Abstract

Sea anemones feed by orchestrated movements of tentacles covered with ciliary cones overlying both nematocytes and sensory neurons and mediating nematocyst discharge into prey. The purpose of this study was to investigate the functional morphology of tentacle sensory receptors on Calliactis parasitica and C. tricolor with a combination of scanning electron microscopy (SEM) of surface features and transmission electron microscopy (TEM) of internal cellular details. We found that the ciliary cones of two types of nematocysts differed: mastigophore-containing nematocytes had an inner ring of large-diameter stereocilia, and basitrich-containing nematocytes had small-diameter stereocilia. Two types of sensory neurons were identified: one had a ciliary cone with an inner ring of large-diameter stereocilia, and the other had a long kinocilium surrounded by a basal ring of short, stubby microvilli. Varying lengths of stereocilia on peripheral supportive cells contributed to both ciliary cones of nematocytes and sensory neurons. Both the supportive epithelial cells with stereocilia and the nonsupportive epithelial cells without stereocilia had a single long kinocilium with a basal body, an accessory centriole, and a thick striated rootlet. Gland cells had a short cilium surrounded by even shorter microvilli. Spirocysts formed apical domes on spirocytes, which had two peripheral rings of short microvilli but no cilium. We believe this combined SEM and TEM study of sensory hairs on tentacles of two species of Calliactis adds to our knowledge of ciliary structures and their cellular associations in sea anemones. Additional key words: ciliary cones, nematocytes, sensory cells, gland cells Sea anemones have feeding tentacles covered with ciliary cones which overlay nematocysts and sensory neurons (Pantin 1942). The ciliary cones have in common a kinocilium central to several rings of stereocilia of varying lengths derived from adjacent supportive cells (Mariscal 1974a,b; Peteya 1975; Mariscal & Bigger 1976). The kinocilium is characterized by a typical 9x2 + 2 pattern of microtubules, whereas the stereocilia have filamentous cores of actin similar to those of vertebrate hair cells (Watson & Roberts 1995). Ciliary cones of sea anemones have been compared to vertebrate hair bundles both morphologically and physiologically (Mariscal 1974a; Watson & Roberts 1995; Mire & Watson 1997). A directional displacement of a vertebrate hair bundle that stretches tip links between adjacent stereocilia and opens transduction channels causes depolarization of the hair cell (Osborne et al. 1984; Markin & Hudspeth 1995). Bundle deflection of sensory neuron ciliary cones having tip links between adjacent stereocilia induces ion channels a Author for correspondence. E-mail: westfall@vet.ksu.edu to open, resulting in depolarization of supportive cells on one side of the complex (Mire & Watson 1997). Ciliary cones of nematocytes and of sensory neurons in sea anemones appear similar. At first, it was believed that chemoreception of N-acetylated sugars by supportive cells caused nematocyte ciliary cones to elongate and frequency tune to movements of swimming prey, leading to discharge of nematocysts (Watson & Hessinger 1989, 1991). This view supports the independent effector hypothesis of nematocyst discharge (Pantin 1942). More recent work, using better optics, has demonstrated that the sensory neuron/supporting cell complexes respond to N-acetylated sugars and elongate their hair bundles to tune to movements of swimming prey (Mire-Thibodeaux & Watson 1994; Watson & Roberts 1995). Those studies suggested that the nervous system plays a role in nematocyst discharge. In the present study, we have used a combination of SEM and TEM to distinguish ciliary cones of sensory neurons from those of the nematocytes and to further differentiate between various kinds of nemaThis content downloaded from 157.55.39.144 on Wed, 21 Sep 2016 05:31:38 UTC All use subject to http://about.jstor.org/terms Sensory structures on tentacles of sea anemones tocytes in the genus Calliactis. We have also investigated the cellular origins of other sensory structures such as kinocilia, stereocilia, and microvilli.

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