nization, 19841, pp. 221-234.128. C. V. Kidd and D. Pimentel, Eds., Integrated Re-

source Management: Agroforestry for Develop-ment (Academic Press, San Diego, 1992).

129. U.S. Bureau of the Census, Statistical Abstract ofthe United States 1990 (Government Printing Of-fice, Washington, DC, 1992).

130. L. Lave and E. Seskin, Air Pollution and HumanHealth (Johns Hopkins Press, Baltimore, MD,1977).

131. F. D. Whitaker and H. G. Heinemann, J. Soil WaterConserv. 28, 174 (1973).

132. W. C. Moldenhauer and M. Amemiya, Iowa FarmSci. 21, 3 (1967).

133. P. Faeth, R. Repetto, K. Kroll, Q. Dai, G. Helmers,Paying the Farm Bill: U.S. Agricultural Policy

and the Transition to Sustainable Agriculture(World Resources Institute, Washington, DC,1991).

134. K. C. McGregor and C. K. Mutchler, Trans. ASAE35, 1841 (1992).

135. R. F. Cullum, ibid., p. 1521.136. C. K. Mutchler, L. L. McDowell, J. D. Greer, ibid. 28,

160 (1985).137. L. C. Johnson and R. I. Papendick, Northwest Sci.

42, 53 (1968).138. K. C. McGregor, C. K. Mutchler, M. J. M. Romkens,

Trans. ASAE 33, 1551 (1990).139. F. H. Bormann, G. E. Likens, T. C. Siccama,

R. S. Pierce, J. S. Eaton, Ecol. Monogr. 44, 255(1974).

140. We thank the following people for reading an

earlier draft of this article, for their many help-ful suggestions, and in some cases, for pro-

viding additional information: I. P. Abrol, D.Wen, R. H. Dowdy, H. E. Dregne, W. Edwards,M. T. El-Ashry, H. A. Elwell, R. F. Follett, D. W.Fyrear, G. E. Hallsworth, H. Hurni, T. N. Khoshoo,R. Lal, G. W. Langdale, W. B. Magrath, K. C.McGregor, G. F. Mcisaac, F. Mumm von Mallinck-rodt, T. L. Napier, K. R. Olson, W. Parham, D.Southgate, B. A. Stewart, M. Stocking, M. S.Swaminathan, D. L. Tanaka, G. B. Thapa, F.Troeh, P. W. Unger, A. Young, R. Bryant, M. Gi-ampietro, T. Scott, and N. Uphoff. Special thanksgo to D. Dalthorp for his many constructive com-ments and his time and enthusiasm dedicated tothis study.

Prehistoric Extinctions of PacificIsland Birds: Biodiversity Meets

ZooarchaeologyDavid W. Steadman

On tropical Pacific islands, a human-caused "biodiversity crisis" began thousands ofyears ago and has nearly run its course. Bones identified from archaeological sites showthat most species of land birds and populations of seabirds on those islands were

exterminated by prehistoric human activities. The loss of birdlife in the tropical Pacific mayexceed 2000 species (a majority of which were species of flightless rails) and thusrepresents a 20 percent worldwide reduction in the number of species of birds. The currentglobal extinction crisis therefore has historic precedent.

species today (I 1). The differences are

mainly technological (snares versus guns

and stone adzes and fire versus chain saws

and fire, for example).On average, fewer species and numbers

of seabirds now nest on tropical or sub-tropical (0 to 350S latitude) than on tem-

perate or subantarctic (above 350S lati-tude) Pacific islands, with lower marineproductivity in the tropics generally citedas the reason for the difference (12).Without prehistoric human impact therewould be less difference. For example, thenumber of nesting species of seabirds hasdeclined on Ua Huka (Marquesas) frommore than 22 to 4 (13) and on Huahine(Society Islands) from more than 15 to 4(14). Today's global patterns of seabirddistribution are not natural.

Human activities are causing major chang-es in the Earth's biota (1). Extinction, theultimate change, is occurring today across a

broad range of terrestrial and aquatic habi-tats (2). Although much of this "biodiver-sity crisis" is due to human impact duringrecent centuries or decades, few plant andanimal communities were unaffected in pre-

industrial times (3). Nowhere is this seen

more dramatically than on islands in thePacific Ocean.

Nearly all islands in Melanesia, Micro-nesia, and Polynesia (Fig. 1) were inhab-ited by prehistoric peoples. Melanesia was

occupied as far east as the Solomon Islandsby 30,000 years before the present (B.P.)or earlier (4). Much later, about 3500years B.P., humans arrived in WestPolynesia and Micronesia, reaching virtu-ally all of Oceania by 1000 years B.P. (5).Native birds vanished as colonists clearedforests, cultivated crops, and raised domes-ticated animals (6). Having evolved in theabsence of mammalian predators, the birdsundoubtedly were tame and easy for peo-ple to hunt (7).

The loss of birds on oceanic islandsmay entail extinction (global loss of a

species), extirpation (loss of a species froman island or region, with one or more

populations surviving elsewhere), or re-

duced population. Extinction and extirpa-tion are long-term losses (8), not short-term departures of populations soon to bereestablished from elsewhere (9). All fam-ilies of Pacific island birds have been af-fected. Land birds have suffered high lev-els of both extinction and extirpation,especially among species of rails, pigeons,doves, parrots, and passerines. Althoughseabird colonies (especially of shearwatersand petrels) have vanished from numerous

islands, species of seabirds have undergonelittle extinction.

Island birds have been lost mainly to

predation by humans and nonnative mam-mals (rats, dogs, and pigs) and because ofthe removal or alteration of indigenousforests through cutting, burning, and in-troduction of nonnative plants. The soilerosion caused by deforestation has elimi-nated nest sites for burrowing seabirds.Although the rate of extinction variedwith ruggedness of terrain and size or per-manence of the prehistoric human popu-lation, we have no evidence that the pro-cesses responsible for prehistoric extinc-tions (10) differed fundamentally fromthose that continue to deplete surviving

SCIENCE * VOL. 267 * 24 FEBRUARY 1995

Remote Outposts: Hawai'i,New Zealand, and Easter Island

The highly endemic land bird faunas ofthe Hawaiian Islands and New Zealandevolved independently from those in thePolynesian heartland the island groups

from Tonga and Samoa to the MarquesasIslands that are the primary focus of thisarticle. The prehistoric record of birds isextensive and well studied in the Hawai-ian Islands (15, 16) and New Zealand(17). As elsewhere in Polynesia, both sea-

birds and land birds were lost, with theland birds sustaining much more species-level extinction.

The Hawaiian Islands are renowned forradiations of endemic drepanidine finchesand flightless ducks, geese, and ibises. Sincehuman arrival at about 1500 to 2000 yearsB.P. (18), 60 endemic species (representingat least 90 populations) of land birds knownonly from bones have become extinct (Table1). Another 20 to 25 species have been lostin the past two centuries. The large island ofHawai'i has the archipelago's richest modemavifauna, although more species are knownfrom O'ahu and Maui because of their richerfossil records.

Temperate New Zealand once featuredendemic radiations of moas, kiwis, water-

1123

The author is at the New York State Museum, 3140Cultural Education Center, Albany, NY 12230, USA.

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fowl, and xenicids. With prehistoric humansettlement, at least 44 endemic species ofland birds became extinct in the past millen-nium. In the well-studied Punakaiti karstarea on the South Island (19), bones revealthe loss of 20 species of land birds (8 moas, 3waterfowl, 2 rails, 1 shorebird, 1 parrot, 1owl, 1 owlet-nightjar, and 3 passerines). To-day, 23 native nonmarine species occupy theregion, with another 7 species known histor-ically but no longer extant. Thus, of the 50species of land birds that once inhabitedPunakaiki, 27 are gone.On isolated Easter Island (162 kiM2, ele-

vation 507 m), bones from the Ahu Naunauarchaeological site date from 900 to 650years B.P. (20). The Ahu Naunau faunadiffers from late prehistoric (less than 500years B.P.) assemblages from Easter Island(21) in that bones of marine mammals andnative birds are much more common,whereas those of fish, humans, and chickensare relatively rare. Although bones of ex-tinct or extirpated seabirds and land birdsoccur throughout the Ahu Naunau deposit,they are more common in the deepest stra-ta, a pattern seen at other East Polynesiansites (22). The indigenous avifauna of sub-tropical Easter Island once included at least25 species of seabirds, of which 8 to 10 nolonger breed on Easter Island and 13 to 16others no longer breed even on any of itsoffshore islets (Table 2). The entire prehis-toric seabird fauna of Easter Island probablyexceeded 30 breeding species, more thanare known from any other single Polynesianisland. Of these, only Phaethon rubricaudastill nests on Easter Island itself.

Ahu Naunau also provides the first evi-dence that indigenous land birds once lived

on Easter Island. Except for a rail (Porzanasp. nov.), the land bird bones found thus farare too fragmentary to identify as to genusbut do represent at least six species in fourfamilies.

Evidently Easter Island lost more of itsindigenous terrestrial biota than did anyother island of its size in Oceania. Beforehuman colonization at about 1500 yearsB.P., most of Easter Island was forested witha palm (Jubaea disperta) and the trees Soph-ora toromiro and Triumfetta sp. (23). Al-though depauperate by Polynesian stan-dards, the terrestrial vegetation sustained in-digenous insects, land snails, and land birds.Deforestation of Easter Island was virtuallycomplete by about 550 years B.P. (24).

The Polynesian Heartland

Outside of the Hawaiian Islands, New Zea-land, and Easter Island, the prehistoricrecord of Polynesian birds is based on bonesfrom Henderson Island (25), the MarquesasIslands (6, 13, 26, 27), the Society Islands(6, 14), the Cook Islands (6, 28, 29), Samoa(30), Tonga (8, 31 ), and Polynesian outliersin Melanesia (32). In West Polynesia, clos-er to the richer vertebrate faunas ofMelanesia, the prehistoric extinctions in-volved lizards and bats (33) as well as birds.

New biogeographic concepts aboutPolynesian land birds derived from prehis-toric bone samples include the following(8): (i) The ranges of most living species aremuch smaller today than they were at thetime of first human contact (Fig. 2). (ii)Few volant species are naturally endemic toonly one or two islands. (iii) Most specieshave become extinct in the past 3000 years.

Table 1. Number of endemic species of land birds recorded on the five largest Hawaiian islands. F, fossilrecord (Holocene only; includes archaeological sites); M, modern record (1 9th or 20th century). F and Mmay represent the same species on any island, which is why the combined total is less than total F plustotal M. Modified from (16).

Bird species and island Kaua'i O'ahu Moloka'i Maui Hawai'i

characteristics M F M F M F M F M F

BirdsIbises(3spp.) - - - - 1 - 2 - - -

Ducksand geese(10spp.) 4 1 4 1 3 1 4 1 3 1Rails (12 spp.) 2 1 3 1 1 1 3 1 3 2Stilts (1 sp.) - 1 1 1 - 1 - 1 - 1Hawks (3 spp.) - - 3 - 2 - 1 - - 1Owls (4 sp.) 1 - 1 - 1 - 1 - - -Crows (3 spp.) - - 2 - 1 - 1 - 1 1Monarchs (1 sp.) 1 1 1 1 - - - - 1 1Thrushes (4 sp.) 2 2 1 1 1 1 1 - 1 1Honeyeaters (7 sp.) 1 1 2 1 1 1 3 - 2 2Finches (51 spp.) 12 9 18 8 11 8 21 10 4 16Total 23 16 36 14 22 13 37 13 16 26Combined total 29 38 31 43 32

Island area (kM2) 1433 1574 676 1887 10,458Elevation (m) 1598 1232 1515 3056 4206Isolation (km to nearest 112 40 13 13 46

island larger than 300 kM2)

(iv) Most or all islands supported one tofour endemic species of flightless rails, vir-tually all now extinct. (v) In many cases,individual islands supported two or threespecies within a genus, unlike the situationtoday. (vi) At least four formerly wide-spread genera (Gallirallus, Porphyrio, Macro-pygia, and Myiagra) now are gone from EastPolynesia. (vii) Although modem distribu-tions of Polynesian land birds continue tobe analyzed as if they were natural (see 34),they do not furnish unbiased data for pro-posing or testing ecological models (6).(viii) Although some of the range losses ofextant species could be restored with con-servation efforts (35), we are centuries toolate to preserve any true likeness to theoriginal Polynesian avifauna.

The Hane archaeological site on UaHuka (78 km2, elevation 855 m), Marque-sas, has yielded the largest bird bone assem-blage from tropical Polynesia (6). Most ofthe approximately 11,000 bones representseven species of shearwaters and petrels,none of which still nests on Ua Huka. Landbirds have declined on Ua Huka from morethan 18 to 5 species, the losses including 2endemic rails, 5 pigeons and doves, and 3parrots. The early part of the Hane site maydate to about 2000 years B.P. (36) and rep-resent the first human settlement of UaHuka. Native birds provided more than halfof all vertebrate food in the early Marquesandiet, a contribution that declined to insig-nificance late in prehistory (22). From near-by Tahuata, bones with much better chro-nostratigraphic control represent at least 15species of seabirds and land birds that didnot survive beyond 700 years B.P. (27).

The Fa'ahia archaeological site on Hua-hine (77 kiM2, elevation 669 m), SocietyIslands, dates to about 1100 to 800 yearsB.P. (14). Fa'ahia shares 12 of its 15 speciesof seabirds with the Hane site but only 5 ofits 15 species of land birds. As at Hane, themost common land birds are rails, pigeons,doves, and parrots. Further sampling surelywould increase the number of species pre-historically attributed to Huahine, whereonly seven species (five of seabirds and twoof land birds) nest today. Thanks to theFa'ahia site, more resident species of birdsare known from Huahine than from themuch larger (1042 kmi2) nearby island ofTahiti, where no prehistoric bird boneshave been reported.

The exploitation of birds can be seenclearly at the Tangatatau Rockshelter (siteMAN-44), Mangaia (52 kmi2, elevation 169m) (29), Cook Islands. The MAN-44 siteranges in age from 1400 to 1000 years B.P.(culturally cryptic zones 1A to 1B) to 200years B.P. (protohistoric zone 17). Bones ofdomesticated animals (pigs, dogs, andchickens) are relatively rare in the loweststrata, increase as the number of native land

SCIENCE * VOL. 267 * 24 FEBRUARY 1995

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ISLANDS

MicronesiaMARSHAUL-ISLANDS

CAROLINE

ISLANDS.A

,,,..GILBERT

~~~~~ISLAN D)SNEN IE ND......

. * .........~ ~ ~ .......... .......

aGUINEA SOLOOND .-' * TOKELAU

BRITAIN ,a,,,s. *.TUVALU........

4WALLIS

.SAMOAVANUATU " '

FIJI d

Melanesia

'\NEW . .TONGA9--- f~CALEDONIA

140' 160° 180

iNPolynesia

LINEISLANDS

- MAROUESASISLANDS

'COOKISLANDS -

SOCIETY 'ISLANDS

TUBUAI

160'

..

* *.-TUAMOTU; *' ARCHIPELAGO

PITCAIRNGROUP

140- 120

Fig. 1. The tropical Pacific Ocean, showing major island groups.

bird bones decreases in higher strata, thendecrease again late in prehistory (zone 15),perhaps because of overconsumption by a

large human population.The number of bones from native birds is

high in zones 1 to 4 of MAN-44, relativelylow in the middle zones, and high again inzones 15 and 17 (Tables 3 and 4). Bones ofextinct or extirpated land birds dominatezones 1 to 4, whereas seabirds account forthe later increase in the number of birdbones. The longer survival of certain speciesof seabirds on Mangaia may be due to itsprecipitous, creviced limestone cliffs, whichprovided relatively rat-free nesting habitat.In spite of this, only two (the Brown Noddyand the Common Fairy Tern) of Mangaia'seight surviving species of seabirds have cur-

rent populations of more than 100 pairs.Bones of extinct or extirpated land birds

from MAN-44 are most numerous in zones 1to 4 (1400 to 700 years B.P.), decliningsharply in zone 5 (Tables 3 and 4). Of 17species of indigenous land birds, 10 are re-

corded in zones 5 to 7 (700 to 600 years B.P.)or higher, even if in reduced numbers. Themost common flightless rail, Porzana rua, lastoccurs in zone 8 (600 to 500 years B.P.). Theonly extinct or extirpated land birds abovezone 8 are two species of doves. Each of thefour surviving species of land birds fromMAN-44 tolerates some forest clearance.

Unlike other East Polynesian sites ofsimilar age, zones 1 to 4 of MAN-44 havenot yielded a single shearwater or petrelbone. Other evidence suggests that zones 1to 4 of MAN-44 postdate the earliest hu-man arrival on Mangaia. A major change inpollen and spore influx from more than 20sediment cores from swamps and lakesshows that, beginning about 2500 yearsB.P., forest tree pollen gave way to fernspores and herb pollen that are indicative of

human disturbance accompanying settle-ment. The first appearance of charcoal andincreased clay influx, with intensification ofthese signals at about 1600 years B.P. (37),accompanied the change in pollen andspores. Evidently human disturbance of thenative biota began 1000 years before theearliest known cultural deposits at MAN-44or other sites on Mangaia. Although extinc-tion of rails, pigeons, doves, parrots, and a

sandpiper is evident at MAN-44 (Table 3),

Nuku Hiva

2 Prehistoric

E0 Modern

MARQUESAS ISLANDS

-1os DuculagaleataNuku Hiva Pigeon

0 10 20 30 40 50 km

3 Ua Huka

Hiva Oa

Tahuata ;R

IN Fatt

14OW

other birds may have been lost during thefirst millennium of human influence. I

would speculate that they included severalspecies of shearwaters and petrels. Mangaiais not unique in disclosing the earliest evi-dence of human occupation by changes inland use revealed in sediment cores ratherthan by the presence of habitation sites.Similar records exist for Easter Island (24),Mo'orea (38), and non-Polynesian islandssuch as Madagascar and Puerto Rico (39).

Fig. 2. The past andpresent distribution ofthe Nuku Hiva Pigeon,Ducula galeata. Regard-ed as endemic to Nuku

Fatu Huku Hiva (4), Marquesas, thisspecies now has prehis-toric or historic records

`k from at least three otherMarquesan islands (5

Motane through 7), as well asMangaia (1), Huahine (2),and Tahiti (3). Before hu-

u Hivaman impact, it probablywas found through mostof East Polynesia.

SCIENCE * VOL. 267 * 24 FEBRUARY 1995

REVILLAGIGEDO

CLIPPERTON

0 500 1,000 km

SALA-Y.GOMEZ

EASTER

100-

6if MARQUESAS

- s-.. ISLANDS

2COOK /ISLANDS .. 2; TUAMOTU

\A SOiETY% 3 ISLANDS;~ISLND

AUSTRAL'ISLANDS PITCAIRN

ISLANDS

140'W

...X

1~~~ 5

I

... ............

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land birds lived on 'Eua in prehuman times(Table 5). Only six of these have survivedinto the past two centuries. Of the 13 in-digenous species of land birds recorded on

'Eua during the past two centuries, 6 are

known from prehuman strata, 3 probablyoccurred in prehuman times but have notbeen sampled, and 4 probably colonized'Eua after the arrival of humans.

The unusual tooth-billed pigeon (Didun-culus), regarded since its European discov-

Table 2. Resident native birds from Easter Island (270S). Prehistoric record categories: x, present;dashes, no record. Modern status categories: B, breeds today on Easter Island; b, breeds today on anoffshore islet or islets but not on Easter Island itself; E, extinct species; and e, extant species that isextirpated on Easter Island and all offshore islets.

ModernBirds Prehistoric Modern latitudinal

record status breedingrange ('S)

SeabirdsAlbatrossesDiomedea sp.

Petrels, shearwatersFulmarus glacialoidesPachyptila vittataPterodroma macroptera

or P. lessoniPterodroma ultimaPterodroma externaPterodroma heraldicaPterodroma neglectaProcellaria sp.Puffinus cameipesPuffinus nativitatisPuffinus griseusProcellariidae sp. nov.

Storm petrelsNesofregetta fuliginosa

Tropic birdsPhaethon rubricaudaPhaethon lepturus

Frigate birdsFregata minor

BoobiesSula dactylatra

TernsSterna fuscataSterna paradisaeaSterna lunataProcelsterna ceruleaAnous stolidusGygis candidaGygis microrhyncha

Total species

Combined total species

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

x

22

25

e

eee

eebbeebeE

e

Be

b/e

b

be?b/ebbbe

B = 1,b = 8to 10,

E = 1,e = 12 to 15

01 to 51

53 to 6836 to 6534 to 50

15 to 2724 to 3308 to 2720 to 3336 to 5031 to 4200 to 2732 to 50

1?

00 to 27

00 to 2700 to 24

00 to 27

00 to 27

00 to 27

00 to 2700 to 3300 to 3300 to 2708 to 10

Land birdsHerons

cf. Ardeidae sp. nov.RailsPorzana sp. nov.cf. Rallidae sp. nov.

Parrotscf. Psittacidae sp. nov. 1cf. Psittacidae sp. nov. 2

Owlscf. Tytonidae sp. nov.

Total species

x

x

x

x

x

x

6

E

E

E

E

E

E

E-=6

ery 150 years ago as endemic to Samoa,once lived on 'Eua, as did the megapodeMegapodius pritchardii, believed to be en-

demic to Niuafo'ou. 'Eua's 23 species ofextinct or extirpated land birds represent 14genera unknown in East Polynesia but liv-ing today in Melanesia or elsewhere inWest Polynesia or in both locations. Thenearest recorded conspecifics or closely re-

lated congeners are from the Solomon Is-lands (one species), New Caledonia (twospecies), Fiji or Samoa or both (nine spe-

cies), elsewhere in Tonga (eight species), or

unknown locations(three species). By elim-inating taxa such as Nycticorax sp. nov.,

Eclectus sp. nov., Eopsaltria sp., and Cettiasp., the anthropogenic extinction of birdson 'Eua has artificially magnified the bio-geographic distinction between Polynesianand Melanesian birds (8).

The impoverishment of 'Eua's land birdcommunity has obvious ecological implica-tions. Of more than 23 extinct or extirpatedspecies, 3 are larger than, and 5 smaller than,any surviving species. The prehuman landbird fauna had more than 27 forest speciesand lacked nonforest species, as comparedwith 9 forest and 4 nonforest species today.All feeding guilds have been depleted (Fig.4). When analyzed by foraging height, thelosses were acute for ground-dwelling species(7 to 0), reflecting predation from humans,rats, dogs, and pigs. The natural means ofpollination or seed dispersal for certainPolynesian forest trees probably has sufferedthrough the loss of so many frugivorous andnectarivorous birds (35) and pteropodid bats(40). As in the Neotropics (41), the future ofPolynesian forests is threatened because ofvertebrate extinctions.

Micronesia and Melanesia

To date, each sample of bird bones fromMicronesian or Melanesian islands is small(less than 1000 and often less than 100specimens). Nevertheless, in Micronesia,cave deposits on Rota (Mariana Islands)have yielded bones of 22 resident species ofbirds, of which 13 are no longer on theisland (1 shearwater, 1 tem, 1 duck, 1 mega-pode, 3 rails, 2 pigeons, 1 parrot, 1 swift, 1monarch flycatcher, and 1 parrot finch)(42). Currently under study are bones,mainly of flightless rails, from sites I exca-

vated on Tinian and Aguiguan (MarianaIslands) in June and July 1994. An archae-ological site on Fais (Yap, Caroline Islands)has yielded 18 resident species of birds, ofwhich 2 petrels, 2 boobies, 5 tems, 1 rail,and 2 pigeons are extirpated, whereas smallbone samples from Pohnpei record the lossof 4 species (1 shearwater, 2 petrels, and 1megapode (43). When it has been morefully studied, I expect that apart from detailsof taxonomy and chronology, the record of

SCIENCE * VOL. 267 * 24 FEBRUARY 1995

Caves on 'Eua (85 kmi2, elevation 300m), Tonga, (Fig. 3), differ from otherPolynesian heartland sites in yielding bonedeposits that predate human arrival by tensof thousands of years (8). The data reveallittle prehuman turnover in land birds on'Eua until the arrival of humans at about3000 years B.P. Climatic and sea-levelchanges at the end of the last glacial periodmay have had virtually no effect on the'Euan land bird fauna. At least 27 species of

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avian extinctions in Micronesia will resem-ble that of Polynesia.On average, the islands of Melanesia are

larger and sustain richer biotas than thoseof Polynesia or Micronesia. Species of landmammals were lost (some translocated) inprehistoric Melanesia (44). Although stud-ies of prehistoric birds are few, the fossilsdisclose the loss of land birds. New Cale-donia (16,750 km2, elevation 1639 m) fea-tures 36 species of nonpasserine land birds,many endemic. It is the only Melanesianisland with more than 1000 identified fossilbird bones (45). Of 16 extinct or extirpatedspecies of nonpasserine land birds from NewCaledonia, 11 are known only from bones.In the case of New Ireland (9974 km2,elevation 2399 m), which is close to NewGuinea, well forested, and has about 108species of resident land birds today, mypreliminary data from 200 bones indicatethe loss of at least 25% of its species sincehuman arrival, including two or more spe-cies of flightless rails.

Extent of Extinction

Combining seabirds and land birds, I esti-mate conservatively that an average of 10species or populations have been lost oneach of Oceania's approximately 800 majorislands (46), yielding a total loss of 8000species or populations. The seven islands inthe Polynesian heartland (Henderson, UaHuka, Tahuata, Hiva Oa, Huahine, Man-gaia, and 'Eua) with more than 300 identi-fied bones all approach or exceed 20 exter-minated species or populations, and none ofthese records is complete. 'Eua, for example,has lost at least 23 species of land birds and10 of seabirds. Although many of the 800major islands in Oceania are lower, smaller,and slightly more isolated than 'Eua, theseislands also have fewer surviving species,typically fewer than five of seabirds andfewer than five of land birds.

Rails have lost the most species to hu-man impact. Most extinct species of railswere flightless forest dwellers, endemic to asingle island, rather than volant wetland orgrassland species. Each of the 19 tropicalPacific islands with 50 or more land birdbones that are 500 or more years old hasyielded one to four endemic species of flight-less rails. Ua Huka, Mangaia, and 'Eua, withrelatively thorough fossil records, each havetwo to four endemic species. Two to threeextinct, endemic flightless species of rails areknown as well from four Hawaiian islands(16). The mere seven land bird bones fromEaster Island include those of two endemicspecies of rails (Table 2). Endemic species ofrails evolved even on small, low, flat islandslike Wake (Galliralus wakensis) and Laysan(Porzana palmeri) and survived there in theabsence of prehistoric colonizers. At one to

four endemic species per island, flightlessrails alone may account for 2000 species ofbirds that would be alive today had peoplenot colonized Oceania. Except for threebarely surviving species of Gallirallus (fromOkinawa, Guam, and the Solomon Islands)(47) and one living species of Porzana (onHenderson Island), only the bones remain asevidence of one of the most spectacular ex-amples of avian speciation.

Knowledge of the prehistory of Polyne-sian birds vastly improves our understand-ing of a group of organisms that had been

considered, prematurely, to be wellknown. With data only from living birds(48), one might not predict that threespecies of Vini parrots once inhabited in-dividual islands in the Marquesas, thatfive species of rails (including three spe-cies in the genus Porzana) coexisted onMangaia, or that six species of pigeons anddoves occupied a typical East Polynesianisland, where only zero to three (usually 0to 2) species per island are known inrecent centuries. In biogeographical anal-yses of Polynesian birds, as in other natu-

Table 3. Bones of birds from the main excavation block, Tangatatau Rockshelter (MAN-44), Mangaia,Cook Islands, expressed in NISP (number of identified specimens). Data are based on 1989 and 1991excavations. Daggers indicate extinct species, asterisks indicate extant species extirpated on Mangaia,and dashes indicate no bones.

ZoneBirds Total

1A 1B 2to3 4 5to7 8 9to 14 15 17

SeabirdsShearwaters, petrels

Puffinus Iherminien*Pterodroma nigripennis

Storm petrels*Nesofregetta fuliginosa

Tropic birdsPhaethon lepturusPhaethon rubricauda

Frigate birdsFregata arielFregata minor

Boobies*Sula sula

TernsAnous stolidusProcelsterna ceruleaGygis candida*Gygis microrhyncha

ChickensGallus gallus

DucksAnas superciliosa

RailstGallirallus ripleyiPorzana tabuensistPorzana ruatPorzana sp. nov.tPorphyrio? sp. nov.

SandpiperstProsobonia sp. nov.

Pigeons, doves*Gallicolumba

erythropteratGallicolumba sp. nov.tGallicolumba nui*Ptilinopus

rarotongensis*Ducula aurorae*Ducula galeata

Parrots*Vini kuhlkitVini vidivici*tVini kuhlii or V. vidivici

KingfishersHalcyon mangaia

WarblersAcrocephalus kerearako

-- - - -. 2 2 10- - - - - 19 23 47

- 1 - 2 3 - 1 1

4 2 19 12 2 - 1 1- 1 - - -

3 1711 100

- 8

- 411

- - - - - 5 - 2 - 7- - 1 - - 4 - - - 5

- - - 1 - - - - - 1

1 1 - - 1 5 3 3 1 15- - - 1 - - - - - 1

2 1 6 2 1 - - - - 12- 4 7 1 - - - - - 12

Introduced birds

- - 22 20 27Native land birds

- - 3 1 2

122

411

16

21

1 1

3 5

432

1 15 2

1

2

10 5

11 44- 2- 1

1 1

3 5

3 31 4

1 23 1

14 4142 142 2

1 2

6 6

16 12 1 2 100

2 8 11 3 30

446

12041

_ _ _ - - 4

_ _ _ _ - 16

- - 7 1 3 11_ _ _ - - 9

- - - 1 - 12

_ _ _ - - 5

- 1 - - - 12

15 23 1 - - - - 943 14 2 - - - - 75- 5 - - 9

2 2 - - - - 1 8

1 2 - - - - - 15

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ral sciences (49), models have overshad-owed data and thereby undermined theirpotential to be meaningful.

Much remains unknown about the bio-geography of South Pacific birds. For exam-ple, DNA might be extracted from well-preserved bones to complement anatomi-cally based taxonomies. We need more pre-historic bone assemblages from acrossOceania, especially Micronesia and Mela-nesia. Sites that represent the first few cen-turies of human occupation are crucial fordocumentation of pristine avifaunas. Noneof the bone records now in hand is com-plete; with each return to Mangaia, 'Eua, orany other island with suitable deposits, I findbones of species previously unknown fromthe island, species that lived there beforehuman intervention. The record of natural(background) extinction deserves greater ef-fort. Was climate change of little or noconsequence in driving species turnover?

Another challenge is to obtain more datafrom atolls and low-raised limestone islands.The largest bone samples in hand are fromhigh-raised limestone islands (Mangaia,Henderson, and 'Eua) or volcanic islands(Easter Island, Huahine, and various Mar-quesan and Hawaiian islands). I recentlyreceived about 400 bird bones from threearchaeological sites (50) on Lifuka and Foaislands (maximum elevation less than 20 m;most land less than 10 m in elevation) inTonga (Fig. 3). The samples include 12 to15 extirpated species of shearwaters, petrels,megapodes, rails, and pigeons. Thus, evenlow sandy islands, which today support alargely anthropogenic vegetation and an im-poverished avifauna, once sustained a di-verse fauna of seabirds and land birds.

Chronology and Cause ofPrehistoric Extinction

The prehistoric extinction of vertebrates onoceanic islands can be calibrated by the richHolocene fossil record of the GalapagosIslands (51 ). Unlike any entire island groupin Polynesia, the Galapagos Islands werenot inhabited by humans before their dis-covery by Europeans in 1535 A.D. Humanimpact, confined to the past 460 years, wasrelatively minor until about 1800 A.D.

About 500,000 Holocene bones of rep-tiles, birds, and mammals, more than 90%of which predate human arrival, have beencollected from lava tubes on five islands inthe Galapagos. They disclose a loss of only0 to 3 vertebrate populations in the 4000 to8000 years preceding human arrival, where-as 21 to 24 populations have been lost onthe same five islands in the few centuriessince the arrival of people (51). Thus, therate of background (prehuman) extinctionin the Galipagos was roughly two orders ofmagnitude less than the rate of human-

1128

Table 4. Summary of bird bones from the main excavation block, Tangatatau Rockshelter (MAN-44),Mangaia, Cook Islands. NISP, number of identified specimens. This table is based on data shown inTable 3.

Bones and Zonespeies andTotalspecies 1A 1B 2 to 3 4 5 to 7 8 9 to 14 15 17

Total NISPAll species 105 143 149 139 42 56 57 79 25 795Allnative species 105 143 127 119 15 40 45 78 23 695Seabirds 7 10 33 19 7 35 30 64 15 220Nativeland birds 98 133 94 100 8 5 15 14 8 475Extinct and extirpated 91 125 86 94 6 2 7 2 3 416

native land birdsPercent of NISP of extinctand extirpated nativeland birdsOf all birds and mammals 72 57 5 21 4 0.4 2 0.5 2 11Of all birds 87 87 58 68 14 4 12 2 12 53Of all native land birds 93 94 92 94 75 40 47 14 38 88

Total speciesAll 15 20 19 22 10 10 8 11 8 30All native 15 20 18 21 9 9 7 10 7 29Seabirds 3 6 4 6 4 5 5 6 3 12Native land birds 12 14 14 15 5 4 2 4 4 17Extinct and extirpated 10 12 10 1 1 4 2 1 2 1 13

native land birds

I N-18e

Kingdom of nga

Fonualei

' Toku

o 20 40 mileso 20 40 60 80 vs

HAAPAI GROUP

- 20

Falcon

, Uinvvur Vava'uHunga 7

Noapapu I KapaLate Ovaka Taunga

Mo'unga'oneKao . .Ha'ano

9 ..Foa

Tofua -: .A LifukaUiha ° Uoleva

NomukaMango- e Lalona

HungaHunga Ha'apai ' Tonga

..Euaiki

Tongatapu 'EuaKalau

176°

TONGATAPU GROUP

0

174

Fig. 3. The Kingdom ofTonga. Informative sites with bones of prehistoric birds are on the islands of 'Eua,Lifuka, and Foa.

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related extinction elsewhere. When undis-turbed by humans, the natural processes ofdispersal, colonization, and evolution mayresult in a very low rate of extinction forvertebrates on tropical oceanic islands.On continents, especially the Americas,

Australia, and northern Eurasia, humanhunting has been implicated in the latePleistocene extinction of mammoth andother large mammals (52). A debate hasfocused on human activity versus changingclimate and habitat as the primary or solecause of megafaunal extinctions, although a

blend of the two factors is plausible (53).Unlike the situation on continents, mostscientists readily accept that prehistoric hu-mans were involved in the loss of island

species, probably because we have seen somany extinctions on Pacific islands in re-cent centuries ( 1 1 ). Even though islands aresubject to natural disasters including

Table 5. Chronology and community ecology of indigenous resident land birds from 'Eua, Tonga.Chronologic and systematic data from (8). Prehuman record, more than 3000 yr B.P.; archaeologicalrecord, 3000 to 200 yr B.P.; historic record, 19th-century specimen. Daggers indicate extinct species;asterisks indicate extirpated species; x, present; dash, no records. Feeding guild categories are definedin Fig. 4.

Pre- Archaeo- His- Extant FedBirds human logical toric in Feeuldn

record record record 1988 g

A30

20-

l0 _

All speces

u-

0 10_

e.0

Ez

C

10-

5-

Foraging height a Aedo Cano* mid.

* Groa

Fig. 4. Long-term changes in theness of forest birds on 'Eua, KingdThe horizontal scale (chronology)to Table 5. (A) All species. (B) Dietarpreference. (C) Foraging height. Fcategories are as follows: Al, aeriaCF, canopy frugivore-granivore;nectarivore; CO, canopy omnivoreraptor; GF, ground frugivore-grEground omnivore; GP, ground pmidlevel-understory frugivore-gramidlevel-understory insectivore; Nspecies; and NR, nocturnal raptor.overlap between canopy and midlevhabitats; some species were assigto one or the other.

HeronsEgretta sacratNycticorax sp. nov.

DucksAnas superciliosa

Hawks*Accipiter cf. rufltorques

MegapodestMegapodius alimentum*Megapodius pritcharditMegapodius sp. nov.

RailstGallirallus sp. nov.Gallirallus philippensis*Porzana tabuensis

(CFRGFMF) tGallinula sp. nov.M (COGO) Porphyrio porphyriovm (Nv.MI) Pigeons and doves

abf (DR,GP.NR) *Gallicolumba stairtDidunculus sp. nov.Ptilinopus porphyraceusPtilinopus perousiltDucula davidtDucula sp. nov.Ducula pacifica

Parrots*Vini solitarius*Vini australis

i (N) tEclectus sp. nov.Wp (CF.CN.CO) Barn owls

(DRMF.MINR) Tyto a/band (GFGO.GP) Swifts

Collocalia spodiopygiaKngfishersHalcyon chloris

TrillersLalage maculosat*cf. Lalage sp.

gg Whistlers, robins% v t*Eopsaltria sp.T Monarchs0000,0 *Clytorhyncus vitiensis

*Myiagra sp.species rich- Warblersom of Tonga. t*Cettia sp.corresponds Thrushesry category or *Turdus poliocephalus:eeding guild Starlingsal insectivore; Aplonis tabuensisCN, canopy Honeyeaters, DR, diurnal *Myzomela cardinalisanivore; GO, Foulehaio carunculata)redator; MF, White-eyesanivore; Ml tZosteropidae sp. nov.F, Total speciesTrnonforest Total extinct andThere may be extirpated species

Je1-understory No. of sites /ined arbitrarily no. of bird bones

xx x

x

xxx

x

x

xxxxxx

xxx

x

x

x

x

x NF- GP

x NF

x

x

xx

x

xxxxxxx

xx

x

x

xx

x

DR

GFGFGF

GONFNFGONF

GFMFCFCFCFCFCF

CNCNCF

NR

Al

Ml

MlMl

Ml

MlMl

Ml

x

x

x

x

x

x x

x xx -

x

x

x

x

x

xx

x xx _

x

x

x

xx

x2721

1/401

x

x

xx

2614

14/888

x

143

- MF

x MF

- CNx CN

CO130

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drought, fire, and severe cyclonic storms, todate the fossil record has revealed no majorloss of species from natural causes.

Once people occupy an island, humanpredation, habitat loss, and introduced pred-ators, competitors, or pathogens appear to beresponsible for the extinctions of birds,whether modem or prehistoric (54). Findingthe bones of extinct species in a culturalcontext does not prove that people causedthe extinctions, even when evidence ofbutchery, cooking, or consumption ispresent. Such bones do indicate human pre-dation on the extinct species which, basedon modem analogy, probably was a factorleading toward extinction. Direct evidencefor prehistoric habitat changes comes notfrom the bones themselves but from paleo-botanical and geological studies (24, 37, 38).

The rate of extinction for island birdsneed not be a matter of two or three cen-turies only, as proposed for North Americanmammals (52). On Mangaia, the ruggedmakatea limestone that covers 56% of theisland provided a forested refuge that al-lowed many species of birds to survive formore than 1000 years after human arrival.The forest disturbance portrayed in theMangaian sediment cores reflects mainlywhat occurred on the inner volcanic hills,not on the makatea, where exploitation ofplants and birds intensified only after thevolcanic hills had been deforested. Eventoday, the most inhospitable areas of Man-gaia's makatea sustain a predominately na-tive forest (55). During the initial period ofMangaian prehistory, from about 2500 to1600 years B.P., there may have been littleor no permanent settlement. Mangaia mayhave been an occasional outpost for fisher-men who ate birds and fruit bats and setfires in the dry season. Probably no nonna-tive mammals were introduced. From about1600 to 1000 years B.P., Mangaia may havebeen visited more frequently, with settle-ments made along the coast. Rats were in-troduced. Fires increased and some forestwas cleared for agriculture. Settlement ex-panded to the island's interior at around1000 years B.P., resulting in further defor-estation and in the occupation of sites suchas MAN-44.We expect extinction after people arrive

on an island. Survival is the exception. Thetime required, whether 102 or 103 years, fora species to become extinct is of interestecologically as well as from a cultural (22)or conservational (56) perspective. For timethat exceeds the 50,000-year range of radio-carbon, these differences are lost within theinherent imprecision of dating methods.

Chronology aside, the loss of Pacific is-land birds is part of a global anthropogenicextinction event in which certain speciesmay be targeted (41) although no majorgroups of organisms are immune (2). Cur-

1130

tailing this event has been and will bedifficult (57). For thousands of years wehave devastated naive faunas and havefound it difficult to manage scarce resourcesin a sustainable way. It appears that theEarth's biota, already much depleted be-cause of human activity, will continue todecline in the foreseeable future.

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2. E. 0. Wilson, The Diversity of Life (Norton, New York,1992); N. Myers, Biodivers. Conserv. 2, 2 (1993).

3. J. M. Diamond, The Third Chimpanzee (Harper-Col-lins, New York, 1992); S. L. O'Hara, F. A. Street-Perrott, T. P. Burt, Nature 362, 48 (1993); W. De-nevan, Assoc. Am. Geogr. Ann. 82, 369 (1992).

4. S. Wickler and M. Spriggs, Antiquity 62, 703 (1988).5. G. Irwin, The Prehistoric Exploration and Coloniza-

tion of the Pacific (Cambridge Univ. Press, Cam-bridge, 1992). The chronology of archaeologicalsites is determined most often by radiocarbon datingof wood charcoal, marine shell, bone, and other or-ganic materials.

6. D. W. Steadman, J. Archaeol. Sci. 16,177 (1989).Bones from paleontological and archaeologicalsites on 40 Pacific islands provide estimates ofprehistoric avifaunas and of the magnitude of ex-tinction. No bone assemblage represents all spe-cies that once lived on a given island. The relationbetween the fossil sample and the actual avifaunais influenced by the number of identified bones, theagent that deposited the bones (humans, otherpredators, or natural trap activity, for example), ageof the bone sample (by late prehistoric times, mostspecies of birds were already gone), and methodsof sampling (screen sizes popular before the pastdecade were too coarse to recover bones of smallspecies).

7. At the time of European contact, such tameness wasnoted on a number of uninhabited oceanic islands.Darwin's finches and other resident land birds onmost of the Galapagos Islands are still remarkablytame.

8. D. W. Steadman, Proc. Natl. Acad. Sci. U.S.A. 90,818 (1993).

9. M. J. Williamson, Philos. Trans. R. Soc. London Ser.B 325, 457 (1989).

10. P. V. Kirch, Archaeol. Oceania 18, 26 (1983).11. N. J. Collar and P. Andrew, Int. Counc. Bird Preserv.

Tech. Publ. 8 (1988); T. H. Johnson and A. J. Stat-tersfield, Ibis 132,167 (1990); D. A. Burney, Am. Sci81, 530 (1993); P. Craig, T. E. Morrell, K. Sooto,Pac. Sci. 48, 344 (1994).

12. R. C. Murphy, Oceanic Birds ofSouthAmerica (Mac-millan, New York, 1936), vol. 1, pp. 59-81; C. J. R.Robertson and B. D. Bell, Int. Counc. Bird Preserv.Tech. Publ. 2, 573 (1984).

13. D. W. Steadman, in Global Climate Change and Lifeon Earth, R. L. Wyman, Ed. (Routledge, Chapmanand Hall, New York, 1991), p. 156.

14. D. W. Steadman and D. S. Pahlavan, Geoarchaeol-ogy 7, 449 (1992).

15. S. L. Olson and H. F. James, Science 217, 633(1982); H. F. James et al., Proc. Natl. Acad. Sci.U.S.A. 84, 2350 (1987).

16. S. L. Olson and H. F. James, Ornith. Monogr. 45(1991); H. F. James and S. L. Olson, ibid. 46 (1991).

17. T. H. Worthy, Nat. Mus. N. Z. Misc. Ser. 17 (1988); A.Anderson, Prodigious Birds: Moas and Moa-huntingin Prehistoric New Zealand (Cambridge Univ. Press,Cambridge, 1989); R. N. Holdaway, N.Z. J. Ecol. 12(suppl.), 11 (1989); A. Anderson and R. McGovern-Wilson, N.Z. Arch. Assoc. Monogr. 18 (1991).

18. P. V. Kirch, Feathered Gods and Fishhooks (Univ. ofHawaii Press, Honolulu, 1985).

19. T. H. Worthy and R. N. Holdaway, J. R. Soc. N.Z. 23,147 (1993).

20. D. W. Steadman, P. Vargas, C. Cristino, Asian Per-spect. 16, 79 (1994).

21. W. S. Ayres, J. Soc. Oceanistes 80,103 (1985).

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23. P. Bahn and J. R. Flenley, Easter Island, Earth Island(Thames and Hudson, London, 1992).

24. J. R. Flenley et al., J. Quat. Sci. 6, 85 (1991).25. D. W. Steadman and S. L. Olson, Proc. Natl. Acad.

Sci. U.S.A. 82,6191 (1985); S. E. Schubel and D. W.Steadman, Atoll Res. Bull. 325 (1989), p. 1; G.Wragg and M. I. Weisler, Notomis 41, 61 (1994).

26. D. W. Steadman and M. C. Zarriello, Proc. Biol. Soc.Wash. 100, 518 (1987); D. W. Steadman, S. E.Schubel, D. S. Pahlavan, ibid. 101, 487 (1988); Nat.Hist. Mus. Los Angeles Cty. Sci. Ser. 36, 329 (1992).

27. B. V. Rolett, J. Polynesian Soc. 101, 86 (1992); D. W.Steadman and B. V. Rolett, J. Archaeol. Sci., inpress.

28. D. W. Steadman, Pac. Sci. 40, 27 (1987); M. S. Allenand D. W. Steadman, Archaeol. Oceania 25, 24(1990); D. W. Steadman, Pac. Sci. 45, 325 (1991).

29. D. W. Steadman and P. V. Kirch, Proc. NatI. Acad.Sci. U.S.A. 87,9605 (1990); P. V. Kirch, J. R. Flenley,D. W. Steadman, F. Lamont, S. Dawson, Nat.Geogr. Res. Explor. 8,166 (1992); P. V. Kirch, D. W.Steadman, V. Butler, J. Hather, M. I. Weisler, Ar-chaeol. Oceania, in press. The numbering system forMangaia's more than 100 archaeological sites in-cludes the prefix MAN to distinguish these from siteselsewhere in the Cook Islands. The TangatatauRockshelter is the 44th site in this system.

30. D. W. Steadman, Univ. Calif. Archaeol. Res. Fac.Contrib. 51, 217 (1993).

31. Proc. Biol. Soc. Wash. 102, 537 (1989).32. J.-C. Balouet and S. L. Olson, ibid. 100, 769 (1987);

D. W. Steadman, D. S. Pahlavan, P. V. Kirch, Occas.Pap. Bemice P. Bishop Mus. 30,118 (1990).

33. G. K. Pregill, Pac. Sci. 47,101 (1993); K. F. Koop-man and D. W. Steadman, Am. Mus. Nov., in press.

34. G. H. Adler, Evol. Ecol. 6, 296 (1992).35. J. Franklin and D. W. Steadman, Conserv. Biol. 5,

506 (1991).36. P. V. Kirch, J. Polynesian Soc. 95, 9 (1986).37. J. C. Ellison, Pac. Sci. 48,1 (1994); P. V. Kirch and J.

Ellison, Antiquity 68, 310 (1994).38. D. Lepofsky, H. C. Harries, M. Kellum, J. Polynesian

Soc. 101, 299 (1992).39. D. A. Bumey, Quat. Res. 40,98 (1993); L. P.

Bumey, R. D. E. MacPhee, J. Archaeol. Sci. 21, 273(1994).

40. W. E. Rainey and E. D. Pierson, U.S. Fish Wildi. Serv.Biol. Rep. 90,111 (1992).

41. K. H. Redford, Bioscience 42, 412 (1992); M. S.Alvard, Hum. Ecol. 21, 355 (1993).

42. D. W. Steadman, Micronesica 25, 71 (1992).43. __ and M. Intoh, Pac. Sci. 48,116 (1994).44. T. F. Flannery and J. P. White, Nat. Geogr. Res.

Explor. 7, 96 (1991).45. F. Hannecart and Y. Letocart, Oiseaux de Nouvelle

Caiddonie et des Loyautbs (Les Editions Cardinalis,Noumba, New Caledonia, 1980, 1983), vols. 1 and2; J.-C. Balouet and S. L. Olson, Smithson. Contrib.Zool. 469 (1989).

46. There are about 260 islands and atolls in Polynesia,120 in Micronesia, and 430 in Melanesia. G. Dou-glas, Micronesica 5, 327 (1969); L. S. Motteler, Bish-op Mus. Misc. Publ. 34 (1986); B. G. Karolle, Atlas ofMicronesia (Bess Press, Honolulu, HI, 1993).

47. J. M. Diamond, Auk 108, 461 (1991).48. E. Mayr, Birds of the Southwest Pacific (Macmillan,

New York, 1945); R. H. MacArthur and E. 0. Wilson,The Theory of Island Biogeography (Pnnceton Univ.Press, Princeton, NJ, 1967); E. Mayr, Evolution andthe Diversity of Life: Selected Essays (Harvard Univ.Press, Cambridge, MA, 1976).

49. N. Oreskes, K. Shrader-Frechette, K. Belitz, Science263, 641 (1994).

50. W. R. Dickinson, D. V. Buriey, R. Shutler Jr., Geoar-chaeol. 9, 85 (1994).

51. D. W. Steadman, Smithson. Contrib. Zool. 413(1986); T. W. Stafford Jr., D. J. Donahue, A.J. T. Jull, Quat. Res. 36,126 (1991).

52. P. S. Martin, in Quaternary Extinctions, P. S. Martinand R. G. Klein, Eds. (Univ. of Arizona Press, Tuc-son, AZ, 1984), p. 354; P. 5. Martin, Palaeogeogr.Palaeoclimatol. Palaeoecol. 82, 187 (1990).

53. P. S. Martin and R. G. Klein, Eds., QuaternaryExtinc-tions (Univ. of Arizona Press, Tucson, AZ, 1984); A.

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J. Stuart, Biol. Rev. 66, 453 (1991).54. J. M. Diamond, Int. Counc. Bird Preserv. Tech. Publ.

3, 17 (1985); D. W. Steadman, E. C. Greiner, C. S.Wood, Conserv. Biol. 4, 398 (1990).

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757 (1988); M. P. Moulton, L. J. Justice,

57.

58.

Philos. Trans. R. Soc. London Ser. 344, 27 (1994).D. Ludwig, R. Hilbom, C. Walters, Science 260,17(1993).Supported by the National Geographic Society(grants 2088 and 4001-89), NSF (grants BSR-8607535 and BNS-9020750), the Smithsonian Insti-tution, the U.S. Fish and Wildlife Service, and the

University of Califomia, Berkeley. For research per-mits and other cooperation, thank governmentagencies in French Polynesia, the Cook Islands,Tonga, Chile, Ecuador, and the Northern MananaIslands. W. L. Fink, J. Harte, H. F. James, P. V. Kirch,E. D. Pierson, S. L. Pimm, and W. E. Rainey com-mented on the manuscript.

* RESEARCH ARTICLE

Head-On Collision Between a DNAReplication Apparatus and RNA

Polymerase Transcription ComplexBin Liu and Bruce M. Alberts*

An in vitro system reconstituted from purified proteins has been used to examine whathappens when the DNA replication apparatus of bacteriophage T4 collides with anEscherichia coli RNA polymerase ternary transcription complex that is poised to move inthe direction opposite to that of the moving replication fork. In the absence of a DNAhelicase, the replication fork stalls for many minutes after its encounter with the RNApolymerase. However, when the T4 gene 41 DNA helicase is present, the replication forkpasses the RNA polymerase after a pause of a few seconds. This brief pause is longerthan the pause observed for a codirectional collision between the same two polymerases,suggesting that there is an inherent disadvantage to having replication and transcriptiondirections oriented head to head. As for a codirectional collision, the RNA polymeraseremains competent to resume faithful RNA chain elongation after the DNA replication forkpasses; most strikingly, the RNA polymerase has switched from its original templatestrand to use the newly synthesized daughter DNA strand as the template.

The Escherichia coli genome is arranged in acurious way, inasmuch as most of the heavi-ly transcribed genes are oriented in thedirection of the leading strand of the DNAreplication fork (1, 2). A similar nonran-dom gene organization is found in otherbacteria (3), plasmids, and bacteriophages(1). These observations suggest that a codi-rectional collision between RNA and DNApolymerases is less disadvantageous to anorganism than an oppositely oriented(head-on) collision.

Using a highly purified in vitro system,we previously examined the consequencesof a collision between a DNA replicationfork and codirectionally moving RNA poly-merase (4, 5). We found that the replica-tion fork can pass the RNA polymeraseternary complex even in the absence of aDNA helicase; surprisingly, the bypassedRNA polymerase ternary complex re-mained bound at its original place on the

The authors are in the Department of Biochemistry andBiophysics, University of California, San Francisco, CA94143-0448, USA.

*On leave as president of the National Academy of Sci-ences, Washington, DC 20418, USA.

DNA template, and it was fully competentto resume RNA chain elongation.We have now examined the conse-

quences of an oppositely oriented collisionbetween a replication fork and an RNApolymerase ternary transcription complex.We found that the replication fork stalls fora long time during such a head-on collisionwith RNA polymerase when no DNA he-licase was present. However, when theDNA helicase was added, the replicationfork passed the RNA polymerase after a

brief pause. We have investigated the con-

sequences of this bypass reaction and foundthat the RNA polymerase switched its tem-plate strand, requiring that its RNA-DNAhelix break up and re-form with a new

DNA partner.A head-on collision between a replica-

tion fork and RNA polymerase. A singlynicked circular DNA molecule containingan appropriately oriented E. coli ur70 pro-

moter was used as a DNA template thatsupports oppositely directed DNA replica-tion and DNA transcription (in this mole-cule, the nick that primes leading-strandDNA synthesis is located in the DNA

SCIENCE * VOL. 267 * 24 FEBRUARY 1995

strand that serves both as the template fortranscription and as the template for lag-ging-strand DNA synthesis). We began ourreaction by adding purified E. coli RNApolymerase and ribonucleoside triphos-phates (NTPs) to this DNA; because weomitted cytidine triphosphate (CTP), theRNA polymerase began synthesis at thepromoter but stopped at the first G nucle-otide on the template. This created a stableternary transcription complex composed ofRNA polymerase, an 1 8-nucleotide (nt)nascent RNA transcript, and the DNAtemplate (6). After purifying this ternarycomplex on Sepharose CI-2B to remove afew other, less stable ternary complexes andany RNA polymerase molecules bound toDNA without a transcript (4), we added theproteins and nucleotides required to startDNA synthesis. Because the or factor andNTPs were removed by the treatment withSepharose Cl-2B, new RNA chains couldnot be initiated during the DNA replica-tion reaction (4).

For DNA synthesis, we used an in vitroreplication system composed of seven high-ly purified bacteriophage T4-encoded pro-teins that catalyze efficient leading-strandDNA synthesis. The proteins were the T4DNA polymerase holoenzyme (consistingof the products of T4 genes 43, 44, 62, and45), a helix-destabilizing single-strandedDNA-binding protein (gene 32 protein),the highly processive DNA helicase (gene41 protein), and the gene 59 protein thatgreatly facilitates the loading of the gene 41protein onto DNA at a replication fork (7).An eighth protein, the gene 61 protein(DNA primase), interacts with the gene 41protein to form the primosome that makesprimers for lagging-strand (Okazaki frag-ment) DNA synthesis; in some experi-ments, this protein was added to completethe T4 replication apparatus that catalyzescoupled leading- and lagging-strand DNAsynthesis at a rate comparable to that ob-served in vivo (7).

Using alkaline agarose gel electrophore-sis (8), we determined the effect of stalledRNA polymerase ternary complexes on themovement of oppositely oriented replica-tion forks by analyzing the rate of increasein DNA strand lengths during replication.We used either naked DNA or purifiedternary complexes as the DNA template inside-by-side reactions. In the absence of thegene 41 DNA helicase, the replication fork

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