A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

Abstract

Polydora tunicola Abe, Hoshino & Yamada, sp. nov., a new spionid species currently considered an obligate symbiont of styelid ascidians, is described based on materials collected from Polycarpa cf. cryptocarpa kroboja (Oka, 1906) and Cnemidocarpa sp. in Izu-Oshima Island and Polycarpa sp. in Wakayama Prefecture, Japan. Polychaete–ascidian symbiotic relationships are known only in two syllid species: Myrianida pinnigera (Montagu, 1808) and Proceraea exoryxae Martin, Nygren & Cruz-Rivera, 2017. The latter has been the only polychaete known to bore into the tunic of an ascidian. Polydora tunicola sp. nov. is the second known example of a tunic-boring polychaete, which constructs U-shaped burrows in the tunic of the host ascidians. Worms were often concentrated near the host siphons and assumed to use water currents created by the filter-feeding host for suspension feeding. Although the boring mechanism into ascidian tunica is unknown, the plate assay and zymography results consistently detected cellulase activities, suggesting that cellulose digestion may enable the worms to bore into the cellulose-rich ascidian tunics. Polydora tunicola sp. nov. is morphologically similar to P. aura Sato-Okoshi, 1998, P. cornuta Bosc, 1802, P. fusca Radashevsky & Hsieh, 2000, P. glycymerica Radashevsky, 1993, P. latispinosa Blake & Kudenov, 1978, P. lingulicola Abe & Sato-Okoshi, 2020, P. nanomon Orensky & Williams, 2009, P. robi Williams, 2000, and P. vulgaris Mohammad, 1972 in having a single median antenna on the caruncle and chaetiger 5 without dorsal superior capillaries but with ventral capillaries. The new species is unique in having a black-rimmed pygidium, distinguishing it from these species. The phylogenetic analyses of the concatenated 18S, 28S, and 16S sequences recovered P. tunicola sp. nov. as the sister species to P. aura within a well-supported clade also including P. lingulicola and P. cf. glycymerica. The bright yellow body color of P. tunicola sp. nov. in life is similar to that of P. aura, however, these two species are distinguished by the former not having modified posterior notochaetae. The symbiotic nature of the association between P. tunicola sp. nov. and styelid ascidians is discussed.