Global Ecological Consequences of the 1982-83 El Nino-Southern Oscillation (Elsevier Oceanography Series)

GLOBAL ECOLOGICAL CONSEQUENCES OF THE 1982-83 EL NINO-SOUTHERN OSCILLATION

FURTHER TITLES IN THIS SERIES 1 J L MERO T t E MINERAL RESOURCES OF THE SEA 2 L M FOMIN THE DYNAMIC METHOD IN OCEANOGRAPHY 3 E J F WOOD MICROBIOLOGY OF OCEANS AND ESTUARIES 4 G NEUMANN OCEAN CURRENTS 5 N G JERLOV OPTICAL OCEANOGRAPHY 6 V VACOUIER GEOMAGNETISM IN MARINE GEOLOGY 7 W J WALLACE THE DEVELOPMENTS OF THE CHLORINITY/ SALINITY CONCEPT IN OCEANOGRAPHY 8 E LlSlTZlN SEA LEVEL CHANGES 9 R H PARKER THE STUDY OF BENTHIC COMMUNITIES 10 J C J NIHOUL (Editor) MODELLING OF MARINE SYSTEMS 11 01 MAMAYEV TEMPERATURE SALINITY ANALYSIS OF WORLD OCEAN WATERS 12 E J FERGUSON WOOD and R E JOHANNES TROPICAL MARINE POLLUTION 13 E STEEMANN NIELSEN MARINE PHOTOSYNTHESIS 14 N G JERLOV MARINE OPTICS 15 G P GLASBY MARINE MANGANESE DEPOSITS 16 V M KAMENKOVICH FUNDAMENTALS OF OCEAN DYNAMICS 17 R.A.GEYER SUBMERSIBLES AND THEIR USE IN OCEANOGRAPHY AND OCEAN ENGINEERING 18 J.W. CARUTHERS FUNDAMENTALS OF MARINE ACOUSTICS 19 J.C.J. NIHOUL (Editor) BOTTOM TURBULENCE 2 0 P.H. LEBLOND and L.A. MYSAK WAVES IN THE OCEAN 2 1 C C VON DER BORCH (Editor) SYNTHESIS OF DEEP-SEA DRILLING RESULTS IN THE INDIAN OCEAN 2 2 P DEHLINGER MARINE GRAVITY 23 J C J NIHOUL (Editor) HYDRODYNAMICS OF ESTUARIES AND FJORDS 24 F T BANNER, M B COLLINS and K S MASSIE (Editors) THE NORTH-WEST EUROPEAN SHELF SEAS: THE SEA BED AND THE SEA IN MOTION 25 J.C.J. NIHOUL (Editor) MARINE FORECASTING 26 H.G. RAMMING and 2. KOWALIK NUMERICAL MODELLING MARINE HYDRODYNAMICS 27 R.A. GEYER (Editor) MARINE ENVIRONMENTALPOLLUTION 28 J.C.J. NIHOUL (Editor) MARINE TURBULENCE 29 M. M . WALDICHUK. G.B. KULLENBERG and M J ORREN (Editors) MARINE POLLUTANT TRANSFER PROCESSES 3 0 A VOlPlOIEditor) THE BALTIC SEA ’ 3 1 E.K. DUURSMA and R. DAWSON (Editors) MARINE ORGANIC CHEMISTRY 32 J.C.J. NIHOUL (Editor) ECOHYDRODYNAMICS 33 R HEKlNlAN PETROLOGY OF THE OCEAN FLOOR

3 4 J.C.J. NIHOUL (Editor) HYDRODYNAMICS OF SEMI-ENCLOSED SEAS 3 5 B. JOHNS (Editor) PHYSICAL OCEANOGRAPHY OF COASTAL AND SHELF SEAS 3 6 J.C.J. NIHOUL (Editor) HYDRODYNAMICS OF THE EQUATORIAL OCEAN 3 7 W . LANGERAAR SURVEYING AND CHARTING OF THE SEAS _3 8 -J C NlHOUL (Editor) REMOTE SENSING OF SHELF SEA HYDRODYNAMICS 3 9 -T ICHIYE (Editor) OCEAN HYDRODYNAMICS OF THE JAPAN AND EAST CHINA SEAS 40 J.C.J. NIHOUL (Editor) COUPLED OCEAN-ATMOSPHERE MODELS 4 1 H. KUNZEDORF (Editor) MARINE MINERAL EXPLORATION 4 2 J.C.J. NIHOUL (Editor) MARINE INTERFACES ECOHYDRODYNAMICS 4 3 P. LASSERRE and J.M. MARTIN (Editors) BIOGEOCHEMICAL PROCESSES AT THE LANDSEA BOUNDARY 4 4 I.P. MARTINI (Editor) CANADIAN INLAND SEAS 4 5 J.C.J. NIHOUL and B.M. JAMART (Editors) THREE-DIMENSIONALMODELS OF MARINE AND ESTUARIN DYNAMICS 4 6 J.C.J. NIHOUL and B.M. JAMART (Editors) SMALL-SCALE TURBULENCE AND MIXING IN THE OCEAN 47 M.R. LANDRY and B.M. HICKEY (Editors) COASTAL OCEANOGRAPHY OF WASHINGTON AND OREGON 4 8 S.R. MASSEL HYDRODYNAMICS OF COASTAL ZONES 49 V.C. LAKHAN and A.S. TRENHAILE (Editors) APPLICATIONS IN COASTAL MODELING 5 0 J.C.J. NIHOUL and B.M. JAMART (Editors) MESOSCALE IN GEOPHYSICALTURBULENCE SYNOPTIC COHERENT STRUCTURES 5 1 G.P. GLASBY (Editor) ANTARCTIC SECTOR OF THE PACIFIC

5

~

Elsevier Oceanography Series, 52

GLOBAL ECOLOGICAL CONSEQUENCES OF THE 1982-83 EL NINO-SOUTHERN OSCILLATI0N Edited by

P.W. GLYNN University of Miami Rosenstiel School of Marine and Atmospheric Science Miami, Florida, U.S.A.

ELSEVIER Amsterdam - Oxford - New York -Tokyo

1990

ELSEVIER SCIENCE PUBLISHERS B.V. Sara Burgerhartstraat 25 P.O. Box 2 1 1 , 1000 AE Amsterdam, The Netherlands Distributors for the United States and Canada:

ELSEVIER SCIENCE PUBLISHING COMPANY INC 655, Avenue of the Americas New York, NY 10010, U.S.A.

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0Elsevier Science Publishers B.V., 1990 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the publisher, Elsevier Science Publishers B.V./ Physical Sciences & Engineering Division, P.O. Box 330, 1000 AH Amsterdam, The Netherlands. Special regulationsfor readers in the USA -This publication has been registered with the Copyright Clearance Center Inc. (CCC), Salem, Massachusetts. Information can be obtained from the CCC about conditions under which photocopies of parts of this publication may be made in the USA. All other copyright questions, including photocopying outside of the USA, should be referred t o the publisher. No responsibility is assumed by the Publisher for any injury and/or damage t o persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. This book is printed on acid-free paper. Printed in The Netherlands

Satellite infrared sea surface temperatures during the peak of the 1982-83 El NiiioSouthern Oscillation (above) and one year later (below). (Courtesy of R. Legeckis, National Oceanic and Atmospheric Administration.)

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vii

PREFACE AND ACKNOWLEDGEMENTS

As originally perceived, El Niiio referred to the warm current that sets southward each year off the coasts of southern Ecuador and northern Peru. At times, the El Niiio event is particularly strong and its influence may extend over much of the tropical and subtropical eastern Pacific region. The El Niiio is a local manifestation of the El Niiio Southern Oscillation (ENSO), a largescale dynamic interaction between the worlds major low-latitude atmospheric pressure centers and basin-wide thermocline/nutricline depths across the Pacific and Indian Oceans. Some of the more obvious effects of El Niiio in the eastern Pacific are (a) anomalous sea surface warming, (b) reduced upwelling or upwelling of nutrient-poor waters, (c) a marked decline in primary productivity and fisheries stocks, (d) intensified storms with higher sea levels, and (e) high rainfall with frequent flooding. These events usually begin soon after Christmas or near Epiphany, Three King's Day (late December to early January), hence the epithets El Niiio (Christ Child), "La Comente El Niiio", and "Los Dias de El Niiio". The 1982-83 El Niiio was exceptionally severe, and was probably the strongest warming of the equatorial Pacific Ocean to occur during this century and perhaps for several centuries before that. Not only was the Ocean warming intense, but it spread over large parts of the Pacific Ocean, penetrated to greater depths than usual, and lasted longer than many previously recorded El Niiio events. Beyond the unprecedented severity of the 1982-83 ENSO, new kinds of global disturbances to marine biota were observed during this period. For example, coral bleaching (a sudden whitening of corals because of the loss of endosymbiotic algae) and widespread coral mortality occurred in numerous areas that experienced ENSO related perturbations: (a) in the equatorial eastern Pacific, including the Galapagos Islands, (b) in the central and western Pacific, (c) in Indonesia, (d) in the Persian (Arabian) Gulf, and (e) in the tropical western Atlantic. Many eastern Pacific coral reefs that had experienced nearly uninterrupted growth for several centuries (until 1983) were devastated (95% - 98% mortality) by the initial impact of this disturbance and are now undergoing extensive bioerosion and little or no recovery. The marked deepening of the thermocline and the resulting trophic impoverishment of surface waters adversely affected numerous marine species that depend upon frequent nutrient replenishment and, directly or indirectly, on algal productivity. The consequent depletion of the plant food base resulted in significant reduction in stocks of zooplankton, bait fish, and squid. This led to a mass migration and near-total reproductive failure of marine birds at Christmas Island. Numerous species faced similar food shortages in the Galapagos Islands and along the mainland coast of Ecuador, Peru and Chile: albatrosses, boobies, swallow-tailed gulls, penguins, cormorants, marine iguanas, fur seals, and sea lions. The abnormally high sea levels and rough seas that accompanied El Niiio in the Galapagos Islands made feeding difficult for certain species that graze near shore, such as marine iguanas. Heavy winter seas uprooted giant kelps along the coast of southern California and the correspondingly high El Niiio sea temperatures during the following summer interfered with the reproduction and recruitment of kelps.

viii

Terrestrial species suffered from drought in Central American rainforests, and at the same time flooding occurred along the west coast of South America. Reduced rainfall extended to western North America where drought conditions were recorded in tree rings. Severe drought conditions in Indonesia spawned forest fires that resulted in extreme damage to the rainforest habitat. In contrast, heavy rainfall along much of the Peruvian coast had a beneficial effect on the flora of the Peruvian "lomas", resulting in a brief flushing of flowering plants. Because of the numerous species affected and its global impact, it is probably fair to include severe ENSO events among the greatest natural perturbations known on our planet. Certainly the 1982-83 ENSO is the most severe on record and comes at a time when attention is being focused on the long-term impact of changes in global climate. ENSO events dramatically show the atmosphere, ocean and land links, and how small changes in sea surface temperatures can alter global climate patterns affecting a vast array of the worlds biota. This recent global disturbance underlines the intricate physical and biotic connections in the biosphere and the fragility of many tropical ecosystems to climatic disturbances. Our efforts in this volume provide detailed documentation of how a large magnitude ENSO event disrupted biotic communities. These observations may allow us to evaluate future changes that result from general warming trends if the Antarctic ice-cap continues to decrease, sea level rise continues or other broad meteorological/oceanographicphenomena occur. Some of the titles of the contributions in this volume denote the occurrence of the ENSO event through 1984 since physical effects and biological responses were often observed at some locations later than 1983. Furthermore, some of the disturbances observed from 1982 to 1984 have continued for several years following the initial disturbance period. A seven year lag in reporting these findings was common, in large part purposeful, in order to assess the effects of the disturbance, as well as post-ENS0 (secondary) disturbances and recovery processes. Emphasis in this volume is placed on disturbances to (a) near-shore populations, (b) benthic communities, especially coral reefs, (c) extratropical regions, and (d) terrestrial communities, topics not yet addressed and integrated in a comprehensive treatment of the subject. For sources emphasizing particular areas affected in 1982-83, and for information on related topics, such as meteorology, physical oceanography, zooplankton, fisheries, and El Nifio in the ancient record, the reader is referred to the references listed at the end of the preface. The contributors to this volume were selected on the basis of their research involvement with the 1982-83 ENSO and expertise in their respective fields of study. All authors were encouraged to present original observations and data to support the topics under discussion. I am grateful to J. A. Brady, J. Espinosa, and M. S. Hart, Meteorological and Hydrographic Branch, Panama Canal Commission, for providing data and insight into the nature of Central American weather systems. D. Heuer, M. Brinkley and R. Suarez, Print and Photo Service, Rosenstiel School of Marine and Atmospheric Science, assisted in numerous ways to prepare camera-ready copies of manuscripts for printing. All contributions were reviewed by at least two anonymous referees and accepted papers were revised before the final printing. In cases involving controversial issues, I have allowed the authors an opportunity to express their views, therefore the conclusions of the various

IX

contributions are not necessarily in total agreement. I am very grateful for the time and care offered by the following who helped in the review process: William M. Balch, Edward A. Boyle, Larry E. Brand, Lee. E. Branscome, K. T. Briggs, Barbara E. Brown, William Burger, F. Chavez, Anthony G. Coates, Laura E. Conkey, Paul K. Dayton, Richard E. Dodge, C. Mark Eakin, J. R. Ehleringer, N. M. Ehrhardt, David B. Enfield, Joshua S. Feingold, A. Gentry, Robert N. Ginsburg, M. P. Harris, Mark E. Hay, Paul L. Jokiel, Cadi Katzir, Gary P. Klinkhammer, Merlin P. Lawson, Egbert G. Leigh Jr., Harris A. Lessios, Ian

G. Macintyre, Harold A. Mooney, William A. Newman, Daniel K. Odell, Donald B. Olson, Richard L. Phipps, Donald C. Potts, Joseph Powers, Stanley A. Rand, Ralph Schreiber, Stephen V. Smith, Steven M. Stanley, Tod F. Stuessy, Peter K. Swart, Alina M. Szmant, Mia J. Tegner, Fritz Trillmich, Geerat J. Vemeij, Gerard M. Wellington, Dagmar I. Werner, Henk Wolda, Klaus Wyrtki, and two anonymous reviewers. Nicholas Polunin and Robin Pellew offered encouragement and helpful advice during the formative stages of this project. Robert L. Goodman and Martin Tanke of Elsevier Science Publishers kindly provided the technical guidance needed to produce the contributions in this volume. I am pleased to acknowledge the help of Symma Finn who skillfully managed editorial matters and prepared the final camera-ready versions of several contributions. Kay K. Hale and Helen D. Albertson offered expert assistance with various literature problems. Thanks are also extended to June M. Eakin, Corell L. Lundy, Lois Reid, Nora I. Rodriguez and David B. Smith for help in the preparation of several manuscripts. I am especially appreciative of the labors of Jorge Cortes who ferreted out numerous errors in the final stages of preparation, and of June Eakin and Joshua Feingold who assembled the volume indexes. Selected references with major emphasis on the 1982-83 El Niiio event: Bibliografia Sobre El Fendmeno de El Niiio Desde 1891 a 1985, 1985. J. Mariategui, A. Ch. de Vildoso and J. VClez, Bol. Inst. Mar Peni, Spec. Vol., Callao, Peni, 136 pp. Boletin ERFEN (El Estudio Regional del Fendmeno de El Niiio), 1982-to date. R. Jordan (ed.), Comisidn Permanente del Pacifico Sur, Bogoti, Colombia. Ciencia, Tecnologia y Agresidn Ambiental: El Fendmeno El Niiio, 1985. M. Vegas (ed.), CONCYTEC Press, Lima, Peni, 692 pp. El Niiio, 1984. Oceanus, 27(2), Woods Hole Oceanographic Institution, Mass. 84 pp. El Niiio: An AGU Chapman Conference, 1987. J. Geophys. Res., 92(C13), 14,187-14,479. El Niiio en Las Islas GalBpagos: El Evento de 1982-1983, 1985. G. Robinson and E. M. del Pino (eds.), Quito, Ecuador: Fundacidn Charles Darwin para las Mas Galipagos, 534 pp. El Niiio North: Niiio Effects in the Eastern Subarctic Pacific Ocean, 1985. W. S. Wooster and D. L. Fluharty, Washington Sea Grant Program, University of Washington, Seattle, 312 pp. "El Niiio", Su Impacto en la Fauna Marina, 1985. W. E. Amtz, A. Landa and J. Tarazona (eds), Bol. Inst. Mar Perh, Spec. Vol., Callao, Peni, 222 pp. Taller Nacional Fenomeno El Niiio 1982-83, 1985. lnstituto de Fomento Pesquero, Invest. Pesq., 32, 254 pp., Santiago, Chile. Taller Sobre El Fenomeno de El Niiio 1982-83, 1984. Comisidn Permanente del Pacifico Sur. Rev. Pacifico Sur, 15,423 pp., Quito, Ecuador. Tropical Ocean-Atmosphere Newsletter, 1983 and 1984. Special issues 1-111, no's. 16.21, and 28.

November 1989 Peter Glynn

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xi CONTENTS Preface and Acknowledgements ....................................................................................................... List of Contributors .......................................................................................................................... PHYSICAL ASPECTS OF THE EL NIRO EVENT OF 1982-1983 D.V. Hansen ...................................................................................................................................

vii xix

1

Introduction ....................................................................................................................... The Global View Some Historical Perspective .............................................................................................. Development of the Event of 1982-1983 ............................. References ..........................................................................................................................

3 4 6 19

NUTRIENTS AND PRODUCTIVITY DURING THE 1982/83 EL NIRO R.T. Barber and J.E. Kogelschatz ..................................................................................................

2I

Introduction ........... ........ ........................................................................ ............................ The Enso Cycle ................................................................................................................... The Basinwide Setting Western Pacific .................................................................................................................. Eastern Pacific Normal Conditions. 5.1 The Equatorial Region .......................................................................................... 5.2 The Coastal Region ............................................................................................... Eastern Pacific Anomalous Conditions 6.1 The Equatorial Region .......................................................................................... 6.2 The Coastal Region Productivity Effects of El Niiio .......................................................................................... 7.1 The Equatorial Region .......................................................................................... 7.2 The Coastal Region .................... Conclusions ......... ......... ........... ................... ........... ............................................. .......... ...... References

21 22 26 28 30 30 32 35 35 39 43 43 43 49 50

CORAL MORTALITY AND DISTURBANCES TO CORAL REEFS IN THE TROPICAL EASTERN PACIFIC P.W. Glynn ....................................................................................................................................

55

Introduction ....................................................................................................................... Coral Bleaching, Mortality and Environmental Correlates ................ 2.1 Onset of the 1982-83 Disturbance .... .................................... 2.2 Extent ofthe 1982-83 Disturbance ...................................................................... 2.3 Condition of Bleached Corals ...... 2.4 Coral Bleaching and Sea Water Temperature Extremes ....................................... 2.5 Reliability of Sea Surface Temperature Observations .......................................... 2.6 Sea Warming and the Timing of Coral Bleaching 2.7 Further Evidence Implicating Sea Warming as th 2.8 Spatial and Temporal Occurrences of El Niiio Warming Events ......................... 2.9 Coral Bleaching and Mortality During Cooling Episodes 2.10 Non-thermal Stressors and Coral Bleaching ......................................................... Community Effects ............................................................................................................ 3. I Immediate Effects ...... 3.2 Long-term Effects ................................................................................................. 3.2. I Coral Community Changes ................................ 3.2.2 Responses and Impacts of Corallivores ............................... .............. ..... 3.2.3 Responses and Impacts of Herbivores ....................................................

55 59 59 60 63 68 70 71 75 77 81 83 87 87 94 94 96 98

1.

2. 3. 4.

1.

2. 3. 4. 5. 6. 7.

8.

I. 2.

3.

1

xii 4. 5.

6.

Interrupted Coral Growth and Reef Framework Accumulation: Indicators of Severe Event Occurrences ................................................................................ Discussion and conclusions ........................................................ 5.1 Sea Warming as the 5.2 El NiAo 1982-83 Compared with Other Disturbance 5.3 Prospects for Coral Reef Recove ry................ 5.4 Predicted Effects of Greenhouse Global Warming Summary ............................................................................. References ..........................................................................................................................

i02 107

1 16 I 17

THE EFFECTS OF THE EL NIRO/SOUTHERN OSCILLATION ON THE DISPERSAL OF CORALS AND OTHER MARINE ORGANISMS 127 R.H. Richmond .......................................................................................................................... 1..

I.

Introduction .................. 2.1 2.2

3. 4.

5.

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

....

The North Equatorial Countercurrent ................................................................. The North Equatorial Current ........................

2.4 The Equatorial Undercurrent Oceanic Currents During tbe 1982-83 Transport of Marine Organisms in Oce 4.1 Transport During Non-El Niii

............................ rrents .......................................................

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

Conclusions ............................................................... References ......................................................,...................................................................

CORAL MORTALITY OUTSIDE OF THE EASTERN PACIFIC DURING 1982-1983: RELATIONSHIP TO EL NIRO M.A. Coffroth, H.R. Lasker and J.K. Oliver .............................................................................. I.

2.

3.

4.

127 128 129 129 130 130 130 132 132 134 137 138

...... 141

........................ Introduction ................... Causes of Coral Bleaching and Mortality ............................................................. I. I ENS0 and Coral Mortality ....................................................... ...................... 2. I Eastern Pacific .......................................... .................................. 2.2 Central Pacific .. .................................. 2.3 Western Pacific. .................................................................. 2.4 Indian Ocean/A 2.5 Caribbean Sea ........................................... ......................... Detailed Case Study 3. I Extent and Timing of Bleaching ........................................................................... 3.2 Oceanographic and Meteorological Data ............................................................. (i) Seawater Temperatures ............ ................................................... (ii) Solar Radiation .................. ................................................... (iii) Wind Speed and Direction. (iv) Rainfall ........................................ (v) Interactive Effects ................................................................................... 3.3 Relationship to El NiAo .................... Detailed Case Study - San Blas Islands, Panama ............................................................... ...................... .................................. Extent and Timing of Bleaching 4. I

(iii)

Solar Radiation ..

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

142 142 146 146 146 148 149 151 152

153 155

155 156 158

159 159 161 161 161 162 163 164 164

...

Xlll

(iv) Wind Speed and Direction ...................................................................... (v) Rainfall and Salinity .................. Relationship to El Niiio ........................................................................................

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

165 i67 169 171 177

EL NIRO AND THE HISTORY OF EASTERN PACIFIC REEF BUILDING M.W. Colgan ................................. .................................................................

183

4.3

Introduction .................................... ................................... Background ........................................................................................................................ 2.1 Eastern Pacific -Physical Setting and Reefs ........................................ 2.2 Past Eastern Pacific Reefs .................................................................................... The 1982-1 983 El Niiio Event and Eastern Pacific Reefs Evidence for Past El Niiio Events ....,......,......................................,.................,....... 4.1 Historical and Proxy Rec .............,......,.........................,...,..... 4.2 Holocene Record, Sedimentological Evidence ..................................................... Ocean Conditions and Past El Niiio Events ...................................................................... Uwina Bay, Galhpagos Islands ............. 6.1 El Niiio Events at Urvina Bay .............................................................................. 6.1.1 Branching Corals ......................................... 6. I .2 Massive Corals ........................ 6.2 Summary Remarks ............................................................................ Discussion ........................,.................. ................ Conclusion ............................................................................................... References ...................,....,..........................,........,.,...........................

198 20 I 202 203 21 1 214 216 218 220

REEF-BUILDING CORALS AND IDENTIFICATION OF E N S 0 WARMING EPISODES E.R.M. Druffel, R.B. Dunbar, G.M. Wellington and S.A. Minnis

233

I. 2.

3. 4.

5. 6.

7. 8.

184 187 187 189 192 196 196 196

Introduction ....................................................................................................................... I. 1 Characteristics of Skeletal Growth in Symbiotic Corals I .2 Effects of Physical Factors on Coral Growth ....................................................... I .3 Effects of Physical Factors on Skeletal Chemistry and Isotopes Study Sites .......................................................................................................................... Methods ................................... .............................................. Stable Isotope Records in Corals ....................................................................................... 4.1 6I8OResults. 4.2 6I3C Results Conclusions ........................................................................................................................ References .................

233 234 235 237 238 24 I 242 243 247 249 250

TRACE ELEMENT INDICATORS OF CLIMATE VARIABILITY IN REEF-BUILDING CORALS G.T. Shen and C.L. Sanford

255

I.

2. 3. 4. 5.

I. 2. 3.

Introduction MinorandT ........................................................... Sample Sites ....................................................................................................

5.

Oceanic Markers of El Niao ............................................................................................... 5. I Upwelling in the Eastern Equatorial Pacific ........................................................ 5.2 Precipitation in the Western Tropical Pacific River Discharge and Circulation in the Caribbean Sea........................................ 5.3

255 256 260 26 1 26 I 26 1 269 272

xiv 6.

Conclusions ........................................................................................................................ References ......,......................,............................................................................................

277 278

HISTORICAL ASPECTS OF EL NIRO/SOUTHERN OSCILLATION - INFORMATION FROM TREE RINGS J.M. Lough and H.C. Fritts ......................................................................................................... ... 285

3. 4.

.................... Site selection and Sample Collection .................. 2. I Crossdating and Measuring ............... .............................................. 2.2 ..................................... 2.3 Chronology Development .................. 2.4 Climatic Reconstruction ........................................................ Tree Rings and the Southern Oscillation: An Example Application ... 3. I Teleconnection Patterns in Dendroclimatic Reconstructions 3.2 Reconstruction of an Index of the Southern Oscillation ...................... ....................................................... Future Directions ....................... 4. I Northern Hemisphere Extra-tropics ......................... 4.2 Tropical Regions ...................... .......................................................... ,.................... .................................

285 287 288 289 289 290 29 I 29 1 298 307 307 309 310 312 314

EFFECTS OF EL NIRO 1982-83 ON BENTHOS, FISH AND FISHERIES OFF THE SOUTH AMERICAN PACIFIC COAST 323 W.E. Arntz and J. Tarazona .......................................................................................................... I. 2. 3.

4.

5.

Introduction ................................................................... Principal Abiotic Changes Induced by EN 1982-83 ......................................................... The Pelagic Subsystem ......................................... 3. I Phyto- and Zooplankton ....................................................................................... ............................................. 3.2 Pelagic Fish ........................ 3.3 Pelagic Fisheries ......................... .............. .................................... .... ............................ .................................. The Benthic Subsystem 4.1 Macrobenthos .................................................... 4.1.2 Soft Bottom 4.2 Exploited Inverte 4.3 Demersal and Co Conclusions ................................................

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

324 325 329 329 330 333 336 336 336 339 342 347 350 353

EFFECTS OF THE 1982-83 EL NIRO-SOUTHERN OSCILLATION EVENT ON MARINE IGUANA (AMBLYRHYNCHUS CRZSTATUS BELL, 1825) POPULATIONS ON GALAPAGOS W.A. Laurie ................................................................................................................................... 361 2.

Study Area ..........................................................................................................................

.......,...................

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

3.2 3.3 3.4 3.5 3.6

Capturing and Marking Iguanas ........................................................................... Observations of Reproductive Behaviour ................ ....................... ,............... Measurements of Iguanas ..................................................................................... Growth Rates ........................................................................................................ Survival Rates.

36 I 364 364 364 364 365 365 366 366

xv

4.2

.................................... .................................. ........................... Changes in Algal Flora ..............................................

5.2 5.3 5.4

....................... t Competition for Food .................................. Growth Rates and Age at First Reproduction ................................. ........,........................ Dominant Cohorts ........................................ .................................... .......... Costs of Breeding

Results .............................

I..

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

References.. .......................

THE GULF OF PANAMA AND EL NIRO EVENTS THE FATE OF TWO REFUGEE BOOBIES FROM THE 1982-83 EVENT N.G. Smith .....................................................................................................................................

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

2. 3. 4. 5.

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

t

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

Natural History of the Boobies ....................................... ................. ......................... The Occurrence ........................ El Niiio Events and the Gulf of Panama ................................................ ........,..................................... Concluding Remarks .............................

...................................,........................................

SEABIRDS AND THE 1982-1984 EL NIRO/SOUTHERN OSCILLATION ............................................................... D.C. Duffy ......................

366 366 367 369 37 I 372 373 375 311 371 378 378 378 319

381 38 I 38 I 383 389 391 392 395

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

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

395 396 396 396 391 398 400 40 1 402 403 403 404 405 406 408 410

EL NIRO EFFECT ON SOUTH AMERICAN PINNIPED SPECIES D. Limberger ..............................................................................................

4 I7

Introduction ......................................................................................... Galapagos Fur Seal. .............................................................................................

419

How El Niiio Affected the Galapagos Fur Seal .................. After Effects of El Niiio, During the Reproductive Season of 1983.....................

422

1.

Introduction

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

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

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

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

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

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

...........

References ....................................................

1.

2.

2.2 2.3

xvi 3.

4. 5.

South American Fur Seal .......................................................................... 3. I General Information ................................................................... ........ 3.2 El Niiio’s Effect on the South American Fur Seal at Punta San J How the Sea Lions in Galhpagos and Punta San Juan Survived the El Niiio Event ......... .................................... 4. I The Galapagos Sea Lion ....................... 4.2 South American Se Summary and Conclusions ..................................... ................................ References ...........................................................................

424 424 425 426 426 427 428 430

BOTTOMS BENEATH TROUBLED WATERS: BENTHIC IMPACTS OF THE 1982-1984 EL NIRO IN THE TEMPERATE ZONE P.K. Dayton and M.J. Tegner ........................................................................................................ 433

I. 2. 3.

4.

5. 6.

Introduction .............................................................................................. 1.1 Nort re Temperate El Niiios: A summary of Physical Factors ..... Biological Effects of the 1982-84 El Niiio on Temperate Pelagic Ecosystems ................... ............................. 2. I Northeastern Pacific ....... 2.2 California ............................................ .................................................................. ENSO Effects on Kelp Forests .................................................................... .......... Effects of the Storms ............................ 3. I Effects of the Warm Water ................................................................................... 3.2 .................................................. 3.3 Other California Kelp Habitats ENSO Impacts on Kelp Forest Animals ............................................. 4. I Sea Urchins ........................................................................................................... .................. 4.2 Abalones ..

.............................................. 4.4 Kelp Forest Fishes Non-kelp Benthic Systems ............................................................ 5.2 ENSO Effects on Intertidal Populations Discussion .......................................................................................................................... .......................................... 6. I Other ENSOs 6.1.2 6. I .3

7.

Japan ....................................................................................................... South Africa ...............................

Conclusions References ......................................... .... . ... . ..

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

THE IMPACT OF THE “EL NIRO” DROUGHT OF 1982-83 ON A PANAMANIAN SEMIDECIDUOUS FOREST E.G. Leigh, Jr., D.M. Windsor, A. Stanley Rand and R.B. Foster ................................................ I. 2. 3.

Introduction ....................................................................................................................... The Severity of the El Niiio Drought . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........ The Impact Upon Plants of the El Niiio Drought 3. I Signs of Stress ....................................................................................................... 3.2 Mortalit .............................................................................. ..........

..... 4. 5.

3.4 Long-term Effects on the Forest ........................................................................... The El Niiio Drought and Animal Populations ................................................................. Concluding Remarks .......................................................................................................... References ..........................................................................................................................

433 434 436 436 438 44 1 442 443 447 450 450 452 453 454 456 456 458 460 460 460 460 46 I 462 464 466

473 473 475 476 476 476 478 479 480 482 484

xvii THE BOTANICAL RESPONSE ON THE ATACAMA AND PERUVIAN DESERT FLORAS TO THE 1982-83 EL NIRO EVENT M.O. Dillon and P.W. Rundel ....................................................................................................... 487 I. 2. 3. 4. 5. 6. 7

Introduction .................................................... Lomas Form ............................................ Coastal Climate .................................................................................................................. Impact of Former Intense El Niiio Events. 1982-83 El NiRo Event ...................................................................................................... Botanical Response to 1982-83 El Niiio Event 6 .I Coastal Peru and Northern Chile ......................................................................... 6.2 Galapagos Islands ................................................................................................. Conclusions. ............................ ....................................................... References ..........................................................................................................................

487 488 49 I 493 494 495 495 498 50 I 503

AN ECOLOGICAL CRISIS IN AN EVOLUTIONARY CONTEXT: EL NIRO IN THE EASTERN PACIFIC

......................................... I. 2. 3.

505

Introduction ...... ENS0 as a Model For Extinction Events ........................................................................... Extinction in the Eastern Pacific ...........................

506

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

51 5

INDICES Subject Index ................................................................................................................. Systematic Index .................................................................... Geographic Index ...............................................................................................................

554

This Page Intentionally Left Blank

XIX

LIST OF CONTRIBUTORS

W. E. ARNTZ

Alfred-Wegener-Institut fur Polar- und Meeresforschung, Columbusstrasse, D-2850 Bremerhaven, Federal Republic of Germany

R. T. BARBER

Monterey Bay Aquarium Research Institute, Pacific Grove, California 93950

M. A. COFFROTH

Division of Marine Biology and Fisheries (formerly Division of Biology and Living Resources), Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149; present address: Department of Biological Sciences, State University of New York at Buffalo, Buffalo, New York 14260

M. W. COLGAN

Earth Sciences Board, University of California, Santa Cruz, California 95064; present address: Department of Geology, College of Charleston, Charleston, South Carolina 29424

P. K. DAYTON

Scripps Institution of Oceanography, A-001, La Jolla, California 92093

M. 0.DILLON

Department of Botany, Field Museum of Natural History, Chicago, Illinois 60605-2496

E. R. M. DRUFFEL

Department of Chemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543

D. C. DUFFY

Institute of Ecology, University of Georgia, Athens, Georgia 30602

R. B. DUNBAR

Department of Geology and Geophysics, and Earth Systems Institute, Rice University, Houston, Texas 77251-1892

R. B. FOSTER

Department of Botany, Field Museum of Natural History, Chicago, Illinois 60605-2496 (mailing address); and Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama.

H. C. FRITTS

Laboratory of Tree-Ring Research, University of Arizona, Tucson, Arizona 85721

P. W. GLYNN

Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149-1098

D. V. HANSEN

NOAA (National Oceanic and Amiospheric Administration)/Atlantic Oceanographic and Meteorological Laboratory, 4301 Rickenbacker Causeway, Miami, Florida 33149; and Cooperative Institute for Marine and Atmospheric Studies, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33 149

J. E. KOGELSCHATZ

Monterey Bay Aquarium Research Institute, Pacific Grove, California 93950

H. R. LASKER

Department of Biological Sciences, State University of New York at Buffalo, Buffalo, New York 14260

xx

W. A. LAURIE

Max-Planck-Institut fur Verhaltensphysiologie, 8131, Seewiesen, West Germany; present address: Large Animal Research Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom

E. G. LEIGH, JR.

Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama; mailing address: Smithsonian Tropical Research Institute, APO Miami 34002-0011 USA

D. LIMBERGER

13, Frayne Road, Ashton Gate, Bristol BS3 IRU, United Kingdom

J. M. LOUGH

Australian Institute of Marine Science, PMB No. 3, Townsville M. C., Queensland, Australia

S. A. MINNIS

Department of Geology and Geophysics, and Earth Systems Institute, Rice University, Houston, Texas 77251-1892

J. K. OLIVER

Sir George Fisher Centre for Tropical Marine Studies, James Cook University of North Queensland, Townsville, Queensland 48 11, Australia

A. S. RAND

Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama; mailing address: Smithsonian Tropical Research Institute, APO Miami 34002-001 1 USA

R. H. RICHMOND

Marine Laboratory, University of Guam, UOG Station, Mangilao, Guam 96923 USA

P. W. RUNDEL

Laboratory of Biomedical and Environmental Sciences, and Department of Biology, University of California, Los Angeles, California 90024

C. L. SANFORD

Lamont-Doherty Geological Observatory of Columbia University, Palisades, New York 10964

G. T. SHEN

Lamont-Doherty Geological Observatory of Columbia University, Palisades, New York 10964; present address: School of Oceanography, WB-10, University of Washington, Seattle, Washington 98195

N. G. SMITH

Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama; mailing address: Smithsonian Tropical Research Institute, APO Miami 34002-001 1 USA

J. TARAZONA

Grupo DePSEA, Facultad de Ciencias Biologicas, Universidad Nacional Mayor de San Marcos, Apartado 1898, Lima 1000, Peru

M. J. TEGNER

Scripps Institution of Oceanography, A-001, La Jolla, California 92093

G. J. VERMEIJ

Department of Geology, University of California, Davis, California 95616

G. M. WELLINGTON

Department of Biology, University of Houston, Houston, Texas 77204-5513

D. M. WINDSOR

Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama; mailing address: Smithsonian Tropical Research Institute, APO Miami 34002-001 1 USA

1

PHYSIC?&

ASPECTS OF THE EL NIfiO EVENT OF 1982-1983

DONALD V. HANSEN NOAA/Atlantic Oceanographic and Meteorological Lab., 4301 Rickenbacker Causeway, Miami, Florida 33149 (USA), and Cooperative Institute for Marine and Atmospheric Studies, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149 (USA)

ABSTRACT Hansen, D.V., 1989. Physical aspects of the El Nifio event of 1982-1983. El Nifio events are marked by the appearance of anomalously warm ocean waters and unusual rainfall in normally arid coastal regions of Ecuador and Peru. During the past century such events have occurred at about four-year intervals on average, and nine of the events have been described as strong or very strong. In the spring of 1982 the heavy rainfall that normally characterizes the IndoPacific archipelago began to shift eastward toward the central Pacific. During the following year the region of anomalous rainfall traversed the ocean to the coast of South America, in phase with anomalous winds, currents, and sea surface temperatures. At the peak of the event in the eastern tropical Pacific, Peru and Ecuador experienced record-setting rainfall leading to flooding and avalanches, near surface ocean currents reversed from their normal direction, sea surface temperature rose t o 5 O C or more above normal, the thermocline plunged to 100 meters or more below normal, and sea level rose to nearly half a meter above normal. Upon reaching the coast, many of the oceanic perturbations propagated poleward along the continenal margins in both hemispheres, carrying the signs and effects of El Nifio to middle and high latitudes in the Pacific. The magnitude of this event made it the "event of the century" in most variables, and the event of several centuries in some. The magnitude of perturbation of the atmosphere in the tropical Pacific sector certainly carried anomalies also in distant regions of the atmosphere, and thereby secondarily in other parts of the ocean. At greater distance, however, it becomes increasingly difficult to distinguish between anomalies resulting from El Nifio and those arising from other kinds of variations of the atmospheric circulation. 1 INTRODUCTION A century or more ago, sailors in and around the port of Paita, on the northern coast of Peru, knew of a warm coastal current that flowed southward along the coast during most (Southern Hemisphere) summers. Because it usually appeared around Christmas time, Los Dias del Nifio, or the Days of the (Christ) Child, they termed it Corriente del Nifio, or El Nifio Current. This current and its warming influence are highly irregular in their occurrence. In some years they may not appear at all, but usually some of the tropical surface water that is always found north of the equator will be carried southward to the coast of Peru. At irregular intervals of a few years there is such massive intrusion of warm tropical waters into the coastal region and a change from the usual desertlike climate to moderate or heavy rainfall as to suggest that these extreme changes are something more than a particularly strong manifestation of the

2

seasonal cycle. It is these often dramatic events at several year intervals that the term El NiHo has been used to identify in recent decades. During the present century of relatively complete and reliable information, nine strong and 14 moderate events have been documented (Quinn g @., 1987). Thus, in the recent global climate regime, El Nifio events have occurred at about four-year intervals on average, and strong events have occurred about once a decade. These average intervals do not, however, imply regularity. No events occurred between 1943 and 1951, but three, including one strong event, are documented during 1939-1943. Although El Niiio is frequently thought of as an oceanic phenomenon, connection to the atmosphere is suggested by the association of unusual rainfall with El Nifio in those places where the phenomenon is most strongly manifest. Interannual variations of atmospheric patterns were documented by Sir Gilbert Walker in connection with studies of the variations of the Indian monsoons. Walker and Bliss (1932) described large-scale atmospheric pressure changes or "swings" over the southeastern Pacific and Indian Oceans that they called the Southern Oscillation. When pressure is high over the Pacific Ocean it tends to be low over the Indian Ocean, and conversely. Rainfall varies in the opposite

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Fig. 1. Historical record of atmospheric pressure variations at Tahiti and Darwin, Australia, and coastal temperature variations at Callao, Peru. Curves show 12-month running average of data.

3

direction to the air pressure. The intimate connection between these largescale pressure changes and sea surface temperature variations in the region of historic El Niao variations is illustrated in Fig. 1. The connection between the El Nifio and the Southern Oscillation as manifestations of the same large-scale, air-sea interaction process appears first to have been pointed out by Bjerknes (1969). He pointed out that the tradewind system over the tropical Pacific Ocean both sustains and is driven in part by the large-scale gradient of surface temperature, cold in the east and warm in the west. Warm water is normally driven westward by the surface winds. Warm surface waters in the west promote ascending motion and convective rainfall there, and the cold surface in the east promotes subsidence and stability in the atmosphere. It follows that if either the atmospheric or the oceanic part of this system is significantly perturbed, that perturbation is communicated to the other part and, therefore, may be sustained or amplified. 2 THE GLOBAL VIEW It is a familiar fact that tropical regions of the earth are more strongly heated by the sun than are the higher latitudes. The tropics, in fact, receive an excess of heat energy over what is locally radiated back into space, while the higher latitudes have a local deficit of radiative energy. The imbalance of radiative heating drives movements of the atmosphere and the ocean. These motions in turn carry heat from low latitudes to higher latitudes, thus maintaining the thermal regime of the earth within normal bounds, and in the process producing weather. All parts of the tropics are not the same in the process, however. Solar radiation is not particularly effective in directly heating the atmosphere. A substantial part of the solar radiation passes through the atmosphere to the surface of the earth where it is transferred to the atmosphere by several secondary processes. One of the most important of these is the evaporation of surface water and subsequent release of latent heat of evaporation when this water condenses as rainfall. Hence, those parts of the tropical atmosphere where the most convection and precipitation occurs are most strongly heated. In the normal (non-ENSO) situation the greatest tropical precipitation tends to occur over the continents, the Amazon Basin and equatorial Africa, and probably for reasons of symmetry and scaling, over the "island continent" of the IndoPacific region (Fig. 2a). These three regions of strong heating of the atmosphere may be thought of as the fire-boxes that energize the circulation of the atmosphere, and through that the ocean. Their locations establish the normal patterns of the general circulation of the atmosphere and the ocean. Probably due to the mobility and thermal properties of its ocean fraction, the island continent in the Indo-Pacific region is less effective at confining the location of precipitation than are the true tropical continents. Perturbations of the atmosphere or the ocean that lead to unusual warming in the central

4

or eastern Pacific can cause the precipitation and heating of the atmosphere to move eastward also (Fig. 2b). Furthermore, the new arrangement tends t o be self-sustaining, as pointed out by Bjerknes and described in more detail with the help of mathematical models (cf. Gill and Rasmusson, 1983). When the largescale pattern of tropical heating that drives the atmospheric circulation is changed so substantially, it is to be expected that the state and circulation of both the atmosphere and the ocean will change globally.

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Fig. 2. Schematic representation of regions of strong tropical rainfall during (a) non-Nifio periods and (b) El Nifio periods. 3 SOME HISTORICAL PERSPECTIVE In-depth research on the historical El Nifio events has been published by Quinn _ et -al. (1978),Woodman (1984), and Quinn &. (1987). Information from the time prior to about 1950 is mostly inadequate to allow much more than identification of events and a general evaluation of their relative strength. Major events during the last century occurred in 1891, 1899-1900, 1911-1912, 1917, 1925-1926, 1932, 1940-1941, 1957-1958, 1972-1973, and 1982-1983. The 1891 event is relatively well described by Eguiguren (1894). Peterson (1935) gives a good account of the 1925-1926 and 1932 events, Both of the above investigators describe primarily meteorological manifestations of the events, but noted the

5

association with high ocean temperatures. Schott (1931) provided the first extensive description of the offshore character of El Nifio, based on observations of the 1925-1926 event. Woodman (1984) concluded from study of mostly rainfall and river flow data and descriptive accounts of events prior to 1925 that 1983 was by far the rainiest year in northern Peru of at least the last 200 years, and quite possibly the rainiest year of the 450 year history of the region. At the surface of the earth ( o r ocean) the changes across the tropical Pacific associated with El Nifio or ENSO warm events appear as decreased rainfall in and around Indonesia, and increased rainfall in the central and eastern Pacific Ocean and coastal regions of tropical South America. Changes in the strength and even in direction of the southeast tradewinds over the Pacific Ocean accompany the changes in the pattern of convection and rainfall. These changes can be expected to exert influences also in the more distant tropics and in higher latitudes. The atmosphere is subject to numerous other influences, however, so that the more distant changes do not appear with the same clarity as those in the tropical Pacific. In most cases they appear as statistical correlations within which counter examples occur frequently. One most investigated distant influence is the Pacific-North American pattern, or PNA, which frequently occurs in the Northern Hemisphere winter in association with ENSO warm events. The PNA is characterized by high atmosphere pressure and warm dry weather over the western half of the continent, and low pressure with unusually low temperatures over the eastern half. Yarnal and Diaz (1986) found that the PNA pattern developed in winter months during 54 percent of the ENS0 warm events during the 32 years from 1947 to 1979. However, it also occurred during 22 percent of the non-warm event winters, which comprised more than half of the occurrences of the PNA pattern, but not at all during the cold event antithesis of El Nifio. A pattern opposite in sense to the PNA was found to occur during half of the ENSO cold events, and at least once during a warm event. Many attempts have been made to explain this variety of experience in regards to the more distant aspects of the El Nifio in the tropical Pacific. Pan and Oort (1983), for instance, found evidence that details of the sea surface temperature anomaly pattern are critically important for distant influences. In particular, they found that variations of global wind and atmospheric temperature are most closely related to sea surface temperature anomalies near longitude 130 degrees west. Hamilton (1988), on the other hand, provides evidence that the PNA pattern tends to occur in association with El Niiio when sea surface temperature in the far western tropical Pacific is also anomalously warm, or at least not overly cold. Some of the distant correlates of El Nifio are surprising. Andrade and Sellers (1988), for example, found a positive correlation between El Nifio and rainfall in Arizona and western New Mexico during spring and a u t m , but not during winter or summer. The explanation seems to be that El Nifio is but one of many influences upon the global atmosphere. During any particular event the

other processes may reinforce or obliterate the distant influence of El Nifio. Climate anomalies observed in other ocean basins during El Nifio can result from anomalous surface wind in those regions. The wind anomalies may or may not be "caused" by the El Nifio. Because the ENS0 event of 1982-1983 was extraordinarily strong, its influence on distant regions may have been uncommonly strong. It should not be assumed, however, that all unusual aspects observed during this time are due to El Nifio. The PNA pattern, for example, did not develop in this winter. It has been remarked in several reports that the El Nifio event of 1982-1983 was unusual. It also has become popular to point out that no two El Nifio events are the same, but a useful description of a typical warm event was provided by Rasmusson and Carpenter (1982) on the basis of data from the seven most significant warm episodes between 1950 and 1973. They superposed data from these seven events by month of the years of onset and maximum development. One of the most familiar aspects of El Nifio is the anomalous warming of the ocean along the coast of Peru. The evolution of ocean temperature anomalies in this region during 1982-1983 is shown in Fig. 3 in comparison to that of the preceding seven events. In this measure, the event of 1982-1983 began several months earlier than the envelope of prior events, and had exceptional amplitude, but followed the pattern of previous events in the timing of its maximum development. Perhaps the major difference in timing compared to the previous events was the appearance of a secondary maximum about half a year in advance of the main peak and the rapid return to normal immediately following the main peak. Most previous events have been characterized by a rapid development of the major maximum, and several have contained a secondary maximum about half a year following the time of maximum anomaly. Some reporters (cf. Taft, 1985; Nicholls, 1987) have chosen to center the chronology of the event of 1982-1983 on 1982 rather than 1983, which brings the initial peak of this event into phase with the secondary peak in some previous events. The best overall comparison between dissimilar events appears to be as shown in Fig. 3, however. 4 DEVELOPMENT OF THE EVENT OF 1982-1983

In addition to its magnitude, the El Nifio event of 1982-1983 was exceptional in that it was the best observed event in history. Information on earlier events was mostly limited to reports from merchant ships, coastal sea level and temperature observations, as well as terrestrial rainfall. During the 1982-1983 event, there were in addition, information on oceanic precipitation, winds, and sea surface temperature from weather satellites. Also, there were in progress some scientific investigations of various aspects of the air-sea interaction, processes associated with El Nifio. In connection with these scientific investigations, observations being made from merchant vessels had been augmented by observations of subsurface temperatures.

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Fig. 3 . Evolution of SST anomalies off the coast of northern Peru during several prior events (thin lines) and during events of 1982-1983 (heavy line). Fig. 4 shows the development of the SST anomaly across the equatorial band of the Pacific Ocean during the same three-year period spanning the 1982-1983 event as shown in Fig. 3. In these data it appears that the first peak of SST anomalies associated with the event developed almost simultaneously everywhere east of the international dateline, and had their maximum development between longitudes llOnW and 14OOW. The principal peak of the SST anomaly shown in Fig. 3 developed near the coast and progressed westward, more or less in accord with

8

the description by Rasmusson and Carpenter (1982). Although this second peak was the strongest of the event at the coast, it is not recognizable westward of about 120"W longitude. Thus, while an observer near the coast would say that the peak of the event was in May-June 1983, an offshore observer of SST would say that the maximum anomaly had passed during December 1982. It is clear that the event is more complicated than a simple movement of anomalies on or offshore. If only the more sparse observations of prior events had been made of the 1982-1983 event, much of the early weaker but spatially more extensive SST anomaly maximum might have been missed. It is presently still not clear whether the development of this event is very unusual. Its amplitude, of course, was extraordinary.

Fig. 4. Time-longitude plot of average SST anomaly in S0N-5"S band across the tropical Pacific. Contours are in decidegrees C. (From CAC, 1984.) As mentioned earlier, the warming of surface water in the central and eastern tropical Pacific tends to draw atmospheric convection and rainfall away from its normal position in the far western Pacific. The associated cloudiness is evident in satellite cloud pictures, and is quantified and archived as outgoing longwave radiation (OLR). Cloud tops are colder than the underlying earth surface and atmosphere and, therefore, they emit less radiative energy. Anomalously cloudy areas are revealed by negative OLR anomalies. Fig. 5 shows the evolution of convection and rainfall across the tropical Pacific during the event of 1982-1983. Early 1982 was near normal, with slightly more than normal rainfall (negative OLR anomalies) in the far western Pacific, and negligible anomalies elsewhere. During the second half of 1982 the western Pacific became

9

Fig. 5. Time-longitude plot of outgoing longwave radiation anomaly (W m-*) in 5ON-5OS band across the tropical Pacific. (From CAC, 1984.) anomalously dry as the region of cloudiness and precipitation moved eastward until by January-March 1983 the entire region west of the international date1 ne was unusually dry and all to the east was rainy. The largest OLR anomalies occurred in February near 150°W. Somewhat weaker, but still large, OLR anomalies continued moving eastward, reaching the coast in April-May. During the summer the rainfall distribution rapidly returned to normal, even became drier than normal near the dateline. The global distribution of tropical and subtropical cloudiness and rainfall during the Northern Hemisphere spring (March-April-May) of 1983 is shown in Fig. 6. Regions of heavy rainfall are manifest as areas of minimum OLR over the Amazon Basin and the Congo region of Africa. The region of heavy rainfall that usually lies across the Indo-Pacific island region, however, is displaced to the central Pacific. Subsequently, the region of heavy rainfall shifted even farther eastward, heavily impacting Ecuador and northern Peru. The annual flow of the Piura River in northern Peru affords a sensitive indicator to the meteorological impact of El Nifio in this normally arid region. Fig. 7 shows the annual discharge of this river since 1952. A l l of the El Nifio event years identified by Rasmusson and Carpenter (1982) (cf. Fig. 3), except the weak to moderate events in 1963 and 1969, stand out as wet years having four to ten times the discharge of the intervening years. In 1983, in turn, the river discharge was more than five times that of 1953, the second ranking year during this thirty-two year period. These extraordinary rains had devastating terrestrial effects, and doubtless contributed to low surface salinity in the oceanic region as well.

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Fig. 8. Time-longitude plot of westerly wind anomaly ( m s - l ) in 5ON-5'S across the tropical Pacific. (From CAC, 1984.)

band

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Associated with the displacement of the precipitation pattern was an alteration of the winds over the ocean surface. The normal wind over the equatorial Pacific Ocean is the southeast tradewind blowing generally westward. On a daily or even a monthly basis the surface winds over much of the tropical ocean are sparsely reported relative to their variability. Although not the wind at the surface which would be most valuable, useful information about variations of wind in the lower atmosphere can be obtained from movements of low level clouds in satellite pictures. In early 1982 the low level zonal winds across the equatorial Pacific were near normal. The easterlies were slightly stronger than normal in the central Pacific, and very slightly weaker than normal in the IndoPacific i;land region (Fig. 8). By July, as the region of convective rainfall moved eastward, the tradewinds in the western Pacific had weakened to the extent that west of the dateline the near equatorial winds had become westerlies. These westerly winds continued to intensify and moved into the eastern Pacific during the first quarter of 1983, while stronger than normal easterlies returned to the far western Pacific. The zonal wind had returned to near normal all across the equatorial Pacific by July 1983. Among the consequences of the rotation of the earth on its axis are strong constraints on the movements of the ocean and atmosphere. Often these movements take the form of wavelike processes on very large scale. Near the equator, wavelike movements that travel rapidly eastward are possible, and appear to be a prominent part of the way in which the ocean responds to varying surface winds, including those variations associated with El Nifio. These eastward propagating features are called equatorial Kelvin waves. A dynamically related kind of movement, the coastal Kelvin wave can propagate along the continental coastlines. Coastal Kelvin waves travel in such a direction as to have the coastline on their right in the Northern Hemisphere, and on their left in the Southern Hemisphere. In regions away from the equator the principal wavelike process is the Rossby wave. Large-scale Rossby waves travel westward. Near the equator their speed is only about one-third that of the Kelvin wave, and is even slower in higher latitudes. The sequence of events that transpires is that an equatorial Kelvin wave is generated by a change of surface wind in the tropical Pacific, and travels eastward to the coast of South America. At the coast it is partly reflected as a westward travelling Rossby wave, and partly converted to coastal Kelvin waves that travel poleward in both hemispheres. Because westward propagation of Rossby waves is so slow in higher latitudes, El Nifio effects that are carried into middle and high latitude coastal regions by the coastal Kelvin waves may persist for many months unless they are obliterated by other processes such as local winds in those regions. In the circumstance of El Nifio the Kelvin waves are of "downwelling" nature. That is, they are associated with an elevation of sea level, but a deepening of the thermocline as they propagate along the equator and the coasts.

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Fig. 9. Zonal displacements of drifting buoys in the 4 O N - 4 O S band of the eastern tropical Pacific. The generally accepted interpretation of the observations made during 19821983 is that the early warming across much of the eastern equatorial Pacific was

a result of eastward surface current and deepening of the thermocline associated with a downwelling Kelvin wave caused by the reversal of the surface winds in the western Pacific. The wind anomaly traversed the ocean more slowly than the SST anomaly. The second peak of SST anomaly in the eastern Pacific appears to have resulted from eastward surface currents driven by the more local winds. AS will be seen, the second peak is more local in several respects. Support for these interpretations is afforded by the movements of satellitetracked drifting buoys released in the tropical Pacific to monitor the surface currents. The zonal movements of several of these buoys in the eastern Pacific is shown in Fig. 9. In the early summer of 1982 drifting buoys near the equator

14

in the eastern Pacific were moving westward at about 60 km per day, indicating moderate to strong currents in the normal direction. During the autumn the currents slowed until by December they had turned weakly eastward over most of the eastern tropical Pacific. The end of this phase coincided with the early maximum in SST anomaly. In early January 1983, and continuing into March, the surface currents again reversed, becoming powerfully westward. Moored current meter observations on the equator at 95OW and ll0W indicate that the Equatorial Undercurrent also ceased during this period (Halpern, 1987). Based on simulation using a numerical ocean circulation model, Philander and Siege1 (1985) traced the spectacular events in the eastern Pacific to the sudden return of easterly winds in the western Pacific (Fig. 8 ) . By March the patch of westerly surface winds had moved into the eastern Pacific, driving a strong jet-like eastward surface current. This eastward surface current was seen only near the equator, although probably there was eastward flow also in the North Equatorial Countercurrent. Elsewhere in the eastern Pacific the surface currents were westward. The eastward current pulse coincided with the development of the second, and at the coast largest, peak in the SST anomaly (Figs. 3, 4). In June easterly winds returned also to the eastern Pacific, the surface currents accelerated westward, and the eastern Pacific cooled rapidly. The eastward surface currents observed in association with the event must have had the effect of substantially increasing the residence time of these waters in the eastern Pacific. Waters found near the Galapagos in June 1983 would in a normal year have been displaced 5,000 to 7,000 km westward. This presumably has significant effects on ecological variables such as nutrient replacement and plankton transport as well as temperature. The disappearance of a primary feature of the tropical ocean circulation, the Equatorial Undercurrent, is extraordinary, but the ecological impact of the phenomenon is a difficult problem. The meridional pattern of evolution of the eastward surface currents is strongly reflected in that of the surface temperature anomalies. The first maximum of the SST anomaly extended into the central Pacific as did the eastward surface current anomalies associated with it. This maximum was observed far to the south along the coast of South America, with slowly attenuating magnitude (Fig. 10). The secondary peak in surface temperature anomaly that occurred only in the eastern Pacific, and was associated with strong eastward surface current anomalies only in the eastern Pacific and only near the equator, substantially exceeded the initial anomaly near the equator ( 5 O S ) in magnitude, but attenuated rapidly with poleward distance along the coast of South America. The first maximum was observed at least as far south as Talcahuano (36.7's) but not at Corral ( 4 O o S ) , Chile (Fonseca, 1985). In the Northern Hemisphere, there is evidence of both temperature anomaly peaks as far north as into the northern Gulf of Alaska (Royer, 1985), but differentiating the second peak north of Vancouver Island becomes difficult.

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1

1983

Evolution of coastal water temperature anomalies at Paita (5OS), Puerto Chicama (7.7OS1, Chucuito (12.loS), Funta Coles (17.7OS), Arica (18.5OS), and Caldera (27's). Below the ocean surface, the thermal anomalies associated with El Niilo are most readily described as deepening of isotherms from their normal levels. In the eastern tropical Pacific, the 2OoC isotherm lies in the upper part of the main thermocline. Increases in its depth can be expected to have direct local ecological effects through change of the thermal habitat, and indirect regional effects by reducing exposure of nutrient-rich waters to surface mixing processes. In the vicinity of the Galapagos Islands and along the coast of Central America and northern South America the 20°C isotherm is normally about 30 meters deep, with temporal variations of about 15 meters (Hansen and Herman, 1988). Westward and toward the subtropical gyres of the North and South Pacific it deepens so that at 140°W it is about 120 meters deep at 20°N and 230 meters deep at 20"s. During September 1982 the 2OoC isotherm had plunged to more than 75 m below its normal depth along the equator in the eastern Pacific (Fig. 11). In subsequent months the deepening increased and propagated poleward along the coasts of Central and South America before attenuating. No intensification of the depth anomaly of the 2OoC isotherm was noted in connection with the second peak in surface temperature anomaly. The second temperature maximum was a quite superficial feature limited to the upper 50 meters or so of the ocean. Poleward of the region shown in Fig. 11, isotherm depressions were observed as far as 2OoS, and doubtless reached farther. At Iquique (20.3OS) the principal temperature m a x i m extended much deeper than 50 meters and was observed from December 1982 through March 1983. A small secondary m a x i m was observed in the upper 20 meters in June 1983 (nenzalida, 1985). In the North Pacific isotherm deepening of up to 200 meters was observed within 150 kilometers of Vancouver

16

meters

0

10

20

30

40

50

Fig. 11. Depth anomaly of the 2OoC isothermal surface in the eastern tropical Pacific during (top) September 23-October 2, 1982, (middle) November 22-December 21, 1983, and (bottom) January 21-February 21, 1983. Contours show deepening in meters, gray tone scales show uncertainty of determination in meters (from Hansen and Herman, 1989).

17

180 -

420

400 380

JARVIS

1

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SANTA CRUZ 160-

140-

\

Fig. 12. Variation of sea level at Nauru Island, Jarvis Island, and Santa Cruz Island in the equatorial Pacific (from Lucas g.,1984).

e

Island during March 1983 (Tabata, 1985), and in the northern Gulf of Alaska (Royer, 1985). Water temperature continued to be above normal to depths in excess of 250 m in the northern Gulf of Alaska until the middle of 1984. The 2OoC isotherm, of course, does not occur at these high latitudes. Another important aspect of El Nifio is its effect on sea level. In normal times the surface of the Pacific ocean slopes upward from east to west due to the westward force of the surface winds. When these winds fail or reverse, as has been described for the El Nifio, the sea level also is affected (Lucas g al., 1984). Fig. 12 shows the variations of sea level at three island sites in the equatorial Pacific. At Nauru Island in the western Pacific (167"E) sea level began lowering in late 1982, falling almost 25 centimeters by March 1983, then over a period of several months returned to its normal level, but less than its level had been in 1982. At Jarvis Island, near 160°W in mid-Pacific, sea level rose to a m a x i m of almost 30 centimeters above normal during the last half of 1982, then fell to a little below normal simultaneously with the development of the initial peak'anomaly of sea surface temperature in the eastern Pacific. As sea level at Jarvis Island was lowering, that at Santa Cruz (90.3OW) in the Galapagos Islands began to rise. It reached a peak anomaly of about 44 centimeters in very early 1983. Sea level in the Galapagos reflects in detail the events that have been described in the evolution of the SST anomaly maxima and the observations of eastward surface currents. The pattern of sea level variations along the coast is shown in Fig. 13. The sea level changes observed at La Libertad, Ecuador (2OS) are similar to those at Santa Cruz, 1,000 kilometers to the west. The first peak of the sea level anomaly propagated rapidly southward along the coast with little attenuation, but the peak associated with the large SST anomaly in May-June 1983 is largest

18

0

i!2 IW

2o

,In

1

Fig. 13. Variations of monthly mean sea level at (top) La Libertad, Ecuador, (middle) Callao, Peru, and (bottom)Antofagasta, Chile. in the tropics, like the SST anomaly and the surface current variations. In the Northern Hemisphere, the first sea level anomaly m a x i m was observed far up the Pacific coast of Alaska (Cannon g g.,1985), and a secondary maximum in June was distinguishable as far as 44.6ON (Huyer and Smith, 1985). A final aspect that may be unique to the El NiTio event of 1982-1983, and one that probably has at least local ecological effects, is the extraordinary waves that assaulted exposed regions of the entire coast from California to Chile early in 1983. The unusual winds in the tropical Pacific coincided with a deepening of the Aleutian low pressure center in the North Pacific, not necessarily due to the El NiTio (Namais, 1983). This resulted in unusually strong westerly winds and a series of severe storms at unusually low latitudes in the subtropical North Pacific. Surface waves generated by these storms radiated out for thousands of kilometers. Severe coastal erosion and damage to facilities were reported from both California and Ecuador, and related problems were experienced as far south as central Chile. The fact that these unusually large waves came in the presence of higher than normal average sea level made them more destructive to coastal features than would otherwise have been the case.

19

Local ecological impacts resulted from the mechanical forces that ravaged the coast (see Dayton and Tegner, and Glynn, this volume), and increased turbidity resulting from coastal erosion, might also have an effect. 5 REFERENCES Andrade, E.R. and Sellers, W.D., 1988. El NiEo and its effect on precipitation in Arizona and western New Mexico. J. Climatology, 8: 403-410. Bjerknes, J., 1969. Atmospheric teleconnections from the equatorial Pacific. Mon. Wea. Rev., 97: 163-172. CAC, 1984. Climate Diagnostic Bulletin. Published monthly by National Meteorological Center, NOAA, Washington, D.C. Cannon, G.A., Reed, R.K. and Pullen, P.E., 1985. Comparison of El Niiio events off the Pacific northwest. In: W.S. Wooster and D.L Fluharty (Editors), El Niiio North. Washington Sea Grant Program, Univ. of Washington, 75-84. Eguiguren, D.V., 1894. Las lluvias en Piura. Bol. SOC. Geograf. Lima, 4(7-9): 241-258. Fonseca, T.R., 1985. Efectos fisicos del fenomeno El Niiio 1982-83 en la costaChilena. Investigacion Pesquera, Num. Esp. Taller Nacional Fenomeno El Nino 1982-83. Santiago, 61-88. Fuenzalida, R., 1985. Aspectos oceanograficos y meteorologicos de El Niiio 1982-83 en la zona costera de Iquique. Investigacion Pesquera, N m . Esp. Taller Nacional Fenomeno El Niiio 1982-83. Santiago, 47-52. Gill, A.E. and Rasmusson, E.M., 1983. The 1982-83 climate anomaly in the equatorial Pacific. Nature, 306: 229-234. Halpern, D., 1987. Observations of annual and El Nifio thermal and flow variations at O o , llOoW and O o , 95OW during 1980-1985. J. Geophys. Res., 92(C8): 8197-8212. Hamilton, K., 1988. A detailed examination of the extratropical response to tropical El Nifio/Southern Oscillation events. J. Climatology, 8: 67-86. Hansen, D.V. and Herman, A., 1988. A seasonal isotherm depth climatology for the eastern tropical Pacific. NOAA Tech. Rept. ERL 434-AOML 33 (Rev.), 35 pp., Atl. Oceanogr. and Meteorol. Lab., Miami, FL. Hansen, D.V. and Herman, A., 1989. Evolution of isotherm depth anomalies in the eastern tropical Pacific Ocean during the El Niiio event of 1982-83. J. Geophys. Res., 94(C10): 14,461-14,473. Huyer, A. and Smith, R.L., 1985. The apparition of El Niiio off Oregon in 1982-83. In: W.S. Wooster and D.L. Fluharty (Editors), El Niiio North. Washington Sea Grant Program, Univ. of Washington, 73-84. Lucas, R., Hayes, S.P. and Wyrtki, K., 1984. Equatorial sea level response during the 1982-83 El Niiio. J. Geophys. Res., 89(C6): 10,425-10,430. Namais, J., 1983. Advance signs of the western hemisphere climate observations observed in winter, spring, and summer 1983. In: Proc. Eighth Ann. Climate Diag. Workshop, NOAA, U.S. Dept. of Corn., Washington, D.C., 55-62. Nicholls, N., 1987. The El Nifio/Southern Oscillation phenomenon. Ch. 1, In: M. Glantz, R. Katz, and K. Krenz (Editors), The Societal Impacts Associated with the 1982-83 Worldwide Climate Anomalies. Report based on the workshop in Lugano, Italy, 11-13 November 1985. National Center for Atmospheric Research, Boulder, CO, 105 pp. Pan, Y.H. and Oort, A.H., 1983. Global climate variations connected with sea surface temperature anomalies in the eastern equatorial Pacific Ocean for the 1958-1973 period. Mon. Wea. Rev., 111: 1244-1258. Peterson, G., 1935. Estudios climatologicos del noroeste Peru. Bol. SOC. Geol. Peru, 7(2): 1-141. Philander, S.G.H. and Siegel, A., 1985. Simulation of El Niiio of 1982-83. In: Proceedings of the Liege Colloquium (1984), World Climate Research Program, J.C.J. Nihoul (Ed.), Coupled Ocean Atmosphere Models, pp. 517-541. Elsevier Science Fubl., Amsterdam, Holland, May 1984. Quinn, W.H., Zopf, D.O., Short, K.S. and Kuo Xang, R.T.W., 1978. Historical trends and statistics of the Southern Oscillation, El Niiio, and Indonesian droughts. Fishery Bull., 76(3): 663-678.

20

Quinn, W.H., Neal, V.T. and Antunez de Mayolo, S.E., 1987. El Nifio occurrences over the past four and a half centuries. J. Geophys. Res., 92(C13): 14,449-14,461. Rasmusson, E.M. and Carpenter, T.H., 1982. Variations in tropical sea surface temperature and surface wind fields associated with the Southern Oscillationfll Niiio. Mon. Wea. Rev., llO(5): 354-384. Royer, T., 1985. Coastal temperature and salinity anomalies in the northern Gulf of Alaska. In: W.S. Wooster and D.L. Fluharty (Editors), El Nifio North. Washington Sea Grant Program, Univ. of Washington, 107-115. Schott, G., 1931. Der Peru-strom und seine nordlichen Nachbargebeite in normalen und anormaler Ausbildung. Ann. Hydr. Mar. Met., 59(5): 161-169, (6): 200-213, (7): 240-253. Tabata, S., 1985. El Nifio effects along and off the Pacific coast of Canada during 1982-83. In: W.S. Wooster and D.L. Fluharty (Editors), El Niao North. Washington Sea Grant Program, Univ. of Washington, 85-96. Taft, B.A., 1985. El Niiio of 1982-83 in the tropical Pacific. In: W.S. Wooster and D.L. Fluharty (Editors), El Niiio North. Washington Sea Grant Program, Univ. of Washington, 1-8. Walker, G.T. and Bliss, E.W., 1932. world weather V. Mem. Roy. Meteor. SOC., 4: 53-84. Woodman, R.F., 1984. Recurrencia del fenomeno El NiEo con intensidad comparable a1 aiio 1982-83. In: Proc., Seminario Regional, Ciencia, Tecnologia y Agresion Ambiental, El Fenomeno El Niiio, CONCYTEC, Lima, 301-332. Yarnal, 8. and Diaz, H.F., 1986. Relationships between extremes of the Southern Oscillation and the winter climate of the Anglo-American Pacific coast. J. Climatology, 6: 197-219.

21

NUTRIENTS AND PRODUCTIVITY DURING T H E 1982/83 EL NINO R.T. BARBER and J.E. KOGELSCHATZ Monterey Bay Aquarium Research Institute, Pacific Grove, California, 93950 USA ABSTRACT Barber, R.T., and Kogelschatz, J.E. 1989. Nutrients and productivity during the 1982/83 El Niiio. The eastern Pacific Ocean, particularly in the low latitude region from 20"s to 20"N, has higher primary productivity than the equivalent region in the western Pacific. Enhanced productivity at the base of the food web supports larger populations and faster growth rates throughout higher trophic levels so that the ecological character of the eastern Pacific is distinctly different from that of the western Pacific. El Niiio is a natural, aperiodic, coupled ocean/atmosphere perturbation of the global heat budget that profoundly modifies the normal east/west asymmetry of both heat content and productivity of the Pacific basin. During the 1982/83 El Niiio a surface layer of warm, nutrient-depleted water appeared in the eastern Pacific and persisted for about 9 months. Nutrient supply, phytoplankton abundance and primary productivity were dramatically reduced by the altered physical conditions of the 1982/83 El Niiio. The decrease of new primary production available to the marine food chain caused proportional reductions in growth, reproduction and survival of marine invertebrates, fish, birds and mammals. Food deprivation together with active and passive redistribution of organisms accounts for most of the biotic changes observed in higher trophic level organisms but direct thermal and sea level effects also were observed, particularly in sessile invertebrates. 1 INTRODUCTION

El Niiio is the appearance and persistence of anomalously warm water in the low latitude eastern Pacific. El Nitio is one facet of a basinwide phenomenon called the El Niiio Southern Oscillation (ENSO) cycle. The ENSO cycle is a natural, aperiodic, coupled ocean/atmosphere cycle that determines both the climatological mean conditions and the major interannual variability of the large-scale heat flux. The ENSO cycle is arguably the most important natural process causing biotic variability in the low latitude Pacific ocean because the cycle itself is responsible for both the "normal" and anomalous ecological conditions that characterize tropical Pacific waters. In that particular context the ENSO driven interannual progression of normal and abnormal years plays a major role in determining the prevailing ecological character of the low latitude Pacific. It has been understood for many decades that the eastern boundary regions of the ocean basins have higher biological productivity than the western boundaries. This truism was perhaps first formally incorporated into a figure by Sverdrup (1955) when he used first principles to make a global estimate of the pattern of relative primary productivity. The principle Sverdrup (1955) used was that the first order process regulating ocean productivity is the transport of inorganic plant nutrients from deep water to the surface layer where there is adequate light. Where seasonal mixing, upwelling or topography enhances the vertical nutrient transport Sverdrup predicted there would be increased productivity. That Sverdrup (1955) quite accurately estimated

22 the gross pattern of primary productivity in the tropical Pacific is shown by comparison of Figure 1 with Figure 2, a map from Fleming (1957) that was based in part on observations of productivity. Later syntheses of large-scale patterns of productivity such as that by Koblentz Mishke el

QI.

(1970) confirm that the eastern Pacific is considerably more productive than the

western Pacific, i.e. there is a strong east/west asymmetry in biological productivity. To understand the biological consequences of El Niiio, it is useful to examine how the east/west asymmetry in basic productivity is created and maintained because, in simplest terms, El Niiio is a dynamic process that redistributes heat in such a manner as to greatly reduce the normal east/west asymmetry of the Pacific. Evidence of the elimination of east/west asymmetry in surface layer heat content in the Pacific basin is shown in Figure 3 where the global sea surface temperature field for the peak of the 1982/83 El Niiio (June 1983) is compared with June 1984 when the Pacific had returned to its normal condition. The global sea surface temperature

summary shows that in June 1983 no water cooler than 25°C was present anywhere in the equatorial Pacific. There is little or no east/west asymmetry in heat content. During normal conditions in June 1984, the eastern third of the equatorial Pacific is occupied by surface water cooler than 25°C and the western third is occupied by water over 29°C. The June 1984 situation shows the east/west asymmetry in heat storage that characterizes the normal Pacific condition. This contribution will examine the nutrient and productivity effects of El Niiio by describing the normal asymmetry, how it is created and maintained, and then will present observations on how the 1982/83 El NiAo modified the basinwide asymmetry causing large-scale changes in nutrient conditions which in turn caused significant decreases in primary productivity that propagated through the food web. 2 THE ENSO CYCLE The ocean/atmosphere phenomenon that determines the basinwide ecological character of the tropical Pacific is the ENSO cycle. The strong trade wind or climatological mean phase of the cycle creates the prevailing characteristics of the basinwide ecosystem (Barber, 1988), and El NiAo, or the anomalous phase of the cycle, determines the environmental extremes of temperature, sea level, and nutrient supply that set limits of abundance and distribution on marine organisms in the affected region (Barber and Chavez, 1986). The El NiAo part of the ENSO name refers to the episodic interannual redistribution of water and heat in the low latitude Pacific; the Southern Oscillation component of the name refers to a coupled oscillation of the South Pacific atmospheric high pressure system and the Indonesian atmospheric low pressure system described in this volume by D.V. Hansen. The surface pressure gradient between these two persistent pressure systems forces the easterly trade winds that dominate the equatorial Pacific. (Figure 2 A in Hansen’s contribution shows how the high and low pressure systems are vertically connected to form a Walker circulation cell and also how the Walker cell over the Pacific connects to other tropical Walker cells.) A long historical analysis of the two pressure systems has established that when pressure rises in the Indonesian low pressure system it falls in the South Pacific high; that is, the two systems show a tightly coupled oscillation that is opposite in sign. This oscillation causes the strength of the atmospheric pressure gradient across

23

Fig. I . Relative potential primary productivity. Light area is low, single hatched area is medium and the cross hatched area is estimated to have highest primary productivity. Re-drawn from Sverdrup (1955).

30

20 10 N

0 10

S 20 30

Fig. 2. Primary production in the equatorial Pacific from 20"N to 20"s in gC/m2/year. Redrawn from Fleming (1957).

24 the tropical Pacific to vary from year to year and drives the low frequency variability in the strength of the easterly trade winds. The climatological mean easterly trade winds (and mid latitude westerlies) set up and maintain the fundamental east/west asymmetry of the Pacific including a basinwide tilt of the thermocline and nutricline with these features deep in the west and shallow in the east (Figure 4). The mean large-scale winds also maintain a basinwide gradient in surface layer heat content with a heat surplus in the west and a deficit in the east. The basic east/west asymmetry is itself the product of coupled ocean/atmosphere processes. The western Pacific contains a "warm pool" of water with an annual mean temperature of > 2 9 T (Figure 3). Solar energy falling on the > 2 9 T water is transferred to the atmosphere by evaporation, convection and back radiation. The convective activity over the warm pool of the western Pacific creates the Indonesian low pressure system that draws air into the upward limb of

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Fig. 3. Sea surface temperature fields in June 1983 and June 1984 in the Pacific and Atlantic Oceans. This analysis blends satellite and shipboard temperature measurements and was provided by Vernon Kousky of the Climate Analysis Center of NOAA. The June 1984 temperature field in the Pacific is close to the climatological mean condition with a well developed "cold tongue" reaching out from the coast of South America and a "warm pool" of water >2YC in the far western Pacific. In June 1983 the "cold tongue" is missing and there are large regions of anomalously warm water off Central and South America.

a Walker circulation cell (Figure 4). This east to west transfer of mass is the easterly trade wind system that characterizes the tropical Pacific. Along the eastern boundary of the low latitude

25 Pacific, equatorward winds force coastal upwelling and in the central and eastern equatorial region the trades force equatorial upwelling. Coastal and equatorial upwelling are circulation patterns in which there is organized vertical transport of subsurface water to replace surface water that has been horizontally displaced by wind. In the surface layer of the ocean this recently upwelled cool water extracts heat from the atmosphere, causing atmospheric subsidence and creating the South Pacific high pressure system. The subsiding air mass feeds into the easterly trades and flows to the west towards the convective center over the warm pool of the western Pacific (Figure 4). The easterly trade winds drive surface water westward in the form of the Equatorial Current System; as this water flows westward it gains heat from the sun. The net effect of the wind driven circulation is to transport heat westward into the warm pool of the western Pacific. Thus the east/west asymmetry in surface layer heat content sets up an atmospheric pressure gradient that drives winds that further accentuate the east/west asymmetry in heat content.

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Fig. 4. The El Nitio Southern Oscillation (ENSO) cycle in relation to the west vs. east temperature gradient and the basinwide thermocline and nutricline tilt. The center of the convective heating during normal conditions is usually further to the west than shown in A; Fig. 3 shows that the > 2 9 T warm pool is between 120"E and 160"E; the convective center is usually also in this region. During the mature phase of the 82/83 El Nifio, in April 1983, the center of convective activity was around 120"W as shown in Panel B. From Barber (1988). The asymmetry in heat and potential energy in the form of a higher stand of sea level in the west increases with each year of normal trade winds. Clearly this cycle of positive feedback from ocean to atmosphere and from atmosphere to ocean cannot indefinitely store more and more heat (and more water) in the western Pacific (Cane and Zebiak, 1985). El Nitio is a process that interrupts the year to year accumulation and serves to redistribute the heat and mass back across the Pacific towards the equilibrium condition; that is, El Nitio decreases the east/west asymmetry. The redistribution is set in motion by variation in the winds. The surface wind stress of the

trades establishes a hydraulic pressure head by accumulating water in the western Pacific by about perhaps 1 m above the equilibrium level. If the easterly trades slacken the wind stress decreases as the square of the change in wind speed. When wind stress is suddenly decreased the potential energy of the water accumulated in the west is released, and a pulse of water travels eastward across the Pacific, in part as a Kelvin wave whose speed of advance is 2 to 3 m/sec (O'Brien ef al., 1981). The wave takes three to four months to cross the basin and carries with it a surge of warm, western Pacific surface water (Harrison and Schopf, 1984). The arrival of the series of Kelvin waves off the coast of South America results in a depression of the thermocline by 100 to 150 m, and a warming of the surface waters. Of course, the redistribution of water causes the sea level in the western tropical Pacific to drop by 0.2 to 0.4 m and rise in the eastern Pacific by a similar amount. Figure 3 shows that in a strong El Nifio such as the 1982/83 event the sea surface temperature asymmetry was eliminated across the Pacific.

For coupled air/sea processes such as the ENSO cycle, the critical boundary is the sea surface where the transfer of heat and momentum between the ocean and the atmosphere takes place; that is, the east/west sea surface temperature asymmetry is the critical gradient driving the coupled air/sea processes. However, for determining the ecological character of an ocean region the critical property is not the sea surface temperature but the quantity of heat stored in the form of warm water in the mixed layer above the thermocline. The thickness of the mixed layer determines the ecological character of an ocean region because the major inorganic nutrient reservoir of the ocean is water below the thermocline; therefore, the thickness of the surface mixed layer is involved in regulating the rate at which nutrients can be mixed o r advected into surface waters where there is adequate light for photosynthesis. Any process that depresses the thermocline, that is, any process that increases the thickness of the mixed layer o r increases heat storage, will decrease the rate of supply of new nutrients and necessarily reduce the biological productivity of a region. Light available for photosynthesis decreases exponentially as a function of water depth even in very clear ocean water, because water molecules absorb much of the available light. The result is that in permanently stratified regions with a deep mixed layer, radiant energy and nutrients are separated spatially and primary production, particularly new primary production in the sense expressed by Dugdale and Goering (1967) and Eppley and Peterson (1979), is reduced. New primary production is that proportion of the total production supported by nutrients that are advected or mixed into the euphotic zone; in that context new production is distinguished from recycled production which is supported by nutrients that are regenerated within the euphotic zone. The ENSO cycle regulates the quantity of heat stored in the mixed layer in the eastern and western Pacific; this is the same as saying ENSO regulates the depth of the thermocline. Covarying with, but not identical to, the thermocline is the nutricline, the gradient that separates the nutrient-depleted surface mixed layer from the deep water nutrient reservoir. The critical gradient for the ecosystem that the ENSO cycle regulates is the depth of the nutricline.

3 THE BASINWIDE SETTING The waters of the eastern tropical Pacific are among the most productive of the world ocean.

27

The map of potential relative productivity (Figure 1) produced by Sverdrup (1955) and the early observations summarized by Fleming (1957) (Figure 2) emphasize the richness of the eastern equatorial and coastal Pacific. The biological richness of the region was recognized as early as the late nineteenth century by Buchanan (1886) who commented that "No waters in the ocean so teem with life as those on the west coast of South America." This region has remarkably cool ocean waters for a tropical region. The June 1984 panel of Figure 3 shows the presence of a "cool tongue" of water along the equator that has surface temperatures of 28"C. During this period there is a strong nutricline from 40 to 80 m where nitrate increases from 4 to 12 pM and there is some expression of a subsurface chlorophyll maximum associated with the nutricline; but surface concentrations of chlorophyll remain quite low, around 0.2 mg/ms. In general, the physical, chemical and biological conditions during the mature phase from December 1982 to mid-June 1983 resemble the typical tropical oceanic conditions that characterize a low-latitude gyre. Associated with the gyre-like oceanic conditions there are changes in the species assemblages. In Table 1, phytoplankton species identifications and counts from April 1983 are compared with April 1966. In April 1966 at 92"W and the equator, the water was 20 to 22"C, and had 10 to 12 pM nitrate and about 0.2 mg/ms chlorophyll (Barber and Ryther, 1969). If the April 1966 conditions are assumed to be "normal," the comparison in Table I demonstrates the biotic changes associated with the anomalous April 1983 condition. The major difference is that there is a 10 fold increase in the abundance of coccolithophores in April 1983 and a decrease in the abundance of diatoms. Interestingly the evenness of the diatom assemblage is much stronger during April 1983. The 1966 dominant diatom Nifzschia delicafissima decreased two orders of magnitude from lo4 to 10' cells/liter. The phytoplankton biomass expressed in chlorophyll concentration is remarkably similar (about 0.2 mg/ms) despite the difference in oceanic conditions, but while the chlorophyll concentration was similar the productivity was about an order of magnitude higher in April 1966 (Barber and Chavez, 1983). The November 1982 to April 1983 progression on the equator emphasizes that as El NiAo develops dramatic changes are taking place. The warm, nutrient-rich, well mixed, low phytoplankton biomass and low productivity condition develops into a very warm, nutrientdepleted, strongly-stratified and moderately-low biomass condition. To estimate the quantitative impact of the 1982/83 event, Chavez and Barber (1985) estimated the duration of the two phases on the basis of nutrient conditions observed in the Galapagos time series. Onset phase is defined as the period when the nutricline deepens but surface nutrient concentrations remain relatively high, about 4 to 8 pM. For the 1982/83 El Nirio, the onset phase extended from September 1982 through November 1982 (90 days). By December 1982, nitrate in the surface layer was depleted to concentrations which limit nutrient uptake (Dugdale, 1967). The low nitrate, or "mature" El Nirio, conditions extended from December 1982 through June 1983 (210 days). The return of surface nitrate concentrations to normal levels took place in mid-July 1983. Large-scale, horizontal, sea surface temperature distributions show reestablishment of the equatorial circulation (Halpern, 1987) and the cool equatorial tongue starting at this time, indicated that throughout the entire equatorial zone normal conditions were returning. 6.2 The coastal region The progression of El NiAo conditions along the west coast of South America can be seen by comparison of the November 1982 (Figure I I ) , March 1983 and May 1983 (Figure 12) sections.

40 TABLE 1 Phytoplankton species composition at 92"W and the equator during April 1966 and April 1983. The April 1966 identifications and counts were provided by Edward Hulburt of Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA. The April 1983 information was provided by Terasa Arcos of the Instituto Nacional de Pesca, Guayaquil, Ecuador.

APRIL 1966 "Normal"

APRIL 1983 El Nfio cells/liter

cells/liter COCCOLITHOPHORES Cyclococcolithusfiagilis Cyclococcolithus leptopoms Eniiliana huleyi Rliabdosphaera slylifer Total

200 50 150 50 450

DIATOMS Asteromphalus heplactis Chaetocerospew vianus Coscinodiscus sp. Heniidiscus cuneifonnis Nitzschia bicapitata Nitschia closteriuni Nitzschia delicatissima Rliizosolenia alata Rliizosolenia bergonii Thalassiotlirix sp. Unidentified pennate diatom Unidentitied diatom

100 50 600 50 100 150 10,400 100 50 100 200 5,200

Total

17,100

DINOFLAGELLATES Emviaella vagi.nula Oxytoxuni variabile Unidentified dinoflagellate

150 50

Total

250

TOTAL CELLS

50

17.800

COCCOLITHOPHORES Acanthoica sp. Cyclococcolithusfraglis Cyclococcolithus leptopoms Coccolithus pelagicus Discosphaera tubifera Emiliana huleyi Helicosphaera sp. Ophioster hidrotius Syracosphaera sp. Unidentified coccolithophore

1,146

Total

4,270

DIATOMS Chaetoceros sp. Hemialus sinensis Thalassiossira sp. Niltrchio sp. Nitzschia delicatissima Nitzschia longiksima Rliizosolenia sp. Rh izosolenia fiagidissinia Rliizosolenia stolterfothii Rhizosolenia alata Ceratulina sp.

521 938 1,536 104 104 833 104 1,875 1,979 208 104

Total

9,583

729 208 104 104 208 938 104 104 625

DINOFLAGELLATES Ceratiuni furca

104

Total

104

TOTAL CELLS

13,957

The November 1982 section was sampled during the onset phase of the event as defined by Chavez and Barber (1985). The temperature anomaly had reached 5"s in late September 1982 (Chavez et al., 1984) so that by November 1982 (Figure 11) the characteristic thermocline and nutricline depression had occurred. The 20°C isotherm, which is the middle of the thermocline,

41

was depressed about 100 m when compared with the November 1983 section. The onshore/offshore surface temperature gradient (Figure 15) is similar in magnitude (24 to 27°C in 1982 and 17 to 22°C in 1983) even though the surface temperatures are about 5°C warmer during November 1982. The existence of the onshore/offshore gradient is evidence that coastal upwelling continued during the onset phase of the event. Coastal wind observations have established that in previous El Nifio events (Enfield, 1981) and in the 1982/83 event (Smith, 1983; Huyer el al., 1987) upwelling favorable winds blowing equatorwards along the coast continue during most of the event.

In the 1982/83 event, coastal

winds and locally forced upwelling were present from the beginning of the anomaly in September 1982 until April 1983; the anomalous warming in the continued presence of upwelling is the result of large-scale thermocline changes. The thermocline was progressively depressed in the September to November 1982 period so that the water entrained into the upwelling circulation at 40 to 80 m depth was about 5°C warmer than average. In November 1982 (Figure I I ) , nutricline depression had occurred to the degree that there was a dramatic reduction in nutrients in the offshore and middle portions of the 5"s section, but an inshore band 75 km wide continued to contain nitrate of 4 to 8 pM. These inshore concentrations are still highly favorable for phytoplankton growth and in the inshore band Chavez (1987) reported that there were concentrations of chlorophyll of 2 to 10 mg/ms. These high concentrations were associated with a bloom dominated by the diatom Asterionella japonica. A comparison of November 1982 and November 1983 demonstrates one important characteristic of El Niiio: a major ecological change during El Nitio is a reduction of the size of the upwelling habitat. In November 1982, the 1982/83 event was clearly underway and many upwelling species had begun to be affected (Barber and Chavez, 1986), but in the narrow inshore band, highly productive conditions continued. The major habitat changes in November 1982 were offshore and subsurface. In strong events like 1982/83, these changes continue to move progressively inshore and towards the surface layer so that eventually the entire coastal upwelling habitat is affected. In weak or moderate El Nitio events, it is likely that the inshore band remains a refuge for species requiring the conditions provided by upwelling. In a weak event like 1975 the inshore coastal band remained very productive (Cowles

el

al., 1977) and in the

moderate event of 1976 nutrient concentrations decreased (Dugdale ef al., 1977) but phytoplankton productivity remained relatively high (see Table 4). Barber and Chavez (1986) speculate that behavior that leads fish to concentrate in the inshore upwelling refuges is adaptive for weak and moderate events, but this same behavior proves lethal in exceptional events like that of 1982/83 because fish become trapped in the inshore pockets instead of moving poleward ahead of the warm water anomaly that is progressing along the coast. The March 1983 section in Figure 12 shows that the thermocline was slightly more shallow than it was in November 1982 and that coastal upwelling continued as shown by the upward tilt of isotherms and isopleths of nitrate and the continued onshore/offshore gradient in surface temperature (Figure 15) and nitrate concentration. High chlorophyll concentrations > I .O mg/ms in March 1983 were limited to a 40 km wide band next to the coast. In contrast, the April 1984 section in Figure 10 shows that the band of high chlorophyll extended 400 km from the coast

42

Longitude on

5"s

85 84 83 82 81

Longitude on 5"s 85 84 83 82 81 I

I

l

l

Longitude on 5"s 85 84 83 82 8l0W

,

Nov 82 25

\

J u l y 83

\ A p r i l 84

20

I5

i

20

%I

Nov 83

Nov 83 10

OJ I

I

I

I

i

r

I

400 200 0 400 200 0 400 200 0 Kilometers Offshore Kilometers Offshore Kilometers Offshore Fig. 15. Surface temperature, chlorophyll and primary production along 5"s from 85"W to the coast of Peru showing the comparison between El Nixio (November 1982, March 1983 and May 1983) conditions and November 1983, April 1984 and July 1983 during normal conditions. From Barber and Chavez (1986). across the entire eastern boundary current system. The May 1983 section in Figure 12 shows the strongest development of the 1982/83 El Niiio. The surface temperatures were about 12°C above the climatological monthly mean of 16.7"C and the 20°C isotherm was depressed below 100 m. In the May 1983 section the isotherms and isopleths of nitrate slope downwards towards the coast indicating that flow was onshore and poleward in the coastal region. The chlorophyll distribution in May 1983 shows that the typically

43 rich eastern boundary region had a biomass character typical of a low-latitude ocean gyre. The highest chlorophyll values found in the May 1983 section were within 5 to 10 km of the shore and were in very low salinity, very high nitrate water. The heavy rainfall that occurred in April and May 1983 washed seabird guano off coastal rocks and formed a thin, but stable lens of high nutrient water. This high nitrate surface lens was limited in area and it varied weekly from being undetectable to having a strong local signal. PRODUCTIVITY EFFECTS O F EL NlNO 7. I The equatorial regiori Hydrographic observations taken during the 1982/83 event indicate that for about 210 days, from December 1982 through June 1983, the surface layer concentration of nitrate was very low, often below the detection limit of 0.2 pM, for an enormous expanse of the equatorial Pacific. Satellite temperature observations such as those shown in Figure 3 indicate that the entire equatorial cold tongue region was occupied by anomalously warm water. The area normally occupied by the cold tongue reaches from the coast of South America at about 80"W westward to the dateline at 180" (Levitus, 1982); therefore, the region affected reaches over about a quarter of the circumference of the earth, roughly 90" of longitude. Over this region the supply of nitrate and other nutrients to the euphotic zone was significantly reduced, necessarily decreasing new primary production. New production is defined as primary production dependent on newly available nitrogen, for example, NO3-N (Dugdale and Goering, 1967) from the deepwater nutrient reservoir.

Eppley and Peterson (1979) argue that

new production is "quantitatively equivalent to the organic matter that can be exported from the total production in the euphotic zone without the production system running down." Therefore, new primary production is newly synthesized organic matter available for export by the higher trophic levels of the food web. This single effect, the reduction of new primary production as a result of nutrient denial, is a consequence of El NiAo that affects the entire ecosystem. Estimates of equatorial productivity and the 1982/83 productivity anomaly made by Chavez and Barber (1985 and 1987), and summarized in Table 2, show that the total primary production rate during the mature phase of El Niiio was 21 to 26% of the rate during normal conditions. The empirical relationship between new production and total primary production found by Eppley and Peterson (1979) indicates that as total production falls below 300 to 400 mgC/m2/day the proportion of new production decreases sharply. As no direct measurement of new production are available for equatorial waters during this period, the global relationship was used to calculate new production. Clearly the new production rate during El NiAo was reduced more strongly than total production. Table 2 shows that the El Niiio rate of new production during the mature phase was only 5 to 6 percent of the normal rate. This 20 fold reduction in new primary production was a pervasive biotic change that affected the entire food web because the equatorial food web is adapted to continuously high levels of new primary production (Vinogradov, 1981). 7.2

The coastal region' In the low latitude coastal regions of the eastern Pacific, from the equator to about 2 0 3 ,

primary productivity is high. On an annual basis it is probably higher than in any other ocean

44 region (Barber and Smith, 1981). The difference between the eastern Pacific coastal upwelling area and other coastal and oceanic environments is a matter of quantity: the large-scale nutricline topography and more or less continuous, local, upwelling favorable winds cause the annual flux of new nutrients to the euphotic zone to exceed that of other regions. Thus, the annual new primary production is high and the quantity of organic material that can be exported from the euphotic layer as a commercial fish catch, loss to sediments and loss to adjacent intermediatedepth waters is much higher. Determining the climatological mean level of primary production is difficult because the same mechanics that make the region highly productive also make it TABLE 2 Comparison of El Nifio and normal total and new primary production rates in the equatorial Pacific. Total production was converted to new production using the model of Eppley and Peterson (1979). This table is modified from Chavez and Barber (1985) with additional data.

Normal

Rate fmnC/m2/dav)

Anomalv (96)

El Niiio

El Niiio/Normal

Onset

Mature

Onset

Mature

Total Primary Production Zonal (0"; 90"W to 180") Meridional (95"W; 2"N to 5 3 )

490 (n=132) 260 (n=8) 605 (n=8) 225 (n=7)

125 (est) 125 (n=8)

53 37

26 21

New Primary Production Zonal (0"; 90"W to 180") Meridional (95"W; 2"N to 5 % )

214 265

14 14

29 20

6 5

63 54

inherently variable (Barber el al., 1985). The ENS0 cycle is an inherent source of interannual variability because it behaves like an aperiodic oscillator (Cane and Zebiak, 1985). Table 3 presents the results of studies carried out in the coastal region during non-El Niiio years in the last two decades with a mean value of 3,840 mgC/m2/day with a standard error of f 250 mgC/m2/day.

Syntheses of existing measurements suggest that the climatological mean value is

between 2,000 and 4,000 mgC/m2/day (Barber and Smith, 1981; Walsh, 1981; Barber ef al., 1986; Chavez and Barber, 1987). Chavez et al. (1988) used a 29 year time series of wind speed and thermocline depth as inputs to a model that estimated the supply of nitrate to the surface layer and calculated the new primary production that would result if all the nitrate was taken up by phytoplankton and converted to new production. In the Peru coastal waters, Dugdale (1985) made a direct measurement of the f-ratio using nitrogen stable isotopes. With this empirical relationship new production was back converted to total production. Calculating total primary production for approximately the same periods that the studies in Table 3 examined, the model predicted a mean value of 3,180 f 70 mgC/m2/day. The agreement of the measured values (3,840 f 250) and the model estimate (3,180 f 70) to within 20% is remarkable and indicated that it would be valuable to evaluate the model predictions for mean productivity during El Niiio events. Chavez el al.

45 (1988) report that during El Nirio events the model calculates a productivity of from 1,700 mgC/m2/day in 1983 to 2,200 mgC/m2/day in 1965. The predicted values are higher than expected because the local wind increases significantly during El Niiio so that there is simply more upwelling; at the same time the nutrient content of upwelled water is so much lower that the model calculates about 50% less total primary production in the coastal region during El Niiio events. However, hydrographic observations indicate that the "El Niiio" prediction of the model may be too high for the 1982/83 El Niiio event. Measurements of currents, pressure and local winds during the 1982/83 event by Huyer el al. (1987) indicate that local upwelling favorable winds did not continue to force upwelling throughout El Nirio. At 10"s Huyer el al. (1987) found that upwelling ceased in May 1983 TABLE 3 Estimates of primary productivity from along the west coast of South America. From Chavez and Barber (1987).

Year

Month

1966 1969 1969 1974 1971 1977 1978

April April June February March November February

Productivity (mgC/m2/day) 6,260 (Barber and Smith, 1981) 5,160 (Barber and Smith, 1981) 1,240 (Walsh, 1981) 4,160 (Sorokin, 1978) 1,960 (Barber and Smith, 1981) 4,260 (Harrison and Platt, 1981) 3.830 (Barber el al., 1986) mean=3,840 f 250

despite continued strong and favorable for upwelling local winds. This cessation of upwelling occurred because the wind-induced offshore flow in the surface layer was balanced and overridden by an onshore geostrophic flow driven by the pressure gradient. The steric height along the shelf break was significantly higher close to the shelf break at 5"s than at 10% setting up a strong north to south pressure gradient. The Huyer et al. (1987) analysis indicates that geostrophic suppression of upwelling and offshore flow were present from mid-March 1983 to mid-June 1983. During this period the wind-driven primary production model of Chavez et al. (1988) would significantly overestimate productivity. This evidence suggests that during the 1982/83 event the inshore productivity supported by wind-driven upwelling may have been significantly less than the 1,700 mgC/m2/day value predicted by the model. Nevertheless, direct measurements of phytoplankton biomass and productivity (Figures 12 and 15) emphasize another important aspect of El Niiio: despite decreases in primary productivity the nearshore ( 0.05). Sea temperature deviations in Panama and at Puerto Chicama indicate some, but by no means total, correspondence between El Niiio occurrences and sea warming in a Central American area (Fig. 19b). A scatter plot of 2-yr smoothed temperature deviations indicates that only the 1972-73 and 1982-83 El Nifio events of strong and very strong intensity resulted in pronounced warming in both regions (Fig. 20). All earlier El Niiio events, including the very strong event of 1925-26 (Quinn et al., 1987), had only minor or no warming effect in Panama. From this analysis, it is possible to conclude that since 1925 only two of six strong to very strong El Nifio events in Peru resulted in synchronous warming episodes as far north as the Gulf of Panama. El Niiio sea level signals are usually detected in Panama (Kwiecinski and Chial, 1987), but higher SST values are not usually found. Unexpectedly, the moderate El Nifio event of 1987 (Quinn et al., 1987) was accompanied by a marked increase in SST in the Gulf of Panama (Fig. 19a). Although no coral bleaching was observed in Panama, bleaching of remnant coral populations that survived the very strong El Nifio event of 1982-83 did occur at Cocos Island, Costa Rica and in the Galapagos Islands during the warming period (Glynn, 1988a). Coral recovery occurred after 4-6 weeks with no significant mortality. The long-term temperature data for the Gulf of Panama reveal a prominent, near-decadal warming trend that began in 1976 (Fig. 19a). This is indicated by the number of days per year with high SST (2 29OC): over a 12 year period (1976-1987), 8 years experienced high SST for 100

79

1968

70

72

74

76

78

80

82

84

86

88

Year Fig. 18. A comparison of the number of days per year with high temperatures (129OC) at the Panama Canal Commission (PCC) and Smithsonian Institution (STRI) observation stations at Naos Island (1969-1987). days/year or more. In 1980, there were 160 warm days, and the 1983 El NiAo event was accompanied by 220 warm days. Only during the 1972 El NiAo did the number of warm days per year (153 days) previously exceed 100 days in the Gulf of Panama since 1915. Quinn and Neal (1983, 1984) and Quinn et al. (1987) have also identified this recent, long-term warming trend, which has affected much of the tropical and subtropical Pacific Ocean over recent years. The largely negative Easter-Darwin Southern Oscillation index anomalies, which generally co-occur with above normal SST, began in early 1976 and have persisted until early 1988 when an apparent reversal was first noted (Quinn, pers. comm.). Quinn and Neal (1983) have hypothesized that this decadal climatic change could be due to a weakening of the southeast trade system off the west coast of South America. Since the tolerance of reef corals is influenced by their thermal history (Jokiel and Coles, 1977), the decadal warming trend that encompassed the 1982-83 El Niiio event complicates our understanding of the stress responses observed during 1983. Several studies conducted on coral growth and reef accumulation rates in the eastern Pacific during this period reported vigorous reef building that rivaled the highest rates known for central and western Pacific reef areas (Chave et al., 1972; Easton and Olson, 1976; Glynn, 1977; Glynn and Macintyre, 1977; Grigg, 1982; Glynn

80

N

0

N

0

-

0

0

0

l n o l n g l n

ln

#

0 #

ln ln

ln

0

81

Fig. 19. (a) Number of days per year with daily mean sea temperature 229OC, Balboa and Naos Island, Gulf of Panama, Panama, 1915-1987. (b) Deviations about historic 2-year running average of number days/year with sea surface temperature 529OC, Panama (heavy line), and of mean annual sea surface temperature, Puerto Chicama, Peru (thin line). Strong and very strong El Niiio Occurrences from 1915-1988 are indicated above (Quinn et al., 1987). Panama temperature data from Panama Canal Commission. Peru temperature data from D. B. Enfield (unpub. data). and Wellington, 1983; Kinsey, 1983). Moreover, the histological condition of coral tissues before 1982-83 indicated a generally healthy state (Glynn et al., 1985b). Whether or not the prior, longterm sea warming period had an interactive effect with the very strong 1982-83 El Niiio event is an intriguing, but as yet unanswered question. 2.9 Coral bleachine and mortalitv dun-

1

Periods of intense sea water cooling, when temperatures drop below 18OC for several days or weeks, occur fairly commonly in the major upwelling centers of the tropical eastern Pacific region (Hubbs and Roden, 1964; Forsbergh, 1969; Dana, 1975; Glynn and Wellington, 1983; Glynn et al., 1983). Compared to non-upwelling areas with relatively rich coral faunas and well developed reefs, upwelling environments are characterized by (a) few reefs per unit area, (b) reefs of limited dimensions, (c) youthful reefs, (d) low coral growth rates, and (e) few reef associated species (Dana, 1975; Glynn and Wellington, 1983; Glynn et al., 1983). During periods of intensified upwelling, e.g. at the height of the Little Ice Age (1675-1800 A.D.), it is likely that an entire Costa Rican reef tract succumbed to environmental chilling ( G l y et ~ al., 1983). Like El Niiio, intense cooling episodes occur unpredictably, but unlike El NiRo, which shows a high inter-event variability in terms of the areas affected, cooling episodes are confined to the major upwelling centers. These thermal disturbances are also different in that extreme low temperatures are fleeting, lasting for only a few hours or days (Glynn and Stewart, 1973; Glynn and D'Croz, in press), whereas extreme high temperatures persist for weeks or months (Figs. 14 and 19). Periods of intense warming and cooling in the eastern Pacific tend to occur in succession, linked by major shifts in the Southern Oscillation. Peak anomalies in the atmospheric pressure indices, i.e. anti-El Niiio type activity with strong upwelling, are often followed by relaxation troughs and the onset of El Niiio sea surface warming (Quinn, 1976). Upwelling was unusually strong in the Pearl Islands, Gulf of Panama in 1972 (18.6T was the lowest temperature recorded), and resulted in tissue sloughing and branch tip mortality in pocilloporid corals (Glynn and Stewart, 1973). This notable upwelling season was followed by a strong El Niiio event in 1972-73 (Quinn et al., 1987) that resulted in sea warming in the Gulf of Panama (Fig. 19), but was not of sufficient intensity to cause coral bleaching or mortality (Glynn, 1977). The 1985 upwelling season was probably more intense than that in 1972, and was unusual in that it followed rather than preceded an El Niiio event (Kwiecinski et al., 1988). Anti-El Niiio type activity, with strong southeast trades and upwelling, typically precedes El Niiio events by a year or less (Quinn, 1974; Wyrtki, 1975; Quinn and Neal, 1983). Richmond (this volume) recorded minimum sea temperatures of 14.2OCin March 1985 on coral reefs in the Pearl Islands. Coral bleaching was widespread on the Saboga Island coral reef in March 1985 with 10.4%

82

PANAMA

+

15~1

-

8

I

'

083

,-.

0

40

32

0

"

" A

0

0

0

CHICAMA

0 5 8 041

0

e25

u 0

0

0

0

8';

8000

Fig. 20. Two year running mean deviations of annual mean sea surface temperature at Puerto Chicama, Peru and number of days per year with sea surface temperature 229°C at Balboa, Panama (1925-1987). Strong and very strong El Niiio years are indicated by occluded circles (Quinn et al., 1987). mortality of pocilloporid corals (Glynn and D'Croz, in press). This mortality was assessed at the end of the strong upwelling season with pulses of extreme low temperatures that began in January. The same coral population had experienced 68.5% mortality during the El NiRo warming event in 1983. The most recent coral bleaching associated with intense upwelling (with minimum temperatures of 16OC) was observed in the Pearl Islands in February 1989, but the extent of mortality due mainly to the cooling has not yet been determined (Eakin et al., 1989). Immediately preceding the 1989 bleaching event numerous reef flat corals suffered high mortality due to extreme mid-day low tidal exposures, which often accompany anti-El NiAo type conditions (see

83 below). 2.10 Non-thermal a s s ors and coral bleaching Because coral bleaching and mortality have occurred during periods of heavy fresh-water runoff and sea water dilution (Goreau, 1964; Stoddart, 1969a; Egaiia and DiSalvo, 1982), the exceptionally high rainfall that accompanied the El Niiio of 1982-83 in some areas could have conmbuted to this disturbance event. Heavy rainfall was experienced in the Galapagos Islands. For example, in Academy Bay, Santa Cruz Island, maximum 24 hour rainfall in 1982 (137.6 mm) and 1983 (122.9 mm) was about 6 times the average of maxima recorded in 1979-81 (22.1 mm) (Robalino, 1985). Total annual rainfall in 1983 (2,768.7 mm) was over 10 times the average annual amount reported in 1979-81 (265.1 mm). Heavy downpours at Floreana Island resulted in significant runoff and sea surface discoloration to slightly more than 1 km offshore (Robinson, 1985). Surface salinities that were monitored 3 times a week for 18 months at a station 7 km southeast of Academy Bay indicated slightly below-normal values during the peak El Niiio rainy period (Fig. 21). However, these offshore salinities were no lower than 32.5 o/oo (Kogelschatz et al., 1985), far above dilution levels known to stress corals (Kinsman, 1964; Endean, 1976; and see below). Also, the coral bleaching and death occurred to 30 m depth, well below the influence of surface salinities (Robinson, 1985). Rainfall on the Pacific coast of the Isthmus of Panama during the El Niiio event was close to the long-term annual average for this region. For example, at Balboa Heights the average annual rainfall for a 56 year period (1930-1985) was 1,800.6 mm and total rainfall in 1982 was 12% below and in 1983 3% above the long-term average (Meteorological and Hydrographic Branch, Panama Canal Commission). The observed salinities in the Gulf of Panama in 1982 and 1983 are in accord with the normal to low rainfall records over this period, and are similar to the seasonal range of mean values reported earlier (Fig. 21). Even the low salinity regime observed in Panama over a 2 month period in 1973 (minimum values 19-20 O/oo ) did not result in coral bleaching or death (Glynn, 1974). Thus, I conclude that El Niiio associated variations in salinity probably did not affect corals adversely in the Galapagos Islands or Panama. Heavy runoff can produce increased rates of siltation, which may cause coral bleaching and death (Johannes, 1975; Bak, 1978; Marszalek, 1981). Despite heavy rainfall and runoff in the Galapagos Islands, no evidence of coral mortality caused by heavy siltation was reported there (Robinson, 1985). Excessive runoff, which is usually accompanied by increased sedimentation and turbidity, was not reported in 1983 in Costa Rica (Cortes et al., 1984; Guzman et al., 1987), Panama (Glynn, 1984a) or Colombia (Prahl, 1985). Sudden sea level lowerings associated with ENS0 events in the west and south Pacific have caused disturbances in shallow coral reef populations. Monthly mean sea level can drop to as low as -40 to -45 cm below mean sea level (Yamaguchi, 1975; Wyrtki, 1985), with presumably additive effects on local tidal amplitudes. Reef flat exposures in Guam,during the 1972-73 El NiRo, resulted in the mass mortalities of diverse reef organisms (Yamaguchi, 1975). The disruption of skeletal growth in old reef flat corals in the New Hebrides (Vanuatu) region has also

84

a GALAPAGOS

I

ISLANDS

36

1982

34

S%o

32

1983

30 28

b/

PANAMA

1

36 34 32 30

S %o

28 26 24 22 20

18 1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

1

J F M A M J J A S O N D J F M A M J J A S O N D

Fig. 21. Surface salinity variations in the Galapagos Islands (a) and Panama (b) in 1982-83 compared with previous, non-El Niiio periods. The 1982-83 record for the Galapagos, a few km south of Academy Bay over the 100 m depth contour, is from Kogelschatz et al. (1985); the earlier record (heavy line) is from pooled data for 1968 (Maxwell, 1974) and 1971-72 (Houvenaghel, 1978) and represents monthly means (ranging from 11-48 observations per month) from various areas throughout the archipelago. All Panama data are from Naos Island, Gulf of Panama. Monthly mean and extreme values are shown in 1982 and 1983. The earlier record (heavy line) is for 1965-1967 (United States Coast and Geodetic Survey observations), and the extreme low salinity record for the wet season in 1973 (after Glynn, 1974). been correlated with some non-seismic emergence events during ENSO occurrences (Taylor et al., 1987). And in early 1983, sea level drops in some areas in French Polynesia and the Tokelau Islands resulted in more recent ENSO disturbances to coral reefs (Glynn, 1984a; Coffroth et al., this volume). Unlike ENSO-related sea level lowerings in the west and south Pacific, eastern Pacific El Niiio events are accompanied by high sea levels (Lucas et al., 1984; Wynki, 1985; Hansen, this volume). Preliminary analysis of tidal observations in Panama (Eakin et al., 1989) indicate that exwme tidal exposures are more frequent during non-El Niiio years. No reef flat coral mortality

85 was reported in the eastern Pacific in 1982-83, nor during the strong El Niiio of 1972 and the moderate El Niiio events of 1976 and 1987. However, 4040% of the surface m a of existing reef flat corals suffered severe mortality in 1974 and 1975 (Glynn, 1976), and 97% partial to complete mortality ( > 50% tissue loss) in 1989 (Eakin et al., 1989), both disturbances occuring about 2 years after the El Niiio events. Observations by Robinson (1985) during the El Niiio disturbance have demonstrated that abnormally high sea levels [30-40 cm above long-term means (Wyrtki, 1985)], in combination with spring tides and large and contrary sea swells, caused extensive mechanical damage to shallow coral communities in the south-central Galapagos Islands. Several large colonies of massive corals (Pontes. Pavona) were dislodged and deposited above the high tide line, branching corals (PocilloDora) were tom loose and reduced to rubble, and numerous free-living coral associates, such as sea urchins (Eucidaris) and sea stars (Nidorellia), were cast ashore. A flourishing patch reef located within the Onslow Island (Devil's Crown) crater was thoroughly transformed by adverse sea conditions in early 1983 (Figs. 3 and 22). Over 90% of the pocilloporid reef frame was broken apart and this section of the reef is now a mixed coral rubblehasalt rock bottom. Most massive corals are still in their original, pre-1983 positions, but contain little (usually c 10%) live tissue. A large patch of loose Psammocora coral, formerly present at the west-central reef margin, is now covered with sand. While such physical disturbances produced dramatic effects locally in the Galapagos Islands, reef structures elsewhere in the eastern Pacific, although often mostly dead, remained largely intact immediately following the 1983 mortality event. The eastern Pacific region is geologically active and because coral reefs can be severely affected by volcanic eruptions (Wood-Jones, 1910). tectonic uplift (Stoddart, 1969a, b; Glynn and Wellington, 1983; Colgan and Malmquist, 1987; Taylor et al., 1987) and earthquakes (Stoddart, 1972), it is also necessary to consider these kinds of disturbances in relation to the 1982-83 event. The only likely link between potentially disruptive geologic events and coral mortality was the occurrence of a strong earthquake near the Panama-Costa Rica border (epicenter: 8'.80N, 83'.11W) in April 1983, during the time that corals were dying (Glynn, 1983). This was a strong earthquake (magnitude: M sub"s" = 7.2, M sub"b" = 6.3) with a deep focus (38 f 1.6 km). No surface rupture was reported and it is doubtful that any gases were released. The static displacement at the earths surface was also slight, about 10-3 microns (Bull. Int. Seismol. Centre, 1983). Moreover, since coral reefs were bleached and damaged nearly simultaneously over large parts of the eastem Pacific, at distant locations and in most instances before the Panama-Costa Rica seismic event, this disturbance can be confidently ruled out. As previously noted, coral bleaching at several localities was often most pronounced on the upper portions of colonies that received direct or nearly direct sunlight. Unfortunately, irradiance levels were not monitored near the sites where coral bleaching occurred. Moreover, no information is available on the flux of incoming solar UV radiation (especially the 290-320 nm UV-B band that can penetrate much of the euphotic zone in clear tropical waters), which can be quite damaging to many shallow marine invertebrates (Jokiel, 1980; Siebeck, 1981, 1988; Jokiel and York, 1982). The instrumentation necessary for the accurate measurement of submarine

86

4

a

-N-

Fig. 22. Planar views of the Onslow Island (Devil’s Crown) coral reef showing distributions of major coral and barnacle communities before (1976) and after (1985) the 1982-83 El NiAo disturbance. Note nearly total absence of the pocilloporid reef frame and extensive bed rock basalt exposures in 1985. Most of the massive corals present at site 1 in 1976 were absent in 1985. Similarly, the Psammocora community present at site 2 in 1976 was reduced to only a few scattered live colonies on a dominantly sand/rock bottom in 1985. The 1976 community map is from Glynn and Wellington (1983).

a7

UV radiation is costly and has been used only in a limited capacity thus far. Since there are indications of subtle interactions between high irradiance and temperature, this topic will be discussed below (also see Coffroth et al., this volume). 3 COMMUNITY EFFECTS 3.1 Immediate effects Reef-associated species responded in various ways to the 1982-83 El NiAo event. Some species were affected before or during the height of the warming period, others toward the end of the disturbance, and still others showed changes for several months to years following the disturbance. Those responses that corresponded closely in timing with the primary disturbance event will be considered first, and delayed or longer-term effects, some of which are still in progress (as of mid 1989), are considered later. The most notable community-wide change during the 1982-83 El NiAo event was the sudden appearance of large tracts of stark white coral, which contrasted with patches of brownish or greenish, normally pigmented corals. Branching scleractinian corals (Pocillopora spp.) and branching or platy hydrocorals (Milleporq spp.) were the first to bleach on reefs in Panama (Glynn, 1983), and this was most pronounced at shallow depths (< 10 m). Pocillopora damicornis also bleached before the massive coral Pontes lobata in Costa Rica (Cortes et al., 1984). At Gorgona Island, Colombia, Pocillopora evdouxi retained zooxanthellae and continued to secrete normal amounts of mucus during the early warming period (Prahl, 1983), but died in large numbers, presumably following bleaching, a month later (Prahl, 1985). No live colonies of a branching acroporid coral (Acropora valid& the only known eastern Pacific population in this family (Prahl and Mejia, 1985), could be found after 1983 (H. von Prahl, pers. comm.). Since normally pigmented colonies of this species were first observed at Gorgona Island in September 1983, two months after the main bleaching event (Fig. 14), it is not known if its disappearance was a direct result of the warming disturbance. Massive, platy and nodular corals (e.g. species in the genera Gardineroseris, Pavona, Porites, and Psammocora) generally bleached a few weeks after the branching species in Panama, but all corals were affected at about the same time in the Galapagos Islands (Robinson, 1985). Pavona gigantea and Psammocora stellata were resistant to bleaching in the Galapagos Islands. In Panama, the small, nodular coral Porites panamensis retained a normal greenish-brown coloration for 2-3 months after other corals were affected, but then suddenly died in large numbers near the end of the warming event (August-September, 1983). The high susceptibility of some branching corals to thermal stress has been observed by several workers (e.g., Mayer, 1917; Edmondson, 1928; Jokiel and Coles, 1974). Generally these corals have higher growth rates than more resistant non-branching species. It has been suggested that the sensitivity of branching corals is related to a high respiratory rate and a consequent lowering of the P:R (photosynthesishespiration) ratio at critically high temperatures (Coles and Jokiel, 1977). While most colonies of branching species and small colonies of non-branching species' that experienced severe bleaching died, most large massive colonies that experienced severe bleaching suffered only partial mortality, usually to the upper portion of the colony. Thus, massive colonies that retained live coral tissues after 1983 had the potential to regenerate, as observed in studies

88 elsewhere (Hughes and Jackson, 1980; Jackson, 1983). Some of these large colonies are undergoing regeneration, but many are continuing to lose live coral tissue due to delayed effects such as bioerosion, predation, and damselfish activities (see below). A noteworthy impact of the 1983 mortality event on coral community structure was the sudden loss of coral species and decline in species diversity. Coral diversity (H'),measured before and after the disturbance, declined markedly in Panama and the Galapagos Islands (Table 2), and to a less degree in Costa Rica (Guzman et al., 1987). Although the diversity values reported here were measured in early 1985, about 1.5 years after the disturbance, there was no indication of further significant coral mortality or recruitment in Panama at that time (Fig. 26a). Based on observations in Panama and near total mortality observed by Robinson (1985), I assume no significant recovery in coral cover in the Galapagos Islands over this same period. In the Gulf of Chiriqui, Panama mean species losses per transect along the reef base ranged from about 50% (Secas reef) to 80% (Uva reef) (see site locations in Fig. 2), and most measures of diversity declined to 0 (Table 2). Most evenness measures also declined. However, increases occurred in 3 transects. The increase in J' values was due in large part to the selective mortality of branching pocilloporid corals, which were the predominant species in these transects before 1983. In general, it appears that the loss of species had a greater effect on coral diversity indexes than changes in species evenness (relative abundances). Mean species losses in the Galapagos transects, which included all reef zones (reef flat, slope and base), amounted to 82%, and all H values declined to 0 (Table 2, Fig. 3). Mean coral species diversity (H) at Caiio Island, Costa Rica in 1980 was 0.69, declining to 0.37 in 1984 (Guzman et al., 1987). This difference was nonsignificant, which is not unexpected in light of the relatively low coral mortality observed at Caiio Island in 1983 (Guzman et al., 1987; Glynn et al., in press). Live coral cover and diversity demonstrated a declining nend along the Uva reef base during 1974 when Acanthaster was abundant and actively feeding in this habitat (Glynn, 1976). This decline in diversity during the mid 1970s was attributed to the selective predation of nonpocilloporid corals, present at low relative abundances, by Acanthaster (Glynn, 1976). Acanthaster usually avoids large, intact colonies of Pocillopora spp., the most abundant community members, because of the coral's protective crustacean guards (Glynn, 1983). A comparison of H values from 1974, median = 0.29 (converted to logarithms with base 10, n = 7 transects, Glynn, 1976), with the pre-1983 values, median = 0.24 (n = 10 transects, Table 2), indicates no significant change over the 7 year period (p > 0.05, Mann-Whitney U test). With the steady decline in Acanthaster abundance during the late 1970s to early 1980s (Glynn, 1985a), live coral cover and diversity stabilized until both suddenly declined during the 1983 El Niiio disturbance. Related to pocilloporid coral bleaching were various changes in the density and behavior of obligate crustacean symbiotes (Trapezia spp. and Alpheus lottini). Quantitative sampling in Panama revealed that crustacean densities declined significantly with the deteriorating condition of their coral hosts, from median densities of 9 inds./colony in normally pigmented corals to c 1 indkolony in dead corals (Fig. 8b). A 60% reduction from normal densities was noted for crustacean symbiotes at Gorgona Island, Colombia (Prahl, 1983). This general decline was

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TABLE 2 (cont'd.)

Locations (Sampling dates)

Galapagos Islands Onslow reef (11-13 Jan. 1975 & 1-3May 1985)

0

Pre 1983

H'b post 1983

0.09 0 0 0.26 0 0.35 0.17

0 0 0 0 0 0 0

Number of Species Pre post 1983 1983

Jd 't'

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post 1983

0.30 0 0 0.88 0 0.74 0.55

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0 1 0 0 1 0 0 0.3

a Locations of sampling sites are indicated in Fig. 2 (Uva and Secas reefs) and Fig. 3 (Onslow reef). b Coral species cover and relative abundances were sampled with a 10-m chain transect (Glynn, 1976). H is the Shannon-Wiener index of diversity

-c

(Pielou, 1975), and was calculated from the equation, H = pi log pi. where pi is the proportion of sampling points encountered in the ith species. i= 1 Differences in H were tested employing the approximate 't'-test of Hutcheson (1970). ns, nonsignificant; *, p5 mm/yr), where the displacement from isotopic equilibrium is approximately constant. All of the corals included in this study displayed linear extension rates of >5 mm/yr, thus conforming to the criteria of McConnaughey (1986). One data set (Urvina Bay) from the Galapagos displayed slightly higher 6180 values than the rest. This is from a site of enhanced upwelling on the western coast of Isabela Island, due to the surfacing of the equatorial undercurrent (Cromwell Current).

Surface waters are about 2°C cooler in this region than

they are at the other coral study sites in the Galapagos, hence the 0.4°/00 shift toward heavier 6180 in the Urvina Bay coral (assuming gradients in salinity are small in comparison). Overall, there are lower 6180 values in the Galapagos records during ENSO events than during non-ENS0 periods (for a detailed discussion see Druffel, 1985).

The average annual decrease of 6180 appears more prominent in corals

from Hood, Academy Bay and Champion Islands, presumably due to the absence of the influence of the Cromwell Current. This approach of using annuallyaveraged 6180 is sufficient for detecting ENSO events of significant duration (>9 months) and/or intensity. 6180 appears to be somewhat proportional to the

severity of the pre-1983 ENSO events, that is 6180 is lowest during the major ENSO's of 1940 and 1972-73,noting that the isotope excursions in the Urvina

244

-3

J

'

i

1930

1

1940

- 4

- --- -

1950

1960

ENSO

I

I

1970

1980

YEAR Fig. 3. Annually-averaged 6180 results for corals from Panama [OUraba (L gigantea), Gulf of Panama; W Uva-A (L p l a n u b ) , A Uva-1 (Eclam%) , A Uva56 (Eclams), Gulf of Chiriqui] and the Galapagos Islands [OUrvina,OHood,O Champion and oAcademy (all p . clavus)]. Annual averages for specimens Uraba, Uva-1, Uva-56, Academy and Champion represent the mean isotopic composition of 5 to 16 individual analyses collected between successive February-March markers in the corals (as determined by density banding and isotope maxima/minima). Bay specimen are only slightly larger than the analytical precision.

The

excursion during 1974 does not correspond to an ENSO year, indicating that it is not possible to detect all ENSO's unambiguously and that there are some light isotopic excursions that do not reflect ENSO's. We also need to point out that because density banding is used as the basis for "annual" sampling, some bias may be introduced when banding becomes difficult to interpret or when the time of band formation shifts relative to the temperature signal. The annually averaged Panama data sets show excursions towards lower 6180 values during 1969 and 1982; there is no clear correlation between the isotopic signal and other ENSO periods. Reasons for this are presented below in the description of the seasonal 6180 record. The average isotopic composition of the three Uva Island samples varies by about 0.5°/00. We attribute this range to differences in location on the Uva Island reef and to species specific offsets from equilibrium (e.g., Gardineroseris Dlanulata and Pavona clavus, see Table 1). In two Galapagos corals (Champion Island and Academy Bay), seasonal variations of 6180 ranged from 0.6-0.8°/oo during the ENSO events of 1972-73, 1976 and 1982-83 (Fig. 4a).

The reduction of the seasonal signals demonstrates

that the coral is recording the warm, low salinity waters that persist at the Galapagos during most of an ENSO year.

245

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1978

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1980

1984

YEAR

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-7

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-5

-7

-6

-5 1

1962

1

1

1964

1

1

1966

1

1

1968

1

1

1970

1

1

1972

I

I

1974

I

I

1976

I

I

1978

I

I I I I I 1980 1982 1984

Year (Feb.-March) Fig. 4 . Seasonal 6180 results for (a) Champion Island ( 0 ,P. clams) and Academy Bay ( 0 ,p . in the Galapagos; (b) Uraba, Gulf of Panama ( 0 , E gieantea), Uva-1 ( 0 , E slams) and Uva-56 ( 0 , E clams) Gulf of Chiriqui, Panama. The time stratigraphy is assigned using both the coral density banding as observed through x-radiography and the seasonal oxygen isotope cycles (after Dunbar et al., 1988). February-March are typically the months of lowest temperatures in the Gulf of Panama and highest temperatures in the Gulf of Chiri ui and at the Galapagos. The year assi ments were therefore made at 180,120 maxima for the Uraba data set and at k80/160minima for the other data sets and confirmed by the position of one major growth band between isotope peaks. The precision on age assignments is estimated at 3 months.

a)

246 However, the relative severity of the ENSO events is not manifest by these data. On the scale of Quinn et al. (1987), the 1982-83 event was longer and more severe (higher SST) than the 1972-73 event, which in turn was longer than the 1976 event. The 6180 data, however, displayed similar seasonal records for the 1976 and 1982-83 events. The intermediate ENSO of 1972-73 was marked by the lowest 6180 values in the Academy Bay coral and values equal to the 1982-83 event in the Champion Island coral. We suspect that the reason the corals did not adequately record the catastrophic 1982-83 event was due to the unprecedented SST of 3O-3l0C,which persisted for at least 3 months in the Galapagos. Bleaching of the corals occurred and accretion of calcium carbonate ceased under these conditions. Much milder conditions prevailed during the 1972-73 and 1976 events, which did not cause bleaching of corals in the Galapagos. Seasonal variation of 6180 ratios was greater in corals from the coast of Panama than in the Galapagos (Fig. 4b), and ranged from an average of 1.g0/oo in the Gulf of Panama (Uraba Island) to l.lO/oo in the Gulf of Chiriqui (Uva Island).

The greater range in the Gulf of Panama reflects the 5" to 8°C

decrease in water temperature during seasonal upwelling as well as the dry season/wet season contrast in salinity. In the Gulf of Panama, Dunbar and Wellington (1981) have estimated that about 30% of the seasonal isotopic variation in branching corals results from salinity changes, and the remainder from temperature. The peaks of isotopic enrichment or depletion are offset by about 4 to 6 months between the Gulf of Chiriqui and Gulf of Panama, as predicted from consideration of the thermal regimes (Fig. 2). As observed in the Galapagos data, the seasonal isotopic range for the Uraba Island specimen is generally reduced during ENSO intervals. This is particularly true for the 1965, 1969, and 1982 events, and observed to a lesser extent in 1972. The relatively minor 1976 ENSO is not evident in either data set and is in fact characterized by some of the greatest enrichments observed in 6180 during the upwelling or cool months of the year. The reduced seasonal isotopic variation results from both lesser l80 enrichment during the upwelling period and lesser l80 depletion during the warmer months of the tropical wet season. The physical process that produces this effect is not yet clear, but it is evident that this type of attenuation of the isotopic signal will obscure the ENSO signal in annually averaged samples. In the Uraba specimen between late 1969 through early 1973, annual growth rates were reduced to about 4 mm/year from a twenty-year average of about 7 mm/year.

This reduction in

growth rate may reflect the deleterious influence of two strong ENSO events on the corals. The reduction in growth rate furthermore reduces the likelihood that the full range of environmental perturbations may be resolved from a coralline isotopic record. The Uva-1 data set reveals a shift to lower

247 180/160ratios during 1982 through early 1983. The cool season maxima and warm

season minima are shifted about 0.5O/oo to lower values relative to the 19731982 averages, corresponding to a seawater warming of about 2°C (Fig. 4b). 4.2 6I3C Results Annually-averaged 6I3C results appear in Figure 5 and seasonal 6I3C results appear in Figure 6. In general, Pavona clavus samples from both the Galapagos gieantea values are about

and Panama have about the same 613C values; the

l0/oo depleted in 6I3C and the Gardineroseris ulanulata samples are about ~ . ~ O / Oenriched O

in 6I3C relative to the P. clavus results.

It appears that

species specific offsets from equilibrium are the dominant control on this large range of values rather than differences in the 6I3C of total dissolved C02 in sea water. There are several other factors controlling the 6I3C value in coralline aragonite. The overall 6I3C signature of the surrounding sea water is considerably lower in waters whose origins are from subsurface water masses, e.g., equatorial surface waters (Kroopnick, 1985).

This could presumably

account for 0.2-0.3°/oo of the offset. Other factors that affect the 613C in skeletal material are ambient light as a function of coral depth in the water column (Weber and Woodhead, 1972; McConnaughey, 1986), cloud cover (Fairbanks and Dodge, 1979), position on the coral colony (McConnaughey, 1986; Wefer and

tI

I

1930

I

- I

1940

I

- - - I

1950

1960

4

1

1970

- ENS0 I

I980

YEAR Fig. 5. Annually-averaged 613C results for corals from Panama [OUraba (E pigantea), Gulf of Panama; mUva-A (G- planulata), rUva-1 (P. clavus), AUva56 (P. clavus ) , Gulf of Chiriqui] and the Galapagos Islands [OUrvina,@Hood,O Champion and OAcademy (all P. clams). Annual averages for specimens Uraba, Uva-1, Uva-56,Academy and Champion represent the mean isotopic composition of 5 to 16 individual analyses collected between successive February-Marchmarkers in the corals (as determined by density banding and isotope maxima/minima).

248 -4

-

-3

--

-2

--

-I

-

a Champion

P

6 "c

-4

Academy Bay

,

1

I

1970

I

I

1972

1

1974

I

I

I

1976

1

1

1978

-3

I

J - I

1

1

I

1982

1980

1984

YEAR

b -4

6'3C -3

-2

-1 I

1962

I

I

1964

1

l

1966

I

I

- -

1968

l

l

1970

I

1

1972

I

I

I

1974

I

1

1976

I

)

1978

I

1

1980

I

I

1982

I

I

1984

Year (Feb.-March)

Fig. 6. Seasonal 613C results for (a) Galapagos Islands: Champion Island ( O E clavus) and Academy Bay ( O E clavua) and (b) Gulf of Panama: Uraba Island ( 0 E gieantea) and Gulf of Chiriqui: Uva Island ( O U v a 56 and Uva 1, both clavus) ,

249

Piitzold, 1985), and shading from adjacent coral colonies. Excess C02 from fossil fuel consumption and biotic sources, admitted to the oceans over the past 100 or so years, has lowered the 613C of the surface sea water by about 0.So/oo in the North Atlantic (Druffel and Benavides, 1986).

This effect may

be present in the annual Uva-A record (Fig. 5 ) , though it is difficult to separate it from other effects that may also have contributed to the range in values noted. The subannual carbon isotope results from Uraba and Uva Islands (Fig. 6b) all show somewhat well-defined seasonal variations with a general tendency towards enrichment in 13C in aragonite accreted during January through April. As water temperatures are at a maximum in the Gulf of Chiriqui and a minimum in the Gulf of Panama during the tropical dry season, we attribute this response primarily to the low cloud cover prevalent over both Gulfs at this time. Small phase offsets between carbon and oxygen isotope minima and maxima are common and variable with the result that l80 - 13C scatterplots often reveal negligible correlation between the two isotope ratios. There is no unique carbon isotope anomaly evident in the seasonal data during ENSO events. 5 CONCLUSIONS 1. We have identified isotope anomalies in a number of coral specimens that show environmental perturbations during the major ENSOs of the past 25 years. 2. Stable oxygen and carbon isotopes do not correctly identify all ENSO events in an unequivocal fashion. 3.

Galapagos corals record higher average water temperature/lower average

salinity during ENSO years. 4.

Seasonal 6180 in Panama corals reveals most ENSO anomalies, but the signal

is complex and may not be readily apparent in annually averaged samples. 5.

An ENSO signature common to both Galapagos and Panama study sites is a

reduction in the seasonal range of 6180 values. 6.

Major ENSOs (as well as any major stress event) may result in cessation of

"normal" growth, thereby reducing the efficacy of the coral as an environmental recorder. 6 ACKNOWLEDGEMENTS We thank Mike Dehn, Sheila Griffin, C. Eben Franks and Danuta Kaminski for assistance with the isotope analyses. We thank Peter Swart and an anonymous reviewer for comments on the manuscript. We are grateful to Molly Lumping and Wanda Blackman for typing the manuscript and to Amy Witter for drafting the figures. This work was supported by a grant from the Petroleum Research Fund of the American Chemical Society (RBD), American Philosophical Society (GMW, RBD), and by NSF through Grant Nos. OCE-8315260 and OCE-8608263 (ERMD), and

2 50

OCE-8415615 (to P.W. Glynn).

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25 1

Druffel, E.M. and Linick, T.W., 1978. Radiocarbon in annual coral rings of Florida. Geophys. Res. Lett., 5: 913-916. Druffel, E.M. and Suess, H.E., 1983. On the radiocarbon record in banded corals: exchange parameters and net transport of 14C02 between atmospheric and surface ocean. J. Geophys. Res., 88: 1271-1280. Druffel, E.R.M. and Benavides, L.M., 1986. Input of excess C02 to the surface ocean based on 13C/12C ratios in a banded Jamaican sclerosponge. Nature, 321: 58-61. Dunbar, R.B. and Wellington, G.M., 1981. Stable isotopes in a branching coral monitor seasonal temperature variation. Nature, 293: 453-455. Dunbar, R.B., Wellington, G.M., Colgan, M. and Glynn, P.W., 1987. Galapagos massive corals: an annual record of eastern tropical Pacific climate during the past 400 years. EOS, 68: 1743. Emiliani, C,, Hudson, J.H., Shinn, E. and George, R.Y., 1978. Oxygen and carbon isotopic growth record in a reef from the Florida Keys and a deep-sea coral from Blake Plateau. Science, 202: 627-627. Fairbanks R.G. and Dodge, R.E., 1979. Annual periodicity of the l80/l6O and 13C/1fC ratios in the coral piontastrea annularis. Geochim. Cosmochim. Acta, 43: 1009-1020. Forsbergh, E.D., 1969. On the climatology, oceanography and fisheries of the Panama Bight. Bull. Inter-Am.Trop. Tuna Comm., 14: 49-385. Franzisket, L., 1970. The atrophy of hermatypic reef corals maintained in darkness and their subsequent regeneration in light. Int. Rev. Gesamten. Hydrobiol., 55: 1-12. Glynn, P.W., 1972. Observations on the ecology of the Caribbean and Pacific coasts of Panama. In: M.L. Jones (Editor), The Panamic Biota: Some Observations Prior to a Sea-level Canal. Bull. Biol. SOC. Wash., 2: 13-30. Glynn, P.W., 1977. Coral growth in upwelling and nonupwelling areas off the Pacific coast of Panama. Environ. Conserv., 11: 133-146. Glynn, P.W., 1983. Extensive bleaching and death of reef corals on the Pacific coast of Panama. Environ. Conserv., 11: 133-146. Glynn, P.W., 1984. Widespread coral mortality and the 1982/83 El Nido warming event. Environ. Conserv., 11: 133-146. Glynn, P.W. and Stewart, R.H., 1973. Distribution of coral reefs in the Pearl Islands (Gulf of Panama) in relation to thermal conditions. Limnol. Oceanogr., 18: 367-379. Glynn, P.W. and Wellington, G.M., 1983. Corals and Coral Reefs of the Galapagos Islands. University of California Press, Berkeley, 330 pp. Glynn, P.W., Druffel, E.M. and Dunbar, R.B., 1983. A dead Central American coral reef tract: possible link with the Little Ice Age. J. Mar. Res., 41: 605-637. Goreau, N.I. and Hayes, R.L., 1977. Nucleation catalysis in coral skeletogenesis. Proc. 3rd Int. Coral Reef Symp., Miami, 2: 439-455. Goreau, T.F., 1961. Problems of growth and calcium deposition in reef corals. Endeavor, 20: 20-39. Goreau, T.F. and Goreau, N.I., 1959. The physiology of skeleton formation in corals. 111. Calcium deposition by hermatypic corals under various conditions in the reef. Biol. Bull., 117: 239-250. Highsmith, R.C., 1979. Coral growth rates and environmental control of density banding. J. Exp. Mar. Biol. Ecol., 37: 105-125. Hubbard, D.K. and Scaturo, D., 1985. Growth rates of seven species of scleractinian corals from Cane Bay and Salt River, St. Croix, USVI. Bull. Mar. Sci., 36: 325-338. Hudson, J.H., 1981. Growth rate in Montastrea annularis: a record of environmental change in Key Largo coral reef marine sanctuary, Florida. Bull. Mar. Sci., 31: 444-459. Hudson, J.H., Shinn, E.A., Halley, R.B. and Lidz, B., 1976. Sclerochronology: a tool for interpreting past environments. Geology, 4: 361-364. Huston, M., 1985. Changes in coral growth rates with depth at Discovery Bay, Jamaica. Coral Reefs, 4: 19-25.

252 Isdale, P., 1984. Fluorescent bands in massive corals record centuries of coastal rainfall. Nature, 310: 578-579. Jaap, W.C., 1979. Observation on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull. Mar. Sci., 29: 414-422. Jokiel, P.L. and Coles, S.L., 1977. Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol., 43: 201-208. Kawaguti, S . and Sakamoto, D., 1948. The effect of light on the calcium deposition of corals. Bull. Oceanogr. Inst. Taiwan.,4: 65-70. Knutson, D.W., Buddemeier, R.W. and Smith, S.V., 1972. Coral chronometers: seasonal growth bands in reef coral. Science, 177: 270-272. Kogelschatz, J . , Solorzano, L., Barber, R., Mendoza, P., 1985. Oceanographic conditions in the Galapagos Islands during the 1982/1983 El Niiio. In: G. Robinson and E.M. del Pino (Editors), El Niiio in the Galapagos Islands: the 1982-1983 Event. Publication of the Charles Darwin Foundation for the Galapagos Islands, Quito, Ecuador, pp. 91-123. Konishi, K., Tanaka, T. and Sakanoue, M., 1981. Secular variation of radiocarbon concentration in seawater: sclerochronological approach. Proc. 4th Int. Coral Reef Symp., Manila, 1: 181-185. Kroopnick, P.M., 1985. The distribution of 13C of sigma-C2 in the world oceans. Deep-sea Res., 32: 57-84. Linn, L.J., Druffel, E.R.M. and Delaney, M.L., 1987. Trace metal concentrations in a Galapagos coral: an ENS0 indicator. EOS, 68: 1743. Madzsar E.M Benninger, L.K. and Freeman, J . H . , 1987. Combined fallout 90Sr and '239*2d0Puin the annual bands of Montastrea annularis, Broward County, Florida. EOS, 68: 1743. McConnaughey, T.A., 1986. Oxygen and carbon isotope disequilibria in Galapagos corals: isotopic thermometry and calcification physiology. Ph.D. Dissertation, University of Washington, 340 pp. Minnis, S.A., 1986. Stable isotope profiles of hermatypic corals: indicators of changing environmental conditions in upwelling and non-upwelling regions o f the Eastern Tropical Pacific. (unpubl.) M.S. Thesis, Rice Unviersity, Houston, Texas, 122 pp. Muscatine, L. and Cernichiari, E., 1969. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull., 137: 506-523 Nozaki, Y., Rye, D.M., Turekian, K.K., and Dodge, R.E., 1978. 13C and I4C variations in a Bermuda coral. Geophys. Res. Lett., 5: 825-828. PBtzold, J . , 1984. Growth rhythms recorded in stable isotopes and density bands in the reef coral Porites lobata (Cebu, Philippines). Coral Reefs, 3: 8790. Pearse, V.B., and Muscatine, L., 1971. Role of symbiotic algae (zooxanthellae) in coral calcification. Biol. Bull., 141: 350-363. Porter, J.W., Battey, J.F. and Smith, G . J . , 1982. Perturbations and change in coral reef communities. Proc. Nat. Acad. Sci., 79: 1678-1681. Purdy, C., Druffel, E.R.M. and Livingston, H., 1987. Strontium-90 activities in banded corals from the North Atlantic. EOS, 68: 1743. Quinn, W.H., Neal, V.T. and Antunez de Mayolo, S.E., 1987. El Nitio occurrences over the past four and a half centuries, J . Geophys. Res., 92: 14,449-14, 461.

Roberts, L., 1987. Coral bleaching threatens Atlantic reefs. Science, 238: 1228-1229. Roberts, L., 1988. Corals remain baffling. Science, 239: 256. Rogers, C.S., 1979. The effect of shading on coral reef structure and function. J . Exp. Mar. Biol. Ecol., 41: 269-288. Schneider, R.C. and Smith, S.V., 1982. Skeletal Sr content and density in Porites spp. in relation to environmental factors. Mar. Biol., 66: 121-131. Shen, G.T. and Boyle, E.A., 1987. Lead in corals: reconstruction of historic industrial fluxes to the surface ocean. Earth Planet. Sci. Lett., 82: 289304. Shen, G.T., Boyle, E.A. and Lea, D.W., 1987. Cadmium in corals as a tracer of historical upwelling and industrial fallout. Nature, 328: 794-796.

253 Smith, D.C., Muscatine, L. and Lewis, D.H., 1969. Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbiosis. Biol. Rev., 44: 17-90. Smith, S.V., Buddemeier, R.W., Radalje, R.C. and Houck, J.E., 1979. Strontiumcalcium thermometry in coral skeletons. Science, 204: 404-407. Stoddart, D.R., 1962. Catastrophic storm effects on the British reefs and cays. Nature, 196: 512-515. Stoddart, D.R., 1969. Ecology and geology of recent coral reefs. Biol. Rev., 44: 433-498. Swart, P.K., 1983. Carbon and oxygen isotope fractionation in scleractinian corals: a review. Earth-Sci. Rev., 19: 51-80. Toggweiler, J . R . , 1983. A six zone regionalized model for bomb-radiotracers and Cog in the upper kilometer of the Pacific Ocean. Ph.D. Dissertation. Columbia University. Toggweiler, J . R . and Trumbore, S . , 1985. Bomb-test Sr-90 in Pacific and Indian Ocean surface water as recorded by banded corals. Earth Planet. Sci. Lett., 74: 306-314. Weber, J.N. and Woodhead, P.M.J., 1972. Temperature dependence of oxygen-18 concentration in reef coral carbonates. J . Geophys. Res., 77: 463-473. Weber, J.N., White, E.W. and Weber, P.H., 1975. Correlation of density banding in reef coral skeletons with environmental parameters: the basis for interpretation of chronological records preserved in the coralla of corals. Paleobiology, 1: 137-149. Wefer, G. and Patzold, J . , 1985. 13C/12C record of atmospheric C02 increase in a coral head from the Philippines (Cebu). Scripps Institution of Oceanography Reference 85-31: 133-135. Weil, S.H., Buddemeier, R.W., Smith, S.V. and Kroopnick, P.M., 1981. The stable isotopic composition of coral skeletons: control by environmental variables. Geochim. Cosmochim. Acta, 45: 1147-1153. Wellington, G.M., 1982. An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia, 52: 311-320. Wellington, G.M. and Glynn, P.W., 1983. Environmental influences on skeletal banding in eastern Pacific (Panama) corals. Coral Reefs, 1: 215-222. Wells, J.W.,1957. Coral reefs. Mem. Geol. SOC. A m . , 67: 609-631. Wethey, D.S. and Porter, J.W., 1976. Sun and shade differences in productivity of reef corals. Nature, 262: 281-282. Woodley, J.D. and 17 co-authors,1981. Hurricane Allen's impact on Jamaican coral reefs. Science, 214: 749-755. Wyrtki, K., 1964. The thermal structure of the eastern Pacific Ocean. Dtsch. Hydrogr. Z . , 8: 1-84. Yonge, C.M. and Nicholls, A.G., 1931. Studies on the physiology of corals. VI. The structure, distribution and physiology of the zooxanthellae. Sci. Rep. Great Barrier Reef Exped., 1: 177-211.

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TRACE ELEMENT INDICATORS OF CLIMATE VARIABILITY IN REEF-BUILDING

cow

G. T. SHEN and C. L. SANFORD Lamont-Doherty Geological Observatory of Columbia University, Palisades, New York 10964 (U.S.A.)

ABSTRACT Shen, G.T. and Sanford, C.L., 1989. Trace element indicators of climate variability in reef-building corals.

An active couple exists between the atmosphere and surface ocean to produce regional-to-global changes in earth's climate. While numerous terrestrial recording systems have revealed meteorological perturbations over the continents, however, historical changes in the surface ocean are largely unknown. This contribution describes recent efforts to develop new paleochemical indicators trapped in the aragonite lattice of reef-building corals. The methodology requires chance combinations of circumstances (crystal lattice compatibility and mechanisms that promote variable surface ocean composition) and great analytical care, yet several applications have surfaced in relation to El Niiio. Cadmium and manganese comprise paleo-upwelling indicators that display great sensitivity in the eastern tropical Pacific Ocean. Barium levels in Caribbean corals reflect seasonal river discharge from South America that may in turn be modulated by the El Niiio Southern Oscillation. Manganese and barium may also track lateral movement of water masses as in continental shelf water advection or river plume migration. Finally, coralline cadmium is seen to respond to ENSO-driven rainfall anomalies in the western equatorial Pacific, though the mechanism behind this response is not clear.

1 INTRODUCTION Clues as to previous climates in Earth's history have come in various forms from the land and sea. Among the recording substrates that exist in the oceans, calcareous plankton have proven to be most useful. The shells of fossil foraminifera in deep-sea sediments have, for example, been used to reconstruct changes in glacial-interglacial ice volumes and ocean temperature and circulation. Periodicities unmasked by such studies have implicated orbital forcing as an important trigger in resetting climate on time scales of tens of thousands of years. In the nearer term past, skeletons of reef-building corals offer the time resolution necessary for detailed reconstructions of climate effects on the surface ocean. Druffel and co-

workers describe aspects of coral growth and use of stable oxygen and carbon

256

isotopes as El Niiio indicators in a separate contribution in this volume. This study introduces the potential of several skeletally-bound trace elements as complementary chemical indicators of El Niiio-related perturbations to the surface ocean. Elements of particular interest include cadmium, manganese, and barium. Depending on the locale, these and possibly other trace seawater constituents may be used to reconstruct historical changes in such diverse phenomena as winds, upwelling, rainfall, river discharge, and advection of surface ocean waters. 2 MINOR AND TRACE ELEMENT GEOCHEMISTRY OF CORALS Chemical studies of fossil marine carbonates to reconstruct paleo-environments began with the alkaline earth metals Mg, Sr, and Ba (Odum, 1951; Chave, 1954; Turekian, 1955; Thompson and Chow, 1955; and many others). The rationale behind investigation of these elements was their chemical similarity to Ca, and expected uptake in CaC03 minerals. Eventually, wider coverage of elements in aragonitic corals included the alkali metals (Amiel et al., 1973; Swart, 1981), various transition metals (Harriss and Almy, 1964; Veeh and Turekian, 1968; Livingston and Thompson, 1971; St. John, 1974), uranium (Broecker, 1963; Gvirtzman et al., 1973; Flor and Moore, 1977; Cross and Cross, 1983), and the rare earth elements (Scherer and Seitz, 1980; Shaw and Wasserburg, 1985). Results of many of these pioneering studies, however, must be interpreted carefully insofar as inferred host phases and incorporation mechanisms. Particularly in the case of the transition and rare earth metals where lattice abundances in corals are in the ppmppb range, tissue or contaminant phase inventories can rival or exceed structurallybound metal levels. A great variety of coralline elements have been identified where because of size and/or charge imbalances, incorporation mechanisms are very uncertain (e.g. Na+, K+, Nd+3). Chemical complexation with seawater anions also raises questions as to deposition mechanisms, especially in the case of metals that exist as anionic complexes (e.g. U, V - see Swart and Hubbard, 1982; Shen and Boyle, 1987). In considering skeletal components as paleoenvironmental indicators, it is imperative that the constituents reflect conditions at the time of carbonate deposition and that they be reproducibly analyzed. This largely rules out organically-bound markers because the organic content of corals is expected to vary with species, location, and age. Studies of metal adsorption (e.g. Cd2+, Mn2+, Zn2+, Co2+) on inorganic calcium carbonate have established that surface coatings may be important, particularly when chemisorption and precipitation co-occur as endpoints of a continuum process (Kitano et al., 1976; McBride, 1979; Morse, 1986; Comans and Middelburg, 1987; Davis et al., 1987, and many others). Still other studies suggest that substitution of metal ions may occur heterogeneously via trace secondary phases (e.g. calcite) (Amiel et al., 1973; Houck et al., 1975; Angus et al., 1979; Swart and Hubbard, 1982). Fortunately, the extent of diffusion, precipitation,

257

and/or recrystallization in biogenic marine carbonates often appears limited, as attested to by paleochemical studies of foraminifera and corals (Druffel and Linick, 1978; Dodge and Gilbert, 1984; Boyle, 1986; Shen and Boyle, 1987, 1988) and successful radiometric dating applications (21oPb, 228Ra, 14C, U-Th), which rely upon closed system behavior (Dodge and Thomson, 1974; Chappell and Polach, 1972; Edwards et al., 1987). Even were surface chemisorbed/precipitated metals to comprise persistent phases (Amiel et al., 1973), though, they would prove difficult to isolate in the presence of other heterogeneous surface phases, and thus are not likely to offer much hope as paleochemical indicators. Conversely, latticesubstituted components cannot be added or removed unless mineral dissolution or alteration occurs, so they have potential as permanent markers. Demonstration of true lattice substitution by elements at ppb levels is not possible by conventional analytical means. Instead one must appeal to physicochemical constraints, observed structures of related minerals, and empirical measures of trace element abundances and partitioning. For example, the ionic radius of Cd2+ is nearly identical to that of Ca2+, as is cadmium's outer electron configuration (4d105d2 versus 4 ~ 2 ) . Furthermore, rhombohedral CdC03 is a known mineral phase (otavite) that exhibits solid solution behavior with calcite (Chang and Brice, 1971). Paleochemical studies of benthic foraminifera by Boyle (1988) have revealed a consistent partitioning of Cd between ocean bottom waters and shells of 4 different species ( K ~ = 2 . 9 ) . Taken together, this information suggests that it is reasonable to assume Boyle's measured Cd levels to be lattice-bound. Furthermore, it is reasonable to envision that parallel Cd substitution in aragonite is possible, though little is actually known of such solution behavior. Structural uptake is argued by Shen et al. (1987) and Shen and Boyle (1988) in their determination of baseline Cd levels in corals from the Florida Keys, Bermuda, and Galapagos Islands. Reported distribution coefficients for divalent cations in aragonitic corals, however, vary widely in the literature and have thus caused controversy as to inferred controls over precipitation. Howard and Brown (1984) interpret this observed variability as evidence of extraskeletal uptake and conclude that structural inclusion by corals does not occur for most metals. Actually, some of the historical discrepancies can be trimmed by correcting earlier estimates of KD using more recently determined concentrations of metals in seawater. Specifically, reliable measurements of Mn, Pb, Cd, Fe, Cu, Zn, Co, and rare earth elements have largely been attained only within the last decade. Elements whose concentrations in seawater are sensitive to contamination (all of the above) may also be prone to contamination as solid aragonitic components because of their trace levels. Retrospective corrections of this nature are not possible. In spite of these complications, observations have indicated that the larger alkaline earth cations (Sr2+, Ba2+, Ra2+) are indiscriminately precipitated from seawater by corals (e.g. Veeh and Turekian, 1968; Buddemeier et al., 1981). In comparing the metal

258

content of skeletons and tissues of both hermatypic and ahermatypic corals, Buddemeier and co-workers (198 1) further concluded that the calcification process is insensitive to bulk tissue concentrations of metals. Extension of this precipitation behavior to several transition metals and possibly rare earth elements has recently been proposed by Shen and Boyle (1988). Such a uniform mineralization process is very convenient for reconstructing seawater paleoenvironments, but what is the physicochemical basis for such distributions? Let us consider thermodynamic controls on uptake of a few of the closest aragonite-compatible elements to see whether C a C 0 3 precipitation by corals is an equilibrium process. If we express metal substitution as:

the resulting equilibrium constant follows

where y s are solid and solution phase activity coefficients, fs represent the fraction of dissolved metal available in uncomplexed divalent form, and Kapp is an apparent equilibrium constant. We can re-express K as the ratio of solubility products for C a C 0 3 (aragonite) and MCO3 which yields the following expression for the apparent constant (or apparent distribution coefficient):

259

Equation (3) can be used to predict the relative equilibrium distributions of various metals in aragonite. Table 1 lists the computed magnitudes of Kapp f o r eight metals that bracket Ca2+ in ionic radius, given our best estimates of yand f. The predicted thermodynamic Ks span 3 orders of magnitude, primarily as a result of large differences in solubilities of the metal carbonates (e.g. PbC03 is sparingly soluble in comparison to SrC03). In contrast, observed distribution coefficients in corals lie conspicuously close to unity. There exist large uncertainties in the activity and species complexing coefficients used in these simple calculations (particularly for Y ~ c o -3 see Stumm and Morgan, 1981, pp. 287-291), however, the results suggest that kinetic control via rapid coprecipitation may supersede thermodynamic equilibrium.

TABLE 1 Predicted thermodynamic and observed distribution coefficients for trace elements in aragonitic corals

Sr2+

1.42 1.29 1.26

ca2+

1.12

Ba2+ Pb2+

1.10 0.96 0.92 0.90 0.90

1.20 8.1 104 6.5

0.86 0.03 0.71

1.3 3 103 5.6

0.81 1.2 io3rd] 12 2.9 x lo2 58 60

0.03 0.58 0.69 0.58 0.46

46 8.6 2.5 x lo2 4.1 34

=1 0.1-1 1-30 =1 200 m in December 1983 (GuillCn et al., 1985). In northern Chile it dropped to 100 - 150 m depth (Blanco and Dfaz, 1985). At the peak of the event, oceanographers traced the warming down to 800 m (GuillCn et al., 1985), and in some cases even beyond 1,000 m (Leetma et al., 1987). A secondary effect of the deepening of the thermocline, and thus the increase of the mixed layer, may have been the dispersal and deepening of phytoplankton populations, which in some cases may have been transported out of the euphotic zone. However, sunlight penetrates the

328

4

3 2

1 0 26 24 22 20 18 16 14 12 10 Aug-81

Sep-82

Oct-83

Nov-84

Dec-85

Jan-87

Feb-88

Fig. 2. Changes in near-bottom oxygen concentration and sea temperature at 15 m depth in Anc6n Bay, Peni, during the period 1981 - 1987. Shaded areas: EN 1982-83 and EN 198687. clear EN waters to a greater depth than the turbid upwelling waters found during normal periods. Nearshore in northern Peni and off Ecuador, where torrential rainfall increased the river discharge, turbidity and sedimentation of coastal waters were strongly elevated during EN, and locally the salinity of surface waters was reduced by about 1 O/OO (Leetma et al., 1987). Generally, however, salinity changes in either direction -- clearly detectable as inflow of equatorial or oceanic waters -- occurred at a lower range, and did not seem to have as important an effect on the upwelling flora and fauna (see below) as did changes in, for example, temperature, sea level and dissolved oxygen (Arntz, 1986; Arntz and Tarazona, 1988). Dissolved oxygen was reduced somewhat in the surface waters off Peni, from normal values > 6 ml l-1 to values around 5 ml l-1, whereas at depths of about 200 m the intruding waters induced a strong 0 2 increase (Fig. 2) in areas that are normally hypoxic or even anoxic (Rosenberg et al., 1983; Arntz et al., 1985; Tarazona et al., 1985a). A comparison of R.V. "Humboldt" data from the cruises 8103/04 (1981, normal conditions) and 8212/8301 (1982-1983, EN) indicated a 3 to 7 fold increase in dissolved oxygen at the seafloor below 50 m off northern and central Peni during EN. At depths c 100 m, 0 2 values often exceeded 3 ml l-1, and between 100 and 200 m they reached 2.5 ml 1-1 (Arntz et al., 1985). Increased

329 oxygenation during EN has been observed all along the Peruvian continental shelf (Fig. 3); there are, however, marked differences between strong and weak events (GuillCn et al., 1985). In contrast to these conditions, surface waters off northem Chile during EN 1982-83 revealed 0 2 values < 1 ml l-1 (Alvial, 1985; Fonseca, 1985; Fuenzalida, 1985).

3 THE PELAGIC SUBSYSTEM 3.1 Phvto- and zooulankton The deepening of the thermo- and numclines, which hampered the transport of numents into the euphotic layer, the strong warming of the surface waters and possibly also the slight reduction of dissolved oxygen in the uppermost offshore layers, induced important changes in the pelagic system. The most obvious consequences were a drastic reduction of biomass and production of phytoplankton, equally strong changes in species composition, and a "tropicalization" due to the transport of equatorial and oceanic species poleward and towards the coast (Barber and ChBvez, 1983; Avaria, 1985; Muiioz, 1985; Rojas de Mendiola et al., 1985).

1

'

1

'

I 3-

1

'

-

1

'

1

'

1

'

1

'

2-

1 10

t-

I

3

1981

I

5

\ : ; \ I

I

7

I

1

I

I

9

LATITUDE

11

( O

I

I

13

1985 I I

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15

S 1

Fig. 3. Latitudinal changes of temperature and dissolved oxygen close to the seafloor at 91 140 m depth during EN (1982-83, 1987) and non-EN years. Peruvian coast, summer values only with the exception of 1982 when spring (November) data were included also.

17

330 According to Peruvian and Chilean net plankton samples during EN 1982-83, the small diatoms characteristic of the upwelling region gradually disappeared and were replaced by (sub)tropical dinoflagellates, coccolithophorids and large diatoms. The extent of these changes depends on the strength of the EN event; during EN 1982-83 it occurred over > 15 degrees of latitude and in a coastal fringe comprising several hundred kilometers. The retreat of the autochthonous diatoms, associated with a reduction of phytoplankton biomass, occurred stepwise (Avaria, 1985; Avaria and Muiioz, 1987). Plankton recovery in most areas off Peni and northern Chile began in September 1983 (Avaria et al., 1988). However, plankton net catches failed to record the minute (picoplankton to nanoplankton) single-celled species that have recently been found responsible for a very large part of the carbon production in tropical seas (Joint, 1986; Stockner, 1988). Although we have not found any literature referring specifically to EN 1982-83,these small organisms must have been a major component of the (sub)tropical plankton community that replaced the traditional upwelling community during this event. The changes at the base of the food web -- reduced food availability and exchange of the autochthonous phytoplankters for both minute and larger species equally unsuitable as food -influenced the higher levels of the food chains, i.e. zooplankton and pelagic fish feeding on plankton, in an unfavorable way. At the same time, the zooplankton and pelagic fish species of the upwelling system were affected themselves by the increased water temperatures. Within these groups, too, the local species were displaced or suffered from mortality, and were replaced by tropical species. In particular there was a change from herbivorous copepods, the biomass of which was reduced to about one-sixth the value before EN, to chaetognaths and other large, predatory organisms such as salps, jellyfish and siphonophores (Tsukayama and Santander, 1986; Carrasco and Santander, 1987). In many cases, even these large forms could not make up for the biomass loss caused by the disappearance of the autochthonous small copepods; since most of the invading plankters were voracious predators, they may even have contributed considerably to the general shortage of food. The reduction of the local holoplankters and the increase of tropical holoplanktonic organisms were accompanied by a reduction of the pelagic larvae of benthic organisms (meroplankton), which spend only part of their lives in the water column. At the same time tropical meroplankton, such as the larvae of shrimps, extended their areas of distribution over several degrees of latitude towards the south (Tarazona et al., 1985b; Carrasco and Santander, 1987). In Anc6n Bay, Peni (ca. 12"N) meroplankton increased before and during the initial phase of EN (Fig. 4) due to the intrusion of large numbers of gastropod larvae. During the first peak of the thermal anomaly, the abundances of gastropod larvae collapsed, and meroplankton densities were low. After EN, bivalve larvae became prominent for some time, and the rapid recovery of intertidal mussel populations followed (see below).

3.2 Pelagic fish Previous EN events to some extent favored the sardine (Surdimps sagax), which contrary to the anchovy (Engruulis ringens) tends to avoid the cold water plumes of the upwelling

33 1

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Jul-83

Jan-84

Aug-84

Fig. 4. Changes in numbers of total meroplankton (above) and of planktonic gastropod and bivalve larvae (below) at a shallow water station in Anc6n Bay between 1981 and 1984. The values correspond to 10 vertical hauls between 15 and 0 m depth taken by standard net and pooled, mesh width 200 pm. centres (Zuzunaga, 1985). However, the 1982-83 event had negative biological effects on both pelagic fish species of greatest commercial importance in the Humboldt Current area. Off Ecuador, relative values of sardine abundance based on monthly standard catches dropped sharply between October 1982 and August 1983 (Menz, 1986) whereas the sardine biomass estimated by echoacoustics off Peni increased between March and April (Santander and Zuzunaga, 1984), leading the latter authors to the assumption that part of the sardine stock must have migrated southward. Off Peni, towards the end of 1982, both sardines and anchovies reacted to the warming and the impoverishment of the epipelagic zone with migrations of different kinds (Zuzunaga, 1985; Amtz, 1986). Part of the shoals withdrew to the remnants of upwelling centres, which at that time still contained some cool, nutrient-rich water close to the shore (cf. section 2). Continued deepening of the thermocline, however, converted these areas into traps, and the fishery took large catches from the densely aggregated shoals as it had done in 1972, when on a single day 170,000 t of anchovies were caught by the Peruvian purse seiner fleet (J. Valdivia, 1978). Another part of the anchovy and sardine populations withdrew to deeper water, often > 100 m depth, where there was little food and a lower oxygen content than there is normally at the surface, but where the temperatures were also lower than in the epipelagic zone (Santander and Zuzunaga, 1984; Amtz, 1986). A third group, especially

332 the sardines, avoided the unfavorable conditions off Peni by migrating even further southward where the impact of EN was less dramatic (Caiibn, 1985). Off northern Chile, where the temperature increase was lower, the sardines remained close to the surface and to the shore (Martinez et al., 1989). There, the feeding conditions were more favorable than at greater depth and further offshore, but they could be taken by the purse seiners, which fish only in the uppermost 50 m (cf. section 3.3). The biological effects on the anchovy off Chile seem to have been similarly as negative as those off Peni, judging from the extremely low catches during 1983 (FAO, 1989). Tagging experiments have been carried out on a relatively small scale; the few data from sardines that were tagged off Peni and recovered later off Chile confirm that southward migration does indeed occur (Torres et al., 1985). The disruption of the pelagic food web and the withdrawal of the pelagic shoaling fish into areas that were almost devoid of food, warmer and less oxygenated than their normal habitat were reflected in changes in stomach contents, poor condition, reduced growth, reduced spawning activity and extremely poor spawning success of both anchovy and sardine. Instead of feeding on their normal food, i.e. small herbivorous copepods and diatoms, sardines off Peni in 1982 mainly fed on subtropical camivorous copepods and dinoflagellates, which occurred in much lower densities, and even fed on fish (Alamo et al., 1988). The average stomach contents were greatly reduced, which led to weight losses of 10 - 20 %, and in extreme cases up to > 30 %, in the sardines in Peni (Dioses, 1985) and weight losses of around 20 % in adult sardines in northern Chile (Martinez et al., 1984). Poor sardine condition off northern Chile was recorded throughout 1983 (Mujica et al., 1985; Alcocer and Kelly, 1987). The consequence was stagnation of growth (Aguayo et al., 1985; CCdenas and Chipollini, 1988), reduction of lipids in the body tissues (Caiibn, 1985; Romo, 1985), and reproductive failure (Pastor, 1984; Santander and Zuzunaga, 1984; Retamales and Gonzlilez, 1985) both off Peni and Chile during 1983. However, the sardines demonstrated partial recovery towards the end of that year and exhibited normal spawning in 1984. Anchovies off Peni lost 30 % or more of their weight (Santander and Zuzunaga, 1984). A complete breakdown in reproduction of the Peruvian part of the anchovy stock occurred throughout 1983 (Santander and Tsukayama, 1984). No published anchovy data seem to be available over this period in Chile. The other two important shoaling fish species of the Humboldt upwelling area, horse mackerel (Truchurusmurphyi) and Spanish mackerel (Scomberjuponicus peruanus), live further offshore than anchovy and sardine under normal conditions. The occurrence of mackerel larvae is positively correlated with SSTs (Muck et al., 1987). During EN the two species approached the shore all the way from Ecuador to Chile. Nearshore migrants of S. juponicus were reported as far south as Puerto Chacabuco (45'30's) in Chile where in midJanuary 1982 a shoal of "caballa" (Pacific mackerel) suffered massive mortality close to the shore presumably from a combination of low 0 2 concentration, low salinity and high temperature (Zamaet al., 1984). Mackerels, like anchovies, often stayed beyond the reach of seines as they remained at greater depths (Vflchez et al., 1988). Neither species suffered from a scarcity of food because they inhabit oceanic waters that are much poorer in food than up-

333 welling areas, and they feed mainly on fish (Konchina, 1982; Muck and Sinchez, 1987). Fish (weak anchovies and sardines) were not scarce during EN in deeper water. Accordingly, horse and Spanish mackerels lost at most 10 % of their body weights (Dioses, 1985), spawning was normal, and the density of larvae even increased (Santander and Zuzunaga, 1984). A large number of predatory tropical fish invaded the pelagic zone of the Peruvian-Chilean upwelling area in 1983 (Hoyos et al., 1985; Kong et al., 1985; VClez and Zeballos, 1985), among them sierra (Scomberomorus sierra), skipjack (Karsuwonuspelamis), yellowfin tuna (Thunnus albacares), dolphinfish (Coryphaena hippurus) and different species of oceanic sharks. Bonito (Sardu chiliensis chiliensis and, possibly also, S. orientalis , which may have extended its range to the south during EN; see Pauly et al., 1987), which had virtually disappeared after the decline of its principal anchovy food, in the first half of the seventies, once again returned to Peruvian coastal waters. All these species may have contributed substantially to an increase in predation on shoaling fish. Most of the invaders disappeared from the upwelling area when the water temperatures returned to normal. Close to shore another pelagic fish species, the silverside (Odontesthes regia regia), which is important in the artisanal driftnet fishery, virtually disappeared from Peruvian waters in January 1983 and did not return until 1985 (cf. Fig. 14, section 4.3). It is not known if these fish migrated southward or withdrew to deep water. 3.3 Pelagic fisheries The effects of EN on the pelagic (i.e. industrial) fisheries were predominantly negative, as can be seen from the reduction of Latin American fish catches by about 3 million t (metric tons) as compared with 1982 (when they were 11.6 million t), a decrease in fish meal production of 64 % in the first 10 months of 1983, and the collapse of fish oil production in that year. However, there were important regional differences. Off Ecuador, the purse seine fishery on Etrumeus teres (Round herring) and other small fish collapsed in 1983; however, 25,000 t of horse mackerel were caught, which in normal years conmbutes minimally to the catches. Off Peni, landings of pelagic fish by the purse seine fleet declined from 3.3 million t in 1982 (of which 1.7 million t were anchovies and 1.5 million t were sardines) to 1.4 million t i n 1983 (1.1 million t sardines and 0.1 million t anchovies; the latter from the first quarter of the year and close to the Chilean border). In 1984 the Peruvian anchovy catches were practically nil, whereas the sardine catches doubled to 2.8 million t. In 1986, the anchovy landings were 3.5 million t and similar to the 1974-1976 level. The sardine catches dropped to only half the landings of the previous year. The horse and Spanish mackerel landings increased during and after EN 1982-83, reaching 270,000 t in the post-EN year 1984, but they never approached the 1977-78 record catches of nearly 0.5 million t (Fig. 5 ) . The Peruvian anchovy landings indicate that each EN after 1960 has had a marked effect on the availability of the stock to the purse seine fishery; even warmer years like 1969 and 1979, which are not considered EN years according to strict thermal criteria, caused a decline in the catches (Fig. 5). However, the landing statistics also reveal that the Peruvian anchovy catches were at a very low level before the appearance of EN 1982-83. An estimate of the Peruvian

334 .. .. .. .. .. .. ., .. .. ... ... ... ... ~

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Fig. 5. Annual landings of the principal pelagic shoaling fish off Per6, 1951-1987. Shaded areas: EN and other years with positive temperature anomaly > 2'C. spawning population of anchovy in 1981, based on the "egg production method", revealed an extremely low value of < 2 million t (Santander et al., 1984) indicating that an excessive share of the stock was being taken at that time. Northern Chile's anchovy catches started in the early sixties and were around 1 million t, revealing a certain impact of larger EN as occurred in Peni, until they dropped to a very low level during EN 1972-73 (Jordh, 1983). During the past five years they contributed < 5 % to total Chilean pelagic catches except in 1986, when they reached a record low value (33 %; Martinez et al., 1989). However, in 1987 catches declined again during the occurrence of another EN. Low anchovy catches per unit of effort during EN years (Serra, 1986) indicate reduced accessibility of the stock to the fisheries during these times, as occurred in Peni (see section 3.2). Sardine (S. s a g a ) catches in Ecuador started to decline in October 1982 and remained at a very low level until August 1983 (Jimknez and Herdson, 1984). After EN 1982-83, landings increased sharply despite the fact that the size of the purse seine fleet remained the same (Maridueiia 1986 fide S e r a and Tsukayama, 1988). In Peni, sardine catches also declined in October 1982, a consequence of reduced availability to the fisheries. They reached their lowest values in June 1983. Catches per unit of effort are not available, but the size of the industrial fleet (= 350 purse seiners) remained about the same during 1981 - 1985 with a reduction of

335 one-third in 1984. Interestingly, the landings in 1983 and 1984 increased steeply (Fig. 6) showing that large quantities of sardines had again become available to the fishery almost immediately after the return to normal conditions. Off Chile, the southward migration of the sardines, their nearshore concentration and the presence of shoals in more superficial waters favored purse seining contrary to the situation in Ecuador and Perli. As a result, Chile became one of Latin America's most important fishing nations. From the 3.9 million t catch in 1983,2.8 million t were sardines (1.0 million t more than in the preceding year). From this total, 3.2 million t were processed into fish meal and oil.

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a

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a 0.5 0 1964

1968

1972

1976

1980

1984

1988

Fig. 6. Annual landings of "sardina", S. sugar, in the countries of major EN impact, 1964 1987. Shaded areas: EN and other years with positive temperature anomaly > 2'C.

Despite these immediate positive effects on the sardine fishery, the medium-term effects were unfavorable. The catches declined by 33 % in 1987 due to continued overfishing, and because the 1983 yearclass, which should have entered the fishery that year, was absent (Martinez et al., 1989). The 1983 year class recruitment failure was confirmed by a population analysis carried out by Martinez and co-workers. Overfishing was caused by a tremendous increase (850 %) in the number of vessels and the modernization of the fishing fleet. Accordingly, catches per unit of effort of sardines that had increased until the first half of 1983 declined by 58 % until 1988 (Martinez et al., 1989). The horse mackerel catches off Chile dropped from 1.5 million t in 1982 to 0.9 million t in 1983 because the fleet concentrated on the easily accessible sardines, and because part of the

336

horse mackerel stock migrated northward. Tropical immigrants such as dolphinfish and skipjack became locally important items of the artisanal fishery during EN, especially off Peni, but almost immediately disappeared from the area when the sea temperatures returned to normal. In 1983, dolphinfish catches reached over 30 t in Chimbote during several summer months, and > 100 t in Callao in May; skipjack landings in the same port were 113 t in April (Vtlez and Zeballos, 1985). Silverside catches, with > 20 t still landed in the port of Callao in December 1982, collapsed in January 1983 for two complete years. Apparently similar shifts occurred during former EN events although dolphinfish never were as abundant off Peni as in 1983 (Del Solar, 1983). 4 THE BENTHIC SUBSYSTEM 4.1 Macrobenthos 4.1.1 Hard bottoms and rockv shores Most of the information available on the impact of EN 1982-83 and 1986-87 on rocky shores is based on qualitative observations; only for hard bottom communities at Anc6n (1 1'46's) and Independencia Bay (14O15'S) are quantitative time series data available (Tarazona et al., 1985b, 19884 Romero et al., 1988). Unfortunately, quantitative sampling has not been continued after these EN events. In the following, reference to an unqualified recent EN refers to the severe event of 1982-83. Under normal, non-EN conditions the intertidal and shallow subtidal zones of the rocky shores of Peni and northern Chile are dominated by rich populations of algae, mytilids and balanids, which compete for the available space. The floral and faunal community smcture seems to be controlled by grazers (sea urchins, chitons, limpets and other gastropods) and predators (sea stars, brachyuran crabs and fish), respectively, resulting in a rather stable balance and the absence of space monopolization by just one group of organisms (Castilla, 1981; Hoyos et al., 1985; Tokeshi et al., 1988, 1989a). Both the mytilid associations and large brown algae -- particularly LRssonia nigrescens and in deeper water "forests" of Macrocystis pyrifera -- provide many niches and refuges for numerous associated species. About

150 animal species live associated with the rhizoids of Lessonia spp.; they can reach densities of up to 8,000 and about 200 g wet weight per rhizoid (Romero et al., 1988). and over 90 species are associated with two, densely packed intertidal mussels Semimytilus algosus and

Perumytilus purpurutus (Paredes and Tarazona, 1980; Tarazona et al., 1988d; Tokeshi et al., 1989b). During EN 1982-83 the balance between the different components of the hard bottom ecosystem was upset. The principal reason for these changes, unlike the changes observed in many soft bottom communities below the intertidal zone, was not due to an increased 0 2 concentration during EN because 0 2 is not limiting in these kinds of communities under normal conditions. Instead, most changes seem to have been caused by a combination of high temperatures, changes in sea level and increased swell, and from biological interactions that resulted from the impact of these physical perturbations. The changes along rocky shores during the first phase of the event involved the mass mortalities of key species, leading to a

337

general impoverishment of the communities in terms of density, biomass and species numbers (Soto, 1985; Tarazona et al., 1985b; Tomicic, 1985). This disturbance was accompanied by predators immigrating from tropical areas (mainly swimming crabs). At a later stage, when ample space was available due to the mass mortalities of species that had formerly occupied the rock substratum, algae increased dramatically in abundance in the intertidal zone and the algae were able to monopolize the available space because of the absence of grazers. Apparently, grazer populations also needed more time to recover than their food: while the algae, especially Ulva cosrara, developed prominent growths in Laynillas (south of Pisco) from about May 1983, the first juveniles of limpets and other snails became visible only as late as December 1983 (Arntz, 1986). Commercial sea urchin stocks had not even recovered by 1988 (Wosnitza-Mendo et al., 1988). In Anc6n Bay, increases in abundance of U . costafa started in March 1983, when sea level increased, and extensive bleaching of the green alga occurred in October, after sea level had returned to normal. In Anc6n Bay, U . cosfata increased in abundance starting in March 1983 when sea level was anomalously high. The green alga also experienced extensive bleaching in October, after sea level had returned to normal. Recolonization by Sernirnyrilus on rocks left bare by the impact of EN in this area (Fig. 7) started only in October 1984 (Tarazona et al., 1988b). In the deeper intertidal and shallow subtidal zones, kelp suffered almost complete mortality during the first months of 1983, and most of the species associated with the rhizoids and foliage of the laminarians were also killed. The post-EN period was characterized by a multitude of biological interactions among the various components of the intertidal hard bottom community (Tarazona et al., 1988d), finally resulting in the reestablishment of the usual set of species, the gradual disappearance of the invaders and the reduction of algal cover and biomass to normal levels. This process took about two years in the intertidal zone. In the subtidal zone, however, recovery occurred much later since the kelps started to recolonize their former habitat only after about three years, and they may still need another couple of years to grow to their former size. At an intertidal location at Ancbn, the normally dominant mytilids were reduced to about 5 % of their former density during the first phase of the 1982-83 EN event. Polychaetes and brachiopods, which normally live in the deeper sublittoral areas, became predominant together with green algae (Ulva costata , which replaced U . lacruca) and tropical species such as the stalked barnacle Pollicipes elegans, which recruited by larval settlement (see section 4.2). Towards the end of EN, several benthic invertebrate species and algae coexisted without any one species monopolizing the available space, and evenness reached an unusually high value for this community (Tarazona et al., 1985b). Apparently, the monopolization of the substrate by a few species, which is typical for these kinds of communities, can be replaced by species assemblages with more even space distributions during EN conditions. However, at other sites where even higher temperatures prevailed, all zoobenthos suffered high mortalities, with the result that algae monopolized the substrate. Alternatively, in some exposed areas populations of stalked barnacles that had settled during the event became community dominants only after EN 1982-83 (Arntz, 1986; Kameya and Zeballos, 1988). Another study site in the Anc6n area, at 5 m depth, was dominated by populations of the

338

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\z L

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d

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. d

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rnm

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2

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Ju 1l-83

Jan'-84

'

AUCJ-84

Fig. 7. Density changes of planktonic bivalve larvae (above) and the mussel, Semimytilus nlgosus (below), in the rocky intertidal of Ancdn Bay during and after EN 1982-83. On the left side, the lower graph presents data from a field experiment (Tarazona et al., 1985b) where colonization was monitored on rock surfaces cleaned of their mussel cover. On the right side, natural recolonization is indicated on rock surfaces freed by EN 1982-83 (Tarazona et al., 198Xd).

mytilid Aulacomya ater and the laminarian Macrocystis pyrifera before EN. Both species died during the event. Experimental substrates were almost totally colonized by the polychaetes Hydroides norvegica and Pomatoceros sp., which occupied nearly all of the space released by the former two species. The reason for the success of the polychaete worms may have been that they were more tolerant of high water temperatures and could not be eaten by the immigrant tropical predators, principally swimming crabs and shrimps. Interestingly, the two tubicolous polychaetes, which normally live on offshore islands, appeared in large numbers in layers 5 cm thick on the hulls of fishing vessels as early as December 1982 whereas they colonized nearshore rocks several months later (Tarazona et al., 1985b). Possibly these vessels acted as dispersion agents for the two polychaete species, which have a short planktonic stage (Thorson, 1946; Wisely, 1958). Generally, the impact of EN on the rocky shores of the northern Humboldt Current area seems to have been predominantly negative, leading to profound changes in the biotic

339 composition and structure of the communities. However, in northern Chile the impact of EN 1982-83 on the rock fauna seems to have been less negative, in some cases even beneficial to certain populations. An example is the mytilid, Semimytilus algosus, which developed favorably in the Iquique-Antofagastd area where the changes brought about by this EN were not so drastic as in central Peni (Soto, 1985; Tomicic, 1985). The implications for commercial invertebrate species are dealt with in section 4.2. 4.1.2 Soft bottoms Soft bottom habitats in the Humboldt Current area include intertidal sandy beaches, shallow subtidal zones, where the sand contains an increasing amount of silt, and the mud bottoms of the oxygen minimum zone, which are hypoxic or even anoxic under normal conditions. EN effects were different in these areas, and the three zones will be dealt with individually for this reason. For more oxygenated habitats below the 0 2 minimum zone, extending from about 700 m to the deep sea (Rosenberg et al., 1983), we have no data. Sandy beach communities in the intertidal zone of Peni and in northern Chile are composed of only a limited number of macrobenthic species (about 30), but they often have high population densities and high biomasses due to the relatively large size of their dominant species, e.g. the surf clams Mesodesma donacium and Donarperuvianus, and the mole crab

Emerita analoga. Four years prior to EN, in Asia, Peni (south of Lima) the average density of the macrobenthos was 3,720 individuals m-2 and the mean biomass was 15.1 kg m-2 wet weight (Tarazona et al., 1986). Both the density and biomass of M . donacium can be even higher at times (see section 4.2). During EN 1982-83, the three numerically dominant species of sandy beaches suffered high mortalities (Arntz et al., 1987). While D. peruvianus and E . analoga survived at low densities, M . donacium, which had exhibited changes in reproductive behaviour in the months before EN, did not survive the high temperatures in February 1983 and became absent in central Peni (Fig. 8). When conditions normalized, small polychaetes of the genera Dispio and Scolelepis became pre-eminent. D . peruvianus and E. analoga increased in density but never reached the dominant role of M . donacium before the event. At this writing (1989), the intertidal sand beach community has not fully recovered and is far below the high biomass values observed before EN 1982-83. Seafloor communities at moderate depths along the South American coast, which are often affected by hypoxic conditions (Gallardo, 1963; Ramorino and Muiiiz, 1970; Gallardo et al., 1972; Rosenberg et al., 1983; Tarazona, 1984; Tarazona et al., 1985a, 1988c), responded to EN in quite a different way. Our observations are based principally on data from two stations at 15 and 34 m depths in Anc6n Bay (Tarazona et al., 1988b). Two months before the front of the Kelvin waves arrived in the first week of October 1982, dissolved oxygen levels increased close to the bottom and maintained higher than normal values until May 1984, nearly one year after the return to normal temperatures (cf. Fig. 2). Several community attributes more or less followed these changes. Between June and July 1982 the number of species increased; between May and September 1984 the number of species decreased and finally returned to the

340

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a

I I

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u)

I

U

I I

-

Mean and standard error

EL NIRO 1982-83

I

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No M. donaclum found

Mean only (no replicate available)

Fig. 8. Density changes and mortality during EN 1982-83 of the surf clam, Mesodesma donacium, in the intertidal zone of the Santa Maria del Mar sandy beach, 1981 - 1983. Vertical lines denote standard error of the mean. Modified after Arntz et al. (1987). low level found before EN. Density and biomass of the community started to increase in October 1982, these attributes decreased to some extent during the periods of maximal thermal anomalies in January and May 1983, and they returned to normal low values between May and August 1984. At 15 m, the species number doubled during the event, the biomass rose from < 1 g dry weight to > 18 g m-2, and total individual density increased from < 4,000 to > 40,000 m-2. At the 34 m station, species number increased by a factor of 5 (Fig. 9), biomass--normally at 0 g or negligibly above--rose to 7 g dry weight, and densities climbed from about 400 to > 13,000 m-2 (Fig. 10). At both stations, species diversity (H) was about 2 - 3 times higher during than before the event. Trophically, there was a change from a dominance of deposit to suspension feeders at the shallower station, and a species replacement among the deposit feeders at the deeper station (Tarazona et al., 1988b). The favorable development of the benthic communities in Anc6n Bay seems to have been caused mainly by the increased 0 2 concentration at the seafloor during and after the event, possibly in connection with higher temperatures (Tarazona, 1984). Under these conditions, colonization on the otherwise oxygen deficient bottom is improved both for autochthonous species and immigrants from tropical or oceanic waters, and growth and production of all faunal components are accelerated. The flexibility of this subsystem, i.e. its capacity for immediate response to a change of environmental conditions, is surprising. Information on the deeper parts of the oxygen minimum zone on the shelf and the upper continental slope is more fragmentary, but the marked increase in dissolved oxygen referred to in section 2 apparently had beneficial effects on macrobenthos whereas it negatively affected the

341

24 N

E

20

N d

0

\

16

m

a, .rl

U

a,

n cn

12

Y-

O

8

L

a,

n

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Z

4 0 Aug-81

Feb-82

Sep-82

Mar-83

Oct-83

Apr-84

Nov-84

Fig. 9. Changes in total number of macrobenthic species and appearance of "new" species (n) before, during and after EN 1982-83 at a 34 m deep station in Anc6n Bay .

1981

1982

1983

1984

Fig. 10. Density changes of macrobenthos at 15 and 34 m deep stations in Anc6n Bay before, during and after EN 1982-83. Vertical lines denote standard errors of means. From Tarazona et al., 1988b.

342 normally dominant spaghetti bacteria (Prokaryota, genus Thioploca) (Amtz et al., 1985; Salzwedel et al., 1988). There were, however, geographical differences: in northern Perh, where 0 2 values at the seafloor are high during normal periods, hardly any changes were observed, but between 10°30 and 12"spolychaetes and nemerteans increased in biomass and population density. We do not know why such positive effects were not evident among some mollusc species, but predation by tropical immigrants may have concealed it. Immediately after EN, increased densities of molluscs were observed in some areas (Amtz et al., in prep.). Species number and diversity of macrobenthos increased all along the coast, even north of 1Oo30'S. The favorable development of the macro-benthos, together with the improved 0 2 conditions, also affected the behavior of demersal fish (see section 4.3). In normal years, swimming crabs do not occur in the Humboldt Current area south of Paita (5"s) but are restricted to the extreme north of Peni, Ecuador and Colombia. In December 1982, large numbers of juveniles of the species Euphylax robustuy and Portunus acuminatus were taken by RV "Humboldt" off Huacho (1 1"s). Within a short time, these two species and three others (Portunus asper, Callinectes arcuatus and Arenaeus mexicanus) appeared all along the Peruvian coast, with C. arcuatus even present in northern Chile. A sixth species (E. dovii), which had been common during EN 1972-73, appeared on the Peruvian coast in 1984 (Arntz and E. Valdivia, 1985; Amtz, 1986). Many swimming crabs spawned during EN in their new habitat and thus enlarged their populations. Bycatches of several hundred kg per night were taken in the shrimp trawl fishery off Chimbote towards the end of EN, and in the shallow waters of Paracas Bay densities of 100 individuals m-2were recorded (Amtz, 1986). When the water temperatures returned to normal, most populations in Peruvian waters were killed but some survived through 1984. In Anc6n Bay A. mexicanus, the only species for which we have a time series, managed to reproduce once more under post-EN conditions (Fig. l l ) , but recruitment was not successful, and the population suffered total mortality soon afterwards. Swimming crabs, besides being a nuisance to the fishermen, are voracious predators and may have been largely responsible for the devastation of benthic fauna during EN both in shallow and deep waters. In Ancdn Bay the food of A. mexicanus during EN consisted mainly of mole crabs (E. analoga), which were taken by all predators both large and small. Some mussels, e.g. S. ulgosu.7, were eaten also, revealing that the swimming crabs took their food both from soft and hard bottoms. After EN, juvenile swimming crabs nearly exclusively fed on small S. algosus, which had become available again in large quantities. 4.2

Exdoited invertebrates ("mariscos") The profound changes in the benthic subsystem described in section 4.1 also affected the commercially exploited invertebrate species. Negative or positive EN effects often become more clearly visible in shellfish populations, even from catch statistics that for some of these species are the only available information (Figs. 12, 13). Certain factors, however, (e.g. changes in the preference for certain shellfish by fishermen and the associated shifts in the distribution of the artisanal fishing fleets, or closed seasons) sometimes conceal population changes. Since catches per unit of effort are seldom available, the only possible approach is to

343

1.5 1.2 0.9 0.6 0.3

0.0 400

300

Arenaeus mexicanus

200

100 0 Apr-81

Nov-81

May-82

Dec-82

Jul-83

Jan-84

Aug-84

Fig. 11. Changes in numbers of brachyuran zoeas (above) and the swimming crab, Arenaeiis mexicanus (below), a tropical invader, in Anc6n Bay, 1981 - 1984. The upper graph pools 10 standard net hauls, 0 - 15 m, mesh size 200 pm; the lower curve presents values from standard beach seine catches taken alongshore in the shallow subtidal zone (see Hoyos et al., 1985). use a combination of observations along the shore with landing statistics. EN effects on "mariscos" off Peni have been discussed extensively by Arntz and E. Valdivia (1985) and Arntz et al. (1987, 1988). The sorts of effects observed during EN 1982-83 and former events during this century (cf. Chirinos de Vildoso, 1976, 1984 and Del Solar, 1983) included (a) mass mortalities, (b) immigration from (sub)tropical areas further north combined with area extensions and southward shifts of certain populations, (c) emigration from shallow areas towards greater depths, (d) increases in abundance of local populations more tolerant of high temperatures and capable of using alternate sources of food, and (e) after EN the temporary survival of exotic species that managed to recruit locally during the event. Mass mortality occurred on sandy beaches, in the rocky intertidal zone and in shallow subtidal areas. This disturbance mostly affected mollusc and crustacean populations, but also sea urchins and ascidians (the latter are used as fishing baits in P e h and for direct human consumption in Chile), and it seems to have been connected mainly to the unusual increase in sea temperature. Other factors that may have contributed to these mortalities were changes in sea level, rough seas, the destruction of kelp stocks that provide shelter for many invertebrates

1970

1972

1974

1976

1978

1980

1982

1984

1986

1988

Fig. 12. Annual landings of three shellfish of major importance (scallop, A . purpuratus; mussel, A. ater; and shrimps of the penaeid family) off the Peruvian coast, 1970 - 1987. Shaded areas: EN and other years with positive temperature anomaly > 2°C. Modified after Arntz et al. (1988). (see Dayton and Tegner, this volume), and the decline in other algae that serve as food for grazers. In northern Peni and Ecuador, where torrential rainfall increased river discharge (and thus sedimentation in coastal waters), decreases in salinity and increases in sedimentation rates also occurred. All mussel beds of Aulacomya ater, which before EN 1982-83 was the most important shellfish species in Perli above 15 m depth from Huacho to Pisco (1 1 - 14OS), died and detached from the substrate in March 1983 although this species demonstrated accelerated growth until February. Only in deeper water (> 30 m) did some populations survive (Soenens, 1985). The destruction of mussel beds induced important population shifts among many species that normally live in this habitat. The shallow water clams Semele spp. and Tagelus dombeii, together with other bivalves of minor commercial importance, became virtually extinct in some areas whereas another clam (Cari solida) living at a greater depth survived and contributed to fishermen's catches in the later phase of EN. Similar depth differences in survival were observed in crab populations. In the case of Cancer spp., C . setosus suffered almost complete mortality similar to another commercially important species (Platyxanthus orbignyi) (Fig. 13) whereas C .porteri and C. coronatus withdrew to deeper water and reappeared in catches half a year after EN (Amtz and Arancibia, in press). On Peruvian rocky shores, thick layers of shells of many grazers, including limpets (Fissurella

345

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

40

i:: A

100 80

=

6o 40

e 1

h

25

3 2o

5 15

a 10 5

1981

D

1982

D

1983

D

1984

D

1985

D

Fig. 13. Monthly landings of brachyuran crabs (Cancer setosus and Platyxanthus orbignyi) and clams of the "almeja" type (Semele spp., Gari solida and others) at the port of Pisco, Peni, 1981 - 1985. Modified after Arntz et al. (1988). spp.), other prosobranch gastropods, chitons and sea urchins, were found in March 1983, while the substrate, normally covered with a rich invertebrate fauna, was practically bare. The disappearance of grazers subsequently led to the proliferation and succession of algae, which, unfortunately, were never studied in detail (Amtz, 1986). However, on Chilean rocky shores mortality of invertebrates was much less intense, and some species even benefited from the EN conditions, e.g. Semimytilus algosus (Soto, 1985) and Acanthopleura echinata (Pefia et al., 1987). On sandy beaches, the surf clam Mesodesma donacium, an easily accessible species for local exploitation, which before EN in some areas produced > 35 kg m-2 (3 kg shell-free dry weight) (Amtz et al., 1987), did not survive along 7 degrees of latitude on the central Peruvian coast at its northern most distribution. At the same time, however, it increased in abundance near its southern distribution limit in the area of Valdivia, Chile (40's). M. donacium is one of the few shellfish species for which population data were available before, during and after EN (cf. Fig. 8). Immigration from tropical and subtropical areas near the equator included both active invasion by juveniles and adults, and an inflow of eggs and larvae of invertebrate species that later became established in the upwelling area off Pert5 and northern Chile. In many cases the immigrant species even reproduced. For most species, it is not possible to distinguish between adult, larval or post-colonization cohorts on the basis of the available data. Only among the crustaceans did immigrant species attain commercial significance although among the molluscs there appeared some spectacular large species such as pearl oysters (Pinctada sp., Pteria sterna), pen shells (Arrina maura) or large gastropods such as Maleu ringens. By far the most important invaders by commercial standards were the penaeid shrimps (cf. Fig. 12) and among these, the species Xiphopenaeus riveti, which in normal periods abounds off Colombia and Ecuador. The first specimens of penaeids appeared in the bottom trawl catches of the Peruvian research vessel "Humboldt" off Huacho as early as December 1982. During 1983 X . riveri extended its range by 13 degrees latitude down to the Peruvian south coast and gave rise to a

P

346

new fishery both with beach seines along the shore and with trawls and trammel nets in deeper water. Even after the pronounced temperature decline in July 1983, catches per boat per night south of Chimbote were between 0.5 and 3 t. During 1984 the shrimp boom off Peni gradually ceased, and towards the end of the year the fishery was once again resmcted to the Paita (5's) area and further north. Some of the larger penaeid species maintained small stocks, e.g. south of Pisco (14OS), where they were caught incidentally in purse seines as late as 1985. Off Colombia and Ecuador the abundances of shallow water shrimps, which were mainly responsible for the invasion in Peni, decreased (as did those of the swimming crabs that also invaded Peruvian waters but were not exploited by the fishery), giving the impression that a major part of the tropical shallow water ecosystem had shifted southward. The deep water shrimp catches, however, especially Penaeus brevirostris and P . californiensis, increased (Mora et al., 1984; Martinez, 1989). While the Ecuadorian shrimp trawl fishery apparently fully exploits this resource, with a relatively constant number of fishing vessels in operation since the beginning of the seventies, the very strong recent increase in shrimp production is a result of shrimp farming that also has expanded recently due to an extension of the area under cultivation (McPadden et al., 1988). After EN, spiny lobsters (Panulirusgracilis) and stalked barnacles (Pollicipes elegans) increased in abundance along the Peruvian central coast; however, the larvae of both species already had been transported into the area during EN. P . elegans occupied spaces in crevices and on rocks that had been vacated during the disappearance of local species during EN. In some areas the stalked barnacles remained alive until 1986 (Kameya and Zeballos, 1988). Emigration from shallow areas, apart from that from the tropical zones just mentioned, occurred on a large scale in upwelling waters. Thermally intolerant species withdrew to greater depths where the temperature increase was not so pronounced. Most of the species in question temporarily disappeared from the landings. Among the brachyurans, two species already mentioned, Cancer porteri and C . coronatus, apparently managed to survive at greater depths during the period of temperature increase (see above). A similar case among the gastropods involved the "false abalone" Concholepas concholepas, a carnivore that was largely deprived of its kelp shelter in shallow water but survived in part at greater depths (Amtz and E. Valdivia, 1985). Similar effects off northern Chile can be seen from the Cruz Grande data presented by Geaghan and Castilla (1987). Increases in the abundance of local populations more tolerant of high temperatures, mostly by species derived from tropical waters, induced the second positive development during and after EN 1982-83, which in economic terms was even more important than the shrimp invasion from the north. The principal species concerned were the Peruvian scallop Argopecten purpuratus (Fig. 12; Wolff, 1984, 1985; lllanes et al., 1985), and to a lesser degree the purple snail Thais chocolata and the octopus Octopusfontaneanus, species that are present at relatively low densities off central and southern Peni and northern Chile and that only modestly contribute to the landings in normal years. Under EN conditions these species are favored possibly not only by the increase in temperature but also because of their ability to exploit alternative food sources. Reduced competition with coexisting species that suffered high

347 mortality during EN may also have been an important factor. Favorable conditions for scallop larvae seem to be more important than favorable conditions during gonadal development and spawning of the adults, as can be seen from the weak correlation between parent stock size and recruitment success (Illanes et al., 1985; Wolff, 1987). The scallop population boom in Paracas Bay, south of Pisco, started with a heavy recruitment event in 1983 and with an extension of the area populated by this species into shallow water. The scallops grew to market size in only 6 months, and with > 100 individuals per square meter (5 - 8 kg m-2) the stock size was about 60 times greater than in normal years. An important processing industry developed at Pisco, and large shell middens covered many square kilometers in the surrounding desert. In 1984 there was a short period of diminished yield due to overfishing of the Paracas Bay stock, but in 1985 another boom occurred in Independencia Bay, south of the Paracas peninsula, which attracted even more fishermen to the area. Despite certain protective measures and closed seasons, the scallop fishery suddenly declined by the end of 1986 (cf. Fig. 12) mainly due to overfishing of the stock and the dumping of shells and waste onto the fishing grounds (Mendo et al., 1988). It is not clear at this time whether a more cautious exploitation would have resulted in a temporal extension of this fishery; in fact, a sustained yield of this species over a long period may be an illusion (Wolff, 1987). Interestingly, however, large ancient shell middens in the Peruvian coastal desert reflect former high abundances of this species that may well have been associated with similarly strong EN events in the past (Amtz et al., 1987). The post-EN development of shellfish was characterized by (a) withdrawal of the allochthonous species, especially the shrimps, although some penaeids managed to survive in the upwelling area for up to two years, (b) mortality of many invaders (especially most of the swimming crabs), (c) persistence of a few economically important invader stocks such as stalked barnacles and rock lobsters, and (d) recovery or reappearance of most autochthonous species within a period of about two years. Mainly as a result of the invasion of shrimp and the increase in abundance of scallops, the overall effect on the shellfish fisheries was rather beneficial. Total landings strongly increased, but their composition changed drastically. Moreover, the changes brought about by EN favored only a small part of the artisanal fishermen, those who owned boats and diving equipment for scallop exploitation, or those who were able to adapt their gear to shrimp fishing. However, the small-scale, shore-based subsistence fishery largely failed during the event and in the years following it.

4.3 Demersal and coastal fish Under normal conditions, the fishery for demersal fish in the Peruvian/Chilean upwelling area is restricted to the well oxygenated waters nearshore, and most of the catch is taken by small-scale artisanal fishermen using trammel and drift nets as well as hook and line. A demersal trawl fishery for finfish is carried out only in a limited area off northern Peni, between Paita (5"s) and Chimbote (9OS), whereas further south the seafloor is practically devoid of demersal fish below 30 m due to the extremely low oxygen values and the

348

narrowness of the shelf, which only north of Chimbote reaches a width of > 100 km. In this fishery, Peruvian hake (Merluccius gayi peruanus) provides about 70 % of the landings (Fig. 14). Part of these catches, however, are taken by purse seiners since this species often moves to shallow depths in the pelagic zone. Other species of commercial importance include a number of sciaenids (especially ayanque, Cynoscion analis, coco, Paralonchurus peruanus, cabinza, Isacia conceptionis, corvina, Sciaena gilberri, and lorna, S. deliciosa), sea bass (cabrilla, Paralabra humeralis), flatfish (Paralichthys adpersus and others), dogfish (tollo, Mustelus spp.), rays (Myliobatis spp.) and mullets (liza, Mugil cephalus and others). Coastal pelagic fish include cojinoba (Seriolella violacea),machete (Opisthonemalibertate) and silverside or pejerrey (Odontesthes regia regia). The increase of temperatures and dissolved oxygen at the seafloor during EN, and the resulting positive development of small benthic species that serve as food for demersal fish, affected the finfish populations just as much as the shelfish although in a somewhat different way.

320 280 240 200 160 120 80 40 0 28 24 20 16 12 8 4 0 1 Fig. 14. Annual landings of hake (M.gayi peruanus), dogfish (Mustelus spp.) and silverside (0.regia regia) off Peni, 1951 - 1987. Shaded areas: EN and other years with positive temperature anomaly > 2OC.

349 Soviet scientists working aboard the research vessel "Prof. Mesyatsev" were the first to detect higher 0 2 values at the bottom and latitudinal shifts in demersal fish populations during EN (Romanova, 1972). In 1972, hake and associated species were detected on the deeper shelf off Pisco (14"S), 5 degrees latitude south of their normal area. In 1982-83, the entire Peruvian and Ecuadorian demersal fish community in the Humboldt Current area apparently shifted to the south and, at the same time, extended its distribution beyond the edge of the continental shelf to the upper slope, thus covering a much wider area than during normal years. A large number of independent observations elucidated this general pattern. Demersal standard hauls obtained off Ecuador for research purposes yielded 30 - 50 % lower catches in April May 1983 than in normal years (Martinez, 1989). Gurnards (Prionotus stephanophrys), which at the onset of EN virtually disappeared from Ecuadorian waters, revealed a reduction in their share of the demersal fish catches from 21 - 36 % to 3 % (Herdson, 1984), and became abundant off Pisco where they are not normally caught. Hake were not recorded from their normal distribution area south of Paita between December 1982 and February 1984 (Castillo, 1985), but were concentrated on the upper slope where they encountered favourable 0 2 and food conditions, as well as temperatures similar to those in their usual habitat during non-EN years (Espino et al., 1985). South of Chimbote R.V. "Humboldt" obtained large catches of dogfish, rays, loma and sea bass in December and January 1982-83, in areas where demersal fish are not normally caught. Loma, which are usually restricted to within 20 km of the shore, were found up to 150 km offshore (Arntz, 1986). In April 1983, most of the local finfish species were absent from the Gulf of Guayaquil whereas tropical species (Fam. Lutjanidae and others) had immigrated into the gulf from more northerly areas (Herdson, 1984). During the much weaker EN 1986-87 most demersal fish again migrated towards the south (to about 10's) and to the margin of the continental shelf, but on a reduced scale. Fish were more dispersed on the seafloor, shoals of pelagic coastal fish could no longer be detected, and the size and age structure of the catches taken by R.V. "Humboldt" in January 1987 was also different from normal years (ComitC Cientifico CPPS, 1987). Thus it appears that demersal fish can benefit from the improved 0 2 and food conditions on the seafloor during EN, avoiding at the same time the high water temperatures found in the northern sector of the Humboldt Current upwelling area and in nearshore shallow waters. According to Espino and Wosnitza-Mendo (1986) hake cannibalism, which is an important source of natural mortality in that species, decreases substantially when hake extend their distribution area, as occurs during EN conditions. If at the same time predation by pelagic shoaling fish on hake larvae becomes less intense, as assumed by Wosnitza-Mendo and Espino (1986a), improved recruitment of Peruvian hake must be expected during strong EN events. During EN 1982-83 the demersal fish also changed their feeding habits. Hake, with a diet normally consisting almost exclusively of fish and euphausiids from the water column, consumed predominantly benthic crustaceans in 1983. Some hake and gurnard stomachs even contained bathypelagic fish that had formerly been recorded only off Central America. Lorna and sharks fed heavily on anchovies that had taken refuge at greater depths. Generally the food of demersal and coastal fish, in contrast to pelagic species, was found to be more diverse

350 during EN conditions (Hoyos et al., 1985; Sinchez de Benites et al., 1985; Tarazona et al., 1988a). Improved feeding conditions during EN 1982-83 may have been the reason for premature spawning in many demersal fish such as seabass (SamamC et al., 1985). Even among species spawning normally, spawning success and recruitment should have been improved because of favorable conditions on the seafloor and a closed fishing season that was enforced due to the dispersal of fish concentrations. During EN years the demersal fish catches off Peni are lower than in normal years (Fig. 14) because of the dispersal of fish and their movement into deeper waters, which decreases their availability and increases the difficulty of detection by means of echoacoustics. In Peni, demersal fish catches decreased from 94,000 t in 1981 (of which 69,000 t were hake) to 51,000 t (hake = 26,000 t) in 1982 and 26,000 t (hake = 6,000 t) in 1983. In 1984 landings rose to 64,000 t but hake landings (12,000 t) remained much below the pre-EN mean. Off Chile, the catches nearly doubled to 71,000 t in 1982 and persisted at a high level in 1983 with 56,000 t, probably due to the southward migration of part of the demersal stocks (IMARPE, unpub.).

5 CONCLUSIONS EN owes its negative reputation as a merely catastrophic event mainly to the dramatic collapse of the anchovy fishery that began in the early 1970s (which, however, was a consequence of continuous overfishing, although in some way it was also related to reproductive failures caused by EN; Jordin, 1983) as well as to certain impacts on organisms that catch the observers’ eye, such as the mortality of guano birds and seals. Before EN 198283, the literature concentrated on these negative aspects (e.g. Jordin, 1964; Boerema et al., 1965; Valdivia, 1978), and only during this exceptionally strong event did it become obvious that there were positive effects as well (Amtz, 1984), and that these beneficial effects occurred predominantly in benthic and nearshore subsystems that had been previously neglected (Amtz and J. Valdivia, 1985). We now know that it is necessary to consider the different subsystems separately. Even within the Humboldt Current upwelling area off South America there were strong gradients in effects from the equator to the south, from oceanic regions towards the shore in pelagic biotas, and from shallow to deep water in benthic environments (Amtz and Tarazona, 1988). The major ecological factors acting in these subsystems were different, ranging from an overall impact of increased temperatures to more local conditions such as increased sedimentation close to some river mouths. In many cases, although the effects of EN were clearly visible, we are not yet able to refer specific causes to them. Much work is still necessary to elucidate the mechanisms that ultimately cause the observed primary effects and the secondary biotic interactions that resulted from them. In the pelagic system, most effects of EN 1982-83 were indeed catastrophic although they were hardly visible in the Peruvian finfish landing figures because continued overfishing before the event has maintained low biomasses of the two principal species (anchovy and sardine).

35 1 Off Chile, however, the effects on the fishery were rather positive due to increased recruitment of sardines prior to the 1982-83 EN event and to the southward migration and near-surface concentration of sardines during the event, which resulted in increased vulnerability and much greater temporary landings of this species. Overall, the general biological impact on anchovies and sardines was negative; the changes in food composition and the almost complete breakdown of their underlying food base led to reproductive failure, lack of recruitment and considerable weight losses in these two shoaling species as well as to reduced stocks after EN. The different fate of the Peruvian and Chilean sardine fishery during the strong 1982-83 EN and later (i.e. during the moderate 1987 event), elucidated particularly well the variable impact of the disturbance on the behavior of pelagic shoaling fish along a latitudinal gradient. The mackerels, which are usually more oceanic, withstood the changes brought about by EN much better, but their presence in nearshore waters did not contribute a great deal to the fisheries. Many immigrant finfish species from oceanic and tropical waters entered the upwelling system, but were only of local importance for a short period in 1983. The total extent of this immigration must have been considerable taking into account the more than 50 fish species recorded off Perli and Chile that are not normal inhabitants of this area (Kong et al., 1985; VClez and Zeballos, 1985). The majority of demersal and nearshore fish such as hake, sciaenids and flatfish withdrew from shallow waters and moved to the edge of the continental shelf, and also undertook southward migrations at the same time, as did many immigrants from (sub)tropical waters (gurnards, snappers, dogfish, and rays, among others). The causes of these movements have to be sought in the increase of dissolved oxygen at the seafloor, the resulting improvement of benthic food resources at the bottom, and most likely in the temperature changes as well: while hake and accompanying species remained in waters of cooler temperatures at greater depth (Wosnitza-Mendo and Espino, 1986b), the tropical immigrants followed the warm waters further south. The effects on the fisheries were unfavorable during and immediately after EN, but the fish themselves could recover, and recruitment was enhanced, which may result in increased catches a few years after the event like those observed in 1978 as a consequence of the 1972-73 EN (Wosnitza-Mendo and Espino, 1986a). The effects on macrobenthos in general and on shellfish in particular were quite varied. Where normally hypoxic conditions prevail, the benthos benefitted from improved 0 2 conditions and developed unusually rich populations during EN and one year after the event. Then, with the final decrease in oxygen concentration, the communities returned to the impoverished state they had shown before EN. On sandy beaches and in the rocky intertidal zone, most invertebrate species (including shellfish) suffered mass mortalities caused presumably by a variety of impacts, with high temperatures, sea level changes, strong swell and increased predation as the most likely sources of disturbance. However, some local species such as scallops, purple snails and octopus, proliferated to unprecedented population levels. At the same time, some tropical immigrants, most of them crustaceans, became enormously abundant. Landings from either group -- especially those of scallops and shrimps - increased the shellfish catches much above the pre-EN level, both in amounts taken and in

352 value. The post-EN effects on the artisand fishery were also favorable at first since the scallop boom continued until 1986. At the present time, most shellfish that suffered during the event seem to have recovered to their pre-EN levels. This review is restricted to the impact of EN on benthos, fish and fisheries. There are many other effects of EN on the communities and species populations of the upwelling system (Amtz, 1986), and some of them are consequences of the effects described in this paper. For example, the disruption of the pelagic food web caused mass mortalities and reproductive failures of guano buds (see Smith, this volume, and Duffy, this volume) and seals (see Limberger, this volume); mortality of grazers in shallow water led to increases in algal biomass, changes in species composition and successional processes that remain to be studied in more detail. On the whole, however, recovery of most species occurred rather quickly, resembling recovery events in temperate areas where most species return to pre-disturbance abundances within 2 - 3 years (Arntz and Rumohr, 1982, 1986; Amtz and Arancibia, in press), and relatively few long-term effects have remained, thus demonstrating the remarkable resiliency of the upwelling ecosystem. One of the long-term effects is the continuing absence of the surf clam M.donucium from central Peruvian waters. Fluctuations of this species have been observed in former years as well, however, and are evident in shell middens along the Peruvian coast. Variations in abundance of surf clams and scallops (A. purpurutus) in shell middens may reflect former cold, anti-EN and warm, EN periods (Arntz et al., 1988). Finally, we would like to stress that EN 1982-83 was an exceptionally strong event (Quinn et al., 1987). During a minor EN event, such as 1976, only some effects were apparent, and the impact was probably resnicted to a limited section of the South American west coast off Ecuador and northem Perii. Only a long-term monitoring program including all major research institutions between Colombia and Chile will enable us to answer the many questions that have remained even after EN 1982-83, and in particular, to clarify the causal mechanisms underlying the ecosystem, community, and population responses described in this paper and, in a wider context, by Amtz (1986) and Glynn (1988). 6 ACKNOWLEDGMENTS Our thanks are offered to the members of the DePSEA group at San Marcos University, Lima, for their cooperation in the field work. Claudia Willeweit has been very helpful with the preparation of the manuscript. Alodia Holierhcek kindly removed some of the worst errors in the English language. Peter Clynn and two anonymous reviewers undertook considerable efforts to improve this paper both from a scientific and language point of view, and called attention to major inconsistencies in the first draft of the text. This work has been completed under an Alexander von Humboldt Foundation fellowship to Juan Tarazona in Germany, which is gratefully acknowledged. Contribution No. 260 from the Alfred-Wegener-Institut fur Polar- und Meeresforschung.

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Paine, R.T., 1986. Benthic community - water column coupling during the 1982-1983 El Niiio. Are community changes at high latitudes atmbutable to cause or coincidence? Limnol. Oceanogr., 31: 35 1-360. Paredes, C. and Tarazona, J., 1980. Las comunidades de mitilidos del mediolitoral rOcoso del Departamento de Lima. Rev. Per. Biol., 2: 59-71. Pastor, A., 1984. El Niiio 1982-83 y su incidencia en algunos aspectos biol6gicos y pesqueros en la costa sur del litoral peruano. Bol. ERFEN, 10: 14-22. Pauly, D., Chirinos de Vildoso, A., Mejia, J., SamamC, M. and Palomares, M.L., 1987. Population dynamics and estimated anchoveta consumption of bonito (Sarda chiliensis) off Per& 1953 to 1982. In: Pauly, D. and Tsukayama, I. (Editors), The Peruvian anchoveta and its upwelling ecosystem: Three decades of change. ICLARM Stud. Rev., 15: 248-267. Pearcy, W.G. and Schoener, A., 1987. Changes in the marine biota coincident with the 19821983 El Niiio in the northeastern subarctic Pacific Ocean. J. Geophys. Res., 92: 14,41714,428. Peiia, R., Zdiiiga, 0. and Rodriguez, L., 1987. Variaci6n estacional del indice gonadosomitico en Acanthpleuru echinaru (Barnes, 1823) (Mollusca: Polyplacophora). Estud. Oceanol., 6: 59-65. Quinn, W.H., Neal, V.T. and Antunez de Mayolo, S., 1987. El Niiio Occurrences over the past four and a half centuries. J. Geophys. Res., 92: 14,449-14,461. Ramorino, L. and Muiiiz, L., 1970. Estudio cuantitativo general sobre la fauna de fondo de la Bahia de Mejillones. Rev. Biol. Mar, Valparaiso, 14: 79-93. Rasmusson, E.M. and Wallace, J.M., 1983. Meteorological aspects of the El Niiio/Southern Oscillation. Science, 222: 1,195-1,202. Retamales, R. and Gonzilez, L., 1985. Incidencia del fen6meno El Niiio 1982-83 en el desove de sardina espaiiola (Sardinops sagau). In: Inst. Fomento Pesquero-Chile (Editor), Taller nacional fen6meno El Nifio 1982-83, Invest. Pesq. (Chile), 32: 161-165. Robinson, G.and del Pino, E.M. (Editors), 1985. El Nifio en las Islas Galipagos, el evento de 1982-1983.Fundacidn Charles Darwin para las Islas Galipagos, Quito, Ecuador, 534 PP. Rojas de Mendiola, B., G6mez, 0. and Ochoa, N., 1985. Efectos del fendmeno "El Niiio" sobre el fitoplancton. In: Arntz, W.E., Landa, A. and Tarazona, J. (Editors), El fendmeno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Peni-Callao (special issue): 3340. Rollins, H.B., Sandweiss, D.H., and Rollins, J.C., 1986. Documentation of large-magnitude El Niiio events using molluscs from coastal archaeological sites (Abstract). In: Chapman conference on El Niiio. Guayaquil, Ecuador, 29. Romanova, N.N., 1972. Investigaciones cientifico-pesqueras en las aguas del OcCano Pacific0 adyacentes a la costa del Peni durante el invierno de 1972.Distribucidn de bentos en la plataforma y en el talud continental de la costa peruana. Ser. Inf. Esp. Inst. Mar Per& Callao, 128: 127-132. Romero, L., Paredes, C. and Chivez, R., 1988. Estructura de la macrofauna asociada a 10s rizoides de Lessonia sp. (LaminarialesPhaeophyta). In: Salzwedel, H. and Landa, A. (Editors), Recursos y dinimica del ecosistema de afloramiento peruano. Bol. Inst. Mar Peni-Callao (special issue): 133-139. Romo, D., 1985. Composici6n quimica de la harina de pescado chilena durante el fen6meno El Niiio 1982-83. In: Inst. Fomento Pesquero-Chile (Editor), Taller nacional fendmeno El Niiio 1982-83, Invest. Pesq. (Chile), 32: 141-151. Rosenberg, R., Arntz, W.E., Chumin de Flores, E., Flores, L.A., Carbajal, G., Finger, I. and Tarazona, J., 1983. Benthos biomass and oxygen deficiency in the upwelling system off Peni. J. Mar. Res., 41: 263-279. Salzwedel, H., Flores, L.A., Ch. de Flores, E., Zafra, A. and Carbajal, G.,1988. Macrozoobentos del sublitoral peruano antes, durante y despuCs de El Niiio 1982-83. In: Salzwedel,H. and Landa, A. (Editors), Recursos y dinimica del ecosistema afloramiento peruano. Bol. Inst. Mar Perii-Callao (special issue): 17-98. Samamt, M., Castillo, J., Flores, L.A. and Vilchez, R., 1978. Estructura, distribuci6n y abundancia de peces demersales. Inf. Inst. Mar Peni-Callao, 47: 1-28. SamamC, M., Castillo, J. and Mendieta, A., 1985. Situaci6n de las pesquerias demersales y 10s cambios durante la presencia del fen6meno "El Niiio". In: Amtz, W.E., Landa, A. and Tarazona, J. (Editors), El fendmeno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Perd-Callao (special issue): 153-158.

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359 Tarazona, J., Amtz, W.E., Canahuire, E., Ayala, Z. and Robles, A., 1985a. Modificaciones producidas durante "El Niiio" en la infauna bentdnica de Leas someras del ecosistema de afloramiento peruano. In: Arntz, W.E., Landa, A. and Tarazona, J. (Editors), El fendmeno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Penl-Callao (specid issue): 5563. Tarazona, J., Paredes, C., Romero, L., Blaskovich, V., GuzmBn, S. and SBnchez, S., 1985b. Caracteristicas de la vida planctdnica y colonizacidn de 10s organismos bentonicos epiliticos durante el fen6meno "El Niiio". In: Amtz, W.E., Landa, A. and Tarazona, J. (Editors), El fendmeno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Peni-Callao (special issue): 41-49. Tegner, M.J. and Dayton, P.K., 1987. El Niiio effects on Southern California kelp forest communities. Adv. Ecol. Res., 17: 243-279. Thompson, L.G., Moseley-Thompson, E. and Morales-Arnao, B., 1984. El Niiio-Southern Oscillation events recorded in the stratigraphy of the tropical Quelccaya Ice Cap, Peni. Science, 226: 50-53. Thorson, G., 1946. Reproduction and larvel development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the Sound (0resund). Medd. Komm. Danm. Fisk.-og Havunders., Ser. Plankton, 4: 523 pp. Tokeshi, M., Estrella, C. and Tarazona, J., 1988. Estudio preliminar de las relaciones predator-presa en Heliasrer helianthus (Asteroidea: Echinodermata). In: Salzwedel, H. and Landa, A. (Editors), Recursos y dinimica del ecosistema afloramiento peruano. Bol. Inst. Mar Pen-Callao (special issue): 141-145. Tokeshi, M., Estrella, C. and Paredes, C., 1989a. Feeding ecology of a size-structured predator population, the South American sun-star Heliasrer helianrhur. Mar. Biol., 100: 493-505. Tokeshi, M., Romero, L. and Tarazona, J., 1989b. Spatial coexistence of mussel-associated free-ranging polychaetes in a subtropical intertidal habitat. J. Anim. Ecol., 58: 681-692. Tomicic, J.J., 1985. Efectos del fendmeno El Niiio 1982-83 en las comunidades litorales de la Peninsula de Mejillones. In: Inst. Fomento Pesquero-Chile (Editor), Taller nacional fendmeno El Niiio 1982-83, Invest. Pesq. (Chile), 32: 209-213. Torres, A., Martinez, C. and Oliva, J., 1985. Migraciones de la sardina espaiiola en el Pacifico Suroriental durante el fendmeno El Niiio 1982-83 y en 1984. In: Inst. Fomento Pesquero-Chile (Editor), Taller nacional fen6meno El Niiio 1982-83, Invest. Pesq. (Chile), 32: 95-100. Tsukayama, I. and Santander, H., 1986. Cambios bidticos y efectos sobre 10s recursos pesqueros y las pesquerias en el Peni. Rev. Com. Perm. Pacifico Sur, 16: 97-166. Valdivia, J., 1978. The anchoveta and "El Niiio". Rapp. P.-v. RCun. CIEM, 173: 196-202. VClez, J.J. and Zeballos, J., 1985. Ampliaci6n de la dismbuci6n de algunos peces e invertebrados durante el fendmeno "El Niiio" 1982-83. In: Amtz, W.E., Landa, A. and Tarazona, J. (Editors), El fenbmeno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Peru-Callao (special issue): 173-180. Vilchez, R., Muck, P. and Gonzales, A., 1988. Variaciones en la biomasa y en la distribucidn de 10s principales recursos peligicos del Peru e n m 1983 y 1987. In: Salzwedel, H. and Landa, A. (Editors), Recursos y dinimica del ecosistema de afloramiento peruano. Bol. Inst. Mar Peru-Callao (special issue): 255-264. Vogt, W., 1940. Una depresidn ecoldgica en la costa peruana. Bol. Cia Adm. Guano, 16(10): 307-329. Vogt, W., 1957. Informe sobre las aves guaneras. Bol. Cia Adm. Guano, 33(3): 1-132. Wisely, B., 1958. The development and settling of a serpulid worm, Hydroides norvegica, Gunnerus (Polychaeta). Aust. J. Mar. Freshw. Res., 9: 351-361. Wolff, M., 1984. Impact of the 1982-83 El Niiio on the Peruvian scallop Argopecren purpuratus. Trop. Ocean-Atmos. News]., 28: 8-9. Wolff, M., 1985. Abundancia masiva y crecimiento de preadultos de la concha de abanico peruana (Argopecrenpurpurarus) en la zona de Pisco bajo condiciones de "El Niiio" 1983. In: Arntz, W.E., Landa, A. and Tarazona, J. (Editors), El fen6meno El Niiio y su impacto en la fauna marina, Bol. Inst. Mar Ped-Callao (special issue): 87-89. Wolff, M., 1987. Population dynamics of the Peruvian scallop Argopecten purpuratus during the El Niiio phenomenon of 1983. Can. J. Fish. Aquat. Sci., 44: 1,684-1,691. Wooster, W.S. and Fluharty, D.L. (Editors), 1985. El Niiio North, Niiio effects in the eastern subarctic Pacific Ocean. Wash. Sea Grant Program, Univ. of Wash., Seattle, 312 PP.

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Wosnitza-Mendo, C. and Espino, M., 1986a. The impact of "El Niiio" on recruitment of the Peruvian hake (Merluccius gayi peruanus). Meeresforsch, 31: 47-5 1. Wosnitza-Mendo, C. and Espino, M., 1986b. La construcci6n de curvas de rendimiento sostenible (Shepherd, 1982) para la merluza peruana. Bol. Inst. Mar Peni-Callao, lO(7): 165-183. Wosnitza-Mendo, C., Espino, M. and VCliz, M., 1988. La pesqueria artesanal en el Peni durante junio de 1986 a junio de 1988. Inf. Inst. Mar Peni-Callao, 93: 144 pp. Wyrtki, K., 1975. El Niiio - the dynamic response of the equatorial Pacific Ocean to atmospheric forcing. J. Phys. Oceanogr., 5: 572-584. Wyrtki, K., 1979. El Niiio. La Recherche, 106: 1,212-1,220. Wyrtki, K., 1982. The Southern oscillation, ocean-atmosphere interaction and El Niiio. Mar. Technol. SOC.J., 16(1): 3-10. Zama, A., Rueda, T. and Cirdenas, E., 1984. Unusual arrival of chub mackerel Scornber juponicus at Puerto Chacabuco, southern Chile (Pisces, Scombridae). Rev. Biol. Mar., Valparaiso, 20: 61-76. Zuzunaga, J., 1985. Cambios del equilibrio poblacional entre la anchoveta (Engruulis ringens) y la sardina (Surdinops sugm) en el sistema de afloramiento frente al Peni. In: Amtz, W.E., Landa, A. and Tarazona, J. (Editors), El fen6meno El Niiio y su impact0 en la fauna marina, Bol. Inst. Mar Peni-Callao (special issue): 107-117.

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EFFECTS OF THE 1982-83 EL NIRO-SOUTHERN OSCILLATION EVENT ON MARINE IGUANA (AMBLYRHYNCHUS CRISTATUS BELL, 1825) POPULATIONS ON GALAPAGOS

W. ANDREW LAURIE Max-Planck-Institut fur Verhaltensphysiologie, 8 131, Seewiesen, West Germany, and Large Animal Research Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom. ABSTRACT Laurie. W. A.. 1989. Effects of the 1982-83 El Niiio-Southern Oscillation event on marine iguana (Amblhhynchus Gristatu Bell, 1825) populations on Galapagos. Y

The effects of the 1982-83 El Niiio-Southern Oscillation event (ENSO) on marine iguanas (Amblvrhvnchus cristatus) were observed during a long term study of marine iguana population dynamics on Santa Fe, Galapagos, begun in 1981. The 1982-83 ENSO was the most severe ever recorded: there were record sea-surface temperatures, sea-levels and rainfall, and a major change in marine algal flora resulted in disappearance of most of the iguanas' preferred food species and colonization of the intertidal zone by the brown alga Giffordia mitchelliae, a species not previously recorded in Galapagos. This led to widespread starvation, with about 60% of the Santa Fe population dying between March and August 1983, and similar mortality on other islands of the archipelago. Adult males and juveniles suffered the highest mortality, with 1982 hatchlings being almost completely exterminated. Body condition and growth rates were greatly depressed during ENSO, with adult growth ceasing almost entirely, but both increased again rapidly after the population crash and reached levels higher than before ENSO. There was almost no breeding in the post ENSO season (1983-84) but since then frequency of breeding, age at first breeding, and clutch size have all increased above pre-ENS0 levels. It is suggested that the increases in rates of growth and reproduction are due to a reduction in competition for food after the return of normal feeding conditions at greatly reduced population density. 1 INTRODUCTION A long term study of marine iguana (AmblYrhvnchusGristatus) population dynamics in Galapagos, begun in 1981, provided an opportunity to study the effects on the iguanas of the 1982-83 El Niiio-Southem Oscillation (ENSO) event (Philander, 1983), the most severe on record (Quinn et al., 1978, 1987; Glynn, 1988). ENSO events are characterized by a massive advection of warm, low salinity, nutrient poor surface water to the south in the eastern tropical Pacific, mainly along the coasts of Ecuador and Peru (Houvenaghel, 1978, 1984; Rasmusson, 1984; Hansen, this volume). The biological productivity of the euphotic zone declines rapidly leading to reduced survival and reproduction of animals at higher trophic levels (Barber and Chavez, 1983, 1986; Trillmich and Limberger, 1985; Arntz, 1986; Barber and Kogelschatz, this volume), although the increased rainfall leads to increased reproduction in land-based ecosystems, for example, in Darwin's finches on Galapagos (Gibbs and Grant, 1987; Grant and Grant, 1987) and in the floras of the "lomas" formations in the Atacama and Peruvian deserts (see Dillon and Rundel, this volume).

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The marine iguana is endemic to Galapagos and is widely distributed over the archipelago with highest concentrations on the western islands (Laurie, 1983a). The iguanas feed on fleshy macrophytic marine algae, either diving for them or grazing on exposed intertidal rocks at low tide (see Trillmich and Trillmich, 1986). They are sexually dimorphic, with adult males typically weighing 70% more than adult females. Adult male body weight varies from a maximum of 12.3 kg on southern Isabela to about 1.2 kg on Genovesa (Laurie, in prep.). Males defend mating territories during the breeding season, and females lay one to six eggs about one month after copulation. The eggs take three months to incubate in nests dug 30-80 cm deep in sand or volcanic ash. The time of the breeding season varies between islands (Fig. l), being earliest (nesting in January) on Santa Fe and latest (nesting in March-April) on southern Isabela and Espaiiola (Laurie, in prep.). During 1983 unusually high mortality of marine iguanas was observed in populations on all the islands of the archipelago, except Wenman and Culpepper, which were not visited (Laurie, 1983b). A major change in marine algal flora was observed during the same period and abnomially high rainfall, sea-surface temperatures (SST) and sea-levels associated with the

Fig. 1. Map of the Galapagos Islands, showing main study site, Miedo. 1982-83 El Niiio-Southern Oscillation event (ENSO) were recorded from November 1982 until July 1983. The mean monthly SST anomaly reached +4.3OC in June 1983 (Fig. 2), and the pattern of SST fluctuations was similar to those on the coast of Peru (Chavez, 1987). The

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tradewinds failed almost completely, and on Santa Cruz, where the mean annual rainfall between 1965 and 1981 was 374 mm, 3,264 mm of rain fell between November 1982 and July 1983 (Robalino, 1985). There was an increase in sea level over the same period that varied between 20 and 45 cm (Wyrtki, 1985). ENS0 events occur frequently but are poorly predictable and vary

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Fig. 2. Monthly mean sea-surface temperature (SST) anomalies (above) and monthly mean seasurface temperature (below) observed on the shore in Academy Bay, 1965-8 (courtesy Charles Darwin Research Station). Broken curve denotes long-term (22 years) annual mean SST. greatly in intensity, extent of influence and duration. Quinn et al. (1987) have documented 24 events of near moderate to very strong intensity since 1900 and 50 between 1800 and 1987, a mean frequency of one event in 3.8 years. The average interval between strong or very strong

364 ENSO events, with mean monthly sea surface temperature anomalies of 3.0 to 5.0OC, is 12.3 years (Quinn et al., 1978,1987) but the 1982-83 ENSO was exceptional, and there is evidence that the last event of comparable magnitude occurred in 1877-78 (Kiladis and Diaz, 1984). 2 STUDY AREA The main study area was at Miedo, on the south coast of Santa Fe (Fig. 1) and consisted of 2 km of low, rocky coastline with extensive intertidal flats and abundant marine algae. There is an old, uplifted beach deposit 300 m inland at the base of an escarpment, and most of the marine iguanas in the study area nested there. A number of other sites were chosen on other islands for comparative observations during regular visits over the study period. The climate of Galapagos is biseasonal: January to May is the hot season, with the only substantial rainfall, and June to December is cool, and frequently overcast, with persistent, very light drizzle (Colinvaux, 1984). 3 METHODS 3.1 Census technicues In order to collect comparative data on population densities and composition on Santa Fe and other islands binoculars were used to count animals and classify them according to sex and size. Iguanas were divided into 11 different size classes, based on snout-vent length and, with practice, animals could be classified accurately to size class without being captured or otherwise disturbed. Differences between the sexes in body size, head width and nuchal crest development were sufficient to determine the sex of most adults without capture. Prominent hemipenes were visible in some younger males when held in the hand but even after capture sex determination was generally possible only for the older animals. Counts of iguanas along the same stretch of coastline produced different results in terms of both numbers and population composition according to the time of day and state of the tide. Experiments showed that the censuses in the late afternoon gave the highest counts, and that consistent estimates of population size and composition can be made by a simple mark, release and count method (Laurie, 1982). An annual census was made each April on Santa Fe using this method: the animals released after weighing and measuring constituted the marked population. 3.2 CaDturine and marking ieuanas A total of 3,833 iguanas was marked over the study period: 3,482 on Santa Fe and 351 on Caamaiio, a small islet off Santa Cruz (Fig. 1). A further 1,440 captures were made on other islands but the animals were weighed, measured and released without marking and may not all be different individuals. Fifty-two recaptures were made of animals marked earlier by C. Rohrbach and N. Rauch on Caamaiio and Punta Nuiiez. Adult iguanas were caught by hand on the shore in the early morning when still torpid, or later with the help of a running noose on a bamboo pole. Hatchlings were caught on emergence at the nesting area in an enclosure fenced by 45 cm high plastic sheeting. An intensive effort was made to recapture all marked animals each year between February and May for measuring and weighing,

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and many adult males and females were recaptured each October or November too, at the start of the breeding season. Permanent marking was achieved by hot branding with wire brands heated in a portable gas burner. Coloured glass beads, threaded on nylon line through the nuchal crest, provided a second method of marking that was less permanent but allowed identification of individuals at greater distances. For very rapid identification of adults during limited periods of detailed observation, particularly over the breeding season, animals were painted with white, orange or yellow paint on both flanks with numbers 5 cm high. A small patch of orange or yellow paint on the neck or base of the tail was used to distinguish animals caught at different sites. There was no evidence that the numbers or the small patches of colour affected the iguanas' behaviour. 3.3 Observations of reproductive behaviour Intensive observations were made during each breeding season from 1981-82 to 1985-86. Observations were made from suitable vantage points above colonies on the coast and the nesting area, during continuous (0700-1730) daytime watches that spanned and were maintained throughout each breeding season. These involved two or three observers who worked in shifts every day for eight weeks each season. Checks were also made during the night, with some prolonged nocturnal observations at the nesting area. The proportion of females that nested each year was estimated from a combination of direct observations and changes in weight of females caught at the beginning and the end of each nesting season (Laurie, in prep.). 3.4. Measurements of ivuana Standard linear measurements were made to the nearest 1 mm on each occasion that animals were captured. They included snout to vent length (SVL), tail length (TL),maximum head width (HW) (at the point on the living animal with maximum width across the quadrates, just in front of the tympanum) and length of longest nuchal crest spine (SL). A 600 mm rigid stainless steel rule and Vernier calipers (Mitutoyo) were used for these measurements. Spring balances (Pesola) were used to determine body weight (WT) to the nearest 1 g up to 100 g, to the nearest 10 g up to 1,000 g, to the nearest 50 g up to 2,500 g and to the nearest 100 g above 2,500 g. Two people are needed to measure an iguana accurately. There appeared to be more potential for error in the way the iguanas were held for measuring, than in the actual measuring, particularly for SVL. So, as I was present throughout the study, I always held the iguanas and a number of different people did the measuring. Accuracy checks were carried out within each season using repeat measurements of 100 animals within an hour of fiist measuring. The standard deviations of measurements were: SVL, 2.2%, TL, 0.8%, HW, 2.5%, SL, 5.0% and WT, 0.5%; with only small differences between size classes. The length measurements of adult males were slightly less consistent (2.25% sd for SVL) than for smaller animals (hatchlings: 2.13%), due to small variations in the extent to which the animals were stretched for measurement. The major error appeared to be in SVL measurement so I tested for consistency between seasons and assistants by comparing the ratio of SVL to total length (SVL + TL) for each size class in each year, first discarding all measurements of animals that had lost part of their tails. If SVL and TL are assumed

366

to have independent errors and the variances are small, the standard deviation of 3.04% in S W ( S V L + TL) corresponds to a standard deviation of 2.15% in SVL measurement between seasons; i.e. the same as within seasons. 3.5 Growth Growth rates were calculated as annual rates, and corrected for differences between years in the actual date of capture, usually not more than one month. Differences in growth rates between years and between size, sex and age classes were tested by an&jsis of variance and the t-test for the difference between means, making full use of the different types of data involved: paired increments (for the same individuals in two years), unpaired increments (for the means of different individuals of the same size class at the beginning of the years in question) and data for hatchlings that can be separated into each year's cohort. 3.6 Survival r m Three sources of data were available for estimating survival rates in each sex and age class: annual recapture of marked individuals, recovery of corpses (marked and unmarked) and the annual censuses. The best data are those on recapture of marked individuals. Estimation of survival was based on the method of Pollock (1981) and reported by Laurie and Brown (in press a). 4 RESULTS 4.1 Morta litv. a w e d with E m Only ten corpses were recorded from the coastline of the study area between April 1981 and October 1982 during eight months on Santa Fe, but between November 1982 and July 1983 more than 800 corpses were recovered during six months on the island. Most corpses were washed away by the sea so the figures indicate an enonnous mortality in a population estimated to number less than 8,000 individuals in June 1982. The data for recaptures of marked individuals were used to estimate annual mortality rates (April to April) for each sex and size class and cohort (Laurie and Brown, in press a). During the 1982-83 ENSO the relative rates for each group were checked using the data from recovery of corpses and the annual census, which, although less accurate, gave very consistent results. Animals began to die as a result of ENSO as early as November 1982, so the annual mortality rates shown in Table 1 do not accurately indicate the size of the effect of ENSO. Further analysis, using November recaptures, showed that mortality over the period November 1982 to November 1983 rose from a pre-ENS0 level of 8-15% in adult males, 2-4% in adult females and 46% in hatchlings to 58% in adult males, 47% in adult females and 84% in hatchlings. These rates have since returned towards pre-ENS0 levels (Table 1) but adults of both sexes have lower survival than before ENSO and the 1985 hatchlings had a survival rate in the first year similar to hatchling survival rate in 1982 and 1983 and considerably lower than in 1981 (Laurie and Brown, in press a). Fig. 3 shows the percentage of animals that survived to the end of each year according to sex (in adults) and cohort (year of emergence).

367 TABLE 1 Estimated percentage annual mortality (April to April) for each adult sex class and cohort. COHORTS Adultmales N = 464 1981-82 1982-83 1983-84 1984-85 1985-86 1986-87

14.7 7.5 57.7 5.3 27.7 (7.2)

Adultfemales 453 3.8 1.5 47.1 13.6 16.9

1980 140

1981 643

1982 404

22.9 11.1 77.7

35.7 47.3 72.9 17.5 13.1 (14.6)

60.6 83.7 7.1 21.5

-

-

1983 422

55.6 13.1 3.1 (14.6)

1985 722

60.4 (10.9)

1986-87 figures are over-estimates (see Laurie and Brown, in press a).

The abnormal mortality started in December 1982 and continued until August 1983, with the highest mortality occurring between April and July 1983 (Laurie, 1983b). Adult iguanas weighed a mean of 54.2% (s.e. 0.9%. n = 42) of their normal weight at death, and were extremely emaciated, with no fat reserves and considerable reduction of musculature, particularly at the base of the tail (Cooper and Laurie, 1987). They were very weak and in the last few days before death could hardly move. Their stomachs generally contained very little: the mean weight of the contents of 89 adults' stomachs was 17 g (s.e. 3 g, range 0-220 g) compared with a mean of 196 g (s.e. 22 g, range 95-228 g) for 6 adults' stomachs collected during normal conditions. Apart from algae, stomach contents included small stones, pieces of crab IGraDsus iguana skin, iguana and sea-lion (7alophus d o r n i a n u ) faeces, sea-lion hairs, and earth. These other items were also observed being picked up on land by animals apparently too weak to venture into the water or the intertidal zone. The algae present in the stomach and the intestines consisted mainly of Giffordia mitchelliap and were largely undigested. In marked contrast to the normal semi-liquid state of algae in marine iguana intestines, Giffordia was relatively dry and fibrous and remained so in the faeces, which are normally liquid and amorphous containing few recognizable parts of algae. Gross and histopathological examination of iguanas that died during ENSO and comparison with others that died under normal conditions indicated that the former died of starvation (Cooper and Laurie, 1987).

m,

4.2 Changes in aleal flora

The normal red algal turf, consisting of Polvsiphonium, aelidium, C e n t r w and Spermothamnium spp. had almost entirely disappeared by March 1983 and was replaced by the brown alga Giffordia mitchelliac, which dominated the intertidal and splash zones (Laurie, 1983b). Giffordia mitchelliae has not been recorded before in Galapagos but may have been present in small quantities. It tolerates a wider range of temperatures than the red algae and was thus able to

a

I

1981

1

1982

1

1983

1984

I

7

1985

1986

1985

1986

YEAR

'"1

O

1981

1982

i 1983

1984

YEAR

Fig. 3. The percentage of animals that survived to the end of each year, adults according to sex ( 3 4 and juveniles according to cohort, or year of emergence (3b).

369 colonize the sites that the red algae had occupied previously (J. Price, pers. comm.). In vitro digestibilities of algae with sheep rumen fluid (Tillev and Terry, 1963) showed that the organic matter digestibility of the Gjffordia was 21% compared with a mean of 78% for the Chaetomorpha and Enteromorpha preferred red algal species and 64% for the green algae spp.) (Laurie and Uryu, in prep.). Brown algae generally contain more cellulose than red and green algae (Black, 1955; Paterson, 1984) and thus would be expected to be more difficult to digest. The sea level and sea-surface temperatures in Galapagos had returned to the normal range for the time of year by September 1983, and the dense mat of Giffordia algae had begun to disappear by early November and was almost completely gone by December, being slowly replaced by red algal turf, and Chaetomorpha spp. The response of the marine iguanas was almost immediate: there was no more than normal mortality after August 1983 and the surviving adults had recovered to near their 1981 condition by November 1983 (Laurie, 1987). 4.3 Growth r a m Mean annual relative increase in snout-vent length decreased in adults from 6.8% in 1981-82 to 0.5% in 1982-83, increased slightly to 1.2% in 1983-84, most of the growth being after August 1983, and then returned to pre-ENS0 levels of 6.3% in 1984-85. Juvenile growth rates recovered much faster after the ENSO, 1983 hatchlings grew faster than 1981 hatchlings in their first year. Figure 4 shows the growth rates of males and females separately; the mean annual increase in SVL (April to April) is plotted against SVL at the beginning of the year for 29 one cm size classes. The data include all records of individuals captured at the beginning and the end of the year under consideration; younger animals that did not reach 225 mm SVL during the study were not sexed, these juveniles of unknown sex are included in both curves. For some individuals there are data for only one year; for others up to six years. Points on the graphs are the means of between 8 and 178 individuals' growth rates. There was a significant decrease in growth rates from 1981-82 to 1982-83 in all size classes (1 1.2 > t > 3.4; p c 0.01), followed in 1983-84 by increased growth rates in hatchlings (16.2 > t > 3.6; p < 0.001), but continued low growth rates in adults (t = 4.73; p c 0.001 for animals of more than 22 cm SVL). Adults of both sexes hardly grew at all between April 1982 and April 1983 (mean of 0.5% increase in SVL). Growth in the year April 1983 to April 1984 was concentrated in the last part of the year after the recovery of the algal flora. The 1984-85 growth rates exceeded the 1982-83 and 1983-84 rates in all size classes (3.0 < t < 13.2; p < 0.01). For juveniles the 1984-85 growth rates were considerably higher, more than double in some size classes, than the pre-ENS0 growth rates of 1981-82 (t = 18.7; p c 0.001 for animals of less than 22 cm SVL). However, adult growth rates in 1985-86 were similar to those of 1981-82, although juvenile growth rates were still considerably higher than in 1981-82. Juvenile growth rates in 1986-87 were lower than in 1985-86 (4.3 c t < 6.2; p c 0.01) and appear to be decreasing towards pre-ENS0 levels. Figure 5 shows the growth curves for each hatchling cohort from 1980-1986 (there were extremely few hatchlings in 1984 and none was measured on emergence). The highest first year growth was recorded for 1985 hatchlings and had decreased again for the 1986 cohort. The rapid

Fig. 4. Mean annual increment in SVL plotted against SVL at beginning of the year for males (4a) and females (4b), 1981-82 to 1986-87.

9

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MEAN GROWTH RATE CM SVL PER YEAR

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MEAN GROWTH RATE CM S V L PER YEAR a,

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370

37 1

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1981

82

83

84

85

86

87

Year Fig. 5. Growth curves of hatchlings of 1980, 1981,1982, 1983, 1985 and 1986 cohorts. growth rates of the 1983 hatchlings resulted in that cohort having a greater mean size at 2 years of age than the 1981 hatchlings had at 3 years of age (Tables 2 and 3). There was also a considerable overlap in size in 1985 between 1982 and 1983 hatchlings; growth rates increased again after the slowed growth during ENSO, showing a plasticity of response to environmental conditions. Figure 6 shows the mean predicted growth in SVL for both sexes, based on the 1981-82 and the 1985-86 data on annual increments in SVL for each one cm size class (Fig. 4). It shows a clear shift to the left, so that both males and females could be expected to reach the mean size of 1981 breeding animals about two years earlier than in 1981.

4.4 Condition The relationship between log SVL and log WT was examined in order to find a suitable index of condition applicable across sex and size classes. Simple regression and principal component analyses both showed that WT/SvL3 varied little over sex and size classes at the time of measurement (Wong, 1985). Figure 7 shows the changes in mean condition of adult iguanas (SVL > 225 mm) on Santa Fe over the seven years 1981-1987. Results for other islands, with the exception of the small islet CaamaAo, are similar (Table 4). The clear trough in 1983, when many animals lost almost 50% of their body weight before either dying or recovering, was followed by a sharp rise in condition to well above the pre-ENS0 level, and then a return to that level. There was a marked decrease in condition of animals well before the 1982-83 ENSO and before the first negative sea surface temperature anomaly of the event (-1.OOC) was recorded in Galapagos by A.

372 TABLE 2 Age specific snout-vent lengths of hatchlings of different cohorts, 1981-1987. Cohort

Emergence

1 yr

2 P

3 P

4 P

5 P

6 P

1981 SVL s.e. n

a 106.7 (0.2) 643

a 136.1 (0.4) 282

a 170.4 (0.8) 181

a 197.7 (1.6) 41

a 247.2 (2.0) 37

a288.5 (3.7) 22

297.0 (5.4) 22

1982 SVL s.e. n

a 107.0 (0.2) 404

a 137.4 a 167.9 (3.1) (0.6) 140 14

b 217.9

(2.5) 19

b 261.2 (3.0) 12

a 286.7 (5.2) 7

1983 SVL s.e. n

ab 107.5 (0.2) 422

b 146.0 b 204.1 (0.8) (1.2) 137 118

c 252.4 (1.6) 94

c 273.1 (2.3) 75

Almost no reproduction took place in 1983-84

1984-1985 SVL s.e. n

a 107.2 (0.1) 743

c 162.0 (0.7) 222

1986 SVL s.e. n

b 108.2 (0.4) 109

d 149.0 (0.7) 75

c 199.4 (1.1) 156

Within years, cohorts with different letters (a,b,c, etc.) have significantly different snout-vent lengths (p < 0.001).

Matson (pers. comm., 1983) in May 1982. There is an inverse correlation (rs = -0.6, p < 0.05) between the condition index (Fig. 7) and the mean monthly sea surface temperature anomaly between 1981 and 1987 (Fig. 8).

4.5 Effects on reproduction The most obvious effect of ENS0 on reproduction was the almost complete failure of breeding in the 1983-84 season. On Santa Fe, territorial defence was less intense than normal, with only 25% of the normal number of territorial males and fewer extended fights (Laurie, 1984), but the main difference from previous years was in the reactions of the females, who consistently avoided the males' approaches. Not a single copulation was seen during one month of observation, although during the same period of observation in each of the other four years of the study between 55 and 70 copulations were recorded. In the 1981-82 and 1982-83 seasons the males finished mating by early January, but in the 1983-84 season temtorial defence continued until early March, with the difference that the territory holders fed more frequently and lost significantly less weight than in a normal year.

373 TABLE 3

Age specific weights of hatchlings of different cohorts, 1981-1987. Cohort

Emergence

1 yr

2yr

3yr

4yr

5yr

6yr

1981 WT(g) s.e. n

a 58.8 (0.3) 643

a 121.1 a203.4 (3.9) (1.3) 282 181

a436.8 (12.7) 41

a 851.9 a 1,288.6 1,413.6 (21.3) (44.7) (81.6) 37 22 22

1982 WT s.e. n

a 59.4 (0.4) 404

b 105.5 b 251.4 (2.1) (12.8) 140 14

b 584.7 (19.9) 19

a 922.5 a 1,271.4 (37.0) (102.9) 12 7

1983 WT s.e. n

b 56.5 (0.4) 422

c 166.8 c468.4 (8.1) (2.8) 137 118

c 826.4 b 1,101.2 (26.0) (15.7) 94 75

Almost no reproduction took place in 1983-84 1984-1985 WT s.e. n

c 62.9 (0.3) 743

d 212.7 (2.8) 222

1986 WT s.e. n

c 63.5 (0.7) 109

e 183.7 (4.4) 75

d 423.5 (6.8) 156

Within years, cohorts with different letters (a,b,c, etc.) have significantly different weights @