: Fourth European Marine Biology Symposium. Crisp DJ, editor. Cambridge University Press, Cambridge; 1971: p.259-80.
  • [66]Allen JA. On the functional morphology of Pinna and Atrina larvae (Bivalvia: Pinnidae) from the Atlantic. J Mar Biol Assoc United Kingdom. 2010; 91:1-7.
  • [67]Allen JA. The development of Pandora inaequivalvis (Linne). J Embryol Exp Morphol. 1961; 9(June):252-68.
  • [68]Croll RP, Jackson DL, Voronezhskaya EE. Catecholamine-containing cells in larval and postlarval bivalve molluscs. Biol Bull. 1997; 193(January):116-24.
  • [69]Kellogg JL. A contribution to our knowledge of the morphology of Lamellibranchiate Mollusks. GPO, Washington; 1892.
  • [70]Vitonis JEVV, Zaniratto CP, Machado FM, Passos FD. Comparative studies on the histology and ultrastructure of the siphons of two species of Tellinidae (Mollusca: Bivalvia) from Brazil. Zool. 2012; 29:219-26.
  • [71]Drew GA. The habits, anatomy and embryology of the giant scallop (Pecten Tenuicostatus Mighels). University of Maine Studies, Maine; 1906.
  • [72]Nelson TC. The feeding mechanism of the oyster. I. On the pallium and the branchial chambers of Ostrea virginica, O. edulis and O. angulata, with comparisons with other species of the genus. J Morphol. 1938; 63:1-61.
  • [73]Dakin WJ. The Anatomy and Phylogeny of Spondylus, with a Particular Reference to the Lamellibranch Nervous System. Proc R Soc London Ser B. 1928; 103:337-54.
  • [74]Ciocco NF. Anatomia de la “vieira tehuelche”, Aequipecten tehuelchus (d’Orbigny, 1846) (=Chlamys tehuelcha). IV. Sistema nervoso y estructuras sensoriales (Bivalvia, Pectinidae). Rev Biol Mar y Oceonografía. 1998; 33:25-42.
  • [75]Speiser DI, Johnsen S. Comparative Morphology of the Concave Mirror Eyes of Scallops (Pectinoidea)*. Am Malacol Bull. 2008; 26(July 2007):27-33.
  • [76]Pairett AN, Serb JM. De Novo Assembly and Characterization of Two Transcriptomes Reveal Multiple Light-Mediated Functions in the Scallop Eye (Bivalvia: Pectinidae). PLoS One. 2013;8.
  • [77]Serb JM, Porath-Krause AJ, Pairett AN. Uncovering a gene duplication of the photoreceptive protein, opsin, in scallops (bivalvia: Pectinidae). Integr Comp Biol. 2013; 53:68-77.
  • [78]Dyachuk V, Odintsova N. Development of the larval muscle system in the mussel Mytilus trossulus (Mollusca, Bivalvia): Original Article. Dev Growth Differ. 2009; 51:69-79.
  • [79]Dyachuk V, Wanninger A, Voronezhskaya EE. Innervation of bivalve larval catch muscles by serotonergic and FMRFamidergic neurons. Acta Biol Hung. 2012; 63:221-9.
  • [80]Spagnolia T, Wilkens LA. Neurobiology of the scallop. II. Structure of the parietovisceral ganglion lateral lobes in relation to afferent projections from the mantle eyes. Mar Behav Physiol. 1983; 10:23-55.
  • [81]Drew GA. The Circulatory and Nervous Systems of the Giant Scallop (Pecten Tenuicostatus, Mighels), with Remarks on the Possible Ancestry of the Lamellibranchiata, and on a Method for Making Series of Anatomical Drawings. Biol Bull. 1907; 12:225-58.
  • [82]Gosselin RE. The cilioexcitatory activity of serotonin. J Cell Physiol. 1961; 58:17-25.
  • [83]Beiras R, Widdows J. Effect of the neurotransmitters dopamine, serotonin and norepinephrine on the ciliary activity of mussel (Mytilus edulis) larvae. Mar Biol. 1995; 122:597-603.
  • [84]Kuang S, Goldberg JI. Laser ablation reveals regulation of ciliary activity by serotonergic neurons in molluscan embryos. J Neurobiol. 2001; 47:1-15.
  • [85]Wada K. Studies on the mineralization of the calcified tissue in molluscs. VII. Histological and histochemical studies of organic matrices in shells. Bull Natl Pearl Res Lab. 1964; 9:1078-86.
  • [86]Timmermans LPM. Studies on shell formation in molluscs. Neth J Zool. 1969; 19:417-523.
  • [87]Furuhashi T, Schwarzinger C, Miksik I, Smrz M, Beran A. Molluscan shell evolution with review of shell calcification hypothesis. Comp Biochem Physiol B Biochem Mol Biol. 2009; 154:351-71.
  • [88]Addadi L, Joester D, Nudelman F, Weiner S. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem Euro J. 2006; 12:980-7.
  • [89]Weiss IM, Schönitzer V. The distribution of chitin in larval shells of the bivalve mollusk Mytilus galloprovincialis. J Struct Biol. 2006; 153:264-77.
  • [90]Bubel A. An electron-microscope investigation of the cells lining the outer surface of the mantle in some marine molluscs. Mar Biol. 1973; 21:245-55.
  • [91]Lee JS, Joo JY, Park JJ. Histology and Ultrastructure of the Mantle Epidermis of the Equilateral Venus, Gomphina Veneriformis (Bivalvia: Veneridae). J Shellfish Res. 2007; 26:413-21.
  • [92]Beedham GE. Observations on the mantle of the Lamellibranchia. Q J Microsc Sci. 1958; 99(June):181-97.
  • [93]Fang Z, Feng Q, Chi Y, Xie L, Zhang R. Investigation of cell proliferation and differentiation in the mantle of Pinctada fucata (Bivalve, Mollusca). Mar Biol. 2008; 153:745-54.
  • [94]Richardson CA, Runham NW, Crisp DJ. A histological and ultrastructural study of the cells of the mantle edge of a marine bivalve, Cerastoderma edule. Tissue Cell. 1981; 13:715-30.
  • [95]Jabbour-Zahab R, Chagot D. Mantle histology, histochemistry and ultrastructure of the pearl oyster Pinctada margaritifera (L.). Aquat Living Resour. 1992; 5:287-98.
  • [96]Beninger PG, Veniot A, Poussart Y. Principles of pseudofeces rejection on the bivalve mantle: integration in particle processing. Mar Ecol Prog Ser. 1999; 178:259-69.
  • [97]Beninger PG, Lynn JW, Dietz TH, Silverman H. Mucociliary transport in living tissue : the two-layer in the Mussel Mytilus edulis L. Biol Bull. 1997; 193:4-7.
  • [98]Beninger PG, St-Jean SD. The role of mucus in particle processing by suspension-feeding marine bivalves: Unifying principles. Mar Biol. 1997; 129:389-97.
  • [99]Marian JEAR. Spermatophoric reaction reappraised: Novel insights into the functioning of the loliginid spermatophore based on Doryteuthis plei (Mollusca: Cephalopoda). J Morphol. 2012; 273:248-78.
  文献评价指标  
  下载次数:118次 浏览次数:16次