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Macrosymbiotic association of the myid bivalve Cryptomyawith thalassinidean shrimps: Examples from modern

and Pleistocene tidal flats of Japan

Masakazu Nara a,⁎, Hirotsugu Akiyama b, Gyo Itani c

a Center for marine Environmental Studies, Ehime University, Matsuyama 790-8577, Japanb Department of Biology and Earth Sciences, Graduate School of Science and Engineering, Ehime University, Matsuyama 790-8577, Japan

c Department of Biology, Faculty of Education, Kochi University, Kochi 780-8520, Japan

Received 27 September 2007; received in revised form 24 December 2007; accepted 7 January 2008

Abstract

Macrosymbiosis, a macroscopic-scale interspecific association, between the myid bivalve Cryptomya and thalassinidean shrimps is described.In modern tidal flats, living individuals of Cryptomya truncata are observed to protrude their posterior ends into the burrow lumen ofthalassinidean shrimps such as Nihonotrypaea japonica and Upogebia yokoyai. Furthermore, a fossil impression of Cryptomya busoensisoccurring in a Pleistocene tidal flat deposit of the Shimosa Group, similarly has attached its posterior end to a fossil upogebiid burrow,Psilonichnus isp. Both Cryptomya species, which are characterized by extremely short siphons, probably utilize the sediment/water interfaceon the internal surface of the burrow. As the fossil record of Cryptomya dates back to the Miocene and such a mode of occurrence can berecognized even in the rock record, careful observation would be expected to reveal the origin and evolution of the characteristic macrosymbiosis.© 2008 Elsevier B.V. All rights reserved.

Keywords: Macrosymbiosis; Cryptomya; Thalassinidean shrimps; Recent; Pleistocene; Japan

1. Introduction

Symbiosis was originally defined as a strict association ofindividuals belonging to two or more species, regardless ofwhether or not they are mutually advantageous (Bary, 1879 inSavazzi, 2001). AmongBivalvia, two categories of symbiosis canbe recognized, namely, microsymbiosis and macrosymbiosis(Savazzi, 2001). The former is referred to the case wheremicroscopic endosymbionts live within a host bivalve (Savazzi,2001). Most of the studies on symbiosis in bivalves can beclassified in this category, because photosymbiosis and chemo-symbiosis, of which endosymbionts aremicroscopic zooxanthellaor bacteria that oxidize sulphides or methane, have receivedmuchattention (e.g., Majima, 1999; Savazzi, 2001; Pervesler andZuschin, 2004; and references therein). On the other hand,

macrosymbiosys is a symbiotic association that can be recognizedat a macroscopic scale (Savazzi, 2001). Although macrosymbio-sis is easily recognized in fossil records if the associatedorganisms are preserved in situ, this has received less attention(Savazzi, 2001).

Savazzi (2001) made a comprehensive review of bivalves'macrosymbioses, and stressed such examples as embedment orattachment of bivalves to host animals, and as bivalves thatprovide habitats for other macrosymbionts. The other style ofmacrosymbiosis, which likely has high preservation potential inthe rock record and therefore is worth considering in palaeo-ecology, is that mediated by a burrow system of a host animal asseen in the small myid bivalve Cryptomya.

Cryptomya is a somewhat compressed bivalve (Keen, 1969),characteristically having extremely short siphons (e.g., Yonge,1951; MacGinitie and MacGinitie, 1968; Haderlie and Abbott,1980; Lawry, 1987; Itani and Kato, 2002). Macrosymbioticassociation of Cryptomya with the other organisms was first

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⁎ Corresponding author. Fax: +81 899279654.E-mail address: nara@sci.ehime-u.ac.jp (M. Nara).

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mentioned by MacGinitie (1934) through his work on thenatural history of the burrowing thalassindean shrimps ofUpogebia pugettensis and Callianassa californiensis. He foundthat Cryptomya californica had attached to burrows of theshrimps and inferred a macrosymbiotic relationship for theseanimals (MacGinitie, 1934; MacGinitie and MacGinitie, 1968).Later, Lawry (1987) observed Cryptomya californica occurringin sandy mudflats of Oregon, USA. According to his ob-servations, Cryptomya californica burrowed beneath the sea-floor, down to 50 cm (Lawry, 1987). Because the bivalve withvery short siphons embedded a part of its shells into the tunnelsof C. californiensis, he confirmed this as a macrosymbioticassociation (Lawry, 1987).

Swinbanks (1981) reported a resin burrow cast of C. cali-forniensis, which had been attached to by many individuals ofCryptomya sp. Although the report was quite instructive ofCryptomya's ecology, it consisted of only one photograph witha brief caption, on a single page of a journal, and details of theinterspecific relationships were not described. This contributionthereafter was made more widely known by Bromley (1996,p. 110) with an informative illustration on macrosymbiosisbetween the clams and shrimps.

The other species of genus Cryptomya, i.e., C. truncata(=Venatomya (Cryptomya) truncata of Okutani, 2000), whichis distributed from central Japan to the East China Sea (Habe,1977; Okutani, 2000), usually occurs sympatrically with suchdeep-burrowing thalassinidean shrimps as Nihonotrypaeajaponica (formerly Callianassa japonica; cf., Manning andTamaki, 1998), Upogebia major and Upogebia yokoyai (Itaniand Kato, 2002). The clams sometimes occur in sediment, a fewmillimetres aside from the thalassinidean shrimp burrows facingtheir posterior ends to the burrows (Itani and Kato, 2002). Basedon such observations, Itani and Kato (2002) also inferredmacrosymbiotic relationships between the shrimps and theclams.

Although macrosymbiosis of Cryptomya has attractedattention as noted above, direct evidence that the siphons ofthe clams were connected to the burrow lumen has not beenshown, except for the Swinbanks' (1981) photograph. Also, the

detailed structure of the connecting portion has not beendescribed. This is probably because the clams commonly wereliving in waterlogged, sandy sediments that are too crumbly toallow easy observation.

Recently, Akiyama and Nara (2007) introduced a techniqueto observe intact three-dimensional sediment fabrics of tidalflats, using a shovel-like apparatus and a peeling technique, andfound burrow systems of U. yokoyai and N. japonica, on whichwere attached many living individuals of C. truncata, fromsandy mudflats of southwestern Japan. Although they pointedout the possibility of the macrosymbiotic relationship betweenthe shrimps and the bivalves, detailed description and dis-cussion were not made.

On the other hand, such an association has also been re-cognized from the rock record. A fossil upogebiid burrowrepresenting Psilonichnus isp. (Nara and Kotake, 1997) andan associated fossil impression of Cryptomya busoensis werefound in Pleistocene tidal flat deposits of the Shimosa Group,which is distributed in the southeastern part of the Kantodistrict, central Japan (cf., Nara and Kotake, 1997).

The aims of this paper are to describe the associated oc-currence of C. truncata with the thalassinidean burrows anddetailed structures of the point of connection, in the moderntidal flat sediments, along with the Pleistocene examples ofC. busoensis.

2. Localities studied

Observations were made in modern tidal flats developed inthe mouth of the Kamo River of the Ehime Prefecture,southwestern Japan, and in tidal flat deposits of the middlePleistocene Yabu Formation in the Boso Peninsula, ChibaPrefecture, central Japan. Descriptions of the localities are asfollows.

The former observations were made in the mouth of theKamo River, which runs into the Seto Inland Sea (Fig. 1).Living specimens of Cryptomya truncata were found in thesandy mudflats where biogenic mounds formed by the cal-lianassid shrimps, Nihonotrypaea japonica, occur commonly.

Fig. 1. Locality maps showing the study point and the modern tidal flats developed in the Kamo River.

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Small burrow apertures of the upogebiid Upogebia yokoyai,which are not associated with biogenic mounds, are alsocommon in the sea floor.

The latter observations were made on outcrops in the south ofShuku (for locality and stratigraphy, see Nara and Kotake, 1997),which is one of the type localities of the Yabu Formation. Theobserved section consists of thinly alternating beds of mud andsandy mud, and intensely bioturbated, mottled sandy mud.Couplets of mud drapes, suggesting tidal influences (Nio andYang, 1991), occur locally. Intertidal to shallow subtidalmolluscan fossils, such as Raeta periculla and Anadara brought-oni, are seen at these horizons. Probable upogebiid burrows, thePsilonichnus isp. of Nara and Kotake (1997), which arecharacteristically seen in tidal flat or shallow bay deposits (Naraand Kotake, 1997), occur abundantly at these levels. Thesesuggest that the sedimentswere deposited under tidally influencedshallow to marginal marine conditions such as tidal flats.

3. Methods

In the Kamo River tidal flats, live specimens of Cryptomyatruncatawere collected through careful digging with shovels, andburrowing depths of the clams were recorded. Internal surfaces ofthe thalassinid burrow were observed on surfaces of excavatedsediment blocks. Peels were taken of some of the block surfacesusing hydrophilic polyurethane grout (OH-1Aof TOHOChemicalIndustry). This peeling technique, developed by Akiyama andNara (2007), allowed observation of the detailed 3-D structure ofthe burrows, ambient sediments, and attached C. truncata.

Pleistocene fossil impressions and associated fossil burrows,Psilonichnus isp. of Nara and Kotake (1997), were observed on

an outcrop surface. Although the muddy linings occurring inmuddy sediments are commonly inconspicuous in a scraped andtrimmed outcrop surface, they are easily observed on the naturallyweathered surface, as a result of differential weathering.

4. Descriptions

In the Kamo River, many living specimens of Cryptomyatruncata were collected from within the sediment, commonlydeeper than 5 cm from the surface. Some of the specimens wereburied up to 20 cm below the surface, but maximum depth ofburial is uncertain due to limited observations. These bivalvesare positioned with their posterior ends attached to the burrowsof Upogebia yokoyai or Nihonotrypaea japonica (Fig. 2). Theirposterior ends are stuck into the burrow linings (Fig. 2B).Viewed from the inside of the burrow, the posterior tips of theshells projected slightly beyond the inner surface, from slit-likeapertures about 4 mm long and 1 mm wide (Fig. 2C).

Fossil impressions of Cryptomya busoensis were found inthe above-mentioned outcrop surface. As the fossil-bearingsediments are semiconsolidated, most of the impressions arepartially eroded. Association of the bivalves and the burrows arethus not preserved in most cases. However, a nearly completespecimen was found (Fig. 3). It occurred in juxtaposition withthe fossil burrow, and its posterior end applied to the burrowwall (Fig. 3B and C).

5. Discussion and conclusions

As noted earlier, Cryptomya possesses extremely shortsiphons (Yonge, 1951; Haderlie and Abbott, 1980; Lawry,

Fig. 2. Photographs of modern Cryptomya truncata (=Venatomya (Cryptomya) truncata of Okutani, 2000) showing life positions. (A) C. truncata attached to aburrow of Upogebia yokoyai. Vertical surface of a sediment peel. (B) C. truncata attached to a burrow of Nihonotrypaea japonica (formerly Callianassa japonica),seen on a sediment peel, plan view. Both of the peels showing three-dimensional relief were collected using a technique developed by Akiyama and Nara (2007).(C) Inside view of a burrow of U. yokoyai. The bivalves clearly formed slit-like apertures and slightly protruded their posterior ends into the burrow lumen (arrows).

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1987; Itani and Kato, 2002). It is thus unlikely that Cryptomyatruncata, living deep within sandy mud, can have direct con-nection to the sediment surface. Judging from the facts thatmany C. truncata had attached themselves to the walls ofthalassinidean burrows (Fig. 2A and B) and protruded theirposterior ends into the burrow lumen (Fig. 3), the clamsprobably utilize the sediment/water interface in the burrow, inorder to take food and oxygen, and to expel wastes (Fig. 4).Such a life-style habit probably protected C. truncata frompredation or such environmental stresses as desiccation andsevere fluctuation of temperature and salinity, as is known forCryptomya californica.

On the other hand, this association seems to be disadvanta-geous for the thalassinidean shrimps. In fact, Griffen et al.(2004) estimated that up to 39% of total suspended particles inthe burrow systems of Upogebia pugettensis might be removedby attached C. californica. This association therefore can beregarded as a mild form of parasitism of the bivalve, albeitwithout a direct physical contact with the host shrimp.

In the case of the Pleistocene example of Cryptomyabusoensis, on the other hand, direct evidence of the symbioticassociation, as for C. truncata, cannot be obtained. However,the mode of the fossil occurrence, i.e., preserved in life position,facing its posterior end to the fossil thalassinid burrow (Fig. 3),is closely similar to that of C. truncata or other Cryptomyaspecies described above. In addition, Itani and Kato (2002) alsoreported that C. busoensis co-occurred with Upogebia majorin modern tidal flats in Japan. In the subsurface cores of

the Japanese Holocene, specimens of C. busoensis also occurexclusively in sandy mud where large fossil burrows are abun-dantly observed (Ishihara et al., 2004). These strongly suggestthat C. busoensis also possesses macrosymbiotic relationshipswith thalassinidean shrimps.

Itani and Kato (2002) made extensive observations ofC. truncata occurring in various tidal flats of Japan andconsidered that several thalassinidean shrimps such as

Fig. 4. Schematic diagram showing macrosymbiotic association of Cryptomyawith a thalassinidean shrimp. The clam, living at a few decimetres depth beneaththe sediment surface, utilized the burrow of the shrimp as a sediment/waterinterface to exchange water carrying food and oxygen.

Fig. 3. The Pleistocene examples. (A) Outcrop surface where Cryptomya busoensis occurs (middle Pleistocene, Yabu Formation). (B) Impressions of C. busoensis.(C) Sketch of the photograph B. One of the bivalves attached its posterior end to the fossil upogebiid burrow of Psilonichnus isp. of Nara and Kotake (1997). Thismode of occurrence strongly suggests a macrosymbiotic association between C. busoensis and the upogebiid shrimp.

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Upogebia major, Upogebia yokoyai, Upogebia carinicauda,and Nihonotrypaea japonica, had direct associations with theclam. They also mentioned Upogebia narutensis, Upogebiaissaeffi and Upogebia pugnax as possible symbiotic hosts of C.truncata, because the clams also co-occurred with the shrimps(Itani and Kato, 2002). Cryptomya californica, on the otherhand, has been reported to utilize not only burrows of theshrimps but also those of the polychaete Arenicola brasiliensis,or the echiurid Urechis caupo (MacGinitie, 1934; MacGinitieand MacGinitie, 1968; Lawry, 1987). A. brasiliensis and Ure-chis sp. also occur in the Kamo river tidal flats treated here, butassociation of C. truncata with such animals has not beenobserved.

As discussed above, some species of the myid bivalveCryptomya are interpreted to show the macrosymbiotic asso-ciation with thalassindean shrimps. Such a symbiotic life habitmay be common in the species of Cryptomya. As the fossilrecord of Cryptomya dates back to the Miocene (Keen, 1969),further observations of mode of Cryptomya occurrence inthe rock record might reveal the origin or evolution of itsmacrosymbiosis with the thalassinidean shrimps.

Acknowledgements

Dr. R.G. Bromley kindly reviewed the manuscript and gavevaluable comments. Comments from the reviewer (Dr. A.G.Beu and an anonymous reviewer) also improved the manu-script. This study was supported in part by Grant-in-Aid No.14740299 and 19540494 provided to MN from the Japan So-ciety for Promotion of Science. These contributions are grate-fully acknowledged.

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