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The cellular basis of photobehavior in the tufted parenchymella larva of demosponges

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Abstract

The mechanisms by which light elicits a phototactic response in sponge larvae remain poorly understood. Here we investigate histological and behavioral aspects of the photoresponse in parenchymella larvae of three demosponges. Two species are photonegative during their entire larval life, while the other, initially photopositive, becomes photonegative only after swimming in the laboratory for 4 h to 6 h. All larvae are bullet-shaped, with a uniformly ciliated surface, except at their posterior end, which is unciliated but surrounded by a distinctive ring of long cilia, the tuft. The short cilia beat metachronally, generating the thrust to move the larva forward with clockwise rotation. The long cilia of the tuft do not beat metachronally and are apparently more involved in maneuvering than in the generation of thrust. Transmission electron microscopy revealed in one species that the axoneme of the short cilia contains a distinctive "9×3+2" microtubule pattern at its base, but the presence of such an arrangement in cilia of the tuft remains uncorroborated. Nevertheless, the differences in beating characteristics between the monociliated cells of the tuft and those in the rest of the body correspond to other cytological differences. Cilia of the tuft have a type-I basal body, a large basal foot, and a branched rootlet, whereas the remaining cilia have a type-II basal body, a smaller and simpler basal foot, and an unbranched rootlet. Furthermore, the cells forming the tuft have a characteristic distal protrusion filled with pigments and mitochondria. Several of these traits suggest that the monociliated cells of the tuft are involved in the larval photoresponse both as sensors and effectors. Drastic changes in light intensity have no effect on the beating of the short cilia. In contrast, they cause a predictable and instantaneous movement of each cilium in the tuft, triggering expansions and contractions of either a part or the entire tuft, which in turn alters the direction of swimming. Observations on free-swimming larvae suggest that the tuft works as a passive light-sensitive rudder in both photonegative species that contract their posterior cilia under high irradiance and in photopositive species that expand their cilia under high irradiance. However, in photonegative larvae that expand the tuft under high irradiance, an active ciliary coordination by the larva needs to be invoked to explain a deviation of the swimming trajectory.

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Notes

  1. The term "cilia" is hereafter used to refer to eukaryotic organelles that are structurally characterized by an essentially identical arrangement of microtubules. Following Nielsen (1987), this definition covers the undulating cilium of many protists and sperm cells to the planar cilium of vertebrate multiciliated cells. The term "flagellum" is used for simpler structures found in the bacteria, which lack microtubules.

References

  • Amano S, Hori I (1994) Metamorphosis of a demosponge. I. Cell and structure of swimming larva. Invertebr Reprod Dev 25:193–204

    Google Scholar 

  • Amano S, Hori I (1996) Transdifferentiation of larval flagellated cells to choanocytes in the metamorphosis of the demosponge Haliclona permollis. Biol Bull 190:161–172

    Google Scholar 

  • Bergquist PR, Sinclair ME (1968) The morphology and behavior of larvae of some intertidal sponges. N Z J Mar Freshw Res 2:426–437

    Google Scholar 

  • Bergquist PR, Sinclair ME, Green CR, Silyn-Roberts H (1979) Comparative morphology and behaviour of larvae of Demospongiae. In: Lévi C, Boury-Esnault N (eds) Biologie des spongiaires. CNRS, Paris

  • Blumer MJ (1998) Alterations of the eyes of Carinaria lamarcki (Gastropoda, Heteropoda) during the long pelagic cycle. Zoomorph 118:183–194

    Article  Google Scholar 

  • Blumer MJF, Salvini-Plawen L, Kikinger R, Büchinger T (1995) Ocelli in a Cnidaria polyp: the ultrastructure of the pigment spot in Stylocoronella riedli (Scyphozoa, Stauromedusae). Zoomorph 115:221–227

    Google Scholar 

  • Bourget E, DeGuise J, Daigle G (1994) Scales of substratum heterogeneity, structural complexity, and early establishment of a marine epibenthic community. J Exp Mar Biol Ecol 181:31–51

    Google Scholar 

  • Boury-Esnault N (1976) Ultrastructure de la larve parenchymella d'Hamigera hamigera (Schmidt) (Démosponge, Poecilosclerida). Origine des cellules grises. Cah Biol Mar 17:9–20

    Google Scholar 

  • Brill B (1973) Untersuchungen zur ultrastruktur der choanocyte von Ephydatia fluviatilis L. Z Zellforsch Mikrosk Anat 144:231–245

    Google Scholar 

  • Chia F-S, Koss R (1979) Fine structural studies of the nervous system and the apical organ in the planula larva of the sea anemone Anthopleura elegantissima. J Morphol 160:275–298

    Google Scholar 

  • Chia F-S, Buckland-Nicks J, Young CM (1983) Locomotion of marine invertebrate larvae: a review. Can J Zool 62:1205–1222

    Google Scholar 

  • Cronin TW (1986) Photoreception in marine invertebrates. Am Zool 26:403–415

    Google Scholar 

  • Eakin RM (1963) Lines of evolution of photoreceptors. In: Mazia D, Tyler A (eds) General physiology of cell specialization. McGraw-Hill, New York

  • Eakin RM, Hermans CO (1988) Eyes. Microf Mar 4:135–156

    Google Scholar 

  • Evans CW (1977) The ultrastructure of larvae from the marine sponge Halichondria moorei Bergquist (Porifera, Demospongiae). Cah Biol Mar 18:427–433

    Google Scholar 

  • Fell PE (1974) Porifera. In: Giese AC, Pearse JS (eds) Acoelomate and pseudocoelomate metazoans. Academic Press, New York and London

  • Forward RB, Cronin TW, Stearns DE (1984) Control of diel vertical migration: photoresponses of a larval crustacean. Limnol Oceanogr 29:146–154

    Google Scholar 

  • Foster KW, Saranak J, Patel N, Zarilli G, Okabe M, Kline T, Nakanishi K (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eucaryote Chlamydomonas. Nature 311:756–759

    CAS  PubMed  Google Scholar 

  • Fry WG (1971) The biology of larvae of Ophlitaspongia seriata from two North Wales populations. Fourth European Mar Biol Symp:155–178

    Google Scholar 

  • Gordon RE (1982) Three-dimensional organization of microtubules and microfilaments of the basal apparatus of ciliated respiratory epithelium. Cell Motil 4:385–391

    Google Scholar 

  • Hard R, Rieder CL (1983) Muciliary transport in newt lungs: the ultrastructure of the ciliary apparatus in isolated epithelial sheets and in functional triton-extracted models. Tissue Cell 15:227–243

    CAS  PubMed  Google Scholar 

  • Harz H, Hegemann P (1991) Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351:489–491

    Google Scholar 

  • Hegemann P (1997) Vision in microalgae. Planta 203:265–274

    Article  CAS  PubMed  Google Scholar 

  • Hills JM, Thomason JC, Milligan JL, Richardson M (1998) Do barnacle larvae respond to multiple settlement cues over a range of spatial scales? Hydrobiologia 375/376:101–111

    Google Scholar 

  • Jaeckle WB (1995) Transport and metabolism of alanine and palmitic acid by field-collected larvae of Tedania ignis (Porifera, Demospongiae): estimated consequences of limited label translocation. Biol Bull 189:159–167

    CAS  Google Scholar 

  • Kamiya R, Witman GB (1984) Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models of Chlamydomonas. J Cell Biol 98:97–107

    CAS  PubMed  Google Scholar 

  • Kaye HR, Reiswig HM (1991) Sexual reproduction in four Caribbean commercial sponges. III. Larval behaviour, settlement and metamorphosis. Invertebr Reprod Dev 19:25–35

    Google Scholar 

  • Konstantinova MI (1966) Characteristic of movement of pelagic larvae of marine invertebrates. Dokl Akad Nauk SSSR 170:726–729

    Google Scholar 

  • Lévi C (1964) Ultrastructure de la larve parenchymella de Démosponge. I. Mycale contarenii (Martens). Cah Biol Mar 5:97–104

    Google Scholar 

  • Leys SP, Degnan BM (2001) Cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201:323–338

    CAS  PubMed  Google Scholar 

  • Leys SP, Cronin TW, Degnan BM, Marshall JN (2002) Spectral sensitivity in a sponge larva. J Comp Physiol [A] 188:199–202

    Google Scholar 

  • Maldonado M, Bergquist PR (2002) Phylum Porifera. In: Young CM, Sewell MA, Rice ME (eds) Atlas of marine invertebrate larvae. Academic Press, San Diego

  • Maldonado M, Uriz MJ (1998) Microrefuge exploitation by subtidal encrusting sponges: patterns of settlement and post-settlement survival. Mar Ecol Prog Ser 174:141–150

    Google Scholar 

  • Maldonado M, Young CM (1996) Effects of physical factors on larval behavior, settlement and recruitment of four tropical demosponges. Mar Ecol Prog Ser 138:169–180

    Google Scholar 

  • Maldonado M, Young CM (1999) Effects of the duration of the larval life on post-larval stages of the demosponge Sigmadocia caerulea. J Exp Mar Biol Ecol 232:9–21

    Article  Google Scholar 

  • Maldonado M, George SB, Young CM, Vaquerizo I (1997) Depth regulation in parenchymella larvae of a demosponge: relative roles of skeletogenesis, biochemical changes and behavior. Mar Ecol Prog Ser 148:115–124

    Google Scholar 

  • Nielsen C (1987) Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool (Stockholm) 68:205–262

    Google Scholar 

  • Pitelka DR (1974) Basal bodies and root structures. In: Sleigh MA (ed) Cilia and flagella. Academic Press, New York

  • Raimondi PT (1990) Patterns, mechanisms, consequences of variability in settlement and recruitment of an intertidal barnacle. Ecol Monogr 60:283–309

    Google Scholar 

  • Sanderson MJ (1984) Cilia. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. 1. Invertebrates. Springer, Berlin Heidelberg New York

  • Sandoz D, Chailley B, Boisvieux-Ulrich E, Lemullois M, Laine M-C, Bautista-Harris G (1988) Organization and functions of cytoskeleton in metazoan ciliated cells. Biol Cell 63:183–194

    Article  CAS  PubMed  Google Scholar 

  • Sarà M, Vacelet J (1973) Ecologie des Démosponges. In: Grassé PP (ed) Spongiaires. Anatomie, physiologie, systématique, ecologie. Masson, Paris

  • Saranak J, Foster KW (1997) Rhodopsin guides fungal phototaxis. Nature 387:465–466

    CAS  PubMed  Google Scholar 

  • Singla CL (1974) Ocelli of Hydromedusae. Cell Tissue Res 149:413–429

    CAS  PubMed  Google Scholar 

  • Thomas MB, Freeman G, Martin VJ (1987) The embryonic origin of neurosensory cells and the role of nerve cells in metamorphosis in Phialidium gregarium (Cnidaria, Hydrozoa). Invert Biol 11:265–287

    Google Scholar 

  • Uriz MJ, Maldonado M, Turon X, Martí R (1998) How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges? Mar Ecol Prog Ser 167:137–148

    Google Scholar 

  • Uriz MJ, Turon X, Becerro MA (2001) Morphology and ultrastructure of the swimming larvae of Crambe crambe (Demospongiae, Poecilosclerida). Invertebr Biol 120(4):295–307

    Google Scholar 

  • Vacelet J (1979) Quelques stades de la reproduction sexuel d'une éponge Sphinctozoaire actuelle. In: Lévi C, Boury-Esnault N (eds) Biologie des spongiaires. CNRS, Paris

  • Vogel S (1994) Life in moving fluids. The physical biology of flow. Princeton University Press, Princeton, N.J.

  • Walters LJ, Wethey DS (1996) Settlement and early post-settlement survival of sessile marine invertebrates on topographically complex surfaces: the importance of refuge dimensions and adult morphology. Mar Ecol Prog Ser 137:161–171

    Google Scholar 

  • Weis VM, Keene DR, Buss LW (1985) Biology of hydractiniid hydroids. 4. Ultrastructure of the planula of Hydractinia echinata. Biol Bull 168:403–418

    Google Scholar 

  • Wolken JJ (1995) Light detectors, photoreceptors, and imaging systems in nature. Oxford University Press, New York

  • Woollacott R (1990) Structure and swimming behavior of the larva of Halichondria melanodocia (Porifera: Demospongiae). J Morphol 205:135–145

    Google Scholar 

  • Woollacott RM (1993) Structure and swimming behavior of the larva of Haliclona tubifera (Porifera: Demospongiae). J Morphol 218:301–321

    Google Scholar 

  • Woollacott RM, Pinto RL (1995) Flagellar basal apparatus and its utility in phylogenetic analyses of the Porifera. J Morphol 226:247–265

    Google Scholar 

  • Young CM, Chia F-S (1984) Microhabitat-associated variability in survival and growth of subtidal littoral ascidians during the first 21 d after settlement. Mar Biol 81:61–68

    Google Scholar 

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Acknowledgements

This study was supported by the Fulbright Association (FU-93-02207057) and two research grants from the Spanish government to M.M. (MEC-PB-98-0485; BMC-2002-01228). This is HBOI contribution number 1515 and SMSFP contribution number 563.

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Authors and Affiliations

  1. Department of Aquatic Ecology, Centro Estudios Avanzados de Blanes (CSIC), Acceso a Cala St. Francesc 14, 17300, Blanes, Girona, Spain

    M. Maldonado

  2. Department of Cell Biology, Faculty of Biology, Universidad de Barcelona, Avenida Diagonal 645, 08071 , Barcelona, Spain

    M. Durfort

  3. Department of Larval Ecology, Harbor Branch Oceanographic Institution, 5600 U.S. Hwy 1 N., Fort Pierce, FL 34946, USA

    D. A. McCarthy

  4. Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, OR 97420, USA

    C. M. Young

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  1. M. Maldonado
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Correspondence to M. Maldonado.

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Communicated by S. A. Poulet, Roscoff

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Maldonado, M., Durfort, M., McCarthy, D.A. et al. The cellular basis of photobehavior in the tufted parenchymella larva of demosponges. Marine Biology 143, 427–441 (2003). https://doi.org/10.1007/s00227-003-1100-1

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