Observations on the Life History and Geographic Range of the Giant Chemosymbiotic Shipworm Kuphus polythalamius (Bivalvia: Teredinidae)

Abstract

Kuphus polythalamius (Teredinidae) is one of the world's largest, most rarely observed, and least understood bivalves. Kuphus polythalamius is also among the few shallow-water marine species and the only teredinid species determined to harbor sulfur-oxidizing chemoautotrophic (thioautotrophic) symbionts. Until the recent discovery of living specimens in the Philippines, this species was known only from calcareous hard parts, fossils, and the preserved soft tissues of a single large specimen. As a result, the anatomy, biology, life history, and geographic range of K. polythalamius remain obscure. Here we report the collection and description of the smallest living specimens of K. polythalamius yet discovered and confirm the species identity of these individuals by using sequences of three genetic markers. Unlike previously collected specimens, all of which have been reported to occur in marine sediments, these specimens were observed burrowing in wood, the same substrate utilized by all other members of the family. These observations suggest that K. polythalamius initially settles on wood and subsequently transitions into sediment, where this species may grow to enormous sizes. This discovery led us to search for and find previously unidentified and misidentified wood-boring specimens of this species within museum collections, and it allowed us to show that the recent geographic range (since 1933) of this species extends across a 3000-mile span from the Philippines to Papua New Guinea and the Solomon Islands.

Secondary Metabolism in the Gill Microbiota of Shipworms (Teredinidae) as Revealed by Comparison of Metagenomes and Nearly Complete Symbiont Genomes

“…Several shipworm species, such as Kuphus polythalamius, live in other substrates. For example, K. polythalamius is often found in sediment habitats (as well as in wood) where its gill symbionts are crucial to sulfide oxidation and carry out carbon fixation (7,22). K. polythalamius lacks significant amounts of cellulolytic symbionts such as T. turnerae and instead contains Thiosocius teredinicola, which oxidizes sulfide and generates energy for the host (23).…”

A rock-boring and rock-ingesting freshwater bivalve (shipworm) from the Philippines

“…All previously described shipworm genera are obligate wood-borers [2,3], including the giant chemoautotrophic shipworm Kuphus polythalamius , which has been shown to inhabit wood early in its life cycle and is now thought to transition to sediments after initial settlement and metamorphosis on wood [5]. However, it seems unlikely that L. abatanica makes a similar transition from wood to rock.…”

“…As the 18S and 28S rRNA gene sequences from both specimens (lot PMS-4316M) were identical, sequence data from only one specimen was concatenated and aligned as in Distel et al [9] and Shipway et al . [7] with sequences representing 11 of 17 recognized genera of Teredinidae [2,5,7,10,11] including: Bankia Gray 1842, Dicyathifer Iredale 1932, Kuphus Guettard 1770, Lyrodus Gould 1870, Nausitora Wright 1864, Neoteredo Bartsch 1920, Spathoteredo Moll 1928, Teredo Linnaeus 1758, Teredora Bartsch 1921, Teredothyra Bartsch 1921, and Tamilokus Shipway, Distel & Rosenberg, 2018, as well as 39 bivalve reference taxa. Phylogenetic analysis was performed using M r B ayes v. 3.2.6 [12] with the GTR + I + Γ nucleotide substitution model as selected using j M odel T est v. 2.1.10 [13] with Akaike Information criterion.…”

“…All teredinids described to date are obligate wood-borers that can complete all or part of their entire life cycle within wood [2,4,5]. This includes the giant, chemoautotrophic shipworm, Kuphus polythalamius Linnaeus 1767 , which has recently been shown to settle on and reach maturity in wood prior to entering the sediment [5]. Remarkably, Lozouet & Plaziat [6] reported a shipworm species, provisionally identified as Spathoteredo sp., but known by the locals as ‘antingaw’, living in a ‘mudstone’ cliff along the Abatan River, Bohol, Philippines.…”

Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius

“…Like most animals that consume wood, teredinids rely on heterotrophic (cellulolytic) bacterial symbionts to supply enzymes that aid in the digestion of wood [5][6][7]. Unlike more typical members of the family Teredinidae, K. polythalamius inhabits both wood and organic-rich marine sediments [8]. It was recently shown that this atypical species harbours intracellular thioautotrophic symbionts instead of cellulolytic bacteria in its gills [9].…”