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

The mechanisms by which light elicits a pho­ totactic response in sponge larvae remain poorly understood. Here we investigate histological and behavioral aspects of the photoresponse in parenchym­ ella larvae of three demosponges. Two species are pho­ tonegative 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 sur­ face, 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 rota­ tion. 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 "9x3 + 2" microtuCommunicated by S. A. Poulet, Roscoff M. Maldonado (12l) Department of Aquatic Ecology, Centro Estudios Avanzados de BJanes (CSIC), Acceso a Cala St. Francese 14, 17300 Blanes, Girona, Spain E-mail: maldonadoeuceab.csic.es Tel.: +34-972-336101 Fax: + 34-972-337806 M. Durfort Department of Cell Biology, Faculty of Biology, Universidad de Barcelona, Avenida Diagonal 645, 08071 Barcelona, Spain D. A. McCarthy Department of Larval Ecology, Harbor Branch Oceanographic Institution, 5600 U.S. Hwy 1 N., Fort Pierce, FL 34946, USA C. M. Young Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, OR 97420, USA bule 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. Fur­ thermore, 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 inten­ sity 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 expan­ sions and contractions of either a part or the entire tuft, which in turn alters the direction of swimming. Obser­ vations on free-swimming larvae suggest that the tuft works as a passive light-sensitive rudder in both pho­ tonegative species that contract their posterior cilia un­ der 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.