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tures, ~200 µm in diameter, surrounding acentral blood vessel. Compact bone, solid tothe naked eye, is modified in places to formtrabecular bone, which consists of manystruts; the spaces between the struts arefilled with marrow (see the f igure, rightpanel). These struts are not randomlyarranged, but are related to the direction ofloads on the bone. The mechanical andother properties of bone depend on theinteraction of all levels of organization (4).

Two more examples of the structural hier-archy of biominerals are the teeth of seaurchins and the “crossed-lamellar” structureof many mollusk shells. The crossed-lamel-lar structure consists almost entirely of cal-cium carbonate in the crystalline form ofaragonite, with a tiny amount of organicmaterial between the crystals. It has five lev-els of organization, and the structures arearranged with high precision to prevent thetraveling of cracks (5, 6). Sea urchin teethhave fewer levels of hierarchy, but their struc-ture is very similar to that of fiber-reinforcedplastics. However, they consist of a compos-ite in which fibers and matrix are chemicallyidentical, being made of calcite, although the

crystals differ greatly in size and orientation,with a layer of organic material surroundingthe fibers (7). Furthermore, the magnesiumcontent of the calcite increases toward themiddle of the tooth, markedly increasing itshardness. The resulting differential wear pro-duces a self-sharpened tooth.

The main mechanical function of thesehierarchical arrangements, almost certainly,is to produce interfaces that will open up inthe presence of potentially dangerous cracks,deflecting the cracks and making their travelenergetically expensive. This makes biomin-eralized skeletons surprisingly tough, giventhat they are made almost entirely of mineral.Bone is a special case, having less mineralthan most other biomineralized skeletons; itcan be remarkably tough.

Apart from their hierarchical arrangement,two other features of biominerals contribute tothe superior mechanical properties of skele-tons made from them. First, at the lowest level,they are often made of tiny crystals that aresmaller than the “Griffith length” necessaryfor cracks to spread (8). Second, the precisionwith which they can be laid down (changingtheir main orientation over a few micrometers,

for instance) allows exquisite adaptations tothe loads falling on the skeletons.

The particular mineral used in a skeleton—calcite, aragonite, apatite, silica, or others—isprobably much less important than the preciseway in which the mineral is arranged in space.Aizenberg et al. show this very clearly for theEuplectella skeleton, although the organiccomponent is also crucial for providing clearinterfaces between the layers.

References and Notes1. J. Aizenberg et al., Science 309, 275 (2005).2. This paragraph reflects the author’s view of the levels

of hierarchy in Euplectella; the levels do not quiteagree with those specified in (1).

3. V. S. Deshpande, M. F. Ashby, N. A. Fleck, Acta Mater. 49,1035 (2001).

4. J.-Y. Rho, L. Kuhn-Spearing, P. Zioupas, Med. Eng. Phys.20, 92 (1998).

5. J. D. Currey,A. J. Kohn, J. Mat. Sci. 11, 1615 (1976).6. S. Kamat, H. Kessler, R. Ballarini, M. Nassirou, A. H.

Heuer, Acta Mater. 52, 2395 (2004).7. R. Z. Wang L. Addadi, S. Weiner, Philos. Trans. R. Soc.

London. B 352, 469 (1997).8. H. J. Gao, B. Ji, L. Jäeger, E. Arzt, P. Fratzl., Proc. Natl.

Acad. Sci. U.S.A. 100, 5597 (2003).9. C. R. Jacobs, M. E. Levenston, G. S. Beaupré, G. C. Simo,

D. R. Carter, J. Biomech. 28, 449 (1995).

10.1126/science.1113954

Rising greenhouse gas concentrationsin the atmosphere are trapping moreinfrared radiation near Earth’s sur-

face. This extra radiation is expected towarm Earth’s surface and lower atmos-phere, but observations indicate that mostof the heat is transported into the oceans(see the figure). On page 284 of this issue,Barnett et al. (1) substantially strengthenthe evidence that human activities areindeed warming the world’s oceans.

Observations have shown that 84% of thetotal heating of the Earth system since the1950s is in the oceans (2). This increasedocean heat content has led to thermal expan-sion of the ocean, contributing at least 25%of the global sea-level rise observed over thesame period (3). Ocean warming may alsolead to greater stratification of the ocean,causing a weakening of the global overturn-ing circulation in most model projections offuture climates (4). Furthermore, the oceansare a key element in the global carbon cycleand are estimated to be storing roughly half

of the total carbon released through humanactivities since preindustrial times (5). Forall these reasons, the oceans are an importantplace to look for changes expected due togreenhouse warming (“fingerprints”).

Many of the changes observed at Earth’ssurface and in the free atmosphere in the 20thcentury can be reproduced by climate modelsthat account for the increase in greenhousegases, aerosols associated with pollution,changes in solar radiation, and reflection byvolcanic aerosols (6, 7). Fingerprint methodsuse detailed information about the climateresponse to these external influences in orderto separate them from each other and fromnatural variability within the climate system.

O C E A N S C I E N C E

Warming the World’s OceansGabriele C. Hegerl and Nathaniel L. Bindoff

G. C . Hegerl is in the Nicholas School of theEnvironment and Earth Sciences, Duke University,Durham, NC 27708, USA. E-mail: hegerl@duke.edu N.L. Bindoff is at IASOS and CSIRO Marine Research,Unversity of Tasmania, Private Bag 80, Hobart 7001,Australia. E-mail: n.bindoff@utas.edu.au

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Heat transfer from atmosphere to ocean. This cross section of the Atlantic Ocean basin illustrateshow atmospheric warming is transferred from the ocean surface to the ocean interior. The isolinesshow potential (that is, pressure-adjusted) temperature. The vertical black arrows show broadlywhere heat penetrates into the ocean surface layer and is then subducted into the upper ocean alongsurfaces of equal density. The combination of winds, sinking processes, and ocean circulation alsoleads to the meridional overturning circulation (and horizontal heat transport) (white arrows). Arrowspointing out of the ocean indicate net heat being transported from the oceans to the atmosphere.(Inset) Location of the cross section. [Adapted from (9)]

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Studies using such methods have shown withhigh confidence that much of the temperaturechange observed at Earth’s surface and in thefree atmosphere over the past 50 years hasbeen caused by increases in greenhouse gasconcentrations (6, 7).

Barnett et al. (1) now apply a fingerprintmethod to the temperature history of theupper 700 m of each ocean basin since 1960.In this depth range, the greatest temperaturechanges are found (1, 2); it is also where wehave the best knowledge of ocean behavior.The authors compare the best available oceanobservation data set to simulations using twodifferent climate models. They find strongevidence that the anthropogenic fingerprintanticipated by the models is present in theobservations. The results show that changesin solar radiation and volcanic forcing cannotexplain the observed pattern of oceanchanges. The fact that the findings are robustfor two different climate models indicatesthat the results are not affected significantlyby differences in model formulation.

The similar pattern of temperaturechange in the observations and in the simu-lations is strong evidence for a large-scaleanthropogenic warming trend in theworld’s oceans. Barnett et al. thus addimportant information to the growing evi-dence that human-induced changes to thecomposition of the atmosphere are chang-ing our climate (7).

Temperature changes in the oceans areimportant not only because they strengthen theevidence for anthropogenic climate change.They are also important for a reliable predic-tion of future warming at the Earth’s surface.Climate feedbacks determine how strongly theatmosphere reacts to rising greenhouse gasconcentrations. But the rate of warming at theEarth’s surface also depends on how much ofthe excess energy trapped by greenhouse gasesis transported into the ocean interior.

For example, if climate feedbacks areweak and little heat penetrates into the ocean,this would in the short term result in a surfaceclimate change similar to one in which cli-mate feedbacks are strong and a lot of heatpenetrates into the ocean (8). However, asthe ocean slowly comes into equilibriumwith the atmosphere, these scenarios woulddiverge sharply, because stronger feedbackswould cause much stronger future warming.Therefore, the demonstration by Barnett etal. (1) that their two climate simulations arein quantitative agreement with the observedocean warming improves our confidence inthe simulated rate of ocean heat uptake andthus in projections of future climate.

The historical ocean data cover a rela-tively short time span (~50 years) and theirspatial coverage is inhomogeneous, particu-larly in the less accessible Arctic andSouthern Oceans. Therefore, it is still a chal-

lenge to validate more complex details ofocean physics in climate models than wasdone in (1). Further work is needed to deter-mine more accurately and in more spatialdetail how temperature and surface salinitychanges penetrate into the ocean. We alsoneed to better understand the ocean’s majormodes of climate variability, particularly ontime scales of a decade or longer, and toquantify the likelihood of sudden oceanchange [such as a collapse of the thermoha-line circulation (4)]. Another question is howocean biogeochemistry and ecosystems, andthus the global carbon cycle, will respond toglobal warming. Therefore, it is importantthat we keep probing the world’s oceans.

References and Notes

1. T. P. Barnett et al., Science 309, 284 (2005); publishedonline 2 June 2005 (10.1126/science.1112418).

2. S. Levitus, J. I. Antonov, T. P. Boyer, Geophys. Res. Lett.32, L02604 (2005).

3. J. I. Antonov, S. Levitus, T. P. Boyer, Geophys. Res. Lett.32, L12602 (2005).

4. U. Cubasch et al . , in Climate Change 2001 : TheScientific Basis. Contribution of Working Group I to theThird Assessment Report of the IntergovernmentalPanel on Climate Change, J. T. Houghton et al., Eds.(Cambridge Univ. Press, New York, 2001), pp. 525–582.

5. C. L. Sabine et al., Science 305, 367 (2004).6. J. F. B. Mitchell et al., in Climate Change 2001: The

Scientific Basis. Contribution of Working Group I to theThird Assessment Report of the IntergovernmentalPanel on Climate Change, J. T. Houghton et al., Eds.(Cambridge Univ. Press, New York, 2001), pp. 695–738.

7. The International Ad Hoc Detection and AttributionGroup, J. Climate 18, 1291 (2005).

8. C. E. Forest et al., Science 295, 113 (2002).9. R. Schlitzer, eWoce–Electronic Atlas of WOCE

Hydrographic and Tracer Data, www.ewoce.org (2003).10. G.C.H. is supported by the NSF, NOAA, and the DOE’s

Office of Biological and Environmental Research. N.L.B.is supported by the Australian Government’sCooperative Research Programme through the AntarcticClimate and Ecosystems Cooperative Research Centre(ACE CRC).

10.1126/science.1114456

What was the impact of earlyhuman populations on pristineecosystems? Studies of this

question have focused on the possibilitythat humans caused extinctions of largemammals. For example, the arrival of mod-ern humans in the Americas ~11,000 yearsago coincided with the disappearance ofmammoths, ground sloths, and many otherlarge mammals (1). However, the role ofhumans is diff icult to determine in thiscase because the climate was also changingrapidly as the last ice age came to an end;climate change, not human impact, mayhave caused the extinctions.

Modern humans reached Australiamuch earlier. Just when they did is stilldebated, but occupation was widespread by45,000 years ago and may have begun sev-eral thousand years earlier (2)—well beforethe climatic upheavals at the end of the lastglacial cycle. Australia should thereforeprovide a clear view of the ecologicalimpacts of human arrival. But environmen-tal changes following human arrival inAustralia have been diff icult to resolve,because very few precisely dated environ-mental records extend through the middleof the last glacial cycle. On page 287 of this

issue, Miller et al. (3) provide such a recordbased on diet reconstructions of the conti-nent’s two largest bird species. The resultsindicate that human arrival resulted in aprofound environmental shift.

Miller et al. studied past diets of the emu(Dromaius novaehollandiae) and an evenlarger flightless herbivorous bird, the extinctGenyornis newtoni (see the first figure), inthe arid and semi-arid regions of the southAustralian interior. By analyzing carbonisotopes in individually dated eggshells,they were able to compare the contributionsof plants that use the C4 photosyntheticpathway (mainly tropical and arid-adaptedgrasses) and those that use the C3 pathway(most shrubs, trees, and nongrass herbs) tothe diet of the birds that laid the eggs. Theircollection of eggshells covers the past140,000 years, encompassing the whole ofthe last glacial cycle.

Miller et al. found a sudden change inemu diet between 50,000 and 45,000 yearsago. Before 50,000 years ago, emus hadvariable diets, with a strong contributionfrom C4 plants; after 45,000 years ago, theyate mostly C3 plants. Genyornis eggshellswere common before 50,000 years ago, butthey abruptly disappeared at the same timeas the diet of the emu changed. Before then,Genyornis also ate a mixture of C3 and C4plants, but its diet was much less variablethan that of the emu through the same

The author is in the School of Tropical Biology, JamesCook University, Townsville, Queensland 4811,Australia. E-mail: christopher.johnson@jcu.edu.au

A N T H R O P O L O G Y

The Remaking of

Australia’s EcologyChristopher N. Johnson

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