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S C I E N C E ’ S C O M PA S S
Measuring Past Biodiversity Jeremy B. C. Jackson and Kenneth G. Johnson
he diversity of animal life on Earth the Cenozoic (65 Ma to today) (2), then increased from near zero at the be- the total might be only 200,000 genera. The five major mass extinctions probaginning of the Cambrian [~540 million years ago (Ma)] to the 4 to 6 million bly decrease these numbers by no more species alive today (1). What was the tra- than 10% (11), whereas earlier peaks in dijectory of this increase? And can we mea- versity above recent values might increase the totals by an unknown amount (3). Resure it empirically with the fossil record? gardless, it is sobering Most attempts to an4 to note that the largest swer these questions available database of have been based on Phanerozoic diversity shell-forming marine 3 contains little more than macroinvertebrates, the MA * 31,000 genera of maanimals with the most 2 rine macroinvertebrates extensive and well-pre(11), just 3 to 16% of served fossil record 1 PPP (2–4). About 300,000 * the total based on the calculations above. living species of marine 0 C O S D Ca P Tr J K T macroinvertebrates have 500 400 300 200 100 0 Global Compilations been described, but estiMillions of years ago (Ma) The database in quesmates that account for inadequate sampling Global number of marine invertebrate tion is the result of the range from ~0.5 to 5 genera during the Phanerozoic. Adapted almost superhuman efmillion (5). Only one- from (34). C, Cambrian; O, Ordovician; S, fort of the late Jack third contain hard parts Silurian; D, Devonian; Ca, Carboniferous; P, Sepkoski, who comPermian; Tr, Triassic; J, Jurassic; K, Cretapiled the stratigraphic likely to be preserved as ceous; T, Tertiary. The lower horizontal line fossils (6). Furthermore, indicates the number of genera of scler- ranges of more than fossil species are often actinian corals, cheilostome and cy- 31,000 genera in ~4000 unnamed. Most compi- clostome bryozoans, shelled mollusks, families of macroinverlations are therefore crustaceans, and echinoderms recovered tebrates from the literabased on genera or fam- from 344 Pliocene samples by the PPP. ture (4). The first and ilies to increase taxo- On the basis of the ratio of extant diver- last reported occurnomic consistency (4). sity between the Indo-West Pacific and rence of each taxon, Assuming 1 million liv- the Caribbean, we would expect to dis- anywhere in the world, ing species and less cover about 2205 genera of these groups was assigned to one of than f ive species per in a project similar in scope in the Malay 81 stratigraphic intervals of ~5 to 7 million genus on average (7–9), Archipelago (MA, upper horizontal line). years duration. The reabout 67,000 genera of living marine macroinvertebrates would be sulting plots of Phanerozoic marine family and generic biodiversity (see the first figure) preserved as fossils. How many such genera have ever were widely seen as the first rigorous assesslived? Fossil marine invertebrate genera ment of the history of the diversity of life. Sepkoski’s paleobiodiversity curves led survive on average about 28 million years (10). If the increase in diversity during the to many important paleontological adPhanerozoic (~540 Ma to today) was lo- vances, including the realization that mass gistic, with a maximum of about 67,000 extinctions are important creative factors genera as today (3), then the total number in the history of life (12) and the critical of fossilizable marine macroinvertebrate reevaluation of evolutionary trends (13). genera that ever lived would be about 1 Potential biases in the compilation, arising million. If Phanerozoic diversity increased for example from variations in geographic exponentially, with most of the increase in extent, outcrop area, volume, preservation of rocks, and sampling locations (mostly North America and Western Europe), were J.B.C . Jackson is at the Scripps Institution of Oceanography, University of California, San Diego, La also evaluated widely (3). Jolla, CA 92093, USA, and the Smithsonian Tropical These biases cannot actually be evaluatResearch Institute, Box 2072, Balboa, Republic of ed, however, because the data are not based Panama. E-mail: [email protected] K. G. Johnson is at the on ecological sampling. Standard statistical Natural History Museum of Los Angeles County, 900 evaluation is thus inappropriate. The situaExhibition Boulevard, Los Angeles, CA 90007, USA.
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tion is analogous to a human census based on attempts to count every citizen instead of estimating population numbers from samples that can be evaluated statistically (14). The problem with total counts is particularly vexing if we lack confidence in some census takers, who may have got lost trying to find certain neighborhoods, were afraid to enter them, or ran out of time. Such problems turn up easily on a standardized data sheet of samples but not in a final total number. Similar problems affect existing compilations of paleobiodiversity. We do not know how many places were sampled and how many samples were obtained from each age interval, nor do we know their quality and geographic distribution. The Phanerozoic Marine Diversity Working Group (11) has begun to address these problems by recompiling the data based on individual collections that can be treated as samples. This ambitious and important project will allow statistical analysis based on randomized subsampling of the data. Nevertheless, there is still extreme variability in the size and quality of collections in the database and in the taxa and stratigraphic intervals that are included, the sampling intervals are coarse, and the paleobiogeographic sampling of the data is extremely limited. These problems cannot be addressed effectively without new data. The Panama Paleontology Project Our own sampling of one small corner of the world has produced a surprisingly large proportion of the supposed global biodiversity for one of the stratigraphic intervals in the Sepkoski analysis. The Panama Paleontology Project (PPP) aimed to examine the consequences of the rise of the Isthmus of Panama and global climate change on the composition and diversity of tropical American marine biota over the past 15 million years (15–17). Occurrences of macrofaunal invertebrates from about half of the Caribbean PPP macrofossil collections were summarized recently for scleractinian corals (8), cheilostome bryozoans (9), and bivalve and gastropod mollusks (17, 18). We found 673 genera of these four groups in 344 collections of Pliocene age (5.3 to 1.7 Ma) (19) and more than 735 Pliocene genera of invertebrate macrofossils overall (20). The latest version of the Sepkoski database contains 4138 Pliocene genera of marine macroinvertebrates worldwide (21). As for all time intervals, this number includes an indeterminate but large number of taxa that range through but do not actually occur in Pliocene collections. Despite the fact that such taxa are not included in our data, our 344 Pliocene collections of macrofossils produced about 18% of the to-
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P E R S P E C T I V E S : PA L E O E C O L O G Y
Thousands of genera
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The Problem of Uneven Sampling Why are the global data so obviously incomplete for the Pliocene? The answer is so simple that it is commonly overlooked in studies of biases in the fossil record, which emphasize factors like outcrop area, taxonomic effort, and the poor preservation of fossils in older rocks (3, 6, 23). There are pitifully few modern, extensive monographic studies of tropical Cenozoic (much less Pliocene) corals, cheilostome bryozoans, bivalves, or gastropods because Europe and North America (the sources of almost all collections in the global database) had largely moved out of the tropics by Cenozoic time (24). Yet the tropics contain the great majority of marine biodiversity today, and as far as we know, this was true throughout the Phanerozoic (24). Estimates without tropical data are doomed to underestimate global diversity severalfold. Contrary to suggestions that diversity was constant throughout the Phanerozoic (3, 11), we conclude that Cenozoic diversity was much higher than Sepkoski observed and more in line with an exponential increase (2, 25). The lack of tropical data also explains why so little is known about the diversification of Cenozoic reef corals in the Pacific (26) and why no one has been able to rigorously test Vermeij’s (27) ideas about evolution and escalation of antipredator morphologies in the Indo-Pacific. How many other periods in the Phanerozoic are as badly sampled as the Cenozoic? The Phanerozoic Marine Diversity Working Group will identify well and poorly sampled intervals, geographic regions, and taxa. Some intervals may be well sampled, such as the tropical shallow seas of the Ordovician and Silurian of the North American Midwest and Europe (28). Moreover, the once controversial impact hypothesis to explain the mass
sides developing new paleontological collections with standard protocols, the projects would require varying amounts of new mapping, stratigraphy, age dating, and reconstruction of paleoenvironments, depending on the information already available. Such an integrated approach is essential to ensure the reliability and utility of the newly collected data. Each study would provide only a few sampling points toward answering the question of how paleobiodiversity evolved through time. But each study would also represent an extraordinary opportunity to gain other new paleontological insights. In the course of the PPP, we discovered that molluscan diversity in the Caribbean was roughly constant over the past 10 million years because mass extinction at the end of the Pliocene was counterbalanced by comparable origination in mollusks (17), although not in reef corals (8, 17), and that the pace of bryozoan speciation was highly punctuated throughout the region (31). The proposed program would also revitalize the education and training of taxonomists, stratigraphers, and field geoloWe Need New Data Ever more complete and detailed compila- gists. Few experts worldwide study many major fossil taxa, taxtions of old data collectonomists and biostratied for different purpos4.5 graphers are retiring, es, by different methods, Shannon’s H and there is a widely with different taxonomic 4.0 600 acknowledged crisis in standards, and without training their replaceabundance data cannot 3.5 400 ments (32). In addition, resolve the problem of many new Ph.D. paleinadequate and inconsis3.0 Number ontologists have done tent sampling. Existing 200 of genera 2.5 little fieldwork because museum collections sufof an increased emphafer from the same sam0 sis on working from the pling problems (18), de75 25 0 50 published literature. spite their great value for Thousands of specimens systematics. We propose Cumulative diversity curves for Our proposal would reinstead an international Pliocene molluscan genera from the quire new taxonomy program of detailed and PPP project. The curves show how diver- and f ieldwork on a intensive sampling of sity estimates change as more samples large scale and could critical intervals and re- are added. Each curve represents the me- support the training of a gions designed to ad- dian of 100 iterations with random input new generation of pracdress fundamental ques- of collections. Shannon’s H is a measure titioners of these endantions in Earth history, of ecological diversity that incorporates gered professions. Bemuch like the highly suc- both the number and proportional abun- cause of the need for geographic replication, cessful Ocean Drilling dance of taxa in an assemblage. the program would have Program. To find out whether marine biodiversi- to be truly international and may thus help ty increased during the Phanerozoic (11), to break down the barriers in stratigraphic we need about 20 studies comparable in practice and taxonomy that still confound scope to the Panama Paleontology Project, global compilations. No science can grow without new data. scattered judiciously in time and location. Depending on location and logistics, each The Ocean Drilling Program and polar ice study would cost roughly $3 to 5 million. cores have revolutionized our understanding At 5 to 10 years per project, done simulta- of Earth’s climatic history. In this regard, paneously, we could have the answer in 10 leontology is at a critical juncture. We have years at a cost of $10 million per year—a achieved great synthesis on the basis of Sepbargain compared with the costs of ongo- koski’s work and the studies it spawned, but our data are inadequate for testing whether ing surveys of living marine biodiversity. In each project, a team of geologists, strati- diversity has been stable or increased subgraphers, and paleontologists would study stantially over the past 500 million years and many groups of fossils at the same time. Be- for identifying the underlying processes. extinction at the end of the Cretaceous stimulated an enormous collection effort, as have attempts to understand the greatest mass extinction of all at the end of the Permian (29). But recent studies in China show (30) that we have barely scratched the surface of Phanerozoic biodiversity for many critical regions and time intervals in Earth history. These new data may allow us to evaluate how well each stratigraphic interval or biogeographic province has been sampled—if paleontologists standardize their collection methods to keep track of individual samples and specimen abundances. Only then will we be able to compare sampling efforts using plots of cumulative taxonomic richness and diversity (17, 18). The results in the second figure suggest that good estimates of diversity can be obtained with a practical amount of effort. However, comparable analyses have not been widely applied elsewhere and could probably not be generally attempted because of inappropriately collected data.
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Shannon’s H
tal Pliocene diversity in the global database (see the first figure) (19). Yet the area of Pliocene deposition in Panama and Costa Rica is less than 0.1% of the 7 million km2 of Pliocene marine sediments worldwide (22). The comparison is even more striking for specific, well-studied taxa. We found 31% of the number of scleractinian coral genera in the global database, 29% of the number of cheilostomes, 22% of the number of bivalves, and 22% of the number of gastropods. We also compared the PPP data with the Phanerozoic Working Group compilation, which considers diversity within 10-Ma intervals (11). The duration of each interval is similar to the time covered by the entire PPP database. The latter includes 847 genera of scleractinian corals, cheilostomes, bivalves, and gastropods from 689 collections (19). Only one of the intervals from the new global database contains as many genera (11).
Number of genera
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S C I E N C E ’ S C O M PA S S Extensive efforts are under way to document the earliest animals in the fossil record (33) and test alternative hypotheses about the big mass extinctions (29). We must extend these efforts in an organized fashion throughout Earth history if we are to make genuine progress in refining the hypotheses about Phanerozoic paleobiodiversity that Sepkoski laid out for us so brilliantly. References and Notes 1. R. M. May, Philos. Trans. R. Soc. London Ser. B 330, 171 (1990). 2. J. W. Valentine, J. Paleontol. 44, 410 (1970). 3. D. M. Raup, Paleobiology 2, 289 (1976). 4. J. J. Sepkoski Jr., Paleobiology 19, 43 (1993). 5. R. M. May, Philos. Trans. R. Soc. London Ser. B 343, 105 (1994). 6. A. K. Behrensmeyer, S. M. Kidwell, R. A. Gastaldo, Paleobiology 26 (suppl.), 103 (2000). 7. K. Roy, D. Jablonski, J. W. Valentine, Philos. Trans. R. Soc. London Ser. B 351, 1605 (1996).
8. A. F. Budd, T. A. Stemann, K. G. Johnson, J. Paleontol. 68, 951 (1994). 9. A. H. Cheetham, J. B. C. Jackson, J. Sanner, Y. Ventocilla, Bull. Am. Paleontol. 357, 159 (1999). 10. D. M. Raup, Paleobiology 17, 37 (1991). 11. J. Alroy et al., Proc. Natl. Acad. Sci. U.S.A. 98, 6261 (2001). 12. D. M. Raup, Proc. Natl. Acad. Sci. U.S.A. 91, 6758 (1994). 13. M. Foote, Evolution 50, 1 (1996). 14. D. Kestenbaum, Science 279, 798 (1998). 15. J. B. C. Jackson, A. F. Budd, A. G. Coates, Eds., Evolution and Environment in Tropical America (Univ. of Chicago Press, Chicago, IL, 1996). 16. L. S. Collins, A. G. Coates, Eds., Bull. Am. Paleontol. 357, 1 (1999). 17. J. B. C. Jackson, K. G. Johnson, Paleobiology 26 (suppl.), 221 (2000). 18. J. B. C. Jackson, J. A. Todd, H. Fortunato, P. Jung, Bull. Am. Paleontol. 357, 193 (1999). 19. See the supplementary material at www.sciencemag.org/cgi/content/full/293/5539/2401/DC1. 20. Based on estimates of numbers of genera of cyclostome bryozoans, brachiopods, serpulids, scaphopods, crustaceans, and echinoderms from work in progress on PPP collections. 21. M. Foote, personal communication.
22. V. Y. Khain, A. B. Ronov, A. N. Balukhovskiy, Int. Geol. Rev. 23, 426 (1981). 23. A. B. Smith, Philos. Trans. R. Soc. London Ser. B 356, 351 (2000). 24. P. A. Allison, D. E. G. Briggs, Geology 21, 65 (1993). 25. J. W. Valentine, Science 180, 1078 (1973). 26. M. E. J. Wilson, B. R. Rosen, in Biogeography and Geological Evolution of Southeast Asia, R. Hall, J. D. Holloway, Eds. (Bachuys, Leiden, Netherlands, 1998), pp. 165–195. 27. G. Vermeij, Evolution and Escalation (Princeton Univ. Press, Princeton, NJ, 1987). 28. J. M. Adrain, S. R. Westrop, B. D. E. Chatterton, L. Ramsköld, Paleobiology 26, 625 (2000). 29. Y. G. Jin et al., Science 289, 432 (2000). 30. E. Stokstad, Science 291, 232 (2001). 31. J. B. C. Jackson, A. H. Cheetham, Paleobiology 20, 407 (1994). 32. E. Pennisi, Science 289, 2306 (2000). 33. S. C. Morris, The Crucible of Creation: The Burgess Shale and the Rise of Animals (Oxford Univ. Press, Oxford, 1998). 34. M. Newman, Proc. Natl. Acad. Sci. U.S.A. 98, 5955 (2001). 35. We thank M. Foote for providing data from the Sepkoski database and K. Roy and M. Kirby for helpful discussions and criticism of the manuscript.
PERSPECTIVES: CELL BIOLOGY
Life Without Caveolae Robert G. Parton
iscovered by electron microscopists in the 1950s, caveolae—small surface pits in the plasma membrane— remain one of the most abundant yet puzzling features of many mammalian cells. The principal components of caveolae are proteins called caveolins. If caveolin-1, the isoform found in nonmuscle cells, is produced by cells normally lacking caveolae, then caveolae are formed (1); if cells that normally produce caveolin-1 become deficient in this protein they lose their caveolae (2). On page 2449 of this issue, Drab et al. (3) provide a thorough characterization of mice deficient in caveolin-1 that apparently have no caveolae. An electron microscopist scanning the surface of a fat cell (adipocyte) that is covered in caveolae could hardly imagine life without these structures. Yet we do not know exactly what they do or how their characteristic shape is related to their cellular tasks (see the figure). It has been proposed that caveolae are important in signal transduction, forming a platform on which different signaling components can congregate (4, 5). In some cases, signaling components in the caveolae may remain inactive, held in check by caveolins until their activation and release by the appropriate external stimulus. The number of caveolae and amount of caveolin decrease dramatically in immortalized (transformed) cultured cells,
D
The author is at the Institute for Molecular Bioscience, Centre for Microscopy and Microanalysis, and School of Biomedical Sciences, University of Queensland, Queensland 4072, Australia. E-mail: [email protected]
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hinting that caveolae are important for inhibiting certain signaling pathways that regulate cellular proliferation (4). However, it is becoming increasingly apparent that surface microdomains termed “lipid rafts,” of which caveolae are a subtype, could account for local concentrations of molecules required for efficient signaling (6). In fact, few signaling proteins are exclusively localized to caveolae, although notable exceptions include several putative calcium regulatory proteins (7). Also,
certain cells with very complex signaling pathways such as lymphocytes and some neurons manage fine without caveolae. Even if these cells have proteins that can take the place of caveolins, they do not seem to need caveolae per se for signaling. Besides signaling, caveolae have been linked to cholesterol regulation: Caveolin binds to cholesterol, its production is controlled by cholesterol, and cells with mutations in caveolin exhibit pertubations in their cholesterol-rich lipid-raft domains (2). Again, although definitive evidence is lacking, these studies suggest that caveolae and caveolins may be involved in the regulation of intracellular and surface cholesterol. Given the variety of possible tasks at-
Proposed functions
Caveolin-deficient mice
• Endothelial transcytosis • Signaling Ras, EGF, trimeric G proteins, PDGF, NOS, PLD, Raf, Mek, insulin Tumor suppression Calcium transport/regulation • Lipid regulation Cholesterol transport/regulation
• Lack of caveolae • Cardiovascular defects Aberrant arterial relaxation, contractility, myogenic tone • Nitric oxide abnormalities • Lung pathology and physical weakness
Caveolin-1,2,3
Caveolae and caveolins. (Left) An electron micrograph of small (65 nm) flask-shaped pits called caveolae in the plasma membrane of a human fibroblast. (Right) Caveolae are formed from caveolins, oligomeric integral membrane proteins. Caveolins are thought to have both their carboxyl and amino termini facing the cytoplasm and have palmitoyl groups (red squiggles) attached to carboxyl-terminus amino acids.
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