Science for 

COASTAL OCEAN PROG 

Decision Analysis Series No. 16 

eport for t 

on Hypoxia in the Gulf o 

Robert J. Diaz and Andrew Solow 

May 1999 

'RODUCTION 

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FISHERY 

YfELD 

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FISH ' I I 

I : SWONAL : : PUIMANFNT BUIlOM ANOXIA 

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OLIGO- : MESO- EU- : DYS-TROPHIC 1 I I 

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NUTRIENT LOADING 

National Ocean Service 

Coastal Ocean Program 
This report is the fourth in a series of six reports developed as the scientific basis for an integrated assessment of the causes and consequences of hypoxia in the 

Gulf of Mexico, as requested by the White House Office of Science and Technology Policy and as required by 

Section 604a of P.L. 105-383. For more information on 

the assessment and the assessment process, please 

contact the National Centers for Coastal Ocean Science at (30 I) 7 1 3-3060. 

The Decision Analysis Series has been established by 

NOAA's Coastal Ocean Program (COP) to present 

documents for coastal decision makers which contain 

analytical treatments of major issues or topics. The issues, topics, and principal investigators have been selected through an extensive peer review process. To 

learn more about the COP or the Decision Analysis 

Series, please write to: 

NOAA 

National Centers for Coastal Ocean Science 

Coastal Ocean Program 

1 3 1 5 East-West Highway, Room 9700 

Silver Spring, Maryland 209 10 

phone: 30 1-7 13-3338 

fax: 30 1 -7 1 3-4044 

web: http://www.cop.noaa.gov 

e-mail: coastalocean@cop.noaa.gov 

Cover image: Location map of the study 

area for the water quality model. 
Science for Solutions 

NOAA COASTAL OCEAN PROGRAM 

Decision Analysis Series No. 16 

Ecological and Economic 

Consequences of Hypoxia 

Topic 2 Report for the Integrated Assessment 

on Hypoxia in the Gulf of Mexico 

Robert J. Diaz, Virginia Institute of Marine Science 

Andrew Solow, Woods Hole Oceanographic Institution 

May 1999 

U.S. DEPARTMENT OF COMMERCE 

William M. Daley, Secretary 

National Oceanic and Atmospheric Administration 

D. James Baker, Undersecretary for Oceans and Atmosphere 

National Ocean Sewice 

Nancy Foster, Assistant Administrator 

National Centers for Coastal Ocean Science 

Donald Scavia, Director 

Center for Sponsored Coastal Ocean Research-Coastal Ocean Program 

David Johnson, Director 
This publication should be cited as: 

Diaz, Robert J., and Andrew Solow. 1999. Ecological and Economic Consequences of Hypoxia: Topic 2 Report for the Integrated Assessment on Hypoxia in the Gulf of Mexico. 

NOAA Coastal Ocean Program Decision Analysis Series No. 16. NOAA Coastal Ocean Program, Silver Spring, MD. 45 pp. 

Corresponding author information: 

Robert J. Diaz 

Virginia Institute of Marine Science 

College of William and Mary 

Gloucester Pt., Virginia 23062 

Andrew Solow 

Marine Policy Center 

Woods Hole Oceanographic Institution 

Crowell House, MS#4 1 

Woods Hole, Massachusetts 02543 

This publication does not constitute an endorsement of any commercial product 

or intend to be an opinion beyond scientific or other result; obtained by the National Oceanic and Atmospheric Administration (NOAA). No reference shall be 

made to NOAA, or to this publication furnished by NOAA, in any advertising or 

sales promotion that would indicate or imply that NOAA recommends or endorses any proprietary product mentioned herein, or that has as its purpose an interest to cause directly or indirectly the advertised product to be used or purchased 

because of this publication. 
Contents 

LIST OF FIGURES AND TABLES .................................................................................................. v 

.. ACKNOWLEDGMENTS ............................................................................................................... V~I 

FOREWORD ................................................................................................................................. ix 

EXECUTIVE SUMMARY ................................................................................................................ 

Scope of This Report ............................................................................................................. I 

Linking Land and Sea ............................................................................................................... I 

Assessing Effects ..................................................................................................................... 3 

METHODS ......................................................................................................................... 5 

Ecological Data Sources ......................................................................................................... 5 

Economic Methods ................................................................................................................. 6 

2.2.1 A conceptual model for economic effects ................................................................. 6 

2.2.2 A proxy for hypoxia .................................................................................................... 7 

Meetings and Workshops ...................................................................................................... 9 

RESULTS ............................................................................................................................. 10 

Background on Hypoxia as a Global Environmental Problem ............................................ I0 

3.1 . 1 Nutrients. eutrophication. and hypoxia ................................................................... I0 

3.1.2 Oxygen budgets around the globe ........................................................................... I I 

3.1.3 System potential for hypoxia ................................................................................... I I 

3.1.4 Type of hypoxia. severity. and system response ..................................................... 12 

Northern Gulf of Mexico. Ecological Analysis of Hypoxia ................................................. 13 

3.2.1 Zooplankton and hypoxia ......................................................................................... 14 

3.2.2 Benthic communities and hypoxia ........................................................................... 14 

3.2.3 Benthic secondary production and hypoxia ............................................................. I8 

3.2.4 Loss of bottom habitat: an example of hypoxic effects on shrimp ......................... 18 

3.2.5 Fish populations ........................................................................................................ 22 

Northern Gulf of Mexico. Economic Analysis of Hypoxia ............................................... ..23 

3.3.1 Economic analysis of shrimp data ............................................................................ 23 

3.3.1 . I Catch per unit effort and hypoxia ............................................................. 24 

3.3.1.2 Depth of landings and hypoxia ................................................................... 26 

3.3.1.3 Shrimp size and hypoxia ............................................................................ 29 
iv Ecolonical and Economic Consequences of Hypoxia 

3.3.1.4 Shrimp and hypoxia: Summary .................................................................. 30 

3.3.2 Economic analysis of menhaden data ....................................................................... 32 

3.3.3 Economic analysis of red snapper data .................................................................... 33 

RESEARCH NEEDS .............................................................. .......................................... 35 

Establishing a Conceptual Framework ................................................................................ 35 

Directed Research ................................................................................................................ 35 

~ONCLUS!ONS AND RECOMMENDAT~ONS ................................................................. 37 

Ecological Effects ................................................................................................................... 37 

Economic Effects ................................................................................................................... 38 

Recommendations ............................................................................................................... 39 
List of Figures and Tables 

FIGURES 

FIGURE 1.1. 

FIGURE 2.1. 

FIGURE 2.2. 

FIGURE 3.1. 

FIGURE 3.2. 

FIGURE 3.3. 

FIGURE 3.4. 

FIGURE 3.5. 

FIGURE 3.6. 

FIGURE 3.7. 

FIGURE 3.8. 

FIGURE 3.9. 

Comparative evaluation of fishery response to nutrients based on data 

from around the world (modified and redrawn from Caddy l993).. ...................... 2 

Hypoxia index used in the economic analysis .......................................................... 8 

Plot of measured hypoxic area vs. hypoxia index used in the economic analysis. .... 9 

Total number of finfish caught in summer (July-August) trawls 

by the SEAMAP program for the years 1987-88 and 1993-94 .......................... 19 

Total number of penaeid shrimp caught in summer Uuly-August) trawls 

by the SEAMAP program for the years 1987-88 and 1993-94 .......................... 20 

Pounds of penaeid shrimp landed versus the relative annual occurrence . . . . of hypoxla in selected statistxal subareas ................................................................ 21 

Boundaries for the 21 statistical subareas established for reporting 

of fisheries landing in the Gulf of Mexico. ........................................................... 23 

July-August catch per unit effort (CPUE) for brown shrimp in 

three fisheries zones. .............................................................................................. 25 

August-September catch per unit effort (CPUE) for white shrimp in 

three fisheries zones. ............................................................................................ ,.26 

Average depth of July-August brown shrimp landings in three fisheries zones. ..27 

Average depth of August-September white shrimp landings in three 

fisheries zones ......................................................................................................... 28 

Average July-August numbers of brown shrimp per landed pound in 

three fisheries zones. .............................................................................................. 29 

FIGURE 3.10. Average August-September numbers of white shrimp per landed pound 

in three fisheries zones. .......................................................................................... 30 

FIGURE 3.11. Spawning stock biomass (SSB) of menhaden in the Gulf of Mexico .................. 32 

FIGURE 3.12. Catch per unit effort (CPUE) of menhaden in the Gulf of Mexico ................... 33 
vi Ecological and Economic Consequences of Hypoxia 

TABLES 

TABLE 1.1. 

TABLE 2.1. 

TABLE 3.1. 

TABLE 3.2. 

TABLE 3.3. 

TABLE 3.4. 

TABLE 3.5. 

TABLE 3.6. 

TABLE 3.7. 

Value of landings in selected Gulf fisheries in 1996 ................................................ 4 

Meetings held for evaluation of ecological effects of hypoxia on 

Gulf of Mexico living resources. .............................................................................. 5 

Comparison of ecological and economic effects of anthropogenic 

hypoxic zones from coastal seas around the globe that are similar to 

the northern Gulf of Mexico hypoxic zone ........................................................... 13 

Comparison of benthic community structure for areas within the 

hypoxic zone experiencing different levels of hypoxia. .......................................... 15 

Long-term average benthic community structure statistics from the 

14-year LOOP (Louisiana Offshore Oil Port) study. Quarterly 

sampling started in November 1980 and ended in 1993. ...................................... 16 

Range of abundance recorded for Gulf of Mexico benthic communities ............. 17 

Lag 1 correlations between July-August log CPUE1 for brown 

shrimp and August-September log CPUE for white shrimp and 

two measures of hypoxia for three zones. .............................................................. 25 

Lag 0 correlations between July-August DEPTH for brown 

shrimp and August-September DEPTH for white shrimp and 

two measures of hypoxia for three zones. .............................................................. 28 

Correlations between July-August log NUMBER for brown 

shrimp and August-September log NUMBER for white shrimp and 

two measures of hypoxia for three zones. .............................................................. 31 
Acknowledgments 

We would like to acknowledge the assistance of many managers and scientists who have contributed insight and/or data on the ecological and economic effects of hypoxia, particularly the 

Task 2 Ecological Effects and Economic Effects Working Group members. 

Ecological Effects Working Group Members 

Denise Breitburg, Philadelphia Academy of Science 

Churchill Grimes, National Marine Fisheries Service, Southeast Fisheries Science Center 

Jim Hanifen, Louisiana Fish and Wildlife Department 

Don Harper, Texas A & M University 

Nancy Marcus, Florida State University 

Nancy Rabalais, Louisiana Universities Marine Consortium 

Gilbert Rowe, Texas A & M University 

Gene Turner, Louisiana State University 

Roger Zimmerman, National Marine Fisheries Service 

Economic Effects Working Group Members 

Otto Doering, Agricultural Economics Department, Purdue University 

Joseph Glauber, Economic Analysis Section, U.S. Department of Agriculture 

Walter Keithley, Coastal Fisheries Institute, Louisiana State University 

Jim Nance, National Marine Fisheries Service, Galveston 

Kenneth Roberts, Louisiana Cooperative Extension Service, Louisiana State University 

Roger Zimmerman, National Marine Fisheries Service 

Other Contributors 

Fred Bryan, U.S. Geological Survey 

Ed Chesney, Louisiana Universities Marine Consortium 

Randal Cutter, Virginia Institute of Marine Science 

John Downing, Iowa State University 

Drew Fillingame, Gulf of Mexico Program 

Rutger Rosenberg, Gothenberg University, Sweden 

Mark Schexnayder, Louisiana Fish and Wildlife Department 

vii 
Foreword 

Nutrient overenrichment from anthropogenic sources is one of the major stresses on coastal 

ecosystems. Generally, excess nutrients increase algal production and the availability of organic 

carbon within an ecosystem-a process known as eutrophication. Scientific investigations in the 

northern Gulf of Mexico have documented a large area of the Louisiana continental shelf with 

seasonally depleted oxygen levels (< 2 mg/l). Most aquatic species cannot survive at such low oxygen levels. The oxygen depletion, referred to as hypoxia, forms in the middle of the most important commercial and recreational fisheries in the conterminous United States and could threaten 

the economy of this region of the Gulf. 

As part of a process of considering options for responding to hypoxia, the U.S. Environmental 

Protection Agency (EPA) formed the Mississippi River/Gulf of Mexico Watershed Nutrient 

Task Force during the fall of 1997, and asked the White House Office of Science and Technology Policy to conduct a scientific assessment of the causes and consequences of Gulf hypoxia 

through its Committee on Environment and Natural Resources (CENR). A Hypoxia Working 

Group was assembled from federal agency representatives, and the group developed a plan to 

conduct the scientific assessment. 

The National Oceanic and Atmospheric Administration (NOAA) has led the CENR assessment, although oversight is spread among several federal agencies. The objectives are to provide 

scientific information that can be used to evaluate management strategies, and to identi5 gaps in 

our understanding of this complex problem. While the assessment focuses on hypoxia in the 

Gulf of Mexico, it also addresses the effects of changes in nutrient concentrations and loads and 

nutrient ratios on water quality conditions within the Mississippi-Atchafalaya River system. 

As a foundation for the assessment, six interrelated reports were developed by six teams with experts from within and outside of government. Each of the reports underwent extensive peer review by independent experts. To facilitate this comprehensive review, an editorial board was 

selected based on nominations from the task force and other organizations. Board members were 

Dr. Donald Boesch, University of Maryland; Dr. Jerry Hatfield, U.S. Department of Agriculture; Dr. George Hallberg, Cadmus Group; Dr. Fred Bryan, Louisiana State University; Dr. 

Sandra Batie, Michigan State University; and Dr. Rodney Foil, Mississippi State University. The 

six reports are entitled: 

Topic 1: Characterization of Hypoxia. Describes the seasonal, interannual, and long-term 

variations of hypoxia in the northern Gulf of Mexico and its relationship to nutrient loadings. Lead: Nancy N. Rabalais, Louisiana Universities Marine Consortium. 
x Ecological and Economic Consequences of Hypoxia 

Topic 2: Ecological and Economic Consequences of Hypoxia. Evaluates the ecological and 

economic consequences of nutrient loading, including impacts on the regional economy. Coleads: Robert J. Diaz, Virginia Institute ofMarine Science, and Andrew Solow, Woods Holc 

Oceanographic Institution, Center for Marine Policy. 

Topic 3: Flux and Sources of Nutrients in the Mississippi-Atchnfalaya River Basin. Identifies the sources of nutrients within the Mjssissipgi-Atchafalaya system and Gulf of Mexico. 

Lead: Donald A. Goolsby, LT S. Gcologicai Survey 

Topic 4: Efects of Reducing Nufrient 1,oads to Suface Waters Within the Mississippi River 

Basin and Gulfof Mexico. Estimates the effects of nutrient-source reductions on water quality. Co-leads: Patrick L. Brezonik, University of Minnesota, and VictorJ Bierman, Jr., LimnoTech, Inc. 

Topic 5: Reducing Nutrient Loads, Especially Nitrate-Nitrogen, to Su face Water, Ground 

Water, and the GulfofMexico. Identifies and evaluates methods for reducing nutrient loads. 

Lead: William J. Mitsch, Ohio State University. 

Topic 6: Evaluation of the Economic Costs and Benefits of Methods for Reducing Nutrient 

Loads to the Gulf of Mexico. Evaluates the social and economic costs and benefits of the 

methods identified in Topic 5 for reducing nutrient loads. Lead: Otto C. Doering, Purdue 

University. 

These six individual reports provide a foundation for the final integrated assessment, which the 

task force will use to evaluai alternative solutions and management strategies called for in Public 

Law 105-383. 

As a contribution to the Decision Analysis Series, this report provides a critical synthesis of the 

best available scientific information regarding the ecological and economic consequences of hypoxia in the Gulf of Mexico. As with all of its products, the Coastal Ocean Program is very interested in ascertaining the utility of the Decision Analysis Series, particularly with regard to its 

application to the management decision process. Therefore, we encourage you to write, fax, call, 

or e-mail us with your comments. Our address and telephone and fax numbers are on the inside 

front cover of this report. 

David Johnson, Director 

Coastal Ocean Program 

Donald Scavia, Chief Scientist 

National Ocean Service 
Executive Summary 

In this report we have attempted to evaluate the ecological and economic consequences of hypoxia in the northern Gulf of Mexico. Although our initial approach was to rely on published 

accounts, we quickly realized that the body of published literature deahng with hypoxia was limited, and we would have to conduct our own exploratory analysis of existing Gulf data, or rely on 

published accounts from other systems to infer possible or potential effects of hypoxia. 

For the economic analysis, we developed a conceptual model of how hypoxia-related impacts 

could affect fisheries. Our model included both supply and demand components. The supply 

model had two components: (1) a physical production function for fish or shrimp, and (2) the 

cost of fishing. If hypoxia causes the cost of a unit of fishing effort to change, then this will result in a shift in supply. The demand model considered how hypoxia might affect the quality of 

landed fish or shrimp. In particular, the market value per pound is lower for small shrimp than 

for large shrimp. 

Given the limitations of the ecological assessment, the shallow continental shelf area affected by 

hypoxia does show signs of hypoxia-related stress. While current ecological conditions are a response to a variety of stressors, the effects of hypoxia are most obvious in the benthos that experience mortality, elimination of larger long-lived species, and a shifting of productivity to nonhypoxic periods (energy pulsing). What is not known is whether hypoxia leads to higher productivity during productive periods, or simply to a reduction of productivity during oxygenstressed periods. 

The economic assessment based on fisheries data, however, failed to detect effects attributable to 

hypoxia. Overall, fisheries landings statistics for at least the last few decades have been relatively 

constant. The failure to identify clear hypoxic effects in the fisheries statistics does not necessarily 

mean that they are absent. There are several possibilities: (1) hypoxic effects are small relative to 

the overall variability in the data sets evaluated; (2) the data and the power of the analyses are not 

adequate; and (3) currently there are no hypoxic effects on fisheries. 

Lack of identified hypoxic effects in available fisheries data does not imply that effects would not 

occur should conditions worsen. Experience with other hypoxic zones around the globe shows 

that both ecological and fisheries effects become progressively more severe as hypoxia increases. 

Several large systems around the globe have suffered serious ecological and economic consequences from seasonal summertime hypoxia; most notable are the Kattegat and Black Sea. The 

consequences range from localized loss of catch and recruitment failure to complete system-wide 

loss of fishery species. If experiences in other systems are applicable to the Gulf of Mexico, then 

in the face of worsening hypoxic conditions, at some point fisheries and other species will decline, perhaps precipitously. 
xii Ecological and Economic Consequences of Hypoxia 

Catch per unit effort for brown shrimp, while variable, has trended down since the late 1970s. 

While fish and shrimp may avoid hypoxia, the effects of avoidance on metabolism and predator 

avoidance are unknown, including the time and space scales over which avoidance is possible. In 

fact, a major difference between the northern Gulf of Mexico hypoxic zone and other such 

zones around the world is that for the last few decades, the Gulf ecosystem has managed to 

maintain energy flow to productive fisheries (crabs and shrimps) that depend on the bottom. 

Any effect of hypoxia in the northern Gulf of Mexico is intertwined with other environmental 

stressors. To understand specifically how hypoxia affects populations in the Gulf, we first need to 

determine the contribution of all natural and anthropogenic sources of mortality and growth to 

population dynamics. We also need to determine what functional aspects of the ecosystem are 

specifically affected by hypoxia. A comprehensive research plan is needed as a focus for efforts 

directed at assessing both the ecological and the economic effects of hypoxia in the Gulf. This 

plan must include elements for both directing new research and synthesizing existing data. Our 

efforts to identify hypoxia-related problems were severely hampered by lack of published data. A 

total ecosystem approach to the problem will be the only successful approach. Consideration of 

how hypoxia and other stressors interact with all aspects of the Gulf ecosystem is essential for 

planning restoration efforts. 
CHAPTER 1 , 

Introduction 

1.1 SCOPE OF THIS REPORT 

An important goal of the CENR hypoxia science assessment was to document the state of 

knowledge of the extent, characteristics, causes, and effects (both ecological and economic) of 

hypoxia in the northern Gulf of Mexico. This report specifically deals with the ecological and 

economic effects of annual hypoxia, which is apparently procreated by excess nutrient loading 

delivered to the Gulf via the Mississippi River Basin. It also examines the impacts of hypoxia on 

Gulf of Mexico fisheries and the regional and national economies, and articulates both the ecological and the economic consequences and, to the extent appropriate, their interaction. 

Other reports in the assessment series compiled existing information on nutrient sources, identified alternatives for reducing nutrient inputs, and examined the costs and benefits associated 

with reducing the nutrient loads. The ecological and economic assessment was built from the 

work of many Gulf of Mexico researchers. 

1.2 LINKING LAND AND SEA 

The direct connection between land and sea is best exemplified by the relationship between estuarine and coastal fisheries production and land-derived nutrients. The most productive fisheries 

zones around the world are always associated with significant inputs of either land- (runoff) or 

deep oceanic- (upwelling) derived nutrients. The basic nutrients carried by land runoff and oceanic upwelling are essential elements that fuel primary production passed through marine food 

webs to species of economic importance. This basic scenario has been played out for eons around 

the world, including the northern Gulf of Mexico (Rabalais et al. 1996). The importance of the 

linkage between land and sea is clearly seen in the Gulf of Mexico, which in 1996 accounted for 

16% of the total commercial landings in the United States, with over half of this total harvested 

from waters surrounding the Mississippi River Delta (Holliday and O'Bannon 1997). 

Problems begin when the nutrients entering the system exceed the capacity of the food chain to 

assimilate them. At first, increased nutrients lead to increased fisheries production. But as production of organic matter production increases, changes occur in the food web that leads to different endpoints. These changes are very predictable and have followed the same path in many 

marine ecosystems (Figure 1.1). The relationship between nutrient loads delivered to the northern Gulf of Mexico and basic ecological responses (e.g., increased primary productivity in the 

water column, increased flux of organic matter to the bottom, bottom-water hypoxia, altered 

energy flow, and stressed fisheries) are typical of other systems' responses around the world (see 
2 Ecological and Economic Consequences of Mypoxia 

COMPARATXVE EVALUATION OF FISHERY ECOSYSTEMS 

RESPONSE TO INCREASING NUTRIENT LOADING 

1 

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NUTRIENT LOADING 

FIGURE I. I. Comparative evaluation of fishery response to nutrients based on data from 

around the world (modified and redrawn from Caddy 1993). NOTE: Each curve represents a 

general guild of species and their reaction to increasing nutrient supplies. The top part of the 

figure lists recent trends for various systems around the world. Vertical dashed lines separate 

general categories of organic production that result from different levels of nutrients. 
Chapter I: Introduction 3 

reviews by Brongersma-Sanders 1957; Caddy 1993; Diaz and Rosenberg 1995). Basically, the 

northern Gulf of Mexico hypoxic zone, popularly know as the "Dead Zone," is a secondary 

manifestation of the larger problem of excess nutrients, which leads to increased production of 

organic matter and, in the case of the Gulf of Mexico, hypoxia. (For, details, see the Topic 1 report, Characterization ofHypoxia.) The increased loading of organic matter is referred to as eutrophication (Nixon 1995). 

1.3 ASSESSING EFFECTS 

Many marine species in the northern Gulf of Mexico are targets of commercial and recreational 

fishing and, therefore, have dn-ect economic value. These species deserve special attention in an 

assessment of the ecological and economic consequences of hypoxia. Moreover, the information 

on which such an assessment could be based is generally more detailed for commercially exploited 

species. 

Despite considerable concern and speculation, to date there appears to have been no rigorous assessment of ecological or economic effects. Accordingly, the decision was made to focus on 

identifying economic effects in existing fisheries data for selected commercial stocks that could 

reasonably be attributed to hypoxia. For identifying ecological effects, the focus was on fisheriesindependent data and other environmental studies conducted primarily for oil and gas development. Although this focus is certainly narrow, it was necessitated by a combination of the requirement for some level of scientific rigor and limitations on project resources. 

The economic assessment was originally envisioned as consisting of two steps: identifying effects 

in the fisheries data that could be attributed to hypoxia, and attaching an economic value to 

those effects. There appears to be only one quantitative assessment of the effects of hypoxia on a 

commercial fishery in the Gulf of Mexico (Zimmerman et al. 1996). Briefly, the main findings 

of that study were that (1) there is a weak relationship between shrimp catch and a measure of 

the frequency of hypoxic conditions, and (2) catch per unit effort is unrelated to the frequency of 

hypoxia. 

In the absence of an existing body of analysis, the study described here involved what should be 

viewed as an exploratory or preliminary analysis of existing data to identify possible hypoxic effects. As described in more detail below, this analysis uncovered only weak evidence of such effects. In interpreting these results, it is important to emphasize three points: 

0 First, the failure to identify hypoxic effects does not necessarily mean that they are absent. 

Rather, it only suggests that their magnitude is small in relation to the overall variability 

in the data. In technical terms, given the data and sample size, the statistical power of 

this analysis may be low. There are many potential sources of variability in the fisheries 

data other than hypoxia. These include measurement errors and other problems with the 

data; variation due to weather and the compounding effects of coastal habitat modifications; and economic and other factors affecting fishing behavior, including variation 

through time and between localities in fisheries regulations. 

0 Second, in connection with the first point, the ability to account empirically for different 

sources of variability in the fisheries data is limited by information about these sources. 

Notably, consistent quantitative data on the severity of hypoxic conditions were limited 

to estimates of the area experiencing oxygen concentrations lower than 2 mg/l (AREA) 

over the period 1985-95, with little to no data for 1989 (see the Topic 1 report, Charac- 
4 Ecological and Economic Consequences of Hypoxia 

terization of Hypoxia). In light of the high variability of fisheries data, this time series is 

simply too short to establish a credible relationship between the severity of hypoxia and 

variables relating to fisheries. In an attempt to overcome this problem, the study group 

used a proxy for hypoxia to extend the analysis over a longer period. However, this proxy, 

described below, is certainly rough. 

Third, even if the failure to identify clear hypoxic effects in the historical data is taken as 

evidence of their absence, this does not imply that effects would not occur should conditions worsen. As noted elsewhere in this report, experience with other hypoxic areas 

shows that ecological effects and fisheries effects become progressively greater as hypoxia 

worsens (Caddy 1993). 

The analysis focused primarily on the two main shrimp species-brown shrimp (Penaeus axtecus) 

and white shrimp (Penaeus setiferus)-for three reasons: 

These species are commercially important (Table 1.1). 

As benthic (i.e., bottom-dwelling) species, the potential for experiencing effects due to 

hypoxia is relatively high. 

The data for these fisheries are relatively good, particularly in terms of geographical resolution. Additional analysis was performed for two other species-Gulf menhaden 

(Brevoortia patronus) and red snapper (Lutjanus campehanus)-to address public concerns that have been raised about the effects of hypoxia on them. 

TABLE I. I. Value of landings in selected Gulf 

fisheries in 1996. 

All $270.8 

Brown Shrimp $6 1.8 

White Shrimp $60.5 

Menhaden $47.4 

Red Snapper $4.2 

Source: National Marine Fisheries Service. 
2.1 ECOLOGICAL DATASOURCES 

Evaluation of ecological effects from the northern Gulf of Mexico hypoxic zone was based primarily on data collected by various investigators and federal programs and secondarily on meetings convened to assess hypoxia in the Gulf (Table 2.1). Most of the data appeared as agency 

reports or gray literature of limited circulation. In almost all cases these studies were commissioned for reasons other than evaluating the effects of hypoxia, usually for compiling fishery statistics or for information related to oil and gas activities. This particular aspect of the available 

data made it difficult to single out either ecological or economic effects associated with excess 

nutrient loading and hypoxia in the Gulf of Mexico. 

TABLE 2.1. Meetings held for evaluation of ecological effects of hypoxia on Gulf of Mexico - -. 

living resources. 

Conference MeetinglWorkshop Location Date(s) 

First Gulf of Mexico 

Hypoxia Management Conference 

Hypoxia Information 

Conference 

Hypoxia Around the 

World-Causes and 

Solutions 

Effects of Hypoxia on 

Living Resources in 

the Northern Gulf of 

Mexico 

Ecological and 

Economic Effects 

of Hypoxia on the 

Northern Gulf of 

Mexico 

Gulf of Mexico Kenner, LA December 5-6, 1995 

Program Meeting 

Joint Agricultural Davenport, IA June 1996 

and Gulf of Mexico 

Program Meeting 

OECD Workshop Anaheim, CA October 30-3 

Sea Grant Work- Baton Rouge, March 1 1-1 3, 

shop LA 

CENR Workshop Baton Rouge, March 14, 1998 

LA 
6 Ecological and Economic Consequences of Hypoxia 

Excess nutrient loading leading to eutrophication and subsequent hypoxia and anoxia are well 

studied phenomena in other places around the world (see Rosenberg 1985; Colombo et al. 1992; 

Nixon 1995; Howarth et al. 1996; Vitousek et al. 1997) and provide information pertinent to 

the northern Gulf of Mexico. In particular, much of the information dealing with estuarine and 

marine ecosystem-level effects of these phenomena on fisheries and benthos was recently summarized by Caddy (1993) and Diaz and Rosenberg (1995). 

The SEAMAP (Southeast Area Monitoring and Assessment Program) Environmental and 

Biological Atlas of the Gulf of Mexico database of the Gulf States Marine Fisheries Commission 

contains large amounts of data on trawlable species that are relevant to the current ecological and 

economic assessment. SEAMAP is a state, federal, and university program for collection, management, and dissemination of fisheries-independent data in the United States. The Gulf program data collection started in 1982, with many stations located in the hypoxic zone. Details on 

the sampling strategy used in collecting these data are contained in a series of summary atlases 

published each year (see Donaldson et al. 1997 as an example). The original data are available at 

the program's FTP site (ftp://conch.ssc.nmfs.gov/pub/seamap). Our ecological assessment was 

based on data from 1987 and 1988 (a time when hypoxia was less extensive) and from 1993 and 

1994 (a time when hypoxia was more extensive). 

2.2.1 A Conceptual Model for Economic Effects 

To focus the analysis on the central issue-namely, the economic impact on fisheries of hypoxia-it was necessary to adopt a conceptual model of how these impacts might arise. Without 

such a model, the appropriate data analysis would be unclear. The conceptual model adopted 

here is as follows. 

Potential economic effects of hypoxia arise through shifts in either the supply or the demand for 

fish. The supply model has two components. The first component is the physical production 

function for fish. A simple model of the production function is: 

CATCH = q EFFORT STOCK (1) 

where q is the catchability coefficient (e.g., Clark 1985). Under this model, catch per unit effort 

(CPUE) is proportional to stock size: 

CPUE = CATCH/EFFORT = q STOCK (2) 

As described below, the analysis of shrimp data was performed for three areas for which estimates of STOCK are not available, but for which estimates of CATCH and EFFORT-and, 

therefore, CPUE-are. Under the assumption that q does not depend on the level of hypoxia, 

an effect of hypoxia on stock can be detected by establishing an empirical relationship between 

CPUE and a hypoxia measure. 

It is important to emphasize that this approach to detecting a hypoxic effect on STOCK does 

not require that EFFORT be independent of hypoxia. This point is sometimes missed. For example, Zimmermann et al. (1996) found no empirical relationship between CPUE and a measure of the frequency of hypoxia in highly spatially resolved data. As shrimp are known to avoid 

hypoxic waters, they suggested that this reflected a combination of reduced STOCK and reduced EFFORT in areas of high hypoxia. However, under the model (I), this argument cannot 
Cha~ter 2: Methods 7 

be correct. Specifically, if a reduction in EFFORT leads to a proportional reduction in 

CATCH, so that CPUE remains constant, then under this model STOCK cannot have 

changed. The approach outlined above does assume that catchability g is independent of hypoxia. If a decline in STOCK due to hypoxia is, in fact, offset by an increase in g, then CPUE 

may remain unchanged, thereby obscuring the STOCK effect. There is anecdotal evidence that 

shrimp leaving the hypoxic zone congregate in high densities at the border of this zone. By increasing catchability, this may obscure an effect of hypoxia on STOCK. This possibility deserves 

further attention. 

The second component of the supply model is the cost of fishing. If hypoxia causes the cost of a 

unit of fishing effort to change, then this will result in a shift in supply. In particular, concern 

has been raised about the possibility that the hypoxia off the Louisiana coast has caused an offshore shift in the distribution of shrimp (and possibly other commercial species). Such a distributional shift could affect the cost of fishing by changing the distance that fishing vessels 

must travel. Detecting such a distributional shift requires relatively detailed information about 

the location of fishing activity. Some information along these lines is available for the shrimp 

fishery. As described below, an attempt was made to detect a distributional shift in that fishery 

that could be attributed to hypoxia. Incidentally, an increase in catchability q due to hypoxia 

could reduce the cost of fishing. 

Finally, hypoxia could cause the demand for fish to shift if it affects the quality of the landed 

fish. In particular, the market value per pound is lower for small shrimp than for large shrimp. 

As a result, if the size of landed shrimp declines as a result of hypoxia (e.g., through an effect on 

the growth of shrimp or on the location of shrimp harvest), then this would result in a loss in 

value, even if the total weight of landings remains unchanged. 

2.2.2 roxy for Hypoxias 

The analysis in this part of the study involved identifyrng empirical relationships between fisheries variables and a measure of hypoxia. One problem with basing the identification of such relationships on the time series of AREA (Figure 2.1) is that this time series is short. Moreover, the 

correlation between the time series of AREA with time itself is nearly 0.8, so that any other 

time series exhibiting a secular change over this relatively short period will be correlated with 

AREA. To overcome this problem, a proxy for hypoxia covering the period 1960-96 was constructed. 

Briefly, hypoxia results from the decay of phytoplankton and other kmds of organic material in 

the bottom waters by oxygen-using bacteria. The amount of phytoplankton in the Gulf depends 

in part on the amount of nutrients supplied to the Gulf by the Mississippi and Atchafalaya RIVers. The amount of nutrients, in turn, depends on the product of the nutrient concentration in 

these rivers and their discharge into the Gulf (see the Topic 3 report, Flux and Sources of Nutrients in the Mississippi-Atchafalaya River Basin). The hypoxia index (INDEX) for the period 

1960-96 is given by: 

where INDEX(t) is the hypoxia index in year t, d(t) is the combined Mississippi-Atchafalaya 

spring discharge, and the exponential term assumes a 2% growth rate of nutrient concentration 

over this period (Turner and Rabalais 1991). 
8 Ecological and Economic Consequences of Hypoxia 

The time series of INDEX (Figure 2.1) is in rough qualitative agreement with the time series of 

AREA (Figure 2.2) over the period 1985-95, with a correlation of 0.60. The correlation between INDEX and time is around 0.7, due mostly to the assumed exponential growth in nutrient concentration. As with AREA, there is a danger of detecting a spurious relationship with a 

variable that also exhibits a secular change over this period. However, in comparison to AREA, 

the danger is reduced somewhat by the length of the INDEX time series. 

In addition to the problem of secular variation, in interpreting analyses based on this index, it is 

important to stress that INDEX-and true hypoxic conditions-are expected to be related to 

climatic conditions, such as temperature and precipitation, and to primary production in the 

Gulf. These factors can, by themselves, affect coastal fisheries. For example, Griffin et al. (1976) 

developed a yield model for brown shrimp in which Mississippi Rtver discharge served as a proxy 

for environmental conditions in estuarine nursery grounds. As a result, the establishment of an 

empirical relationship between a fisheries variable and INDEX-or even between a fisheries 

variable and true hypoxic conditions, were they known-does not necessarily imply the existence 

of an effect due to hypoxia. Instead, the effect may be due to a climatic or other covariates of 

INDEX. As described below, an attempt was made to avoid this problem in the analysis of the 

shrimp data by using fisheries data from different parts of the northern Gulf. 

J! I I I I I I I 

1957 1962 1967 1972 1977 1982 1987 1992 1s 

Year 

FIGURE 2.1. Hypoxia index used in the economic analysis. 
Index 

FIGURE 2.2. Plot of measured hypoxic area vs. hypoxia index used in the economic analysis. 

2.3 MEETlNGS AND ORKSHOPS 

A series of meetings and workshops dealing specifically with hypoxia-related issues provided insight and data regarding recent changes to the global picture and the northern Gulf of Mexico. 

The participants in these meetings were very helpful, and many provided relevant insight into 

the ecological and economic effects of hypoxia (Table 2.1). 

As part of the CENR assessment, we formed two hypoxic effects working teams that specifically 

provided insight and data on the Gulf of Mexico ecological and economic dynamics. We met 

and communicated with our teams through the process of developing this assessment. All members are listed in the Acknowledgments section in the beginning of this report. 
CHAPTER 3 

esults 

3.1 BACKGROUND OF HYPOXIAAS AGLOBAL 

ENVIRONMENTAL PROBLEM 

3.1.1 Nutrients, Eutrophication, and Hypoxia 

Excess nutrient loading leads to eutrophication of coastal seas, a widespread problem around the 

globe in general (Nixon 1980, 1995; Howarth et al. 1996). The primary factor driving this marine coastal eutrophication is an imbalance in the nitrogen cycle that can be directly linked to 

increased population whether through urbanization in coastal river drainages or expanded agricultural activities. In many areas hypoxia follows from eutrophication, which results from the 

underlying nutrient problem. An examination of the distribution of hypoxic zones around the 

world showed that they were closely associated with developed watersheds or coastal population 

centers that deliver large quantities of nutrients to coastal seas, with nitrogen being the most important nutrient. (See the Topic 1 report, Characterization ofHypoxia, and the Topic 3 report, 

Flux and Sources of Nutrients in the Mississippi-Atchafalaya River Basin.) Although agriculture 

and, to a much lesser degree, industry are regarded as the key causes, population growth and rising living standards are in fact driving the need for industry and agriculture to produce. 

The scenario linking nutrient additions to the formation of hypoxia and impacts to fisheries via 

eutrophication can be summarized as follows. Excess nutrients lead to increased primary production, which is new organic matter added to the ecosystem. Because shallow estuarine and coastal 

systems tend to be tightly coupled (benthic-pelagic coupling), much of this organic matter 

reaches the bottom. This increased primary productivity may also lead to increased fisheries production (Caddy 1993). At some point, however, the ecosystem's ability to process organic matter 

in a balanced manner is exceeded, and if physical dynamics permit stratification, water quality is 

degraded and hypoxic conditions develop. Initially, the increased fisheries production may offset 

any detrimental effects of hypoxia. But as eutrophication increases and hypoxia expands in duration and area, the fisheries production base is.affected and declines. This graded reaction to the 

combined problems of excess nutrients and hypoxia has been documented for many systems 

around the globe. 

The linkage of the Mississippi River and northern Gulf of Mexico continental shelf has led to a 

highly productive system that yields significant landings of fish and shellfish to the region. Annual landings have exceeded 1 billion pounds since 1969 (U.S. Department of Commerce Fishery Statistics; see Holliday and O'Bannon 1997 as an example). In the Caddy (1993) model that 

relates fishery yield to nutrients supplied, the northern Gulf of Mexico is currently somewhere in 
Chapter 3: Results I I 

the eutrophic category (Figure 1.1). To a point, nutrient enrichment may increase fishery yields; 

but beyond a certain level, it is negative in effect (Caddy 1993). 

3.1.2 Oxygen Budgets Around the Globe 

The dissolved oxygen conditions of many major coastal ecosystems around the world have been 

adversely affected through the process of eutrophication. Most of these coastal systems recorded a 

steady (monotonic) decline in dissolved oxygen through time, in most cases starting from initial 

oxygen measurements, usually in the 1950s (Rosenberg 1990). For systems that have historical 

data from the turn of the century, the declines in oxygen levels started in the 1950s and 1960s. 

However, for the Baltic Sea, declining dissolved oxygen levels were noted as early as the 1930s 

(Fonselius 1969). 

From a historical perspective it is clear that many of the systems that are currently hypoxic were 

not when they were first studied. The best examples of systems with long-term data come from 

Europe, where it can be seen that benthic hypoxia was not reported prior to the 1950s in the 

Baltic Sea (Fonselius 1969), 1960s in the northern Adriatic (Justid 1987), 1970s in the Kategatt 

(Baden et al. 1990), and 1980s on the Northwest continental shelf of the Black Sea (Mee 1992). 

Except in areas of natural upwelling, coastal hypoxia is not a natural condition. 

By the 1970s ecosystems around the world were becoming saturated with organic matter, and 

many of them manifested hypoxia for the first time. Once it had occurred, hypoxia quickly became an annual event and a prominent feature that controlled ecosystem energy flow (Diaz and 

Rosenberg 1995). From the 1980s to the present, the distribution of hypoxia around the world 

has not appreciably changed. Only in systems that have experienced intensive regulation of nutrient inputs have oxygen conditions improved. There are many examples of small-scale hypoxia 

reversals associated with improvements in treatment of sewage and pulp mill effluents 

(Rosenberg 1972,1976). 

In the United States, the improved water quality in Lake Erie is the best example and evidence 

that large ecosystems do respond positively to nutrient regulation, but that the time interval for 

achieving noticeable improvements many be long (Boyce et al. 1987; Charlton et al. 1993). The 

extent of hypoxia in Lake Erie was similar between 1970 and 1990, despite the reduced nutrient 

loads. The delayed improvement in oxygen conditions may be consistent with mechanisms and 

processes that contribute to the ecosystem's resilience (Charlton et al. 1993). Improvements in 

oxygen may not be noticed for decades and could be complicated by climatic changes (DiToro 

and Blumberg 1990). The Lake Erie example points to the need to have knowledge of a system's 

response to the complex problems associated with eutrophication before conclusions can be 

drawn as to the effectiveness of management actions. 

3.1.3 System Potential for Hypoxia 

Because of their geomorphology and circulation patterns, some marine systems have a greater 

tendency for hypoxic conditions to develop. The basic features of a system that make it prone to 

hypoxia are low physical energy (tidal, currents, or wind) and large freshwater input. These features combine to form stratified or stable water masses near the bottom that become hypoxic 

when they are isolated from reoxygenation with surface waters. The first investigations of bottom water quality in Chesapeake Bay in the 1930s reported hypoxia in deep channel areas of the 

mainstem (Newcombe and Horne 1938). In Mobile Bay there are accounts of "Jubilees"-likely 

hypoxia-related then as they are now (Schroeder and Wiseman 1988)-from the 1860s (J. Pen- 
I2 Ecological and Economic Consequences of Hypoxia 

nock, personal communication). Better mixed or flushed systems do not have a tendency toward 

hypoxia. The Baltic Sea and the Kattegat showed no historical tendency toward hypoxia 

(Pearson et al. 1985; Elmgren 1989). It was not until the 1950s and 1970s, respectively, that 

oxygen was found to be a problem, even though there were oxygen readings in both systems that 

go back to the turn of the century (Rosenberg unpublished data). Similarly, the northern Adriatic, with oxygen data from the 1910s, did not exhibit hypoxia until the 1960s (Justit 1987). 

A historical picture of oxygen conditions for the northern Gulf of Mexico, derived from reading 

the geochronology of sediment cores, indicates that hypoxia was most likely not a prominent 

feature of the shallow continental shelf prior to the 1950s (Rabalais et al. 1996 and Sen Gupta et 

al. 1996 in the Topic 1 report, Characterization of Hypoxia). A longer (2,000-year) geochronology done in Chesapeake Bay pointed to early European settlement of the Bay's watershed as a 

key feature that led to changes in most paleoenvironmental indicators and set the stage for current oxygen problems as much as 300 years ago (Cooper and Brush 1991). 

3.1.4 Type of Hypoxia, Severity, and System Response 

Annual summertime hypoxia was the most common form of low dissolved oxygen event recorded around the globe (30 of 47 known anthropogenic hypoxic zones, Diaz and Rosenberg 

1995). So in this respect, the northern Gulf of Mexico is not unique. Interestingly, the degree of 

obvious ecological and economic effects related to the hypoxia varies from system to system. The 

most serious ecological and economic effects of the combined problems of eutrophication and 

hypoxia are seen in the Black Sea and Baltic Sea, where demersal trawl fisheries have been either 

eliminated or severely stressed (Mee 1992; Elmgren 1984). A comparison of effects from three 

similar coastal hypoxic zones with the Gulf indicates that, at least for now, significant declines in 

fishery production attributable to hypoxia have not been documented for the Gulf of Mexico 

(Table 3.1). 

In the Kattegat, the sea between Denmark and Sweden, indications of troubled waters were 

seen by the mid-1970s (increased frequency of algal blooms), with seasonal summertime hypoxia 

observed since the early 1980s. Initially, hypoxia caused mass mortality of commercial and noncommercial species. Now large-scale migrations and/or mortality among demersal fish and the 

Norway lobster (Nephrops) continue, resulting in a changed species composition and reduced 

growth and biomass. Hypoxia in this area is believed to be partly responsible for the overall decline in the stock size, recruitment, and landings of commercial fish over the last two decades 

(Baden et al. 1990, Pihl unpublished data). However, hypoxia is not the only stress factor. Other 

factors implicated in declining stocks or populations are eutrophication (Caddy 1993), bycatch 

(Andrew and Pepperell 1992; Chesney et al. in press), trawl disturbance (Currie and Parry 1996), 

fishing pressure (Turkstra et al. 1991), habitat loss (Chesney et al. in press), and harmful algal 

blooms (Karup et al. 1993). Given the complexity and potential synergism of stressors, the effects 

of hypoxia are more clearly expressed in other coastal systems around the world than the northern Gulf of Mexico. Like the Gulf of Mexico, many systems around the world have gradually 

become eutrophic and hypoxic, but other systems have reached a point were fisheries are clearly 

negatively affected. 

If hypoxia in the Gulf gradually increased in size and duration from its inception-most likely in 

the 1950s (Sen Gupta et al. 1996)-then the ecosystem's response may also have been gradual 

and to date not catastrophic. In this scenario the northern Gulf of Mexico ecosystem, while 

certainly affected by hypoxia and other stressors, has for the last few decades maintained fishery 

production at a level that we have not been able to distinguish from that experienced previously 
Chapter 3: Results 13 

(Chesney et al. in press). Any scenario that had hypoxia appearing suddenly would have precipitated an ecosystem response similar to the 1976 hypoxic event off the coast of New York/New 

Jersey, which caused mass mortality of many commercial and noncommercial species (Azarovitz 

et al. 1979; Boesch and Rabalais 1991). While mass mortality events have been reported in the 

northern Gulf of Mexico (McEachron et al. 1994), current ecological conditions and lack of any 

recorded hypoxia-related mass mortality of fishery species, other than "Jubilees," tend to support 

the scenario of hypoxia developing gradually through time. 

TABLE 3.1. Comparison of ecological and economic effects of anthropogenic hypoxic zones 

from coastal seas around the globe that are similar to the northern Gulf of Mexico hypoxic 

zone. 

Louisiana Shelf 

Kattegat, 

SwedenDenmark 

Black Sea 

Northwest 

Shelf 

Baltic Sea 

15,000 Mortality Annual Stressed, but still highly 

productive. No reports 

of mortality, except 

"Jubilees." 

2,000 Mass Mortality Slow Collapse of Norway 

lobster, reduction of 

demersal fish. Hypoxia 

prevents recruitment of 

lobsters. 

20,000 Mass Mortality Annual Loss of demersal fisheries; shift to planktonic 

species. 

100,000 Eliminated None Loss of demersal fisheries; shift to planktonic 

species. Hypoxia is bottleneck for cod recruitment 

NOTE: Data are from various sources cited in text 

3.2 NORTHERN GULF OF MEXICOECOLOGICAL ANALYSIS OF HYPOXIA 

From an ecological standpoint, hypoxia in the northern Gulf of Mexico has become one of the 

many factors that at present control or influence the population dynamics of the regions of 

many pelagic and benthic species (Chesney et al. in press). Hypoxia exerts its control at two levels: 

First, and most obvious, is the loss of bottom and near-bottom habitat through the seasonal depletion of oxygen levels. From all indications, few if any, mobile organisms stay 

on bottoms that are hypoxic (Pavela et al. 1983; Leming and Stuntz 1984). This forced 

movement could increase population losses due to predation of species dependent on the 
14 Ecological and Economic Consequences of Hypoxia 

seabed for their survival. But when hypoxia dissipates, mobile organisms return 

(SEAMAP database). 

Second, and not so obvious, is the alteration of energy flows. During hypoxia, significant 

amounts of the system's energy are shunted to microbial decomposition (Rosenberg and 

Diaz 1993; Grant et al. 1995), the primary biological process that creates and maintains 

the hypoxia. In the northern Gulf of Mexico the major sources of this energy seem to be 

organic matter produced in the surface waters and benthic biomass (mostly small worms, 

snails, and clams) (Harper et al. 1991; Rabalais et al. 1993, 1995). Energy flows between 

trophic levels (mediated largely by predatodprey interactions) are also altered. In Chesapeake Bay, demersal fish and blue crab abruptly stopped feeding when dissolved oxygen 

declined below approximately 2.1 mg/l (Nestlerode and Diaz 1998). But they quickly returned to affected areas when hypoxia dissipated, and resumed feeding activity before 

stressed infauna were able to return to normal living positions in the sediment (Pihl et al. 

1992). Breitburg et al. (1997) also found hypoxia altered predator-prey interactions to affect the survival of larval fish. 

Considering all the potential sources of stress to the Gulf ecosystem, the most likely contemporary ecological impacts of hypoxia involve altered energy flows and community structure. Annual 

hypoxia affects energy flows in three primary ways, which unfortunately are not exclusive responses to hypoxia: (1) pelagic species not dependent on direct contact with the bottom take on 

a more prominent role; (2) energy is diverted from invertebrates to microbes (Pearson and 

Rosenberg 1992); and (3) the pulsing of energy flow through the ecosystem favors opportunistic 

species with shorter life cycles, which can take advantage of the shortened time bottom habitats 

are available. A reduction in the overall biodiversity of the ecosystem is also associated with energy-pulsed systems, since longer-lived species tend to be eliminated (Odum 1981). The first 

point, enhancement of pelagic species, is a basic ecosystem response to eutrophication and not 

hypoxia; the third point is a response to the hypoxia; and the second point is a response to both. 

3.2.1 Zooplankton and Hypoxia 

Zooplankton are an important trophic link between primary production and fisheries species, 

particularly for larvae, and also contribute to the flux of organic matter to the bottom through 

the sinking of fecal pellets. Unfortunately, the effects of hypoxia on zooplankton are not very 

well understood. In addition to mortality, which reduces their population numbers, the documented responses of zooplankton to hypoxia are avoidance for adults, interference with vertical 

migration, and changes in the composition of smaller species that carry their eggs (Powers 1997; 

Zaitsev 1992; Qureshi 1995; Stalder and Marcus 1997). Copepods, the dominant zooplankton 

in the northern Gulf of Mexico, were lower in abundance or absence when dissolved oxygen was 

(1 mg/l (Qureshi 1995). A similar reaction to hypoxia has been documented in Chesapeake Bay 

(Roman et al. 1993). While scant data indicate that there may be some avoidance of hypoxia and 

interference with vertical migration (Powers 1997; Qureshi 1995)) the overall abundance and 

community composition of zooplankton populations appear to be similar to other coastal areas. 

3.2.2 Benthic Communities and Hypoxia 

The response of northern Gulf of Mexico benthic communities to hypoxia-primarily noncommercial species, which form the base of the food web for shrimp and most demersal fishhas been similar to that of communities from other systems around the globe. In all cases of 

summertime hypoxia, varying degrees of benthic community mortality were reported, with 
Chapter 3: Results 15 

recolonization of the bottom after hypoxia dissipated. (For Gulf studies, see Gaston 1985; Murrell and Fleeger 1989; Harper et al. 1991; Rabalais et al. 1991, 1993, 1995; Gaston et al. 1998; 

Vittor &Assoc. 1998. For global studies, see Diaz and Rosenberg 1995.) 

There are no historical benthic data sets that can be used for a comparison of pre- and posthypoxic conditions. The earliest data come from a series of surveys from 1951 to 1957 of the 

Louisiana-Texas continental shelf by Parker (1960)) which mostly described the large fauna 

(molluscs, echinoderms, crustaceans) associated with shelf regions. Most of the species that 

Parker (1956, 1960) listed as common were collected by various recent studies (summarized in 

appendix C of Gaston et al. 1998)) but because of gear differences and area sampled, direct quantitative comparison was not possible. The small opportunistic bivalve Mdinia lateralis stands out 

as having been recorded as a dominant component of the fauna in shallow muddy areas in the 

1950s and in the 1980s-90s. 

Recent data on benthos in the northern Gulf of Mexico come mostly from areas on the eastern 

side of the hypoxic zone, but showed general signs of hypoxic stress that are most likely found 

throughout the hypoxic zone. Mortality of benthos was the prominent effect, with the degree of 

mortality directly related to the severity of hypoxia (Boesch and Rabalais 1991; Rabalais et al. 

1993, 1995). Giammona and Darnell (1990) studied the effects of brine discharge on benthos 

and found that the community around the brine difiser experienced less mortality due to the 

mixing effect of the diffuser, which did not allow the dissolved oxygen to decline as much relative to areas away from the diffuser. Areas that experience severe hypoxia, with near-anoxic conditions, experienced greater mortality and had fewer species and lower biomass than areas with 

intermittent or less severe hypoxia (Table 3.2). Even though mortality from hypoxia was widespread, no study of Gulf benthos has recorded azoic bottom. Recolonization of benthos, while 

variable from year to year, appeared to occur annually. 

TABLE 3.2. Comparison of benthic community structure for areas within the hypoxic zone 

experiencing different levels of hypoxia. 

Hypoxia Intermittent, Not Severe 

Spring 1990 8,600 2.6 22 

Fall 1990 1,400 0.4 12 

Spring 1991 2,900 0.9 16 

Hypoxia Prolonged and Severe 

Spring 1990 18,400 2.9 5 1 

Summer 1990 700 0.2 4 

Spring 1991 6,500 1.6 2 2 

Summer 1991 1,300 0.5 8 

Source: Rabalais et al. 1995. 

In 1980, the Louisiana Department of Wildlife and Fisheries started a long-term benthic 

monitoring program to investigate the possible effects of oil activities associated with the Louisiana Offshore Oil Port (LOOP). Two study areas located in the Gulf were subjected to hypoxia 

and provided insight into how benthos respond in the long term. While both study areas were 
16 Ecolonical and Economic Conseauences of Hv~oxia 

27 km apart, the shallower nearshore site experienced more frequent and more severe hypoxia 

than the deeper offshore site on the offshore edge of the hypoxia. Recruitment at the nearshore 

stations was pronounced and occurred mainly in the spring. Bivalves (mostly Mulinia lateralis) 

dominated the spring pre-hypoxia recruitment, with polychaetes (mostly Paraprionospio pinnata) dominating the summer and fall post-hypoxia recruitment. At the offshore stations recruitment was not pronounced and tended to occur in the summer (Table 3.3). While hypoxia 

was more severe at the nearshore area, it also had higher densities of organisms relative to the 

offshore area (Table 3.3). However, much of the difference between the nearshore and offshore 

areas could also be related to timing of recruitment or differences in predation pressure, depth, 

and/or sediment type. Considering this mix of physical and biological processes that are known 

to affect community structure, the lack of obvious long-term hypoxic effects on benthic community structure is not surprising. The LOOP study also did not find any benthic effects attributable to oil development activities (Ihtor & Assoc. 1998). Most of the dominant species 

reported are opportunists, which are tolerant of a wide range of environmental stressors, including hypoxia (Diaz and Rosenberg 1995), and adapted to rapidly recolonize disturbed areas 

(Boesch and Rosenberg 1981). 

TABLE 3.3. Long-term average benthic community structure statistics from the 14-year 

LOOP (Louisiana Offshore Oil Port) study. Quarterly sampling started in November 1980 

and ended in 1 993. 

Nearshore Brine Diffuser Stations2 

Winter 

Spring 

Summer 

Fall 

Offshore Pumping Station Complex3 

Winter 

Spring 

Summer 

Fall 

'Hypoxic seasons refers to the number of times hypoxia occurred during each of the seasons from 1980 to 1993. 

There was a maximum of 14 seasons for the nearshore area and 13 seasons for the offshore area. 

'The Nearshore Brine Diffuser area had four stations, whose averages were based on 53 quarterly collections. The 

stations were about 6 km from shore, on the inshore edge of the hypoxic zone, for 9 of 14 years, from 1980 to 

1993 ('8 1, '82, '86, '87, '80, '90, '9 1, '92, '93). Depth: 10 m; sediments: I &23% sand; interstitial salinity: 29-35 psu. 

3The Ofshore Pumping Station Complex area had three stations, whose averages were based on 50 quarterly collections. The stations were about 28 km from shore, on the seaward edge of the hypoxic zone, for 8 of 13 years, 

from 1980 to 1992 ('80, '83, '85, '87, '88, , '89, '90, '9 1, '92). Data for 1993 were not given. Depth: 2 7-34 m; sediments: 532% sand; interstitial salinity: 29-35 psu. 

Source: Vittor & Associates 1998. 
Chapter 3: Results 17 

Overall, the range of abundance reported for hypoxia-stressed bottoms is well within that reported throughout Louisiana's coastal waters (Table 3.4). Comparison of benthic communities 

between the area affected by hypoxia with those unaffected in nearby Mississippi Sound indicated that a functional shift has occurred, away from a better-developed, late successional stage, 

"equilibriumn-type community toward an early successional stage iiisturbance, adapted community (Pearson and Rosenberg 1978; Rhoads and Germano 1986). Few large, long-lived, deepburrowing species were present in the areas affected by hypoxia, where there are more small, 

short-lived species (Rabalais et al. 1993, 1995; Gaston et al. 1998; Vittor & Assoc. 1998). This 

influences the ability of the benthos to process sediments (D'Andrea et al. 1996) and store energy (Diaz and ~chiffner 1990). ow ever, there is evidence that shrimp feed heavily on these 

short-lived species (Harper et al. 1991) and may even benefit from the shift to a smaller-bodied, 

shallower-dwelling infauna (McTigue and Zimmerman 1998). This basic difference between 

the LA and MS shallow continental shelf is at least consistent with stress from hypoxia. 

TABLE 3.4. Range of abundance recorded for benthic communities around the Gulf of Mexico. 

South TX shelf <45 m 

Southwest FL shelf 

Mississippi-Alabama-Florida, 

Offshore 

Mississippi Sound, Offshore 

Mississippi Sound, Estuaries 

Offshore Disposal Sites, LA 

Central Louisiana, Offshore 

Chandeleur-Breton Sounds 

West Hackberry 

West Hackberry, Offshore 

LOOP, Nearshore 

LOOP, Offshore 

West Delta 

South Timbalier 

No 

No 

? ? ? 

No 

??? 

??? 

? ? ? 

No 

Yes 

Yes 

Yes 

Yes 

Yes 

Yes 

Flint I98 1 

Phillips et al. 1990 

Gaston et al. 1998 

Gaston et al. 1998 

Gaston et al. 1998 

Gaston et al. 1998 

Gaston et al. 1998 

Gaston et al. 1998 

Giammona & Darnel1 1990 

Gaston et al. 1998 

Vittor & Assoc. 1998 

Vittor & Assoc. 1998 

Rabalais et al. 1995 

Rabalais et al. 1993 
18 Ecological and Economic Consequences of Hypoxia 

The reduction in numbers of long-lived, deep-burrowing species has a direct negative effect on 

the linkage between benthic and pelagic communities within the system. Long-lived species 

tend to be larger than short-lived species and perform two important ecosystem hnctions. First, 

they can store large amounts of energy as biomass, buffering the ecosystem against the pulsing of 

energy (Odum 1981). Second, they burrow deep into the sediments and aid in the cycling of 

nutrients and other sediment-bound substances (Rhoads 1974). This "aeration" of sediment in 

turn helps to prevent the buildup of organic matter (Aller and Aller 1998). Without long-lived 

species, it is more difficult for the ecosystem to regulate and store the energy that comes to the 

bottom. Energy is then recycled over shorter time intervals because it is passed on to smaller 

short-lived species that undergo boom-and-bust cycles (very quickly building large populations 

that crash to near zero when energy is exhausted or other factors come into play, such as predation or hypoxia). Short-lived species are not good biomass revisions for energy and are of minimal help in oxygenating sediments. 

3.2.3 Benthic Secondary Production and Hypoxia 

As far as benthic communities are concerned, hypoxia takes the bottom out of production for a 

period of time-possibly as long as half a year for the northern Gulf of Mexico, depending on 

the duration of hypoxia. (See the Topic 1 report, Characterization ofHypoxia.) Mortality of affected communities is obvious, but the question that remains is: Is the overall secondary productivity of the system affected? 

The quality and quantity of secondary production are important, since benthic invertebrates are 

the major prey base for brown shrimp and other bottom-feeding fish and crabs. Unfortunately, 

there are no measurements from other systems that are directly comparable. In general, however, 

bottoms that are exposed to extensive periods of anoxia have low annual production (Rainer and 

Fitzhardinge 1981). The amount of productivity in these severely stressed habitats is a function 

of how quickly benthos can recruit and grow during periods of normal oxygen. 

In a near-anoxic basin-Port Hacking, Australia-productivity was almost 16 times lower than 

at a nearby station that only experienced hypoxia (Rainer and Fitzhardinge 1981). In Chesapeake Bay, areas that experience anoxia have about half the annual productivity of areas that are 

only hypoxic. While some areas affected by seasonal anoxia have lower productivity, the trend is 

inconsistent across habitat types. This results from a combination of duration of exposure to anoxia and rapid recovery of benthos. Annual secondary production of Chesapeake Bay habitats 

known to experience only seasonal hypoxia was of the same magnitude as habitats that always 

had normal oxygen levels, although the qualitative nature of the production differed (Diaz and 

Schaffner 1990; Neubauer 1993). 

3.2.4 Loss of Bottom Habitat: An Example of 

Hypoxic Effects on Shrimp 

Hypoxia clearly disrupts the movement and migration patterns of many species. Trawl data from 

the fishery-independent SEAMAP database (1987, 1988, 1993, 1994) showed a very consistent 

pattern that whenever dissolved oxygen declined and approached 3 and 1 mg/l, catch of shrimp 

and fish, respectively, rapidly declined to zero (Figures 3.1 and 3.2). 
Chapter 3: Results 19 

Bottom Dissolved Oxygen (rngn) 

FIGURE 3.1. Total number of finfish caught in summer @~ly-August) trawls by the SE. 

program for the years 1987-88 and 1993-94. NOTE: The shelf was divided into three areas: 

LA = off Louisiana; TX = west of Louisiana, Freeport to Galveston, TX; and ELA = east of 

Louisiana to Alabama. Data are from the SEAMAP database and have been standardized to 

numbers trawled per hour. 
20 Ecological and Economic Consequences of Hypoxia 

BottM DISSM Oxygen (rngll) 

FIGURE 3.2. Total number of penaeid shrimp caught in summer (July-August) trawls by the 

SEAMAP program for the years 1987-88 and 1993-94. NOTE: The shelf was divided into 

three areas: LA = off Louisiana; TX = west of Louisiana, Freeport to Galveston, TX; and ELA = 

east of Louisiana to Alabama. Data are from the SEAMAP database and have been standardized to numbers trawled per hour. 
Cha~ter 3: Results 2 1 

In laboratory experiments, both white and brown shrimp were able to detect and attempted to 

avoid hypoxic water (<2 mgA) (Renaud 1986). Because shrimp must move from inshore wetland 

nurseries to offshore feeding and spawning grounds, hypoxia poses a major problem to their migration. Gazey et al. (1982) found that juvenile brown shrimp leaving marsh nurseries moved 

farther offshore when hypoxia was not present-an indication that if hypoxia were not present 

shrimp could exploit more bottom area. Analyses of the distribution of shrimp catch and the localization of catch on the shelf in relation to hypoxia also suggest that hypoxia interferes with 

shrimp migration (Zimmerman et al. 1996), and where hypoxia was extensive, catch of shrimp 

was consistently low (Figure 3.3). 

The blocking effect of hypoxia on shrimp migration reveals that hypoxia impedes offshore 

movement, so nearshore abundance of shrimp may be higher. Shrimp are actually capable of 

moving far distances relative to their small size. Sheridan et al. (1987) reported brown shrimp 

were capable of moving 1.3-1.6 km/day. The maximum distance traveled was 620 krn in 320 

days. Hypoxic conditions can easily cause brown shrimp to redistribute hundreds of kilometers to 

more favorable conditions elsewhere, such as the Texas or Mississippi shelves. A similar blocking 

effect for bluefish was recorded for the 1976 New York/New Jersey hypoxic event. This event 

clearly demonstrated that coastal hypoxia cannot only displace demersal fish but can also block 

the migration of pelagic fish. Northward-migrating bluefish that encountered the hypoxic zone 

did not pass through or go around it, but stayed to the south, waiting for it to dissipate and then 

continued their migration north (Azarovitz et al. 1979). If it is important for fish and shrimp to 

reach critical nursery or feeding areas at certain times in their lives, then hypoxia may have an 

Percentage of Statistical Subarea Effected by Hypoxia 

FIGURE 3.3. Pounds of penaeid shrimp landed versus the relative annual occurrence of hypoxia in selected statistical subareas (see Figure 3.4). NOTE: Line is a least-squares regression 

fit to the data, indicating a significant negative relationship. Data are for the years 1985, 

1986, 1990, 199 1, 1992, 1993, and 1994. (From Zimmermanet a/. 1 996.) 
22 Ecological and Economic Consequences of Hypoxia 

indirect effect on populations by delaying arrival to spawning or feeding grounds. In such cases, 

the cost of delayed migration in terms of population mortality and production is unknown. 

The brown shrimp catch in the Gulf (mostly caught in Louisiana and Texas) declined from a 

record high in 1990 to below the historical average during 1992-97. This decline coincides with 

years of greatly increased hypoxia. By comparison, white shrimp catch within the same area and 

time period did not exhibit a similar decline. A greater negative effect on adult and large subadult 

brown shrimp would be expected from enlargement of the hypoxic zone because they require 

offshore shelf habitat, whereas white shrimp do not (they require nearshore habitat). Thus, the 

differences in life-cycle requirements are more likely to expose brown shrimp than white shrimp 

to the offshore effects of hypoxia. 

Also, there continues to be the pattern of low shrimp catch and shrimping effort in offshore 

Louisiana. Geographic comparison of distribution of shrimping effort in Texas and Louisiana 

shows lower shrimping effort in Louisiana to be coincident with shelf hypoxia. Moreover, although Louisiana's management strategy favors inshore fisheries, it does not preclude offshore 

shrimping and does not adequately explain the low catch patterns on the Louisiana offshore 

shelf, where subadult and adult brown shrimp are expected to occur. 

3.2.5 Fish Populations 

Unfortunately, there have been no studies of how hypoxia affects fish populations in the northern Gulf of Mexico. However, data collected by the SEAMAP program will be instrumental in 

determining any hypoxic effects. Preliminary analysis of this data set indicates that there may be 

a herding effect, with higher abundance of fish on the edge of the hypoxic zone (Crowder and 

Craig, personal communication). 

Some effects of hypoxia that have been seen in the Kattegat, Baltic Sea, and Chesapeake Bay are 

difficult to detect without directed studies, but could occur in the northern Gulf of Mexico. Pelagic eggs of economically and ecologically important species can sink into hypoxic bottom waters and die. For example, oxygen concentrations from 4 to 5 mg/l reduced the survival of cod 

eggs (Nissling and Vallin 1996). Eggs sinking into hypoxic water is thought to be an important 

factor that leads to the decline of cod in the Baltic Sea (Nissling et al. 1994) and may be an important source of mortality for Chesapeake Bay anchovy (Kiester et al. unpublished). Habitat restriction can also increase the predation mortahty of fish (Breitburg 1992; Breitburg et al. 1997) 

and can force fish into areas with poor growth potential (Coutant 1985). And hypoxia may increase the incidence of disease and parasitism in exposed fish populations. Mellergaard and Nielsen (1995) found the relative risk of contracting lyrnphocystis, a viral disease that affects many 

marine fish worldwide, significantly increased in the Kattegat from 1984 to 1986, compared to 

1987 to 1991, years of severe hypoxia. 

Also of concern to fisheries populations is the increased incidence of harmful algal blooms in 

coastal waters resulting from eutrophication (Goldberg 1995). Harmful algal blooms have long 

been linked to fish kills (Brongersma-Sanders 1957), but recent developments along the Atlantic East Coast indicate how serious they can be (Burkholder et al. 1992). There is also a strong 

relationship between bloom-related mortality and hypoxia. (See Burkholder et al. 1995 as a recent example. For more details on phytoplankton community changes, see the Topic 1 report, 

CJaracterixation of Hypoxia.) 
Chapter 3: Results 23 

3.3.1 Economic Analysis of Shrimp Data 

As noted, the analysis focused mainly on brown shrimp (Penaeus aztecus) and white shrimp 

(Penaues setiferus). The biology and fisheries characteristics of these species are described in detail 

in the Fishe y Management Plan for the Shrimp Fishe y of the Guy ofMexico, United States Waters (Gulf of Mexico Fishery Management Council 1981) and in subsequent amendments. The 

data used in this analysis were extracted from the extensive database of monthly statistics maintained by the National Marine Fisheries Service (NMFS) Laboratory in Galveston, Texas 

(Poffenberger 1991). 

Statistics are maintained for 21 statistical areas (Figure 3.4). The offshore waters of each area are 

divided into depth zones of 5-fathom increments out to 40 fathoms. In the analysis described 

here, the statistical areas were grouped into three zones: eastern Louisiana (ELA), covering 

zones 11 and 12; Louisiana (LA), covering zones 13 through 17; and Texas (TX) covering zones 

18 through 21. As the hypoxic zone in the northern Gulf lies within the zone designated as LA, 

the other two zones serve as a kind of control. It is important to have such a control to distinguish between effects due to hypoxia-which would be confined to LA-and effects due to climatic or other covariates-which could also appear in ELA, TX, or both. The decision to group 

the statistical areas in this way was based on an extensive analysis of the data for each of the 21 

statistical areas. In particular, there is considerable variability between statistical areas, and combining them in this way into zones reduces this considerably, while retaining the value of comparisons between zones. 

FIGURE 3.4. Boundaries for the 21 statistical subareas established for reporting of fisheries 

landing in the Gulf of Mexico. NOTE: Data used in the economic assessment came from 

subareas 1 1-1 2 (ELA), 13-1 7 (LA), and 19-2 1 (TX). 

The analysis involved the calculation of correlations between INDEX and selected fisheries variables for each of the three zones-ELA, LA, and TX. Correlations were based on annual values, 

although, as with INDEX, the annual values of the fisheries variables were calculated using data 

for selected months (e.g., brown shrimp CPUE (cost per unit effort) during July-August). As 
24 Ecological and Economic Consequences of Hypoxia 

the effect of hypoxia in a particular year may be felt on shrimp in the following year, for certain 

fisheries variables, both contemporaneous and lagged correlations were calculated, with the largest in magnitude reported below. In the latter case, INDEX lagged the fisheries variable by one 

year. For completeness, correlations between AREA and the fisheries variables are also presented. However, the time series of AREA was felt to be too short to serve as an adequate basis 

for empirical analysis, and the analytical effort was directed at the correlations with INDEX. 

It is well known that the presence of secular trend can produce spurious correlations or obscure 

genuine correlations between time series. To avoid this problem, estimated trends were removed 

from both the INDEX and the fisheries variables by subtracting seven-year moving averages. As 

noted, this analysis should be viewed as exploratory. The basic idea is that an effect could be attributed to hypoxia if it involved a correlation of reasonably large magnitude that occurred in LA, 

but not in ELA or TX. To supplement the ordinary correlations, the partial correlation between 

INDEX and each fisheries variable for LA, with the "effects" of the same fisheries variable in 

ELA and TX removed, was also calculated. This amounts to treating the time series for 

ELAand TX as proxies for the effects of climatic and other factors that do not involve hypoxia. 

This involves the strong assumption that the effects of these factors in LA are linearly related to 

their effects in ELA and TX. 

Although no formal assessment of statistical significance was attempted, as a rough guide, under 

the unrealistic assumption that each of the individual time series is serially independent, a correlation or partial correlation would have to be around 0.35 in magnitude to achieve significance at 

the 0.05 level. This critical value would have to be adjusted to account for serial dependence. The 

assessment of statistical significance would also be complicated by the consideration of so large a 

number of (not necessarily independent) correlations and by the decision to select (e.g., via the 

consideration of multiple lags) the largest magnitude correlations. 

3.3.1.1 CATCH PER UNIT EFFORT AND HYPOXIA 

In Figure 3.5, annual time series of combined July and August catch per unit effort (CPUE) for 

brown shrimp are shown for the three zones for the perFod 1960-$6. The July-August period 

covers the most intensive fishing period for this species. Figure 3.6 shows the same time series for 

white shrimp during the August-September period, which covers the most intensive fishing for 

this species. In Table 3.5, lag 1 correlations between AREA and log CPUE and between detrended INDEX and detrended log CPUE are reported for each species within each of the 

three zones. Also reported in Table 3.5 are the partial correlations between detrended INDEX 

and detrended log CPUE in LA, with the effects of detrended log CPUE in ELA and TX removed. The logarithmic transformation of CPUE reflects the natural assumption of a multiplicative, rather than additive, effect. 

The partial correlations (Table 3.5) are the best evidence of a hypoxic effect uncovered in this 

analysis. While both are rather modest in magnitude, each has the expected sign. However, in 

this regard, it is important to point out that these estimated partial correlations are not independent of each other and, therefore, cannot be taken as independent pieces of evidence of a hypoxic effect. To illustrate the potential for overinterpretation, the partial correlation between 

detrended INDEX and detrended log CPUE for brown shrimp in ELA with the effects of LA 

and TX removed is -0.30. This cannot be attributed to hypoxia, which is absent in ELA. 
Cha~ter 3: Results 25 

Brown shrimp 

0 I I 1 

57 67 77 87 Z 

Year 

FIGURE 3.5. July-August catch per unit effort (CPUE) for brown shrimp in three fisheries zones. 

TABLE 3.5. Lag I correlations between July-August log CPUE' for brown shrimp and AugustSeptember log CPUE for white shrimp and two measures of hypoxia for three zones. 

AREA E LA 0.18 0.48 

LA 0.14 -0.23 

TX -0.09 -0.30 

-- 

'CPUE = catch ber unit effort 

'In calculating the correla'kons with INDEX, all time series were detrended by 

subtracting a 7-year moving average. Also reported in parentheses for each 

species is the lag I partial correlation between INDEX and log CPUE in LA, with 

the effects of kg CPUE in eastern LA (€LA) and TX removed. 
26 Ecological and Economic Consequences of Hypoxia 

White shrim 

0 1 I I I 

57 67 77 87 f 

Year 

FIGURE 3.6. AugustSeptember catch per unit effort (CPUE) for white shrimp in three fisheries zones. 

3.3.1.2 DEPTH OF LANDINGS AND HYPOXIA 

To address the concern that hypoxia has caused an offshore shift in the distribution of shrimp, 

thereby increasing the cost of fishing, annual time series of the mean depth of landings 

(DEPTH) were constructed for brown and white shrimp for ELA, LA, and TX and were 

correlated with the hypoxia measures. It is worth noting that the assessment of the depth of 

landings is made separately from the assessment of landings themselves and is, in some ways, 

rougher. In each year, the value of DEPTH for each species was formed by a weighted sum of 

the mid-point depths for the eight offshore depth zones. In each year, the weight that each 

mid-point depth received in this sum is given by the proportion of total landings in that year 

that were made in the corresponding depth zone. The time series of DEPTH for brown shrimp 

and white shrimp are shown in Figures 3.7 and 3.8, respectively. 

A striking feature of Figure 3.7 is a relatively sharp reduction in DEPTH occurring in 1977 in 

both ELA and LA. According to information provided by the Louisiana Department of Wildlife and Fisheries, this shift appears to have been due to the closure of inshore waters, resulting in 

a shift in fishing effort to the shallowest offshore waters. As landings in inshore waters are not 

included in the calculation of DEPTH, this results in the apparent shift to lower values of 

DEPTH. This illustrates the importance of removing secular trends: Without it, this shift 

would almost certainly be attributed to hypoxia. 
Cha~ter 3:Results 27 

0 ', I 1 I 

57 67 77 87 

Year 

FIGURE 3.7. Average depth of July-August brown shrimp landings in three fisheries zones. 

The lag 0 correlations between AREA and DEPTH and between detrended INDEX and detrended DEPTH are reported in Table 3.6, along with the partial correlations between detrended INDEX and detrended DEPTH in LA. The correlations between detrended INDEX 

and detrended DEPTH are positive in all three zones for brown shrimp and negative for white 

shrimp. It is notable that for both species this correlation is smallest in LA. As a result, the partial correlations are both negative, suggesting that any hypoxic effect would be to shift harvest 

toward inshore waters. However, the magnitudes of these partial correlations are small, and it is 

difficult to attach any significance to them. 
28 Ecological and Economic Consequences of Hypoxia 

o! I I I 

57 67 77 87 $ 

Year 

FIGURE 3.8. Average depth of AugustSeptember white shrimp landings in three fisheries zones. 

TABLE 3.6. Lag 0 correlations between July-August DEPTH for 

brown shrimp and AugustSeptember DEPTH for white shrimp 

and two measures of h y poxia for three zones. 

AREA E LA 0.19 0.46 

Period: 1985-88, LA 0.12 0.79 

1990-96 TX 0.06 0.2 1 

INDEX ' E LA 0.40 -0.05 

Period: 1960-96 LA 0.12 -0.17 

(-0.08) (-0.16) 

TX 0.29 -0.09 I I 

'In calculating correlations with INDEX, all time series were detrended by subtracting a 7-year moving average. Also reported in parentheses is the lag 0 partial correlation between INDEX and DEPTH in M, with the effects of DEPTH in 

eastern M (EM) and TX removed. 
Chapter 3: Results 29 

3.3. I .3 SHRIMP SIZE AND HYPOXIA: SUMMARY 

To address the question as to whether hypoxia affects the size of landed shrimp, annual time series of the mean number of shrimp per landed pound (NUMBER), which is inversely related to 

size, were calculated for July and August landings of brown shrimp and August and September 

landings of white shrimp in ELA, LA, and TX. These time series are shown in Figures 3.9 and 

3.10. It is clear from these figures that there has been an overall tendency for NUMBER to increase for both species in all three zones. 

Brown shrimp 

Year 

FIGURE 3.9. Average July-August numbers of brown shrimp per landed pound in 

three fisheries zones. 
30 Ecolonical and Economic Consequences of Hypoxia 

White shrimp 

25 ! I 1 I 

57 67 77 87 E 

Year 

FIGURE 3.10. Average AugustSeptember numbers of white shrimp per landed 

pound in three fisheries zones. 

Correlations between AREA and log NUMBER and between detrended INDEX and detrended log NUMBER are given in Table 3.7. For this variable, lag 0 correlations were generally 

larger in magnitude for brown shrimp, while lag 1 correlations were generally larger in magnitude for white shrimp. The logarithmic transformation reflects the assumption of a multiplicative, rather than additive, effect on growth. Table 3.7 reflects a tendency in both species for the 

correlation to decline from east to west. The partial correlations between detrended INDEX 

and detrended log NUMBER for LA, which are also reported in Table 3.7, are small in magnitude and, as with DEPTH, cannot be taken as significant. 

3.3.1.4 SHRIMP AND HYPOXIA: SUMMARY 

As the analysis of the shrimp data constitutes the bulk of this part of the report, it is worth 

pausing to summarize the results. However, before doing so, it is also worth briefly restating the 

underlying logic of the approach. 
Chapter 3: Results 3 1 

TABLE 3.7. correlations between July-August log NUMBER for 

brown shrimp and August-September log NUMBER for white 

shrimp and two measures of hypoxia for three zones. 

AREA E LA 0.80 0.5 1 

Period: 1985-88, LA 0.62 0.35 

1990-96 TX 0.3 3 0.52 

INDEX ' E LA 0.35 0.2 1 

Period: 1960-96 LA 0.2 1 0.10 

(0.15) (0.10) 

TX 0.06 -0.14 

'In calculating correlations with INDEX, all time series were detrended by subtracting a 7-point moving average. Also reported in parentheses are partial correlations between INDEX and log NUMBER in LA, with the effects of log 

NUMBER in eastern LA (EM) and TX removed. 

The goal of the analysis was to relate variations in fisheries data to variations in hypoxia. A fundamental problem is that variation in hypoxic conditions is not the only source of variation in 

the fisheries data. As a result, it is possible that a hypoxic effect is obscured by variability due to 

these other sources. While it would be possible, in principle, to control for these other sources of 

variability, such an analysis would require additional resources. A second serious problem for an 

empirical analysis is that variation in hypoxic conditions is almost certainly correlated with variation in climatic and other factors that, by themselves, can affect shrimp populations. As a result, 

even with additional data, it may be extremely difficult to disentangle effects due to hypoxia from 

effects due to covarying factors. 

In an attempt to circumvent these problems, data from zones to the east (ELA) and west (TX) 

of the main hypoxic zone (LA) were also analyzed. The hope is that these data, which are free of 

a hypoxic effect, will reflect other sources of variation that are also present in LA. If this hope is 

well founded, then the time series for ELA and TX serve as a rough control. This notion is 

formalized in the use of partial correlations, which essentially treat the time series for ELA and 

TX as proxies for variability not due to hypoxia. 

In addition to the problem of multiple, covarying sources of variability, the quality of the data is 

also open to question. The hypoxia index is certainly far from perfect. There are also problems 

with the fisheries data. It should be borne in mind that these data were collected for reasons 

other than the detection of a hypoxic effect. 

Unfortunately, the results of this analysis are equivocal. Even in the absence of a formal assessment of significance, from a purely statistical point of view, it is difficult to claim that a significant relationship has been established between the index of hypoxia and the fisheries variables. 

However, there is a sufficient hint of such a relationship-at least for CPUE-that the possibility cannot be dismissed. Some suggestions for improving this analysis are given below. 
32 Ecolonical and Economic Conseauences of Hwoxia 

3.3.2 Economic Analysis of Menhaden Data 

Gulf menhaden (Brevoortiapatronus) is a pelagic species found in coastal waters throughout the 

northern Gulf. Adult menhaden feed primarily on phytoplankton. The biological characteristics 

of this species are described in Nelson and Ahrenholz (1986) and Vaughan et al. (1996). Menhaden are exploited in the northern Gulf through an extensive purse-seine fishery, which is described in detail in Christmas et al. (1988). 

During this project, a nonspecific concern was raised about the possible effects of hypoxia on the 

Gulf menhaden fishery. To address this concern, time series of spawning stock biomass (SSB) 

(Vaughan, personal communication) and CPUE (Vaughan et al. 1996) were analyzed. The 

time series for SSB, shown in Figure 3.11, covered the period 1964-89, and the time series for 

CPUE, shown in Figure 3.12, covered the period 1964-92. Correlations between detrended 

INDEX and detrended log CPUE and detrended SSB were calculated. As the period of overlap 

between AREA and these variables is so short, these correlations were not calculated. Both lag 0 

and lag 1 correlations were calculated. In no case was the correlation larger than 0.05 in magnitude, and there is clearly no significant relationship between these time series. 

It is interesting to note that, despite considerable interannual variability, CPUE for menhaden 

exhibited no obvious trend during a period in which SSB first increased and then decreased. In 

other words, CPUE was not proportional to SSB over this period. Vaughan et al. (1996) attributed this to a dynamic aggregation process in schooling species like menhaden (Clark and Mangel 1979), whereby catchability declines with increasing stock level. 

Menhaden 

I I I 

67 77 87 E 

Year 

FIGURE 3.1 I. Spawning stock biomass (SSB) of menhaden in the Gulf of Mexico. 
Chapter 3: Results 33 

Menhaden 

I I 

67 77 87 I 

Year 

FIGURE 3.12. Catch per unit effort (CPUE) of menhaden in the Gulf of Mexico. 

3.3.3 Economic Analysis of Red Snapper Data 

Red snapper (Lutjanus campehanus) is perhaps the premier food fish in the Gulf of Mexico. The 

biological and fisheries characteristics of this groundfish are described in Goodyear (1995). During the project, a nonspecific concern was raised about possible hypoxic effects on red snapper. 

This concern appeared to stem from a dramatic decline in the red snapper stock over the past 50 

years. It is important to point out that red snapper have been heavily exploited over that period 

and the conventional wisdom holds that this decline is due primarily to overfishing. Although it 

was not possible to undertake as detailed an analysis of data for red snapper as for shrimp and 

menhaden, the results described here tend to support this conventional wisdom. 

Bottom trawl surveys of groundfish have been conducted by NOAA's National Marine Fisheries 

Service (NMFS) during the fall in the northern Gulf since 1972 (Nichols 1989), and summer 

surveys have been conducted as part of the SEAMAP program since 1982. The individuals 

caught in these surveys are typically pre-recruit juveniles, so they should be viewed primarily as 

measuring recruitment in the following yea.. These data suggest an overall decline in recruitment during the mid-1980s, with a slight tendency for higher recruitment in the early 1990s. 

Unfortunately, stock assessment data for red snapper were not available to the project at the time 

of this writing. 

Estimates of commercial landings of red snapper from U.S. waters of the Gulf of Mexico are 

available for the period 1964-95 (Figure 44 of Goodyear 1995). Commercial landings were stable 

from 1964 to around 1976, after which they experienced an irregular decline, rebounding slightly 
34 Ecological and Economic Consequences of Hypoxia 

in the early 1990s. Gulf-wide estimates of combined commercial and recreational landings of red 

snapper over the period 1979-94 exhibit a similar trend (Figure 70 of Goodyear 1995). There is 

also a significant bycatch of juvenile red snapper by shrimp trawls (Nance and Scott-Denton 

1997). The rebound in landings after 1990 appears to be due to conservation actions, such as 

closures (Goodyear 1995). Effort data are only available over the last few years of the record, so it 

was not possible to perform a time-series analysis of CPUE for red snapper. 

The best evidence against a hypoxic effect on red snapper is the spatial distribution of landings 

(Figure 46 of Goodyear 1995). From 1975 to 1995, landings have been highest in ELA and LA 

and lower to the east and to the west. Although landings declined generally between 1975 and 

1990, the decline was most pronounced in Florida and, to a lesser extent, in Texas. Similarly, the 

rebound in landings since 1990 has been greatest in Louisiana and particularly in the waters 

most affected by hypoxia. 
CHAPTER 4 

Research Needs 

4.1 ESTABLISHING ACONCEPTUAL FRAMEWORK 

Empirical analysis of the kind attempted here is difficult. Direct, quantitative information about 

the severity and extent of hypoxia is lacking. For example, the shXmp data, which are certainly 

among the most amenable to analysis, are still far from perfect. The fisheries-and the shrimp 

stocks themselves-are subject to a number of factors other than hypoxia, including environmental factors that are almost certainly related to the hypoxia (e.g., climate, temperature). Although the analysis could be improved by the acquisition and use of more data, the problems are, 

to some extent, fundamental to a purely empirical approach. 

In many ways, a more promising approach would involve the use of biological and processoriented models-for example, Browder (1993) for a biomass model or the Topic 4 report 

(Efects of Reducing Nutrient Loads to Surface Wbters Within the Mississippi River Basin and the 

GulffMexico) for an oxygen budget model. Although the available models were not designed 

to assess the effects of hypoxia, it may be possible to use them for this purpose. For example, even 

a relatively simple model may be useful in assessing the effects of hypoxia on the seasonal loss of 

habitat in the hypoxic region. A more complex model that explicitly incorporates the behavior of 

shrimp may be useful for assessing the effects of hypoxia on migratory patterns. A model-based 

approach is almost certainly needed to assess the impact on fisheries of scenarios for future hypoxia. The reason is that certain scenarios may involve effects that have not yet occurred and, 

therefore, cannot be seen in historical data, however high the quality. Of course, the results of a 

model-based approach to assessing the impact of hypoxia on fisheries are only as good as the 

model itself and the data from which it is built. 

Finally, in addition to improving the estimation of the actual economic effects of hypoxia, it may 

be useful to estimate the economic value of potential effects. For example, it may be relatively 

straightforward to estimate the cost to society of a hypothetical reduction in shrimp stocks. This 

information could prove useful in formulating a public policy response to hypoxia, even without 

firm estimates of what a future reduction may be. 

4.2 DIRECTED RESEARCH 

The northern Gulf of Mexico is a large, open ecosystem whose populations are influenced by 

many interacting factors. This is clearly seen in both the ecological and the economic analyses, 

where data were not available to account for the many sources of variability that influence population dynamics and landings, respectively. To understand how any subset of factors-like nutrient enrichment and hypoxia-affect populations, a complete picture is needed of what role each 
36 Ecological and Economic Consequences of Hypoxia 

factor plays in regulating the three basic elements of population dynamics: mortality (all forms of 

loss), recruitment, and growth. 

In the case of fisheries populations and hypoxia, an understanding of the importance of each of 

the following factors is needed: 

* Natural sources of mortality, from larvae through adults. 

Losses of essential habitat (natural and anthropogenic), from larvae through adults. 

Commercial landings with catch location and measurement of effort. 

* Recreational landings with catch location and measurement of effort. 

e Bycatch. 

* Trawling effects. 

For the ecological processes and populations that support fisheries species, directed studies that 

examine the interactions between hypoxia and the following are needed: 

e Composition of primary producers' populations. 

* Population dynamics and secondary productivity. 

Direct and indirect effects on food webs. 

e Spatial interaction of organisms, particularly predator-prey interactions. 

Long-term climatic variation. 

Geochemical cycling. 

o Eutrophication. 

After the models are developed and evaluated, different lines of research should be prioritized to 

predict basic responses of the system components (from primary producers to fish) to stressors 

(eutrophication, hypoxia, salinity, etc.). 

In addition to the complexity of the interactions among physical, chemical, and biological processes that shape the northern Gulf of Mexico ecosystem, two key elements hindered this assessment of the effects of hypoxia: (1) lack of detail on the actual occurrence and distribution of 

hypoxia and (2) accessibility of data on various ecosystem components. To resolve these critical 

issues, a long-term monitoring program needs to be established that would measure dissolved 

oxygen at proper spatial and temporal scales, and a database management system needs to be developed to facilitate future synthesis of existing data on fishery and nonfishery species. 
CHAPTER 5 

Conc~usions and Recommen 

5.1 ECOLOGICAL EFFECTS 

To date, surprisingly few studies are directed at understanding the ecological effects of hypoxia in 

the northern Gulf of Mexico. It is likely, however, judging from documented responses of other 

systems to hypoxia, that the northern Gulf of Mexico has already undergone change prior to scientific investigation, and what we now see is a disturbed system. 

This is most obvious in the benthos that has responded to seasonal hypoxia with mortality and 

by becoming a pulsed system (in the sense of Odum 1981) by shifting productivity to nonhypoxic periods of the year. Gulf studies in the late 1970s indicate that the benthos was already responding to hypoxia and that population dynamics, while variable, pulsed from year to year. 

Unfortunately, these documented changes could also be due to the other sources of stress that 

disturb sediments, such as trawling. 

To date, there are no clear indications of hypoxic effects in fisheries or fish populations in the 

published literature or data evaluated. It is possible that eutrophication resulting from nutrient 

enrichment associated with the Mississippi River watershed has offset the negative effects of hypoxia, as has been documented in other systems (Caddy 1993), or that effects are small relative to 

other sources ofvariance in the data. Mobile species seem to avoid hypoxia; if any mortality occurs, it is dispersed and, other than "Jubilee" events, not reported. Hypoxia appears to develop in 

such a way that allows mobile species to escape it by their getting off the bottom or moving 

ahead of the encroaching hypoxia. Fish populations appear to aggregate or herd on the edge of 

the hypoxic zone (Crowder and Craig, personal communication). 

Lack of identified hypoxic effects in available fisheries and fish population data does not imply 

that effects would not occur should conditions worsen. Experience with other hypoxic zones 

around the globe shows that both ecological and fisheries effects become progressively more severe as hypoxia worsens. Several large systems around the globe have suffered serious ecological 

and economic consequences from seasonal summertime hypoxia-most notably, the Kattegat 

and Black Sea. The consequences range from localized loss of catch and recruitment failure to 

complete system-wide loss of fishery species. If experiences in other systems are applicable to the 

Gulf of Mexico, then in the face of worsening hypoxic conditions, at some point fisheries and 

other species will decline, perhaps precipitously. Catch per unit effort for brown shrimp, while 

variable, has trended down since the late 1970s (Figure 3.5). While shrimp and fish can avoid 

hypoxia, at what cost, for how long, and to what spatial extent are unknown. In fact, a major 

difference between the northern Gulf of Mexico hypoxic zone and other such zones around the 
38 Ecological and Economic Consequences of Hypoxia 

world is that, to date, the Gulf ecosystem for the last few decades has managed to maintain energy flow to productive fisheries (crabs and shrimps) that depend on the bottom. 

Any effect of hypoxia in the northern Gulf of Mexico is intertwined with other environmental 

stressors. To understand how hypoxia affects populations in the Gulf, we first need to determine 

the contribution of natural and anthropogenic sources of mortality and growth to population 

dynamics-for example, gas production (Wilson-Ormond et al. 1994)). We also need to understand what functional aspects of the ecosystem are specifically affected by hypoxia. The Caddy 

(1993) model of ecosystem response to eutrophication, which encompasses hypoxia, may give us 

insight into the Gulf of Mexico situation. With an increase in nutrient loading, there is an initial increase in fisheries production. As nutrient loading continues to increase, the system approaches a saturation point, and the extra energy coming in can no longer be processed by fishery 

species. As hypoxia develops, it becomes a predominant force in regulating energy flow (Diaz and 

Rosenberg 1995), with processes and pathways that are favored by hypoxic conditions 

(opportunistic species, microbial food web) taking larger portions of the ecosystem's energy. The 

question is, Where on this curve is the Gulf of Mexico? The lack of obvious detrimental ecological and economic effects does not preclude the possibility of future ecological and economic disaster. 

5.2 ECONOMIC EFFECTS 

The economic assessment based on fisheries data failed to detect effects attributable to hypoxia. 

Overall, fisheries landings statistics for at least the last few decades have been relatively constant 

(Chesney et al. in press). There are several possibilities: (1) hypoxic effects are small relative to the 

overall variability in the data sets evaluated; (2) the data are not adequate for making an assessment of hypoxic effects; and (3) currently, there are no hypoxic effects. 

In interpreting these results, it is important to emphasize three points. 

First, the failure to identify hypoxic effects does not necessarily mean that they are absent, 

only that the design for monitoring catch and effort failed to identify the reasons for 

variability in the data. There are many potential sources of variability in the fisheries data. 

These include: measurement error and other data problems; variation due to climate and 

weather, coastal development, and economic factors affecting fishers; and variation 

through time and between localities in fisheries practices and regulations. 

Second, in connection with the first point, the ability to account for different sources of 

variability in the fisheries data is limited by information about these sources. Most notably, direct information about the severity of hypoxic conditions was limited to estimates 

of the area experiencing oxygen concentrations of less than 2 mg/l (AREA) over the period 1985-95, with only partial data for 1989 (see the Topic 1 report, Characterization of 

Hypoxia). In light of the high variability of fisheries data, this time series may be too 

short to establish a relationship between the severity of hypoxia and variables relating to 

fisheries. To overcome this problem, a proxy for hypoxia was also used to extend the 

analysis over a longer period. 

Third, the failure to identify hypoxic effects in historical data does not imply that economic effects would not occur should conditions worsen. As noted elsewhere in this report, experience with other hypoxic areas shows that ecological effects and fisheries 

effects become progressively larger as hypoxia worsens (Caddy 1993) and can cause economic effects (Baden et al. 1990). 
Chapter 5: Conclusions and Recommendations 39 

5.3 ECOMMENDATIONS 

A comprehensive research plan is needed as a focus for efforts directed at assessing the ecological 

and economic effects of hypoxia in the northern Gulf of Mexico. This plan must include elements for both directing new research and synthesizing existing data. 

Our efforts to identify hypoxia-related problems were severely hampered by lack of published 

data. In the case of fish populations, a large database exists (SEAMAP); however, it has not 

been analyzed. Although we did find tantalizing bits and pieces of data pointing to differences ' 

and responses consistent with hypoxia-related effects, we could not isolate confounding factors 

that could also produce similar responses. 

A total ecosystem approach to the problem will be the only successful one. Consideration of how 

hypoxia and other stressors interact with all aspects of the Gulf ecosystem is essential prior to 

planning any restoration efforts. 
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OTHER TITLES IN THE DEClSlON ANALYSIS SERIES 

No. 1 

No. 2 

No. 3 

No. 4 

No. 5 

No. 6 

No. 7 

No. 8 

No. 9 

Able, Kenneth W., and Susan C Kaiser. 1994. Synthesis of Summer Flounder Habitat Parameters. 

Matthews, Geof&ey A, and Thomas J. Minello. 1994. Technology and Success in Restoration, 

Creation and Enhancement of Spartina Altern$ora Marshes in the United States. 2 vols. 

Collins, Elaine V., Maureen Woods, Isobel Sheifer, and Janice Beattie. 1994. Bibliography of 

Synthesis Documents on Selected Coastal Topics. 

Hinga, Kenneth R., Heeseon Jeon, and Noelle F. Lewis. 1995. Marine Eutrophication Review. 

Lipton, Douglas W., Katherine Wellman, Isobel C Sheifer, and Rodney F. Weiher. 1995. Economic Valuation of Natural Resources: A Handbook for Coastal Policymakers. 

Vestal, Barbara, Alison Reiser, et al. 1995. Methodologies and Mechanisms for Management of 

Cumulative Coastal Environmental Impacts. Part I-Synthesis with Annotated Bibliography, 

Part 11-Development and Application of a Cumulative Impacts Assessment Protocol. 

Murphy, Michael L 1995. Forestry Impacts on Freshwater Habitat of Anadromous Salmonids in 

the Pacific Northwest and Alaska-Requirements for Protection and Restoration. 

Wiarn F. Kier Associates. 1995. Watershed Restoration-A Guide for Citizen Involvement in 

California. 

Valigura, Richard A, WinstonT. Luke, Richard S. Artz, and Bruce B. Hicks. 1996. Atmospheric 

Nutrient Inputs to Coastal Areas-Reducing the Uncertainties. 

No. 10 Boesch, Donald F., et al. 1997. Harmful Algal Blooms in Coastal Waters: Options for Prevention, 

Control and Mitigation. 

No. 11 McMurray, Gregory R, and Robert J. Bailey, editors. 1998. Change in Pacific Northwest Coastal 

Ecosystems. 

No. 12 Fonseca, Mark S., W. Judson Kenworthy, and Gordon W. Thayer. 1998. Guidelines for the Conservation and Restoration of Seagrasses in the United States and Adjacent Waters. 

No. 13 Macklin, S. Allen, editor. 1998. Bering Sea FOCI (1991-1997)pFinal Report. 

No. 14 Wiseman, Wiam, editor. 1999. Nutrient Enhanced Coastal Ocean Productivity in the Northern 

Gulf of Mexico. 

No. IS Rabalais, N.N., RE. Turner, D. Justic QDortch, and W.J. Wiseman, Jr. 1999. Characterization of Hypoxia: Topic 1 Report for the Integrated Assessment on Hypoxia in the Gulf of Mexico. 

No. 16 Diaz, R.J., and A. Solow. 1999. Ecological and Economic Consequences of Hypoxia: Topic 2 Report 

for the Integrated Assessment on Hypoxia in the Gulf of Mexico. 

No. 17 Goolsby, D.A., W.A. Battaglin, G.B. Lawrence, RS. Artz, B.T. Aulenbach, R.P. Hooper, D.R. 

Keeney, and G.J. Stensland. 1999. Flux and Sources of Nutrients in the Mississippi-Atchafalaya 

River Basin: Topic 3 Report for the Integrated Assessment on Hypoxia in the Gulf of Mexico. 

No. 18 Brezonik, P.L., V.J. Bierman, Jr., R Alexander, J. Anderson, J. Barko, M. Dortch, L. Hatch, G.L. 

Hitchcock, D. Keeney, D. Mulla, V. Smith, C. Walker, T. Whitledge, and W.J. Wiseman, Jr. 1999. 

Effects of Reducing Nutrient Loads to Surface Waters within the Mississippi River Basin and the 

Gulf of Mexico: Topic 4 Report for the Integrated Assessment on Hypoxia in the Gulf of Mexico. 

No. 19 Mitsch, WJ., J.W. Day, Jr., J.W Gilliam, P.M. Groffman, D.L. Hey, G.W. Randall, and N. 

Wang. 1999. Reducing Nutrient Loads, Especially Nitrate-Nitrogen, to Surface Water, Ground 

Water, and the Gulf of Mexico: Topic 5 Report for the Integrated Assessment on Hypoxia in the 

Gulfof Mexico. 

No. 20 Doering, O.C., F. Diaz-Hermelo, C. Howard, R. Heimlich, F. Hitzhusen, R. Kazmierczak, J. 

Lee, L. Libby, W. Milon, T. Prato, and M. Ribaudo. 1999. Evaluation of the Economic Costs and 

Benefits of Methods for Reducing Nutrient Loads to the Gulf of Mexico: Topic 6 Report for the 

Integrated Assessment on Hypoxia in the Gulf of Mexico. 
U.S. Department of Commerce 

ministration 

Silver Spring, Maryland 209 10