Abstract
Today molecular data recover three higher taxa in nemerteans, Palaeonemertea, Pilidiophora and Hoplonemertea. Hubrechtella dubia, a former palaeonemertean taxon was excluded from palaeonemerteans and is now supported as the sister group to heteronemerteans. This taxon is called Pilidiophora, because H. dubia and Heteronemertea share a pilidium larva. To find additional morphological evidence for Pilidiophora, the nervous system of 13 species of this taxon were investigated using different histological techniques. The central or medullated nervous system of nemerteans consists of a ring-shaped brain and lateral branching medullary cords. While the brain of basally branching nemerteans shows no or only slightly posterior enlargement, the brain of Pilidiophora expands caudally. Pilidiophora possess a conspicuous sensory organ, the cerebral organ. Although this organ is also found in hoplonemerteans and certain palaeonemertean species, only in Pilidiophora this organ is directly connected to the dorsal lobe of the brain. Additionally, this organ terminates in a layer of neurons close to the blood vessel in all pilidiophoran species. The analysis indicates that although in H. dubia some characters of the nervous system show the plesiomorphic state, the morphology of the cerebral organ provides an apomorphic character for a taxon Pilidiophora.
Similar content being viewed by others
References
Amerongen HM, Chia FS (1982) Behavioral evidence for a chemoreceptive function of the cerebral organs in Paranemertes peregrina Coe (Hoplonemertea: Monostilifera). J Exp Mar Biol Ecol 64:11–16
Andrade S, Strand M, Schwartz M, Chen H, Kajihara H, von Döhren J, Sun S, Junoy J, Thiel M, Norenburg JL, Turbeville JM, Giribet G, Sundberg P (2012) Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28:141–159
Andrade S, Montenegro H, Strand M, Schwartz M, Kajihara H, Norenburg JL, Giribet G (2014) A transcriptomic approach to ribbon worm systematics (Nemertea): resolving the Pilidiophora problem. Mol Biol Evol msu 253
Beckers P (2012) Nemertean nervous system: a comparative analysis. Phd thesis. Rheinische Friedrich-Wilhelm Universität Bonn, Mathematisch, Naturwissenschaftliche Fakultät
Beckers P, Faller S, Loesel R (2011) Lophotrochozoan neuroanatomy: an analysis of the brain and nervous system of Lineus viridis (Nemertea) using different staining techniques. Front Zool 8:17. doi:10.1186/1742-9994-8-17
Beckers P, Loesel R, Bartolomaeus T (2013) The nervous systems of basally branching Nemertea (Palaeonemertea). PLoS One 8(6):e66137. doi:10.1371/journal.pone.0066137
Bianchi S (1969a) On the neurosecretory system of Cerebratulus marginatus (Heteronemertini). Gen Comp Endocrinol 12:541–548
Bianchi S (1969b) The histochemistry of the neurosecretory system in Cerebratulus marginatus (Heteronemertini). Gen Comp Endocrinol 13:206–210
Bullock TH, Horridge GA (1965) Structure and function of the nervous system of invertebrates, vol 2. Freeman and company, San Francisco
Bürger O (1895) Die Nemertinen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. In: Friedländer, Sohn R (eds) Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte, Berlin
Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S et al (2012) TrakEM2: software for neural circuit reconstruction. PLoS One 7(6):e38011
Chernyshev AV, Magarlamov TY, Turbeville JM (2013) Morphology of the proboscis of Hubrechtella Juliae (Nemertea, Pilidiophora): implications for Pilidiophoran monophyly. J Morphol 274:1397–1414
Döhren VJ, Bartolomaeus T (2007) Ultrastructure and development of the rhabdomeric eyes in Lineus viridis (Heteronemertea, Nemertea). Zoology 110:430–438
Faller S, Loesel R (2008) Immunohistochemistry of the polyplacophora (mollusca) nervous system. J Morphol 269:1482
Fernández-Álvarez FA, Anadón N (2012) Oligodendrorhynchus hesperides gen. et sp. n. (Heteronemertea) from the Bellingshausen Sea. Pol Polar Res 33:81–98. doi:10.2478/v10183-012-0006-3
Ferraris JD (1985) Putative neuroendrocrine devices in the Nemertina: an overview of structure and function. Amer Zool 25:73–85
Gibson R (1972) Nemerteans. Hutchinson University Library, London
Gibson R (1977) A new genus and species of Lineid Heteronemertean from South Africa, Polybrachiorhynchus dayi (Nemertea: Anopla), possessing a multibranched proboscis. Bull Mar Sci 27:552–571
Golding DW (1992) Polychaeta nervous system. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates Vol 7, Annelida. Wiley-Liss, New York, pp 153–179
Grobe P, Vogt L (2008) MorphDBase-A: morphological description database. J Morphol 269:1478–1479
Grobe P, Vogt L (2014) Documenting morphology: Morph D base. In: Wägele JW, Bartolomaeus T (eds) Deep Metazoan phylogeny: The backbone of the tree of life. DeGruyter, Berlin, pp 475–503
Harrel R, Tanzer ML (1993) Extracellular matrix 3: evolution of the extracellular matrix in invertebrates. FASEB J 12:1115–1123
Heuer CM, Loesel R (2008) Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida). Cell Tissue Res 331:713–724
Heuer CM, Loesel R (2009) Three-dimensional reconstruction of mushroom body neuropils in the polychaete species Nereis diversicolor and Harmothoe areolata (Phyllodocida, Annelida). Zoomorphology 128:219–226
Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76
Kvist S, Laumer C, Junoy J, Giribet G (2014) A further contribution to the phylogeny, systematics and DNA barcoding of Nemertea. Inverteb Syst 28:287–308
Ling EA (1969) The structure and function of the cephalic organ of a nemertine Lineus ruber. Tissue Cell 3:503–524
Ling EA (1970) Further investigations on the structure and function of cephalic organs of a nemertine Lineus ruber. Tissue Cell 2:569–588
Nicaise G (1973) The gliointerstitial system of molluscs. Int Rev Cytol 34:251–332
Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G et al (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29. doi:10.1186/1742-9994-7-29
Rothe BH, Schmidt-Rhaesa A (2008) Variation in the nervous system in three species of the genus Turbanella (Gastrotricha, Macrodasyida). Meiofauna Marina 16:175–184
Rutka JT, Apodaca G, Stren R, Rosenblum M (1988) The extracellular matrix of the central and peripheral nervous systems: structure and function. J Neurosurg 69:155–170
Scharrer B (1941) Neurosecretion. III. The cerebral organ of the nemerteans. J Comp Neurol 74:109–130
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 7:676–682
Schmidt-Rhaesa A (2007) Evolution of organ systems. Oxford University Press
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Senz W (2000) Neue Nemertinen aus dem Golf von Arabien 1. Palaeonemertini. Ann Naturhist Mus Wien B 102:321–373
Senz W (2001) Neue Nemertinen aus dem Golf von Arabien 2. Heteronemertini und monostilifere Hoplonemertini. Ann Naturhist Mus Wien B 103:13–75
Thollesson M, Norenburg JL (2003) Ribbon worm relationships: a phylogeny of the phylum Nemertea. Proc R Soc Lond B 1513:407–415
Turbeville JM (1991) Nemertinea. In: Harrison FW, Bogitsh BJ (eds) Microscopic anatomy of invertebrates Vol 3, Platyhelminthes and Nemertinea. Wiley- Liss, New York, pp 258–328
Wollesen T, Loesel R, Wanninger A (2008) FMRFamide-like immunoreactivity in the central nervous system of the cephalopod mollusc, Idiosepius notoides. Acta Biol Hung 59:111–116
Acknowledgements
The author thanks two anonymous reviewers who helped to improve the manuscript. The author thanks Malin Strand for collecting Hubrechtella dubia, Daria Krämer for collecting Cerebratulus fuscus and Notospermus geniculatus. Alexej Chernyshev gently provided specimen of Baseodiscus hemprichii. Christiane Wallnisch for technical support and Thomas Bartolomaeus for discussions and suggestions on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Andreas Schmidt-Rhaesa.
Rights and permissions
About this article
Cite this article
Beckers, P. The nervous systems of Pilidiophora (Nemertea). Zoomorphology 134, 1–24 (2015). https://doi.org/10.1007/s00435-014-0246-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-014-0246-3