Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21

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Palaeogeography, Palaeoclimatology, Palaeoecology

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End-Guadalupian of the Permian gigantic bivalve Alatoconchidae: End of gigantism in tropical seas by cooling

Yukio Isozaki a,⁎, Dunja Aljinović b a Department of Earth Science and Astronomy, The University of Tokyo, Meguro, Tokyo 153-8902, Japan b Faculty of Mining Geology and Petroleum Engineering, The University of Zagreb, Zagreb 10000, Croatia article info abstract

Article history: The unique Permian bivalve family Alatoconchidae has aberrant shell forms and extraordinary size up to 1 m, Received 14 May 2007 representing the largest bivalve group in the Paleozoic. Their occurrence is reported sporadically from Received in revised form 4 November 2008 Lower–Middle Permian shallow-marine carbonates in 9 areas in the world (Tunisia, Croatia, Oman, Iran, Accepted 15 August 2009 Afghanistan, Thailand, Malaysia, the Philippines, and Japan) that cover low-latitudes of both the Tethyan and Available online 9 September 2009 Panthalassan domains. Alatoconchids almost always occurred in close association with large-tested fusulines (Verbeekinidae) and/or rugose corals (Waagenophyllidae) of the typical Tethyan assemblage, suggesting Keywords: “ ” Gigantism their preferential adaptation to shallow warm-water (tropical) environments. This tropical trio Capitanian (Alatoconchidae, Verbeekinidae, and Waagenophyllidae) became extinct either during the Late Guadalupian Permian or around the Guadalupian–Lopingian boundary (G–LB). Their intimate association and occurrence range Mass extinction suggest that these 3 taxonomically distinct clades may have shared not only a common habit but also a photosymbiosis common cause of extinction. The shell structure of alatoconchids suggests their symbiosis with Eutrophication photosynthetic organisms (algae+cyanobacteria) in order to maintain their large body size that required high energy-consuming metabolism in contrast to smaller forms. The Alatoconchidae attained their largest size in the Wordian (Middle Guadalupian), probably maximizing the benefits of photosymbiosis. The subsequent extinction of the warm-water-adapted “tropical trio” both in Tethys and Panthalassa positively supports the explanation that a critical cooling took place on a global scale, including low-latitude oceans. The end of the gigantism in fusulines and bivalves in the Capitanian (Late Guadalupian) was likely caused by the collapse of photosymbiotic systems during a temporary temperature drop of seawater (Kamura cooling event) coupled with eutrophication that was detrimental to the tropical fauna adapted particularly to oligotrophic conditions. Gigantism of bivalves occurred several times in the Phanerozoic; e.g., Siluro- Devonian, Permian, Triassic–Early , and Jurassic–Creataceous, mostly in warm periods. The sea-level change in the Phanerozoic apparently synchronized with the intermittent rise and decline of bivalve gigantism, suggesting that the photosymbiosis-related gigantism in low-latitudes may serve as a potential monitor of global warming/cooling in the past. © 2009 Elsevier B.V. All rights reserved.

1. Introduction structure. Although the actual mechanisms of driving body size and their meanings in evolution have not been sufficiently explained, Size variations of fossil animals and their changes over geological biotic interactions among various organisms and nutrient availability time have long attracted intense curiosity of paleontologists ever likely contributed to the determination of the size of fossil animals since the 19th century. For example, an apparent trend recognized in (e.g., Vermeij, 1977; Brasier, 1995). fossil records led to the empirical concept known as Cope's rule, i.e., As to the balance between body size and population size, orthogenesis towards large size. Stanley (1973) re-interpreted this MacArthur and Wilson (1967) tried to formulate the ecological classic perspective in a modern way by emphasizing the common structure of modern animal communities in terms of the dichotomy of pattern recognized in many higher taxa (order and class) with small- K-selection and r-selection. This classic approach was further size ancestors and large-size descendants, such as bivalves, ammo- emphasized by Pianka (1978), which, however, was not favored by noids, and fusulines. Later, Jablonski (1996) challenged this view by contemporary ecologists because the suggested trade-off relations pointing out sampling bias with respect to the skewed population between the two selections cannot be recognized in many modern cases. Nonetheless, fossil records suggest that some ancient taxa did deploy the r-strategy under extremely stressful conditions in the ⁎ Corresponding author. Dept. of Earth Science and Astronomy, Univ. Tokyo, Japan. Tel.: +81 3 5454 6608; fax: +81 3 5465 8244. geologic past, particularly in the aftermaths of major mass extinction E-mail address: [email protected] (Y. Isozaki). events (e.g., Urbaneck, 1993; Schubert and Bottjer, 1995; Twitchett,

0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.08.022 12 Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21

1999; Fraiser and Bottjer, 2004). The term “Lilliput effect” was coined likewise explained in terms of photosymbiosis (e.g., Vogel, 1975; by Urbaneck (1993) for describing such remarkable minimalism in Yancey and Boyd, 1983; Kauffman and Johnson, 1988; Seilacher, the fossil record. 1990; de Freitas et al., 1993) on the basis of indirect lines of evidence, On the other hand, as large fossils are eye-catchers not only for i.e., analogy with modern examples in large size, aberrant form, and amateur fossil collectors but also for professional paleontologists, unique shell structures. gigantism in fossil records has been recognized and discussed with Among the above-listed fossil giant clams, the Permian bivalve respect to modern examples. Among modern bivalves, Tridacna gigas family Alatoconchidae (Fig. 1) appears the most noteworthy not in the Indo-Pacific region is known as the biggest (a single valve may merely because it represents the largest fossil bivalve ever since the reach weights of more than 110 kg; Yonge, 1936) that is clearly out of Cambrian radiation of metazoans but also because it became extinct the 2-sigma range in the normal distribution of modern and ancient abruptly near the end of the Guadalupian (Middle Permian) that bivalve sizes (e.g., Nicol, 1964). In fossil records, gigantism in bivalves marks the timing of one of the major mass extinction events in the appeared repeatedly at least 4 times; i.e. Siluro-Devonian mega- Phanerozoic (Stanley and Yang, 1994; Jin et al., 1994; Isozaki and Ota, lodonts, Permian alatoconchids, Late Triassic–Early Jurassic mega- 2001; Isozaki, 2007a,b, 2009). lodonts/lithiotids, and Late Jurassic–Cretaceous rudists/inoceramids, This article reviews the occurrences of the Permian bivalve family although most of them were not necessarily related in direct lineages. Alatoconchidae to date, and discusses the geological implications of In general, the advantage of attaining a large body size includes their gigantism and extinction pattern. By emphasizing the intimate efficiency/advantage in 1) collecting food of various sizes, 2) association of tropical-adapted Alatoconchidae, Verbeekinidae (large- , 3) protection from other animal's predation, 4) reproduc- tested fusulines) and Waagenophyllidae (rugose corals), possible tion, and 5) maintaining internal-body homeostasis (e.g., Pianka, climate-tuning of the intermittent rise/decline of bivalve gigantism in 1978). However, these advantages detract from small population the Phanerozoic is also discussed in the light of photosymbiosis in sizes, long maturation time, specialized habit, and/or large amount of tropical shallow-marine environments. required nutrients/energy, which may act as disadvantages when environmental conditions change into different modes. Thus, in order 2. Permian giant clam Alatoconchidae to achieve unusual gigantism out of the normal size range of a clade, animals need to overcome these disadvantages by trading off Alatoconchidae is a unique Permian bivalve family characterized some benefits in being small and by deploying unusual strategies. by an aberrant shell form (Fig. 1) and an extraordinarily large size up Yonge (1936) first pointed out the occurrence of symbiotic algae to 1 m in length. The occurrence of this bivalve family was first zooxanthellae (= dinoflagellate genus Symbiodium)inTridacna, and described from a Middle Permian limestone in Japan with a new other modern examples (e.g., Corculum, Fragum, and Hippopus) were genus/species name Shikamaia akasakaensis Ozaki; however, the added later in the list (e.g., Kawaguti, 1983). As for ancient bivalves, original specimen was treated as a paleontological problematica the gigantism in rudists and other aberrant gigantic fossil clams was simply because its bizarre shape appeared too distinct from those of

Fig. 1. Morphology of Alatoconchidae. A–C: Reconstructed general shell morphology of Alatoconchidae, D–E: the holotype of Shikamaia (=Tanchintongia) ogulineci (Kochansky-Devidé) stored in the Croatian Natural History Museum in Zagreb. Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21 13 ordinary bivalves (Ozaki, 1968). Despite such taxonomic confusion Alatoconchidae, the size of which can be compared with that of the in the beginning, additional occurrences of Alatoconchidae were largest modern bivalve Tridacna gigas. sporadically reported later from Lower and Middle Permian rocks in Alatoconchidae is equivalved; two valves are arranged symmet- Malaysia, Afghanistan, Iran, Croatia, and Tunisia (Termier et al., 1973; rically with respect to the orthothetic plane of commissure (Fig. 1). Runnegar and Gobbett, 1975; Kochansky-Devidé, 1978; Boyd and The bivalve is elongated in the anterior–posterior direction, but Newell, 1979; Thiele and Ticky, 1980). The family name Alatoconchidae compressed in the dorsal–ventral direction. The most striking feature was given by Termier et al. (1973) who first identified them as bivalves is the lateral flange formed by the horizontal extension of umbonal and demonstrated their overall shell morphology with ligament carinae. The ventral surface forms a large planer surface, whereas the structure, although their reconstruction was oriented up-side-down. dorsal side forms a crest extending perpendicular to the flat ventral Runnegar and Gobbett (1975) correctly illustrated a general morphol- surface. There is a remarkable contrast in shape between the anterior ogy for alatoconchids, and Kochansky-Devidé (1978) discussed their and posterior halves. The height of dorsal crest reaches the apex in the unique morphological adaptation with respect to ecological habitat. On anterior half and decreases sharply in the mid-shell, whereas the the basis of all these previous data and interpretations plus new width of shell decreases gradually towards the posterior. Thus the material added later, Yancey and Boyd (1983) and Yancey and Ozaki posterior half of the bivalve has pronounced flat lateral flanges. An (1986) summarized the paleobiology and taxonomy of the entire overall profile of the bivalve across the main axis forms a triangle in family, as briefly described below. the anterior and an extremely flat oval in the posterior half. The family Alatoconchidae comprises two subfamilies; i.e., Such a large size and aberrant form of shell suggest that Alatoconchinae and Saikraconchinae. The former includes the genus alatoconchids were epifaunal suspension-feeders, and that they Shikamaia Ozaki and the subgenus Alatoconcha (Yancey & Boyd), were not very capable either of moving around or of frequent whereas the latter contains the genus Saicraconcha Yancey & Boyd opening/closing of their shells (Termier et al., 1973; Runnegar and and the subgenus Dereconcha Yancey & Boyd. Genus Tanchintongia Gobbett, 1975; Kochansky-Devide, 1978). It is noteworthy that Runnegar & Gobbett was regarded as a synonym of Shikamaia Ozaki. alatoconchids preferentially occur in a bituminous black lime Due to their three-dimensionally twisted and fragile shell form mudstone facies (Yancey and Boyd, 1983; Sano, 1988; Kiessling and (Fig. 1), most of the described specimens occur as broken fragments Flügel, 2000; Isozaki, 2006; Aljinović et al., 2008; Fig. 2 left and (Fig. 2). In addition, as shells are often embedded tightly within middle). Alatoconchids may have adapted to the soft fine-grained limestone matrices, it is generally difficult to isolate free individual sediment surface of wackestone- to lime mudstone-dominant facies valves. Nonetheless, by virtue of some exceptionally well-preserved by developing a flat-bottom in order to maintain their position on soft specimens (Fig. 1C and D) and intensive studies by the above- substrates against their heavy shell weight, i.e., like snowshoe or mentioned workers, their general three-dimensional shell form was outrigger (e.g., Seilacher, 1990). In-situ shell concentrations indicate a reasonably reconstructed (Fig. 1A–C). The length of individual gregarious habitat in low to middle-energy environments of a shallow alatoconchid shell mostly ranges from 5 to 60 cm with an average sea (Yancey and Boyd, 1983; Fig. 2 left and middle). Some cases with around 30 cm (Fig. 1A). Yancey and Ozaki (1986) mentioned that the random alignment of shell fragments suggest a reworked origin in maximum size of adults likely had reached nearly 1 m in length. One storm beds (Fig. 2 right). of the present authors (Y.I.) observed a nearly 0.8 m-long specimen As to the shell structure, Alatoconchidae is characterized by the with a shell thickness over 5 cm in Japan. There is no known bivalve development of a unique external layer in a double-layered shell family in the Permian or in the Paleozoic that reached this size except (Yancey and Boyd, 1983; Isozaki, 2006; Fig. 3). The external layer is

Fig. 2. Field occurrence of Alatoconchidae. Left: Alatoconchidae gen. et sp. indet. from the Neoschwagerina Zone in Kamura (Japan), upper middle: Shikamaia akasakaensis Ozaki from the Pseudofusulina ambigua Zone in Neo (Japan), lower middle: juvenile form of Alatoconchidae from the Yabeina Zone in Brušane, the Velebit Mountains (Croatia), right: Shikamaia bed of the Yabeina Zone at Akasaka (Japan). Scale for the left photo is 20 cm long. Note that alatoconchids occur preferentially in wackestone and lime mudstone, suggesting a less agitated shallow-marine environment for their habitat. The example in Akasaka (right) occurs in a debris flow bed in which alatoconchid shells are scattered in randomly. 14 Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21

Fig. 3. Shell structure of Alatoconchidae. Left: large specimen of alatoconchid from the Yabeina Zone in Brusane, Croatia (upper) and prismatic calcite layer of the external shell on a broken surface (lower). Right: large specimen of alatoconchid from the Neoschwagerina Zone in Kamura, Japan (upper) and prismatic calcite layer of the external shell in thin section (lower). composed of prismatic calcite aligned perpendicularly to the shell Afghanistan (Termier et al., 1973), Oman (Pillevat, 1993; Wiedlich surface, whereas the internal one consists of mosaic granular calcite. and Bernecker, 2007), Thailand (Udchachon et al., 2007), Malaysia The development of long prismatic calcite, sometimes reaching over (Runnegar and Gobbett, 1975), the Philippines (Kiessling and Flügel, 1 cm in length (fig. 2e in Isozaki, 2006), is significant with respect to 2000), and Japan (Ozaki, 1968; Yancey and Ozaki, 1986; Saito et al., the bivalve's ecological habit of photosymbiosis, as these crystals can 2005; Isozaki, 2006; Matsuda et al., 2006). The first 7 cases were serve as optic fibers that let sunlight penetrate into the interior of reported all from shallow-marine carbonates deposited around bivalves even when closed. A similar structure is known in modern Tethys along the eastern coast of Pangea, and they are characterized photosymbiotic bivalve groups, such as Corculum (e.g., Kawaguti, by their co-occurrence with typical Tethyan faunal assemblages that 1983; Seilacher, 1990). The extraordinarily large size, generally flat include large-tested fusulines of Verbeekinidae and rugose corals of shell form, and the transparent shell structure suggest that the Waagenophyllidae (Yancey and Boyd, 1983). Most of the bivalve Permian aberrant alatoconchids performed symbiosis with photosyn- localities were apparently in low-latitude domains near the paleo- thetic microorganisms (algae or cyanobacteria; just like modern equator. Oman and Malaysia localities were rather southerly zooxanthellae) in the photic zone in shallow-marine environments positioned around 30° S with respect to the rest, nonetheless, still less than 50 m deep (Yancey and Boyd, 1983; Seilacher, 1990). within a narrow Neo-Tethys probably washed by warm waters. In contrast, the last two cases in the Philippines and Japan were 3. Paleogeographic distribution reported from Permian shallow-marine limestones contained in Jurassic accretionary complexes (Isozaki et al., 1987; Isozaki, 1997b; The occurrence of the Permian alatoconchids has been reported to Zamoras and Matsuoka, 2004). In Japan, all alatoconchid-bearing date from 9 areas in the world as shown in Table 1 and Fig. 4; i.e., from limestones represent Permian mid-oceanic, atoll-type carbonate west to east, Tunisia (Boyd and Newell, 1979), Croatia (Kochansky- buildups developed on seamounts that were primarily located in Devidé, 1978; Aljinović et al., 2008), Iran (Thiele and Ticky, 1980), the middle of the superocean Panthalassa. Their tectono-sedimentary

Table 1 List of the occurrences of the Permian bivalve family Alatoconchidae. Pa: Pseudofusulina ambigua Zone, Pk: Parafusulina kaerimizuensis Zone, N: Neoschwagerina Zone (Nc: N. craticulifera Zone, Nm: N. margaritae Zone), Zone, Y: Yabeina Zone, L: Lepidolina Zone, Art: Artinskian, Word: Wordian, Cap: Capitanian.

Locality Unit Biozone Age References (Fm)

List of occurrences of Alatoconchidae 1. Japan a. Akasaka Upper Pk–Y Road–Cap Ozaki (1968), Ota and Isozaki (2006) b. Neo Funabuseyama Pa Art Yancey and Ozaki (1986); Sano (1988) c. Kamura Iwato Nc–L Word–Cap Isozaki (2006) d. Shiroiwayama – N Word Matsuda et al. (2006) e. Tomochi Hashirimizu N Word–Cap? Saito et al. (2005) 2. Philippines (Palawan) Minilog Nc Word Kiessling and Flügel (2000) 3. Malaysia (Kinta Valley) – Pa Art Runnegar and Gobbett (1975) 4. Thailand (Khao Khwang) Saraburi N–L Word–Cap Udchachon et al. (2007) 5. Afghanistan (Al-e Say Pass) – Nm Word Termier et al. (1973) 6. Iran a. Kuh e Ahmad – ?? Thiele and Ticky (1980) b. Mahallt – ?? Thiele and Ticky (1980) c. Shahpoor – ?? Thiele and Ticky (1980) 7. Oman (Saih Harat) Saiq N Word Pillevat (1993), Wiedlich and Bernecker (2007) 8. Croatia (Velebit Mtn.) Velebit Nc–Y Word–Cap Kochansky-Devidé (1978), Aljinović et al. (2008) 9. Tunisia (Saikra) Saikra N Word Boyd and Newell (1979) Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21 15

Fig. 4. Paleogeographic distribution of Alatoconchidae (compiled from the references listed in the text and Table 1; map based on Scotese and Langford (1995) and modified from Isozaki (2006)). Note that the occurrences are concentrated in the low-latitude domains of both Tethys and Panthalassa. history, from the mid-Panthalassa deposition in the Permian to the alatoconchids in these two American continental blocks needs to be final accretion to the Asian continental margins in the Jurassic, was explained somehow, e.g., in terms of paleo-provincialism under a clearly documented by detailed field mapping and radiolarian dating unique setting with one supercontinent and one superocean. (e.g., Wakita, 1988; Sano, 1988). In addition to Akasaka where the first alatoconchid specimen was described (Ozaki, 1968), their occurrence 4. Stratigraphic range has been reported from 4 different areas in SW Japan; i.e. Neo (Yancey and Ozaki, 1986; Sano, 1988), Kamura (Isozaki, 2006), Shiroiwayama The biostratigraphic range of alatoconchids is apparently restricted (Matsuda et al., 2006), and Tomochi (Saito et al., 2005). These mid- to the Cisuraian and Guadalupian, and no large bivalves have been Panthalassan carbonate buildups are characterized by the dominant reported from the Lopingian, although the fossil localities are not occurrence of Tethyan fauna (e.g., Ozawa and Nishiwaki, 1992; Zaw many in total (Table 1). Fig. 5 depicts the biostratigraphic range of Win, 1999) as well as the above-mentioned 7 examples of bona fide Alatoconchidae reported from the 9 areas mentioned above. The Tethyan origin. This suggests that at least the western domain of low- oldest known alatoconchid is the Artinskian (Pseudofusulina ambigua latitude Panthalassa had a strong link with Paleo-Tethys, and that Zone) Shikamaia (= Tanchintongia) perakensis (Runnegar & Gobbett) alatoconchids were no doubt adapted to such a tropical shallow- described from Malaysia (Runnegar and Gobbett, 1975) and Shikamaia marine environment, as well as Verbeekinidae and Waagenophylli- akasakaensis Ozaki from Neo (Japan). The latter was originally dae. The paleo-latitude of the Permian atoll limestone at Kamura in reported from the Neoschwagerina craticulifera Zone (Yancey and Japan was recently revealed to be 12° S (Kirschvink and Isozaki, 2007). Ozaki, 1986) but Sano (1988) later corrected the biostratigraphic In North Palawan, west Philippines, Kiessling and Flügel (2000) horizon of the same section into the P. ambigua Zone. The occurrences reported the occurrence of alatoconchids from the Guadalupian part of limited to Malaysia and Japan may indicate that Alatoconchidae the Minilog Formation composed of shallow-marine carbonates. Judging originated in western Panthalassa and secondarily migrated towards from their geological description plus geotectonic setting and continuity the west through Tethys. to the neighboring Calamian islands to the north (Isozaki et al., 1987; On the other hand, the youngest is Alatoconchidae gen. et sp. indet. Zamoras and Matsuoka, 2004), the alatoconchid-bearing Permian from the Capitanian (Yabeina–Lepidolina Zone) Iwato Formation in limestone of the Minilog Formation probably occurs as exotic blocks Japan, Saraburi Group in Thailand, and Velebit Formation in Croatia within a Mesozoic (probably Jurassic) accretionary complex. If this (Isozaki, 2006; Udchachon et al., 2007; Aljinović et al., 2008). example is reasonable, the Permian Minilog limestone may have been Alatoconchids occur most frequently from the Wordian (or Murgabian; deposited not along the eastern margin of South China (Yangtze block) as Middle Guadalupian) Neoschwagerina Zone (Termier et al., 1973; originally reported but somewhere in the midst of Panthalassa, as in Kochansky-Devidé, 1978; Boyd and Newell, 1979; Yancey and Ozaki, Japan. As to the Minilog Formation, the complete absence of coralline 1986; Kiessling and Flügel, 2000; Isozaki, 2006). It is noteworthy that sponges, a major dissimilarity to coeval Tethyan reef fauna pointed out their size and shell thickness also reached a maximum in the Neosch- by Kiessling and Flügel (2000), can be better explained in the above- wagerina Zone. The highest horizon of Alatoconchidae to date is in the mentioned paleogeographic framework and context. Although the Capitanian Lepidolina Zone (fusuline) in Japan (Isozaki, 2006), and in the precise paleo-latitude of that in the Philippines is unknown, the Capitanian Yabeina Zone in Croatia (Aljinović et al., 2008). Alatoconch- associated Tethyan fusulines and corals likewise suggest a warm-water idae from the Lepidolina Zone are much smaller than those from the domain, as in the same low-latitude tropical sea in western Panthalassa. Neoschwagerina Zone. Thus the distribution of Alatoconchidae was restricted largely to Because no occurrence has ever been reported from the Lopingian, the shallow-marine environments in warm, low-latitude domains alatoconchids likely became extinct at the end of the Guadalupian both of Tethys and Panthalassa. There is no report of alatoconchids both in Tethys and western Panthalassa. In other words, the Permian from South China and North and South America despite their low- gigantic bivalve family was likely involved in the end-Guadalupian latitude positions during the Permian (Fig. 4). The absence of mass extinction. 16 Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21

Fig. 5. Stratigraphic range of Alatoconchidae (compiled from the references shown in the text). Note the frequent occurrence from the Wordian Neoschwagerina Zone. The shell size reached its maximum in this zone both in Tethys and Panthalassa.

5. G–LB extinction effect sensu lato, suggesting the development of a harsh condition also in the mid-superocean Panthalassa (Isozaki, 2007a, 2009). The mass at the Guadalupian–Lopingian bound- In addition, the G–LB extinction was confirmed in shallow-marine ary (G–LB; ca. 260 Ma) had long been overlooked by a great shadow of communities of mid-Panthalassan reefal carbonates primarily deposited the Permo–Triassic boundary (P–TB; ca. 252 Ma) event; however, Jin on ancient seamounts (Ota and Isozaki, 2006). Across the G–LB, the et al. (1994) and Stanley and Yang (1994) re-evaluated paleontolog- large-tested fusulines (sessile benthos) and a great variety of rugose ical and stratigraphic records mostly from South China and confirmed corals that flourished throughout the Early–Middle Permian (e.g., Ozawa that the magnitude of the G–LB event was almost identical to that of and Nishiwaki, 1992; Zaw Win, 1999) were completely terminated at the P–TB event. Major victims of the G–LB event include fusulines, the G–LB. In particular, large-tested fusulines (Verbeekinidae and rugose corals, ammonoids, radiolarians, etc. The great diversity Schwagerinidae according to Ross (1995)) became totally extinct at decline in the end-Paleozoic biosphere was thus explained as a the end of Guadalupian, and the Wuchiapingian (Lower Lopingian) combined consequence of two independent within a interval was occupied solely by small-sized and simple-structured taxa short-time interval of less than 10 million years. The significance of (Schubertellidae, Ozawainelllidae, and Staffellidae) (Ota and Isozaki, the G–LB event was later emphasized by many (e.g., Hallam and 2006). In other words, the G–LB extinction highlights a remarkable Wignall, 1999; Isozaki and Ota, 2001; Wilde, 2002; Yang et al., 2004; contrast between the Guadalupian pre-extinction gigantism and the Erwin, 2006; Isozaki, 2007a, 2009; Retallack et al., 2008). Early Lopingian post-extinction Lilliput effect. The same pattern in The discovery of an unusually long-term anoxic event in mid- fusuline turnover was also identified in the Tethyan shelf carbonates oceanic deep-sea chert (superanoxia) added further significance to (e.g., Leven, 1993)aswellasinSouthChina(Yang et al., 2004). These the G–LB event particularly from a different viewpoint (Isozaki, prove that the low-latitude, shallow-marine communities, character- 1997a), as the onset of this unusual global phenomenon apparently ized by long lasting stable ecological structures/food-web system, was coincides with the G–LB. Radiolarians were the major silica-secreting reformed drastically at the G–LB on a global scale. unicellular plankton of the Paleozoic and the major component of mid-oceanic deep-sea chert. The Albaillellaria group of radiolarians, in 6. Discussion particular, recorded a remarkable morphology change across the G–LB appreciably before the total extinction of the Paleozoic radiolarians at 6.1. Extinction of the Permian giant clams the P–TB. For example, Pseudoalbaillella was predominant from the Pennsylvanian to Guadalupian for ca. 100 million years (e.g., Ishiga, The Permian giant bivalve family Alatoconchidae flourished during 1990), and both the diversity and size of the genus decreased abruptly the Early–Middle Permian and became extinct in the Capitanian at the end of the Guadalupian. This represents not merely a major appreciably before the G–LB, as shown in Table 1 and Fig. 5. It was plankton turnover on a global scale but also an example of the Lilliput recently confirmed that the alatoconchids disappeared together with Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21 17

Verbeeknidae fusuline; i.e., at the top of the Lepidolina Zone in in length) simultaneously both in Tethys and Panthalassa. In the mid- Kamura, and at the top of the Yabeina Zone in Akasaka, Japan (Isozaki, Capitanian (the Lepidolina Zone), however, their shell size decreased 2006; Ota and Isozaki, 2006). Particularly at Kamura, the extinction remarkably down to less than 30 cm in length, and they became extinct both of Alatoconchidae and Verbeekinidae occurred at ca. 11 m below in the late Capitanian together with the other two members of the the G–LB, leaving a barren interval in the uppermost Capitanian (Ota “tropical trio”. This suggests that the stable conditions in shallow-marine and Isozaki, 2006). Also in the Velebit Mountains in Croatia, environments were perturbed in the Capitanian; in particular the alatoconchids occur throughout the N100 m-thick Yabeina Zone and optimized photosymbiotic systems for the “tropical trio” were halted by disappear together with Yabeina below a dolomite that probably certain changes in conditions, such as temperature and nutrient supply. belongs to the Lopingian (Aljinović et al., 2008). The additional For shallow-marine biota in low-latitudes in general, there is a occurrence from the Lepidolina Zone in Thailand (Udchachon et al., threshold temperature for survival, particularly on the lower side. 2007) likewise supports the above-mentioned extinction horizon, When global climate turns into cooling, there is no escape for tropical- though it is not yet well-constrained biostratigraphically. Other adapted organisms, and they may suffer from severe diversity loss or alatoconchid localities (Table 1) have no direct constraint on the even extinction, owing to inefficient metabolism under low tempera- upper range limit; however, it is apparent that Alatoconchidae tures and possibly to a malfunction in photosymbiotic systems. In survived up to the Capitanian but could not extend their lineage general, a drop in sea surface temperature may have lowered into the Lopingian both in Panthalassa and Tethys. metabolic rates in various marine invertebrates (Hochachka and It is noteworthy that the extinction of alatoconchids took place Somero, 1984), and probably halted photosymbiotic communities simultaneously with that of Verbeekinidae in mid-Panthalassa efficiently by killing symbiont algae. Modern reef-forming corals with (Isozaki, 2006) and also in western Tethys (Aljinović et al., 2008), symbiotic algae have a strict temperature limit, i.e., winter-minimum located almost on the opposite side of the globe (Fig. 4). The of 18–19 °C (Johnston, 1980). Wilde (2002), Yang et al. (2004), and extinction of Verbeekinidae was also accompanied by the sharp Ota and Isozaki (2006) suggested that the end-Guadalupian decline of diversity decline in the rugose coral family Waagenophyllidae and of large-tested fusulines (Verbeekinidae and Schwagerinidae) was large gastropods (e.g., Bellerophon, Pleurotomaria, etc. over 10 cm in probably related to certain problems in maintaining the photosym- diameter) at Akasaka (Hayasaka and Hayasaka, 1953; Minato and biotic system. Wang and Sugiyama (2002) demonstrated the sharp Kato, 1965). Alatoconchidae, Verbeekinidae, and Waagenophyllidae, diversity loss of Permian corals at the G–LB, and these possible i.e. “tropical trio” by Isozaki (2006), occurred in intimate association photosymbiotic organisms may have suffered in the same manner. (Yancey and Boyd, 1983), representing the typical Tethyan (low- The Permian, in particular, the mid-Permian has been generally latitude and tropical) shallow-marine fauna. The synchronous regarded as an interval of global warming after the Gondwana extinction/decline of the Guadalupian “tropical trio” in Panthalassa glaciation that lasted for nearly 50 million years from the Late and Tethys indicates that they were involved in a major environ- Carboniferous to the Early Permian (e.g., Crowell, 1999; Jones and mental change of global context; i.e. the G–LB event. It is noteworthy Fielding, 2004). Throughout the late Early and Middle Permian, the that the Capitanian global change appreciably before the G–LB may biodiversity stayed almost constant at the highest level of the have preferentially affected low-latitude shallow-marine communi- Paleozoic (Sepkoski, 1984) until the end of the Guadalupian when a ties and consequently led them to extinction. major mass extinction occurred for the first time since the Late Devonian. The ultimate cause of the G–LB extinction has not been 6.2. Collapse of photosymbiosis deciphered yet; however, the recent documentation of a N3 million 13 year-long interval of high positive δ Ccarb values in the Capitanian The common pattern of expansion/extinction indicates that the carbonates suggests that a temporary cooling (Capitanian Kamura Guadalupian “tropical trio” essentially shared not only the same event) appeared and worked as a potential kill mechanism for the habitat but also the same extinction scenario regardless of their shallow-marine biota in low latitudes at the end-Guadalupian (Isozaki mutual distances in taxonomy. In this respect, living habit such as et al., 2007a,b, 2009). For the Guadalupian “tropical trio” too adapted photosymbiosis was the most likely significant common feature to warm-water conditions, the Capitanian Kamura cooling event was among the three distinct clades. As the tropical shallow-marine particularly crucial. environment in mid-ocean is generally poor in nutrients, animals with The appearance of a temporary cooling in the Capitanian is relatively weak, diffusion-dependent metabolism generally cannot supported by the eustatic sea-level change that records the Phaner- afford large body size. In order to pursue gigantism in such an ozoic lowest stand straddling the G–LB (Hallam and Wignall, 1999; oligotrophic condition, the bivalves and foraminifers need to deploy Tong et al., 1999; Haq and Schutter, 2008), i.e., the termination of the unusual but appropriate strategies. Just like the modern giant clam major reef complex in Texas and extensive unconformity in South Tridacna and large benthic foraminifera hosting photosymbiont China, by the mid-Permian chert event in high latitudes (Beauchamp algae (e.g., Cowen, 1983; Hallock, 1999), Alatoconchidae and and Baud, 2002), and also by the short-time glaciation in Ver- Verbeekinidae probably performed photosymbiosis, as their shell/ khoyansk–Omolon (northeastern Russia) and in eastern Australia test structures are analogous to those of modern counterparts (Ustritsky, 1973; Fielding et al., 2008). In addition, some Early–Middle functioning for hosting symbiont algae/cyanobacteria (Ross, 1972; Permian brachiopods derived from middle-high latitude domains Yancey and Boyd, 1983; Seilacher, 1990; Wilde, 2002; Vachard et al., (e.g., Attenuatella, Waagenites, Strophalosiina, and Comuqia) migrated 2004). The history of photosymbiosis in metazoans likely tracks back towards low latitudes and first appeared in the tropical zone in the to the Cambrian archeothyatids (Cowen, 1988) that are known as the Capitanian (Shen and Shi, 2002), supporting the development of first reef-building metazoans, and the Paleozoic shallow-marine cooling. In general, a low-latitude sea is insensitive to temperature environments may have fostered various photosymbiotic couples change compared with a high latitude sea due to its high heat many times. In addition to the large bivalves and fusulines, some capacity; therefore, a temperature drop in low latitudes directly Paleozoic rugose corals may likewise have performed photosymbiosis indicates the appearance of global cooling. These relations suggest in the shallow-marine photic zone like tabulate corals, although this that the late Middle Permian cooling was not restricted to the low- has yet to be confirmed. latitude domains but was global in extent. The “tropical trio” probably performed photosymbiosis during the Accordingly, all these observations suggest that the extinction of Early-Middle Permian both in Panthalassa and Tethys. Alatoconchidae the “tropical trio” was related to the Capitanian global cooling likely optimized the photosymbiotic system particularly in the Wordian (Kamura event; Fig. 6). Temporary cooling in the middle of the (Middle Guadalupian), as their size reached their maximum (up to 1 m post-Gondwanan long-term warming trend may have been 18 Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21 influential particularly for tropical-adapted, photosymbiosis-depen- of black bituminous limestone with TOC over 0.1 wt.% (remarkably dant biota. Stanley (1988) once discussed that a cooling event caused higher than the gray limestone below and above with TOC less than the P–TB extinction but his idea is likely applicable to the G–LB event 0.01 wt.%). This proves that the demise of the “tropical trio” occurred rather than P–TB per se. The collapse of photosymbiotic systems may in the midst of high primary productivity associated with the have played a significant role not only in the mass killing of the dominant burial of organic material, i.e., eutrophication of a shallow “tropical trio” but also in disturbing the Late Guadalupian ecological sea. The extinction of Alatoconchidae under eutrophic conditions may structures including food web composed of other shallow-marine, represent an actual case in the fossil record of the “paradox of sessile benthos. enrichment” predicted from numerical modeling (Rosenzweig, 1971). The environmental stress(es) may have appeared accumulatively 6.3. Eutrophication shock rather than abruptly. The “tropical trio” were terminated by and large at the same time when the stress(es) exceeded the threshold for Hallock and Schlager (1986) pointed out that eutrophication is survival. fatal to the survival of coral reefs and carbonate platforms. When the In the Capitanian Kamura cooling event, the tropical-adapted world climate changes into cooling, global oceanic circulation gigantic clams plus large-tested fusulines became extinct, and the becomes accelerated and enhances upwelling of abundant nutrients contemporary rugose corals also faced a sharp diversity loss. Although from the deep-sea to the ocean surface. Additional input of nutrients it is not yet clear whether the die-off of symbiont algae by low to the surface will elevate the level of primary productivity through temperature, eutrophication-driven dimming in the water-column, or algal blooming that will make surface waters less transparent. By a combination of the two was critically responsible for the killing, the dimming the photic zone in shallow-water carbonate facies, such Guadalupian photosymbiosis-dependent communities characterized eutrophication can damage photosymbiosis-dependent sessile ben- by the unusual gigantism disappeared dramatically in low-latitude thos fully adapted to oligotrophic conditions with a clear water- domains both in Tethys and Panthalassa. This might have consider- column. In the Holocene mid-oceanic reefs and/or carbonate plat- ably changed the ecological structure, including the food web, in the forms, various carbonate-secreting organisms were terminated by aftermath of the extinction. For a possible cause of the Capitanian eutrophication associated with cooling (Hallock and Schlager, 1986). cooling, and of the G–LB event per se, please refer to Isozaki (2007b, By demonstrating another example in the Eocene, Brasier (1995) 2009) who discussed a contemporary mantle plume activity and pointed out that a similar change from an oligotrophic to a eutrophic relevant effects on the surface environments. condition in shallow-marine environments triggered the extinction of large-tested foraminifera. 6.4. Bivalve gigantism tuned by climate The extinction pattern of the Guadalupian “tropical trio” appears analogous to these cases in several aspects (Fig. 6). The extinction of Gigantism in bivalves has had a long history since the middle Alatoconchidae and Verbeekinidae in the middle of the Kamura Paleozoic. Giant bivalves appeared intermittently at least 5 times in cooling event was not likely a matter of contingency but a new line of the Phanerozoic, i.e. 1) the Silurian–Devonian megalodonts, 2) evidence for intimate cause–effect linkage between the cooling and Permian Alatoconchidae, 3) Late Triassic to Early Jurassic mega- extinction (Isozaki et al., 2007a,b). The topmost part of the Capitanian lodonts/lithiotids, 4) Late Jurassic to Cretaceous rudists/inoceramids, in mid-oceanic paleo-atoll carbonates at Kamura, even above the and 5) Miocene–modern tridacnids (Fig. 7). Most of these aberrant extinction horizon of Alatoconchidae and Verbeekinidae, is composed bivalves lived in shallow-marine environments of low-latitude

Fig. 6. Schematic diagram showing the extinction pattern of the “tropical trio” (Alatoconchidae, Verbeekinidae, and Waagenophyllidae) and relevant environmental/ecological change in the Capitanian (Late Guadalupian). The extinction of the “tropical trio” occurred in the midst of the Kamura cooling event, suggesting that the low sea surface temperature was responsible for collapse of photosymbiotic systems in shallow-marine environments in low-latitude Tethys and Panthalassa. Y. Isozaki, D. Aljinović / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 11–21 19

Fig. 7. History of bivalve gigantism. Ranges of giant bivalves are after Kauffman and Johnson (1988), de Freitas et al. (1993), and this study. Sea-level curve is modified from Hallam (1992) based on Hallam and Wignall (1999), Tong et al. (1999), and Haq and Schutter (2008). Note the 5 intervals of bivalve gigantism punctuated by cool/cold periods that include the well-known Pennsylvanian–Early Permian Gondwana glaciation and recently documented Capitanian (Late Guadalupian) Kamura cooling event. The Toarcian event at the end of the Early Jurassic and the K–TB event at the end of the Cretaceous may have accompanied short-term cool spikes. domains or under extremely warm climates (e.g., Yancey and Boyd, their total range consists of 2 distinct peaks, one in the Siluro- 1983; Kauffman and Johnson, 1988; Seilacher, 1990; de Freitas et al., Devonian and the other in the Late Triassic–Early Jurassic, which are 1993). This suggests that the gigantism represents a common style separated by a remarkably long interval of decline/disappearance in of adaptation to warm-water (probably tropical) shallow-marine the Late Paleozoic that included the well-known Gondwana glacial environments for bivalves regardless of age, and that bivalves period. Their disappearance in the Early Devonian (de Freitas et al., probably attained their extraordinary size through symbiosis. Most 1993) may also have been related to a short-term sea-level drop that of them, including the oldest, most likely performed photosymbiosis, was probably driven by cooling. As to the extinction of the Permian whereas others (e.g., lithiotids and inoceramids) may have deployed Alatoconchidae during the Kamura event, cooling even with a short different (non-photosymbiotic) strategies, such as chemosymbiosis duration, appears to have been a crucial cause for terminating (Seilacher, 1990)likemodernCalyptogena. As demonstrated in gigantism. The extinction of megalodonts at the end of the Early Fig. 7, the rise of photosymbiotic giant bivalves preferentially Jurassic and that of rudists at the end of the Cretaceous likewise may occurred during warming periods. Ohno et al. (1995) postulated have been related to short-term cooling/eutrophication possibly that algal–bivalve symbiosis was established several times in his- associated with the Toarcian event and K–Tboundaryevent, tory, and that the bivalves changed their habit from an infaunal to respectively. Likewise, the gradual increase in size of rudist apparently an epifaunal style via sciaphilous (shade-loving) stages once they occurred during a period of warming, whereas their sharp decline acquired photosymbiosis. took place during times of short-term cooling, as across the Jurassic/ The gigantism of bivalves, specialized for the tropical domain, Cretaceous boundary, in the Middle–Late Aptian, in the Early–Late appears to have been fragile, because their survival was highly Cenomanian, and in the Middle–Late Maastrichtian (Kauffman and dependent on the stability of warm environments. Although the Johnson, 1988; personal communication from Bogdan Jurkovsek). symbiosis between bivalves and photosynthetic bacteria/algae likely Further study of the fundamental processes of bivalve gigantism in started in the Early Silurian (de Freitas et al., 1993), it is noteworthy the light of climate-tuned radiation/extinction patterns is definitely that none of the gigantic bivalves lasted a long time, not longer than needed; however, the gigantism in tropical shallow-marine environ- two geologic periods (Fig. 7). The historical pattern in occurrence of ments may potentially serve as a sensitive monitor for seawater the photosymbiotic giant bivalves in the Phanerozoic suggests that temperature in low-latitude areas in the past. their intermittent rise and decline may have been controlled by a long-term change in global climate. 7. 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