Anterior sense organs in Sabellaria alveolata (Annelida, Sedentaria, Spionida) with special reference to ultrastructure of photoreceptor elements presumably involved in shadow reflex
The reef-building sedentary polychaete, Sabellaria alveolata, is well known for its specialized anterior end, the operculum, which is exposed to the environment during vital activities, such as feeding or as it seals its tube when the animal withdraws. This region represents the most important sensory structure in Sabellariidae. It comprises two lobes, tentacular filaments, protective chaetae (paleae), a median organ, and a median ridge, and bears various pigmented spots. Worms swiftly withdraw into tubes triggered by abrupt light change (shadow reflex). We suspected that the pigmented spots were photoreceptive and responsible for the shadow response. To test this hypothesis, the median organ and median ridge of S. alveolata were investigated by applying light microscopy, confocal laser scanning microscopy, scanning, and transmission electron microscopy. Besides unciliated supportive cells, these organs consist of numerous multiciliated and glandular cells on their ventral surfaces. The multiciliated cells are of two types: epidermal supportive and receptor cells. The median organ is innervated directly from the brain by two longitudinal basiepithelial nerves. The presence of multiciliated cells and mucocytes suggests that the organ is sensory, involved in both feeding and tube-building behavior. Furthermore, we found two pairs of eyespots on the lateral posterior part of the median ridge, situated close to the neurite bundles anterior to the brain. These eyes are simple in structure and resemble larval-type eyes. They are composed of only two cells each, one rhabdomeric photoreceptor cell and one pigmented supportive cell. The pigmented eyes on the median ridge are clearly involved in photoreception and very likely involved in shadow reflex.
KeywordsPhotoreceptor cells Eyes Polychaetes Operculum Median ridge Median organ (dorsal hump) Sensory cells
We are grateful to the head of our department, Professor Dr. A. Paululat, Osnabrück, for various kinds of support. Professor Dr. T. Bartolomaeus and Dr. E. Tilic, Bonn, Germany, kindly helped fixing specimens from Mont St. Michel. Thanks are also due to K. Etzold and W. Mangerich, Osnabrück, for various kinds of technical assistance, particularly for introducing CM to electron microscopy techniques. Funding was provided by National Council for Scientific and Technological Development, Brazil (CNPq – SWE 201233/2015-0) and Muséum National d’Histoire Naturelle.
Note added in proof
While this paper was in type setting another study on a sabbellariid median organ was published (Helm et al. 2018): The authors regard the median organ as a structure comparable to nuchal organs and describe the eyes of Idanthyrsus australensis differing in structure, number and position from those described here for S. alveolata.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
We neither used endangered species nor were the investigated animals collected in protected areas. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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- Amieva MR, Reed CG, Pawlik JR (1987) Ultrastructure and behavior of the larva of Phragmatopoma californica (Polychaeta: Sabellariidae): identification of sensory organs potentially involved in substrate selection. Mar Biol 95:59–266Google Scholar
- Capa M, Hutchings P (2014) Sabellariidae Johnston, 1865. In: Westheide W, Purschke G, Böggemann M (eds) Handbook of zoology online. A natural history of the phyla of the animal kingdom; Annelida: Polychaetes. De Gruyter, Berlin. http://www.degruyter.com/view/db/zoology/bp_029147-6_63. Accessed 15 Oct 2014Google Scholar
- Dales RP (1952) The development and structure of the anterior region of the body in the Sabellariidae, with special reference to Phragmatopoma californica. Q J Microsc Sci 93:435–452Google Scholar
- Eckelbarger KJ (1976) Larval development and population aspects of the reef-building polychaete Phragmatopoma lapidosa from the east coast of Florida. Bull Mar Sci 26:117–132Google Scholar
- Eckelbarger KJ (1977) Larval development of Sabellaria floridensis from Florida and Phragmatopoma californica from southern California (Polychaeta: Sabellariidae), with a key to the sabellariid larvae of Florida and a review of development in the family. Bull Mar Sci 27:241–255Google Scholar
- Eckelbarger KJ (1978) Metamorphosis and settlement in the Sabellariidae. In: Chia F-S, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 145–164Google Scholar
- Hausen H (2001) Untersuchungen zur Phylogenie “spiomorpher” Polychaeten (Annelida). Logos, Berlin, pp 1–142Google Scholar
- Kirtley DW (1994) A review and taxonomic revision of the family Sabellariidae Johnston, 1865 (Annelida; Polychaeta) (series 1). Sabecon Press Science, Los Angeles, pp 1–223Google Scholar
- Lechapt JP, Kirtley DW (1996) Bathysabellaria spinifera (Polychaeta: Sabellariidae), a new species from deep water off New Caledonia, Southwest Pacific Ocean. Proc Biol Soc Wash 109:560–574Google Scholar
- Martínez A, Purschke G, Worsaae K (2017) Protodrilidae Hatschek, 1888. In: Westheide W, Purschke G, Böggemann M (eds) Handbook of zoology online. A natural history of the phyla of the animal kingdom; Annelida: Polychaetes. http://www.degruyter.com/view/Zoology/pb029147-6_8. Accessed 19 Sept 2017Google Scholar
- Orrhage L (1978) On the structure and evolution of the anterior end of the Sabellariidae (Polychaeta, Sedentaria). With some remarks on the general organisation of the polychaete brain. Zool Jb Anat 100:343–374Google Scholar
- Pawlik JR (1990) Natural and artificial induction of metamorphosis of Phragmatopoma lapidosa californica (Polychaeta: Sabellariidae), with a critical look at the effects of bioactive compounds on marine invertebrate larvae. Bull Mar Sci 46:512–536Google Scholar
- Purschke G (2016) Annelida: basal groups and pleistoannelida. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 254–312Google Scholar
- Purschke G, Müller MC (1996) Structure of photoreceptor-like sense organs in Protodriloides species (Polychaeta, Protodrilida). Cah Biol Mar 37:205–219Google Scholar
- Randel N, Jékely G (2015) Phototaxis and the origin of visual eyes. Philos Trans R Soc 371:1–12Google Scholar
- 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, Møller OS, Müller CHG, Rieger V, Rothe BH, Stegner MEJ, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29CrossRefGoogle Scholar
- Rouse GW, Pleijel F (2001) Polychaetes. Oxford University Press, New York, 345 ppGoogle Scholar