The brain in three crustaceans from cavernous darkness

BMC Neuroscience

Christian S Wirkner²  Stefan Richter²  Thomas M Iliffe³  Torben Stemme¹  Martin EJ Stegner² 

[1] Division of Cell Biology, University of Veterinary Medicine Hannover, Bischhofsholer Damm 15, Hannover, 30173, Germany;Allgemeine und Spezielle Zoologie, Institut für Biowissenschaften, Universität Rostock, Universitätsplatz 2, Rostock, 18055, Germany;Department of Marine Biology, Texas A&M University at Galveston, 200 Seawolf Parkway, Galveston 77553, TX, USA

关键词: Mechanosensory neuropil;    Ventral nerve cord;    Olfactory lobe;    Olfactory globular tract;    Neurophylogeny;    Hemiellipsoid body;    Central complex;    Optic neuropil;   

Others  :  1170537
DOI  :  10.1186/s12868-015-0138-6

 received in 2014-03-28, accepted in 2015-01-08,  发布年份 2015

【 摘 要 】

Background

While a number of neuroanatomical studies in other malacostracan taxa have recently contributed to the reconstruction of the malacostracan ground pattern, little is known about the nervous system in the three enigmatic blind groups of peracarids from relict habitats, Thermosbaenacea, Spelaeogriphacea, and Mictocarididae. This first detailed description of the brain in a representative of each taxon is largely based on a combination of serial semi-thin sectioning and computer-aided 3D-reconstructions. In addition, the mictocaridid Mictocaris halope was studied with a combination of immunolabeling (tubulin, nuclear counter-stains) and confocal laser scanning microscopy, addressing also the ventral nerve cord.

Results

Adjacent to the terminal medulla, all three representatives exhibit a distal protocerebral neuropil, which is reminiscent of the lobula in other Malacostraca, but also allows for an alternative interpretation in M. halope and the thermosbaenacean Tethysbaena argentarii. A central complex occurs in all three taxa, most distinctively in the spelaeogriphacean Spelaeogriphus lepidops. The deutocerebral olfactory lobe in M. halope and S. lepidops is large. The comparably smaller olfactory lobe in T. argentarii appears to be associated with a unique additional deutocerebral neuropil. A small hemiellipsoid body exists only in the protocerebrum of T. argentarii. Distinctive mechanosensory neuropils corresponding to other malacostracans are missing.

Conclusions

The considerable reduction of the optic lobe in the studied taxa is higher than in any other blind malacostracan. The large size of deutocerebral olfactory centers implies an important role of the olfactory sense. The presence of a distinctive central complex in the blind S. lepidops adds further support to a central-coordinating over a visual function of this structure. The lack of a hemiellipsoid body in M. halope and S. lepidops suggests that their terminal medulla takes over the function of a second order olfactory center completely, as in some other peracarids. The reduction of the optic lobe and hemiellipsoid body is suggested to have occurred several times independently within Peracarida. The missing optic sense in the studied taxa is not correlated with an emphasized mechanosense.

【 授权许可】

   
2015 Stegner et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Richter S, Scholtz G: Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 2001, 39:113-36.
• [2]Bowman TE, Garner SP, Hessler RR, Iliffe TM, Sanders HL: Mictacea, a new order of Crustacea Peracarida. J Crustacean Biol 1985, 5:74-8.
• [3]Martin JW, Davis GE: An updated classification of the recent Crustacea. Nat Hist Mus Los Angel Cty, Sci Ser 2001, 39:1-124.
• [4]Poore GCB: Peracarida: monophyly, relationships and evolutionary success. Nauplius 2005, 13:1-27.
• [5]Gutu M: Spelaeogriphacea and Mictacea (partim) suborders of a new order, Cosinzeneacea (Crustacea, Peracarida). Trav Mus Hist Nat ‘Grigore Antipa’ 1998, 40:121-9.
• [6]Gutu M, Iliffe TM: Description of a new hirsutiid (n.g., n.sp.) and reassignment of this family from Order Mictacea to the new Order, Bochusacea (Crustacea, Peracarida). Trav Mus Hist Nat ‘Grigore Antipa’ 1998, 40:93-120.
• [7]Wagner G: A monographic review of the Thermosbaenacea (Crustacea: Peracarida). A study on their morphology, taxonomy, phylogeny and biogeography. Nationaal Natuurhistorisch Museum Leiden, Leiden; 1994.
• [8]Wirkner CS, Richter S: Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 2010, 26:143-67.
• [9]Holmgren N: Zur Vergleichenden Anatomie des Gehirns von Polychaeten. Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Vorstudien zu einer Phylogenie der Arthropoden. Kungl Svenska Vetenskapsakad Handl 1916, 56:1-303.
• [10]Hanström B: Vergleichende Anatomie des Nervensystems der wirbellosen Tiere unter Berücksichtigung seiner Funktion. Springer Verlag, Berlin; 1928.
• [11]Hanström B: The brain, the sense organs, and the incretory organs of the head in the Crustacea Malacostraca. Kungliga Fysiografiska Sallskapets Handlingar N F 1947, 58:1-44.
• [12]Loesel R, Nässel DR, Strausfeld NJ: Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 2002, 31:77-91.
• [13]Beltz BS, Kordas K, Lee MM, Long JB, Benton JL, Sandeman DC: Ecological, evolutionary, and functional correlates of sensilla number and glomerular density in the olfactory system of decapod crustaceans. J Comp Neurol 2003, 455:260-9.
• [14]Harzsch S: Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Struct Dev 2003, 32:17-37.
• [15]Harzsch S: Neurophylogeny: Architecture of the nervous system and a fresh view on arthropod phylogeny. Integr Comp Biol 2006, 46:182-94.
• [16]Harzsch S: The architecture of the nervous system provides important characters for phylogenetic reconstructions: examples from the Arthropoda. Species, Phylogeny Evol 2007, 1:33-57.
• [17]Schachtner J, Schmidt M, Homberg U: Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struc Dev 2005, 34:257-99.
• [18]Strausfeld NJ: Brain organization and the origin of insects: an assessment. Proc Biol Sci 2009, 276:1929-37.
• [19]Harzsch S, Hansson BS: Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci 2008, 9:58.
• [20]Krieger J, Sandeman RE, Sandeman DC, Hansson BS, Harzsch S: Brain architecture of the largest living land arthropod, the giant robber crab Birgus latro (Crustacea, Anomura, Coenobitidae): evidence for a prominent central olfactory pathway? Front Zool 2010, 7:25.
• [21]Krieger J, Sombke A, Seefluth F, Kenning M, Hansson BS, Harzsch S: Comparative brain architecture of the European shore Crab Carcinus maenas (Brachyura) and the Common hermit Crab Pagurus bernhardus (Anomura). Cell Tissue Res 2012, 348:47-69.
• [22]Kenning M, Müller C, Wirkner CS, Harzsch S: The Malacostraca (Crustacea) from a neurophylogenetic perspective: new insights from brain architecture in Nebalia herbstii Leach, 1814 (Leptostraca, Phyllocarida). Zool Anz J Comp Zool 2013, 252:319-36.
• [23]Sullivan JM, Beltz BS: Evolutionary changes in the olfactory projection neuron pathways of eumalacostracan crustaceans. J Comp Neurol 2004, 470:25-38.
• [24]Sandeman D, Scholtz G: Ground plans, evolutionary changes, and homologies in decapod crustacean brains. In The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. Edited by Breidbach O, Kutsch W. Birkhäuser, Basel; 1995:329-347.
• [25]Johansson KUI, Hallberg E: The organization of the olfactory lobes in Euphausiacea and Mysidacea (Crustacea, Malacostraca). Zoomorphology 1992, 112:81-9.
• [26]Moreau X, Benzid D, De Jong L, Barthélémy RM, Casanova JP: Evidence for the presence of serotonin in Mysidacea (Crustacea, Peracarida) as revealed by fluorescence immunohistochemistry. Cell Tissue Res 2002, 310:359-71.
• [27]Hanström B: Neue Untersuchungen über Sinnesorgane und Nervensystem der Crustaceen.II. Zool Jahrb Abt Anat Ontog Tiere 1933, 56:387-520.
• [28]Oelze A: Beiträge zur Anatomie von Diastylis rathkei. Zool Jahrb Abt Anat Ontog Tiere 1931, 54:235-94.
• [29]Stegner MEJ, Fritsch M, Richter S: The central complex in Crustacea. In Deep Metazoan Phylogeny: The backbone of the Tree of Life. Edited by Wägele JW, Bartholomäus T. De Gruyter, Berlin; 2014:361-84.
• [30]Strausfeld NJ: Evolution of Crustacean Optic Lobes and Origins of Chiasmata. Arthropod Struct Dev 2005, 34:235-56.
• [31]Harzsch S, Rieger V, Krieger J, Seefluth F, Strausfeld NJ, Hansson BS: Transition from marine to terrestrial ecologies: changes in olfactory and tritocerebral neuropils in land-living isopods. Arthropod Struct Dev 2011, 40:244-57.
• [32]Kenning M, Harzsch S: Brain anatomy of the marine isopod Saduria entomon Linnaeus, 1758 (Valvifera, Isopoda) with special emphasis on the olfactory pathway. Front Neuroanat 2013, 7:32.
• [33]Henry L: The nervous system and the segmentation of the head in the Annulata. Section IV Arthropoda. Microentomol 1948, 13:1-23.
• [34]Ungerer P, Geppert M, Wolff C: Axogenesis in the central and peripheral nervous system of the amphipod crustacean Orchestia cavimana. Integr Zool 2011, 6:28-44.
• [35]Wirkner CS, Richter S: The circulatory system and its spatial relations to other major organ systems in Spelaeogriphacea and Mictacea (Malacostraca, Crustacea) – a three-dimensional analysis. Zool J Linn Soc 2007, 149:629-42.
• [36]Wirkner CS, Richter S: The hemolymph vascular system in Tethysbaena argentarii (Thermosbaenacea, Monodellidae) as revealed by 3D reconstruction of semi-thin sections. J Crustacean Biol 2009, 29:13-7.
• [37]Bowman TE, Iliffe TM: Mictocaris halope, a new unusual peracaridan crustacean from marine caves on Bermuda. J Crustacean Biol 1985, 5:58-73.
• [38]Gordon I: On Spelaeogriphus, a new cavernicolous crustacean from South Africa. Bull br Mus nat Hist Zool 1957, 5:31-47.
• [39]Wagner HP: A monographic review of the Thermosbaenacea (Crustacea: Peracarida) – A study on their morphology, taxonomy, phylogeny and biogeography. Zool Verhand 1994, 291:3-338.
• [40]Monod T, Cals P: Ordre des Thermosbaenacés (Thermosbaenacea Monod, 1927). In Traité de Zoologie. Anatomie, Systématique, Biologie. Tome VII, Fascicule IIIA, Crustacés Péracarides. Edited by Forest J. Mémoires de l’Institut Océanographique Fondation Albert Ier, Prince de Monaco 19, Paris; 1999:11-34.
• [41]Jaume D: Global diversity of spelaeogriphaceans & thermosbaenaceans (Crustacea; Spelaeogriphacea & Thermosbaenacea) in freshwater. Hydrobiologia 2008, 595:219-24.
• [42]Harzsch S: Phylogenetic significance of the crustacean optic neuropils and chiasmata: a re-examination. J Comp Neurol 2002, 453:10-21.
• [43]Strausfeld NJ: Arthropod Brains: Evolution, Functional Elegance, and Historical Significance. Harvard University Press, Cambridge, London; 2012.
• [44]Homberg U: Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 2008, 37:347-62.
• [45]Loesel R, Richter S: Neurophylogeny - from description to character analysis. In Deep Metazoan Phylogeny: The backbone of the Tree of Life. Edited by Wägele JW, Bartholomäus T. De Gruyter, Berlin; 2014:505-14.
• [46]Schram FR, Hof CHJ: Fossils and the interrelationships of major crustacean groups. In Arthropod Fossils and Phylogeny. Edited by Edgecombe GD. Columbia University Press, New York; 1998:233-302.
• [47]Wills MA: A phylogeny of recent Crustacea derived from morphological characters. In Arthropod Relationships. Edited by Fortey RA, Thomas RH. Chapman and Hall, London; 1998:189-209.
• [48]Siewing R: Untersuchungen zur Morphologie der Malacostraca (Crustacea). Zool Jahrb Abt Anat Ontog Tiere 1956, 75:39-176.
• [49]Ax P: Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik. Stuttgart, Jena, Lübeck, Ulm, Gustav Fischer Verlag; 1999.
• [50]Watling L: Towards understanding the relationship of the peracaridan orders: the necessity of determing exact homologies. In Crustaceans and the Biodiversity Crisis. Proceedings of the Fourth International Crustacean Congress. Edited by Schram FR, Vaupel Klein JC. Brill, Leiden; 1999:73-89.
• [51]Meland K, Willassen E: The disunity of “Mysidacea” (Crustacea). Mol Phylogenet Evol 2007, 44:1083-104.
• [52]Jenner RA, Ní Dhubhghaill C, Ferla MP, Wills MA: Eumalacostracan phylogeny and total evidence: limitations of the usual suspects. BMC Evol Biol 2009, 9:21.
• [53]Sombke A, Harzsch S, Hansson BS: Organization of deutocerebral neuropils and olfactory behavior in the centipede Scutigera coleoptrata (Linnaeus, 1758) (Myriapoda: Chilopoda). Chem Senses 2011, 36:43-61.
• [54]Stegner MEJ, Richter S: Morphology of the brain in Hutchinsoniella macracantha (Cephalocarida, Crustacea). Arthropod Struct Dev 2011, 40:221-43.
• [55]Sandeman DC, Sandeman RE, Derby C, Schmidt M: Morphology of the brain of crayfish, crabs, and spiny lobsters - a common nomenclature for homologous structures. Biol Bull 1992, 183:304-26.
• [56]Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, et al.: Invertebrate neurophylogeny - suggested terms and definitions for a neuroanatomical glossary. Front Zool 2010, 7:29.
• [57]Stella E: Monodella argentarii n. sp. di Thermosbaenacea (Crustacea Peracarida) limnotroglobio di Monte Argentario. Arch Zool Ital 1951, 36:1-15.
• [58]Sandeman DC, Scholtz G, Sandeman RE: Brain evolution in decapod Crustacea. J Exp Zool 1993, 265:112-33.
• [59]Huckstorf K, Wirkner CS: Comparative morphology of the hemolymph vascular system in Krill (Euphausiacea; Crustacea). Arthropod Struct Dev 2011, 40:39-53.
• [60]Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ: Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 2003, 467:150-72.
• [61]Elofsson R, Hessler RR: Central nervous system of Hutchinsoniella macracantha (Cephalocarida). J Crustacean Biol 1990, 10:423-39.
• [62]Fanenbruck M, Harzsch S, Wägele JW: The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc Natl Acad Sci U S A 2004, 101:3868-73.
• [63]Brenneis G, Richter S: Architecture of the nervous system in Mystacocarida (Arthropoda, Crustacea) - an immunohistochemical study and 3D-reconstruction. J Morphol 2010, 271:169-89.
• [64]Culver DC, Wilkens H: Critical review of the relevant theories of the evolution of subterranean animals. In Ecosystems of the world. Vol. 30, Subterranean ecosystems. Edited by Wilkens H, Culver DC, Humphreys WF. Elsevier, Amsterdam; 2001:381-98.
• [65]Stemme T, Eickhoff R, Bicker G: Olfactory projection neuron pathways in two species of marine Isopoda (Peracarida, Malacostraca, Crustacea). Tissue Cell 2014, 46:260-3.
• [66]Fanenbruck M, Harzsch S: A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct Dev 2005, 34:343-78.
• [67]Stemme T, Iliffe TM, Bicker G, Harzsch S, Koenemann S: Serotonin immunoreactive interneurons in the brain of the Remipedia: new insights into the phylogenetic affinities of an enigmatic crustacean taxon. BMC Evol Biol 2012, 12:168.
• [68]Harzsch S, Dircksen H, Beltz BS: Development of pigment-dispersing hormone-immunoreactive neurons in the American lobster: homology to the insect circadian pacemaker system? Cell Tissue Res 2009, 335:417-29.
• [69]Friedrich M: Biological clocks and visual systems in cave-adapted animals at the dawn of speleogenomics. Integr Comp Biol 2013, 53:50-67.
• [70]Pfeiffer K, Homberg U: Organization and functional roles of the central complex in the insect brain. Annu Rev Entomol 2014, 59:165-84.
• [71]Utting M, Agricola H, Sandeman RE, Sandeman DC: Central complex in the brain of crayfish and its possible homology with that of insects. J Comp Neurol 2000, 416:245-61.
• [72]Thompson KS, Zeidler MP, Bacon JP: Comparative anatomy of serotonin-like immunoreactive neurons in isopods: putative homologues in several species. J Comp Neurol 1994, 347:553-69.
• [73]Boyan G, Reichert H: Mechanisms for complexity in the brain: generating the insect central complex. Trends Neurosci 2011, 34:247-57.
• [74]Langworthy K, Helluy S, Benton J, Beltz BS: Amines and peptides in the brain of the American lobster: immunocytochemical localization patterns and implications for brain function. Cell Tissue Res 1997, 288:191-206.
• [75]Boyan G, Reichert H, Hirth F: Commissure formation in the embryonic insect brain. Arthropod Struct Dev 2003, 32:61-77.
• [76]Ammar D, Nazari EM, Rauh Müller YM, Allodi S: New insights on the olfactory lobe of decapod crustaceans. Brain Behav Evol 2008, 72:27-36.
• [77]Sullivan JM, Beltz BS: Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans. J Comp Neurol 2001, 441:9-22.
• [78]Wolff G, Harzsch S, Hansson BS, Brown S, Strausfeld N: Neuronal organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus: correspondence with the mushroom body ground pattern. J Comp Neurol 2012, 520:2824-46.
• [79]Bellonci G: Nuove ricerche sulla struttura del ganglio ottico della Squilla mantis. Mem D Accad d Sc d Ist di Bologna Ser. 4, T. 3 1882, 419-426.
• [80]Hanström B: Neue Untersuchungen der Sinnesorgane und Nervenzentren der Crustaceen. I. Zool Jahrb Abt Anat Ontog Tiere 1931, 23:80-236.
• [81]Sandeman DC, Okajima A: Statocyst-induced eye movement in the crab Scylla serrata. I. The sensory input from the statocyst. J Exp Biol 1972, 57:187-204.
• [82]Fraser PJ: Interneurones in crab connectives (Carcinus maenas (L.)): directional statocyst fibres. J Exp Biol 1974, 61:615-28.
• [83]Sandeman DC, Denburg JL: The central projections of chemoreceptor axons in the crayfish revealed by axoplasmic transport. Brain Res 1976, 115:492-6.
• [84]Yoshino M, Kondoh Y, Hisada M: Projections of the statocyst sensory neurons associated with crescent hairs in the crayfish, Procambarus clarkii Girard. Cell Tissue Res 1983, 230:37-48.
• [85]Roye DB: The central distribution of movement sensitive afferent fibers from the antennular short hair sensilla of Callinectes sapidus. Mar Behav Physiol 1986, 12:181-96.
• [86]Blaustein DN, Derby CD, Simmons RB, Beall AC: Structure of the brain and medulla terminalis of the spiny lobster Panulirus argus and the crayfish Procambarus clarkii, with an emphasis on olfactory centers. J Crustacean Biol 1988, 8:493-519.
• [87]Schmidt M, Ache BW: Antennular projections to the midbrain of the spiny lobster. III. Central arborizations of motoneurons. J Comp Neurol 1993, 336:583-94.
• [88]Derby CD, Fortier JK, Harrison PJ, Cate HS: The peripheral and central antennular pathway of the Caribbean stomatopod crustacean Neogonodactylus oerstedii. Arthropod Struct Dev 2003, 32:175-88.
• [89]Tautz J, Müller-Tautz R: Antennal neuropile in the brain of the crayfish: morphology of neurons. J Comp Neurol 1983, 218:415-25.
• [90]Fryer G: Studies on the functional morphology and feeding mechanisms of Monodella argentarii (Thermosbaenacea). Trans R Soc Edin 1964, 66:49-90.
• [91]Stella E: Sur Monodella argentarii Stella, espèce de Crustacé Thermosbenacé des eaux d’une grotte de l’Italie centrale (Monte Argentario, Toscana). Hydrobiologia 1953, V:226-332.
• [92]Mulloney B, Tschuluun N, Hall WM: Architectonics of crayfish ganglia. Microsc Res Tech 2003, 60:253-65.
• [93]Harzsch S, Sandeman DC, Chaigneau J: Morphology and development of the central nervous system. In Treatise on Zoology – Anatomy, Taxonomy, Biology. The Crustacea. Edited by Forest J, Vaupel Klein JC. Brill, Leiden; 2012:9-236.
• [94]Bouvier EL: Le système nerveux des crustacés décapodes et ses rapports avec l’appareil circulatoire. Dissertation, École supéricure de pharmacie de Paris; 1889.
• [95]Sandeman DC: Vascular circulation in the brain, optic lobes and thoracic ganglion of the crab Carcinus. Proc Roy Soc B 1967, 168:82-90.
• [96]Keiler J, Richter S, Wirkner CS: Evolutionary morphology of the hemolymph vascular system in hermit and king crabs (Crustacea: Decapoda: Anomala). J Morph 2013, 274:759-78.
• [97]Claus C: Über den Organismus der Nebaliden und die systematische Stellung der Leptostraken. Arbeiten aus dem zoologischen Institut der Universität Wien und der zoologischen Station Triest 1888, 8:1-148.
• [98]Manton SM: On the embryology of the crustacean Nebalia bipes. Philos Trans R Soc Lond B Biol Sci 1934, 223:163-238.
• [99]Ando H, Kuwasawa K: Neuronal and neurohormonal control of the heart in the stomatopod crustacean, Squilla oratoria. J Exp Biol 2004, 207:4663-77.
• [100]Schmitz EH: Anatomy of the central nervous system of Armadillidium vulgare (Latreille) (Isopoda). J Crustacean Biol 1989, 9:217-27.
• [101]Kreissl S, Weiss T, Djokaj S, Balezina O, Rathmayer W: Allatostatin modulates skeletal muscle performance in crustaceans through pre- and postsynaptic effects. Eur J Neurosci 1999, 11:2519-30.
• [102]Chaudonneret J: La phylogenèse du système nerveux annélido-arthropodien. Bull Soc Zool France 1978, 103:69-95.
• [103]Bullock TH, Horridge GA: Structure and Function in the Nervous Systems of Invertebrates. W.H. Freeman and Company, San Francisco; 1965.
• [104]Schneider H, Trimmer BA, Rapus J, Eckert M, Valentine DE, Kravitz EA: Mapping of octopamine-immunoreactive neurons in the central nervous system of the lobster. J Comp Neurol 1993, 329:129-42.
• [105]Sombke A, Rosenberg J, Hilken G: Chilopoda – Nervous system. In Treatise on Zoology – Anatomy, Taxonomy, Biology. The Myriapoda. Edited by Minelli A. Brill, Boston; 2011:217-34.
• [106]Stegner MEJ, Brenneis G, Richter S: The ventral nerve cord of Cephalocarida (Crustacea): New insights into the ground pattern of Tetraconata. J Morphol 2014, 275:269-94.
• [107]Manton S: On some points in the anatomy and habits of the lophogastrid Crustacea. T Roy Soc Edin-Earth 1928, 56:103-19.
• [108]Manton S: On the embryology of a mysid crustacean, Hemimysis lamornae. Philos Trans R Soc Lond B Biol Sci 1928, 216:363-463.
• [109]Hickman VV. The embryology of the syncarid crustacean, Anaspides tasmaniae. Papers and Proceedings of the Royal Society of Tasmania 1937, 1-35.
• [110]Chaudonneret J: Remarques sur le système nerveux des derniers segments thoraciques de la Squille (Crustacé Stomatopode). Ann Sci Nat Zool 1957, 19:225-32.
• [111]Chaudonneret J: Le système nerveux de la région gnathale de l’écrivisse Cambarus affinis (Say). Ann Sci Nat Zool 1956, 18:33-61.
• [112]Delaleu JC: Le système nerveux intrapéricardique et ses relations avec le système nerveux central chez trois Oniscoides: Porcellio dilatatus (B.), Helleria brevicornis (E.) et Ligia oceanica (L.). Bull Soc Zool Fr 1970, 95:201-10.
• [113]Demassieux C: Le système neurosécréteur du Crustacé Isopode Asellus aquaticus (Linné). Crustaceana 1979, 37:71-9.
• [114]Weiss T, Kreissl S, Rathmayer W: Localization of a FMRFamide-related peptide in efferent neurons and analysis of neuromuscular effects of DRNFLRFamide (DF2) in the crustacean Idotea emarginata. Eur J Neurosci 2003, 17:239-48.
• [115]Kirsch R, Richter S: The nervous system of Leptodora kindtii (Branchiopoda, Cladocera) surveyed with confocal scanning microscopy (CLSM), including general remarks on the branchiopod neuromorphological ground pattern. Arthropod Struct Dev 2007, 36:143-56.
• [116]Stegner MEJS, Richter S. Development of the nervous system in Cephalocarida (Crustacea): early neuronal differentiation and successive patterning. Zoomorphology, in press.
• [117]Legendre R: Contribution à l’étude du système nerveux des Aranéides. Ann Sci Nat Zool 1959, 1:339-473.
• [118]Fritsch M, Richter S: The formation of the nervous system during larval development in Triops cancriformis (Bosc) (Crustacea, Branchiopoda): an immunohistochemical survey. J Morphol 2010, 271:1457-81.
• [119]Harzsch S, Anger K, Dawirs RR: Immunocytochemical detection of acetylated alpha-tubulin and Drosophila synapsin in the embryonic crustacean nervous system. Int J Dev Biol 1997, 41:477-84.
• [120]Stemme T, Iliffe TM, von Reumont BM, Koenemann S, Harzsch S, Bicker G: Serotonin-immunoreactive neurons in the ventral nerve cord of Remipedia (Crustacea): support for a sister group relationship of Remipedia and Hexapoda? BMC Evol Biol 2013, 13:119.