We report a single whale bone associated with many molluscan fossils from the Omma Formation, Lower Pleistocene shallow marine deposits, along the Sai-gawa River, Kanazawa City, in central Japan. Most molluscan species which are commonly found in the Omma Formation show disarticulated and/or damaged shells, indicating semi-autochthonous or allochthonous modes of occurrence. However, the assemblage contained chemosynthetic bivalves, such as lucinid, solemyid and thyasirid bivalves, which are rare in the Omma Formation. The lucinids and solemyids show a high articulation ratio, along with some predatory and scavenging gastropods, such as naticids, nassariids and borsoniids whose well-preserved shells indicate an autochthonous mode of occurrence. In addition, most of the lucinid bivalves show an umbo-upward position similar to the life position of Recent species. Recent lucinid, solemyid and most thyasirid bivalves harbor chemosymbiotic bacteria in their gills and are well known members of the chemosynthetic community. These lines of evidence indicate that the community, mainly comprising lucinid bivalves and other autochthonous molluscan species associated with the whale bone, is an ancient whale-fall community. This shallowest fossil whale-fall community differs from deep-water cases in the dominance of infaunal bivalves, such as lucinids, and in the lack of epifaunal and semi-infaunal chemosynthetic bivalves, such as bathymodiolins and vesicomyids. This community supports a previous suggestion that the difference in characteristic species of the whale-fall communities depends on the water depth.
Introduction
The whale carcass is the largest organic matter supplied to the seafloor. The carcass creates a sulfide-rich environment on the seafloor, which is inhabited by characteristic invertebrates such as mollusks with sulfur-oxidizing bacteria in their body. These characteristic faunal assemblages of whale-fall communities are similar to the communities found around hydrocarbon seeps and hydrothermal vents in the deep sea (Smith et al., 1989, 2015; Smith and Baco, 2003). At least some animals of the whale-fall communities have ancestors that lived in vents and seeps. These features prompted the hypothesis that whale carcasses may have acted as agents of dispersal and as evolutionary stepping stones for taxa of hydrocarbon seeps and hydrothermal vents (Distel et al., 2000; Smith and Baco, 2003), although recent network analysis has questioned importance of the whale-fall community in the dispersal of vent and seep organisms (Kiel, 2016; see also discussions by Smith et al., 2017 and Kiel, 2017). Hence, revealing the spatiotemporal change in the whale-fall communities is important to understand the evolution of the deep-sea ecosystem. However, fossil records of whale-fall communities are scarce and there is a need to discover more material. Sahling et al. (2003) showed that the community structure of cold seep communities is related to ocean depth. Seep communities in shallow waters usually lack epifauna and semi-infauna in contrast to communities in deep waters, which have both epi- and infauna. This could be because of the higher predatory pressure in shallow water than in the deep ocean and/or other physicochemical properties (Sahling et al., 2003). Nevertheless, studies of faunal composition of whale-fall communities in relation to depth have been limited so far due to the paucity of reports on shallow-water whale-fall communities. Until now, only a single ancient whale-fall community, including chemosynthetic mollusks, from an obviously shallow-water setting (shallower than the outer shelf) has been recorded from Italy (Dominici et al., 2009; Danise et al., 2010; Danise and Dominici, 2014). Reports on shallow-depth whale-fall communities are limited not only by ancient records, but also in the modern ocean. Several experimental studies have identified taxa specialized for whale-falls such as the annelid Osedax from whale carcasses deployed in shallow water (Dahlgren et al., 2006; Fujiwara et al., 2007). This suggests that shallow-water whale-fall communities exist in both modern and ancient oceans, and there is a need to identify characteristics of more shallow-water whale-fall communities.
Figure 1.
Locality map of the single whale bone (ISKW-Fo-0000008) associated with the Omma whale-fall community from the Okuwa area, Kanazawa City, Japan. A, Map of Kanazawa City, central Japan; B, Detailed map with distribution of formations. The Omma whale bone was found from the area indicated by a dashed-line circle (Matsuura, 1996b, figure 2). The map was redrawn based on Kitamura (1991), Matsuura (1996b), and Yamada et al. (2017).
In this paper, we report an example of a shallow-water whale-fall community from the Pleistocene Omma Formation in Kanazawa City, Ishikawa, central Japan.
Geological setting
The Omma Formation is characterized by sandstones with episodic shell beds and is exposed in the type section along the Saigawa River in Okuwa, Kanazawa City (Figure 1; Motiduki, 1930; Ichihara et al., 1950). The type section of the Omma Formation is subdivided into the lower, middle, and upper parts by litho- and biofacies (Kitamura and Kondo, 1990). Kitamura et al. (1994) revealed cyclic changes in sedimentary facies and molluscan species composition due to glacial and interglacial cycles with a 41,000-year-periodic sea-level change during the Early Pleistocene.
The whale bone identified as Balaenopteridae gen. et sp. indet. reported herein was recovered from the lower part of the Omma Formation (Matsuura, 1996b, 2009, pl. Ⅵ-8, fig. 4). Matsuura (1996b) indicated the approximate sampling point of the specimen (Figure 1; Matsuura, 1996b, fig. 2).
The age of the lower part of the Omma Formation at the type locality has been assigned based on the nannofossil occurrences as Early Pleistocene, dated approximately at 1.5 to 1.4 Ma (Kitamura, 2016). According to the molluscan assemblages, the Omma Formation was deposited between low-tide and a depth of 120 m. These depth changes correspond to the glacial-interglacial sea-level changes (Kitamura, 1991).
Figure 2.
Right radius bone of Balaenopteridae gen. et sp. indet. (ISKW-Fo-0000008) from the Omma Formation. The bone was covered with carbonate concretion with many invertebrate fossils. Estimated upper side (A) and lower side (B) of the whale bone when deposited on the seafloor. Upper-lower direction has been determined by the lucinid shell's geopetal structure (Figure 4B). Arrows indicate Lucinoma sp., which possessed sulfur-oxidizing bacteria.
Materials and methods
The specimen in this study is the right radius bone of a balaenopterid whale and stored at the Ishikawa Prefectural Natural History Museum as repository number ISKW-Fo-0000008 (Matsuura, 1996b, 2009; Matsuura and Nagasawa, 2000). The whale bone, found by Toshiharu Ota in 1993, was found parallel to the bedding plane (Matsuura, 1996b, fig. 3). The bone is ca. 0.8 m long and 0.3 m wide, and it is covered with 10 to 20 mm thick cemented fine-grained sandstone as a concretion. The concretion contained many invertebrate fossils, such as gastropods, bivalves, and echinoderms (Figure 2).
Invertebrate fossils in the concretion were mechanically prepared by using air scribe and chisels. The invertebrate specimens were identified to the lowest taxonomic levels possible and the individual number of each species was counted. For the bivalves, each valve is considered half of an individual. The articulation ratio for bivalves was calculated as N1/(N1 + N2) × 100 (%), where N1 and N2 denote the number of articulated and disarticulated individuals, respectively.
Umbonal orientations of all the articulated chemosynthetic bivalves, Lucinoma sp., were measured to assess whether the species maintained their original life position. The orientations were measured against the bedding plane. Since there was no obvious indication signifying the upside deposition of the bone in Matsuura (1996b), we determined the bedding plane and upside using geopetal structures, which are visible in several articulated bivalve specimens within the concretion.
Results
Molluscan fossils
The molluscan species identified from the cemented sediment surrounding the bone are listed in Table 1. A total of 20 molluscan species were found, comprising 12 gastropods and eight bivalves, as well as one echinoid species (Figure 3; Table 1). The most common species was Lucinoma sp., which has a moderate size ranging from 16.7 to 40.9 mm in shell length, a high articulation ratio (94.7%), with some situated very close to the bone (Figure 4A). The rest of the bivalves were disarticulated except for a single Acharax sp. Among the identified gastropods, three species, nassariids Reticunassa, borsoniids Suavodrillia declivis and Ophiodermella? sp., and several specimens of Euspira are not fragmented nor abraded, suggesting almost no transportation.
Table 1.
List of invertebrate fossils from the concretion enclosing the whale bone (ISKW-Fo-0000008). A single valve was counted as a half individual for bivalve. *: One individual of Lucinoma could not be judged as disarticulated or articulated, therefore we counted as 0.5 individual. Trophism information is derived from the Encyclopedia of life, available from https://eol.org (accessed January 18, 2020). The Bathymetric ranges are based on Okutani (2000), Ogasawara (1977), and Matsuura (1985) for mollusks and the database of Smithsonian Natural Museum Invertebrate Zoology collection for echinoids, available from https://collections.nmnh.si.edu/search/iz/.
Orientation of Lucinoma
The umbonal direction of Lucinoma sp., relative to the bedding plane, determined from the geopetal structure within a single Lucinoma specimen (Figure 4B), is as shown in Figure 5. Among the total 19 specimens of Lucinoma sp., 15 showed an umbo upward position, resembling the life orientation of Recent lucinids (Stanley, 1970).
Figure 3.
Photographs of selected molluscan fossils from the concretion enclosing the whale bone (ISKW-Fo-0000008). A, Suavodrillia declivis (Martens, 1888); B, Turritella (Neohaustator) saishuensis (s.l.); C, Euspira pila (Pilsbry, 1911); D, Reticunassa spurca (Gould, 1860); E, Cyclocardia ferruginea (Clessin, 1888); F, Felaniella usta (Gould, 1861); G, Thyasira tokunagai Kuroda and Habe, 1951; H, Yoldia (Cnesterium) notabilis Yokoyama, 1922; I, J, Acharax sp.; K, Lucinoma sp.; Scale bars for A–J, 5 mm; K, 10 mm.
Figure 4.
Characteristic mode of occurrence of Lucinoma sp. within concretion enclosing the whale bone (ISKW-Fo-0000008). A, Lucinoma sp. situated in proximity to the whale bone. The white arrow indicates exposed area of the whale bone surface. B, Three Lucinoma sp. found on the proximal end of the bone. One of the Lucinoma (white arrow) shows the geopetal structure indicating upward direction (depositional upward is same as upward directions of the figure).
Figure 5.
Umbonal directions, relative to the estimated bedding plane by geopetal structure (Figure 4B), of all the articulated Lucinoma specimens, n = 19, from the concretion enclosing the whale bone (ISKW-Fo-0000008) are shown as a Rose diagram.
Discussion
Recognizing the whale-fall community
Autochthonous bivalve species associated with the whale bone, Lucinoma sp. and a single individual of Acharax sp. (Figure 3; Table 1) were not transported for the following reasons. Both species showed high articulation ratios; furthermore, Lucinoma sp. showed an umbo upward position similar to the life position of their modern relatives. Other identified bivalves associated with the whale bone were considered common and cold-water species in the Omma Formation (Ogasawara, 1977; Kitamura, 1991; Matsuura, 1996a), and these were disarticulated. Although disarticulation may indicate transportation, well-preserved thin shells suggest that those bivalves were transported either a very short distance or washed out from sediments at their living site. Although Lucinoma had been previously found from the Omma Formation, it was very rare and never a dense occurrence (Kaseno and Matsuura, 1965; Ogasawara, 1977; Kitamura, 1991; Matsuura, 1996a). Thus, this is the first time abundant and densely distributed Lucinoma sp. were found from the Omma Formation.
All investigated species of Recent lucinid bivalves possess chemosynthetic sulfur-oxidizing bacteria in their gills (Taylor and Glover, 2000), and dense populations of lucinid bivalves are generally found at cold seeps (Callender and Powell, 1997) and in oxygen-minimum zones (Bottjer et al., 1995; Oliver and Holmes, 2006). Acharax are also known to harbor chemosynthetic bacteria in their gills (Reid, 1990) and are generally present in seeps, vents, whale-falls, and other oxygen-depleted environments (Reid, 1990; Dufour, 2005; Braby et al., 2007). In addition, most Thyasira species possess chemosynthetic bacteria (Dufour, 2005). Therefore, Thyasira tokunagai associated with the bone might be a member of the Omma whale-fall community, although it was found as disarticulated valves. Thyasirids originally lacked teeth, therefore shells are easily separated into two valves, facilitating its disarticulation.
The Omma Formation shows no evidence of either a cold-seep or an oxygen-minimum environment. Thus, the possible hydrogen sulfide source for the chemosynthetic bivalves, Lucinima sp., Acharax sp. and Thyasira tokunagai, was most likely released from the whale carcass during its decay, and we interpret this fossil association from the lower part of the Omma Formation as an ancient whale-fall community, calling it the Omma whale-fall community. The presence of chemosynthetic organisms in the Omma whale-fall community indicates that the whale-fall was in the sulphophilic stage of the ecological successional stages proposed by Smith and Baco (2003). We consider that relatively well-preserved carnivorous and scavenging gastropods, for example, naticids and nassariids, might also be members of the whale-fall community in addition to the lucinids and solemyid bivalves.
It is noteworthy that a single whale bone can support a chemosynthetic community. We do not know the minimum size of a whale bone that can maintain a whale-fall community. Pyenson and Haasl (2007) showed that a Miocene whale-fall community dominated by vesicomiyd bivalves was sustained by a partially articulated small baleen whale bones (estimated body length; 3.3 m). In addition, Jenkins et al. (2017) reported the Cretaceous reptile-fall community sustained by a basal leatherback sea turtle (estimated total carapace length of 700 mm). A modern experimental study showed a deployed whale skull sustained Adipicola sp., a chemosynthetic bivalve, at the water depth of ca. 880 m off the northwest Chatham Islands, New Zealand (Lorion et al., 2010). These results demonstrate that 1-m-sized bone would be of sufficient size to sustain whale-fall communities.
Formation process of the Omma whale-fall community
The whale bone was found in a single disarticulated condition in a shell bed with many fragmented molluscan fossils. Apparently, the whale bone was transported from a much shallower environment along with the allochthonous molluscan fossils because of its single disarticulated mode of occurrence. On the other hand, dead whales can float because of their increasing buoyancy caused by methane and/or other gases produced during the decay (Allison et al., 1991). Thus, it is possible that only the right limb was disarticulated while the dead whale was floating, and subsequently it sunk to the sea floor. The deposited paleodepth is estimated at 20 to 60 m deep, based on the obtained molluscan and echinoid fossils such as Punctoterebra lischkeana and Felaniella usta. Although we do not know how the bone was transported to its depositional place, the isolated bone was quickly and completely buried in sediment based on the lack of the encrusting organisms.
Table 2.
Fossil whale-fall communities from Japan with information on formation, age, paleodepth, and generic compositions. For the Omma whale-fall community, it is uncertain that the Thyasira was a member of the whale-fall communities, therefore, it is noted in brackets.
Sulfate reduction, a process by which hydrogen sulfide is produced during the decay of organic matter in or around the bone, would have occurred within the sediment because the Lucinoma, known as a deep burrower (Stanley, 1970), autochthonously occurred both on the lower and the upper side of the bone. The sulfate reduction would have continued for at least several years for the lucinid bivalves found around the bone to reach their size of 40.9 mm in length. The occurrence of sulfate reduction is also supported by the carbonate concretion covering the bone. The sulfate reduction process produces bicarbonate ions as a byproduct of hydrogen sulfide, and this increases the alkalinity to precipitate carbonate minerals (Berner, 1968).
Comparison of whale-fall communities
Four fossil whale-fall communities, all from the Miocene, have been reported from Japan (Table 2; Hachiya, 1992, 1993; Amano and Little, 2005; Amano et al., 2007; Jenkins et al., 2018). The Omma whale-fall community reported herein is the youngest and shallowest among the previously reported fossil communities in Japan.
Paleobathymetry revealed that these communities were in the bathyal zone or deeper, although the Nupinai whale-fall could have been deposited at a much shallower depth (see Table 2). The Nupinai Formation, which yielded the Nupinai whale-fall community, was possibly formed in shallow water, because paleobathymetry roughly estimated the depth to be 50 m to 500 m based on molluscan fossil assemblages (Amano et al., 2007). Although the estimated depth slightly overlaps the paleobathymetry of the Omma Formation, which is estimated at 20 to 60 m deep, the Nupinai Formation would have been formed in much deeper environments than that of the Omma Formation. It possibly formed on the outer shelf because the Nupinai Formation is mainly composed of mudstone, whereas the Omma Formation is composed of sandstone. Characteristic molluscan species of previously known Japanese fossil whale-fall communities are epifaunal mussels Adipicola and gastropods Provanna and semi-infaunal clams Vesicomya and Calyptogena (see Table 2). On the contrary, the Omma whale-fall community is characterized by infaunal Lucinoma with no epifaunal or semi-infaunal species. A similar situation was reported in the late Pliocene Orciano Pisano whale-fall community, which is characterized by the abundant occurrence of lucinids and rare epifaunal chemosynthetic species from the shelf deposits of Italy (Dominici et al., 2009), whereas Miocene Carpineti whale-fall community characterized by densely populated epifaunal Adipicola formed on outer shelf to upper slope environments (Danise et al., 2016). Thus, the shallow water whale-fall community is characterized by abundant infaunal chemosynthetic species with no or few epifaunal chemosynthetic species. Several studies on whale carcasses deployed in modern oceans support this conclusion. Danise et al. (2014) reported no epifaunal chemosynthetic bivalves and dominance of an infaunal chemosynthetic bivalve Thyasira, from a whale carcass deployed at the 125 m depth off the Swedish west coast. Fujiwara et al. (2007) reported densely packed Adipicola, epi- and semi-infaunal chemosynthetic bivalves, and infaunal chemosynthetic bivalves, Solemya and Lucinoma, from a whale bone deployed at a depth of 200 to 300 m off Japan. This combination of fossil and modern whale fall studies suggests transition depths to have little or no contribution to the epifaunal chemosynthetic bivalves within the outer shelf.
The lack of epifauna is similar to the community structures in hydrocarbon seeps in shallow environments (Sahling et al., 2003). The lack of epifaunal species in seep environments could be attributed to several factors: for example, predators could eliminate epifaunal species in shallow environments, as well as physicochemical factors, such as bottom water currents, sedimentation regimes, and oxygen concentration (Sahling et al., 2003). These possible reasons for seep community structure can also be applied to the whale-fall community. We could not specify reasons why the Omma whale-fall community did not include epifaunal chemosynthetic bivalves, although burying can be recognized as a possible factor because the dense populations of lucinid were found on both the upper and lower sides of the whale bone. The fast sedimentation rate or rapid burial at a shallow depth produced the bone's sedimentary cover, which in turn caused the loosening of hard substrates for sessile epifauna, such as Idas and Adipicola as suggested by Amano et al. (2007). Furthermore, the relatively deep burial of the bone makes it difficult to access hydrogen sulfide released from the decaying bone at the sea floor level. As a result, semi-infaunal chemosynthetic bivalves, e.g. vesicomyids, could get enough hydrogen sulfide at the sea floor level. In contrast to these epifauna and semi-infauna, many lucinid bivalves can burrow deeply (Stanley, 1970), thereby avoiding predation and allowing hydrogen sulfide uptake in relatively deeper sediment.
Our finding suggests that the shallow water whale-fall community begins to form after the carcass is buried. This can also occur in the modern oceans, but the community would not be visible from sea floor observations. There is a need for further exploration of shallow water whale-fall communities under the sea floor and/or experimental studies on deployed whale carcasses.
Conclusion
We report a whale-fall community found from the Lower Pleistocene Omma Formation in Ishikawa Prefecture, Japan. The community is characterized by a dense population of lucinid bivalves with a single solemyid bivalve. This is the second report in the world of a fossil shallow-water whale-fall community dominated by infaunal lucinid bivalves. Together with the first record of the Italian Orciano Pisano whale-fall community (Dominici et al., 2009), this finding suggests that shallow water whale-fall communities were characterized by infaunal species. The possible reasons for the dominance of infaunal species in shallow water whale-falls include higher predatory pressure and faster deposition rate at shallow depths than in deep water, similar to the reasons for their absence in cold seep communities (Sahling et al., 2003).
Acknowledgments
We thank Amano Kazutaka, an anonymous reviewer and editors for polite, insightful, and constructive comments that improved the quality of this article. For their assistance with museum collections under they care, we thank Y. Katsura and M. Mitani (both at the Ishikawa Prefectural Natural History Museum) for allowing us to use the material. We also thank K. Sato (Waseda University) for helping with the identification of the solemyid bivalve. The research was supported by JSPS KAKENHI Grant Number 19K21898 and 16H05740.
References
Appendices
Author contribution
A.S. is primarily responsible for the observations and identification of fossil material, and overall context of the research. R.G.J. was found the material at the Ishikawa Prefectural Natural History Museum and realized possibility of the material as a fossil whale-fall community. Both wrote the manuscript together.
