Cell and Tissue Research

, Volume 348, Issue 1, pp 47–69 | Cite as

Comparative brain architecture of the European shore crab Carcinus maenas (Brachyura) and the common hermit crab Pagurus bernhardus (Anomura) with notes on other marine hermit crabs

  • Jakob KriegerEmail author
  • Andy Sombke
  • Florian Seefluth
  • Matthes Kenning
  • Bill S. Hansson
  • Steffen Harzsch
Regular Article


The European shore crab Carcinus maenas and the common hermit crab Pagurus bernhardus are members of the sister taxa Brachyura and Anomura (together forming the taxon Meiura) respectively. Both species share similar coastal marine habitats and thus are confronted with similar environmental conditions. This study sets out to explore variations of general brain architecture of species that live in seemingly similar habitats but belong to different major malacostracan taxa and to understand possible differences of sensory systems and related brain compartments. We examined the brains of Carcinus maenas, Pagurus bernhardus, and three other hermit crab species with immunohistochemistry against tyrosinated tubulin, f-actin, synaptic proteins, RF-amides and allatostatin. Our comparison showed that their optic neuropils within the eyestalks display strong resemblance in gross morphology as well as in detailed organization, suggesting a rather similar potential of processing visual input. Besides the well-developed visual system, the olfactory neuropils are distinct components in the brain of both C. maenas and P. bernhardus as well as the other hermit crabs, suggesting that close integration of olfactory and visual information may be useful in turbid marine environments with low visibility, as is typical for many habitats such as, e.g., the Baltic and the North Sea. Comparing the shape of the olfactory glomeruli in the anomurans showed some variations, ranging from a wedge shape to an elongate morphology. Furthermore, the tritocerebrum and the organization of the second antennae associated with the tritocerebrum seem to differ markedly in C. maenas and P. bernhardus, indicating better mechanosensory abilities in the latter close to those of other Decapoda with long second antennae, such as Astacida, Homarida, or Achelata. This aspect may also represent an adaptation to the “hermit lifestyle” in which competition for shells is a major aspect of their life history. The shore crab C. maenas, on the other hand seems to rely much less on mechanosensory information mediated by the second antennae but in water, the visual and the olfactory senses seem to be the most important modalities.


Nervous system Crustaceans Immunohistochemistry Neuroanatomy Olfaction 



We are indepted to Erich Buchner (Würzburg) for the kind provision of the SYNORF1 synapsin antibody. We wish to thank Hans Agricola (Friedrich Schiller University Jena) for the allatostatin antiserum and Verena Rieger (Greifswald) for providing the photograph of Carcinus maenas. The authors are grateful for the assistance of Gilles Maron and Franck Gentil at the Station Biologique de Roscoff in France for provision of Pagurus bernhardus and for their general support. We would like to express our gratitude to Guido Dehnhardt and the staff of the Marine Science Center in Rostock for free provision of diving equipment and the permission to sample Carcinus maenas on-site. We cordially thank C. H. G. Müller (Greifswald) for providing specimens of the marine anomurans of the Mediterranean Calcinus tubularis, Clibanarius eythropus and Diogenes pugilator from the island of Ibiza. David C. Sandeman is acknowledged for kindly commenting on this paper.


  1. Abbott NJ (1971) The organization of the cerebral ganglion in the shore crab, Carcinus maenas. Cell Tissue Res 120:401–419Google Scholar
  2. Ache BW, Derby CD (1985) Functional organization of olfaction in crustaceans. Trends Neurosci 8:356–360CrossRefGoogle Scholar
  3. Bamber SD, Naylor E (1996) Mating behaviour of male Carcinus maenas in relation to a putative sex pheromone: behavioural changes in response to antennule restriction. Mar Biol 125:483–488Google Scholar
  4. Beltz BS, Kordas K, Lee MM, Long JB, Benton JL (2003) Ecological, evolutionary, and functional correlates of sensilla number and glomerular density in the olfactory system of decapod crustaceans. J Comp Neurol 455:260–269PubMedCrossRefGoogle Scholar
  5. Berrill M (1982) The life cycle of the green crab Carcinus maenas at the northern end of its range. J Crust Biol 2:31–39CrossRefGoogle Scholar
  6. Bethe A (1897a) Das Nervensystem von Carcinus maenas, ein anatomisch–physiologischer Versuch I. Theil I. Arch Mikrosk Anat 50:460–546CrossRefGoogle Scholar
  7. Bethe A (1897b) Das Centralnervensystem von Carcinus maenas. Ein anatomisch–physiologischer Versuch I. Theil II. Arch Mikrosk Anat 50:589–639CrossRefGoogle Scholar
  8. Bethe A (1898) Das Centralnervensystem von Carcinus maenas. Ein anatomisch–physiologischer Versuch. II. Theil. Arch Mikrosk Anat 51:382–452CrossRefGoogle Scholar
  9. Borradaile LA (1916) Crustacea. I. Decapoda II. Porcellanopagurus; an instance of carcinization. British Antarctic Terra Nova Expedition. 1910. Brit Mus (Nat Hist) Report Zoology 3:75–126Google Scholar
  10. Cape SS, Rehm KJ, Ma M, Marder E, Li L (2008) Mass spectral comparison of the neuropeptide complement of the stomatogastric ganglion and brain in the adult and embryonic lobster, Homarus americanus. J Neurochem 105:690–702PubMedCrossRefGoogle Scholar
  11. Case J, Gwilliam G (1961) Amino acid sensitivity of the dactyl chemoreceptors of Carcinides maenas. Biol Bull 121:449–455CrossRefGoogle Scholar
  12. Christie AE, Sousa GL, Rus S, Smith CM, Towle DW, Hartline DK, Dickinson PS (2008) Identification of A-type allatostatins possessing-YXFGI/Vamide carboxy-termini from the nervous system of the copepod crustacean Calanus finmarchicus. Gen Comp Endocrinol 155:526–533PubMedCrossRefGoogle Scholar
  13. Christie AE, Stemmler EA, Dickinson PS (2010) Crustacean neuropeptides. Cell Mol Life Sci 67:4135–4169PubMedCrossRefGoogle Scholar
  14. Darbyson EA, Hanson JM, Locke A, Willison JHM (2009) Survival of European green crab (Carcinus maenus L.) exposed to simulated overland and boating-vector transport conditions. J Shellfish Res 28:377–382CrossRefGoogle Scholar
  15. Derby CD, Atema J (1988) Chemoreceptor cells in aquatic invertebrates: peripheral mechanisms of chemical signal processing in decapod crustaceans. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 365–385CrossRefGoogle Scholar
  16. Dircksen H, Keller R (1988) Immunocytochemical localization of CCAP, a novel crustacean cardioactive peptide, in the nervous system of the shore crab, Carcinus maenas L. Cell Tissue Res 254:347–360CrossRefGoogle Scholar
  17. Dircksen H, Zahnow CA, Gaus G, Keller R, Rao KR, Riehm JP (1987) The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean sinus glands: identification by an antiserum against a synthetic PDH. Cell Tissue Res 250:377–387CrossRefGoogle Scholar
  18. Dircksen H, Skiebe P, Abel B, Agricola HJ, Buchner K, Muren JE, Nässel DR (1999) Structure, distribution, and biological activity of novel members of the allatostatin family in the crayfish Orconectes limosus. Peptides 20:695–712PubMedCrossRefGoogle Scholar
  19. Dockray GJ (2004) The expanding family of RFamide peptides and their effects on feeding behaviour. Exp Physiol 89:229–235PubMedCrossRefGoogle Scholar
  20. Duve H, Johnsen AH, Maestro JL, Scott AG, Jaros PP, Thorpe A (1997) Isolation and identification of multiple neuropeptides of the allatostatin superfamily in the shore crab Carcinus maenas. Eur J Biochem 250:727–734PubMedCrossRefGoogle Scholar
  21. Duve H, Johnsen AH, Scott AG, Thorpe A (2002) Allatostatins of the tiger prawn, Penaeus monodon (Crustacea: Penaeidea). Peptides 23:1039–1051PubMedCrossRefGoogle Scholar
  22. Eales AJ (1973) Sex pheromone in the shore crab Carcinus maenas, and the site of its release from females. Mar Behav Physiol 2:345–355CrossRefGoogle Scholar
  23. Elwood RW, McClean A, Webb L (1979) The development of shell preferences by the hermit crab Pagurus bernhardus. Anim Behav 27:940–946CrossRefGoogle Scholar
  24. Fu Q, Christie AE, Li L (2005) Mass spectrometric characterization of crustacean hyperglycemic hormone precursor-related peptides (CPRPs) from the sinus gland of the crab, Cancer productus. Peptides 26:2137–2150PubMedCrossRefGoogle Scholar
  25. Gherardi F, Tricarico E (2007) Can hermit crabs recognize social partners by odors? And why? Mar Freshwat Behav Physiol 40:201–212CrossRefGoogle Scholar
  26. Gherardi F, Tricarico E (2011) Chemical ecology and social behavior of anomura. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 297–312Google Scholar
  27. Ghiradella HT, Case JF, Cronshaw J (1968) Structure of aesthetascs in selected marine and terrestrial decapods: chemoreceptor morphology and environment. Am Zool 8:603–621PubMedGoogle Scholar
  28. Gleeson RA (1982) Morphological and behavioral identification of the sensory structures mediating pheromone reception in the blue crab, Callinectes sapidus. Biol Bull 163:162–171CrossRefGoogle Scholar
  29. Goldstone MW, Cooke IM (1971) Histochemical localization of monoamines in the crab central nervous system. Cell Tissue Res 116:7–19Google Scholar
  30. Greenberg MJ, Price DA (1992) Chapter 3: relationships among the FMRFamide-like peptides. In: Joosse J, Buijs RM, Tilders FJH (eds) The peptidergic neuron. Elsevier, Amsterdam, pp 25–37CrossRefGoogle Scholar
  31. Hallberg E, Skog M (2011) Chemosensory sensilla in crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 103–121Google Scholar
  32. Hallberg E, Johansson KUI, Elofsson R (1992) The aesthetasc concept: structural variations of putative olfactory receptor cell complexes in Crustacea. Microsc Res Tech 22:325–335PubMedCrossRefGoogle Scholar
  33. Hansson BS, Harzsch S, Knaden M, Stensmyr MC (2011) The neural and behavioral basis of chemical communication in terrestrial crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 149–173Google Scholar
  34. Hanström B (1925) The olfactory centers in Crustaceans. J Comp Neurol 38:221–250CrossRefGoogle Scholar
  35. Hardege JD, Jennings A, Hayden D, Müller CT, Pascoe D, Bentley MG, Clare AS (2002) Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas. Mar Ecol Prog Ser 244:179–189CrossRefGoogle Scholar
  36. Hardege JD, Bartels-Hardege HD, Fletcher N, Terschak JA, Harley M, Smith MA, Davidson L, Hayden D, Müller CT, Lorch M, Welham K, Walther T, Bublitz R (2011) Identification of a female sex pheromone in Carcinus maenas. Mar Ecol Prog Ser 436:177–189CrossRefGoogle Scholar
  37. Harzsch S (2002) The phylogenetic significance of crustacean optic neuropils and chiasmata: a re-examination. J Comp Neurol 453:10–21PubMedCrossRefGoogle Scholar
  38. Harzsch S, Dawirs RR (1993) On the morphology of the central nervous system in larval stages of Carcinus maenas L. (Decapoda, Brachyura). Helgoland Mar Res 47:61–79Google Scholar
  39. Harzsch S, Hansson BS (2008) Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci 9:58PubMedCrossRefGoogle Scholar
  40. Harzsch S, Müller CHG (2007) A new look at the ventral nerve centre of Sagitta: implications for the phylogenetic position of Chaetognatha (arrow worms) and the evolution of the bilaterian nervous system. Front Zool 4:14PubMedCrossRefGoogle Scholar
  41. Harzsch S, Anger K, Dawirs RR (1997) Immunocytochemical detection of acetylated alpha-tubulin and Drosophila synapsin in the embryonic crustacean nervous system. Int J Dev Biol 41:477–484PubMedGoogle Scholar
  42. Harzsch S, Miller J, Benton JL, Dawirs RR, Beltz BS (1998) Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. J Exp Biol 201:2465–2479PubMedGoogle Scholar
  43. Harzsch S, Miller J, Benton JL, Beltz BS (1999) From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum. J Neurosci 19:3472–3485PubMedGoogle Scholar
  44. Harzsch S, Rieger V, Krieger J, Seefluth F, Strausfeld NJ, Hansson BS (2011) Transition from marine to terrestrial ecologies: Changes in olfactory and tritocerebralneuropils in land-living isopods. Arthropod Struct Dev 40:244–257PubMedCrossRefGoogle Scholar
  45. Hazlett BA (1968) Effects of crowding on the agonistic behavior of the hermit crab Pagurus bernhardus. Ecology 49:573–575CrossRefGoogle Scholar
  46. Hazlett BA (1970) Tactile stimuli in the social behavior of Pagurus bernhardus (Decapoda, Paguridae). Behaviour 36:20–48CrossRefGoogle Scholar
  47. Hazlett BA (1981) The behavioral ecology of hermit crabs. Annu Rev Ecol Syst 12:1–22CrossRefGoogle Scholar
  48. Hejnol A, Martindale M (2009) Coordinated spatial and temporal expression of Hox genes during embryogenesis in the acoel Convolutriloba longifissura. BMC Biol 7:65PubMedCrossRefGoogle Scholar
  49. Helm F (1928) Vergleichend-anatomische Untersuchungen über das Gehirn, insbesondere das “Antennalganglion” der Dekapoden. Z Morph Ökol Tiere 12:70–134CrossRefGoogle Scholar
  50. Homberg U (1994) Distribution of neurotransmitters in the insect brain. In: Rathmayer W (ed) Progress in zoology Vol. 40. Gustav Fischer, StuttgartGoogle Scholar
  51. Huybrechts J, Nusbaum MP, Bosch LV, Baggerman G, Loof AD, Schoofs L (2003) Neuropeptidomic analysis of the brain and thoracic ganglion from the Jonah crab, Cancer borealis. Biochem Biophys Res Commun 308:535–544PubMedCrossRefGoogle Scholar
  52. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner E, Buchner S (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165PubMedGoogle Scholar
  53. Klassen G, Locke A (2007) A biological synopsis of the European green crab, Carcinus maenas. Can J Fish Aquat Sci 2818:1–87Google Scholar
  54. Kreis TE (1987) Microtubules containing detyrosinated tubulin are less dynamic. EMBO J 6:2597–2606PubMedGoogle Scholar
  55. Kreissl S, Strasser C, Galizia CG (2010) Allatostatin Immunoreactivity in the Honeybee Brain. J Comp Neurol 518:1391–1417PubMedCrossRefGoogle Scholar
  56. Krieger J, Sandeman RE, Sandeman DC, Hansson BS, Harzsch S (2010) 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 7:25PubMedCrossRefGoogle Scholar
  57. Lancaster I (1988) Pagurus bernhardus (L.)-An introduction to the natural history of hermit crabs. Field Studies 7:189–238Google Scholar
  58. Langworthy K, Helluy S, Benton JL, Beltz BS (1997) Amines and peptides in the brain of the American lobster: immunocytochemical localization patterns and implications for brain function. Cell Tissue Res 288:191–206PubMedCrossRefGoogle Scholar
  59. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species - a selection from the Global Invasive Species Database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), 12 ppGoogle Scholar
  60. Ma M, Chen R, Sousa GL, Bors EK, Kwiatkowski MA, Goiney CC, Goy MF, Christie AE, Li L (2008) Mass spectral characterization of peptide transmitters/hormones in the nervous system and neuroendocrine organs of the American lobster Homarus americanus. Gen Comp Endocrinol 156:395–409PubMedCrossRefGoogle Scholar
  61. Ma M, Bors EK, Dickinson ES, Kwiatkowski MA, Sousa GL, Henry RP, Smith CM, Towle DW, Christie AE, Li L (2009a) Characterization of the Carcinus maenas neuropeptidome by mass spectrometry and functional genomics. Gen Comp Endocrinol 161:320–334PubMedCrossRefGoogle Scholar
  62. Ma M, Szabo TM, Jia C, Marder E, Li L (2009b) Mass spectrometric characterization and physiological actions of novel crustacean C-type allatostatins. Peptides 30:1660–1668PubMedCrossRefGoogle Scholar
  63. Ma M, Gard AL, Xiang F, Wang J, Davoodian N, Lenz PH, Malecha SR, Christie AE, Li L (2010) Combining in silico transcriptome mining and biological mass spectrometry for neuropeptide discovery in the Pacific white shrimp Litopenaeus vannamei. Peptides 31:27–43PubMedCrossRefGoogle Scholar
  64. Mangerich S, Keller R (1988) Localization of pigment-dispersing hormone (PDH) immunoreactivity in the central nervous system of Carcinus maenas and Orconectes limosus (Crustacea), with reference to FMRFamide immunoreactivity in O. limosus. Cell Tissue Res 253:199–208PubMedCrossRefGoogle Scholar
  65. Mangerich S, Keller R, Dircksen H, Rao KR, Riehm JP (1987) Immunocytochemical localization of pigment-dispersing hormone (PDH) and its coexistence with FMRFamide-immunoreactive material in the eyestalks of the decapod crustaceans Carcinus maenas and Orconectes limosus. Cell Tissue Res 250:365–375CrossRefGoogle Scholar
  66. McLaughlin PA, Lemaitre R (1997) Carcinization in the Anomura—fact or fiction? I. Evidence from adult morphology. Contrib Zool 67:79–123Google Scholar
  67. McLaughlin PA, Lemaitre R, Tudge CC (2004) Carcinization in the Anomura-fact or fiction? II. Evidence from larval, megalopal and early juvenile morphology. Contrib Zool 73:165–206Google Scholar
  68. Mercier AJ, Friedrich R, Boldt M (2003) Physiological functions of FMRFamide–like peptides (FLPs) in crustaceans. Microsc Res Tech 60:313–324PubMedCrossRefGoogle Scholar
  69. Nässel DR (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res 273:1–29PubMedCrossRefGoogle Scholar
  70. Nässel DR, Elofsson R (1987) Comparative anatomy of the crustacean brain. In: Gupta AP (ed) Arthropod brain: Its evolution, development, structure, and functions. Wiley & Sons, New York, pp 111–133Google Scholar
  71. Nässel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1–24PubMedCrossRefGoogle Scholar
  72. Paul DH (2003) Neurobiology of the Anomura: Paguroidea, Galatheoidea and Hippoidea. Mem Mus Vict 60:3–11Google Scholar
  73. Price DA, Greenberg MJ (1989) The hunting of the FaRPs: the distribution of FMRFamide-related peptides. Biol Bull 177:198–205CrossRefGoogle Scholar
  74. Reese ES (1962) Shell selection behaviour of hermit crabs. Anim Behav 10:347–360CrossRefGoogle Scholar
  75. Reese ES (1963) The behavioral mechanisms underlying shell selection by hermit crabs. Behaviour 21:78–126CrossRefGoogle Scholar
  76. Reese ES (1969) Behavioral adaptations of intertidal hermit crabs. Integr Comp Biol 9:343–355CrossRefGoogle Scholar
  77. Reimann A, Richter S, Scholtz G (2011) Phylogeny of the Anomala (Crustacea, Decapoda, Reptantia) based on the ossicles of the foregut. Zool Anz 250:316–342CrossRefGoogle Scholar
  78. Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Döring C, Faller S, Fritsch M, Grobe P, Heuer CM, Kaul S, Möller OS, Müller CHG, Rieger V, Rothe BH, Stegner MEJ, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29PubMedCrossRefGoogle Scholar
  79. Rudolph PH, Spaziani E (1990) Distribution of serotonergic neurons in the eyestalk and brain of the crab, Cancer antennarius. Comp Biochem Physiol C Pharmacol 97:241–245CrossRefGoogle Scholar
  80. Sandeman DC (1982) Organization of the central nervous system. In: Atwood HL, Sandeman DC (eds) The biology of crustacea — neurobiology, structure and function. Academic Press, New York, pp 1–61Google Scholar
  81. Sandeman DC, Mellon DF Jr (2002) Olfactory centers in the brain of freshwater crayfish. In: Wiese K (ed) The crustacean nervous system. Springer, New York, pp 386–404Google Scholar
  82. Sandeman DC, Scholtz G (1995) Ground plans, evolutionary changes and homologies in decapod crustacean brains. In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser Verlag, Basel, pp 329–347CrossRefGoogle Scholar
  83. Sandeman DC, Varju D (1988) A behavioural study of tactile localization in the crayfish Cherax destructor. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 163:525–536CrossRefGoogle Scholar
  84. Sandeman DC, Sandeman RE, Derby CD, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304–326CrossRefGoogle Scholar
  85. Sandeman DC, Scholtz G, Sandeman RE (1993) Brain evolution in decapod crustacea. J Exp Zool 265:112–133CrossRefGoogle Scholar
  86. Sandeman DC, Kenning M, Harzsch S (in press) Adaptive trends in malacostracan brain form and function related to behavior. In: Derby C and Thiel M (eds.) Crustaceans as model system in neurobiology. Springer, New YorkGoogle Scholar
  87. Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257–299CrossRefGoogle Scholar
  88. Schmidt M (1989) The hair-peg organs of the shore crab, Carcinus maenas (Crustacea, Decapoda): ultrastructure and functional properties of sensilla sensitive to changes in seawater concentration. Cell Tissue Res 257:609–621CrossRefGoogle Scholar
  89. Schmidt M (1997a) Continuous neurogenesis in the olfactory brain of adult shore crabs, Carcinus maenas. Brain Res 762:131–143PubMedCrossRefGoogle Scholar
  90. Schmidt M (1997b) Distribution of presumptive chemosensory afferents with FMRFamide- or substance P-like immunoreactivity in decapod crustaceans. Brain Res 746:71–84PubMedCrossRefGoogle Scholar
  91. Schmidt M (1997c) Distribution of centrifugal neurons targeting the soma clusters of the olfactory midbrain among decapod crustaceans. Brain Res 752:15–25PubMedCrossRefGoogle Scholar
  92. Schmidt M (2007) The olfactory pathway of decapod crustaceans—an invertebrate model for life-long neurogenesis. Chem Senses 32:365–384PubMedCrossRefGoogle Scholar
  93. Schmidt M, Ache BW (1996) Processing of antennular input in the brain of the spiny lobster, Panulirus argus. I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and median antennular neuropils. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 178:579–604CrossRefGoogle Scholar
  94. Schmidt M, Ache BW (1997) Immunocytochemical analysis of glomerular regionalization and neuronal diversity in the olfactory deutocerebrum of the spiny lobster. Cell Tissue Res 287:541–563PubMedCrossRefGoogle Scholar
  95. Schmidt M, Mellon DF Jr (2011) Neuronal processing of chemical information in crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 123–147Google Scholar
  96. Semmler H, Chiodin M, Bailly X et al (2010) Steps towards a centralized nervous system in basal bilaterians: Insights from neurogenesis of the acoel Symsagittifera roscoffensis. Dev Growth Differ 52:701–713PubMedCrossRefGoogle Scholar
  97. Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ (2003) Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467:150–172PubMedCrossRefGoogle Scholar
  98. Skiebe P (1999) Allatostatin-like immunoreactivity in the stomatogastric nervous system and the pericardial organs of the crab Cancer pagurus, the lobster Homarus americanus, and the crayfish Cherax destructor and Procambarus clarkii. J Comp Neurol 403:85–105PubMedCrossRefGoogle Scholar
  99. Snow PJ (1973) Ultrastructure of the aesthetasc hairs of the littoral decapod, Paragrapsus gaimardii. Cell Tissue Res 138:489–502Google Scholar
  100. Sombke A, Harzsch S, Hansson BS (2011) Organization of deutocerebral neuropils and olfactory behavior in the centipede Scutigera coleoptrata (Linnaeus, 1758) (Myriapoda: Chilopoda). Chem Senses 36:43–61PubMedCrossRefGoogle Scholar
  101. Stay B, Tobe SS (2007) The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annu Rev Entomol 52:277–299PubMedCrossRefGoogle Scholar
  102. Stay B, Tobe SS, Bendena WG (1995) Allatostatins: identification, primary structures, functions and distribution. Adv Insect Physiol 25:267–337CrossRefGoogle Scholar
  103. Stevcic Z (1971) The main features of brachyuran evolution. Syst Zool 20:331–340CrossRefGoogle Scholar
  104. Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34:235–256CrossRefGoogle Scholar
  105. Strausfeld NJ, Nässel DR (1980) Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology. Springer, New YorkGoogle Scholar
  106. Sullivan JM, Beltz BS (2001) Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans. J Comp Neurol 441:9–22PubMedCrossRefGoogle Scholar
  107. Sullivan JM, Beltz BS (2005a) Adult neurogenesis in the central olfactory pathway in the absence of receptor neuron turnover in Libinia emarginata. Eur J Neurosci 22:2397–2402PubMedCrossRefGoogle Scholar
  108. Sullivan JM, Beltz BS (2005b) Integration and segregation of inputs to higher-order neuropils of the crayfish brain. J Comp Neurol 481:118–126PubMedCrossRefGoogle Scholar
  109. Sullivan JM, Benton JL, Sandeman DC, Beltz BS (2007) Adult neurogenesis: a common strategy across diverse species. J Comp Neurol 500:574–584PubMedCrossRefGoogle Scholar
  110. Sztarker J, Strausfeld NJ, Tomsic D (2005) Organization of optic lobes that support motion detection in a semiterrestrial crab. J Comp Neurol 493:396–411PubMedCrossRefGoogle Scholar
  111. Sztarker J, Strausfeld NJ, Andrew D, Tomsic D (2009) Neural organization of first optic neuropils in the littoral crab Hemigrapsus oregonensis and the semiterrestrial species Chasmagnathus granulatus. J Comp Neurol 513:129–150PubMedCrossRefGoogle Scholar
  112. Tautz J, Müller-Tautz R (1983) Antennal neuropile in the brain of the crayfish: morphology of neurons. J Comp Neurol 218:415–425PubMedCrossRefGoogle Scholar
  113. Taylor RC (1975) Integration in the crayfish antennal neuropile: topographic representation and multiple-channel coding of mechanoreceptive submodalities. J Neurobiol 6:475–499PubMedCrossRefGoogle Scholar
  114. Tsvileneva VA, Titova VA (1985) On the brain structures of decapods. Zool Jahrb Abt Anat Ontog Tiere 113:217–266Google Scholar
  115. Tsvileneva VA, Titova VA, Kvashina TV (1985) Brain topography of the shore crab Hemigrapsus sanguineus. J Evol Biochem Physiol 21:394–400Google Scholar
  116. Utting M, Agricola HJ, Sandeman RE, Sandeman DC (2000) Central complex in the brain of crayfish and its possible homology with that of insects. J Comp Neurol 416:245–261PubMedCrossRefGoogle Scholar
  117. Van Der Meeren GI (1994a) Sex-and size-dependent mating tactics in a natural population of shore crabs Carcinus maenas. J Anim Ecol 63:307–314CrossRefGoogle Scholar
  118. van der Meeren GI (1994b) Sex-and size-dependent mating tactics in a natural population of shore crabs Carcinus maenas. J Anim Ecol 63:307–314CrossRefGoogle Scholar
  119. Vilpoux K, Sandeman RE, Harzsch S (2006) Early embryonic development of the central nervous system in the Australian crayfish and the Marbled crayfish (Marmorkrebs). Dev Genes Evol 216:209–223PubMedCrossRefGoogle Scholar
  120. Vitzthum H, Homberg U, Agricola H (1996) Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369:419–437PubMedCrossRefGoogle Scholar
  121. Wight K, Francis L, Eldridge D (1990) Food aversion learning by the hermit crab Pagurus granosimanus. Biol Bull 178:205–209CrossRefGoogle Scholar
  122. Wilson E (2007) Pagurus bernhardus. Hermit crab. Marine Life Information Network: biology and sensitivity key information sub-programme. Marine Biological Association of the United Kingdom, Plymouth [on-line]Google Scholar
  123. Wood DE, Derby CD (1996) Distribution of dopamine-like immunoreactivity suggests a role for dopamine in the courtship display behavior of the blue crab, Callinectes sapidus. Cell Tissue Res 285:321–330PubMedCrossRefGoogle Scholar
  124. Yasuda-Kamatani Y, Yasuda A (2006) Characteristic expression patterns of allatostatin-like peptide, FMRFamide-related peptide, orcokinin, tachykinin-related peptide, and SIFamide in the olfactory system of crayfish Procambarus clarkii. J Comp Neurol 496:135–147PubMedCrossRefGoogle Scholar
  125. Yin GL, Yang JS, Cao JX, Yang WJ (2006) Molecular cloning and characterization of FGLamide allatostatin gene from the prawn, Macrobrachium rosenbergii. Peptides 27:1241–1250PubMedCrossRefGoogle Scholar
  126. Zajac J, Mollereau C (2006) RFamide peptides. Editorial introduction. Peptides 27:941–942PubMedCrossRefGoogle Scholar
  127. Zeil J, Sandeman RE, Sandeman DC (1985) Tactile localisation: the function of active antennal movements in the crayfish Cherax destructor. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 157:607–617CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Jakob Krieger
    • 1
    Email author
  • Andy Sombke
    • 1
  • Florian Seefluth
    • 1
  • Matthes Kenning
    • 1
  • Bill S. Hansson
    • 2
  • Steffen Harzsch
    • 1
    • 2
  1. 1.Zoological Institute and Museum, Department of Cytology and Evolutionary BiologyUniversity of GreifswaldGreifswaldGermany
  2. 2.Department of Evolutionary NeuroethologyMax Planck Institute for Chemical EcologyJenaGermany

Personalised recommendations