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Structure, function and development of the digestive system in malacostracan crustaceans and adaptation to different lifestyles

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Abstract

The digestive system of the malacostracan crustaceans, namely the decapods, isopods, amphipods and mysids, is among the most complex organ systems of the animal kingdom serving multiple functions such as food processing, absorption and storage of nutrients, synthesis of digestive enzymes and blood proteins, detoxification of xenobiotics and osmoregulation. It is rather well investigated compared to other invertebrates because the Malacostraca include many ecological keystone species and food items for humans. The Decapoda and Peracarida share food processing with chewing and filtering structures of the stomach but differ with respect to morphology and ultrastructure of the digestive glands. In the Peracarida, the digestive glands are composed of few, relatively large lateral caeca, whereas in the Decapoda, hundreds to thousands of blindly ending tubules form a voluminous hepatopancreas. Morphogenesis and onset of functionality of the digestive system strongly depend on the mode of development. The digestive system is early developed in species with feeding planktonic larvae and appears late in species with direct lecithotrophic development. Some structures of the digestive system like the stomach ossicles are rather constant in higher taxa and are of taxonomic value, whereas others like the chewing structures are to some degree adapted to the feeding strategy. The nutrient absorbing and storing cells of the digestive glands show considerable ultrastructural variation during moult cycle, vitellogenesis and starvation. Some of the various functions of the digestive system are already assigned to specific sections of the digestive tract and cell types, but others still await precise localization.

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References

  • Abdu U, Yehezkel G, Sagi A (2000) Oocyte development and polypeptide dynamics during ovarian maturation in the red-claw crayfish Cherax quadricarinatus. Invert Reprod Dev 37:75–83

    Article  Google Scholar 

  • Abrunhosa F, Kittaka J (1997a) Functional morphology of mouthparts and foregut of the last zoea, glaucothoe and first juvenile of the king crabs Paralithodes camtschaticus, P. brevipes and P. platypus. Fish Sci 63:923–930

    Article  CAS  Google Scholar 

  • Abrunhosa F, Kittaka J (1997b) Morphological changes in the midgut, midgut gland and hindgut during the larval and postlarval development of the red king crab Paralithodes camtschaticus. Fish Sci 63:746–754

    Article  CAS  Google Scholar 

  • Abrunhosa F, Melo M (2008) Development and functional morphology of the foreguts of larvae and postlarvae of three crustacean decapods. Braz J Biol 68:221–228

    Article  CAS  PubMed  Google Scholar 

  • Abrunhosa F, Melo M, Lima JF, Abrunhosa J (2006) Developmental morphology of mouthparts and foregut of the larvae and postlarvae of Lepidophthalmus siriboia Felder & Rodrigues, 1993 (Decapoda: Callianassidae). Acta Amaz 36:335–342

    Article  Google Scholar 

  • Abrunhosa FA, Simith DJ, Monteiro JR, Souza Junior AN, Oliva PA (2011) Development and functional morphology of the larval foregut of two brachyuran species from Northern Brazil. An Acad Bras Cienc 83:1269–1278

    Article  PubMed  Google Scholar 

  • Abubakr MA, Jones DA (1992) Functional morphology and ultrastructure of the anterior mid-gut diverticulae of larvae of Penaeus monodon Fabricius, 1798 (Decapoda, Natantia). Crustaceana 62:142–158

    Article  Google Scholar 

  • Ahearn GA (1987) Nutrient transport by the crustacean gastrointestinal tract: recent advances with vesicle techniques. Biol Rev 62:45–63

    Article  CAS  Google Scholar 

  • Ahyong ST, Lowry JK, Alonso M, Bamber RN, Boxshall GA, Castro P, Gerken S, Karaman GS, Goy JW, Jones DS, Meland K, Rogers DC, Svavarsson J (2011) Subphylum Crustacea Brünnich, 1772. Zootaxa 3148:165–191

    Article  Google Scholar 

  • Al-Mohanna SY, Nott JA (1986) B-cells and digestion in the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda). J Mar Biol Assoc UK 66:403–414

    Article  Google Scholar 

  • Al-Mohanna SY, Nott JA (1987) R-cells and the digestive cycle in Penaeus semisulcatus (Crustacea: Decapoda). Mar Biol 95:129–137

    Article  Google Scholar 

  • Al-Mohanna SY, Nott JA (1989) Functional cytology of the hepatopancreas of Penaeus semisulcatus (Crustacea: Decapoda) during the moult cycle. Mar Biol 101:535–544

    Article  Google Scholar 

  • Al-Mohanna SY, Nott JA, Lane DJW (1985a) Mitotic E- and secretory F-cells in the hepatopancreas of the shrimp Penaeus semisulcatus (Crustacea: Decapoda). J Mar Biol Assoc UK 65:901–910

    Article  Google Scholar 

  • Al-Mohanna SY, Nott JA, Lane DJW (1985b) M-‘midget’ cells in the hepatopancreas of the shrimp, Penaeus semisulcatus De Haan, 1844 (Decapoda, Natantia). Crustaceana 48:260–268

    Article  Google Scholar 

  • Anger K (2001) The biology of decapod crustacean larvae. Crustacean issues 14. A.A. Balkema, Rotterdam

  • Anger K, Storch V, Anger V, Capuzzo JM (1985) Effects of starvation on moult cycle and hepatopancreas of stage I lobster (Homarus americanus) larvae. Helgol Meeresunters 39:107–116

    Article  Google Scholar 

  • Ashley CM, Simpson MG, Holdich DM, Bell DR (1996) 2,3,7,8-Tetrachloro-dibenzo-p-dioxin is a potent toxin and induces cytochrome P 450 in the crayfish, Pacifastacus leniusculus. Aquat Toxicol 35:157–169

    Article  CAS  Google Scholar 

  • Bettica A, Shay MT, Vernon G, Witkus R (1984) An ultrastructural study of cell differentiation and associated acid phosphatase activity in the hepatopancreas of Porcellio scaber. Symp Zool Soc Lond 53:199–215

  • Bettica A, Witkus R, Vernon GM (1987) Ultrastructure of the foregut-hindgut junction in Porcellio scaber Latreille. J Crust Biol 7:619–623

    Article  Google Scholar 

  • Biesiot PM, McDowell JE (1995) Midgut-gland development during early life-history stages of the American lobster Homarus americanus. J Crust Biol 15:679–685

    Article  Google Scholar 

  • Bode W, Gomis-Rüth FX, Huber R, Zwilling R, Stöcker W (1992) Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 358:164–167

    Article  CAS  PubMed  Google Scholar 

  • Bogataj U, Praznik M, Mrak P, Štrus J, Tušek-Žnidarič M, Žnidaršič N (2018) Comparative ultrastructure of cells and cuticle in the anterior chamber and papillate region of Porcellio scaber (Crustacea, Isopoda) hindgut. In: Hornung E, Taiti S, Szlavecz K (eds) Isopods in a changing world. ZooKeys, vol 801, pp 427–458

    Google Scholar 

  • Böhm H (1996) Activity of the stomatogastric system in free-moving crayfish, Orconectes limosus Raf. Zoology 99:247–257

    Google Scholar 

  • Bouchon D, Zimmer M, Dittmer J (2016) The terrestrial isopod microbiome: an all-in-one toolbox for animal microbe interactions of ecological relevance. Front Microbiol 7:1472

    Article  PubMed  PubMed Central  Google Scholar 

  • Brösing A (2010) Recent developments on the morphology of the brachyuran foregut ossicles and gastric teeth. Zootaxa 2510:1–44

    Article  Google Scholar 

  • Brösing A, Türkay M (2011) Gastric teeth of some thoracotreme crabs and their contribution to the brachyuran phylogeny. J Morphol 272:1109–1115

    Article  PubMed  Google Scholar 

  • Browne WE, Price AL, Gerberding M, Patel NH (2005) Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149

    Article  PubMed  Google Scholar 

  • Castejon D, Ribes E, Dufort M, Rotlland G, Guerao G (2015a) Foregut morphology and ontogeny of the mud crab Dyspanopeus sayi (Smith, 1869) (Decapoda, Brachyura, Panopeidae). Arthropod Struct Dev 44:33–41

    Article  PubMed  Google Scholar 

  • Castejon D, Rotlland G, Ribes E, Dufort M, Guerao G (2015b) Foregut morphology and ontogeny of the spider crab Maja brachydactyla (Brachyura, Majoidea, Majidae). J Morphol 276:1109–1122

    Article  PubMed  Google Scholar 

  • Castejon D, Rotlland G, Ribes E, Dufort M, Guerao G (2018) Morphology and ultrastructure of the esophagus during the ontogeny of the spider crab Maja brachydactyla (Decapoda, Brachyura, Majidae). J Morphol 279:710–723

    Article  PubMed  Google Scholar 

  • Ceccaldi HJ (2006) The digestive tract: anatomy, physiology, and biochemistry. In: Forest J, von Vaupel Klein JC (eds) Treatise on zoology – anatomy, taxonomy, biology. The Crustacea, vol 2. Brill, Leiden, pp 85–203

    Google Scholar 

  • Cerenius L, Liang Z, Duvic B, Keyser P, Hellmann U, Palva ET, Iwanaga S, Söderhäll K (1994) Structure and biological activity of a 1,3-ß-D-glucan-binding protein in crustacean blood. J Biol Chem 269:29462–29467

    CAS  PubMed  Google Scholar 

  • Christie AE, Kutz-Naber KK, Stemmler EA, Klein A, Messinger DI, Goiney CC, Conterato AJ, Bruns EA, Hsu Y-WA, Li L, Dickinson PS (2007) Midgut epithelial endocrine cells are a rich source of the neuropeptides APSGFLGMRamide (Cancer borealis tachykinin-related peptide Ia) and GYRKPPFNGSIFamide (Gly1-SIFamide) in the crabs Cancer borealis, Cancer magister and Cancer productus. J Exp Biol 210:699–714

    Article  CAS  PubMed  Google Scholar 

  • Coleman CO (1992) Foregut morphology of Amphipoda (Crustacea). An example of its relevance for systematics. Ophelia 14:346–370

    Google Scholar 

  • Coleman CO (1994) Comparative anatomy of the alimentary canal of hyperid amphipods. J Crust Biol 4:346–370

    Article  Google Scholar 

  • Coruzzi L, Witkus R, Vernon GM (1982) Function-related structural characters and their modifications in the hindgut epithelium of two terrestrial isopods, Armadillidium vulgare and Oniscus asellus. Exp Cell Biol 50:229–240

    CAS  PubMed  Google Scholar 

  • Davis LE, Burnett AL (1964) A study of growth and cell differentiation in the hepatopancreas of the crayfish. Dev Biol 10:122–153

    Article  CAS  PubMed  Google Scholar 

  • De Grave S, Pentcheff ND, Ahyong ST, Chan TY, Crandall KA, Dworschak PC, Felder DL, Feldmann RM, Fransen CHJM, Goulding LYD, Lemaitre R, Low MEY, Martin JW, Ng PKL, Schweitzer CE, Tan SH, Tshudy D, Wetzer R (2009) A classification of living and fossil genera of decapod crustaceans. Raffles Bull Zool (Suppl 21:1–109

    Google Scholar 

  • Del Ramo J, Pastor A, Torreblanca A, Medina J, Díaz-Mayans J (1989) Cadmium-binding proteins in midgut gland of freshwater crayfish Procambarus clarkii. Bull Environ Contam Toxicol 42:241–246

    Article  PubMed  Google Scholar 

  • Diaz AC, Fernandez Gimenez AV, Velurtas SM, Fenucci JL (2008) Ontogenetic changes in the digestive system of Pleoticus muelleri (Decapoda, Penaeoidea). Invertebr Reprod Dev 52:1–12

    Article  Google Scholar 

  • Eberl R (2012) Distribution, habitat and food preferences of sympatric high intertidal isopod species Ligia occidentalis and Ligia pallasii (Ligiidae: Oniscidea). J Nat Hist 46:29–30

    Article  Google Scholar 

  • Factor RJ (1981) Development and metamorphosis of the digestive system of larval lobsters, Homarus americanus (Decapoda: Nephropidae). J Morphol 169:225–242

    Article  PubMed  Google Scholar 

  • Factor RJ (1982) Development and metamorphosis of the feeding apparatus of the stone crab, Menippe mercenaria (Brachyura, Xanthidae). J Morphol 172:299–312

    Article  PubMed  Google Scholar 

  • Friesen JA, Mann KH, Willison JHM (1986) Gross anatomy and fine structure of the gut of marine mysid shrimp Mysis stenolepis. Can J Zool 64:431–441

    Article  Google Scholar 

  • Garm A (2004) Mechanical functions of setae from the mouth apparatus of seven species of decapod crustaceans. J Morphol 260:85–100

    Article  PubMed  Google Scholar 

  • Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801

    Article  CAS  PubMed  Google Scholar 

  • Gherardi F, Souty-Grosset C, Vogt G, Diéguez-Uribeondo J, Crandall KA (2010) Infraorder Astacidea Latreille, 1802 p.p.: the freshwater crayfish. In: Schram FR, von Vaupel Klein JC (eds) Treatise on zoology – anatomy, taxonomy, biology. The Crustacea. Vol 9, part A: Eucarida: Euphausiacea, Amphionidacea, and Decapoda (partim). Brill, Leiden, pp 269–423

    Chapter  Google Scholar 

  • Graf F, Michaut P (1980) Fine structure of the midgut posterior caeca in the crustacean Orchestia in intermolt: recognition of two distinct segments. J Morphol 165:261–284

    Article  PubMed  Google Scholar 

  • Greenaway P (1985) Calcium balance and moulting in the Crustacea. Biol Rev 60:425–454

    Article  CAS  Google Scholar 

  • Gruner H-E (1993) 1. Klasse Crustacea. In: Gruner H-E (Hrsg) Lehrbuch der Speziellen Zoologie. Band 1: Wirbellose Tiere, 4. Teil: Arthropoda (ohne Insecta). Gustav Fischer Verlag, Stuttgart, pp 448–1030

  • Hall M, Wang R, van Antwerpen R, Sottrup-Jensen L, Söderhäll K (1999) The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc Natl Acad Sci U S A 96:1965–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hames CAC, Hopkin SP (1989) The structure and function of the digestive system of terrestrial isopods. Zoology 217:599–627

    Article  Google Scholar 

  • Hames CAC, Hopkin SP (1991) A daily cycle of apocrine secretion by the B cells in the hepatopancreas of terrestrial isopods. Can J Zool 69:1931–1937

    Article  Google Scholar 

  • Hartenstein R (1964) Feeding, digestion, glycogen, and the environmental conditions of the digestive system in Oniscus asellus. J Insect Physiol 10:611–612

    Article  CAS  Google Scholar 

  • Hassall M, Jennings JB (1975) Adaptive features of gut structure and digestive physiology in the terrestrial isopod Philoscia muscorum (Scopoli) 1763. Biol Bull 149:348–364

    Article  CAS  PubMed  Google Scholar 

  • Herring P (1976) Bioluminescence in decapod Crustacea. J Mar Biol Assoc UK 56:1029–1047

    Article  Google Scholar 

  • Herring P (1982) The comparative morphology of hepatic photophores in decapod Crustacea. J Mar Biol Assoc UK 61:723–737

    Article  Google Scholar 

  • Hinton DJ, Corey S (1979) The mouthparts and digestive tract in the larval stages of Homarus americanus. Can J Zool 57:1413–1423

    Article  Google Scholar 

  • Holdich DM, Mayes KR (1975) A fine-structural re-examination of the so-called ‘midgut’ of the isopod Porcellio. Crustaceana 29:186–192

    Article  Google Scholar 

  • Hopkin S, Martin M (1982) The distribution of zinc, cadmium, lead and copper within the hepatopancreas of a woodlouse. Tissue Cell 14:703–715

    Article  CAS  PubMed  Google Scholar 

  • Hornung E (2011) Evolutionary adaptation of oniscidean isopods to terrestrial life: structure, physiology and behaviour. Terr Arthropod Rev 4:95–130

    Article  Google Scholar 

  • Hryniewiecka-Szyfter Z, Storch V (1986) The influence of starvation and different diets on the hindgut of isopoda (Mesidotea entomon, Oniscus asellus, Porcellio scaber). Protoplasma 134:53–59

    Article  Google Scholar 

  • Hu KJ, Leung PC (2007) Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comp Biochem Physiol B 146:69–80

    Article  CAS  PubMed  Google Scholar 

  • Icely JD, Nott JA (1984) On the morphology and fine structure of the alimentary canal of Corophium volutator (Pallas) (Crustacea: Amphipoda). Phil Trans R Soc Lond B 306:49–78

    Article  Google Scholar 

  • Icely JD, Nott JA (1992) Digestion and absorption: digestive system and associated organs. In: Harrison FW, Humes AG (ed) Microscopic anatomy of invertebrates. Vol 10: Decapod Crustacea. Wiley-Liss, New York, pp 147–201

  • James MO, Boyle SM (1998) Cytochromes P450 in Crustacea. Comp Biochem Physiol 121C:157–172

    CAS  Google Scholar 

  • Kao D, Lai AG, Stamataki E, Rosic S, Konstandinides N, Jarvis E, Di Donfrancesco A, Pouchkina-Stancheva N, Sémon M, Grillo M, Bruce H, Kumar S, Siwanowicz I, Le A, Lemire A, Eisen MB, Extavour C, Browne WE, Wolff C, Averof M, Patel NH, Sarkies P, Pavlopoulos A, Aboobaker A (2016) The genome of the crustacean Parhyale hawaiensis, a model for animal development, regeneration, immunity and lignocellulose digestion. eLife 5:e20062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khayat M, Funkenstein B, Tietz A, Lubzens E (1995) In vivo, in vitro and cell-free synthesis of hemocyanin in the shrimp Penaeus semisulcatus (de Haan). Comp Biochem Physiol B 112:31–38

    Article  Google Scholar 

  • Kobusch W (1998) The foregut of the Mysida (Crustacea, Peracarida) and its phylogenetic relevance. Phil Trans R Soc Lond B 353:559–581

    Article  Google Scholar 

  • Köhler H-R, Hüttenrauch K, Berkus M, Gräff S, Alberti G (1996) Cellular hepatopancreatic reactions in Porcellio scaber (Isopoda) as biomarkers for the evaluation of heavy metal toxicity in soils. Appl Soil Ecol 3:1–15

    Article  Google Scholar 

  • Kostanjšek R, Štrus J, Avguštin G (2002) Genetic diversity of bacteria associated with the hindgut of the terrestrial crustacean Porcellio scaber (Crustacea: Isopoda). FEMS Microbiol Ecol 40:171–179

    Article  PubMed  Google Scholar 

  • Kostanjšek R, Avguštin G, Drobne D, Štrus J (2003) Morphological and molecular examination of bacteria associated with the wall of the papillate region of the gut in Porcellio scaber. In: Sfenthourakis S, Araujo PB, Hornung E, Schmalfuss H, Taiti S, Szlavecz K (eds) The biology of terrestrial isopods. Crustaceana monographs 2. Brill, Leiden, pp 103–120

    Google Scholar 

  • Kostanjšek R, Štrus J, Lapanje A, Avguštin G, Rupnik M, Drobne D (2006) Intestinal microbiota of terrestrial isopods. In: König H, Varma A (ed) Soil biology, Vol 6: intestinal microorganism in soil invertebrates. Springer, Berlin, pp 115–131

  • Kostanjšek R, Štrus J, Avguštin G (2007) “Candidatus Bacilloplasma”, a novel lineage of Mollicutes associated with the hindgut wall of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). Appl Environ Microbiol 73:5566–5573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostanjšek R, Milatovič M, Štrus J (2010) Endogenous origin of endo-β-1,4-glucanase in common woodlouse Porcellio scaber (Crustacea, Isopoda). J Comp Physiol B 180:1143–1153

    Article  CAS  PubMed  Google Scholar 

  • Kozlovskaja LS, Striganova BR (1977) Food digestion and assimilation in desert woodlouse and their relations to the soil microflora. Ecol Bull 25:240–245

    Google Scholar 

  • Kummer G, Keller R (1993) High-affinity binding of crustacean hyperglycemic hormone (CHH) to hepatopancreatic plasma membranes of the crab Carcinus maenas and the crayfish Orconectes limosus. Peptides 14:103–108

    Article  CAS  PubMed  Google Scholar 

  • Lehnert SA, Johnson SE (2002) Expression of hemocyanin and digestive enzyme messenger RNAs in the hepatopancreas of the Black Tiger Shrimp Penaeus monodon. Comp Biochem Physiol B 133:163–171

    Article  PubMed  Google Scholar 

  • Lemmens JWTJ, Knott B (1994) Morphological changes in external and internal feeding structures during the transition phyllosoma-puerulus-juvenile in the western rock lobster (Panulirus cygnus, Decapoda: Palinuridae). J Morphol 220:271–280

    Article  CAS  PubMed  Google Scholar 

  • Lešer V, Drobne D, Vilhar B, Kladnik A, Žnidaršič N, Štrus J (2008) Epithelial thickness and lipid droplets in the hepatopancreas of Porcellio scaber (Crustacea: Isopoda) in different physiological conditions. Zoology 111:419–432

    Article  PubMed  Google Scholar 

  • Linton SM, Greenaway P, Towle DW (2006) Endogenous production of endo-beta-1,4-glucanase by decapod crustaceans. J Comp Physiol B 176:339–348

    Article  CAS  PubMed  Google Scholar 

  • Loizzi RF (1971) Interpretation of crayfish hepatopancreatic function based on fine structural analysis of epithelial cell lines and muscle network. Z Zellforsch Mikrosk Anat 113:420–440

    Article  CAS  PubMed  Google Scholar 

  • Lovett DL, Felder DL (1989) Ontogeny of gut morphology in the white shrimp Penaeus setiferus (Decapoda, Penaeidae). J Morphol 201:253–272

    Article  PubMed  Google Scholar 

  • Loya-Javellana GN, Fielder DR, Thorne MJ (1995) Foregut evacuation, return of appetite and gastric fluid secretion in the tropical freshwater crayfish, Cherax quadricarinatus. Aquaculture 134:295–306

    Article  Google Scholar 

  • Manship BM, Walker AJ, Davies AJ (2011) Brooding and embryonic development in the crustacean Paragnathia formica (Hesse, 1864) (Peracarida: Isopoda: Gnathiidae). Arthropod Struct Dev 40:135–145

    Article  PubMed  Google Scholar 

  • Martin JW, Davis GE (2001) An updated classification of the recent Crustacea. Science Series 39. Natural History Museum of Los Angeles County, Los Angeles

  • McGaw IJ, Curtis DL (2013) A review of gastric processing in decapod crustaceans. J Comp Physiol B 183:443–465

    Article  PubMed  Google Scholar 

  • Mickėnienė L (1999) Bacterial flora in the digestive tract of native and alien species of crayfish in Lithuania. Freshwater Crayfish 12:279–287

    Google Scholar 

  • Mikami S, Greenwood JG, Takashima F (1994) Functional morphology and cytology of the phyllosomal digestive system of Ibacus ciliatus and Panulirus japonicus (Decapoda, Scyllaridae and Palinuridae). Crustaceana 67:212–225

    Article  Google Scholar 

  • Milatovič M, Kostanjšek R, Štrus J (2010) Ontogenetic development of Porcellio scaber: staging based on microscopic anatomy. J Crust Biol 30:225–235

    Article  Google Scholar 

  • Möhrlen F, Baus S, Gruber A, Rackwitz H-R, Schnölzer M, Vogt G, Zwilling R (2001) Activation of pro-astacin. Immunological and model peptide studies on the processing of immature astacin, a zinc-endopeptidase from the crayfish Astacus astacus. Eur J Biochem 268:2540–2546

    Article  PubMed  Google Scholar 

  • Mrak P, Bogataj U, Štrus J, Žnidaršič N (2015) Formation of the hindgut cuticular lining during embryonic development of Porcellio scaber (Crustacea, Isopoda). In: Taiti S, Hornung E, Štrus J, Bouchon D (eds) Trends in terrestrial isopod biology. ZooKeys, vol 515, pp 93–109

    Google Scholar 

  • Muhammad F, Zhang ZF, Shao MY, Dong YP, Muhammad S (2012) Ontogenesis of digestive system in Litopenaeus vannamei (Boone, 1931) (Crustacea: Decapoda). Ital J Zool 79:77–85

    Article  Google Scholar 

  • Mykles DL (1979) Ultrastructure of alimentary epithelia of lobsters, Homarus americanus and H. gammarus, and crab, Cancer magister. Zoomorphol 92:201–215

    Article  Google Scholar 

  • Nair SG (1956) On the embryology of the isopod Irona. J Embryol Exp Morph 4:1–33

    Google Scholar 

  • Nair GA, Attia FA, Saeid NH (1994) Food preference and growth-rates of the woodlouse Porcellio scaber Latreille, 1804 (Isopoda, Oniscidea, Porcellionidae). Afr J Ecol 32:80–84

    Article  Google Scholar 

  • Nakamura K, Seki K (1990) Organogenesis during metamorphosis in the prawn Penaeus japonicus. Nippon Suisan Gakkaishi 56:1413–1417

    Article  Google Scholar 

  • Nishida S, Quigley BD, Booth BD, Nemoto T, Kittaka J (1990) Comparative morphology of the mouthparts and foregut of the final-stage phyllosoma, puerulus, and postpuerulus of the rock lobster Jasus edwardsii (Decapoda: Palinuridae). J Crust Biol 10:293–305

    Article  Google Scholar 

  • Nishida S, Takahashi Y, Kittaka J (1995) Structural changes in the hepatopancreas of the rock lobster, Jasus edwardsii (Crustacea: Palinuridae) during development from the puerulus to post-puerulus. Mar Biol 123:837–844

    Article  Google Scholar 

  • Odendaal JP, Reinecke AJ (2003) Quantifying histopathological alterations in the hepatopancreas of the woodlouse Porcellio laevis (Isopoda) as a biomarker of cadmium exposure. Ecotoxicol Environ Saf 56:319–325

    Article  CAS  PubMed  Google Scholar 

  • Pakes MJ, Weis AK, Mejia-Ortiz L (2014) Arthropods host intracellular chemosynthetic symbionts, too: cave study reveals an unusual form of symbiosis. J Crust Biol 34:334–341

    Article  Google Scholar 

  • Palackal T, Faso L, Zung JL, Vernon G, Witkus R (1984) The ultrastructure of the hindgut epithelium of terrestrial isopods and its role in osmoregulation. Symp Zool Soc Lond 53:185–198

    Google Scholar 

  • Phupet B, Pitakpornpreecha T, Baowubon N, Runsaeng P, Utarabhand P (2018) Lipopolysaccharide- and β-1,3-glucan-binding protein from Litopenaeus vannamei: purification, cloning and contribution in shrimp defense immunity via phenoloxidase activation. Dev Comp Immunol 81:167–179

    Article  CAS  PubMed  Google Scholar 

  • Prosi F, Dallinger R (1988) Heavy metals in the terrestrial isopod Porcellio scaber Latreille. I. Histochemical and ultrastructural characterization of metal-containing lysosomes. Cell Biol Toxicol 4:81–96

    Article  CAS  PubMed  Google Scholar 

  • Queiroz LD, Abrunhosa FA, Maciel CR (2011) Ontogenesis and functional morphology of the digestive system of the freshwater prawn, Macrobrachium amazonicum (Decapoda: Palaemonidae). Zoologia 28:395–402

    Article  Google Scholar 

  • Reedy AR (1935) The structure, mechanism and development of the gastric armature in Stomatopoda with a discussion as to its evolution in Decapoda. Proc Natl Acad Sci India B Biol Sci 1:650–675

    Google Scholar 

  • Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136

    Article  Google Scholar 

  • Rode J, Drašlar K (1998) The structure of the digestive system of woodlouse Cylisticus convexus de Geer (Crustacea: Isopoda: Oniscoidea): hindgut and hepatopancreas. Acta Biol Slov 42:25–37

    Google Scholar 

  • Roldan BM, Shivers RR (1987) The uptake and storage of iron and lead in cells of the crayfish (Orconectes propinquus) hepatopancreas and antennal gland. Comp Biochem Physiol 86C:201–214

    CAS  Google Scholar 

  • Saborowski R (2015) Nutrition and digestion. In: Chang ES, Thiel M (eds) The natural history of the Crustacea. Vol 4: physiological regulation. Oxford University Press, New York, pp 285–319

    Google Scholar 

  • Santos EA, Nery LEM, Keller R, Gonçalves AA (1997) Evidence for the involvement of the crustacean hyperglycemic hormone in the regulation of lipid metabolism. Physiol Zool 70:415–420

    Article  CAS  PubMed  Google Scholar 

  • Schmitz EH (1992) Amphipoda. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates. Vol 9: Crustacea. Wiley-Liss, New York, pp 43–528

    Google Scholar 

  • Schram FR (1986) Crustacea. Oxford University Press, New York

    Google Scholar 

  • Schultz TW (1976) The ultrastructure of the hepatopancreatic caeca of Gammarus minus (Crustacea, Amphipoda). J Morphol 149:383–400

    Article  PubMed  Google Scholar 

  • Shechter A, Berman A, Singer A, Freiman A, Grinstein M, Erez J, Aflalo ED, Sagi A (2008) Reciprocal changes in calcification of the gastrolith and cuticle during the molt cycle of the red claw crayfish Cherax quadricarinatus. Biol Bull 214:122–134

    Article  CAS  PubMed  Google Scholar 

  • Skiebe P (2003) Neuropeptides in the crayfish stomatogastric nervous system. Microsc Res Tech 60:302–312

    Article  CAS  PubMed  Google Scholar 

  • Sonakowska L, Włodarczyk A, Poprawa I, Binkowski M, Śróbka J, Kamińska K, Kszuk-Jendrysik M, Chajec L, Zajusz B, Rost-Roszkowska MM (2015) Structure and ultrastructure of the endodermal region of the alimentary tract in the freshwater shrimp Neocaridina heteropoda (Crustacea, Malacostraca). PLoS One 10:e0126900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soroka Y, Milner Y, Sagi A (2000) The hepatopancreas as a site of yolk protein synthesis in the prawn Macrobrachium rosenbergii. Invert Reprod Dev 37:61–68

    Article  CAS  Google Scholar 

  • Spitzner F, Meth R, Krüger C, Nischik E, Eiler S, Sombke A, Torres G, Harzsch S (2018) An atlas of larval organogenesis in the European shore crab Carcinus maenas L. (Decapoda, Brachyura, Portunidae). Front Zool 15:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Stöcker W, Raeder U, Bijlholt MMC, Wichertjes T, van Bruggen EFJ, Markl J (1988) The quaternary structure of four crustacean two-hexameric hemocyanins: immunocorrelation, stoichiometry, reassembly and topology of individual subunits. J Comp Physiol B 158:271–289

    Article  Google Scholar 

  • Storch V (1982) Der Einfluß der Ernährung auf die Ultrastruktur der großen Zellen in den Mitteldarmdrüsen terrestrischer Isopoda (Armadillidium vulgare, Porcellio scaber). Zoomorphol 100:131–142

  • Storch V (1984) The influence of nutritional stress on the ultrastructure of the hepatopancreas of terrestrial isopods. Symp Zool Soc Lond 53:167–184

  • Storch V (1987) Microscopic anatomy and ultrastructure of the stomach of Porcellio scaber (Crustacea: Isopoda). Zoomorphol 106:301–311

    Article  Google Scholar 

  • Storch V, Anger K (1983) Influence of starvation and feeding on the hepatopancreas of larval Hyas araneus (Decapoda, Majidae). Helgol Meeresunters 36:67–75

    Article  Google Scholar 

  • Storch V, Štrus J (1989) Microscopic anatomy and ultrastructure of the alimentary canal in terrestrial isopods. Monit Zool Ital Monogr 4:105–126

    Google Scholar 

  • Storch V, Štrus J (2004) Comparative electron microscopic study of the stomach of Orchestia cavimana and Arcitalitrus sylvaticus (Crustacea: Amphipoda). J Morphol 259:340–346

    Article  PubMed  Google Scholar 

  • Storch V, Bluhm BA, Arntz WE (2001) Microscopic anatomy and ultrastructure of the digestive system of three Antarctic shrimps (Crustacea: Decapoda: Caridea). Polar Biol 24:604–614

    Article  Google Scholar 

  • Storch V, Štrus J, Brandt A (2002) Microscopic anatomy and ultrastructure of the digestive system of Natatolana obtusata (Vanhöffen, 1914) (Crustacea, Isopoda). Acta Zool 83:1–14

    Article  Google Scholar 

  • Stromberg JO (1964) On the embryology of the isopod Idotea. Arkiv för Zoologi 17:421–473

    Google Scholar 

  • Stromberg JO (1967) Segmentation and organogenesis in Limnoria lignorum (Rathke) (Isopoda). Arkiv för Zoologi 20:91–139

    Google Scholar 

  • Štrus J (1987) The effects of starvation on the structure and function of the hepatopancreas in the isopod Ligia italica. Inv Pesq 51:505–514

    Google Scholar 

  • Štrus J, Blejec A (2001) Microscopic anatomy of the integuments and digestive system in the moult cycle of Ligia italica (Oniscidea). In: Kensley B, Brusca RC (eds) Isopod systematics and evolution. AA Balkema, Rotterdam, pp 343–352

    Google Scholar 

  • Štrus J, Drašlar K (1988) Ultrastructural evidence of the midgut cells in the isopod Ligia italica (Isopoda: Crustacea). Inst Phys Conf Ser 93:149–150

    Google Scholar 

  • Štrus J, Storch V (1991) Moulting of the alimentary canal in Ligia italica Fab. and Porcellio scaber L. (Crustacea, Oniscoidea). In: Juchault P, Mocquard JP (ed) Proceedings of the Third International Symposium on the Biology of Terrestrial Isopods, Poitiers, pp. 189–194

  • Štrus J, Burkhardt P, Storch V (1985) The ultrastructure of the midgut glands in Ligia italica under different nutritional conditions. Helgol wiss Meeresunters 39:367–374

    Article  Google Scholar 

  • Štrus J, Drobne D, Ličar P (1995) Comparative anatomy and functional aspects of the digestive system in amphibious and terrestrial isopods (Isopoda: Oniscidea). In: Alikhan MA (ed) Terrestrial isopod biology. AA Balkema, Rotterdam, pp 15–23

    Google Scholar 

  • Štrus J, Klepal W, Repina J, Tušek-Žnidarič M, Milatovič M, Pipan Ž (2008) Ultrastructure of the digestive system and the fate of midgut during embryonic development in Porcellio scaber (Crustacea: Isopoda). Arthropod Struct Dev 37:287–298

    Article  PubMed  Google Scholar 

  • Suh H, Toda T, Hong S (1994) Ontogeny of foregut morphology in the euphausiid Euphausia pacifica. J Crust Biol 14:47–53

    Article  Google Scholar 

  • Szyfter Z (1966) The correlation of moulting and changes occurring in the hepatopancreas of Porcellio scaber Latr. (Crustacea, Isopoda). Bull Soc Amis Sci Lett Poznan 7:95–114

    Google Scholar 

  • Takahashi Y, Hishida S, Kittaka J (1994) Histological characteristics of fat bodies in the puerulus of the rock lobster Jasus edwardsii (Hutton, 1875) (Decapoda, Palinuridae). Crustaceana 66:318–325

    Article  Google Scholar 

  • Talbot P, Clark WH, Lawrence AL (1972) Fine structure of the midgut epithelium in the developing brown shrimp, Penaeus aztecus. J Morphol 138:467–485

    Article  PubMed  Google Scholar 

  • To TH, Brenner TL, Cavey MJ, Wilkens JL (2004) Histological organization of the intestine in the crayfish Procambarus clarkii. Acta Zool 85:119–130

    Article  Google Scholar 

  • Trevisan M, Leroy D, Decloux N, Thomee JP, Compere P (2014) Moult-related changes in the integument, midgut and digestive gland in the freshwater amphipod Gammarus pulex. J Crust Biol 34:539–551

    Article  Google Scholar 

  • Tziouveli V, Bastos-Gomez G, Bellwood O (2011) Functional morphology of mouthparts and digestive system during larval development of the cleaner shrimp Lysmata amboinensis (de Man, 1888). J Morphol 272:1080–1091

    Article  PubMed  Google Scholar 

  • Tzuc JT, Escalante DR, Herrera RR, Cortés GG, Ortiz MLA (2014) Microbiota from Litopenaeus vannamei: digestive tract microbial community of Pacific white shrimp. SpringerPlus 3:280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ullrich B, Storch V (1993) Development of the stomach in Euphausia superba Dana (Euphausiacea). J Crust Biol 13:423–431

    Article  Google Scholar 

  • Van den Oord A (1966) The biosynthesis of the emulsifiers of the crab Cancer pagurus L. Comp Biochem Physiol 17:715–718

    Article  PubMed  Google Scholar 

  • Vannier J, Liu J, Lerosey-Aubril R, Vinther J, Daley AC (2014) Sophisticated digestive systems in early arthropods. Nat Commun 5:3641

    Article  CAS  PubMed  Google Scholar 

  • Vernon GM, Herold L, Witkus ER (1974) Fine structure of the digestive tract epithelium in the terrestrial isopod Armadillidium vulgare. J Morphol 144:337–359

    Article  CAS  PubMed  Google Scholar 

  • Vogt G (1985) Histologie und Cytologie der Mitteldarmdrüse von Penaeus monodon (Decapoda). Zool Anz 215:61–80

    Google Scholar 

  • Vogt G (1993) Differentiation of B-cells in the hepatopancreas of the prawn Penaeus monodon. Acta Zool 74:51–60

    Article  Google Scholar 

  • Vogt G (1994) Life-cycle and functional cytology of the hepatopancreatic cells of Astacus astacus (Crustacea, Decapoda). Zoomorphol 114:83–101

    Article  Google Scholar 

  • Vogt G (2002) Functional anatomy. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 53–151

    Google Scholar 

  • Vogt G (2008a) Investigation of hatching and early post-embryonic life of freshwater crayfish by in vitro culture, behavioral analysis, and light and electron microscopy. J Morphol 269:790–811

    Article  PubMed  Google Scholar 

  • Vogt G (2008b) The marbled crayfish: a new model organism for research on development, epigenetics and evolutionary biology. J Zool 276:1–13

    Article  Google Scholar 

  • Vogt G, Quinitio ET (1994) Accumulation and excretion of metal granules in the prawn, Penaeus monodon, exposed to water-borne copper, lead, iron and calcium. Aquat Toxicol 28:223–241

    Article  CAS  Google Scholar 

  • Vogt G, Štrus J (1998) Diseases of the shrimp Palaemon elegans (Crustacea, Decapoda) in the Bay of Piran, Adriatic Sea. J Nat Hist 32:1795–1806

    Article  Google Scholar 

  • Vogt G, Štrus J (1999) Hypogean life-style fuelled by oil. Naturwiss 86:43–45

    Article  CAS  Google Scholar 

  • Vogt G, Storch V, Quinitio ET, Pascual FP (1985) Midgut gland as monitor organ for the nutritional value of diets in Penaeus monodon (Decapoda). Aquaculture 48:1–12

    Article  Google Scholar 

  • Vogt G, Stöcker W, Storch V, Zwilling R (1989a) Biosynthesis of Astacus protease, a digestive enzyme from crayfish. Histochem 91:373–381

    Article  CAS  Google Scholar 

  • Vogt G, Quinitio ET, Pascual FP (1989b) Interaction of the midgut gland and the ovary in vitellogenesis and consequences for the breeding success: a comparison of unablated and ablated spawners of Penaeus monodon. In: De Pauw N, Jaspers E, Ackefors H, Wilkins N (eds) Aquaculture – a biotechnology in progress. European Aquaculture Society, Bredene, pp 581–592

    Google Scholar 

  • Wägele J-W (1992) Isopoda. In: Harison FW, Humes AG (eds) Microscopic anatomy of invertebrates. Vol 9: Crustacea. Wiley-Liss, New York, pp 529–617

    Google Scholar 

  • Wägele J-W, Welsch U, Müller W (1981) Fine structure and function of the digestive tract of Cyathura carinata (Krøyer) (Crustacea, Isopoda). Zoomorphol 98:69–88

    Article  Google Scholar 

  • Wang YC, Chang PS, Chen HY (2007) Tissue expressions of nine genes important to immune defence of the Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 23:1161–1177

    Article  CAS  PubMed  Google Scholar 

  • Warburg MR (1987) Isopods and their terrestrial environment. Adv Ecol Res 17:187–242

    Article  Google Scholar 

  • Warburg MR, Rosenberg M (1989) Ultracytochemical identification of NA+, K+-ATPase activity in the isopodan hindgut epithelium. J Crust Biol 9:525–528

    Article  Google Scholar 

  • Watling L (2013) Feeding and digestive system. In: Watling L, Thiel M (eds) The natural history of the Crustacea. Vol 1: functional morphology and diversity. Oxford University Press, New York, pp 237–260

    Chapter  Google Scholar 

  • Wieser W (1966) Cooper and the role of isopods in degradation of organic matter. Science 153:67–69

    Article  CAS  PubMed  Google Scholar 

  • Wieser W, Klima J (1969) Compartmentalization of copper in the hepatopancreas of isopods. Mikroskopie 24:1–9

    CAS  PubMed  Google Scholar 

  • Wolfe SH, Felgenhauer BE (1991) Mouthpart and foregut ontogeny in larval, postlarval, and juvenile spiny lobster, Panulirus argus Latreille (Decapoda, Palinuridae). Zool Scr 20:57–75

    Article  Google Scholar 

  • Wolff C (2009) The embryonic development of the malacostracan crustacean Porcellio scaber (Isopoda, Oniscidea). Dev Genes Evol 219:545–564

    Article  PubMed  Google Scholar 

  • Zhang N, Song C, Wang M, Liu Y, Hui M, Cui Z (2017) Diversity and characterization of bacteria associated with the deep-sea hydrothermal vent crab Austinograea sp. comparing with those of two shallow-water crabs by 16S ribosomal DNA analysis. PLoS One 12:e0187842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda: Oniscidea): an evolutionary-ecological approach. Biol Rev 77:455–493

    Article  PubMed  Google Scholar 

  • Zimmer M, Topp W (1998) Microorganisms and cellulose digestion in the gut of the woodlouse Porcellio scaber. J Chem Ecol 24:1397–1408

    Article  CAS  Google Scholar 

  • Žnidaršič N, Štrus J, Drobne D (2003) Ultrastructural alterations of the hepatopancreas in Porcellio scaber under stress. Environ Toxicol Pharmacol 13:161–174

    Article  CAS  PubMed  Google Scholar 

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This work was supported and financed by the Slovenian Research Agency (ARRS), MR grants Nos. 1000-11-310087 and 1000-15-0510 and the research program Integrative Zoology and Speleobiology No. P1-0184.

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Štrus, J., Žnidaršič, N., Mrak, P. et al. Structure, function and development of the digestive system in malacostracan crustaceans and adaptation to different lifestyles. Cell Tissue Res 377, 415–443 (2019). https://doi.org/10.1007/s00441-019-03056-0

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