Coastal Hypoxia: Consequences for Living Resources and Ecosystems

465 Pages·2001·1.47 MB·English

by  Claire J. Creutzfeldt

Coastal
and Estuarine Studies
58
Nancy N. Rabalais and R. Eugene Turner (Eds.)
Coastal Hypoxia
Consequences for Living Resources and
Ecosystems
American Geophysical Union
Washington,
Published under the aegis of the AGU Books Board
John E. Costa, Chair; David BercoviciA, ndrewD essler,J effrey M. Forbes,W . RockwellG eyer,
Rebecca Lange, Douglas S. Luther, Darrell Strobel, and R. Eugene Turner, members.
Library of Congress Cataloging-in-Publication Data
Coastal Hypoxia: consequences for living resources and ecosystems/ Nancy N. Rabalais and
R. Eugene Turner, editors.
p. cm -- (Coastal and estuarine studies; 58) (Coastal and estuarine studies; 58)
Based on papers from a workshop held in Baton Rouge, La., Mar. 1998.
Includes bibliographicalr eferences.
ISBN 0-87590-272-3
1. Coastal ecology--Congresses. 2. Water--Dissolved oxygen--Environmentaal spects. I.
Rabalais, Nancy N., 1950-II. Turner, R. E. (Robert Eugene), 1945- III. American Geophysical
Union. IV. Series. V. Series: Coastal and estuarine studies; 58
QH541.5.C65 C5914 2001
577.5'1--dc21 00-065060
ISSN 0733-9569
ISBN 0-87590-272-3
Copyright 2001 by the American GeophysicalU nion, 2000 Florida Ave., NW, Washington,D C
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CONTENTS
Preface
NancyN . Rabalaisa ndR . EugeneT urner. ..................... v
1 Hypoxia in the Northern Gulf of Mexico:D escriptionC, ausesa nd Change
Nancy N. Rabalais and R. EugeneT urner ....................... 1
Section I: Plankton
2 Impactso f ChangingS i/N Ratiosa nd PhytoplanktonS peciesC omposition
Quay Dortch,N ancyN . Rabalais,R . EugeneT urner,
and Naureen, 4. Quresh.i. .................................. 37
3 Zooplankton:R esponsesto and Consequenceosf Hypoxia
Nancy H. Marcus ......................................... 49
4 Distribution of Zooplankton on a SeasonallyH ypoxic Continental Shelf
Naureen, 4. Qureshia nd Nancy N. Rabalais. .................... 61
5 PelagicC nidarians and Ctenophoresin Low DissolvedO xygen
Environments: A Review
JenniferE . Purcell, DeniseL . Breitburg,M ary Beth Decker,
144'IllarMe. Graham,M arshd . Youngblutha,n d KevinA . Raskoff .... 77
Section II: Physiology and Behavior
6 PhysiologicalR esponsest o Hypoxia
Louis E. Burnett and 14qlliam B. Stickle ....................... 101
7 Responseso f Nekton and Demersal and Benthic Fauna
to Decreasing Oxygen Concentrations
NancyN . Rabalais,D onald E. Harper,J r., and R. EugeneT urner ... 115
Section III: Benthos
8 Overview ofAnthropogenica!!y-InducedH ypoxic Effects on
Marine Benthic Fauna
RobertJ . Diaz and Rutget Rosenberg. ....................... 129
9 Benthic Foraminiferal Communitiesi n Oxygen-Depleted
Environments of the Louisiana Continental Shelf
Emil Platon and Barun K. Sen Gupta. ........................ 147
10 Effects of Hypoxia and Anoxia on Meiofauna: A Review with
New Data from the Gulf of Mexico
Markus ,4. WetzelJ, ohn W.F leeger,a nd SeanP . Powers .......... 165
11 Effect of Hypoxia/Anoxia on the Supply and Settlement of Benthic
Invertebrate Larvae
.SeanP . Powers,D onald E. Harper, Jr., and NancyN . Rabalais. .... 185
12 Effects of SeasonalH ypoxia on Continental Shelf Benthos
Nancy N. Rabalais,L oreneE . Smith,D onald E. Harper, Jr.,
and Dubravko Justic .....................................
Section IV: Fish and Fisheries
13 Effects of Low DissolvedO xygen on the Behavior, Ecology and Harvest of
Fishes:A Comparisono f the ChesapeakeB ay and Baltic-Kattegat Systems
Denise L. Breitburg,L eif Pihl, and Sarah E. Kolesar. ............ 241
14 Ecological Effects of Hypoxia on Fish, Sea Turtles, and Marine Mammals in
the Northwestern Gulf of Mexico
d. Kevin Craig, Larry B. Crowder,C harlotteD . Gray,
Cartie d. McDaniel, TyrrellA . Henwood,a nd damesG Hanifen ..... 269
15 Effects of Hypoxia on the Shrimp Fishery of Louisiana and Texas
Roger d. Zimmermana nd damesM . Nance .................... 293
16 Distribution of Catch in the Gulf Menhaden, Brevoortiap atronus,P urse Seine
Fishery in the Northern Gulf of Mexico from Logbook Information:
Are There Relationships to the Hypoxic Zone?
dosephW . Smith. ........................................ 311
Section V: Food Webs and Ecosystems
17 The Effects of Hypoxia on the Northern Gulf of Mexico Coastal Ecosystem:A
Fisheries Perspective
Edward J. Chesneya nd Donald M. Baltz ...................... 321
18 A Brief Overview of Catchment Basin Effects on Marine Fisheries
dohn E Caddy .......................................... 355
19 Some Effects of Eutrophication on Pelagic and Demersal Marine Food Webs
R. Eugene Turner. ....................................... 371
Section VI: Perspectives
20 An Economic Perspectiveo f Hypoxia in the Northern Gulf of Mexico
WalterR . Keithly,d r, and dohnM . Ward ...................... 399
21 Hypoxia, Nutrient Managementa nd Restorationi n Danish Waters
Daniel d. Conleya nd Alf B. doseJ3on... ...................... 425
22 Future Perspectivesf or Hypoxia in the Northern Gulf of Mexico
Dubravkod ustic,N ancy N. Rabalais,a nd R. EugeneT urner ....... 435
Summary
23 Commonality and the Future
R. EugeneT urnera nd NancyN . Rabalais ..................... 451
Index ............................................................ 455
List of Contributors ................................................
PREFACE
Youm ust notj ust live on the earth.
You must live with the Earth.
Will you leave it a little better than wheny ouf ound it?
W Niering, CommencemenCt onvocationC, onnecticuCt ollege, 1993
Hypoxia is a conditiont hat occursw hen dissolvedo xygenf alls below the level
necessaryto sustainm ost animal life. In U.S. coastalw aters,a nd in the entirew est-
ernA tlantic,w e find the largesth ypoxicz onei n the northernG ulf of Mexico on the
Louisiana/Texasc ontinentals helf. The area affected,w hich is about the size of the
stateo f New Jerseya t its maximale xtent,h asi ncreaseds incer egularm easurements
begani n 1985. Sedimentc oresf rom the hypoxicz onea lsos howt hat algal produc-
tion and deposition,a s well as oxygens tressw, ere much lower earlier in the 1900s
andt hat significantin creaseso ccurredin the latterh alf of the twentiethc entury.W e
publisht his book against he backgroundo f suchm easurementsa,n d to review how
the developinga nd expandingh ypoxicz oneh asa ffectedl iving resourceso n this con-
tinental shelf.
Human alterationso f the landscapew ithin the MississippRi iver watersheda nd
increasesi n nutrient loading particularlyf rom agriculturala ctivitiesa re directly
linked to the changingc oastale cosystemi,n cludingt he worseningo f hypoxia.A s
thesec hangesp arallel global patternso f increasingn utrientl oadst o estuarinea nd
coastawl aters,w e considetrh en orthernG ulf of Mexicoh ypoxica reaa ss ymptomatic
of similar situationsw orldwide. The continentals caleo f the watershed,t he immense
sizeo f the Gulf hypoxicz one( up to 20,000 km2),a ndt he relativelyo penc oastals ys-
tem into which the MississippiR iver dischargesh, owever,c reated ifferentp hysical
and biologicald imensionsth at boundt he ecologicael ffects.
Fisheryr esourceso f the Gulf are amongt he mostv aluablei n the United States.
Gulf commerciall andingso f fish and shellfishh ave an annual docksidev alue of
about$ 700 million (approximately$ 1.4 billion when processedw), hile recreational
andc ommerciafl isheriest ogetherg eneratea round$ 2.8 billion per year.B ut defining
the ecologicala nd economicc onsequenceosf hypoxiao n the living resourceso f the
northernG ulf hasp rovend ifficult.L ackingh erei s an historicd atab asea gainstw hich
to detect environmentalc hanges,o r no changes,i n the fisheriest hemselvesA. lso
lackingi s currentd ata specifict o the distributiona nd abundanceo f living resources.
Althoughe cologicals ystemsh ave changeda nd living resourcesa re affectedi n the
Gulf as a resulto f nutriento ver-enrichmenatn dh ypoxia,a vailablee conomicin dica-
tors do not necessarilytr anslatee xcessn utrientsto losso f fishingr evenue.I f experi-
encesi n otherc oastala ndm arines ystemsa re applicableto the Gulf of Mexico, how-
ever,t he potentiali mpacto f worseningh ypoxicc onditionsm ay promptt he decline
(perhapsp recipitouso) f ecologicallya ndc ommerciallyim portant
Initially, we designedth is bookt o identifyt he stateo f knowledgef or the Gulf of
Mexico with regardt o the effectso f nutriento ver-enrichmenatn dh ypoxiao n living
resourcesf,r omp hytoplanktotno marinem ammalsA. mbitiousa st hisg oalm ay seem,
there were many individualsw ithin the Gulf and elsewherew orking on just these
aspects.I t soonb ecamec lear that we would be able to define the limits, and more
clearly define the numerousu ncertaintieso, f our knowledgeA. lthoughr elevantd ata
existed,t hey were insufficienfto r a completea nalysiso f the Gulf. In thisr espectt,h e
informationa nd experienceo f thosew orkingo utsidet he Gulf becameq uitev aluable
in our attemptt o craft a syntheticid ea of what might be happeningin the Gulf. Our
interestsin the subject,a nd in completingth is book, did not take placei n an admin-
istrativeo r managerialv acuum,n or were they confinedt o academics.
An effort to embarko n nutrientm anagemenwt ithin the MississippRi iver water-
shedb egani n earnesti n 1994, followinga dramatici ncreasein the size of the Gulf
hypoxicz one and legal actionst akenb y environmentaol rganizationsM. obilization
of the necessaryp oliticala nds ocialf orcest o supporta nutrientm anagemenptl ant hat
might affect 41% of the lower 48 United Statesu nfortunatelyn ecessitatetdh e identi-
fication of a "smokingg un" of environmentadl egradationin the Gulf. (Elsewherei n
the world-- e.g., ChesapeakeB ay, TampaB ay, the Baltic Sea,N orth Sea,a nd Long
Island Sound- - statesa ndn ationsh avem ovedf orwardw ith nutrientr eductionp lans
for the benefit of improvingc oastalw ater quality.)A s part of the processt owards
implementinga nutrientm anagemenpt lan, the MississippiR iver/Gulf of Mexico
Task Force commissioneda serieso f studiest hrought he White HouseC ommitteeo n
Environmenta nd Natural Resources(C ENR), includinga studyo n the "Ecological
andE conomicC onsequenceosf Hypoxia."T he CENR effortw as a broad-brusshy n-
thesis of available publishedi nformationw ithout new data analyses.I n a parallel
effort, we obtaineds upport hrought he competitiveS ea Grant Programf or a synthe-
siso f the effectso fhypoxia on living resourcesin the Gulf of Mexico. The two efforts
came togetheri n a workshopo n "Effects of Hypoxia on Living Resourcesin the
Northern Gulf of Mexico" in March 1998 in BatonR ouge,L ouisiana.N early 70 Gulf
of Mexico, U.S. and internationals cientistsm et to determine our current level of
understandinogn the Gulf, draw comparisonfsr om othera reaso f the world, discuss
necessarrye searchto betterd efinet he effectso f hypoxiao n Gulf resourcesa,n dp lan
this book.
Contributinga uthorsp rovider eviews and analysesf rom differentp erspectives,
ranging from planktont o benthosa nd fish, from an organism'sp erspectiveto an
ecosystemv iew, and from a scientist'sa nalyticala nd empirical experienceto that
describingth e complexi nteractionos f managemenpt,o liticsa nda dministrationT.h is
is a complexs ubject o covert horoughlya, nd we thankt he authorsf or their scientif-
ic leadershipa ndu sefuli nsightsin this regard.C hapterb y chaptero, ur authorsid en-
tify mucht o accomplishs, o as to thoroughlya ddressa ll aspectso f concerna nd to
identify optionsf or future work toward our commong oal: to sustaint he natural
resourceb asea nd societaln eedsw ithin a well-ventilated,i nformed,a ndt imely deci-
sion-makingp rocessC. ertainlyw, e do not believet hatt he problemsw e faceh erec an
be "solved" in a brief, few years. We also understandt hat they will never be
addresseds atisfactorilyw ithoutt he effortso f authors,s ucha s thosew e present,w ho
have written for an audienceo f informedc itizens,c olleges tudentsp, racticings cien-
tists, and resourcem anagers.
The March 1998 workshop was co-sponsoredb y the Louisiana Sea Grant
CollegeP rogram( Grant No. NA86RG0073, R166753A&B to N. N. Rabalaisa nd R.
E. Turner); the Hypoxia Working Group, Committeeo n Environmentala nd Natural
ResourcesW, hite HouseO ffice of Sciencea nd TechnologyP olicy (grant to R. Diaz
and A. Solow); Louisiana UniversitiesM arine Consortium;a nd Louisiana State
University, CoastalE cology Institute.T he editorsg ratefullya cknowledgef undsf or
completiono f the book from the LouisianaS ea Grant College Programa nd the
Departmento f Energy( DE-FG02-97ER12220t o N. N. Rabalais),a nd from the San
Diego Foundationfo r supporot f colorp latesa ndp hotographsW. e particularlya ppre-
ciate the work of the three-to-fourr eviewersf or eachc hapterw ho providedc ritical-
ly constructivea nd timely reviews.
Nancy N. Rabalais
R. Eugene Turner
Editors
Take'em down - to the riverside
and thro'em over the side
to be sweptu p by a current,
then taken to the ocean,
to be eaten by somef ishes,
who were eaten by somef ishes,
and swallowedb y a whale,
who grew so old,
he decomposed
he died, and left his body
to the bottomo f the ocean.
Now, everybodyk nows
that whena bodyd ecomposes
the basic elements
are given back to the ocean
and the sea doesw hat it ought'ta.
Harry Nilsson,t he song" Think AboutY our Troubles"
from The Point
Hypoxia in the Northern Gulf of Mexico'
Description,C ausesa nd Change
Nancy N. Rabalaisa nd R. EugeneT urner
Abstract
Nutrient over-enrichmenti n many areas around the world is having pervasive
ecologicael ffectso n coastale cosystemsT. hesee ffectsi ncluder educedd issolvedo xygen
in aquatics ystemsa nd subsequenitm pactso n living resources. The largestz one of
oxygen-depletedc oastalw aters in the United States,a nd the entire western Atlantic
Ocean, is found in the northern Gulf of Mexico on the Louisiana/Texasc ontinentals helf
influencedb y the freshwaterd ischargea ndn utrientl oad of the MississippRi iver system.
Them id-summbeor ttoma reael xtenot f hypoxiwc aters(< 2 mg1 - • 02) in 1985-1992
average8d,0 00t o 9,000k m2 b uti ncreasetod u pt o 16,000to 20,000k m2 i n 1993-2000.
Hypoxicw atersa re mostp revalentf rom late springt hroughl ate summer,a ndh ypoxiai s
more widespreada nd persistenti n some years than in others. Hypoxic waters are
distributedfr om shallowd epthsn ear shore( 4 to 5 m) to as deepa s 60 m water depthb ut
more typicallyb etween5 and 30 m. Hypoxia occursm ostlyi n the lower water column
but encompasseass much as the lower half to two-thirdso f the water column. The
MississippiR iver systemi s the dominants ourceo f fresh water and nutrientst o the
northernG ulf of Mexico. MississippiR iver nutrientc oncentrationasn d loading to the
adjacecnot ntinenstahle lhf avec hangeind t hel asth alfo ft he2 0t hc enturyT.h ea verage
annualn itratec oncentrationd oubled,a ndt he means ilicatec oncentratiown as reducedb y
50%. There is no doubt that the averagec oncentrationa nd flux of nitrogen (per unit
volume dischargei)n creasedfr om the 1950st o 1980s,e speciallyin the spring. There is
considerable videncet hat nutriente nhancedp rimaryp roductioni n the northernG ulf of
Mexico is causallyr elatedt o the oxygend epletioni n the lower water column. Evidence
from long-termd atas etsa ndt he sedimentarrye cordd emonstratteh ath istorici ncreasesin
CoastaHl ypoxiaC: onsequencfoersL ivingR esourceasn dE cosystems
Coastaal ndE stuarineS tudiesP, ages1 -36
Copyrigh2t 001 by theA mericanG eophysical
2 Gulf of Mexico Hypoxia
rivefined issolvedin organicn itrogenc oncentratioann dl oadso vert he last 50 yearsa re
highlyc orrelatewdi thi ndicatorosf increasepdr oductivitiyn theo verlyingw aterc olumn,
i.e., eutrophicationf t he continentaslh elfw atersa, nds ubsequewnot rseninogf oxygen
stressin the bottomw aters. Evidencea ssociateisn creasedc oastaol ceanp roductivitya nd
worseninogx ygend epletiown ithc hangeisn landscapues ea ndn utrienmt anagemetnhta t
resultedin nutriente nrichmenotf receivingw aters.T hus,n utrienftl ux to coastasl ystems
has increasedo ver time due to anthropogenaicc tivitiesa nd has led to broad-scale
degradationo f the marinee nvironment.
Introduction
There is increasingc oncerni n many areasa roundt he world that an oversupplyo f
nutrientsf rom multiple sourcesis having pervasivee cologicale ffectso n shallowc oastal
and estuarine areas. Marine plants provide essential habitat, and there are well-
establishedp ositive relationshipsb etween dissolved inorganic nitrogen flux and
phytoplanktonp rimary production( e.g., Nixon et at. [1996], Lohrenze t al. [1997]). In
addition, data from 36 marine systemss how a relationshipb etweenf isheriesy ield and
primary production[ Nixon, 1988]. There are thresholdsh, owever,w here the load of
nutrientst o a marine systemc ausesw ater quality degradationa nd detrimentalc hangest o
fisheries[ Caddy, 1993].
While a variety of changesm ay resulti n the increaseda ccumulationo f organicm atter
in a marine system( = eutrophicationa, s defined by Nixon [1995]), the most common
factor is an increasei n the amount of nitrogen and phosphorusm arine waters receive.
With an increasein the world populationa, focusingo f that populationi n coastalr egions
and agriculturale xpansioni n major river basins,e utrophicationis becominga major
environmentapl roblemi n coastalw aterst hroughouth e world. Humansh ave alteredt he
global cycles of nitrogena nd phosphoruso ver large regionsa nd increasedt he mobility
and availability of thesen utrientst o marine ecosystems[P eierlse t al., 1991; Howarth et
al., 1995, 1996; Vitousek et al., 1997; Howarth, 1998; Caraco and Cole, 1999]. These
human-controlledi nputs are the result of human populationsa nd their activities,
particularlyt he applicationo f nitrogen and phosphorusfe rtilizers,n itrogen fixation by
leguminousc rops, and atmosphericd epositiono f oxidized nitrogen from fossil-fuel
combustion. Changes in the relative proportionso f these nutrients may exacerbate
eutrophicationf,a vor noxiousa lgal bloomsa nd aggravatec onditionso f oxygend epletion
[Officer and Ryther, 1980; Smayda, 1990; Conley et al., 1993; Justic' et al. 1995a,b;
Turner et at., 1998].
The impairmento f watersf rom nutriento ver-enrichmengt oesw ell beyonds cummy-
looking water to threatening the suitability of water for human consumptiona nd
impairingt he sustainedp roductiono f usefulf ormso f aquaticl ife. Excessn utrientsl ead
to degradedw ater quality throughi ncreasedp hytoplanktono r filamentousa lgal growth.
Increasingn utrientl oadsa re the causeo f somen oxiouso r harmfula tgatb looms( HABs),
including some toxic forms. Secondarye ffects include increasedt urbidity or oxygen-
depletedw aters( = hypoxia)a nd eventuallyl osso f habitatw ith consequencetos marine
biodiversitya nd changesi n ecosystems tructurea nd function. Over the last two decades
it has becomei ncreasinglya pparent hat the effectso f eutrophicationi,n cluding
Rabalais and Turner 3
depletiona,r e not minora nd localizedb, ut havel arge-scailme plicationasn d are
spreadinragp idly[R osenbe1rg9,8 5D; iaza ndR osenber1g9,9 5A; nderso1n9, 95N; ixon,
1995; Paerl, 1995, 1997].
Watewr ithl essth an2 mg1 -• dissolvoexdy geins c onsidehreydp oxicH. ypoxia
occurnsa turalliyn manyp artso f thew orld'ms arinen vironmenstusc, ha s0 ordsd, eep
basinso, peno ceano xygenm inimumzo nesa, ndo xygenm inimumzo nesa ssociatewdit h
westerbno undaruyp wellinsgy stem[sK amykowsakni dZ entara1, 990]. Hypoxica nd
anoxic(n oo xygenw) atersh avee xistetdh roughoguet ologitcim e,b utt heiro ccurrencine
shallocwo astanl de stuarianree aasp peatrosb ei ncreasi[nDgi aza ndR osenbe1rg9,9 5].
The largeszto neo f oxygen-deplecteoda stawl atersin theU nitedS tatesa,n dt hee ntire
western Atlantic Ocean, is in the northernG ulf of Mexico on the Louisiana/Texas
continentsahl elfa t thet erminuosf theM ississipRpiiv ers ystem(P late1 ). Thes izeo f
theG ulfo f Mexicoh ypoxizco nere ache2s0 ,000k m2 in mid-summ[Rera balai1s9, 99],
andr ankst hirdi n areab ehinds imilarc oastahl ypoxicz oneso nt hen orthwestesrnh elfo f
theB lackS eaa ndi n theB alticb asinsT. heh ypoxicz onei n then ortherGn ulfo f Mexico
(averagfeo r 1993-1999i)s abouth e sizeo f the stateo f New Jerseyo r the stateso f
Rhode Island and Connecticuct ombined. Its extent on the bottomi s twice the total
surfacaer eao ft hew holeC hesapeaBkaey ,a ndit sv olumies s everaolr derosf magnitude
greatetrh ant heh ypoxicw aterm asso f ChesapeaBkea y[ Rabalais1,9 98].
The watershedth at drainst hrought he Mississippia nd AtchafalayaR ivers to the Gulf
of Mexico is also immense( Plate 1). The MississippiR iver systemr anks amongt he
world's top ten rivers in length, freshwaterd ischargea nd sedimentd elivery and drains
41% of the lower forty-eightU nited States[ Milliman and Meade, 1983]. Thus, the
dimensionso f the problem and the drainages ystemt hat affect it are of much greater
magnitudeth anm ostn utrient-drivene utrophicatiopnr oblemse lsewhere.
The linked MississippiR iver systema nd the northernG ulf of Mexico is an example
of the worldwide trend of increasingr iverbornen utrientsa nd worseningc oastalw ater
quality. Model simulationsr,e searchs tudiese, mpiricalr elationshipsa nd retrospective
analyseso f the sedimentarrye cordh ave producedc onsiderablev idencet hat nutrient
loadingf rom the MississippRi iver systemis the dominantf actori n controllingt he extent
andd egreeo fhypoxiaa ndi ts worseningin the lastc entury[ Rabalaise t al., 1996, 1999].
Despite recent advancesi n identifying links between Mississippi River system
dischargea nd nutrient loads and coastalh ypoxia in the Gulf of Mexico, defining the
ecologicaal nde conomicc onsequenceosf hypoxiao n the living resourceso f the northern
Gulf of Mexico has proven difficult. Long-termf isheriesd ata are lacking, as are data
specifict o present-dayd istributiona nd abundanceo f living resources.E cosystemle vel
changesh ave occurred,h owever,c onsistenwt ith changesin MississippiR iver system
dischargea nd nutrientl oads. In this chapterw, e describeth e phenomenono f hypoxiai n
the Gulf of Mexico, its physicala nd biologicalc ausest,h e closec ouplingo f hypoxiaw ith
MississippiR iver effluents,a nd the historicalc hangesin river constituentsa nd hypoxia
that parallele acho ther. Againstt his backgroundo f watershedla ndscapec hangesh, uman
activities, and worseningh ypoxic conditionsi n the Gulf of Mexico, the subsequent
chaptersd etailt he stateo f knowledgeo f hypoxiao n living resourceos f the northernG ulf
within the broaderc ontexto f patternsa lreadyd emonstratedel sewherei n the world's
coastal