Benton, M.J. and Simms, M.J. 1995. Testing the Marine and Continental

Home , Gnathostomata (echinoid), Phymosomatoida

Downloaded from geology.gsapubs.org on 18 January 2009

Geology

Testing the marine and continental fossil records

M. J. Benton and M. J. Simms

Geology 1995;23;601-604 doi:10.1130/0091-7613(1995)023<0601:TTMACF>2.3.CO;2

Email alerting services click www.gsapubs.org/cgi/alerts to recieve free email alerts when new articles cite this article Subscribe click www.gsapubs.org/subscriptions/index.ac.dtl to subscribe to Geology Permission request click http://www.geosociety.org/pubs/copyrt.htm#gsa to contact GSA

Copyright not claimed on content prepared wholly by U.S. government employees within scope of their employment. Individual scientists are hereby granted permission, without fees or further requests to GSA, to use a single figure, a single table, and/or a brief paragraph of text in subsequent works and to make unlimited copies of items in GSA's journals for noncommercial use in classrooms to further education and science. This file may not be posted to any Web site, but authors may post the abstracts only of their articles on their own or their organization's Web site providing the posting includes a reference to the article's full citation. GSA provides this and other forums for the presentation of diverse opinions and positions by scientists worldwide, regardless of their race, citizenship, gender, religion, or political viewpoint. Opinions presented in this publication do not reflect official positions of the Society.

Notes

M. J. Benton Department of Geology, University of Bristol, Bristol BS8 1RJ, United Kingdom M. J. Simms Department of Geography and Geology, Cheltenham and Gloucester College of Higher Education, Francis Close Hall, Cheltenham GL50 4AZ, United Kingdom

ABSTRACT phylogenies of echinoderms was tested for The fossil record of continental vertebrates is as good as that of echinoderms at the fossil-record quality (Table 1). Data for 72 family level, as shown by tests of the match of cladistic and stratigraphic data and of listed cladograms of vertebrates have been relative completeness. If echinoderms and vertebrates are typical of their environments, the published (Benton and Storrs, 1994, 1995). continental fossil record is not worse than the marine, despite the fact that, at a local level, For purposes of comparison, the nine clad- fossils are usually more abundant in marine sequences than in continental successions. The ograms of marine taxa (Actinopterygii, explanation of this paradox may be that vertebrates have attracted more intensive study Gnathostomata, Sarcopterygii, Sauroptery- than echinoderms, and thus the level of knowledge of their fossil record is some decades gia, Teleostei) were excluded, leaving 63 ahead of that of echinoderms. This finding validates the use of different kinds of fossil data trees of continental vertebrates. in broad-scale phylogenetic studies. If skeletonized marine shelf invertebrates have a markedly better fossil record than INTRODUCTION branching as indicated by phylogenetic data, continental animals, then the echinoderm It has often been asserted that the fossil and (2) the relative completeness of fossil test cases should show more examples of sta- record of marine shelf benthic organisms is records based on independent evidence for tistically significant rank order correlation better than that of continental organisms the size of gaps. than the vertebrates. The results of SRC (Benton, 1985; Flessa, 1990; Jablonski, The test of stratigraphic (age) and phylo- tests (Fig. 2, A and B) apparently show the 1991; Raup, 1979; Valentine, 1969). This as- genetic (clade) evidence about the origins of opposite. Fewer echinoderm cladograms sumption has been made by scaling up field groups (Norell, 1992, 1993; Norell and No- (38%) showed significant (P Ͻ 0.05) match- observations on Phanerozoic rocks. Typi- vacek, 1992a, 1992b) consists of comparing ing of clade order and age order than did the cally, limestones and clastic rocks laid down the rank order of nodes on a published clad- continental vertebrate cladograms (63%). on the shallow continental shelf yield abun- ogram (Fig. 1, A and B) with the rank order The same is true for highly significant cor- dant fossils of skeletonized invertebrates, of group appearances as documented in the relations (P Ͻ 0.01), found in 26% of cases such as brachiopods, molluscs, corals, ar- paleontological literature (Fig. 1C). The for echinoderms but in 41% of cases for con- thropods, bryozoans, and echinoderms match of clade and age data is assessed by tinental vertebrates. (Fu¨rsich, 1990; Kidwell, 1986). Continental the Spearman rank correlation (SRC) test. The low pass rate for echinoderm clad- sedimentary sequences generally yield less This approach depends upon the obser- ograms was surprising, especially in compar- abundant faunas of freshwater fishes and vation that there are three essentially inde- ison with cladograms of continental verte- molluscs, terrestrial insects, and vertebrates pendent methods of disentangling the se- brates. This result is almost certainly an (Behrensmeyer and Hill, 1980; Retallack, quence of events in the history of life: (1) the artifact of the small size of many of the echi- 1984). This differentiation may largely be an order of fossils in the rocks (stratigraphic noderm cladograms, 13 (21%) of which in- effect of the nature of the sediments: sedi- data); (2) cladograms, based generally on clude only 4 taxa. Such a small sample size mentation in river systems and lakes is assessments of the sequence of acquisition cannot yield critical values for the SRC co- highly episodic compared to the more con- of morphological characters; and (3) molec- efficient (Sprent, 1989). When the small tinuous deposition on marine shelves and ular phylogenies, founded on sequencing of (n ϭ 4) echinoderm cladograms are ex- particularly in abyssal areas of oceans nucleic acids or proteins, or on DNA-DNA cluded, the SRC scores match more closely (Sadler, 1981). hybridization. If it is accepted that these those discovered for continental vertebrates We test here the idea that groups of or- three approaches, stratigraphic, cladistic, (Fig. 2A), but still show a poorer pass rate ganisms known from a rich supply of fossils and molecular, are essentially independent, than do the cladograms of continental in the field necessarily have a fuller and bet- then mutual cross testing should be possible. vertebrates. ter-documented picture of large-scale phy- The comparison tests do not assume that The SRC test of matching between clade logeny than groups represented by sparse any one technique is better than another: and age order considers only one aspect of fossil materials. The test groups were echi- they merely compare the matching and as- the quality of the fossil record. Another cru- noderms (marine invertebrates) and tetra- sume that, if a large enough sample is used, cial feature is the relative completeness of pods (continental vertebrates). These the results will have statistical validity. particular examples, and this may be as- groups were selected for comparison be- Equivalent tests are available (Huelsenbeck, sessed by comparing the proportion of cause there is a sufficient number of clad- 1994) to test the quality of cladograms known fossil records to gaps, the relative ograms available for each and because both against stratigraphic data. completeness index (RCI) of Benton and groups consist of multielement taxa, the Comparative studies (Benton, 1994, 1995; Storrs (1994) (Fig. 1). skeletons of which may be preserved com- Benton and Storrs, 1994, 1995; Gauthier et If marine invertebrates have a better fos- pletely or may break up before burial. al., 1988; Norell, 1992, 1993; Norell and No- sil record than continental vertebrates, the vacek, 1992a, 1992b) have shown a good RCI values for the former should be mark- TESTING THE QUALITY OF THE match between cladistic branching order edly higher than those for the latter. This FOSSIL RECORD and the order of first fossil representatives does not appear to be the case. The RCI The quality of the long-term global-scale for 55%–73% of cladograms of vertebrates. values for echinoderms and vertebrates fossil record may be tested by comparison of A first attempt is made here to extend the range from Ϫ5% to 100%, but continental (1) the order of origin of groups from the tests to cladograms of nonvertebrates. vertebrates have more complete fossil stratigraphic record with the order of A sample of 63 cladograms and molecular records than do echinoderms (Fig. 2, C

Geology; July 1995; v. 23; no. 7; p. 601–604; 3 figures; 1 table. 601 Figure 1. Methods for assessing quality of fossil record by comparing branching order in cladograms (A–C) with stratigraphic data and by comparing relative amount of gap and known record (C). Cladistic rank is determined by counting sequence of pri- mary nodes in cladogram (A). In many cases, published cladograms do not con- form to simple pectinate pattern in which all terminal taxa are simple side branches of single main stem. Frequently, there are more complex topologies in which some branches subdivide further (A), or some nodes may be partially unresolved, and give rise to more than one branch. In these cases, cladogram is reduced to pectinate form (B), and groups of taxa that meet main axis at same point are combined and treated as single unit. Stratigraphic sequence of clade appearance is assessed from earliest known fossil representative of sister groups, and clade rank and stratigraphic rank may then be compared (C). Minimum implied gap (MIG, diagonal rule) is difference between age of first representative of lineage and that of its sister, because oldest known fossils of sister groups are rarely of same age. MIG is minimum estimate of stratigraphic gap, as true age of lineage divergence may lie well before oldest known fossil. Relative completeness of fossil record may be assessed by comparing proportion of known range (standard range length, SRL) to ghost range, in form of relative completeness index (RCI), defined as:

͚(MIG) RCI ϭ 1 Ϫ ϫ 100%. [ ͚(SRL)]

(SRL ؍ Values of RCI range from 0% (MIG Negative values also .(0 ؍ to 100% (MIG occur when MIG > SRL. Single standard source of stratigraphic information (Ben- ton, 1993) has been used throughout our work.

602 GEOLOGY, July 1995 Figure 2. Comparison of measures of completeness of fossil record of echinoderms and continental vertebrates. A and B: Assessments of statistical significance of Spearman rank correlation (SRC) tests, re- corded as negatively correlated (neg), not significantly correlated (ns), or significantly correlated at P < 0.05 *, P < 0.025 **, P < 0.01 ***, and P < 0.005 ****. Many more cladograms of Figure 3. Comparison of relative complete- continental vertebrates ness of fossil record of echinoderms and con- (B), 40 out of 63 (63%), tinental vertebrates, based on distribution of show statistically signif- relative completeness indices (RCI). In all icant (P < 0.05) matches cases, most cladograms show RCI values of clade and age order >50%. Sample of cladograms of all echino- -for echi ;%66 ؍ has mean RCI (63 ؍ than do cladograms of derms (n echinoderms (A) (24 out noderm cladograms with more than four ter- and for ;%70 ؍ mean RCI ,(50 ؍ of 63; 38%). Figures for minal taxa (n ,(63 ؍ highly significant corre- continental vertebrate cladograms (n Continental vertebrates do not .%70 ؍ lations (P < 0.01) show mean only 16 cases (25%) for have fossil record significantly different (Kol- echinoderms (A), but 26 mogorov-Smirnov test) from that of echino- cases (41%) for conti- derms, whether all echinoderm cladograms, nental vertebrates (B). When smallest echinoderm cladograms are excluded, those with four or larger echinoderm cladograms only. terminal taxa (A), figures are more comparable: 46% of cladograms show significant (P < 0.05) correlations of clade and age data, whereas 30% show highly significant (P < 0.01) correlations. Distributions are not significantly different (Kolmogorov-Smirnov test). C and D: Comparison of phylogeny. Dinosaur fossils may be rare on relative completeness index (RCI) values for echinoderms and continental vertebrates. In both cases, many more cladograms have RCI values >50% (i.e., more known record than cladistic the ground, but their fossil record is no minimum implied gap, MIG) than <50%. Of echinoderm cladograms (C), 78% show higher RCI worse than that of skeletonized marine in- values (RCI > 50%), compared to 95% of continental vertebrate cladograms (D). vertebrates for large-scale studies.

ACKNOWLEDGMENTS and D, 3), although the frequency distribu- different, when assessed on a global scale. Supported in part by the Leverhulme Trust. We thank Derek Briggs, Glenn Storrs, Karl Flessa, tions cannot be distinguished statistically. The macroevolutionary quality of the fossil and Doug Erwin for helpful comments. This surprising discovery matches the find- record is determined by the number of strat- ings of the SRC test. igraphic horizons at which identifiable finds REFERENCES CITED The echinoderm fossil record may seem have been made, and improvements can oc- Behrensmeyer, A. K., and Hill, A. P., 1980, Fossils poorer because the test cladograms are gen- cur only by discovery of new sections. in the making: Vertebrate taphonomy and paleoecology: Chicago, University of Chi- erally smaller (mean number of terminal The surprisingly good quality of the con- cago Press, 338 p. taxa ϭ 6.3) than are those of continental tinental vertebrate fossil record may reflect Benton, M. J., 1985, Mass extinction among nonvertebrates (n ϭ 10.7). It is unclear whether the fact that it has been exploited more in- marine tetrapods: Nature, v. 316, p. 811–814. there is a relation between cladogram size tensively than has that of echinoderms. The Benton, M. J., 1993, The fossil record 2: London, Chapman and Hall, 839 p. and RCI values: for echinoderms there is no number of active taxonomists working on Benton, M. J., 1994, Palaeontological data, and correlation, but for vertebrates the RCI tetrapods is much greater than the number identifying mass extinctions: Trends in Ecol- value is inversely proportional to cladogram studying any invertebrate phylum (Gaston ogy and Evolution, v. 9, p. 181–185. size (P Ͻ 0.01). When smaller echinoderm and May, 1992). Thus, it is probable that a Benton, M. J., 1995, Testing the time axis of phy- cladograms (n ϭ 4) were culled from the higher proportion of fossilized tetrapod taxa logenies: Royal Society of London Philosoph- ical Transactions, ser. B, v. 349. comparative sets, the distributions of RCI than echinoderm taxa has been identified. Benton, M. J., and Storrs, G. W., 1994, Testing the values for both groups still could not be dis- This may explain the counterintuitive dis- quality of the fossil record: Paleontological tinguished statistically (Fig. 3). covery that continental tetrapods have a bet- knowledge is improving: Geology, v. 22, ter fossil record than echinoderms, but it in p. 111–114. CONTINENTAL RECORDS AS GOOD Benton, M. J., and Storrs, G. W., 1995, Diversity no way detracts from that finding. Ulti- in the past: Comparing cladistic phylogenies AS MARINE? mately, when an equivalent number of hours and stratigraphy, in Hochberg, M. E., et al., These results show that studies of the rel- of study has been devoted to both groups, eds., The genesis and maintenance of biolog- ative abundance of specimens of different echinoderms may prove to have a more ical diversity: Oxford, United Kingdom, Ox- phyla in fossiliferous sites are not a guide to complete fossil record than continental tet- ford University Press. Blake, D. B., 1987, A classification and phylogeny their value in larger scale studies of phylog- rapods at the family and/or stage level. of post-Palaeozoic sea stars (Asteroidea: eny and macroevolution. In marine shelf The discovery that continental verte- Echinodermata): Journal of Natural History, sites, echinoderm fossils may be immensely brates have a fossil record of quality equiv- v. 21, p. 481–528. abundant, whereas continental vertebrate alent to that of echinoderms, despite enor- David, B., 1988, Origins of the deep-sea holaste- roid fauna, in Paul, C. R. C., and Smith, fossils are typically sparse. Nevertheless, the mous differences in local abundance of A. B., eds., Echinoderm phylogeny and evo- amount of error inherent in the fossil fossils in both settings, vindicates the value lutionary biology: Oxford, United Kingdom, records of both groups is not significantly of the fossil record for large-scale studies of Clarendon Press, p. 331–346.

GEOLOGY, July 1995 603 Donovan, S. K., 1988, The early evolution of the Norell, M. A., and Novacek, M. J., 1992b, Con- Smith, A. B., 1990, Echinoid evolution from the Crinoidea, in Paul, C. R. C., and Smith, A. B., gruence between superpositional and phylo- Triassic to Lower Liassic: Cahiers de eds., Echinoderm phylogeny and evolution- genetic patterns: Comparing cladistic pat- l’Universite´ Catholique de Lyon, Se´ries Sci- ary biology: Oxford, United Kingdom, Clar- terns with fossil records: Cladistics, v. 8, entifique, v. 3, p. 79–117. endon Press, p. 235–244. p. 319–337. Smith, A. B., 1992, Echinoderm phylogeny: Mor- Durham, J. W., 1966, Clypeasteroids, in Moore, Paul, C. R. C., 1988, The phylogeny of the cyst- phology and molecules approach accord: R. C., ed., Treatise on invertebrate paleon- oids, in Paul, C. R. C., and Smith, A. B., eds., Trends in Ecology and Evolution, v. 7, tology, Part U, Echinodermata 3(2): Boul- Echinoderm phylogeny and evolutionary bi- p. 224–229. der, Colorado, Geological Society of Amer- ology: Oxford, United Kingdom, Clarendon Smith, A. B., and Arbizu, M. A., 1987, Inverse ica (and University of Kansas Press), Press, p. 199–213. larval development in a Devonian edrioas- p. U450–U491. Paul, C. R. C., and Smith, A. B., 1984, The early teroid from Spain and the phylogeny of Emlet, R. B., 1988, Crystallographic axes of echi- radiation and phylogeny of the echinoderms: Agelacrinitinae: Lethaia, v. 20, p. 49–62. noid genital plates reflect larval form: Some Biological Reviews, v. 59, p. 443–481. Smith, A. B., and Hollingworth, N. T. J., 1990, phylogenetic implications, in Paul, C. R. C., Raff, R. A., and eight others, 1988, Molecular Tooth structure and phylogeny of the Upper and Smith, A. B., eds., Echinoderm phylog- analysis of distant phylogenetic relationships Permian echinoid Miocidaris keyserlingi: eny and evolutionary biology: Oxford, United in echinoderms, in Paul, C. R. C., and Smith, Yorkshire Geological Society Proceedings, Kingdom, Clarendon Press, p. 299–310. A. B., eds., Echinoderm phylogeny and evo- v. 48, p. 47–60. Feral, J.-P., and Derelle, E., 1990, in Yanagisawa, lutionary biology: Oxford, United Kingdom, Smith, A. B., and Wright, C. W., 1989, British T., et al., eds., Echinoderm biology: Rotter- Clarendon Press, p. 29–41. Cretaceous echinoids. Part 1, General intro- dam, Netherlands, A. A. Balkema, p. 331–338. Raup, D. M., 1979, Biases in the fossil record of duction and Cidaroida: Palaeontographical Flessa, K. W., 1990, The ‘‘facts’’ of mass extinc- species and genera: Carnegie Museum of Society Monographs, v. 141, p. 1–101. tions, in Sharpton, V. L., and Ward, P. D., Natural History Bulletin, v. 13, p. 85–91. Smith, A. B., and Wright, C. W., 1990, British eds.,GlobalcatastrophesinEarthhistory:Ge- Retallack, G., 1984, Completeness of the rock and Cretaceous echinoids. Part 2, Echinothuri- ological Society of America Special Pa- fossil record: Some estimates using fossil oida, Diademodontoida and Stirodonta (1, per 247, p. 1–7. soils: Paleobiology, v. 10, p. 59–78. Calycina): Palaeontographical Society Mono- Fu¨rsich, F. T., 1990, Fossil concentrations and life Sadler, P. M., 1981, Sediment accumulation rates graphs, v. 143, p. 101–198. and death assemblages, in Briggs, D. E. G., and the completeness of stratigraphic sec- Smith, A. B., and Wright, C. W., 1993, British and Crowther, P. R., eds., Palaeobiology; a tions: Journal of Geology, v. 89, p. 569–584. Cretaceous echinoids. Part 3, Stirodonta 2, synthesis: Oxford, United Kingdom, Black- Seilacher, A., 1979, Constructional morphology Hemicidaroida and Phymosomatoida, Part 1: well Scientific, p. 235–239. of sand dollars: Paleobiology, v. 5, p. 191–221. Palaeontographical Society Monographs, Gale, A. S., 1987, Phylogeny and classification of Simms, M. J., 1988, The phylogeny of post- v. 147, p. 199–267. the Asteroidea (Echinodermata): Linnean Palaeozoic crinoids, in Paul, C. R. C., and Smith, A. B., Lafay, B., and Christen, R., 1992, Society Zoological Journal, v. 89, p. 107–132. Smith, A. B., eds., Echinoderm phylogeny Comparative variation of morphological and Gaston, K. J., and May, R. M., 1992, Taxonomy of and evolutionary biology: Oxford, United molecular evolution through geologic time: taxonomists: Nature, v. 356, p. 281–282. Kingdom, Clarendon Press, p. 269–284. 28S ribosomal RNA versus morphology in Gauthier, J., Kluge, A. G., and Rowe, T., 1988, Simms, M. J., 1993, Echinodermata, in Benton, echinoids: Royal Society of London Philo- Amniote phylogeny and the importance of M. J., ed., The fossil record 2: London, Chap- sophical Transactions, ser. B, v. 338, fossils: Cladistics, v. 4, p. 105–209. man and Hall, p. 491–528. p. 365–382. Huelsenbeck, J. P., 1994, Comparing the strati- Simms, M. J., 1994, Reinterpretation of thecal Sprent, P., 1989, Applied nonparametric statisti- graphic record to estimates of phylogeny: Pa- plate homology and phylogeny in the Class cal methods: London, Chapman and Hall, leobiology, v. 20, p. 470–483. Crinoidea: Lethaia, v. 26, p. 303–312. 259 p. Jablonski, D., 1991, Extinctions: A paleontologi- Simms, M. J., and Sevastopulo, G. D., 1993, The Valentine, J. W., 1969, Patterns of taxonomic and cal perspective: Science, v. 253, p. 754–757. origin of articulate crinoids: Palaeontology, ecological structure of the shelf benthos dur- Jensen, M., 1981, Morphology and classification v. 36, p. 91–109. ing Phanerozoic time: Palaeontology, v. 12, of the Euechinoidea Bronn, 1860—A cladis- Smiley, S., 1988, The phylogenetic relationships p. 684–709. tic analysis: Videnskabelige Meddelelser fra of holothurians: A cladistic analysis of the Dansk Naturhistorisk Forening i Kjoben- extant echinoderm classes, in Paul, C. R. C., Manuscript received December 27, 1994 havn, v. 143, p. 7–99. and Smith, A. B., eds., Echinoderm phylog- Revised manuscript received March 23, 1995 Kidwell, S. M., 1986, Models of fossil concentra- eny and evolutionary biology: Oxford, Manuscript accepted March 29, 1995 tions: Paleobiologic implications: Paleobiol- United Kingdom, Clarendon Press, p. 69–84. ogy, v. 12, p. 6–24. Smith, A. B., 1984a, Classification of the Echino- Matsumura, T., Hasegawa, M., and Shigei, M., dermata: Palaeontology, v. 27, p. 431–459. 1979, Collagen biochemistry and phylogeny Smith, A. B., 1984b, Echinoid palaeobiology: of echinoderms: Comparative Biochemistry London, George Allen and Unwin, 190 p. and Physiology, v. 62B, p. 101–105. Smith, A. B., 1985, Cambrian eleutherozoan Milsom, C., Simms, M. J., and Gale, A. S., 1994, echinoderms and the early diversification Phylogeny and palaeobiology of Marsupites of edrioasteroids: Palaeontology, v. 28, and Uintacrinus: Palaeontology, v. 38, p. 715–756. p. 595–607. Smith, A. B., 1988a, Fossil evidence for the rela- Mooi, R., 1990, Paedomorphosis, Aristotle’s lan- tionships of extant echinoderm classes and tern, and the origin of the sand dollars (Echi- their times of divergence, in Paul, C. R. C., nodermata: Clypeasteroida): Paleobiology, and Smith, A. B., eds., Echinoderm phylog- v. 16, p. 25–48. eny and evolutionary biology: Oxford, Norell, M. A., 1992, Taxic origin and temporal United Kingdom, Clarendon Press, p. 85–97. diversity: The effect of phylogeny, in No- Smith, A. B., 1988b, Patterns of diversification vacek, M. J., and Wheeler, Q. D., eds., Ex- and extinction in early Palaeozoic echino- tinction and phylogeny: New York, Colum- derms: Palaeontology, v. 31, p. 799–828. bia University Press, p. 89–118. Norell, M. A., 1993, Tree-based approaches to understanding history: Comments on ranks, rules, and the quality of the fossil record: American Journal of Science, v. 293A, p. 407–417. Norell, M. A., and Novacek, M. J., 1992a, The fossil record and evolution: Comparing cladistic and paleontologic evidence for vertebrate history: Science, v. 255, p. 1690–1693.

604 Printed in U.S.A. GEOLOGY, July 1995