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Cell and Tissue Research

, Volume 377, Issue 3, pp 475–503 | Cite as

Structure and function of the digestive system in molluscs

  • Alexandre Lobo-da-CunhaEmail author
Review
  • 105 Downloads

Abstract

The phylum Mollusca is one of the largest and more diversified among metazoan phyla, comprising many thousand species living in ocean, freshwater and terrestrial ecosystems. Mollusc-feeding biology is highly diverse, including omnivorous grazers, herbivores, carnivorous scavengers and predators, and even some parasitic species. Consequently, their digestive system presents many adaptive variations. The digestive tract starting in the mouth consists of the buccal cavity, oesophagus, stomach and intestine ending in the anus. Several types of glands are associated, namely, oral and salivary glands, oesophageal glands, digestive gland and, in some cases, anal glands. The digestive gland is the largest and more important for digestion and nutrient absorption. The digestive system of each of the eight extant molluscan classes is reviewed, highlighting the most recent data available on histological, ultrastructural and functional aspects of tissues and cells involved in nutrient absorption, intracellular and extracellular digestion, with emphasis on glandular tissues.

Keywords

Digestive tract Digestive gland Salivary glands Mollusca Ultrastructure 

Notes

Compliance with ethical statements

Conflict of interest

The author declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by the author.

References

  1. Aktipis SW, Giribet G, Lindberg DR, Ponder WF (2008) Gastropoda: an overview and analysis. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the Mollusca. University of California Press, Berkeley, pp 201–237Google Scholar
  2. Aldred RG, Nixon M, Young JZ (1983) Cirrothauma murrayi Chun, a finned octopod. Phil Trans Roy Soc Lond 301:1–54Google Scholar
  3. Alexander CG, Rae JC (1974) The structure and formation of the crystalline style of Telescopium telescopium (Linnaeus) (Gastropoda:Prsobranchia). Veliger 17:56–60Google Scholar
  4. Andrews EB (1991) The fine structure and function of the salivary glands of Nucella lapillus (Gastropoda: Muricidae). J Molluscan Stud 57:111–126Google Scholar
  5. Andrews EB (1992) The fine structure and function of the anal gland of the muricid Nucella lapillus (Neogastropoda) (and a comparison with that of the trochid Gibbula cineraria). J Molluscan Stud 58:297–313Google Scholar
  6. Andrews EB, Thorogood KE (2005) An ultrastructural study of the gland of Leiblein of muricid and nassariid neogastropods in relation to function, with a discussion on its homologies in other caenogastropods. J Molluscan Stud 71:269–300Google Scholar
  7. Andrews EB, Elphick MR, Thorndyke MC (1991) Pharmacologically active constituents of the accessory salivary and hypobranchial glands of Nucella lapillus. J Molluscan Stud 57:136–138Google Scholar
  8. Andrews EB, Page AM, Taylor JD (1999) The fine structure and function of the anterior foregut glands of Cymatium intermedius (Cassoidea: Ranellidae). J Molluscan Stud 65:1–19Google Scholar
  9. Ball A, Taylor J, Andrews EB (1997) Development of the acinous and accessory salivary glands in Nucella lapillus (Neogastropoda: Muricoidea). J Molluscan Stud 63:245–260Google Scholar
  10. Barber AH, Lu D, Pugno NM (2015) Extreme strength observed in limpet teeth. J R Soc Interface 12:20141326Google Scholar
  11. Beninger PG, Le Pennec M (1993) Histochemistry of the bucco-oesophageal glands of Mytilus edulis: the importance of mucus in ingestion. J Mar Biol Ass UK 73:237–240Google Scholar
  12. Beninger PG, Le Pennec M, Donval A (1991) Mode of particle ingestion in five species of suspension-feeding bivalve molluscs. Mar Biol 108:255–261Google Scholar
  13. Beninger PG, St-Jean SD, Poussart Y (1995) Labial palps of the blue mussel Mytilus edulis (Bivalvia: Mytilidae). Mar Biol 123:293–303Google Scholar
  14. Beninger PG, Le Pennec G, Le Pennec M (2003) Demonstration of nutrient pathway from the digestive system to oocytes in the gonad intestinal loop of the scallop Pecten maximus L. Biol Bull 205:83–92Google Scholar
  15. Bergmeier FS, Brandt A, Schwabe E, Jörger KM (2017) Abyssal Solenogastres (Mollusca, Aplacophora) from the Northwest Pacific: scratching the surface of deep-sea diversity using integrative taxonomy. Front Mar Sci 4(410):1–22Google Scholar
  16. Betcher MA, Fung JM, Han AW, O’Connor R, Seronay R, Concepcion GP, Distel DL, Haygood MG (2012) Microbial distribution and abundance in the digestive system of five shipworm species (Bivalvia: Teredinidae). PLoS One 7(9):e45309Google Scholar
  17. Bigatti G, Sacristán H, Rodríguez MC, Stortz CA, Penchaszadeh PE (2010) Diet, prey narcotization and biochemical composition of salivary glands secretions of the volutid snail Odontocymbiola magellanica. J Mar Biol Ass UK 90:959–967Google Scholar
  18. Boer HH, Kits KS (1990) Histochemical and ultrastructural study of the alimentary tract of the freshwater snail Lymnaea stagnalis. J Morphol 205:97–111Google Scholar
  19. Bolognani Fantin AM, Bolognani L, Ottaviani E, Franchini A (1982) The digestive apparatus of Murex brandaris (L.) and Trunculariopsis trunculus (L.). Z Mikrosk Anat Forsch 96:561–582Google Scholar
  20. Bonnaud-Ponticelli L, Bassaglia Y (2014) Cephalopod development: what we can learn from differences. OA Biol 2:6Google Scholar
  21. Boucaud-Camou E (1972a) Premières données sur l'infrastructure du foie de Sepia officinalis L. Bull Soc Zool Fr 97:149–156Google Scholar
  22. Boucaud-Camou E (1972b) Étude infrastructurale du pancréas de Sepia officinalis L. Bull Soc Zool France 97:197–203Google Scholar
  23. Boucaud-Camou E (1977) Structure et fonction de l'épithélium caecal de Sepia officinalis L. Biol Cell 29:55–60Google Scholar
  24. Boucaud-Camou E, Boucher-Rodoni R (1983) Feeding and digestion in cephalopods. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 5 part 2. Academic, New York, pp 149–187Google Scholar
  25. Boucaud-Camou E, Yim M (1980) Fine structure and function of the digestive cell of Sepia officinalis (Mollusca: Cephalopoda). J Zool Lond 191:89–105Google Scholar
  26. Boucher-Rodoni R, Boucaud-Camou E (1987) Fine structure and absorption of ferritin in the digestive organs of Loligo vulgaris and L. forbesi (Cephalopoda, Teuthoidea). J Morphol 193:173–184Google Scholar
  27. Bourne NB, Jones GW, Bowen ID (1991) Endocytosis in the crop of the slug, Deroceras reticulatum (Müller) and the effects of the ingested molluscicides, metaldehyde and methiocarb. J Molluscan Stud 57:71–80Google Scholar
  28. Boyle PR (1975) Fine structure of the subradular organ of Lepidochitona cinereus (L), (Mollusca, Polyplacophora). Cell Tissue Res 162:411–417Google Scholar
  29. Brodie GD (2001) Some comparative histological aspects of the dendrodorid genera Doriopsilla and Dendrodoris (Opisthobranchia: Nudibranchia). Boll Malacol 37:99–104Google Scholar
  30. Budelmann BU, Schipp R, Boletzky S (1997) Cephalopoda. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6A, Mollusca II. Wiley-Liss, New York, pp 119–414Google Scholar
  31. Bush MS (1988) The ultrastructure and function of the intestine of Patella vulgata. J Zool 215:685–702Google Scholar
  32. Bush MS (1989) The ultrastructure and function of the oesophagus of Patella vulgata. J Molluscan Stud 55:111–124Google Scholar
  33. Cajaraville MP, Völkl A, Fahimi HD (1992) Peroxisomes in the digestive gland cells of the mussel Mytilus galloprovincialis Lmk. Biochemical, ultrastructural and immunocytochemical characterization. Eur J Cell Biol 56:255–264Google Scholar
  34. Camus PA, Cid YY, Cisterna L, Caceres CW (2009) Consumption and digestion of animal food by rocky intertidal herbivores: an evaluation of digestive flexibility and omnivory in three grazing species. Lat Am J Aquat Res 37:191–197Google Scholar
  35. Cockburn TC, Reid RGB (1980) Digestive tract enzymes in two aeolid nudibranchs (Opisthobranchia: Gastropoda). Comp Biochem Physiol B 65:275–281Google Scholar
  36. Colgan DJ, Ponder WF, Beacham E, Macaranas J (2007) Molecular phylogenetics of Caenogastropoda (Gastropoda: Mollusca). Mol Phylo Evol 42:717–737Google Scholar
  37. Costa PM, Rodrigo AP, Costa MH (2014) Microstructural and histochemical advances on the digestive gland of the common cuttlefish, Sepia officinalis L. Zoomorphology 133:59–69Google Scholar
  38. Dimitriadis VK (2001) Structure and function of the digestive system in Stylommatophora. In: Barker GM (ed) The biology of terrestrial molluscs. CABI Publishing, New York, pp 237–257Google Scholar
  39. Dimitriadis VK, Andrews EB (2000) Ultrastructural and cytochemical study of the digestive gland cells of the marine prosobranch Nucella lapillus (L.) in relation to function. Malacologia 42:103–112Google Scholar
  40. Dimitriadis VK, Hondros D (1992) Effect of starvation and hibernation on the fine structural morphology of digestive gland cells of the snail Helix lucorum. Malacologia 34:63–73Google Scholar
  41. Dimitriadis VK, Konstantinidou V (2002) Origin of the excretory cells in the digestive gland of the land snail Helix lucorum. Malacologia 44:145–151Google Scholar
  42. Dimitriadis VK, Hondros D, Pirpasopoulou A (1992) Crop epithelium of normal fed, starved and hibernated snails Helix lucorum: a fine structural-cytochemical study. Malacologia 34:343–354Google Scholar
  43. Dimitriadis VK, Domouhtsidou GP, Cajaraville MP (2004) Cytochemical and histochemical aspects of the digestive gland cells of the mussel Mytilus galloprovincialis (L.) in relation to function. J Mol Histol 35:501–509Google Scholar
  44. Dudek M, Adams J, Swain M, Hegarty M, Huws S, Gallagher J (2014) Metaphylogenomic and potential functionality of the limpet Patella pellucida’s gastrointestinal tract microbiome. Int J Mol Sci 15:18819–18839Google Scholar
  45. Eernisse DJ, Reynolds PD (1994) Polyplacophora. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 5. Mollusca I. Wiley-Liss, New York, pp 55–110Google Scholar
  46. Endean R (1972) Aspects of molluscan pharmacology. In: Florkin M, Scheer BT (eds) Chemical zoology, Mollusca, vol 7. Academic, New York, pp 421–466Google Scholar
  47. Fänge R, Lidman U (1976) Secretion of sulphuric acid in Cassidaria echinophora Lamarch (Mollusca: Mesogastropoda, marine carnivorous snail). Comp Biochem Physiol 53A:101–103Google Scholar
  48. Fioroni P (1982) Larval organs, larvae, metamorphosis and types of development of Mollusca—a comprehensive review. Zool Jb (Anat) 108:375–420Google Scholar
  49. Fioroni P (1990) Our recent knowledge of the development of the cuttlefish (Sepia officinalis). Zool Anz 224:1–25Google Scholar
  50. Foster GG, Hodgson AN, Boyd CS (1999) Polysaccharolytic activity of the digestive enzymes of the macroalgal herbivore, Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Comp Biochem Physiol B 122:47–52Google Scholar
  51. Franchini A, Ottaviani E (1992) Intestinal cell types in the freshwater snail Planorbarius corneus: histochemical, immunocytochemical and ultrastructural observations. Tissue Cell 24:387–396Google Scholar
  52. Franchini A, Ottaviani E (1993) Histochemical and ultrastructural study of the digestive gland of the freshwater snail Panorbarius corneus (L.) (Gastropoda, Pulmonata). Anim Biol 2:191–198Google Scholar
  53. Fretter V (1937) The structure and function of the alimentary canal of some species of Polyplacophora (Mollusca). Trans Roy Soc Edin 49:119–164Google Scholar
  54. Fretter V, Graham A (1994) British prosobranch molluscs. Their functional anatomy and ecology. The Ray Society, LondonGoogle Scholar
  55. Fretter V, Hian KB (1979) The spelization of the Aplysiid gut. Malacologia 18:7–11Google Scholar
  56. Gallardo P, Olivares A, Martínez-Yáñez R, Caamal-Monsreal C, Domingues PM, Mascaró M, Sánchez A, Pascual C, Rosas C (2017) Digestive physiology of Octopus maya and O. mimus: temporality of digestion and assimilation processes. Front Physiol 8:355Google Scholar
  57. Garcia-Esquivel Z, Felbeck H (2006) Activity of digestive enzymes along the gut of juvenile red abalone, Haliotis rufescens, fed natural and balanced diets. Aquaculture 261:615–625Google Scholar
  58. Gibbs PE, Nott JA, Nicolaidou A, Bebianno MJ (1998) The composition of phosphate granules in the digestive glands of marine prosobranch gastropods: variation in relation to taxonomy. J Molluscan Stud 64:423–433Google Scholar
  59. Giribet G (2008) Bivalvia. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the Mollusca. University of California Press, Berkeley, pp 105–141Google Scholar
  60. Godoy MS, Castro-Vazquez A, Vega IA (2013) Endosymbiotic and host proteases in the digestive tract of the invasive snail Pomacea canaliculata: diversity, origin and characterization. PLoS One 8(6):e66689Google Scholar
  61. Golding ER, Ponder WF (2010) Homology and morphology of the neogastropod valve of Leiblein (Gastropoda: Caenogastropoda). Zoomorphology 129:81–91Google Scholar
  62. Golding RE, Ponder WF, Byrne M (2009) The evolutionary and biomechanical implications of snout and proboscis morphology in Caenogastropoda (Mollusca: Gastropoda). J Nat Hist 43:2723–2763Google Scholar
  63. Gonçalves CI, Lobo-da-Cunha A (2013) Seasonal and starvation-induced changes on gonads and lipid reserves of the digestive gland of Nucella lapillus (Caenogastropoda). J Mar Biol Ass UK 93:817–824Google Scholar
  64. Gosliner TM (1994) Gastropoda: Opisthobranchia. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, Mollusca I, vol 5. Wiley-Liss, New York, pp 253–355Google Scholar
  65. Greenfield ML (1972) Feeding and gut physiology in Acanthopleura spinigera (Mollusca). J Zool 166:37–47Google Scholar
  66. Hadfield M, Strathmann M, Strathmann R (1997) Ciliary currents of non-feeding veligers in putative basal clades of gastropods. Invertebr Biol 116:313–321Google Scholar
  67. Handl CH, Todt C (2005) Foregut glands of Solenogastres (Mollusca): anatomy and revised terminology. J Morphol 265:28–42Google Scholar
  68. Haszprunar G, Ruthensteiner B (2013) Monoplacophora (Tryblidia)—some unanswered questions. Am Malacol Bull 31:189–194Google Scholar
  69. Haszprunar G, Schaefer K (1997) Monoplacophora. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6B. Mollusca II. Wiley-Liss, New York, pp 415–457Google Scholar
  70. Henry M, Boucaud-Camou E, Lefort Y (1991) Functional micro-anatomy of the digestive gland of the scallop Pecten maximus (L.). Aquat Living Resour 4:191–202Google Scholar
  71. Henry M, Benlimame N, Boucaud-Camou E, Mathieu M, Donval A, Van Wormhoudt A (1993) The amylase-secreting cells of the stomach of the scallop, Pecten maximus: ultrastructural, immunohistochemical and immunocytochemical characterizations. Tissue Cell 25:537–548Google Scholar
  72. Hookham B, Page LR (2016) How did phytoplankton-feeding larvae re-evolve within muricid gastropods? A view from developmental morphology. Mar Biol 163:11Google Scholar
  73. Ibarra-García LE, Tovar-Ramírez D, Rosas C, Campa-Córdova AI, Mazón-Suástegui JM (2018) Digestive enzymes of the Californian two-spot octopus, Octopus bimaculoides (Pickford and McConnaughey, 1949). Comp Biochem Physiol B 215:10–18Google Scholar
  74. Ivanov DL, Scheltema AH (2008) Western Atlantic Prochaetodermatidae from 35°N south to the Argentine Basin including the Gulf of Mexico (Mollusca: Aplacophora). Zootaxa 1885:1–60Google Scholar
  75. Jörger KM, Stöger I, Kano Y, Fukuda H, Knebelsberger T, Schrödl M (2010) On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evol Biol 10:323Google Scholar
  76. Kamenev YO, Eliseikina MG, Maslennikov SI, Dolmatov IY (2018) The ultrastructural features of embryonic and early larval development in Yesso scallop, Mizuhopecten yessoensis. Tissue Cell 53:76–86Google Scholar
  77. Kano Y, Brenzinger B, Nützel A, Wilson NG, Schrödl M (2016) Ringiculid bubble snails recovered as the sister group to sea slugs (Nudipleura). Sci Rep 6:30908Google Scholar
  78. Katsuno S, Sasaki T (2008) Comparative histology of radula-supporting structures in Gastropoda. Malacologia 50:13–56Google Scholar
  79. Kohn AJ (1983) Feeding biology of gastropods. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 5 part 2. Academic, New York, pp 1–63Google Scholar
  80. Koueta N, Boucaud-Camou E (1986) Comparative study of the secretion of the posterior salivary glands of decapod cephalopods. I. Sepia officinalis L. Cell Mol Biol 32:333–341Google Scholar
  81. Kress A, Schmekel L, Nott JA (1994) Ultrastructure of the digestive gland in the opisthobranch mollusk, Runcina. Veliger 37:358–373Google Scholar
  82. Kristensen JH (1972) Structure and function of crystalline styles of bivalves. Ophelia 10:91–108Google Scholar
  83. Le Pennec M, Dorange G, Beninger P, Donval A, Widowati I (1991) Les relations trophiques anse intestinale-gonade chez Pecten maximus (Mollusque Bivalve). Haliotis 21:57–69Google Scholar
  84. Le Pennec M, Beninger PG, Herry A (1995) Feeding and digestive adaptations of bivalves in sulfide-rich environments. Comp Biochem Physiol A 111:183–198Google Scholar
  85. Le Pennec G, Le Pennec M, Beninger PG (2001) Seasonal digestive gland dynamics of the scallop Pecten maximus in the Bay of Brest (France). J Mar Biol Ass UK 81:663–671Google Scholar
  86. Leal-Zanchet AM (1998) Comparative studies on the anatomy and histology of the alimentary canal of the Limacoidea and Milacidae (Pulmonata: Stylommatophora). Malacologia 39:39–57Google Scholar
  87. Leal-Zanchet AM (2002) Ultrastructure of the supporting cells and secretory cells of the alimentary canal of the slugs, Lehmannia marginata and Boettgerilla pallens (Pulmonata: Stylommatophora: Limacoidea). Malacologia 44:223–239Google Scholar
  88. Linares M, Caamal-Monsreal C, Olivares A, Sánchez A, Rodríguez S, Zúñiga O, Pascual C, Gallardo P, Rosas C (2015) Timing of digestion, absorption and assimilation in octopus species from tropical (Octopus maya) and subtropical-temperate (O. mimus) ecosystems. Aquat Biol 24:127–140Google Scholar
  89. Lindberg DR (2009) Monoplacophorans and the origin and relationships of mollusks. Evo Edu Outreach 2:191–203Google Scholar
  90. Lindberg DR, Ponder WF, Haszprunar G (2004) The Mollusca: relationships and patterns from their first half-billion years. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, New York, pp 252–278Google Scholar
  91. Liu J, Xu F, Ji P, Li L, Zhang G (2018) Involvement of clustered oyster Wnt genes in gut formation. J Ocean Limnol 36:1746–1752Google Scholar
  92. Lobo-da-Cunha A (1997) The peroxisomes of the hepatopancreas in two species of chitons. Cell Tissue Res 290:655–664Google Scholar
  93. Lobo-da-Cunha A (2001) Ultrastructural and histochemical study of the salivary glands of Aplysia depilans (Mollusca, Opisthobranchia). Acta Zool 82:201–212Google Scholar
  94. Lobo-da-Cunha A (2002) Cytochemical localisation of lysosomal enzymes and acidic mucopolysaccharides in the salivary glands of Aplysia depilans (Opisthobranchia). J Submicrosc Cytol Pathol 34:217–225Google Scholar
  95. Lobo-da-Cunha A, Batista-Pinto C (2003) Stomach cells of Aplysia depilans (Mollusca, Opisthobranchia): a histochemical, ultrastructural, and cytochemical study. J Morphol 256:360–370Google Scholar
  96. Lobo-da-Cunha A, Batista-Pinto C (2005) Light and electron microscopy studies of the oesophagus and crop epithelium in Aplysia depilans (Mollusca, Opisthobranchia). Tissue Cell 37:447–456Google Scholar
  97. Lobo-da-Cunha A, Batista-Pinto C (2007) Ultrastructural, histochemical and cytochemical characterisation of intestinal epithelial cells in Aplysia depilans (Gastropoda, Opisthobranchia). Acta Zool 88:211–221Google Scholar
  98. Lobo-da-Cunha A, Calado G (2008) Histological and ultrastructural study of the salivary glands of Bulla striata (Mollusca, Opisthobranchia). Invert Biol 127:33–44Google Scholar
  99. Lobo-da-Cunha A, Batista C, Oliveira E (1994) The peroxisomes of the hepatopancreas in marine gastropods. Biol Cell 82:67–74Google Scholar
  100. Lobo-da-Cunha A, Ferreira I, Coelho R, Calado G (2009) Light and electron microscopy study of the salivary glands of the carnivorous opisthobranch Philinopsis depicta (Mollusca, Gastropoda). Tissue Cell 41:367–375Google Scholar
  101. Lobo-da-Cunha A, Oliveira E, Alves A, Coelho R, Calado G (2010a) Light and electron microscopic study of the anterior esophagus of Bulla striata (Mollusca, Opisthobranchia). Acta Zool 91:125–138Google Scholar
  102. Lobo-da-Cunha A, Oliveira E, Ferreira I, Coelho R, Calado G (2010b) Histochemical and ultrastructural characterization of the posterior esophagus of Bulla striata (Mollusca, Opisthobranchia). Microsc Microanal 16:688–698Google Scholar
  103. Lobo-da-Cunha A, Santos T, Oliveira E, Alves A, Coelho R, Calado G (2011a) Microscopical study of the crop and oesophagus of the carnivorous opisthobranch Philinopsis depicta (Cephalaspidea, Aglajidae). J Molluscan Stud 77:322–331Google Scholar
  104. Lobo-da-Cunha A, Malheiro AR, Alves A, Oliveira E, Coelho R, Calado R (2011b) Histological and ultrastructural characterisation of the stomach and intestine of the opisthobranch Bulla striata (Heterobranchia: Cephalaspidea). Thalassas 27:61–75Google Scholar
  105. Lobo-da-Cunha A, Alves A, Oliveira E, Calado C (2016) Comparative study of salivary gland cells in carnivorous and herbivorous cephalaspideans (Gastropoda, Euopisthobranchia). J Molluscan Stud 82:43–54Google Scholar
  106. Lobo-da-Cunha A, Alves A, Oliveira E, Guimarães F, Calado G (2018) Endocytosis, lysosomes, calcium storage and other features of digestive gland cells in cephalaspidean gastropods (Mollusca, Euopisthobranchia). J Molluscan Stud 84:451–462Google Scholar
  107. Lobo-da-Cunha A, Oliveira E, Alves A, Calado G (2019) Giant peroxisomes revealed by a comparative microscopy study of digestive gland cells of cephalaspidean sea slugs (Gastropoda, Euopisthobranchia). J Mar Biol Ass UK 99:197–202Google Scholar
  108. Luchtel DL, Martin AW, Deyrup-Olsen I, Boer HH (1997) Gastropoda: Pulmonata. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6B. Mollusca II. Wiley-Liss, New York, pp 459–718Google Scholar
  109. Mackenzie AL, Marshall C (2014) Polysaccharidases in the crystalline styles of selectively bred greenshell mussel (Perna canaliculus Gmelin). J Shellfish Res 33:687–694Google Scholar
  110. Mangold KM, Young RE (1998) The systematic value of the digestive organs. In: Voss NA, Vecchione M, Toll RB, Sweeney MJ (eds) Systematics and biogeography of cephalopods, vol 1. Smithson Contrib Zool 586:21–30Google Scholar
  111. Martin R (2003) Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina. Mar Biol 143:533–541Google Scholar
  112. Martin GG, Bessette T, Martin A, Cotero R, Vumbaco K, Oakes C (2010) Morphology of epithelial cells lining the digestive tract of the giant keyhole limpet, Megathura crenulata (Mollusca; Vetigastropoda). J Morphol 271:1134–1151Google Scholar
  113. Martin GG, Martin A, Tsai W, Hafner JC (2011) Production of digestive enzymes along the gut of the giant keyhole limpet Megathura crenulata (Mollusca: Vetigastropoda). Comp Biochem Physiol A 160:365–373Google Scholar
  114. Martin R, Walther P, Tomaschko KH (2013) Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa). Zoomorphology 132:253–259Google Scholar
  115. Martoja M (1971) Données histologiques sur les glandes salivaires et oesophagiennes de Thais lapillus (L.) (=Nucella lapillus Prosobranche Néogastropode). Arch Zool Exp Gén 112:249–291Google Scholar
  116. Meeuse BJD, Fluegel W (1958) Carbohydrate-digesting enzymes in the sugar gland juice of Cryptochiton stelleri. Arch Neerl Zool 13:301–313Google Scholar
  117. Minniti F (1986) Morphological and histochemical study of pharynx of Leiblein, salivary glands and gland of Leiblein in the carnivorous Gastropoda Amyclina tinei Maravigna and Cyclope neritea Lamarck (Nassariidae: Prosobranchia Stenoglossa). Zool Anz 217:14–22Google Scholar
  118. Moreno FJ, Piñero J, Hidalgo J, Navas P, Aijón J, Lópes-Campos JL (1982) Histochemical and ultrastructural studies on the salivary glands of Helix aspersa (Mollusca). J Zool 196:343–354Google Scholar
  119. Morse MP (1984) Functional adaptations of the digestive system of the carnivorous mollusc Pleurobranchaea californica MacFarland, 1966. J Morphol 180:253–269Google Scholar
  120. Morse MP, Zardus J (1997) Bivalvia. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6A. Mollusca II. Wiley-Liss, New York, pp 7–118Google Scholar
  121. Morton B (1983) Feeding and digestion in Bivalvia. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 5 part 2. Academic, New York, pp 65–147Google Scholar
  122. Moura KRS, Terra WR, Ribeiro AF (2004) The functional organization of the salivary gland of Biomphalaria straminea (Gastropoda: Planorbidae): secretory mechanisms and enzymatic determinations. J Molluscan Stud 70:21–29Google Scholar
  123. Moya J, Serrano MT, Ângulo E (1992) Ultrastructure of the salivary glands of Arion ater (Gastropoda, Pulmonata). Biol Struct Morph 4:81–87Google Scholar
  124. Nixon M, Mangold K (2006) The early life of Sepia officinalis, and the contrast with that of Octopus vulgaris (Cephalopoda). J Zool Lond 245:407–421Google Scholar
  125. Okoshi K, Ishii T (1996) Concentrations of elements in the radular teeth of limpets, chitons, and other marine mollusks. J Mar Biotechnol 3:252–257Google Scholar
  126. Orive E, Berjon A, Fernandez Otero MP (1979) A comparative study of intestinal absorption in Arion empiricorum and Helix pomatia. Comp Biochem Physiol A 64:557–563Google Scholar
  127. Owen G (1966) Digestion. In: Wilbur W, Yonge CM (eds) Physiology of Mollusca, vol 2. Academic, New York, pp 53–96Google Scholar
  128. Owen G (1973) The fine structure and histochemistry of the digestive diverticula of the protobranchiate bivalve Nucula sulcata. Proc R Soc Lond B 183:249–264Google Scholar
  129. Owen G (1974) Feeding and digestion in the Bivalvia. In: Lowenstein O (ed) Advances in comparative physiology and biochemistry, vol 5. Academic, New York, pp 1–35Google Scholar
  130. Page LR (2009) Molluscan larvae: pelagic juveniles or slowly metamorphosing larvae? Biol Bull 216:216–225Google Scholar
  131. Page LR, Hookham B (2017) The gastropod foregut—evolution viewed through a developmental lens. Can J Zool 95:227–238Google Scholar
  132. Page LR, Hildebrand IM, Kempf SC (2019) Siphonariid development: quintessential euthyneuran larva with a mantle fold innovation (Gastropoda; Panpulmonata). J Morphol 280:634–653Google Scholar
  133. Palais F, Jubeaux G, Dedourge-Geffard O, Biagianti-Risbourg S, Geffard A (2010) Amylolytic and cellulolytic activities in the crystalline style and the digestive diverticulae of the freshwater bivalve Dreissena polymorpha (Pallas, 1771). Moll Res 30:29–36Google Scholar
  134. Parkhaev PY (2017) Origin and the early evolution of the phylum Mollusca. Paleontol J 51:663–686Google Scholar
  135. Peterson BJ (1998) The morphology, ultrastructure and function of the feeding apparatus of Sayella fusca (C.B. Adams, 1839) (Gastropoda: Pyramidellidae). J Molluscan Stud 64:281–296Google Scholar
  136. Pfeiffer CJ (1992) Intestinal ultrastructure of Nerita picea (Mollusca, Gastropoda), an intertidal marine snail of Hawaii. Acta Zool 73:9–47Google Scholar
  137. Pipe RK (1986) Light and electron microscope localization of ß-glucuronidase activity in the stomach and digestive gland of the marine gastropod Littorina littorea. Histochem J 18:175–183Google Scholar
  138. Ponte G, Modica MV (2017) Salivary glands in predatory molluks: evolutionary considerations. Front Physiol 8:580Google Scholar
  139. Ponte G, Sykes AV, Cooke GM, Almansa E, Andrews P (2017) The digestive tract of cephalopods: towards non-invasive in vivo monitoring of its physiology. Front Physiol 8:403Google Scholar
  140. Ponte G, Almansa E, Andrews PLR (2018) Editorial: The digestive tract of cephalopods: at the interface between physiology and ecology. Front Physiol 9:1409Google Scholar
  141. Power AJ, Keegan BF, Nolan K (2002) The seasonality and role of the neurotoxin tetramine in the salivary glands of the red whelk Neptunea antiqua (L.). Toxicon 40:419–425Google Scholar
  142. Purchon RD (1987) The stomach in the Bivalvia. Phil Trans R Soc Lond B 316:183–276Google Scholar
  143. Rebecchi B, Franchini A, Bolognani Fantin AM (1996) The digestive gland of Viviparus ater (Mollusca, Gastropoda, Prosobranchia): an ultrastructural and histochemical study. Tissue Cell 28:731–739Google Scholar
  144. Reid RGB, Friesen JA (1980) The digestive system of the moon snail Polinices lewisii (Gould, 1847) with emphasis on the role of the oesophageal gland. Veliger 23:25–34Google Scholar
  145. Reynolds PD (2002) The scaphopoda. Adv Mar Biol 42:137–236Google Scholar
  146. Robledo Y, Cajaraville MP (1996) Ultrastructural and cytochemical study of the Golgi complex of molluscan (Mytilus galloprovincialis) digestive cells. Cell Tissue Res 284:449–458Google Scholar
  147. Robledo Y, Marigómez I, Angulo E, Cajaraville MP (2006) Glycosylation and sorting pathways of lysosomal enzymes in mussel digestive cells. Cell Tissue Res 324:319–333Google Scholar
  148. Roeselers G, Newton ILG (2012) On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl Microbiol Biotechnol 94:1–10Google Scholar
  149. Rosa M, Ward JE, Shumway SE (2018) Selective capture and ingestion of particles by suspension-feeding bivalve molluscs: a review. J Shellfish Res 37:727–746Google Scholar
  150. Rosenberg G (2014) A new critical estimate of named species-level diversity of the recent Mollusca. Am Malacol Bull 32:308–322Google Scholar
  151. Ruthensteiner B, Schröpel V, Haszprunar G (2010) Anatomy and affinities of Micropilina minuta Warén, 1989 (Monoplacophora: Micropilinidae). J Molluscan Stud 76:323–332Google Scholar
  152. Sabbadin F, Pesante G, Elias L, Besser K, Li Y, Steele-King CG, Stark M, Rathbone DA, Dowle A, Bates R, Shipway JR, Cragg SM, Bruce NC, McQueen-Mason SJ (2018) Uncovering the molecular mechanisms of lignocellulose digestion in shipworms. Biotechnol Biofuels 11(59):1–14Google Scholar
  153. Sahlmann B (1973) Untersuchungen zur histologie und nahrungsbiologie der scaphopoden. Ph.D. dissertation, Universität Kiel, Institute für MeereskundGoogle Scholar
  154. Salvini-Plawen L (1981) The molluscan digestive system in evolution. Malacologia 21:371–401Google Scholar
  155. Salvini-Plawen L (1988) The structure and function of molluscan digestive systems. In: Clarke M, Trueman E (eds) The Mollusca, vol 11. Form and function. Academic, San Diego, pp 301–379Google Scholar
  156. Samadi L, Steiner G (2010) Conservation of ParaHox genes’ function in patterning of the digestive tract of the marine gastropod Gibbula varia. BMC Dev Biol 10:74Google Scholar
  157. Sasaki T, Saito H (2005) Feeding of Neomenia yamamotoi Baba, 1975 (Mollusca: Solenogastres) on a sea anemone. Venus 64:191–194Google Scholar
  158. Schaefer K, Haszprunar G (1997) Anatomy of Laevipilina antarctica, a Mooplacophoran limpet (Mollusca) from Antarctic waters. Acta Zool 77:295–314Google Scholar
  159. Scheltema AH (1981) Comparative morphology of the radulae and alimentary tracts in the Aplacophora. Malacologia 20:361–383Google Scholar
  160. Scheltema AH, Tscherkassky M, Kuzirian AM (1994) Aplacophora. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 5. Mollusca I. Wiley-Liss, New York, pp 13–54Google Scholar
  161. Scherholz M, Redl E, Wollesen T, Todt C, Wanninger A (2013) Aplacophoran mollusks evolved from ancestors with polyplacophoran-like features. Curr Biol 23:2130–2134Google Scholar
  162. Schipp R, Boletzky S (1976) The pancreatic appendages of dibranchiate cephalopods. I. The fine structure of the “pancreas” in Sepioidea. Zoomorphologie 86:81–98Google Scholar
  163. Schultz MC (1983) A correlated light and electron microscopic study of the structure and secretory activity of the accessory salivary glands of the marine gastropods, Conus flavidus and C. vexillum (Neogastropoda, Conacea). J Morphol 176:89–111Google Scholar
  164. Señarís MP, García-Álvarez O, Urgorri V (2014) Morphology of Falcidens vasconiensis (Mollusca, Caudofoveata, Chaetodermatidae), including a 3D reconstruction of the internal anatomy. J Nat Hist 48:2871–2884Google Scholar
  165. Serrano T, Gómez BJ, Angulo E (1996) Light and electron microscopy study of the salivary gland secretory cells of Helicoidea (Gastropoda, Stylommatophora). Tissue Cell 28:237–251Google Scholar
  166. Shimek R, Steiner G (1997) Scaphopoda. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 6B. Mollusca II. Wiley-Liss, New York, pp 719–781Google Scholar
  167. Sigwart JD, Lindberg DR (2015) Consensus and confusion in molluscan trees: evaluating morphological and molecular phylogenies. Syst Biol 64:384–395Google Scholar
  168. Steiner G (1994) Variations in the number of intestinal loops in Scaphopoda (Mollusca). Mar Ecol 15:165–174Google Scholar
  169. Sutton MD, Briggs DEG, Siveter DJ, Siveter DJ, Sigwart JD (2012) A Silurian armoured aplacophoran and implications for molluscan phylogeny. Nature 490:94–97Google Scholar
  170. Swift K, Johnston D, Moltschaniwskyj N (2005) The digestive gland of the Southern dumpling squid (Euprymna tasmanica): structure and function. J Exp Mar Biol Ecol 315:177–186Google Scholar
  171. Taïeb N (2001) Distribution of digestive tubules and fine structure of digestive cells of Aplysia punctata (Cuvier, 1803). J Molluscan Stud 67:169–182Google Scholar
  172. Taïeb N, Vicente N (1999) Histochemistry and ultrastructure of the crypt cells in the digestive gland of Aplysia punctata (Cuvier, 1803). J Molluscan Stud 65:385–398Google Scholar
  173. Thaib NT (1976) Anatomy, histology and histochemistry of the alimentary canal of Dentalium entalis L., with some observations on living animals. Ph.D. dissertation, University of GlasgowGoogle Scholar
  174. Thomas K (1993) The functional morphology of the digestive system of Lyonsia hyalina Conrad, 1831 (Bivalvia: Anomalodesmata: Pandoroidea). J Molluscan Stud 59:175–186Google Scholar
  175. Todt C (2006) Ultrastructure of multicellular foregut glands in selected Solenogastres (Mollusca). Zoomorphology 125:119–134Google Scholar
  176. Todt C, Salvini-Plawen L (2004a) Ultrastructure of the midgut epithelium of Wirenia argentea (Mollusca: Solenogastres). J Molluscan Stud 70:213–224Google Scholar
  177. Todt C, Salvini-Plawen L (2004b) Ultrastructure and histochemistry of the foregut in Wirenia argentea and Genitoconia rosea (Mollusca, Solenogastres). Zoomorphology 123:65–80Google Scholar
  178. Todt C, Salvini-Plawen L (2005) The digestive tract of Helicoradomenia (Solenogastres, Mollusca), aplacophoran molluscs from the hydrothermal vents of the East Pacific Rise. Invert Biol 124:230–253Google Scholar
  179. Todt C, Okusu A, Schander C, Schwabe E (2008) Solenogastres, Caudofoveata, and Polyplacophora. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the Mollusca. University of California Press, Berkeley, pp 71–96Google Scholar
  180. Tsuji A, Tominaga K, Nishiyama N, Yuasa K (2013) Comprehensive enzymatic analysis of the cellulolytic system in digestive fluid of the sea hare Aplysia kurodai. Efficient glucose release from sea lettuce by synergistic action of 45 kDa endoglucanase and 210 kDa ß-glucosidase. PLoS One 8(6):e65418Google Scholar
  181. Tsuji A, Nishiyama N, Ohshima M, Maniwa S, Kuwamura S, Shiraishi M, Yuasa K (2014) Comprehensive enzymatic analysis of the amylolytic system in the digestive fluid of the sea hare, Aplysia kurodai: unique properties of two α-amylases and two α-glucosidases. FEBS Open Bio 4:560–570Google Scholar
  182. Uribe JE, Zardoya R (2017) Revisiting the phylogeny of Cephalopoda using complete mitochondrial genomes. J Molluscan Stud 83:133–144Google Scholar
  183. Vinther J (2015) The origins of molluscs. Palaeontology 58:19–34Google Scholar
  184. Voight JR (2015) Xylotrophic bivalves: aspects of their biology and the impacts of humans. J Molluscan Stud 81:175–186Google Scholar
  185. Voltzow J (1994) Gastropoda: Prosobranchia. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates, vol 5. Mollusca I. Wiley-Liss, New York, pp 111–252Google Scholar
  186. Walker G (1970) The cytology, histochemistry, and ultrastructure of the cell types found in the digestive gland of the slug Agriolimax reticulatus (Müller). Protoplasma 71:91–109Google Scholar
  187. Walker G (1972) The digestive system of the slug, Agriolimax reticulatus (Müller): experiments on phagocytosis and nutrient absorption. Proc Malacol Soc London 40:33–43Google Scholar
  188. Walker AJ, Glen DM, Shewry PR (1999) Bacteria associated with the digestive system of the slug Deroceras reticulatum are not required for protein digestion. Soil Biol Biochem 31:1387–1394Google Scholar
  189. Wanninger A, Wollesen T (2019) The evolution of molluscs. Biol Rev Camb Philos Soc 94:102–115Google Scholar
  190. Weinstein JE (1995) Fine structure of the digestive tubule of the eastern oyster, Crassostrea virginica (Gmelin, 1791). J Shellfish Res 14:97–103Google Scholar
  191. West DJ, Andrews EB, McVean AR, Osborne DJ, Thorndyke MC (1994) Isolation of serotonin from the accessory salivary glands of the marine snail Nucella lapillus. Toxicon 32:1261–1264Google Scholar
  192. Westermann B, Schipp R (1998a) Morphology and histology of the digestive tract of Nautilus pompilius and Nautilus macromphalus (Cephalopoda, Tetrabranchiata). Zoomorphology 117:237–245Google Scholar
  193. Westermann B, Schipp R (1998b) Cytological and enzyme-histochemical investigations on the digestive organs of Nautilus pompilius (Cephalopoda, Tetrabranchiata). Cell Tissue Res 293:327–336Google Scholar
  194. Westermann B, Beuerlein K, Ruth P, Schipp R (2000) Tracer studies of food absortion in the digestive tract of Nautilus pompilius (Cephalopoda, Tetrabranchiata). Cell Tissue Res 300:173–179Google Scholar
  195. Westermann B, Ruth P, Litzlbauer HD, Beck I, Beuerlein K, Schmidtberg H, Kaleta EF, Schipp R (2002) The digestive tract of Nautilus pompilius (Cephalopoda, Tetrabranchiata): an X-ray analytical and computational tomography study on the living animal. J Exp Biol 205:1617–1624Google Scholar
  196. Wollesen T, Rodríguez Monje SV, McDougall C, Degnan BM, Wanninger A (2015) The ParaHox gene Gsx patterns the apical organ and central nervous system but not the foregut in scaphopod and cephalopod mollusks. EvoDevo 6:41Google Scholar
  197. Zapata F, Wilson NG, Howison M, Andrade SCS, Jörger KM, Schrödl M, Goetz FE, Giribet G, Dunn CW (2014) Phylogenomic analyses of deep gastropod relationships reject Orthogastropoda. Proc R Soc B 281:20141739Google Scholar
  198. Zimmer KP, De Laffolie J, Barone M, Naim H (2016) Endocytosis in enterocytes. Wien Med Wochenschr 166:205–210Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS)University of PortoPortoPortugal
  2. 2.Interdisciplinary Centre of Marine and Environmental Research (CIIMAR)MatosinhosPortugal

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