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Bivalve borings, bioclaustrations and symbiosis in corals from the Upper Cretaceous (Cenomanian) of southern Israel
Palaeogeography, Palaeoclimatology, Palaeoecology 414 (2014) 243–245
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo
Bivalve borings, bioclaustrations and symbiosis in corals from the Upper Cretaceous (Cenomanian) of southern Israel Mark A. Wilson a,⁎, Olev Vinn b, Timothy J. Palmer c a b c
Department of Geology, The College of Wooster, Wooster, OH 44691, USA Institute of Ecology and Earth Sciences, University of Tartu, Ravila 14A, 50411 Tartu, Estonia Institute of Geography and Earth Sciences, Aberystwyth University, Aberystwyth, Wales SY23 3DB, United Kingdom
a r t i c l e
i n f o
Article history: Received 27 July 2014 Received in revised form 4 September 2014 Accepted 9 September 2014 Available online 16 September 2014 Keywords: Cenomanian Trace fossils Corals Bivalves Symbiosis Israel
a b s t r a c t Specimens of the small compound coral Aspidiscus cristatus (Lamarck, 1801) containing evidence of symbiosis with bivalves have been found in the En Yorqe'am Formation (Upper Cretaceous, early Cenomanian) of southern Israel. The corals have paired holes on their upper surfaces leading to a common chamber below, forming the trace fossil Gastrochaenolites ampullatus Kelly and Bromley, 1984. Apparently gastrochaenid bivalve larvae settled on living coral surfaces and began to bore into the underlying aragonitic skeletons. The corals added new skeleton around the paired siphonal tubes of the invading bivalves, eventually producing crypts that were borings at their bases and bioclaustrations at their openings. When a boring bivalve died its crypt was closed by the growing coral, entombing the bivalve shell in place. This is early evidence of a symbiotic relationship between scleractinian corals and boring bivalves (parasitism in this case), and the earliest record of bivalve infestation of a member of the Suborder Microsolenina. It is also the earliest occurrence of G. ampullatus. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Scleractinian corals and boring bivalves today have complex symbiotic relationships (Kleemann, 1980, 1983, 1994; Morton, 1990). A critical question has been whether the origin of living relationships between corals and endolithic bivalves is relatively recent or has a long evolutionary history back into the Mesozoic (Morton, 1990). Gastrochaenid and lithophagid bivalves have a long record of boring into dead coral substrates (see Kleemann, 1983, and Morton, 1990), but how long have they excavated their domiciles in living corals? Is this coral-bivalve symbiosis one of the many features of the Mesozoic Marine Revolution (Vermeij, 1977; Aberhan et al., 2006) in response to new predatory pressures? As further evidence for the development of this relationship, we describe here an unequivocal symbiosis between a gastrochaenid bivalve (possibly Spengleria) and a compound coral of the Suborder Microsolenina in the Cenomanian (Upper Cretaceous) of southern Israel. 2. Location and geological setting The coral-bivalve symbiosis specimens were found in the En Yorqe'am Formation (early Cenomanian) approximately 20 m from its base in Nahal Neqarot, southern Israel (coordinates: 30.65788°, E 35.08764°; Fig. 1). ⁎ Corresponding author. E-mail addresses: [email protected] (M.A. Wilson), [email protected] (O. Vinn), [email protected] (T.J. Palmer).
http://dx.doi.org/10.1016/j.palaeo.2014.09.005 0031-0182/© 2014 Elsevier B.V. All rights reserved.
The En Yorqe'am Formation in Nahal Neqarot is a chalky argillaceous limestone and marl with a thick oyster-rich unit at its base and a rich abundance of invertebrate fossils above, including calcareous sponges, corals, brachiopods, gastropods, bivalves, ammonites, echinoids and ostracodes (see Arkin and Braun, 1965; Hirsch and Braun, 1994). It has been dated by the occurrence of early Cenomanian ammonites (Avnimelech and Shoresh, 1962; Lewy and Raab, 1976). The environment of the En Yorqe'am deposits was an open marine carbonate shelf formed during an early Cenomanian sea level rise (Hirsch and Braun, 1994). 3. Materials and methods Ten specimens of the compound scleractinian coral Aspidiscus cristatus (Lamarck, 1801) were collected from a surface exposure of the En Yorqe'am Formation (approximately 20 m from its base) in Nahal Neqarot during fieldwork in April 2014. (See locality information above.) The corals are externally well preserved and required no preparation beyond sectioning to reveal details of the ichnofossils. The skeletons were originally aragonitic and have been calcitized. Most internal details of the corals have thus been lost to recrystallization. 4. Systematic paleontology The specimens used in this study are deposited in the National Natural History Collections at The Hebrew University of Jerusalem, Israel (referred herein as HUJ.PAL).
244
M.A. Wilson et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 414 (2014) 243–245 F Zone
LEBANON
SYRIA Mediterranean Sea West Bank
1994 y Lin
Gaza 0 e
ISRAEL
Nahal Neqarot
JORDAN
Fig. 2. Aspidiscus cristatus oral surface with paired apertures of Gastrochaenolites ampullatus visible in the upper half (HUJ.PAL 100-21).
Remarks — The A cristatus corals are found in a marly subunit of the En Yorqe'am Formation that is richly fossiliferous with other scleractinian corals, calcareous sponges, bivalves, gastropods and terebratulid brachiopods. Some of the A. cristatus specimens originally settled on shelly debris, which produced external molds on their undersurfaces.
EGYPT 50 km
4.2. Trace fossils
Fig. 1. Location of Nahal Neqarot in southern Israel.
4.1. Corals The most recent assessment of Aspidiscus cristatus is by Pandey et al. (2011). We are following their taxonomic and morphologic schemes below. Please see that paper for the most recent synonymy list. Order Scleractinia Bourne, 1900. Suborder Microsolenina Morycowa and Roniewicz, 1995. Family Latomeandridae Alloiteau, 1952. Genus Aspidiscus König, 1825. A. cristatus (Lamarck, 1801). Figs. 2–4. Material — Ten complete specimens of A. cristatus, HUJ.PAL 100.20– 100.29. They range in diameter from 20 to 43 mm and height from 8 to 20 mm. Four of these specimens (HUJ.PAL 100.20–100.23) host Gastrochaenolites ampullatus trace fossils. Description — Almost all workers with Aspidiscus describe it as “attractive in shape” (see Thomas and Omara, 1957; Gill and Lafuste, 1987, p. 921; Pandey et al., 2011, p. 33) because of its biscuit-like appearance and elongated monticules on its oral surface. A. cristatus has a circular, colonial corallum with concave aboral and convex oral surfaces. Its calical arrangement is hydnophoroid (meandroid with discontinuous walls). The peripheral crown of A. cristatus is distinct with a sharp margin. Septa are at right angles to the margin and continue across the aboral surface. The aboral surface also has thin concentric growth lines with some folds. No attachment region is present. The oral surface is characterized by short ridge-like monticules. Internal microstructures, such as pennulae, are not visible because of recrystallization.
Ichnogenus Gastrochaenolites Leymerie, 1842 (See Kelly and Bromley, 1984, p. 797, for complete synonymy.). G. ampullatus Kelly and Bromley, 1984. Figs. 2–4. Material. — Four specimens of Aspidiscus A. cristatus contain a total of eight paired apertures of the trace fossil G. ampullatus (HUJ.PAL 100.20–100.23). Description — The apertures of G. ampullatus range from 0.6 to 2.2 mm in diameter, with the apertures within a pair roughly the same size. From center to center, the apertures within a pair range from 1.4 to 4.9 mm apart. The apertures are surrounded by uncut coral skeleton that has in some cases grown slightly upwards along the margin, giving a low chimney-like effect. Three G. ampullatus specimens were vertically sectioned to show cross-sections of the structure. The aperture necks are very short (less than a millimeter on the outside from the aperture to
Fig. 3. Paired apertures of Gastrochaenolites ampullatus in the coral Aspidiscus cristatus (HUJ.PAL 100.21).
M.A. Wilson et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 414 (2014) 243–245
245
Embedding within a live coral host is not easy for bivalve larvae as they must avoid being consumed by the coral's polyps and have a way of penetrating its epithelium down to the aragonitic skeleton. This may be why so few modern bivalves infest living corals (Kleemann, 1982, 1994; Morton, 1990). For those bivalves that establish this relationship, Kleemann (1994) suggests several advantages, including a substrate that increases with growth rather than decreases with continuous bioerosion, and minimal space competition. Kleemann (1994, p. 138) also postulates that there is an advantage to the host coral in this relationship because when the “bivalve has died because of senility, the decaying tissues can provide a nutritial source for the coral”. We suggest that this would be a minimal benefit to the coral at most, outweighed by competition for suspended nutrients with the bivalve, loss of polyp space, and a weakened skeleton due to the boring. We thus consider this example of bivalve-coral symbiosis to have been parasitic. Jagt et al. (2009, p. 140) list G. ampullatus as occurring “in the Maastrichtian type area”, which is the earliest record of the ichnospecies. This Cenomanian occurrence from southern Israel is thus a range extension downwards for G. ampullatus. Fig. 4. Polished cross-section through a specimen of Gastrochaenolites ampullatus in an Aspidiscus cristatus coral (HUJ.PAL 100.21). In the lower left of the chamber are layered carbonates (A) representing boring linings produced by the bivalve. An articulated bivalve shell (B) is preserved in the chamber. The chamber has been roofed over by coral growth (C).
the coral surface) and lead down to a common chamber with an irregular rounded base approximately as wide as the aperture pair above (4.8 to 8.0 mm in the three sectioned specimens). The length of the entire trace from base to apertures ranges from 6.0 to 10.9 mm. The interiors of the chambers contain recrystallized, finely laminated carbonate linings with calcite cement and pelleted sediment in the open spaces. One specimen (HUJ.PAL 100.21) has the calcitized remnants of an articulated aragonitic bivalve shell visible in cross-section. Remarks — The diverging double aperture of this trace, along with remnants of an aragonitic lining and the bivalve shell in cross section, indicate that G. ampullatus in this study was produced by the boring gastrochaenid bivalve Spengleria rostrata or some similar form (see Carter, 1978; Donovan and Hensley, 2006, and Kelly and Bromley, 1984). These traces are thus borings at their bases and bioclaustrations at the apertures as the corals grew around the bivalve incurrent and excurrent siphons. The multiple linings at the base of one chamber may have been formed as the bivalve moved upwards to keep pace with coral growth, similar to what has been shown for mytilid bivalves in living corals by Kleemann (1994). 5. Discussion and conclusions This occurrence of a bivalve-scleractinian symbiosis is one of the earliest in which the living relationship between the two organisms can be demonstrated. Detecting whether a bivalve bored into living coral tissue is difficult (see Kleemann, 1982), but these Gastrochaenolites ampullatus traces in A. cristatus show that the coral was creating new skeleton above the bivalve crypt and bioclaustrating the siphons. In one case the bivalve was entombed inside the coral as it roofed over the apertures. Boring bivalves today prefer to excavate dead coral skeleton, but there are a few species that specialize in infesting live coral tissues (see Kleemann, 1994, for review). Other clear examples of coral-bivalve symbiosis are known from the Upper Cretaceous, and it is “quite likely” that coral and mytilid bivalve living associations were present in the Jurassic and “probably since the Upper Triassic” (Kleemann, 1994, p. 131). The previously known fossil examples of symbiosis in the Late Cretaceous involve only massive and branching corals (Kleemann, 1994), so the occurrence described here is the first such symbiosis known from small platter-like corals.
Acknowledgments We thank D.K. Pandey of the University of Rajasthan for assistance with the coral identification, and Yoav Avni of the Geological Survey of Israel for field advice and help. Zeev Lewy and Carl Brett provided helpful reviews of the manuscript. We also are grateful for support from the Faculty Development Fund and Wengerd Fund at The College of Wooster. References Aberhan, M., Kiessling, W., Fürsich, F.T., 2006. Testing the role of biological interactions in the evolution of mid-Mesozoic marine benthic ecosystems. Paleobiology 32, 259–277. Arkin, Y., Braun, M., 1965. Type sections of Upper Cretaceous formations in the northern Negev (southern Israel). Isr. Geol. Surv. 1–19 (Report 2a). Avnimelech, M., Shoresh, R., 1962. Les céphalopodes Cénomaniens des environs de Jérusalem. Bull. 528–535 (S.G.F. 7, IV). Carter, J.G., 1978. Ecology and evolution of the Gastrochaenacea (Mollusca, Bivalvia) with notes on the evolution of the endolithic habitat. Pea. Mus. Bull. 41, 1–92. Donovan, S.K., Hensley, C., 2006. Gastrochaenolites Leymerie in the Cenozoic of the Antillean region. Ichnos 13, 11–19. Gill, G.A., Lafuste, J.G., 1987. Structure, répartition et signification paléogéographique d'Aspidiscus, hexacoralliaire cénomanien de la Téthys. Bull. Soc. Geol. Fr. vol. 5, number 115 (sér. 8), 921–934 (t. 3). Hirsch, F., Braun, M., 1994. Mid Cretaceous (Albian–Cenomanian) carbonate platforms in Israel. Cuad. Geol. Iber. 18, 59–82. Jagt, J.W., Neumann, C., Donovan, S.K., 2009. Petroxestes altera, a new bioerosional trace fossil from the upper Maastrichtian (Cretaceous) of northeast Belgium. Bull. Inst. R. Sci. Nat. Belg. Sci. Terre 79, 137–145. Kelly, S.R.A., Bromley, R.G., 1984. Ichonological nomenclature of clavate borings. Palaeontology 27, 793–807. Kleemann, K., 1980. Boring bivalves and their host corals from the Great Barrier Reef. Aust. J. Moll. Stud. 46, 13–54. Kleemann, K., 1982. Atzmuscheln im Ghetto? Lithophaga (Bivalvia) aus dem Leithakalk (Mittel-Miozän: Badenien) von Mülllendorf im Wiener Becken. Österr. Beitr. Paläont. Osterr. 9, 211–231. Kleemann, K., 1983. Catalogue of recent and fossil Lithophaga (Bivalvia). J. Moll. Stud. Suppl. 12, 1–46. Kleemann, K., 1994. Associations of corals and boring bivalves since the Late Cretaceous. Facies 31, 131–140. Lewy, Z., Raab, M., 1976. Mid Cretaceous stratigraphy of the Middle East. Ann. Mus. Hist. Nat. Nice 32, 1–20 IV. Morton, B., 1990. Corals and their bivalve borers: the evolution of a symbiosis. In: Morton, B. (Ed.), The Bivalvia: Proceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge (1899–1986) at the 9th International Malacological Congress, 1986. Hong Kong University Press, Hong Kong, Edinburgh, Scotland, UK, pp. 11–46. Pandey, D.K., Fürsich, F.T., Gameil, M., Ayoub-Hannaa, W.S., 2011. Aspidiscus cristatus (Lamarck) from the Cenomanian sediments of Wadi Quseib, east Sinai. Egypt. J. Palaeontol. Soc. India 56, 29–37. Thomas, H.D., Omara, S., 1957. The Cenomanian compound coral, Aspidiscus cristatus (Lamarck), from Nezzazat, western Sinai. Geol. Mag. 94, 151–155. Vermeij, G.J., 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258.
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo
Bivalve borings, bioclaustrations and symbiosis in corals from the Upper Cretaceous (Cenomanian) of southern Israel Mark A. Wilson a,⁎, Olev Vinn b, Timothy J. Palmer c a b c
Department of Geology, The College of Wooster, Wooster, OH 44691, USA Institute of Ecology and Earth Sciences, University of Tartu, Ravila 14A, 50411 Tartu, Estonia Institute of Geography and Earth Sciences, Aberystwyth University, Aberystwyth, Wales SY23 3DB, United Kingdom
a r t i c l e
i n f o
Article history: Received 27 July 2014 Received in revised form 4 September 2014 Accepted 9 September 2014 Available online 16 September 2014 Keywords: Cenomanian Trace fossils Corals Bivalves Symbiosis Israel
a b s t r a c t Specimens of the small compound coral Aspidiscus cristatus (Lamarck, 1801) containing evidence of symbiosis with bivalves have been found in the En Yorqe'am Formation (Upper Cretaceous, early Cenomanian) of southern Israel. The corals have paired holes on their upper surfaces leading to a common chamber below, forming the trace fossil Gastrochaenolites ampullatus Kelly and Bromley, 1984. Apparently gastrochaenid bivalve larvae settled on living coral surfaces and began to bore into the underlying aragonitic skeletons. The corals added new skeleton around the paired siphonal tubes of the invading bivalves, eventually producing crypts that were borings at their bases and bioclaustrations at their openings. When a boring bivalve died its crypt was closed by the growing coral, entombing the bivalve shell in place. This is early evidence of a symbiotic relationship between scleractinian corals and boring bivalves (parasitism in this case), and the earliest record of bivalve infestation of a member of the Suborder Microsolenina. It is also the earliest occurrence of G. ampullatus. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Scleractinian corals and boring bivalves today have complex symbiotic relationships (Kleemann, 1980, 1983, 1994; Morton, 1990). A critical question has been whether the origin of living relationships between corals and endolithic bivalves is relatively recent or has a long evolutionary history back into the Mesozoic (Morton, 1990). Gastrochaenid and lithophagid bivalves have a long record of boring into dead coral substrates (see Kleemann, 1983, and Morton, 1990), but how long have they excavated their domiciles in living corals? Is this coral-bivalve symbiosis one of the many features of the Mesozoic Marine Revolution (Vermeij, 1977; Aberhan et al., 2006) in response to new predatory pressures? As further evidence for the development of this relationship, we describe here an unequivocal symbiosis between a gastrochaenid bivalve (possibly Spengleria) and a compound coral of the Suborder Microsolenina in the Cenomanian (Upper Cretaceous) of southern Israel. 2. Location and geological setting The coral-bivalve symbiosis specimens were found in the En Yorqe'am Formation (early Cenomanian) approximately 20 m from its base in Nahal Neqarot, southern Israel (coordinates: 30.65788°, E 35.08764°; Fig. 1). ⁎ Corresponding author. E-mail addresses: [email protected] (M.A. Wilson), [email protected] (O. Vinn), [email protected] (T.J. Palmer).
http://dx.doi.org/10.1016/j.palaeo.2014.09.005 0031-0182/© 2014 Elsevier B.V. All rights reserved.
The En Yorqe'am Formation in Nahal Neqarot is a chalky argillaceous limestone and marl with a thick oyster-rich unit at its base and a rich abundance of invertebrate fossils above, including calcareous sponges, corals, brachiopods, gastropods, bivalves, ammonites, echinoids and ostracodes (see Arkin and Braun, 1965; Hirsch and Braun, 1994). It has been dated by the occurrence of early Cenomanian ammonites (Avnimelech and Shoresh, 1962; Lewy and Raab, 1976). The environment of the En Yorqe'am deposits was an open marine carbonate shelf formed during an early Cenomanian sea level rise (Hirsch and Braun, 1994). 3. Materials and methods Ten specimens of the compound scleractinian coral Aspidiscus cristatus (Lamarck, 1801) were collected from a surface exposure of the En Yorqe'am Formation (approximately 20 m from its base) in Nahal Neqarot during fieldwork in April 2014. (See locality information above.) The corals are externally well preserved and required no preparation beyond sectioning to reveal details of the ichnofossils. The skeletons were originally aragonitic and have been calcitized. Most internal details of the corals have thus been lost to recrystallization. 4. Systematic paleontology The specimens used in this study are deposited in the National Natural History Collections at The Hebrew University of Jerusalem, Israel (referred herein as HUJ.PAL).
244
M.A. Wilson et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 414 (2014) 243–245 F Zone
LEBANON
SYRIA Mediterranean Sea West Bank
1994 y Lin
Gaza 0 e
ISRAEL
Nahal Neqarot
JORDAN
Fig. 2. Aspidiscus cristatus oral surface with paired apertures of Gastrochaenolites ampullatus visible in the upper half (HUJ.PAL 100-21).
Remarks — The A cristatus corals are found in a marly subunit of the En Yorqe'am Formation that is richly fossiliferous with other scleractinian corals, calcareous sponges, bivalves, gastropods and terebratulid brachiopods. Some of the A. cristatus specimens originally settled on shelly debris, which produced external molds on their undersurfaces.
EGYPT 50 km
4.2. Trace fossils
Fig. 1. Location of Nahal Neqarot in southern Israel.
4.1. Corals The most recent assessment of Aspidiscus cristatus is by Pandey et al. (2011). We are following their taxonomic and morphologic schemes below. Please see that paper for the most recent synonymy list. Order Scleractinia Bourne, 1900. Suborder Microsolenina Morycowa and Roniewicz, 1995. Family Latomeandridae Alloiteau, 1952. Genus Aspidiscus König, 1825. A. cristatus (Lamarck, 1801). Figs. 2–4. Material — Ten complete specimens of A. cristatus, HUJ.PAL 100.20– 100.29. They range in diameter from 20 to 43 mm and height from 8 to 20 mm. Four of these specimens (HUJ.PAL 100.20–100.23) host Gastrochaenolites ampullatus trace fossils. Description — Almost all workers with Aspidiscus describe it as “attractive in shape” (see Thomas and Omara, 1957; Gill and Lafuste, 1987, p. 921; Pandey et al., 2011, p. 33) because of its biscuit-like appearance and elongated monticules on its oral surface. A. cristatus has a circular, colonial corallum with concave aboral and convex oral surfaces. Its calical arrangement is hydnophoroid (meandroid with discontinuous walls). The peripheral crown of A. cristatus is distinct with a sharp margin. Septa are at right angles to the margin and continue across the aboral surface. The aboral surface also has thin concentric growth lines with some folds. No attachment region is present. The oral surface is characterized by short ridge-like monticules. Internal microstructures, such as pennulae, are not visible because of recrystallization.
Ichnogenus Gastrochaenolites Leymerie, 1842 (See Kelly and Bromley, 1984, p. 797, for complete synonymy.). G. ampullatus Kelly and Bromley, 1984. Figs. 2–4. Material. — Four specimens of Aspidiscus A. cristatus contain a total of eight paired apertures of the trace fossil G. ampullatus (HUJ.PAL 100.20–100.23). Description — The apertures of G. ampullatus range from 0.6 to 2.2 mm in diameter, with the apertures within a pair roughly the same size. From center to center, the apertures within a pair range from 1.4 to 4.9 mm apart. The apertures are surrounded by uncut coral skeleton that has in some cases grown slightly upwards along the margin, giving a low chimney-like effect. Three G. ampullatus specimens were vertically sectioned to show cross-sections of the structure. The aperture necks are very short (less than a millimeter on the outside from the aperture to
Fig. 3. Paired apertures of Gastrochaenolites ampullatus in the coral Aspidiscus cristatus (HUJ.PAL 100.21).
M.A. Wilson et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 414 (2014) 243–245
245
Embedding within a live coral host is not easy for bivalve larvae as they must avoid being consumed by the coral's polyps and have a way of penetrating its epithelium down to the aragonitic skeleton. This may be why so few modern bivalves infest living corals (Kleemann, 1982, 1994; Morton, 1990). For those bivalves that establish this relationship, Kleemann (1994) suggests several advantages, including a substrate that increases with growth rather than decreases with continuous bioerosion, and minimal space competition. Kleemann (1994, p. 138) also postulates that there is an advantage to the host coral in this relationship because when the “bivalve has died because of senility, the decaying tissues can provide a nutritial source for the coral”. We suggest that this would be a minimal benefit to the coral at most, outweighed by competition for suspended nutrients with the bivalve, loss of polyp space, and a weakened skeleton due to the boring. We thus consider this example of bivalve-coral symbiosis to have been parasitic. Jagt et al. (2009, p. 140) list G. ampullatus as occurring “in the Maastrichtian type area”, which is the earliest record of the ichnospecies. This Cenomanian occurrence from southern Israel is thus a range extension downwards for G. ampullatus. Fig. 4. Polished cross-section through a specimen of Gastrochaenolites ampullatus in an Aspidiscus cristatus coral (HUJ.PAL 100.21). In the lower left of the chamber are layered carbonates (A) representing boring linings produced by the bivalve. An articulated bivalve shell (B) is preserved in the chamber. The chamber has been roofed over by coral growth (C).
the coral surface) and lead down to a common chamber with an irregular rounded base approximately as wide as the aperture pair above (4.8 to 8.0 mm in the three sectioned specimens). The length of the entire trace from base to apertures ranges from 6.0 to 10.9 mm. The interiors of the chambers contain recrystallized, finely laminated carbonate linings with calcite cement and pelleted sediment in the open spaces. One specimen (HUJ.PAL 100.21) has the calcitized remnants of an articulated aragonitic bivalve shell visible in cross-section. Remarks — The diverging double aperture of this trace, along with remnants of an aragonitic lining and the bivalve shell in cross section, indicate that G. ampullatus in this study was produced by the boring gastrochaenid bivalve Spengleria rostrata or some similar form (see Carter, 1978; Donovan and Hensley, 2006, and Kelly and Bromley, 1984). These traces are thus borings at their bases and bioclaustrations at the apertures as the corals grew around the bivalve incurrent and excurrent siphons. The multiple linings at the base of one chamber may have been formed as the bivalve moved upwards to keep pace with coral growth, similar to what has been shown for mytilid bivalves in living corals by Kleemann (1994). 5. Discussion and conclusions This occurrence of a bivalve-scleractinian symbiosis is one of the earliest in which the living relationship between the two organisms can be demonstrated. Detecting whether a bivalve bored into living coral tissue is difficult (see Kleemann, 1982), but these Gastrochaenolites ampullatus traces in A. cristatus show that the coral was creating new skeleton above the bivalve crypt and bioclaustrating the siphons. In one case the bivalve was entombed inside the coral as it roofed over the apertures. Boring bivalves today prefer to excavate dead coral skeleton, but there are a few species that specialize in infesting live coral tissues (see Kleemann, 1994, for review). Other clear examples of coral-bivalve symbiosis are known from the Upper Cretaceous, and it is “quite likely” that coral and mytilid bivalve living associations were present in the Jurassic and “probably since the Upper Triassic” (Kleemann, 1994, p. 131). The previously known fossil examples of symbiosis in the Late Cretaceous involve only massive and branching corals (Kleemann, 1994), so the occurrence described here is the first such symbiosis known from small platter-like corals.
Acknowledgments We thank D.K. Pandey of the University of Rajasthan for assistance with the coral identification, and Yoav Avni of the Geological Survey of Israel for field advice and help. Zeev Lewy and Carl Brett provided helpful reviews of the manuscript. We also are grateful for support from the Faculty Development Fund and Wengerd Fund at The College of Wooster. References Aberhan, M., Kiessling, W., Fürsich, F.T., 2006. Testing the role of biological interactions in the evolution of mid-Mesozoic marine benthic ecosystems. Paleobiology 32, 259–277. Arkin, Y., Braun, M., 1965. Type sections of Upper Cretaceous formations in the northern Negev (southern Israel). Isr. Geol. Surv. 1–19 (Report 2a). Avnimelech, M., Shoresh, R., 1962. Les céphalopodes Cénomaniens des environs de Jérusalem. Bull. 528–535 (S.G.F. 7, IV). Carter, J.G., 1978. Ecology and evolution of the Gastrochaenacea (Mollusca, Bivalvia) with notes on the evolution of the endolithic habitat. Pea. Mus. Bull. 41, 1–92. Donovan, S.K., Hensley, C., 2006. Gastrochaenolites Leymerie in the Cenozoic of the Antillean region. Ichnos 13, 11–19. Gill, G.A., Lafuste, J.G., 1987. Structure, répartition et signification paléogéographique d'Aspidiscus, hexacoralliaire cénomanien de la Téthys. Bull. Soc. Geol. Fr. vol. 5, number 115 (sér. 8), 921–934 (t. 3). Hirsch, F., Braun, M., 1994. Mid Cretaceous (Albian–Cenomanian) carbonate platforms in Israel. Cuad. Geol. Iber. 18, 59–82. Jagt, J.W., Neumann, C., Donovan, S.K., 2009. Petroxestes altera, a new bioerosional trace fossil from the upper Maastrichtian (Cretaceous) of northeast Belgium. Bull. Inst. R. Sci. Nat. Belg. Sci. Terre 79, 137–145. Kelly, S.R.A., Bromley, R.G., 1984. Ichonological nomenclature of clavate borings. Palaeontology 27, 793–807. Kleemann, K., 1980. Boring bivalves and their host corals from the Great Barrier Reef. Aust. J. Moll. Stud. 46, 13–54. Kleemann, K., 1982. Atzmuscheln im Ghetto? Lithophaga (Bivalvia) aus dem Leithakalk (Mittel-Miozän: Badenien) von Mülllendorf im Wiener Becken. Österr. Beitr. Paläont. Osterr. 9, 211–231. Kleemann, K., 1983. Catalogue of recent and fossil Lithophaga (Bivalvia). J. Moll. Stud. Suppl. 12, 1–46. Kleemann, K., 1994. Associations of corals and boring bivalves since the Late Cretaceous. Facies 31, 131–140. Lewy, Z., Raab, M., 1976. Mid Cretaceous stratigraphy of the Middle East. Ann. Mus. Hist. Nat. Nice 32, 1–20 IV. Morton, B., 1990. Corals and their bivalve borers: the evolution of a symbiosis. In: Morton, B. (Ed.), The Bivalvia: Proceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge (1899–1986) at the 9th International Malacological Congress, 1986. Hong Kong University Press, Hong Kong, Edinburgh, Scotland, UK, pp. 11–46. Pandey, D.K., Fürsich, F.T., Gameil, M., Ayoub-Hannaa, W.S., 2011. Aspidiscus cristatus (Lamarck) from the Cenomanian sediments of Wadi Quseib, east Sinai. Egypt. J. Palaeontol. Soc. India 56, 29–37. Thomas, H.D., Omara, S., 1957. The Cenomanian compound coral, Aspidiscus cristatus (Lamarck), from Nezzazat, western Sinai. Geol. Mag. 94, 151–155. Vermeij, G.J., 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258.