Journal of Shellfish Research, Vo1. 18, No. 1, 251-257, 1999.

HISTOLOGICAL ANALYSIS OF MANTLE-CAVITY CILIATES IN DREISSENA POLYMORPHA: THEIR LOCATION, SYMBIOTIC RELATIONSHIP, AND DISTINGUISHING MORPHOLOGICAL CHARACTERISTICS

F. LARUELLE¹, D. P. MOLLOY², S. I. FOKIN³, AND M. A. OVCHARENKO⁴

¹ UMR CNRS 6539

Institut Universitaire Europeen de la Mer

UBO, Place Nicolas Copernic

Technop6le Brest-lroise 29280 Plouzane, France

²Biological Survey, New York State Museum

The State Education Department

Cultural Education Center

Albany, New York 12230

³ Biological Research Institute

St. Petersburg State University

St. Petersburg 198904, Russia

⁴ Institute of Hydrobiology Ukrainian Academy of Sciences

12 Prospect Geroyev Stalingrada

Kiev-2IO 254655, Ukraine

ABSTRACT: Dissection has traditionally been the sole method used in investigations of the parasites and other endosymbionts of zebra mussels, Dreissena polymorpha. This study demonstrates the value of histological analysis as a complementary technique capable of precisely determining the location of ciliates within zebra mussels and characterizing their symbiotic relationships at the cellular level. The photomicrographs included herein represent the first published histological images of mantle-cavity ciliates of zebra mussels, and we have highlighted morphological characteristics useful in distinguishing individual ciliate species in histological sections. Although zebra mussels from both North America and Europe were sampled for this study, only European populations were found to harbor mantle-cavity ciliates, and five species were observed. The host-specific species Conchophthirus acuminatus (Scuticociliatida: Conchophthiridae) was frequently recorded from epithelium covering the outer gill surfaces and occasionally from visceral mass epithelium, but also found in four previously unreported regions: frequently within gill water tubes and occasionally on labial palps, mantle epithelium, and within suprabranchial cavities. Although we sometimes observed zebra mussel sperm in food vacuoles of C. acuminatus, epithelial tissues in contact with high densities of these ciliates showed no evidence of pathology, thus confirming this species' commensal nature. The host-specific species Sphenophrya dreissenae (Rhynchodida: Sphenophryidae) was frequently recorded attached to mantle cavity epithelium and outer gill surfaces, but also found in three previously unreported regions: frequently within the gill water tubes, occasionally on the visceral mass, and rarely within the suprabranchial cavities. High-intensity infections with this parasitic ciliate did induce hyperplasia, cell hypertrophy, and vacuolization of the epithelia. The host-specific species Hypocomagalma dreissenae (Rhynchodida: Ancistrocomidae) was most frequently observed attached to epithelial cells lining outer gill surfaces, but also in five previously unreported regions: occasionally on the visceral mass, the mantle cavity epithelium, and in gill water tubes, and rarely on labial palps and within the suprabranchial cavities. This parasitic ciliate feeds on the contents of epithelial cells using a suctorial tentacle. The intensity of H. dreissenae infection, however, was usually very low, and no adverse effects on parasitized cells or nearby tissues were evident. The ciliate Ancistrumina limnica (Scuticociliatida: Ancistridae), a nonhost-specific commensal of mollusks, was recorded frequently within gill water tubes, occasionally on outer gill epithelia, and rarely within suprabranchial cavities. This species was also observed to have ingested D. polymorpha sperm cells. Commensal Peritrichia ciliates were also occasionally observed within the mantle cavity, but were likely carried there passively by water currents from their typical location on shell surfaces. The presence of "mantle cavity" ciliate species in the gill water tubes and the suprabranchial cavities of zebra mussels suggests that these ciliates probably can exit into surrounding waters to infect other zebra mussels via the exhalant siphon.

KEY WORDS: zebra mussels, ciliophora, Conchophthirus, Sphenophrya, Hypocomagalma, Ancistrumina, Peritrichia