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by: Daren Beatty Jr.
Daren Beatty Jr.
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This 9 page Class Notes was uploaded by Daren Beatty Jr. on Thursday October 22, 2015. The Class Notes belongs to ME 158 at University of California Santa Barbara taught by Staff in Fall. Since its upload, it has received 40 views. For similar materials see /class/227091/me-158-university-of-california-santa-barbara in Mechanical Engineering at University of California Santa Barbara.

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Date Created: 10/22/15
ECOLOGY THROUGH TIME Historical Overfishing and the Recent Collapse of Coastal Ecosystems Jeremy B C Jackson1392 Michael X Kirby3 Wolfgang H Berger1 Karen A Bjorndal4 Louis W Botsford5 Bruce J Bourque6 Roger H Bradbury7 Richard Cooke2 Jon Erlandson8 James A Estes Terence P Hughes Susan Kidwell11 Carina B Lange1 Hunter S Lenihan12 John M Pandolfi13 Charles H Peterson12 Robert S Steneck14 Mia J Tegner1T Robert R Warner15 Ecological extinction caused by overfishing precedes all other pervasive human disturbance to coastal ecosystems including pollution degrada tion of water quality and anthropogenic climate change Historical abun dances of large consumer species were fantastically large in comparison with recent observations Paleoecological archaeological and historical data show that time lags of decades to centuries occurred between the onset of overfishing and consequent changes in ecological communities because unfished species of similar trophic level assumed the ecological roles of overfished species until they too were overfished or died of epidemic diseases related to overcrowding Retrospective data not only help to clarify underlying causes and rates of ecological change but they also demonstrate achievable goals for restoration and management of coastal ecosystems that could not even be contemplated based on the limited perspective of recent observations alone Few modern ecological studies take into ac count the former na a abundances of large marine vertebrates There are dozens of places in the Caribbean named a er large sea turtles whose adult populations now number in the tens of thousands rather than the tens of mil lions of a few centuries ago I 2 Whales Scripps Institution of Oceanography University of California San Diego La Jolla CA 9209370244 USA 2Center for Tropical Paleoecology and Archeology Smithsonian Tropical Research Institute Box 2072 Balboa Republic of Panama 3National Center for Ecological Analysis and Synthesis 735 State Street Suite 300 Santa Barbara CA 93101 USA AAr ie Carr Center for Sea Turtle Research and Department of Zoology University of Florida Gainesville FL 32611 USA 5Department of Wildlife Fish and Con servation Biology University of Cali ornia Davis CA tengill Hall Bates College Lewiston ME 04240 USA entre or Resource and Environmental Studies Aus tralian National University Canberra ACT 0200 Aus tralia BDepartment of Anthropology University of Oregon Eugene OR 97403 USA US Geological Survey A316 Eart 39 University of California Santa Cruz CA 95064 USA mCenter for Coral Reef Biodiversity De artment of Marine Biology James Cook University Townsville D 4811 Aus ralia Department of Geophysical Sciences University of Chicago 5734 South Ellis Av enue Chicago IL 60637 USA 12Institute of Marine Sciences University of Nort Carolina at Chapel Hill 3431 Arendell Street Morehead City NC 28557 USA 13Department of Paleobiology National Museum of Natural Histony Smithsonian Institution Washington DC 2056070121 USA MSchool of Marine Sciences University of Maine Darling Marine Center Orono ME 04573 USA 15Department of Ecology Evolution Barbara CA 93106 USA To whom correspondence should be addressed E mailjbcjucsde u iDeceased manatees dugongs sea cows monk seals croc odiles codfish jewfish swordfish sharks and rays are other lar e marine vertebrates that are now functionally or entirely extinct in most coastal ecosystems 3710 Place names for oysters earls and conches conjure up other navigation 1 but are witnessed now only by massive garbage heaps of empty shells S osts represent a far more profound problem for ecological understanding and management than currently realized Evi dence from retrospective records strongly suggests that major s c al and functional changes due to overfishing I 2 occurred worldwide in coastal marine ecosystems over many centuries Severe overfishing drives species to ecological extinction because over fished populations no longer interact signifi can y wi other species in the community 5 Overfishing and ecological extinction predate an precondition modern ecological investigations and the collapse of marine eco systems in recent times raising the possibil ity that many m e marine ecosystems ma be vulnerable to collapse in the near e Importance of Historical Data historical perspective I 8 13 Such observa tions fail to encompass the lifespans of many ecologically impormnt species I 3 I 4 and crit ical y 39 portant environmenml disturbances such as extreme cyclones or ENSO El Nifioi Southern Oscillation events 8 as well as longer term cycles or shi s in oceanographic regimes and productivity 15717 To help ad dress this pro em we describe ecosystem using welldated time series based on biological 18 I9 biogeochemical 20 21 physical 22 and historical 23 proxies that are infor ma 39ve over a variety of spatial scales and bio geographic realms 24 Although proxies vary in precision and clarity of the signals they mea sure the use of multiple proxies that give the same ecological signal greatly increases confi dence in results Precision in age dating varies from centuries to a single year season or event in the exceptional case of varved sediments ice cores and written historical records 25 Pre cision decreases with the amount of biologica or physical disturbance to the sediment ana lyzed 26 We exploited data from many disciplines that span the period over which anthropogen ing marine ecosystems since they first learned how to fish our time periods need to begin well before the human occupation or European colonization of a coastal region Broadly our data fall into four categories and time perio s l Paleoecological records from marine sediments from about 125000 years ago to the present coinciding with the rise of mod ern H mm sapiens 2 Archaeological records from human coastal settlements occupied a er about 10000 years before the present yr BP when worldwide sea level approached present levels These document human ex ploitation of coastal resources for food and materials by past populations that range from smallscale aboriginal societies to towns cit ies and em ires 3 Historical records from documents 39ournals and charts from the 15th century to the present that document the p Time Periods Geography and Analysis We recognize three different but overlapping periods of human im act on mar39 tems aboriginal colonial and global Ab original use refers to subsistence exploitation of nearshore coastal ecosys ems y h cultures with relatively simple watercra and extractive technologies that varied widely in Ina 39tude and geographic extent Colonial use comprises systematic exploitation and de pletion of coastal and shelf seas by foreign ECOLOGY THROUGH TIME mercantile powers incorporating distant re sources into a developing market economy Global use involves more intense and geo graphically pervasive exploitation of coastal h ocean39c h 39 s e an eries integrae into global patterns of resource consumption with more frequent exhaustion and substitution of fisheries In Africa Europe and Asia these cultural stages are strongly confounded in time and space so t their differential sig nificance is dif th to establish However in BEFORE FISHING AFI39ER FISHING Kelp Forests AluknCalllornla Gull al Malne Gulf of Milne Klller whulac Klller whole P Pl 7 5 Sheer Soc 5 yard or head Lmlnk c alters n I 7 Lowe Lo 7 l Sea Abel is s Ar 7 sst cm ones quotTIquot 9 Abalones urchin P Kelp Kip Coral Reefs D a Croeodllac Fig 1 Simplified coastal food webs showing changes in m e important topdown so e of th interactions due to overfishing before left side and after right side fishing A and B Kelp forests u forAlaska and southern California left box an reefs and seagrass mea ows E nd F if of Maine rrght box C and D Tropicalcoral b emperate estuaries The re resentation of food we 5 a ter fishing is necessarily more arbitrary than those before fishing because of rapidly changing recent events 0 r example sea urchins are once again rare in the Cu 0 Marne as they were before the overfishing of cod due to the recent fishing of sea urchins that has also permrtted the recovery of elp Bold font represents abundant normal font represents rare crossedoutquot represents extinct Thick arrows represent strong interactions thin arrows represent weak interactions 27 jULY 2001 the Americas New Zealand and Australia the different stages are well separated in time stages as well as between human impacts and natural changes due to changing climate The addition of a deep historical dimen sion to analyze and interpret ecological prob the apparent precision and anayt prized by ecologists I 13 I4 Paleoeco logical archaeological and historical data were collected for man ses vary wide ly in methods of collection and qua 39ty and are less amenable to many types of statistical analysis than wellcontrolled experiments But none of these problems outweighs the benefits of a historical approach Clearly we cannot generate realistic null hypotheses about the composition and dynamics of eco 0 most certamly chan and natural environmental factors 8 I6 27 28 Here we brie y review longterm hu systems that point to new strategies for mit igation and restoration that are unlikely to emerge from modern monitoring programs Kelp Forests Kelp forests characterize shallow rocky hab it emperate to subarctic re gions worldwide and provide complex envi ronments for man ommercially important fishes and invertebrates 29 No em Hemi s and deforestation due to population explosions of herbivores following the re moval of apex predators by fishing Fig l A and B Phase shi s between forested and deforested states the latter lmown as sea urc 39 us result from intense grazing due to increased abundance and altered for aging pattems of sea urchins made possible in uman removal of their predators and competitors 7 8 30732 he kelp forest ecosystem of the Northern Paci c arose during the last 20 million years w39 the evolution of kelps strongylocent rotid sea urchins sea otters and the extinct Steller s sea cow 6 Sea cows were widely distributed across the northern Pacific Rim ou e Late Pleistocene They may have been eliminated from most of their range by aboriginal hunting at the end of the Pleisto cene and in the early Holocene because they survived thousands of years longer in the western Aleutian Islands that were not peo pled until about 4000 yr BP 6 Bythe time of European contact in 1741 sea cows per VOL 293 SCIENCE wwwsciencemagorg sisted only in the Commander Islands the only islands of the Aleutians unoccupied by aboriginal people European fur traders killed the last sea cow 27 years later in 1768 We have no idea to what extent abundant sea cows grazed kelp forests although their ap parent inability to dive deeply probably lim ited their grazing to the surface canopy of kelps and to seaweeds lining the shore 6 Northern Pacific kelp forests presum ably ourished before human settlement because predation by sea otters on sea ur chins prevented the urchins from overgraz ing kelp 30 Aboriginal Aleuts greatly diminished sea otters beginning around 2500 yr BP with a concomitant increase in the size of sea urchins 31 Fur traders subsequently hunted otters to the brink of extinction in the 1800s with the attendant collapse of kelp forests grazed away by sea urchins released from sea otter predation Legal protection of sea otters in the 20th century partially reversed this scenario However kelp forests are again being de pleted in areas of Alaska because of in creased predation on sea otters by killer whales 33 The whales shifted their diet to sea otters from seals and sea lions which are in drastic decline A similar sequence of events occurred in kelp forests of the Gulf of Maine 7 34 Sea otters were never present but Atlantic cod and other large ground fish are voracious predators of sea urchins These fishes kept sea urchin populations small enough to allow persistence of kelp forests despite intensive aboriginal and early European hookandline fishing for at least 5000 years New mecha nized fishing technology in the 1920s set off a rapid decline in numbers and body size of coastal cod in the Gulf of Maine 7 Fig 2A and Table 1 that has extended offshore to Georges Bank 35 Formerly dominant pred atory fish are now ecologically extinct and have been partially replaced by smaller and commercially less important species Lob sters crabs and sea urchins rose in abun dance accordingly 7 Kelp forests disap peared with the rise in sea urchins due to removal of predatory fish and then reap peared when sea urchins were in turn reduced to low abundance by fishing The more diverse food web of southern California kelp forests historically included spiny lobsters and large sheephead labrid fish in addition to sea otters as predators of sea urchins as well as numerous species of aba lone that compete with sea urchins for kelps Fig l A and B 36 Aboriginal exploita tion began about 10000 yr BP and may have had local effects on kelp communities 37 The fur trade effectively eliminated sea otters by the early 1800s 38 but kelp forests did not begin to disappear on a large scale until the intense exploitation and ecological ECOLOGY THROUGH TIME extinction of sheephead spiny lobsters and abalone starting in the 1950s 8 36 Table l and Fig l A and B Subsequent fishing of the largest sea urchin species in the 1970s and 1980s resulted in the return of welldevel oped kelp forests in many areas that as in the Gulf of Maine effectively lack trophic levels higher than that of primary producers 36 39 Coral Reefs Coral reefs are the most structurally complex and taxonomically diverse marine ecosys tems providing habitat for tens of thousands of associated fishes and invertebrates 40 Aboriginal fishing in coral reef environments began at least 35000 to 40000 years ago in the western Pacific 41 but appears to have had limited ecological impact Recently cor al reefs have experienced dramatic phase shifts in dominant species due to intensified human disturbance beginning centuries ago I Fig l C and D The effects are most pronounced in the Caribbean 42 but are also apparent on the Great Barrier Reef in Austra lia despite extensive protection over the past three decades 43 Large species of branching Acropora cor als dominated shallow reefs in the tropical western Atlantic for at least half a million years 44746 until the 1980s when they declined dramatically 42 47 Fig 2B and Fig 2 Retrospective data showing baselines before ecosystem collapse A Time series of mean body length of Atlantic cod from kelp forests in the coastal Gulf of Maine The earlier five data points are derived from archaeological records whereas the last three points are from fisheries data 113 Vertical bars represent the standard error Horizontal bars represent the time range of data for a single interval of observations B Paleoecological and ecological data showing the percentage of Caribbean lo calities with Acropora palmata A or A cervi cornis I as the dominant shallowwater coral in the Late Pleistocene Holocene before 1983 and after 1983 114 Percentages of localities are significantly different over the four time periods for A palmata X2 340 P lt00001 df 3 and A cervicornis X2 224 P lt00001 df 3 Vertical and horizontal bars are as in C Paleoecological and fisheries data from Chesapeake Bay showing the ratio in abundance of planktonic to benthic dia toms dotted line 77 and landings of the oyster Crassostrea virginica solid line 80 The planktonic to benthic diatom ratio is a proxy for eutrophication that shows the rel ative amount of planktonic to benthic prima ry production 77 For over 1200 years this ratio remained fairly constant at about 11 but then increased threefold coincidentally Table 1 Patterns of community membership and dominance of coral species were also highly predictable 44 so that there is a clear baseline of pristine coral community compo sition before human impact Western Atlantic reef corals suffered sud den catastrophic mortality in the 1980s due to overgrth by macroalgae that exploded in abundance after mass mortality of the su perabundant sea urchin Diadema antillarum that was the last remaining grazer of macroal gae 42 47 Early fisheries reports suggest that large herbivorous fishes were already rare before the 20th century 48 However macroalgae were held in check until the last major herbivore Diadema was lost from the system through disease 42 4 7 Corals on the Great Barrier Reef have experienced recurrent mass mortality since 1960 due to spectacular outbreaks of the crownofthorns starfish Acanthaster planci that feeds on coral 49 The causes of out breaks are controversial but they are almost certainly new phenomena There are no early records of Acanthaster in undisturbed fossil deposits in aboriginal folklore or in accounts of European explorers and fishers Now in recent decades the frequency and intensity of outbreaks have exceeded the capability of longer lived species to recover as outbreaks have become more chronic than episodic 50 Mean cod length cm m o I I a o l I Percent of localities with Acropora dominant A O I Oyster landings x105 metric tons PIanktonicbenthic diatom ratio I I I I I u 105 1o5 10quot 1000 100 10 1 Years before present with increased runoff of sediments and nutrients due to European agriculture after 1750 The ratio remained at about 31 between 1830 and 1930 after which it increased dramatically to about 81 Oyster landings show an initial increase in the early 19th century peak in 1884 and subsequent collapse as deep channel reefs were destroyed by mechanical dredging 80 These data strongly imply that oysters were able to limit the potential for eutrophication induced by increased inputs of nutrients between 1750 and 1930 until oyster populations collapsed as a result of overfishing www5ciencemagorg SCIENCE VOL 293 27JULY 2001 631 632 27 jULY 2001 VOL293 SCIENCE www seiencemagnrg Table 1 Retrospective records from coastal ecosystems that offer baselines that contrast With recent observations Data source P paleoecologial A archaeological H historical F fisherie E ecological Inferred causes 1 fishing 2 mechanical hab 115 are located on Science Online itat destruction by fishing 3 inputs AbbreVIations BSi biologically bound silica DOP degree of pyritization of iron dec decreas nc increase References after I I I Parameter of interest Proxy Time of baseline yr BPI Baseline obsenation or estimate Recent obsenation or estimate Tren d Kelp forests Sea Otter Stellar39s sea cow Atlantic cod White abalone Coral reefs Coral Coral Monk seal Coral Tropical and subtropical seag39ass beds Green turtle Green turtle Seagrass beds Dugong Dugong Oysters and eutrophication Inputs Eutrophication Eutrophication Eutrophication II nnnn Area estimates Herd size Cod vertebrae Number per area sites with A palmata dominant sites with A cervicornis dominant Standardized abundance of A cenicornis Rela e abundance Coral cover at 10 m Coral cover at 10 m Historical reports Acropora dominance in fossil reefs Biomass estimates Hun g biomass estimates Area Herd size Herd size Sedimentation rate Total organic carbon Centricpennate diatom ratio Dinoflagellate cysts Spiniferites 5PP 260 259 3550 30 125000 125000 125000 3130 27 23 gt300 8000 gt300 gt300 121 gt100 gt100000 individuals lt5000 sea cows Mean body length of 10 m gt2000 per ha 80 of Pleistocene sites 63 of Pleistocene sites 12 A cenicornis dom ant 54 coral cover 73 coral cover Abundant Dominated reefs throughout Bay gt161 X 106 50kg turtles gt33 X 107 adult turtles 301970 ha gt10 X 106 estimated dugongs gt104000 estimated dugongs 004 cm year 026 mg cm 2 year I 11 ratio 50 rela ive abundance 30000 ind duals 0 Mean body length of 03 m 10 t 04 per ha 15 of post1982 sites 0 of post1982 sites A cervicornis absent 31 coral cover 4 coral cover 0 Only one small Acropora reef left gt11 x106 50kg turtles gt11 x106 50kg turtles 101759 ha 140 estimated 02 cm year l 23 mg cm 2 year l 81 ratio 80 relative abundance gt33fold dec Extinction 3fold dec gt2000fold dec 53fold dec 100 loss 12fold dec 100 loss 17fold dec 18fold dec Decrease 15fold dec 30fold dec 3fold dec gt74 fold dec gt208fold dec 5fold inc 9fold inc 8fold inc 16fold inc m 116 117 113 118 114 114 119 2 122 1 122 123 124 125 126 125 127 ECOLOGY THROUGH TIME Table 1 Continued Inferred cause Tren d Recent obsenation or estimate Baseline obsenation or estimate Time of baseline yr BP Proxy Data source Parameter of interest Location 17fold dec 52fold dec 16 ha 273 ha 63 Area H F Fleets Bay CB Chesapeake Bay Seagrass beds 012 X 105 metric tons Oyster landings 62 X 105 metric tons Oyster reefs 100 loss year l Area F Tangier Sound C B Oyster reefs 051 DOP 188 ha 032 DOP 1900 Degree of pyritization Botany Bay Seagrass beds ECOLOGY THROUGH TIME h N am V 0 NO 2 2 a 3 22 2 2 m m m m NN mm m m U 2 u L Lid U E u E E 33 EE 5 u e 2 13 13 31 BE 3 2 6 2 3 3 22 22 e 2 o o oo o I N no 7 2quot N m m N wN mm Ko 1 1 Tu cu La 2 u E 3 32 k E c f 5 gt13 3 E 393 o a L E 22 n i 0 N m cu N D 3 g 172 i r quot1 v NSN ltu gwo E 2 lt 8 sci a w mu 5 WE HgE U O mu Ex2 9 50 5 u no a N E OE a xv x w o X230 Ex a o o o m 000 m eo W no h 0 1 1 1 l w m 1 Lu 2 Na C cu 3 g L E 5 E 2 x m 6 m E D i E 3 a E U 6 E 39 L gt Q E cu m E u N II in 3 cu 2 gm 2394 i u gt D E m c mUN m g E Q 45 g wu z gt no In D Omum o CEE 2 Fame 52 2 no a 23 o Him EM u N m 2 BMW o N Nltr o 8 N m m 0N N w O w 0 L110 Ln 0 KO Ln m o g mo 0 N no N N N N E E g 2 cu m 2 m E 2 E a L 2 83239 532 23 2 2 a 39geE uEnm 2 n gage 2 E u 31 Du 2 0390 0 D emuzen 55 4qu 5m KU39ENV39 134 quotMN d gtCdx D Cmc cm mo 0 39U Vua a mu ua u u UcLEu 39gt ULE Egg om o2 I15 4quotqu ltuD nadu o A rmu u out oou V x 5 E a name 528 E I 3 5quot Ei m LLI u n a rut an NN 22 212 22 2 m m m mag 55 a 3 3 5 cu cu m2 2 Z w w E m m was 2 u 2 2 2 2 25 DD D K K 4 4 g 239 a a Eoo 3 3 3 3 i m m mELLLL 00 0 lt lt a c a U E c c g c c c o 2 2 Law 22 2 2 c E E E39Wt HE E E E 2 2 leg 22 2 2 4 again E39EEE 5 e 2 554m 22 g e e S 4 4 dadt 4 4 5 gt a a a 88 as I a a a n o www5ciencemagorg SCIENCE VOL 293 One possible explanation for Acanthaster outbreaks is that overfishing of species that e highly cryptic predatoravoiding behavior of juvenile starfish their formidable antipreda tor defenses as subadults and adults and the reduction of some generalized predatory fish a to down rc a recreational shing as well as indirect effects of intensive trawling for prawns are likely explanations for decreased abundance r 2 a i O H m 0 0 due to increased runoff of nutrients from land 53 In either case the explanation is almost certainly historical and anthro ogenic and cannot be resolved by recent observa tions alone Expeditions occurred annually to northern Australia from th Malay Archipelago throughout the 18th and 19th centuries to vest an century 55 Whales dugongs turtles pearl sters and T rochus shell were each heavily exploited only to rapidly collapse and all hav 39 39 smal irig of pelagic and reef fishes sharks an prawns has continued to the present although catch per unit effort has declined greatly 58 Tropical and Subtropical Seagrass Beds Seagrass beds cover vast areas of tropical and subtropical bays lagoons and conti nental shelves 59 Seagrasses provide for age and habitat for formerl enormous s invertebrates iriclu ing man ly important species 59762 Fig l C and D Like coral reefs seagrass beds seemed to be highly resilient to human disturbance until recent decades when mass mortality of seagrasses became common an 39 e spread 63765 Examples include the die off of turtlegrass in Florida Bay and the Gulf of Mexico in the 1980s 65 and the near disappearance of subtidal seagrasses h l n ar H1 5 F 3 B years 63 64 roxirnate causes of these losses include recent increases in sedimen tation turbidity or disease 63765 How ever extirpation of large herbivorous ver tebrates beginning centuries ago had al ready profoundly altered the ecology of 27 jULY 2001 seagrass beds in ways that increased their vulnerability to recent events Vast populations of Ver large green tuitles were eliminated from the Americas before the 19th century I 2 Table 1 Formerly great populations of green turtle 39 Moreton Bay Australia also were greatly reduced by the early 20th century 66 Moreover there are no estimates of abundances of turtles I1 Australia al numbers lost All turtle species continue to decline at unsustainable rates along the Great Barrier Reef today 67 Abundant green turtles closely crop turtlegrass and greatly reduce the flux of organic mater and nutrients to sediments 59762 68 In the near absence of green turtles today turtlegrass beds grow longer blades that baffle currents shade the bot tom start to dec 39 39 disease 65 Deposition within the beds of vastly more plant detritus also fuels micro bial populations increases the oxy en de mand of sediments and promotes hypoxia beds in Florida Bay 65 except for chang es in temperature and salinity can be at tributed to the ecological extinction of green turtles 27 uropean colonists did not exploit tropical American manatees as systematically as ey exploited green turtles so the data re fisheries are poor We lmow however that manatees were extensively shed by aboriginal people and by early colonists 68 In Australia 1 e numbers reported by early colonists were vast Three or fourmilelong herds com prising tens of thousands of 1ar e individuals were observed in Wide Bay in about 1870 69 and in Moreton Bay as recently as 1893 70 Widespread colonial exploitation of dugongs fo e39 d 39 along the south Queensland coast resulted in the crash of the dugong fishery by the beginning of the 20th century 3 Table 1 Ironically scientists re 39 ry of a large popu 300 individuals 71 Further north numbers of dugongs in the vast southern half of the Great Barrier Reef had dwindled to fewer than 4000 when they were rst accurately counted in 1986787 with a further 50 to 80 decline in recent years 72 These increasingly fragment ed populations represent the last re ts of the vast herds of the early 19th century and before The ecological implications of these re ductions are at least as impressive as those for green turtles Moderate sized herds of dug 27JULY 2001 ECOLOGY THROUGH TIME ongs remove up to 96 of aboveground biomass and 71 of belowground biomass of seagrasses 73 Their grazing rips up large areas of seagrass beds oviding space for colonization by competitively inferior species of seagrasses Dugong grazing also produces massive amounts of oating debris and dung that are exported to adjacent ecosystems The decline in seagrasses in Moreton Bay is cer tainly due in large part to the dramatic decline in water quality due to eutrophication and runoff of sediment 63 64 Nevertheless as noted for green turtles and turtlegrass in Flor ida Bay the cessation of systematic plowin of the bay floor by once abundant dugongs must also have been a major factor Oysters and Eutrophication in Estuaries Temperate estuaries worldwide are undergo ing profound changes in oceanography and ecology due to human exploitation and pol lution renderin them the most degraded of 39 e ecosystems 74776 Fig 1 E and F The litany of changes includes increased sed imentation and turbidity 77 enhanced epi sodes ofhypoxia or anoxia 74 75 77 loss of seagrasses 78 and dominant suspension feeders 79 with a general loss of oyster reef habitat 80 shifts from ecosystems once dominated by benthic primary production to those dominated b planktonic primary pro duction 77 eutrophication 74776 and en hanced microbial production 81 and higher frequency and duration of nuisance algal and toxic dino agellate blooms 82 83 out breaks of jellyfish 79 and fish kills 83 Most explanations for these phenomena em phasize bottomup increases in nutrients 39 osphorus as causes of ankton blooms an eutrophication 74776 an interpretation consistent with the role of estuaries as the focal point and sewer for many landbased human activities Nev ertheless longterm records demonstrate that reduced topdown control resulting from losses in benthic suspension feeders predated eutrophication The oldest and longest records come from cores in sediments from Chesapeake Bay 77 and Pamlico Sound 84 in the eastern United States and from the Baltic Sea 85 that extend back as far as 2500 yr BP Fig 2C and Table 1 A general sequence of ecological change is apparent in all three cases but the timing of speci c ecological transitions differs among estuaries in kee 39 g 7339 E 7a difference that rules out a s imatic explanation Increased sedimentation and burial of organic carbon be an in the midi 18th century in Chesapeake Bay coincident with widespread land clearance for agricul ture by European colonists 77 The main ecological response was a gradual shi in the taxa responsible for primary production that began in the late 18th century Seagrasses and p1 on in the water column corresponding ly increased However anoxia and hypoxia were not widespread until the 1930s when fauna 75 77 Fig 2C and Table 1 Similar changes began in the 1950s in the Baltic Sea with widespread expansion of the extent of anoxic laminated sediments 74 85 and in Vast oyster reefs were once prominent structures in Chesape e Bay 11 where they may have filtered the equivalent of the entire water column every 3 days 79 De mechanical harvesting with dredges in 1870s that deep channel reefs were seriously affected 79 80 Oyster catch was rapidly reduced to a few percent of peak values by had collapsed did hypoxia anoxia and other symptoms of eutrophication begin to occur in the 1930s 75 77 and outbreaks of oyster parasites became prevale e B o E lt B E quality and disease were secondary factors 80 However now that oyster reefs are destroyed the effects of eutrophication disease hypoxia and continued dredging interact to prevent the recovery of oysters and associated communities 86 Field ex periments in Pamlico Sound demonstrate that oysters grow well survive to maturity and resist oyster disease when elevated above the zone of summer oxiai even in the presence of modern levels of en trophication and pollution 87 Overf1s ing of oysters to the point of eco logical extinction is just one example in a general pattern of removal of species capable o topdown control of community structure in estuaries Dense populations of oysters and other suspensionfeeding bivalves graze plankton so ef ciently that they limit blooms of phytoplankton and prevent symptoms of eutrophication 88 89 just as occurs with azing y zoopl on in freshwater ecosys 90 The ecological consequences of own Gray whales now extinct in the Atlantic dol phins manatees river otters sea turtles alli gators giant sturgeon sheepshead sharks an rays were all once abundant inha itants of Chesapeake Bay but are now virtually d eliminate VOL 293 SCIENCE www5ciencemagorg Offshore Benthic Communities Continental shelves cover more of the ocean e halibut plaice rays and a host of other ground shes scallops cockles and oysters have been shed intensively for centuries from conti nental shelves of Europe and North America and more recently throughout the world 5 7 10 91 Hookand line shing was replaced by intensive use of the beam trawl during the 18th century and industrialized fishing was further intensi ed with the advent of large steam and dieselpowered vessels and the otter trawl at the end of the 19th century Reports of severely depleted sh stocks and shi ing of fishing grounds farther and farther from home ports into the North Sea and the outer Grand Banks were commonplace by the beginning of the 19th century Scientific in vestigation consistently lagged behind eco nomic realities of depleted stocks and inexo rable exploitation of moredistant shing grounds As late as 1883 Thomas Huxley claimed that fish stocks were inexhaustible 92 a view discredited by the be inning the 20th century 5 Today several formerly abundant large sh as well as formerly dense assemblages of suspension feeders are eco logically extinct over vast areas 7710 93 o o 9 o H The Primacy of Overfishing in Human Disturbance to Marine Ecosystems Over shing of large vertebrates and shell sh was the first major human disturbance to all coastal ecosystems examined Table 1 Eco logical changes due to over shing are strik ineg similar across ecosystems despite the obvious differences in detail Fig l A to F verywhere e magnitu enormous in terms of biomass and abun ance of large animals that are now effectively ab sent from most coastal ecosystems world e Americas and Paci c closely tracks European colonization and exploitation in most cases However aboriginal over shing also had ef fects as exempli ed by the decline of sea otters and possibly sea cows in the northeast Paci c thousands of years a 0 There are three important corollaries to the primacy of overfishing The first is that pollution eutrophication physical destruc tion of habitats outbreaks 0 disease inva sions of introduced species and human induced climate change all come much later than overfishing in the standard sequence of historical events Fig 3 The pattern holds regardless of the initial timing of colonial over shing that be an in the Americas in the 16th and 17th centuries and in Australia and New Zealand in the 19th www5ciencemagorg SCIENCE ECOLOGY THROUGH TIME century The full sequence of events is most characteristic of temperate estuaries like Chesapeake Bay Not all the human distur bances illustrated in Fig 3 have affected all ecosys ems yet But wherever these events have occurred the standard chronological sequence of human disturbance and modi fication of ecosystems is recognizable The second important corollary is that ease or species introductions to occur 27 For example eutrophication and hypoxia did not occur in Chesapeake Bay until the 1930s nearly two centuries after clearing of land for agriculture greatly increased runoff of sedi m nts and nutrients into the estuary 77 Suspension feeding by still enormous popu lations of oysters was suf cient to remove most of the increased production of phyto plankton and enhanced turbidity until me chanical harvesting progressively decimated oyster beds from the 1870s to the 1920s 77 80 Fig 2C The consequences of overfishing for out breaks of disease in the next lower trophic level fall into two categories The most straightfor c susceptible to disease as a result of greatly increased rates of transmission 94 This was presumably the case for the sea urchinDiadema on Caribbean reefs and the seagrass Malaysia in Florida Bay In contrast among oysters dis ease did not become impormnt in Chesapeake Bay until oysters had been reduced to a few percent of their original abundance 80 a pat tern repeated in Pamlico Sound 86 87 and Foveaux Strait New Zealand 93 Two factors may be responsible First oysters may ve become less t owing to stresses like hypoxia or sedimentation making them less resistant to disease 87 Alternatively suspension feeding by dense populations of oysters and associated species on oyster reefs may have indirectly E Fl 3 Historical se que e of human distur b affecting coastal 39 step outbreaks of microbial populations 88 The third important corollary is that changes in climate are unlikely to be the primary reason for microbial outbreaks and disease The rise of microbes has occurred at different times and under different climatic conditions in different places as exempli ed by the time lag between events in Chesapeake Bay and Pamlico Sound 77 79 80 84 Anthropogenic climate change may an impo ant confounding factor but it was not the original cause Rapid expansion of introduced species in recent decades 95 may have a similar explanation in addition to increase in frequency and modes of transport Massive removal of suspension feeders graz ers and predators must inevitably leave ma rine ecosystems more vulnerable to invasion 96 97 Synergistic Effects of Human Disturbance Ecological extinction of entire trophic levels systems more vulnerable to other natural and human disturbances such as nu trient loading and eutrophication hypoxia disease storms and c imate change E p sion and intensi cation of different forms of human disturbance an their ecological ef fects on coastal ecosystems have increased and accelerated with human population 0 checked exploitation of biological resources technological advance and the in creased geographic scale of exploimtion through globalization of markets Moreover the effects are synergistic so that the whole response is much greater than the sum of individual disturbances 98 This is perhaps most apparent in the rise of eutrophication ter reefs by mechanical harvesting of oysters 79 80 86 Other possible examples are outbreaks of seagrass wasting disease due to the removal of grazers of seagrasses like the green turtle 27 A striking feature of such synergistic effects is the suddenness of the transition in abundance 5 Climate change 4 Introductions 7a ase X I W Human Mechanical the basis for our h oth pri 3 ch of expanSion hab39ta 902me overfishing in the deterlo desm ct39on atlon of coastal ecosys 2 terns wor i bse Pollution vary in or er 1 Fishing Then quotnuquotIIN wu VOL 293 27 jULY 2001 635 of different kinds of organisms and com munity composition due to threshold ef fects 99 Ecological diversity and redun een the onset of fishing and the subsequent threshold response 42 100 The importance of biodiversity in the form forests in southern California compared with Alaska after the extirpation f sea otters Sheephead f1sh spiny lobsters and abalone in the more diverse Californian kelp forests kept sea urchin populations in check until these predators and competitors 0 sea urchins had also been effectively eliminated 8 36 Similarly the seaur 39 Diadema kept macroalgae in check long a er the extreme overfishing of herbivo rous fishes on Caribbean coral reefs 42 lapse is the elimination f1shed refuges that were protected historically because of distance or expense of access For example reef f1shes all around Jamaica in the Jamaican reefs at that time must have come from undiscovered populations in Jamaica or elsewhere 101 But as more and more reefs have been over shed the potential sources of such recruits must have effectively disap peared over wider areas 102 A similar sce nario has been proposed for the American lobster with regard to loss of larvae from deepwater offshore stocks 103 Microbialization of the Global Coastal Ocean Most recent changes to coastal marine eco systems subsequent to overfishing involve population explosions of microbes responsi ble for increasing eutrophication 74776 81 diseases of marine species 104 toxic blooms 82 83 and even diseases such as cholera that affect human health 104 105 Chesapeake Bay 81 and the Baltic Sea 74 are now bacterially dominated ecosystems with a trophic structure totally different from mou the Adriatic Sea 107 Nowhere is the lack of historical perspec tive more damaging to scientific un erstand 39 than for microbial outbre Plans for remediation of eutrophication of estuaries are still based on the belief that eutrophication is caused only by increased nutrients without regard to overfishing of suspension feeders Even more remarkable is the attribution of the use in marine diseases to climate change and pollution 104 without regard to the th of the Mississippi River 106 and to 27 JULY 2001 ECOLOGY THROUGH TIME pervasive removal of higher trophic levels asynchronous outbreaks of disease in different ecosystems that belie a simple cli matic explanation Historical Perspectives for Ecosystem Restoration The characteristic sequence of human distur bance to marine ecosystems Fig 3 provides a framework for remediation and restoration that is invisible without a historical perspec tive More speci c paleoecological arc eo logical and historical dam should be obtained to refine the histories of specific ecosystems and as a tool for management but the overall attems are clear The historical magnitudes of losses of large animals and oysters were so great as to seem unbelievable based on mod ern observations alone Table 1 Even seem ineg gloomy estimates of the global percent age of sh stocks that are overfished 108 are almost certainly far too low The shi ing baseline syndrome is thus even more insidi ous and ecologically widespread than is com monly realized On the other hand recognition of these losses shows what coastal ecosystems could be like and the extraordinary Ina Iiitude of economic resources that are retrievable if we are wi ling to act on the basis of historical knowledge The central point for successful restoration is that loss of economically im portant fisheries degradation of habitat at tractive to landowners and tourists and emer gence of noxious toxic and lifethreatening microbial diseases are all part of the same standard sequence of ecosystem deterioration that has deep historical roots 2 7 Respond ing only to current events on a casebycase basis carmot solve these problems Instead they need to be addressed by a series of bold experiments to test the success of integrated management for multiple goals on the scale of entire ecosystems With few exceptions such as the Caribbean monk seal and Steller s a cow most species that are ecologically extinct probably survive in suf 1cient num bers for successful restoration This optimism is in stark contrast with the state of many terrestrial ecosystems where many or most 1 irnals are already extinct 28 More animals like sea turtles sirenians sharks and large groupers We can then use these data to build tentative models of the consequences of the renewed abundance of these species in their native environments that can in turn be used to design largescale adaptive experi ments for ecosystem restoration exploitation and management 96 108 110 One obviously timely and overdue exper iment is to attempt the amelioration of eu trophication hypoxia and toxic blooms in Chesapeake Bay by massive restoration of oys ter reefs 79 Experiments I1 Pamlico Sound tial restorat39on of oysters would red trophication substantially 110 Aquaculture of suspensionfeeding bivalves like oysters might be promoted to reverse the effects of eutroplii cation and to restore water quality in degraded estuar es er important examples include the restoration of coral reefs and seagrass beds by protection of fishes sharks turtles and sire Iiians in very large reserves on the scale of all of Florida Bay and the Florida Keysian ap proach recently advocated for terrestrial ecosys tems 11 On fishes could reverse the overgrowth of corals by macroalgae on a massive scale The potential for reducing diseases of corals and turtlegrass by restoring natural levels of grazing is unprov n ummar longterm effects of fishing provides a hereto foremissing perspective for successful man agement and restoration of coastal marine eco systems Previous attempts have failed because ha focused only on the most recent symptoms of the problem rather than on their deep historical causes Contrary to romantic notions of the oceans as the last frontier and of the supposedly superior ecological wisdom of nonWestem and precolonial societies s demonstrates that overfishing fundamentally altered coastal marine ecosystems during each of the cul tural periods we examined Changes in eco system structure and function occurred as early as the late aboriginal and early colo nial stages although these pale in compar ison with subsequent events Human im pacts are also accelerating in their magni tude rates of change and in the diversity of over quent disturbance and thus preconditioned the collapse we are witnessing References and Notes 1 J B C Jackson Coral Reef 16 23 1997 Bolten M Y Chaloupka Ecol Appl 10 269 2000 3 G C L Bernam C K Ricardo Bertram Biol Linn Soc 5 297 1973 K W Kenyon Mammal 58 97 1977 5 D H Cushing The Providenr Sea Cambridge Univ Press Cambridge UK 1988 6 J A Estes D O Duggins G B Rathbun Conrerv Biol 3 252 1989 R S Steneck in Proceeding of me Gulf of Maine m Dynamic Scienn39 c Symposium and Workshop RARGOM Report 9171 Regional Associr ation for Research 39n the Gulf of Maine Hanover NH 1997 pp 1517155 P K Da ton M J Tegner P B Edwards K L Riser Ecol Appl 8 309 1998 9 J M Casey R A Myers Science 228 690 1998 10 J A Hutchings Narure 406 882 2000 5 1 VOL 293 SCIENCE www5ciencemagorg 11 N w G J 00 Fossil Benthic Commu N 0 NN N N 10 N 5 N m NNN a WWW eons 200403 1978 E Sala C F Boudouresque M HarmelianiVien 10 N w w w 5 w m w a cow J 10 8 3 quotFishingquot is J J B C Jackson Bio R C Francis S R 8 D H JanZen P S P K J A Estes J F Palmisano Science185 10581974 JAEs BJB E Ingersoll in The History and Present Condition of me Fishery Industries G B Goode Ed US Departr f the Interior Tenth Census of the United States Washington DC 1 pp 17252 the original and most general term in the English language for hunting and gathering all kinds of organisms in the oceans including plants invertebrates and vertebrates ranging from sharks to Hue fishes to whales Overfishing is the reducr tion of a species well below the sustainable yield or to such low abundance that it may not recover even if fishing ceases H Brown Macroecology Univ of Chicago Press Chicago IL 1995 Science 41 475 1991 Hare Fish Oceanogr 3 279 1 994 A D MacCall Calif Coop Fish Invest 37 100 996 1 C B Lange S K Burke W H Berger Clim Change 16 319 1990 B C Jackson in Biotic Interactions in Recent and nin39es M J S Teve P L McCall Eds Plenum New York 1983 pp 397120 avis The Archaeology of Animals Yale Univ Press New Haven CT 1987 C er W H Berger J Bijima G Fischer in Use of Proxies in Paleoceanography Examples from the South Adann39c G Fischer G Wefer Eds Springer Verlag Berlin 1999 pp 176 D S Jones Paleontol Soc Pap 4 37 1998 C W F1nkl Jr 1 Coast Res Spec Iss 17 402 199 5 A W Crosby Ecological Imperialism The Biological 900 Expansion of Europe a 900 Cambridge Univ Press Cambridge UK 1986 Biological proxies include fossils or archaeological remains that may indicate presence abundance age growth rate health or body size among other factors of selected taxa Biogeochemical proxies include concentrau39ons of inorganic or organic conr stituents and isotopic ratios in sediments or skeler tons that track former abundances of unpreserved organisms and variations in parameters such as temperature salinity oxygen nutrient chemistly uctivity Physical proxies include sedimenr taIy structures and composiu39on that reflect water movements runoff from the land and rate of sed imentau39on Historical proxies include demographic customs and commercial records as well as explorr nd naturalists39 descripu39ons of sights and nautical charts marking reefs coastal wetlands and other landmarks R S Bradley Paleoclimatologyi Reconsnucting Clia mates of the Quaternary Academic Press San Dir ego ed 2 1999 I S M Kidwell K W FlessaAnnu Rev Ecol Syst 26 259 1995 I 7 J B C Jackson Proc Natl Acad Sci USA 98 5411 2001 Martin Science 215 19 1982 Dayton Annu Rev Ecol Syst 16 215 1985 C A S1mensta I J A Estes K W Kenyon Science Oikos 2 425 1998 tes M T Tinker T M Williams D F Doak Science 282 473 ourque Diversig and Complexin in Prehistoric Marin39me Societies A Gulf of Maine Perspecn39ve Plea num New York 1995 K Sherman Ecol Appl 1 349 1991 M J Tegner P K Dayton ICES Int Counc Expi 000 Sea 1 Mar Sci 57 579 2 J M Erlandson et al Radiocarbon 38 355 1996 8 A O den The California Sea Otter Trade Univ of California Press Berkeley 1941 9 M J Tegner P K Dayton Mar Ecol Prog Ser 77 49 1991 N Knowlton Proc Natl Acad Sci U S A 98 5419 2001 J Allen C Gosden J P White Ann39guig 63 548 989 1 T P Hughes Science 255 1547 1994 www5ciencemagorg SCIENCE VOL 293 27JULY 2001 ECOLOGY THROUGH TIME 43 R A Kenchington Managing Marine Environments Taylor and Francis New York 1990 44 J M Pandolfi J B c Jackson Ecol Monogr 71 49 2001 45 ebb a youoxi m 0 m m m mm 93 m m m m 9 1 m 5 2 m N 323 m m m m a 5 9 1 J 0 J N 8 coco N 83 5 J 1 5 D T Neil in IVVVVVV DV Jabs 0 9 RE Newell in Unders n R B Aronson W F Precht I G Maclntyre Coral Reefs 17 223 1998 Geister Proc 3rd Int Coral Reef Symp 1 23 977 H A Lessios Annu Rev Ecol Syst 19 371 1988 J E Duerden West Indian Bull 1901 121 1901 What Is Natural Coral Reef Crisis Oxford Univ Press New York 1999 R eymour R H Bradbury Mar Ecol Prog Ser 176 1 1999 R Ormond et al in Acanmaster and me Coral Reef A Theoretical Perspective R H Bradbury E SpringerrVerlag Berlin 1990 p 1897207 en An Analysis of Fishing Activin39es on Possia ble Predators of the Crown of Thorns Star sh Acanr thaster planci of the Great Barrier Reef Prepared for the Great Barrier Reef Marine Park Authority Townsville Australia 1988 39 nd Mar Biol 59 175 1982 Press Melbourne Ausnalla 1 76 Moreton Bay and Catchment I R Tibbetts N J Hall W C Dennison Eds Univ of Queensland Brisbane Australia 1998 p 3754 of Tangalooma Nautical Asr sociation of Australia Melbourne 1980 R Ganter The PearlaSheIlers of Torres SHait Rea source Use Development and Decline 186 Melbourne Univ Press Melbourne Australia 1994 R H Quinn Fisheries Resources of me Moreton Bay Region Queensland Fish Management Authority Brisbane Australia 1993 O den in Handbook of Seagrass Biology An Ecosystem Perspective R Phillips C P McRoy Eds Garland STPM New York 1980 pp 1737198 G a er D W Engel K A Bjorndalj Exp Mar Biol Ecol 62 173 1982 J C Ogden L Robinson H Whitlock H Daganhart R Cebulaj Exp Mar Biol Ecol 66 199 1983 Thayer K A Bjorndahl J C Og en S L Williams J C Zieman Estuaries 7 351 1984 H Kirkman Aguat Bot 5 E G Abal W C Dennison Mar Freshw Res 47 763 1995 J C Zieman J W Fourqurean T A Frankovich Estuaries 22 460 1999 C J Limpus P J Couper M A Read Mem Queensa land Mus 35 139 1994 C J Limpus in State of me GreatBarrier Reef World Heritage Area Workshop D Wachenfeld J Oliver K Davis ds Great Barrier Reef Marine Park Au orr ity Townsville Australia 1995 pp 2587265 W Dampier A New Voyage around the World Dor ver New York 1968 E Thorne The Queen of me Colonies Sampson Low Marson Searle and Rivington London 18 G M Allen Am Comm Int Wildl Protect Pub 11 1 1942 G E Heinsohn R J B R Gardner Environ Conserv 5 91 1978 H Marsh P Corkeron I Lawler J Lanyon A Preen Great Barrier Reef Marine Park Authority Rep 41 1 1 996 a E a ISpec Lear M M Br den H Marsh A Preen Mar Ecol Prog Ser 124 201 1995 1989 9 1995 G S Brush Estuaries 16 617 1993 A M ore Science 222 51 1983 La 39 eEstuaryAdvach eake Bay Research M P Lynch E C peake Bay Research Consortium Baltimore MD 1988 pp 535545 1 R J Orth K 1997 T Smay a in Toxic Marine PIytoplankton E Graneli et al Eds Elsevier Science New York 1990 pp 29740 J M Burkholder et al Nature 358 407 1992 3 8 C B Officer T J Smay 3898 LOLO wN J Stachow1c1 R B N Knowlton A S J Munro ICLAR R R Colwell


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