COMMENTARY Evolution of habitat depth in the ammonoids

Kazuyoshi Moriya1 oxygen isotopic analyses of shell materials of Department of Earth Sciences, Faculty of Education and Integrated Arts and Sciences, ammonoids reveal the temperature at which Waseda University, Shinjuku-ku, Tokyo 169-8050, Japan the shell was secreted. This technique, called oxygen isotopic thermometry, has been widely Ammonoids, a of with body and close modern relatives. For used in paleoclimatological and paleobiologi- external chambered shells, arose in the early example, although one may usually imagine that cal research. It was also applied to ammonoid and went extinct at the Cretaceous/ ammonoids were planktic or nektic organisms fossils more than 40 y ago (2, 3). Many scien- (K/Pg) boundary. During their 340- within a water column, like the ,which tists, however, assumed that ammonoids were planktic or nektic organisms, so their discus- million-y history, ammonoids suffered three is the sole surviving bearing an sion focused mainly on growth rates inferred major diversity crises at the end of the Devonian, external chambered shell, there is very little by identifying sinusoidal patterns, hence sea- , and Periods, and the terminal direct evidence showing the habitat depth of sonality, in the temperature data. Among event at the K/Pg boundary. Because ammonoids within an ancient water column. those previous workers, Anderson et al. (4) of their rapid morphological evolution and rich Sessa et al. (1) shed new light on the habitat analyzed oxygen isotopic composition of the record, ammonoids have been used to depth of the Cretaceous ammonoids using geo- ammonoids and compared determine the relative age of marine strata and chemical proxy records. When calcium carbon- the results with those of co-occurring benthic correlation since the dawn of . ate, which composes the shell material of many and planktic organisms. The isotopic tempera- Although the morphological analyses of shell marine invertebrates, is secreted within the tures of () were materials have provided some insights into ocean,thestableoxygenisotopiccomposition significantly warmer than those of benthic ontogeny and evolution, their biological nature of the carbonate is predominantly determined bivalves and slightly cooler than those of sur- is poorly understood because of the lack of soft by the ambient ocean temperature. Therefore, face-dwelling organisms, indicating a planktic or nektic mode of life of Kosmoceras (i.e., a position high in the water column) (Fig. 1). Phylogeny and evolution of mode of life In contrast, when Moriya et al. (5) analyzed Ma of the Jurassic–Cretaceous ammonoids isotopic temperatures of the Period ammonoids and co-occurring planktic and ben- 70 (1) (1) thic organisms, isotopic temperatures of all 75

Campanian ratoidea

e ammonoids analyzed, regardless of their taxo-

(5) (5) (5) Hoplitoidea (5) Turrilitoidea hoc nomic and morphological relationships, were

Coniacian nt dea a c oi essentially identical to those of benthic fora-

Turonian t i A Acanthoceratoidea minifers and bivalves, and significantly cooler 100 aph (8) c (8) S Scaphitoidea

a than those of planktic foraminifers, indicating dea i

sitoidea a demersal (bottom dwelling) habitat of these e

nctoide ammonoid species (Fig. 1). Because paleontol- hi gonito Cretaceous shay a r sp e a ogists working on ammonoids expected that 125 D Deshayesitoidea eri Douvilleiceratoidea Tet Tetragonitoidea ide P the morphological features of the external

Hauterivian ato (9) r e shells must, at least partly, represent their ecol-

Valanginian d toidea o a

Berriasian yl ogy, these results raised many arguments c a n de A Ancyloderatoidea

150 idea on ammonoid ecology. Since the works of

Kimmeridgian hanocer ato Anderson et al. (4) and Moriya et al. (5), the use

Oxfordian er c Step Stephanoceratoidea

Callovian o l (6) of isotopic thermometry on ammonoid fossils Spiroceratoi Spiroceratoidea (4) Hap for identifying their ecology has becomes more 175 widespread (6–8) (Fig. 1). However, because of technical difficulties in identifying thermal Jurassic Planktic or nektic structure of the water column with analyzing Demersal

Eoderoceratoidea apparent planktic and benthic organisms, a full Lytoceratoidea Phylloceratoidea Psiloceratoidea (Bottom dwelling) set of data for planktic and benthic organisms

Fig. 1. Phylogeny and evolution of mode of life of the Jurassic–Cretaceous ammonoids. Age of each stage boundary is from Gradstein et al. (16). Phylogeny of ammonoids is cited from Yacobucci (17). Open white circles represent Author contributions: K.M. wrote the paper. isotopic results indicating demersal (bottom dwelling) habitat at the age plotted on each lineage. Gray filled circles The author declares no conflict of interest. indicate planktic or nektic habitat. Numbers at left bottom of each circle represent references for each data. Pink bar, (5); orange bar, (5); yellow bar, ; pale green bar, Haploceratina; pale blue, See companion article on page 15562. Perisphinctina (4–6, 8, 9); purple bar, (1, 5, 8). 1Email: [email protected]

15540–15541 | PNAS | December 22, 2015 | vol. 112 | no. 51 www.pnas.org/cgi/doi/10.1073/pnas.1520961112 Downloaded by guest on October 1, 2021 co-occurring with ammonoids have rarely been tion, and other ecological factors must K/Pg terminal . Alternatively, COMMENTARY described since Moriya et al. (5). An additional have been critical for ammonoids at the habitat of hatchling and juvenile ammonoids unanswered question is how habitat depth pref- K/Pg boundary. One potential hypothesis is the other candidate for the fatal ecology for erences evolved in ammonoids, especially in the is the food habit. Kruta et al. (10) presented the latest Cretaceous ammonoids. On the latest Cretaceous time just before the terminal that the late Cretaceous preyed basis of their small embryonic shell size (0.5– extinction event. For discussing mechanisms upon planktic microorganisms. Because it is 1.8 mm in diameter) and the occurrence of and dynamics of paleobiodiversity, paleoecosys- massive accumulation of embryonic shells, tem, and extinction events, a fundamental The report by Sessa eggs and hatchlings are thought to have been knowledge about habitat depth of ammonoids et al. is the first paper to planktic, feeding during early development is crucial. describe the habitat of on planktic microorganisms (12–14). If this The report by Sessa et al. (1) is the first werethecase,theabruptdemiseofplanktic paper to describe the habitat of ammonoids ammonoids in the latest ecosystems at the K/Pg boundary would have in the latest Cretaceous Western Interior Seaway Cretaceous Western In- had a great impact on the survival of newly of North America with a full set of concrete terior Seaway of North hatched ammonoids, but not on the direct- evidence from oxygen isotopic thermometry. developing . However, Landman Isotopic temperatures calculated from planktic America with a full set et al. (15) pointed out the differences in foraminifers inhabiting the mixed layer of the of concrete evidence the timing of extinction between cosmo- water column and benthic organisms on the sea politan and endemic ammonoids. Although floor show temperatures of ∼26 °C and ∼19 °C, from oxygen isotopic ∼ both cosmopolitans and endemics share the respectively, indicating 7 °C differences thermometry. similar embryonic shell size, only endemics between surface and bottom waters. The went extinct at the K/Pg boundary, and few mean isotopic temperatures of the latest Cre- expected that marine planktic ecosystem of cosmopolitans survived into the earliest Pa- taceous ammonoids, Eubaculites carinatus microorganisms was severely damaged at leocene, indicating embryonic shell size; hence, and Eubaculites latecarinatus (Turrilitoidea), the K/Pg boundary (11), Kruta et al. (10) embryonic ecology may not have been the and iris (Scaphitoidea) are es- proposed that the collapse of the ma- keytosurvival.However,theterminationof timated as ∼18 °C, comparable to those of rine planktic food web was the trigger of all ammonoids—including cosmopolitans— benthic organisms (1). In addition to isotopic the ammonoid extinction event. However, results, careful examination of the preservation Tanabe (12) argued that other groups of at the earliest ad extremum, and of shell materials excludes potential postmor- ammonoids with a jaw apparatus similar to the survival of the cephalopods, tem drift, often a concern in organisms with modern nautiloids (e.g., phylloceratids and indicate that the fatal ecology for ammo- potentially buoyant shells. These lines of evi- gaudryceratids), which are assumed to prey noids has yet to be identified. The hypothe- dence clearly indicate that these ammonoid on macroorganisms, also became extinct at ses mentioned above can be tested further species were demersal (bottom dwelling) or- the boundary, indicating that feeding habits with developments of new analytical tech- ganisms, providing the first direct evidence of at submature and mature growth stages were niques and using exceptionally well-preserved habitat depths for the latest Cretaceous lineages also not related to loss of ammonoids in the materials. that became extinct at or just above the K/Pg boundary (9), Although data are still sparse, an overview of 1 Sessa JA, et al. (2015) Ammonite habitat revealed via isotopic 9 Landman NH, Garb MP, Rovelli R, Ebel DS, Edwards LE (2012) – composition and comparisons with co-occurring benthic and Short-term survival of ammonites in New Jersey after the End- evolutional history of habitats of the Jurassic planktonic organisms. Proc Natl Acad Sci USA 112:15562–15567. Cretaceous Bolide impact. Acta Palaeontol Pol 57(4):703–715. Cretaceous ammonoids indicates a very interest- 2 Stahl W, Jordan R (1969) General considerations on isotopic 10 Kruta I, Landman NH, Rouget I, Cecca F, Tafforeau P (2011) The ing view (Fig. 1). Although many previous paleotemperature determinations and analyses of Jurassic role of ammonites in the marine food web revealed by jaw ammonites. Earth Planet Sci Lett 6(3):173–178. preservation. Science 331(6013):70–72. workers expected that ammonoids were 3 Jordan R, Stahl W (1970) Isotopische Paläotemperatur 11 Huber BT, MacLeod KG, Norris RD (2002) Abrupt extinction and predominantly planktic or nektic organisms, Bestimmungen an jurassischen Ammoniten and grundsätzliche subsequent reworking of Cretaceous planktonic across the Cretaceous- boundary: Evidence from the subtropical isotopic data suggest that bottom-dwelling hab- Voraussetzungen für diese Methode. Geol Jahrb 89:33–62. 4 Anderson TF, Popp BN, Williams AC, Ho L-Z, Hudson JD (1994) The North Atlantic. Catastrophic Events and Mass Extinction: Impacts itat seems to be more frequent among the am- stable isotopic record of fossils from the Member, and Beyond, eds Koeberl C, MacLeod KG (Geological Society of America, Boulder, CO), pp 277–289. Clay Formation (Jurassic), UK: Palaeoenvironmental monoids after the Triassic/Jurassic diversity 12 Tanabe K (2011) . The feeding habits of ammonites. implications. J Geol Soc London 151(1):125–138. crisis. Additionally, in Perisphinctoidea, habitat Science 331(6013):37–38. 5 Moriya K, Nishi H, Kawahata H, Tanabe K, Takayanagi Y (2003) 13 Landman NH, Tanabe K, Shigeta Y (1996) Ammonoid embryonic depth reverted back from demersal to planktic/ Demersal habitat of Late Cretaceous ammonoids: Evidence from development. Ammonoid Paleobiology, eds Landman NH, Tanabe K, oxygen isotopes for the (Late Cretaceous) northwestern nektic even within a lineage. As Sessa et al. (1) David RA (Plenum, New York), pp 343–405. Pacific thermal structure. 31(2):167–170. show, many groups of ammonoids (Phyllocer- 14 De Baets K, et al. (2015) Ammonoid embryonic development. 6 Lécuyer C, Bucher H (2006) Stable isotope compositions of a late atoidea, Tetragonitoidea, Desmoceratoidea, Ammonoid Paleobiology: From Anatomy to Ecology, eds Klug C, Jurassic ammonite shell: A record of seasonal surface water Korn D, de Baets K, Kruta I, Mapes RH (Springer, The Netherlands), pp – Scaphitoidea, and Turrilitoidea), which possessed temperatures in the southern hemisphere? eEarth 1:1 7. 113–205. a demersal habitat, went extinct at the K/Pg 7 Henderson RA, Price GD (2012) Paleoenvironment and 15 Landman NH, et al. (2014) Ammonite extinction and nautilid paleoecology inferred from oxygen and carbon isotopes of survival at the end of the Cretaceous. Geology 42(8):707–710. boundary (Fig. 1). However, the planktic/ subtropical mollusks from the Late Cretaceous (Cenomanian) of 16 Gradstein FM, Ogg JG, Schmitz MD, Ogg GM (2012) The nektic group (Acanthoceratoidea) also went ex- Bathurst Island, Australia. Palaios 27(9-10):618–627. 2012 (Elsevier, Boston). tinct at the same time. These facts suggest that 8 Stevens K, Mutterlose J, Wiedenroth K (2015) Stable isotope data 17 Yacobucci MM (2015) Macroevolution and paleobiology of (δ18O, δ13C) of the ammonite genus Simbirskites—Implications for Jurassic–Cretaceous ammonoids. Ammonoid Paleobiology: From the habitat depth of submature and mature habitat reconstructions of extinct cephalopods. Palaeogeogr Macroevolution to Paleogeography, eds Klug C, Korn D, de Baets K, individuals was not the determinant of extinc- Palaeoclimatol Palaeoecol 417:164–175. Kruta I, Mapes RH (Elsevier, The Netherlands), pp 189–228.

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