Benthic Foraminifera in Two Stressed Environments of the Northern Gulf of Mexico

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2001 Benthic Foraminifera in Two Stressed Environments of the Northern Gulf of Mexico. Emil Platon Louisiana State University and Agricultural & Mechanical College

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. BENTHIC FORAMINIFERA IN TWO STRESSED ENVIRONMENTS OF THE NORTHERN GULF OF MEXICO

A Dissertation

submitted to the Graduate Faculty of Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy

The Department of Geology and Geophysics

by Emil Platon DIPLOMA, University of Bucharest, 1985 MS, Louisiana State University, 2000 May, 2001

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. UMI Number 3016570

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Bell & Howell Information and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGMENTS

I gratefully acknowledge my advisor, Banin K. Sen Gupta, who introduced me to

the ecology of Recent benthic Foraminifera and shared with me his priceless experience.

I am greatly indebted to him for always being there to answer my questions, give advice,

and encourage me. He provided financial support, sampling opportunities, samples, and

data. I would also like to thank him for proofreading this report, a major contribution to

the final form of my work.

Grateful thanks are also due to my other committee members, Nancy Rabalais,

Paul Aharon, Arnold Bouma, Eugene Turner, John Wrenn, and Abner Hammond, who

helped me with their advice, comments, and suggestions along the way. I am grateful to

Nancy Rabalais and Eugene Turner for providing sampling opportunities and data and for

always being there to help. I thank Paul Aharon who offered isotope data and guided me

through the work on foraminiferal isotope composition.

Thanks also go to Mathew Hackworth who offered some of his unpublished data

and Christopher Wheeler who performed isotope analysis. I thank Quay Dortch

(LUMCON) for sampling opportunities. Thanks also go to Gary Byelry and Xiaogang

Xie who allowed me to use the facilities in the Louisiana State University Department of

Geology and Geophysics Electron Microprobe Laboratory and provided assistance when

necessary. I would like to thank my friend Samuel Huisman for help and support

This project was supported by Minerals Management Service (MMS-LSU Coastal

Marine Institute) Grant No. 14-35-0001-3 and partially by Integrated Interpretation

Center of Conoco Inc., Houston, Texas.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS

ACKNOWLEDGMENTS...... ii

LIST OF TABLES...... vii

LIST OF FIGURES...... ix

LIST OF PLATES...... xiii

ABSTRACT...... xiv

CHAPTER 1 INTRODUCTION...... 1 BACKGROUND: THE GULF OF MEXICO...... 2 General Features ...... 2 The Mississippi Influence ...... 4 GULF OF MEXICO BENTHIC FORAMINIFERA...... 5 General Features of the Distribution ...... 5 Seasonal Hypoxia on the Continental Shelf...... 7 Hydrocarbon Seeps on the Continental Slope...... 10 RELEVANT STUDIES FROM OUTSIDE THE GULF OF MEXICO 12 Pollution ...... 12 Coastal Hypoxia ...... 14 Hydrocarbon Seeps ...... 15 THIS PROJECT...... 16

CHAPTER 2 BENTHIC FORAMINIFERAL COMMUNITIES IN OXYGEN-DEPLETED ENVIRONMENTS OF THE LOUISIANA CONTINENTAL SHELF...... 19 INTRODUCTION...... 20 FORAMINIFERAL RESPONSE TO LOW OXYGEN CONCENTRATIONS...... 20 Microaerophiles and Facultative Anaerobes in Controlled Experiments ...... 20 Microhabitat Considerations ...... 22 METHODS...... 23 HYPOXIA AND FORAMINIFERAL DISTRIBUTION PATTERNS ON THE LOUISIANA CONTINENTAL...... 25 Microhabitats of Common Species ...... 25 Historical Trends of Species Abundances ...... 32 The Ammonia-Elphidium Index ...... 36 CONCLUSIONS...... 38

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 3 TWENTIETH-CENTURY CHANGES IN THE BENTHIC FORAMINIFERAL COMMUNITY OF THE LOUISIANA CONTINENTAL SHELF...... 41 INTRODUCTION...... 42 METHODS...... 45 BACKGROUND: WORLDWIDE COASTAL AND OPEN SHELF HYPOXIA...... 47 SEDIMENTS AND BENTHIC FORAMINIFERA...... 53 SPECIES DIVERSITY...... 56 SPECIES DISTRIBUTION...... 59 Dominant Species ...... 59 Ammonia and Elphidium ...... 60 Minor Components ...... 61 Quinqueloculina...... 62 DISTRIBUTION OF AGGLUTINATED AND PORCELANEOUS GROUPS...... 64 COMMUNITY CHANGE...... 67 ADDITIONAL DATA...... 74 HISTORICAL RECORD OF FORAMINIFERA: IMPLICATIONS REGARDING HYPOXIA...... 83 Species Richness and Diversity ...... 83 Taxon Distribution ...... 85 Dominant Species ...... 85 Minor Components ...... 86 Porcelaneous and Agglutinated Taxa Density Distribution.. 86 Assemblage Structure and Its Changes ...... 90 Foraminiferal Indicators of Hypoxia ...... 93 Model of Foraminiferal Response to the Progressive Hypoxia in Northern Gulf of Mexico ...... 95 CONCLUSIONS...... 98 APPENDIX...... 101 Species Abundance Data for F35 and E60 Cores ...... 101 F35 - Raw Data...... 101 F35 - Relative Proportions ...... 105 E60 - Raw Data...... 110 E60 - Relative proportions ...... 114

CHAPTER 4 FORAMINIFERAL COLONIZATION OF HYDROCARBON-SEEP BACTERIAL MATS AND UNDERLYING SEDIMENT, GULF OF MEXICO SLOPE...... 118 INTRODUCTION...... 119 SAMPLE COLLECTION, ON-BOARD PROCESSING, AND LABORATORY TECHNIQUES...... 119 Foraminiferal Census ...... 121 Ultrastructure ...... 121 Stable Isotope Analysis ...... 122

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. BACKGROUND: ANOXIA IN BEGGIATOA MATS...... 123 FORAMINIFERAL ABUNDANCE AND SPECIES DISTRIBUTION.... 124 Sediment-Water Interface ...... 124 Subsurface Layers ...... 127 ULTRASTRUCTURE...... 128 STABLE ISOTOPE COMPOSITIONS...... 131 DISCUSSION AND CONCLUSIONS...... 135

CHAPTER 5 BENTHIC FORAMINIFERA OF HYDROCARBON SEEPS OF THE NORTHERN GULF OF MEXICO: MICROHABITATS AND HISTORICAL TRENDS...... 141 INTRODUCTION...... 142 MATERIAL AND METHODS...... 146 BENTHIC FORAMINIFERA AT COLD SEEPS...... 148 Earlier Work ...... 148 Present Data ...... 150 Remmarks: Adaptation to Vent Habitats ...... 153 Survival and Reproduction Under Sulfidic Conditions ...... 155 STRATIGRAPHIC DISTRIBUTION...... 156 Multivariate Analysis ...... 162 STABLE ISOTOPE RECORDS OF BENTHIC FORAMINIFERAL TESTS...... 167 Previous Work on Stable Isotope Composition of Cold Seep Benthic Foraminifera ...... 167 Isotope Compositions of Selected Foraminiferal Species ...... 168 Diagenetic and Biogenic Isotopic Signature ...... 177 DISCUSSION...... 179 Historical Record of Seep Foraminifera ...... 179 Carbon Isotope Record ...... 181 Significant Biological Trends ...... 183 CONCLUSIONS...... 185 APPENDIX...... 187 Species Abundance Data for JSL2900-PC2 Core ...... 187 JSL2900 - PC2 - Raw Data...... 187 JSL2900 - PC2 - Relative Proportions ...... 196 Species Abundance Data for EP9, EP10 and EP11 Locations 205

CHAPTER 6 BENTHIC FORAMINIFERA FROM LOW-OXYGEN SHELF AND SLOPE ENVIRONMENTS OF THE NORTHERN GULF OF MEXICO: TAXONOMIC SUMMARY...... 206 INTRODUCTION...... 207 SPECIES DOMINANCE...... 207 Continental Shelf (Hypoxia Study) ...... 207 Continental Slope (Hydrocarbon Seeps Study) ...... 208 TAXONOMY...... 209 Shelf Species ...... 210

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Slope Species ...... 213

CHAPTER 7 SUMMARY AND CONCLUSIONS ...... 264

REFERENCES...... 270

APPENDIX: LETTERS OF PERMISSION...... 288

VITA...... 290

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES

Table 2.1. Identified species ...... 25

Table 2.2. Absolute abundances of common living foraminiferal species in: October 1995 cores (F35, G40, D80) ...... 27

Table 3.1. Eigenvalues for E 60 data ...... 69

Table 3.2. Factor loadings for 12 foraminiferal taxa in E60 core ...... 70

Table 3.3. Factor scores for 12 samples in E60 core...... 71

Table 3.4. Eigenvalues for BL10 core data ...... 77

Table 3.5. Factor loadings for 18 foraminiferal species from BL 10 core ...... 77

Table 3.6. Factor scores for 49 samples in BL10 core ...... 78

Table 4.1. Dive and sample information...... 120

Table 4.2. Mean abundance variations of dominant Foraminifera ...... 122

Table 4.3. Identified species ...... 125

Table 4.4. Foraminiferal specimens collected from Beggiatoa mats and examined for ultrastucture ...... 129

Table 5.1. Sample information ...... 147

Table 5.2. Locations of cores whose analysis revealed the existence of living Foraminifera ...... 151

Table 5.3. Foraminiferal species identified in JSL2900-PC2 ...... 159

Table 5.4. Eigenvalues ...... 163

Table 5.5. PC A. Factor loadings for 21 variables obtained from the analysis of JSL2900-PC2 data...... 163

Table 5.6. PCA on data from JSL2900-PC2 ...... 164

Table 5.7. Stable isotope values (8l3C ) of planktonic and benthic Foraminifera.... 169

vii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 5.8. Stable isotope values (513C ) of planktonic and benthic Foraminifera from control samples in western Gulf of Mexico ...... 170

viii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES

Figure 1.1. Schematic figure showing the relationship between salt diapirs, faults and seepage ...... 10

Figure 1.2. Sample locations ...... 18

Figure 2.1. Hypoxia frequency of occurrence, 1985-1999 ...... 24

Figure 2.2. Distribution of living Foraminifera in October 1995 cores ...... 28

Figure 2.3. Distribution of living Foraminifera in July 1996 ...... 31

Figure 2.4. Variations in foraminiferal assemblage density ...... 34

Figure 2.5. Stratigraphic variations in the proportions of Bolivina lanceolata and Bolivina albatrossi in the foraminiferal assemblage of D80 in the past two decades ...... 35

Figure 2.6. Stratigraphic variations in the proportion of Elphidium gunteri in the foraminiferal assemblage of G40 from 1853 to 1995 ...... 35

Figure 2.7. Stratigraphic variations in the proportions of Buliminella morgani, Epistominella vitrea , Nonionella basiloba , and Elphidium gunteri/excavatum in the foraminiferal assemblage of F35 in the past four decades ...... 36

Figure 2.8. A-E index recorded in cores from different water depths ...... 37

Figure3.1. Corelocations ...... 45

Figure 3.2. Dead and live individuals during assemblage burial down to a depth o f 7 cm ...... 55

Figure 3.3. Species richness distribution through time ...... 57

Figure 3.4. Species diversity index (Shannon-Wiener) distribution through time... 58

Figure 3.5. Dominant species distribution through time ...... 59

Figure 3.6. Temporal distribution of Ammonia - Elphidium Index in core F35.... 60

Figure 3.7. Temporal distribution of the relative abundances of the species Bulimina marginata, Cancris sagra, Fursenkoina pontoni, Saccammina diflugiformis, and Uvigerina hispido-costata ...... 61

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 3.8. Temporal distribution of the relative abundances of the species Bulimina marginata and Bolivina lowmani ...... 62

Figure 3.9. Distribution change in relative abundance of Quinqueloculina, core E60 ...... 63

Figure 3.10. Distribution change in relative abundance of Quinqueloculina, core F35 ...... 63

Figure 3.11. Distribution of agglutinated Foraminifera in E60 ...... 64

Figure 3.12. Distribution change in relative abundance of porcelaneous species, core E60 ...... 65

Figure 3.13. Distribution change in relative abundance of agglutinated species, coreF35 ...... 66

Figure 3.14. Distribution change in relative abundance of porcelaneous species, core F35 ...... 66

Figure 3.15. Cluster analysis of E60 data ...... 67

Figure 3.16. Cluster analysis of F35 data ...... 68

Figure 3.17. Scree plot for the eigenvalues for E60 core data ...... 69

Figure 3.18. Factor loadings, E60 ...... 71

Figure 3.19. Factor loadings, E60 ...... 72

Figure 3.20. Plots of factor scores against time, E60 ...... 73

Figure 3.21. Distribution change in relative abundance of genus Quinqueloculina, core G27 ...... 74

Figure 3.22. Cluster analysis of BL10 core data ...... 75

Figure 3.23. Scree plot for the eigenvalues for the data from BL10 core ...... 76

Figure 3.24. Factor loadings, core E60 ...... 79

Figure 3.25. Plots of factor scores against time, core BL10 ...... 80

Figure 3.26. U.S. fertilizer application ...... 81

Figure 3.27. A-P index, cores BL10, E60, and F35 ...... 95

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 3.28.One-hundred year-foraminiferal change in northern Gulf of Mexico ...... 97

Figure 4.1. Dive sites, indicated by Johnson Sea-Link dive numbers ...... 120

Figure 4.2. Surface to subsurface variations in foraminiferal assemblage density (number of Rose-Bengal-stained individuals in 30 cc of sediment) 128

Figure 4.3. Transmission electron micrographs ...... 130

Figure 4.4. Carbon and oxygen isotope compositions of benthic Foraminifera from seeps ...... 132

Figure 5.1. Schematic figure showing the relationship between salt, sediments, faults, and vent-seep-related features ...... 142

Figure 5.2. Dive sites, indicated by Johnson Sea-Link dive numbers ...... 147

Figure 5.3. Downcore variations in foraminiferal assemblage density ...... 152

Figure 5.4. Species diversity distribution in JSL2900-PC2 ...... 157

Figure 5.5. JSL2900-PC2; Distribution of equitability and number of specimens per 1 gram of dry sediment ...... 158

Figure 5.6. Vertical distribution of selected fossil foraminiferal taxa in JSL2900-PC2...... 161

Figure 5.7. Scree plot of eigenvalues for Principal Component Analysis ...... 162

Figure 5.8. Plots of factor scores of factor 1 and factor 2 ...... 165

Figure 5.9. Plots of factor loadings for foraminiferal data in JSL2900-PC2 ...... 166

Figure 5.10. Plots of factor loadings for foraminiferal data in JSL2900-PC2 ...... 166

Figure 5.11.5l3C vertical distribution ...... 171

Figure 5.12. Vertical distribution of % total carbonate and fine fraction /large fraction ratio ...... 172

Figure 5.13. Globigerinoides ruber ...... 173

Figure 5.14. Authigenic carbonate growth on Bolivina ordinaria ...... 174

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.15. Bolivina albatrossi ...... 175

Figure 5.16. Globigerinoides ruber ...... 176

Figure 5.17. Polynomial regression fit to Globigerinoides SI3C data in JSL2900-PC2 and vertical distribution of Bolivina 8l3C from which carbon isotopic departures in Globigerinoids have been subtracted ...... 178

xii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF PLATES

Plate 2.1. Common benthic Foraminifera of the Louisiana Bight ...... 39

Plate 4.1. Scanning electron micrographs ...... 139

Plate 6.1. Saccamminidae, Rzehakinidae, Haplophragmodidae, Lituolidae, Textulariidae, and Hauerinidae ...... 217

Plate 6.2. Hauerinidae, Nodosariidae, and Vaginulinidae ...... 222

Plate 6.3. Nodosariidae, Glandulinidae, Vaginulinidae, Lagenidae, Polymorphinidae, Ellipsolagenidae, Epistominidae, and Bolivinidae ...... 229

Plate 6.4. Bolivinidae and Cassidulinidae ...... 239

Plate 6.5. Cassidulinidae, Stainforthiidae, Siphogenerinoididae, Buliminidae, and Uvigerininidae ...... 244

Plate 6.6. Uvigerininidae, Reussellidae, Fursenkoinidae, Bagginidae, Eponididae, Discorbidae, Rosalinidae, Siphoninidae, and Parrelloididae ...... 250

Plate 6.7. Parrelloididae, Pseudoparrellidae, Planulinidae, Nonionidae, and Gavelinellidae ...... 255

Plate 6.8. Osangulariidae, Gavelinellidae, Rotaliidae, and Elphidiidae ...... 260

xiii

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT

This is a study of Foraminifera from two stressed environments of the northern

Gulf of Mexico: one of coastal seasonal hypoxia, the other of hydrocarbon seeps in

bathyal depths - oxygen depletion being the common stressor. Many species of benthic

Foraminifera survive the extreme oxygen depletion of Louisiana shelf waters in spring

and summer. The dominant species are infaunal and have an adaptive tolerance to near

anoxia or anoxia. A census of foraminiferal species present in dated sediment core

samples reveals significant changes in the composition of the Louisiana-shelf benthic

foraminiferal community in the past century. Agglutinated and porcelaneous orders living

in water depths between 27 and 60 m suffered a noticeable decline or even disappeared

during this time. The declining trend of agglutinated and porcelaneous taxa agrees with

the rising trend of the Ammonia-Elphidhtm index that was previously noticed in cores

from <30-m depths. These trends may be explained by an increase in the severity of

seasonal hypoxia in Louisiana coastal waters. Current data indicate that this hypoxia,

related to eutrophication and water stratification, worsened in the past century, even near

the outer edge of the present-day zone of oxygen depletion in spring and summer.

Communities of living benthic Foraminifera were found in association with the

chemolithotrophic, sulfide oxidizing bacterium Beggiatoa in hydrocarbon seeps of the

northern Gulf of Mexico. Populations of foraminiferal species survive under Beggiatoa

mats to a substrate depth of 4 -5 cm where anoxia, H 2 S, and gaseous and/or liquid

petroleum are major environmental stressors. The few commonly occurring live species

found in surface and subsurface sediments at cold seeps can survive limited amounts of

both oil and H 2 S but none of the species apparently benefits from these compounds.

xiv

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Stable carbon isotope composition of calcitic foraminiferal tests from a 24-cm long core

shows a progressively decreasing trend with time, which match well the trend of

assemblage density, percentage of total carbon, and increased coarse sediment fraction.

These findings reflect temporal variations in seep activity and show that 513C values of

foraminiferal tests are good indicators of hydrocarbon releases, and can be used in their

historical reconstructions.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 1

INTRODUCTION

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This study is concerned with the analysis of benthic Foraminifera from two

stressed environments in the northern Gulf of Mexico. Stress can be defined as “the

response of the cell or organism, to any demand placed on it such that it causes an

extension of a physiological state beyond the normal resting state” (Iwama, 1998). Most

studies of benthic Foraminifera under environmental stress have been from continental

shelf waters affected by some type of pollution. Several characteristics of benthic

Foraminifera make them ideal indicators of the effects of ocean pollution (Bandy et al.,

1964a): 1) they are usually very abundant; 2) their tests show growth patterns and are

preserved after the death of the organism; 3) statistically significant numbers of

individuals are available for analysis. Many studies have analyzed foraminiferal response

in polluted environments (Yanko et al., 1994). Nevertheless, many aspects of

foraminiferal communities in naturally stressed environments are poorly understood. In

the present project, foraminiferal communities and their historical records were studied

from two stressed environments: one of coastal seasonal hypoxia, the other of

hydrocarbon seeps in bathyal depths - oxygen depletion being the common stressor. In

addition, seep environments pose problems of H 2 S toxicity and the presence o f petroleum

components.

BACKGROUND: THE GULF OF MEXICO General Features Due to its topographic complexity, the Gulf of Mexico has received the attention

of many geological investigators (Uchupi, 1975). The Gulf of Mexico is a semi-enclosed,

intercontinental, marginal sea surrounded by the North American continent, including the

states of Texas, Louisiana, Mississippi, Alabama, and Florida on the north, Mexico on the

west, and Florida on the east The Straits of Florida (north of the island of Cuba) and a

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. line arbitrarily drawn from Cabo Catoche on the Yucatan Peninsula to Key West, Florida,

form the southern boundary of the Gulf (Murray, 1961; Gore, 1992).

The continental shelf, with a width that varies between 13 and 217 km, extends

almost continuously around the Gulf. The widest segments of the shelf are located off

western Florida (188 km), off the mouth of Sabine River (Texas-Louisiana border) (177

km), and north of the Yucatan Peninsula (217 km). The continental slope extends

between the 200 and 2000 m water depths, and numerous submerged banks, ridges,

domes, and basins off Louisiana and Texas give its surface a rough, irregular appearance.

All these morphological features were largely formed by intruding subsurface masses of

salt (Murray, 1961; Poag, 1981b). Four major submarine canyons cut across the outer

margin of the continental slope: De Soto Canyon off the Florida panhandle, the

Mississippi Trough off central Louisiana, the Alaminos Canyon off Texas, and

Campeche Canyon along the western margin of the Campeche Shelf (Poag, 1981b).

The Gulf of Mexico is connected to the Caribbean Sea by the Yucatan Strait and

to the Atlantic Ocean by the Florida Straits. At the Yucatan Strait, a sill of approximately

2000 m prevents deep Caribbean waters from entering the Gulf, whereas a sill of about

1000 m allows only shallow water masses of the Gulf to flow into the Atlantic Ocean

through the Florida Straits. A major surface current in the Gulf of Mexico, the Loop

Current, forms as water flow enters the Gulf through the Yucatan Strait. This current

flows northward, sometimes almost to the Mississippi Delta, turns southeastward, and

then exits by way of the Florida Straits, creating the Gulf Stream (Morrison and Nowlin,

1977). Oceanographic studies have shown that the Gulf sea water consists of several

water masses that can be identified by their temperature, salinity, and oxygen content.

From the surface to the deepest water depth in the Gulf, they are: the Surface Mixed

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Layer (0-100 m), the Subtropical Underwater (100-300 m), Oxygen Minimum Water

(300-900 m), Antarctic Intermediate Water (900-1050 m), North American Deep Water

(1050-1500 m), and Gulf Basin Water (< 1500 m ) (Nowlin, 1971 [in Poag, 1981b]).

Two major types of sediments, siliciclastic and biogenic carbonate, can be

distinguished within the Gulf of Mexico. Siliciclastic sediments in the Gulf of Mexico are

mainly provided by the Mississippi River (Mississippi Regime) whose load is rich in silt,

clay, and organic detritus. Sediments from the Mississippi River system are deposited

within its huge delta, along the eastern half of the Texas-Louisiana coast (muddy

substrate) as well as in deep water where they form the Mississippi fan. Numerous rivers

around the Gulf also supply siliciclastic sediments within the Central Texas Regime, Rio

Grande Regime, Mexican Regime, and Eastern Gulf Regime. Two major areas of the

Gulf are blanketed by organic carbonate. One extends from the middle part of the West

Florida Shelf down to the upper part of the adjacent slope (Florida Carbonate Regime);

the other occupies the Banco de Campeche and Campeche Slope (Campeche Carbonate

Regime) (Poag, 1981b).

The Mississippi Influence

The Mississippi River system, one of the world's top ten rivers in terms of

freshwater and sediment inputs to the coastal ocean area, drains an area of 41% of the

conterminous United States (Milliman and Meade, 1983). Organic and inorganic

components resulting from natural continental weathering and anthropogenic activity are

transported by the river and discharged into the Gulf of Mexico at two sites, the

Mississippi birdfoot delta and the mouth of the Atchafalaya River. The total sediment

transported by the two rivers into the Gulf is estimated to be about 678,000 tons/day

(Coastal Wetlands Planning, Protection and Restoration Act [CWPPRA]). Changes in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. land-use and anthropogenic nutrient additions that took place this century are responsible

for significant increases in nutrient loading (especially nitrate) in the Mississippi River

System. The mean annual concentration of nitrate as measured in the Lower Mississippi

River, doubled since the 1950s, whereas the silicate mean annual concentration decreased

by 50% over the last several decades (Turner and Rabalais, 1991; Rabalais etal., 1996).

Although extremely variable through time, total phosphorus concentrations have also

increased in the last few decades (Rabalais et al., 1996). Changes in nutrient ratios, Si:N,

N:PandSi:P, have also taken place. The current Si:N:P ratio (16:16:1) suggests a

balanced nutrient composition for the Lower Mississippi River waters (Justic et al., 1995;

Rabalais et al., 1996).

GULF OF MEXICO BENTHIC FORAMINIFERA

General Features of the Distribution

In his book “Ecology and Distribution of Recent Foraminifera,” Fred Phleger

(I960) summarized the ecology and the distribution of modem Foraminifera. His

generalization was largely based on previous studies in the northern Gulf of Mexico (e.g.,

Lowman, 1949; Phleger, 1951; Bandy, 1954,1956; Parker, 1954). Phleger clearly

established that major depth related changes in species assemblages in the northern Gulf

of Mexico take place at about 100 m (80-120 m), 200 m, 500 m, 1000 m, and 2000 m. He

also showed that distinct foraminiferal assemblages can be found in distinct environments

such as marine marshes, estuaries, coastal lagoons, beaches and nearshore areas, the

continental shelf, and the continental slope-abyssal plain. Foraminiferal data from 77

papers published between 1918 and 1981 were summarized and published in the form of

five catalogues and 296 distribution maps by Culver and Buzas (1981). Other authors

summarized foraminiferal studies from more local areas within the Gulf. Poag and Sweet

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (1972) dealt with Foraminifera from carbonate banks and reefs on the Texas-Louisiana

and west Florida shelves. Walton (1964) focused on Foraminifera from northeastern Gulf

of Mexico.

An ecological atlas of benthic Foraminifera of the Gulf of Mexico was published

by Poag (1981b). Poag recognizes 42 foraminiferal (generic level) predominance facies

within several geographic domains: bays, lagoons and estuaries, continental shelf,

continental rise, Florida Plain, Sigsbee Plain, and Mississippi Fan. Foraminiferal

communities of bays, lagoons, and estuaries are generally dominated by the agglutinated

genus Ammotium (Ammotium predominance facies) and two hyaline taxa, Ammonia

(Ammonia predominance facies) and Elphidium (.Elphidium predominance facies).

Furthermore, a miliolid predominance facies occupies a relatively large area within

Laguna Madre and lower Baffin Bay, Texas (Poag, 1981b). On the continental shelf, the

predominance facies form elongate strips that succeed one another in seaward direction.

However, the generic predominance also changes in a direction parallel to the coast. The

most widespread predominance facies next to the shore is that of the genus Ammonia.

The Ammonia “strip” extends almost continuously from the tip of Florida to Laguna de

Terminos (Poag, 1981b). Ammonia briefly loses its predominance at the Mississippi

Delta and shares it with that of Elphidium, forming the Ammonia-Elphidium

predominance facies along the Texas and Mexican shelves. Around the Mississippi Delta,

small hyaline taxa such as Epistominella and Nonionella form two distinct predominance

facies. They are replaced by Brizalina, Goesella, and Bulimina predominance facies in a

basinward direction. Aside from Ammonia and Ammonia-Elphidium predominance

facies, several other predominance facies exist on the Texas-Louisiana shelf. The middle

shelf is characterized by Fursenkoma, Saccammina-Amobaculites, Elphidium-

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Hanzawaia, Buliminella, Bigenerina, and Elphidium whereas on the outer shelf,

Brizalina , Cibicidoides and, locally, Uvigerirta constitute main predominance facies

(Poag, 1981b).

Foraminiferal predominance on the west Florida shelf is quite different from that

of the Texas-Louisiana shelf. Foraminiferal genera associated with coral reefs are

characteristic of this area. Along the western shelf of Florida, miliolid predominance

facies replace Ammonia predominance facies in a basinward direction. This facies is

strongly developed off southern Florida (Poag, 1981b). The median area of the Florida

shelf is occupied by Asterigerina, Rosalina and several soritids. Hanzawaia and

Planulina dominate the shelf between this area and the shelf-edge where Cibicidoides is

the dominant genus. Miliolid facies dominate the Campeche shelf and Cibicidoides forms

a predominance facies at its outer edge. A miliolid -Archais-Homotrema predominance

facies characterizes the emergent reefs (Poag, 1981b).

Ecological studies of Foraminifera in the northern Gulf of Mexico also include the

following: Phleger, 1951, 1954, 1955; Phleger and Parker, 1951; Bandy, 1954; Moore,

1957; Lankford, 1959; Shifflett, 1961; Lynts, 1962, 1965,1966; Walton, 1964; Seiglie,

1968; Poag, 1978, 1981a, 1984; Spencer, 1992; Miller and Lohmann, 1982; Corliss and

Fois, 1990; Corliss and Emerson 1989; Culver and Buzas, 1981; Denne and Sen Gupta,

1991,1993. All of these studies relate the distribution patterns of Foraminifera to factors

such as temperature, salinity, water depth, nature of substrate, dissolved oxygen, total

organic carbon content, distance from the shore, and integrated water-mass properties.

Seasonal Hypoxia on the Continental Shelf

The Mississippi River and its distributaries contribute large volumes of fresh

water to the Gulf of Mexico (Rabalais et al., 1991). On the continental shelf adjacent to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the deltas of the Mississippi and Atchafalaya Rivers, the freshwater discharge rapidly

forms the Louisiana Coastal Current, a highly stratified coastal current that, in general,

flows westward along the Louisiana coast and southward along the Texas coast (Rabalais

et al., 1991,1994,1996). Reversed flow directions (towards the north and east) take place

during late spring and summer when the Texas coast becomes favorable for upwelling.

Salinity is the major controlling factor of stratification in the Louisiana Coastal Current

(Rabalais et al., 1991,1994,1996). Stratification is easily broken down when winds are

strong enough to cause vertical mixing within the water column (Wiseman et al., 1992).

This usually takes place during winter when intense wind mixing is controlled by cold air

outbreaks and frontal passages (Rabalais et al., 1994).

The high nutrient inputs into the Gulf of Mexico mediate high biological

productivity in the immediate and extended plumes of the Mississippi River. In spite of

the lower silicate concentration delivered by the Mississippi River, the accumulation of

biologically-bound silica (BSi) in dated sediment cores indicates increased diatom

productivity for the last century (Rabalais et al., 1994,1996). Nutrient changes, increased

phytoplankton production, water column stratification, and water circulation patterns in

the northern of Gulf of Mexico, all contribute to the largest, most severe, and most

persistent zone of hypoxia (O 2 < 2 mg/1, i.e., 1.4 ml/1) in the United States coastal waters

(Rabalais et al., 1991). The area impacted by hypoxia during mid-summer periods can be

as large as 20,000 km2 and extends from the Mississippi River delta to the upper Texas

coast (Rabalais et al., 1994,1999,2000). Hypoxic waters extend from the shallow depths

o f 4 to 5 m to as deep as 60 m water depth. However, bottom water hypoxia most

commonly occurs at depths between 5 and 30 m (Rabalais et al., 1999).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Low bottom water oxygen concentrations are responsible for seasonal reduction

in benthic macrofauna and meiofauna (Gaston, 1985; Murrell and Fleeger, 1989; Boesch

and Rabalais, 1991; Rabalais and Harper, 1992). Investigations of hypoxia effects on

meiofaunal communities on the southeastern Louisiana shelf revealed a modest decrease

in the nematode density coincident with the hypoxia. However, it has been found that

hypoxia may be responsible for a virtual elimination of benthic copepods and

kinorhynchs (Murrell and Fleeger, 1989). It has been shown (Boesch and Rabalais, 1991)

that even in the presence of H 2 S, the sediments may not be completely defaunated and

survivors have the potential to reproduce as soon as hypoxia is reduced. Hypoxia stress

reactions in motile organisms have been also observed on the Louisiana shelf. Thus,

when oxygen concentrations reach levels below 2.0 but not yet 0.0 ppm, epibenthic

invertebrates respond by attempting to move at least part of their bodies higher into the

water column (Rabalais and Harper, 1992).

Benthic foraminiferal responses to seasonal hypoxia in Mississippi River plume

on Louisiana continental shelf have been documented by Blackwelder et al. (1996),

Rabalais et al. (1996,2000), Sen Gupta et al. (1996), Platon and Sen Gupta (1997), and

Platon and Sen Gupta (in press). High abundances of Epistominella vitrea recorded from

the Mississippi River plume vicinity suggest tolerance to rapid sedimentation. The

historical record of species distribution shows an increasing trend of Buliminella morgani

abundance coincident with worsening hypoxia (Blackwelder et al., 1996). Although both

Epistominella vitrea and Buliminella morgani dominate the total assemblages of benthic

Foraminifera in areas located off the Mississippi River plume, Buliminella morgani is the

dominant species among the living (Rose Bengal stained) individuals (Platon and Sen

Gupta, 1997). The Ammonia-Elphidium Index (A-E index = N a/(N a + N e)X 100) is a

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. useful proxy for hypoxia. The stratigraphic trend of A-E Index corroborated with

biogenic silica data provides a historical record of paleohypoxia on the Louisiana

continental shelf (Sen Gupta et al., 1996).

Hydrocarbon Seeps on the Continental Slope

In the Gulf of Mexico, traps for hydrocarbon accumulations and hydrocarbon

seepage are directly related to salt diapirs (Aharon et al., 1997; Roberts and Carney,

1997). Large growth faults and small faults associated with salt movement constitute

pathways for the transport of hydrocarbons to the sea floor (Roberts and Carney, 1997;

see Figure 1.1).

Figure 1.1. Schematic figure showing the relationship between salt diapirs, faults and seepage (modified from Roberts and Carney, 1997).

Benthic communities similar to those of deep sea hydrothermal vents have been

found in many cold-water sulfide-methane seep environments. Dense biological

communities associated with regions of oil and gas seepage were reported from different

sites on the Louisiana continental slope. Hydrocarbon vent organisms, represented by

bivalves, gastropods, and vestimentiferan tube worms, were recovered from water depths

o f600 to 700 m in the Green Canyon area (Kennicutt et al., 1985). The survival

mechanism adopted by hydrocarbon vent populations is thought to be similar to that of

organisms inhabiting deep sea hydrothermal vents. The hydrocarbon vent fauna use

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. organic matter produced in situ by chemoautotrophic, sulfide-oxidizing bacteria and

endosymbiotic chemoautotrophs. Carbon isotope analysis performed on the mantle and

foot tissue of bivalves suggests that the food source of these animals results from

chemosynthesis, rather than terrestrial or marine photosynthetic organic carbon. The

measured 8,3C values (-31 to -35°/oo) support the idea that sulfur- or hydrocarbon-

oxidizing bacteria in this hydrocarbon/sulfide-rich environment are the main food

component of the bivalves (Kennicutt et al., 1985).

Chemical and isotopic analysis performed on mussels, clams, and tube worms

from hydrocarbon vents have revealed symbiotic relationships of these organisms with

chemoautotrophic bacteria. It has been shown that some vestimentiferan tube worms and

clams contain intracellular, autotrophic sulfur bacteria symbionts (Childress et al., 1986;

Brooks et al., 1987; Fisher et al., 1987) whereas some mussels harbor methanotrophic

symbionts (Brooks et al., 1987).

Little is known about living Foraminifera of hydrocarbon vents. However, the

presence of living benthic Foraminifera (detected by Rose Bengal stain) and preliminary

results of their vertical distribution have been reported (Sen Gupta and Aharon, 1994; Sen

Gupta et al., 1997). Scarce foraminiferal communities were found especially in

association with undisturbed, large, mat-forming Beggiatoa. Small populations of a few

species survive within and under the bacterial mats, down to a substrate depth of 2 or 3

cm. Although the high dominance of species such as Bolivina ordinaria, Gavelinopsis

translucens , Cassidulina neocarinata , Bolivina subaenariensis, and Uvigerina laevis

could not be directly related to the vent areas but rather to the water depth, it has been

shown that diverse species of benthic Foraminifera live in mats of the sulfide-oxidizing

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. bacteria Beggiatoa (Sen Gupta et al., 1997). The foraminiferal community of

hydrocarbon seeps is exposed to severe oxygen depletion and possible H 2S toxicity (Sen

Gupta et al., 1997). We do not yet know the mechanism these protists employ to survive

in these hostile environments. However, it has been both inferred and shown by

laboratory experiments that Foraminifera may be facultative anaerobes (Moodley and

Hess, 1992; Bernhard, 1993; Sen Gupta and Machain-Castillo, 1993; Bernhard and Sen

Gupta, 1999). Furthermore, it has been suggested that particular physiological strategies

such as non-oxidative metabolism through fermentation or nitrate reduction, metabolic

dormancy, encystment, or incorporation of bacterial endosymbionts may help

Foraminifera to survive anoxia (Bernhard, 1993). Ultrastructure studies of benthic

Foraminifera species recovered from hydrocarbon seeps in Green Canyon (Sen Gupta et

al., 1997) showed that Cassidulina neocarinata forms a thickened lining to seclude its

cytoplasm from the surrounding environment. This has been envisioned as a possible

manifestation of dormancy.

RELEVANT STUDIES FROM OUTSIDE THE GULF OF MEXICO

Pollution

Pollution related foraminiferal research has been concentrated on the effects of

industrial, agricultural, and domestic waste, paper processing, and hydrocarbon (oil-gas)

seepages (Yanko et al., 1994). In the vicinity of municipal sewage outfalls foraminiferal

abundance increases close to the effluent source (Watkins, 1961; Bandy et al., 1964a,

1964b, 1965; Schafer, 1973). This might be due to the increase in organic and nutrient

content or to reduced predation (Alve, 1995). However, the excess in organic content

seems to be responsible for the reduced oxygen conditions that develop in the vicinity of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the source of chemical and organic effluents in several of the studied areas (Bandy et al.,

1964a; Schafer, 1973).

In areas of heavy metal and chemical pollution, the abundance and species

diversity of benthic Foraminifera may decrease with increasing metal concentrations

(e.g., Alve, 1991). However, in Guyanilla Bay, Puerto Rico, Seiglie (1975) found that

Foraminifera are more resistant to chemical contaminants than nematodes are.

The biological response to an oil-polluted environment has been documented in

areas with natural seeps, petroleum operations, and oil tanker accidents. Dermitzakis and

Alafousu (see Alve, 1995) analyzed benthic foraminiferal communities in a naturally oil-

polluted marine environment south of Zakythos Island (off western Greece). Casey et al.

(1980) investigated the impact produced by the Ixtoc / and Burmah Agate oil spills on

living benthic Foraminifera and microzooplankton in the Gulf of Mexico. It was shown

that an increase in standing crop of benthic Foraminifera and the appearance of Brizalina

lowmani were trends related to the oil spill. Several species of benthic Foraminifera from

the Lower York River, Virginia, have been studied with the aim of assessing the effects

of oil pollution (Whitcomb, 1977). The response of Ammonia beccarii and Allogromia

laticolaris to oil exposure was tested in a culture study. The results showed that crude oil

triggers inhibition of both growth and reproduction whereas oil distillates proved to be

highly toxic inducing the death of studied specimens (Whitcomb, 1977). Foraminiferal

communities around petroleum production platforms on the southwestern Louisiana Shelf

were studied by Locklin and Maddocks (1982). No negative effects of petroleum

operations on the benthic Foraminifera were noted.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Coastal Hypoxia

The increasing hypoxia on many continental shelves has triggered an interest in

the study of benthic communities of oxygen poor habitats. A review by Diaz and

Rosenberg (1995) concluded that “there is no other environmental parameter of such

ecological importance to coastal marine ecosystems that has changed so drastically in

such a short period as dissolved oxygen.” Alve (1990) analyzed the diversity of

agglutinated Foraminifera in the oxygen-depleted environment of Drammensfjord,

Norway. She found that a low-diversity fauna of mainly agglutinated Foraminifera

characterizes waters with oxygen content > 2 ml/1 (= 2.86 mg/l) whereas only a few

species such as the calcareous Stainforthia Jusiformis and the agglutinated

Spiroplectamina biformis tolerate severe hypoxia (< 0.5 ml/l O 2 = 0.7 mg/l O 2) and the

presence of H 2 S. Sen Gupta and Machain Castillo (1993), in their review of Foraminifera

in low oxygenated habitats, concluded that species that are tolerant of severe oxygen

depletion are opportunistic, they have wide geographic distributions, they include both

calcareous and agglutinated forms, and some of them are able “to stand spells of anoxia.”

The history of seasonal oxygen depletion in Louisiana coastal waters has been analyzed

by means of selected species of benthic Foraminifera (Sen Gupta et al., 1996). It was

concluded that the increase of the Ammonia-Elphidium Index (index based on relative

abundances of the two genera) coincides with the increase of biologically bound silica

and thus, it is a useful qualitative proxy for hypoxia stress.

High amounts of nutrients and organic detritus supplied by the Po River into the

shallow basin of the northern Adriatic Sea (< 50 m) fuel significant algal blooms during

the spring and summer seasons (Justic et al., 1995). Thus, when the water column is

strongly stratified, the decomposition of phytoplankton remains causes severe oxygen

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. depletion (van der Zwan and Jorissen, 1991). Opportunistic foraminiferal taxa such as

Buliminar Valvulineria, and Nonionella , tolerate low oxygen concentration and thus,

profit from the high food availability (van der Zwan and Jorissen, 1991).

Several indicators recorded in dated sediments from Chesapeake Bay were used

for reconstructing a long-term history of anoxia and eutrophication in the bay. Increased

sedimentation rates, anoxic conditions, and eutrophication were suggested by variations

in pollen, diatoms, organic carbon, nitrogen, sulfur, and an estimate of the degree of

pyritization of iron (Cooper and Brush, 1991,1993). A significant environmental change

recorded for the post European settlement period (from the early 17th to early 18th

century) suggested anthropogenic influences on the watershed (Cooper and Brush,

1993). The historical record of benthic Foraminifera from Chesapeake Bay reveals a

significant change in the relative abundances of the species Ammonia parkinsoniana.

From being absent prior to the late I?111 century, Ammonia parkinsoniana became the

most abundant species (80-90%) beginning in the early 1970s (Karlsen et al., 2000).

Historical trends of benthic foraminifera as related to the evolution of hypoxia

within Long Island Sound have been assessed by Thomas et al. (2000). A decrease in the

relative abundance of Elphidium excavation clavatum towards western Long Island

correlates well with a strong increase in the relative abundance of Ammonia beccarii

(Thomas et al., 2000)

Hydrocarbon Seeps

Foraminifera from cold seeps of Monterey Bay, California (900-1000 m) were

analyzed by Bernhard et al. (in press). Two independent vital methods ([ATP], cellular

ultrastructure) and conventional Rose Bengal (rB) staining were used to determine if

living Foraminifera inhabit methane-rich sulfide rich cold seeps in this region (Bernhard

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. et al., in press). Samples assayed for both rB and ATP showed little difference in

determining living organisms between the two procedures. However, Rose Bengal

stained specimens of Globobulimina from one sample were determined to be dead by

[ATP]. Abundances of few species were higher in seep samples than they were in non-

seep samples and many of rB stained specimens found in seep samples belong to small

sized taxa. Prokaryote ectosymbionts were found in pores of one specimen of Uvigerina

peregrina (Bernhard et al., in press).

Increased abundances of Ruthefordoides comuta and Bulimina striata were

reported from cold seeps in Sagami Bay, Japan (Akimoto et al., 1994). In the North Sea,

cold-seep assemblages are dominated by Uvigerina peregrina , Cassidulina laevigata,

Hyalina balthica, and Elphidium clavatum (Jones, 1993).

THIS PROJECT

This study is concerned with foraminiferal microhabitat distribution and temporal

variation of species richness, species diversity, and/or abundance of foraminiferal species

in two areas on the continental margin of the Gulf of Mexico. (1) Spatial and temporal

variations of foraminiferal communities were investigated in the context of seasonal

changes in the oxygen content of Louisiana continental shelf bottom waters. (2) On the

continental slope, living and fossil communities were analyzed with the aim of better

understanding foraminiferal distribution and adaptation in and under cold-seep Beggiatoa

mats, as well as to evaluate their potential for historical reconstruction of hydrocarbon

emissions. The main objectives of this study are: (1) to provide a detailed picture of the

spatial and temporal change in the distribution and diversity of benthic Foraminifera in

stressed environments of the northern Gulf of Mexico (seasonal hypoxia in Louisiana

coastal waters and hydrocarbon seeps in deep water areas); (2) to analyze the change in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. vertical habitat range and vertical distribution of live populations of benthic foraminifera

in stressed environments of the northern Gulf of Mexico; (3) to reconstruct the history of

the environmental change in the context of seasonal coastal hypoxia and hydrocarbon

emissions at cold seeps; and (4) to evaluate the utility of benthic Foraminifera as

indicators of a stressed environment and to provide additional insight into our

understanding of biological response in these environments.

Samples used in this project were collected during several cruises between 1993

and 1997 (Figure 1.2). Three stations located in the Louisiana Bight at 80,40, and 35 m

water depth were sampled in October, 1995. Another set of samples were collected from

one location also located in Louisiana Bight during a cruise that took place between 21st

and 24th of March 1996. Two locations were sampled during the NECOP shelfwide

cruise (N. Rabalais, LUMCON; July 1996). Sediment samples were also collected during

the Pseudonitzschia cruise (Q. Dorch, LUMCON) that took place in April 1997 (F35 and

E60 stations). Sixty eight samples collected from hydrocarbon seeps located in Green

Canyon were provided by Dr. B. K. Sen Gupta. Another set of seven stations located in

the hydrocarbon seep area of Green Canyon were sampled in August 1997. Thus, 200

samples from seven stations placed on the Louisiana continental shelf and 126 samples

from 26 locations from the continental slope, collected during all the cruises mentioned

above, have been processed and analyzed for their foraminiferal content. Additionally,

previously published data (Sen Gupta et al., 1996; Blackwelder et al., 1996) have been

used in the analyses and interpretations. Chapter 3 has been published, and Chapter 2 is

in press.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. GREEN CANYON

92°______9f

Figure 1.2. Sample locations. (A) Shelf samples: F35, G40, D80: October 1995; F20: March 1996; AA1, A5: July 1996 (shelfwide cruise); E60: April 1997 (Pseudonitzschia Cruise); (B) Slope samples: 2635-2900; medium solid circle: locations of sample provided by Dr. Sen Gupta; large open circles: August 1997.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 2

BENTHIC FORAMINIFERAL COMMUNITIES IN OXYGEN-DEPLETED ENVIRONMENTS OF THE LOUISIANA CONTINENTAL SHELF*

* F.mil Platon and Banin K. Sen Gupta; In press in: Coastal Hypoxia: Consequences for Living Resources and Ecosystems; Editors, Nancy N. Rabalais and R. Eugene Turner, American Geophysical Union, Coastal and Estuarine Science Series 58, Washington, D. C.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

Numerous species of benthic Foraminifera have the ability to withstand very low

oxygen concentrations or even anoxic conditions. In addition, there is ample evidence

that in dysoxic to anoxic marine sediments, benthic Foraminifera may migrate through

the sediment to find optimal habitat conditions, although factors other than oxygen also

affect this migration. On the Louisiana continental shelf, the effects of seasonal hypoxia

and the Mississippi River plume on benthic Foraminifera have been documented by

Nelsen et al. (1994), Sen Gupta et al. (1996), Blackwelder et al. (1996), Rabalais et al.

(1996) and Platon et al. (1997). High abundances of certain species in substrates from the

vicinity of the Mississippi River suggest their tolerance to rapid sedimentation.

Furthermore, the historical record of species distribution shows a trend of increasing

relative abundances of putatively opportunistic species with increasing hypoxia. In

particular, the Ammonia-Elphidium index (A-E index) is a useful proxy for present and

past hypoxia, and the stratigraphic trend of the A-E index provides a historical record of

paleohypoxia on the shelf (Sen Gupta et al., 1996). The aim of this chapter is to (1)

examine the summer (hypoxic) and fall (non-hypoxic) distributions (and microhabitats)

of living Foraminifera present in sediment cores from the Louisiana continental shelf, and

(2) assess the historical trend of common benthic foraminiferal species from the

stratigraphic record of the last few decades.

FORAMINIFERAL RESPONSE TO LOW OXYGEN CONCENTRATIONS

Microaerophiles and Facultative Anaerobes in Controlled Experiments

Both field and laboratory observations show that many benthic foraminiferal

species can survive extreme oxygen depletion or even anoxia, at least for a short time

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (reviewed in Sen Gupta and Machain-Castillo, 1993; Bernhard, 1996; Bernhard and Sen

Gupta, 1999). Many laboratory experiments on foraminiferal subsurface activity have

been reported in the literature, but concomitant oxygen levels in sediment pore water

have been measured in only a few studies. In a study of nearshore species from McMurdo

Sound, Antarctica, Bernhard (1989) used an adenosine triphosphate (ATP) assay to

recognize living individuals and found that several agglutinated and calcareous species

were viable even in anoxic layers. Furthermore, she subjected these Antarctic

Foraminifera to anoxic or reducing conditions for 30 days and determined that 30% of the

analyzed individuals could withstand such conditions (Bernhard, 1993). Ultrastructural

investigations revealed the presence of chemolithotrophic-type bacteria beneath the

organic lining of Globocassidulirta sp. cf. G. biora, leading to the suggestion that these

bacteria may help in anaerobic survival of this foraminifer (Bernhard, 1993).

Using foraminiferal species from a Norwegian fjord in which bottom waters are

periodically dysoxic, Alve and Bernhard (1995) performed a laboratory experiment in

which the oxygen level was reduced to < 0.3 mg/l (0.21 ml/1) three months and

maintained at this low level for five weeks. In response, the species migrated upward in

the sediment into pore water with higher oxygen concentrations. In another experiment,

four species were kept in anoxic seawater (purged with nitrogen) for over three weeks.

These species, apparently facultative anaerobes, survived anoxia (based on ATP assays)

in different (mostly unknown) ways, including dormancy (Bernhard and Alve, 1996). In a

comparable experiment with Foraminifera collected from the Adriatic Sea shelf, Moodley

et al. (1997) showed that many species can withstand anoxia (and the presence of H 2 S)

for several weeks; the conclusion that the individuals were still alive was based on Rose

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Bengal staining and on life activity checks. Migratory activity of selected common

species and mixed foraminiferal assemblages through sediment of varying pore-water

oxygen was examined in the laboratory by Moodley et al. (1998). Upward migration was

evident when species were buried in sediments without an oxic zone, indicating that

anoxic conditions may stimulate migration. The investigators suggested that the presence

of particular species in deeper sediment layers is related to their tolerance to prolonged

anoxia and to sediment mixing by physical and biological factors.

Microhabitat Considerations

A foraminiferal "microhabitat" is defined as a micro-environment characterized

by a combination of physical, chemical and biological conditions [oxygen, food, toxic

substances, biological interactions, etc. (Jorissen, 1999)]. A species has a microhabitat

preference if it shows greater abundances at the sediment surface or at some depth

beneath the surface (Hunt and Corliss, 1993). Recognition of foraminiferal microhabitats

and factors responsible for vertical distribution in sediment is of great importance in

assessing foraminiferal responses to environmental changes and in reconstructing past

environments of sedimentation.

In the absence of animal burrows, pore-water oxygen concentration usually

diminishes sharply with substrate depth, falling below detection limits within a few

centimeters (Fenchel and Finlay, 1995). Thus, species with microhabitats in deeper parts

of the sediment column [e.g., Globocassichdina sp. cf. G. biora living at seven cm

(Bernhard, 1993)] may be microaerophiles or facultative anaerobes. Certain benthic

Foraminifera may be able to track seasonal fluctuation of oxygen levels within the

sediment, and their temporal distribution pattern should reflect such seasonal variations

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Jorissen, 1987; Van der Zwaan and Jorissen, 1991). Distribution data are available from

the northern Adriatic Sea, where ample nutrient availability during the summer results in

phytoplankton blooms, which, together with terrestrial material, lead to very high loads

of organic matter. Water stratification and decomposition of organic matter cause severe

depletion of bottom-water oxygen during late summer and autumn (Jorissen et al., 1992).

In order to assess foraminiferal response to this seasonal lowering of oxygen,

Barmawidjaja et al. (1992) analyzed data from a time series of seven samples (December

1988 to November 1989) from one station and showed that bottom-water or pore-water

oxygen is a major factor controlling the faunal densities. Three microhabitat-related

species groups were recognized: epifaunal, predominantly infaunal, and potentially

infaunal. Larger variations of epifaunal taxa support the idea that the tolerance of this

group to low oxygen levels is less than that of infaunal taxa. The "potentially infaunal"

species (with seasonally adjusted microhabitats, from sediment surface to a few

centimeters below the surface) apparently follow some critical oxygen level.

METHODS

Sediment core samples from six stations located on the Louisiana continental

shelf (Louisiana Bight west of the Mississippi River birdfoot delta, Figure 2.1) were

analyzed for this study. Box cores were collected in (1) October 1995 from 35-, 40- and

80-m water depths (stations F35, G40 and D80, respectively); (2) April 1996 from 20-m

water depth (station F20); and (3) July 1996 from 11- and 30-m water depths (stations

AA1 and AS, respectively). Each box core was examined for disturbance after retrieval

and was considered undisturbed if the overlying water was clear and surface tracks and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. open burrows were visible. Cylindrical sediment cores were obtained from these box

cores with 7-cm diameter plastic tubes that were sliced at 1-cm intervals. These 1-cm

Figure 2.1. Hypoxia frequency of occurrence, 1985-1999; core locations, Louisiana Bight. October 1995: F35, G40, D80; April 1996: F20; M y 1996: AA1, A5. [Note added in dissertation: The areas colored in gray tones (< 25%, > 25%, >50%, > 75%) indicate the 30’ I >75% 28030; frequency of occurrence of I >50% hypoxia during mid-summer of I >25% 1985-1999.] <25% GULF OF MEXICO 900 00* 89° 30' I__ I___ sections became the primary samples for the foraminiferal study. Samples from the top

15 cm of the sediment cores were stained with a solution of Rose Bengal in ethanol. All

samples were washed over a 63-pm sieve and dried. For the microhabitat study,

specimens with bright red coloration of one or more chambers were considered living at

the time of collection, and 300 stained specimens (if present) were picked from the

sample. If the number of stained specimens was less than 300 (the usual case), all such

specimens were picked. For the historical trend study, the residue was split with a

microsplitter to provide an aliquot of approximately 300 shells of benthic Foraminifera.

Identification and counting of these specimens yielded the species census; in samples

with fewer than 300 specimens, all specimens were counted.

Two measures of species diversity were computed from the foraminiferal counts:

(1) species richness (S), i.e., the number of species present in the sample or aliquot, and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (2) equitability (E), given by the equation E=eH(S)/S (Buzas and Gibson, 1969), where

H(S) is the Shannon Wiener function (= -Epjlnpj, where pi is the proportion of the i*

species). Absolute ages of samples were obtained from 2l0Pb data (R. E. Turner, unpubl.

data).

HYPOXIA AND FORAMINIFERAL DISTRIBUTION PATTERNS ON THE LOUISIANA CONTINENTAL SHELF

Microhabitats of Common Species

Two groups of samples were analyzed to assess the vertical distribution of living

Foraminifera in the sediment The first group consisted of samples collected from stations

F35, G40, and D80 in October 1995; the second group (AA1 and A5) consisted of July

1996 samples (Figure 2.1). Seventy-three species of benthic Foraminifera (Table 2.1)

were identified, but most of these were rare, and their microhabitat preference could not

be ascertained with the present data. The distributions of dominant species is discussed

Table 2.1. Identified species.

Ammonia parkinsoniana Laterostomella sp.? Ammotium salsum f. dilatatum Lenticulina calcar Angulogerina bella Lenticulina sp. Bigenerina irregularis Lenticulina sp. cf. L. sp. "F' Bolivina albatrossi Lenticulina sp. L. sp ." B" Bolivina barbata Marginulina obesa Bolivina cf. B.fragilis Marginulina sp. cf. M. glabra Bolivina goessi Miliolidae sp. Bolivina lanceolata Miliolinella werreni Bolivina lowmani Neoeponides antilarum Bolivina pusilla Nodosaria sp. Bolivina sp. Nonion grateloupe Bolivina sp. B. fragilis Nonionella basiloba Bolivina sp. cf. B. pusilla Nonionella morgani Bolivina subanaerensis Prolixoplecta parvula Brizalina lowmani Pseudononion atlanticus Bulimina aculeata Pseudononion grateloupe Bulimina marginata Pullenia buloides (Table 2.1 continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Bulimina marginata-translucens Pyrgo sp. Bulimina morgani Pyrgo carinata ? Bulimina sp. Q sp. Anderson Bulimina tenuis Q. lamarkiana Bulimina translucens Rectobolmna advena Cancris sagra Reophax Jusiformis Cassidulina subglobosa Reusella miocenica Discammina compressa Ruatoria ruatori Discorbinella bertholdi Saccammina difligiformis Dorothia sp. Saracenaria sp. Elphidium excavatum Sigmoilina distorta Elphidium gunteri f. salsum Siphotextularia affinis Elphidium poeyanum Spiroloculina sp. cf. S. antilarium Epistominella vitrea Textularia candeiana Fursenkoina elegantisima Textularia porrecta Fursenkoina pontoni Triloculina trigonula Globobulimina sp. ? Uvigerina hispido-costata Hanzawaia concentrica Uvigerina laevis Haplophragmoides sp. Uvigerina peregrina Lagena sp. Uvigerina sp Lagena sp. cf. L laevis Uvigerina sp. cf. U. laevis Lagena sp. cf. L. spicata ______Vaginulinopsis sp. ______

below. Scanning electron micrographs of these are given in Plate 2.1. The absolute

abundance data on living Foraminifera are summarized in Table 2.2.

Relative abundance data from October 199S core samples are depicted in

Figure 2.2. In general, Buliminella morgani dominated the living assemblages of benthic

Foraminifera from the sediment-water interface down to a sediment depth of 5-10 cm,

possibly in severe dysoxic, or even anoxic, microhabitats. Based on species richness as

well as on living foraminiferal density, three microhabitats were discriminated between

the sediment-water interface and the 15-cm depth level. A high dominance of Buliminella

morgani, a relatively high species richness, and presence of both calcareous and

agglutinated forms characterized the first few centimeters (usually 3-5 cm) beneath the

sediment-water interface. A severe reduction in species richness and an increase in the

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. proportion of Brizalina lowmani marked a second vertical zone, extending to about the

10-cm depth level. Below this level, Brizalina lowmani was the dominant or the only

living foraminifer. B 100-1 f l a w 80 60 40 3 20 San 0 120 •s aCL 100 Q 80 s ’ 60 tOan 1 ZD 1 40 •§ 3 u > 20 13 c3 0 □ I 120 i ISan 100 0 S 10 No. of species 80 Brizalina 60 Buliminella morgani 40 Epistominella vitrea Nonionella 20 0 5 10 Depth (cm) Figure 2.2. Distribution of living Foraminifera in October 1995 cores: A, relative abundance of dominant species; B, mean species richness.

The number of Rose Bengal stained specimens (i.e., living foraminifer

assemblage density) was high at the top of each core, but the maximum, in all cases, was

recorded 2-4 cm below the sediment-water interface. This number decreased

continuously from this level down to a depth of about 15 cm. The mean species richness,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. computed from values recorded in F3S, G40, and D80, decreased steadily from the core

top to the depth of 15 cm (Figure 2.2B), but several differences regarding the number of

species identified at different locations and different sediment depths were noted. A total

of 15 living species was identified in core G40. Within these samples, the species

richness varied between 10 at the core top and 6 at the deepest level of foraminiferal

occurrence, but the decrease was not linear, and the mean value was 6. At D80, the total

number of living species was 11, and the maximum (at core top), minimum (at deepest

levels), and mean values of species richness were 7,1, and 5, respectively. Low values of

richness (maximum 4, minimum 2, mean 3) were recorded from the F35 samples, and the

total number of living species in this core was only 6. These data suggest that water depth

as well as the distance from the Mississippi River plume influence microhabitat

distribution.

As mentioned earlier, it is generally agreed that factors such as bottom-water

dissolved oxygen concentration, food availability, competition and predation, and

bioturbation are major determinants of foraminiferal microhabitats. The high nutrient

amounts delivered by the Mississippi River in the study area (Blackwelder et al., 1996)

should ensure sufficient food supply for both epifaunal and infaunal foraminifers. In

general, organic matter within the sediment is less labile, and food quality decreases with

sediment depth. Nevertheless, bioturbation by macrofauna may introduce a fresh food

supply within the sediment and create conduits for oxygen penetration. At the top of each

core, the species richness maximum and relatively high assemblage density indicate

"normal" environmental conditions. More sensitive species such as Bolivina lanceolata,

B. albatrossi, Fursenkoina pontoni, and Uvigerina laevis decline with sediment depth due

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. to possible pore-water oxygen depletion and lower food quality. More tolerant taxa are

able, to a certain degree, to cope with both reduced oxygen concentration and low-

nutrition food. Thus, the association of maximum assemblage density and a diminished

number of species recorded a few centimeters beneath the sediment-water interface is

apparently controlled by the combination of at least three factors: very low oxygen

concentrations, reduced ratios of fresh/old food supplies and, presumably, reduced

predation and competition. Species such as Buliminella morgani, Brizalina lowmani, and

Nonionella basiloba flourish in this microhabitat

Foraminiferal data from two July 1996 stations (AA1 and A5) are presented in

Figure 2.3. Bottom-water oxygen data collected during this cruise (N. N. Rabalais,

unpubl. data) show that the summer of 1996 was a season of widespread hypoxia in the

Gulf of Mexico, with an estimated bottom extent of 17,920 km2. Dissolved oxygen was

measured at 2.52 mg/l (1.79 ml/1) at A5 (water depth 30 m), but fell to a much lower

value of 0.56 mg/l (0.39ml/l) at AA1 (water depth 11 m). We assume that both of these

measured values were much lower than the corresponding October 1995 levels. Oxygen

data were not collected at the time of the October 1995 cores, but bottom-water oxygen

concentrations at a station in 20-m water depth within 50 km of the Louisiana Bight was

consistently between 4 and 5 mg/l (2.8 and 3.5 ml/1) for the month of October (N. N.

Rabalais, unpubl. data). The number of species identified in the top 15 cm of the AA1

core ranged from 2-3 in the 8-15 cm interval to 6 in the 4-7 cm interval. The assemblage

density maximum was located in the 2-3 cm interval and followed the trend seen in the

cores retrieved during the fall of 1995. The species distribution pattern showed a striking

dominance of Brizalina lowmani over species such as Nonionella basiloba, Buliminella

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. morgani, and Ammonia parkinsoniana. This dominance was persistent throughout the

core, and no vertical zonation was discerned. In contrast, in A5 samples (species richness

1-5, mean 2.5), the assemblage was dominated by Buliminella morgani from the

sediment-water interface to a sediment depth of 15 cm. Species such as Nonionella

basiloba, Ammonia parkinsoniana, and Brizalina lowmani were present, but scarce,

100

60 ] • Ammonia g 40 "j parkinsonian 8 20 i •mm§ Brizalina e s 0 + » • Buliminella marginata ■8 O 120 "I AAl • Buliminella morgani 1 100 v o 0* 80 t ■ Epistominella vitrea 60 • 4 0 ; 20 . o 5 10 15 Depth (cm)

B A5 AAl 0

San £ a. Q F 3 lOan ! Van F=>

I5an Ban, 0 2 4 6 — 0 2 4 6 8 Number of species

Figure 2.3. Distribution of living Foraminifera in July 1996 cores: A. relative abundances of dominant and common species; B. species richness.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. in the 0-8 cm interval. Judged by Rose Bengal staining, Buliminella morgani was the

only putative survivor below the depth of 8 cm. The maximum assemblage density was in

the 0-1 cm interval.

Reduced species numbers and high relative abundances of Brizalina lowmani

(maximum 98%) are two conspicuous features of the foraminiferal community at AAl.

High relative abundances of B. lowmani (up to 56%) have been reported previously from

a nearshore (< 20 m) location in this area (Blackwelder et al., 1996), and we infer that the

microhabitat distribution of the species at AAl is strongly affected by both water depth

and environmental stress related to the oxygen depletion. A comparison of microhabitat

data from F35 (fall 1995,35 m water depth) with that of nearby A5 station (summer

1996,30 m water depth) reveals differences that may be related to seasonal hypoxia. (1)

Buliminella morgani was persistently dominant in A5 (July), but not in F35 (October), in

which Brizalina lowmani dominated the samples below a depth of 6 cm. (2) The mean

density of living individuals was less in A5 (July) that in F35 (October).

Historical Trends of Species Abundances

Historical records of benthic foraminiferal abundance variations in the past 2-14

decades were obtained from three dated sediment cores (F35, G40, and D80) from

different water depths, different distances from the Mississippi River plume and differing

frequency of bottom-water hypoxia (Fig. 2.1). hi this exercise, the contamination of older

(210Pb-dated) foraminiferal assemblages by living populations of infaunal species was not

considered a problem, because the number of dead individuals was always much higher

(below a substrate depth of 4 cm, orders of magnitude higher) than that of living

individuals.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Locations at which foraminiferal assemblages exhibit the lowest species richness

and the highest species dominance were considered the most stressful or most recently

stressed, whereas those with the highest richness and equitability (a measure of evenness

of distribution) were considered to represent the most stable environments (Engen, 1979).

In the area impacted by the Mississippi River plume, previous workers have found

considerably large ranges of species richness (S to 39 species) and evenness, indicating

different degrees of ecological stress (Blackwelder et al., 1996). Within the core samples

from D80, equitability varied between 0.26 and 0.51, and the species richness ranged

between 8 and 15 (mean 11.7). In the G40 samples, equitability values were 0.26 to 0.58,

and the richness values were 9 to 25 (mean = 15.4). The station at 35 m water depth (F35)

was the most frequently affected by seasonal hypoxia, and core samples from this station

had relatively low species richness (3 to 11, mean = 8). Corresponding equitability values

showed a wide range (0.23 to 0.89), but the very high value of 0.89 (1 being the highest

value for this measure) was associated with an extremely low species count of 3 and just

a few individuals, and thus may be anomalous.

Total (living + dead) foraminiferal assemblages at these three stations were

generally dominated by Epistominella vitrea, Buliminella morgani, and Nonionella

basiloba. Epistominella vitrea was the dominant species at all levels in the cores, but its

relative abundance was considerably less in the living assemblages. Because of the

known high abundance of E. vitrea in the Mississippi River plume (Blackwelder et al.,

1996), we infer that NE-SW and E-W transport processes have enhanced the

concentration of shells of this species in our samples. On the basis of 210Pb dating, the

estimated sedimentation rate in the core varied from 0.12 to 220 cm/y. Progressively

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. restrictive environmental conditions are suggested by an overall decrease of foraminiferal

density from 1981 to 1990 at the deepest (80 m) site, and from 1958 to 1994 at the

shallowest (35 m) site (Figure 2.4). Furthermore, in the core from 35 m, the foraminiferal

1995 F35

1992 1989 1990 1981 1988

1974 198S

1967 1983

1960 1981 0 200000 400000 0 50000 150000 250000

Figure 2.4. Variations in foraminiferal assemblage density (x axis, shells per 100 cc o f sediment).

density is highest for the mid 1960s and the lowest (zero values) for most of the 1970s.

No conspicuous dominance shifts were observed in the stratigraphic records of the

benthic Foraminifera, but several trends were discernible in relative abundances of

species. At the 80-m station, the proportion of Bolivina lanceolata decreased, whereas

that o f Bolivina albatrossi increased, from 1985 to 1995 (Figure 2.5). At the 40-m station,

the almost continuous decrease in the relative abundance of Elphiditan gunteri/excavatum

from 1853 to 1995 was interrupted by a positive trend between 1929 and 1945

(Figure 2.6). Because of the low proportions of these species in the assemblages (usually

< 5%) and small numbers of the individuals counted, the observed trends may or may not

have paleoenvironmental significance. More pronounced trends were recognized at the

35 m station (Figure 2.7). After a slight decrease from 1960 to 1971, the density of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Buliminella morgani increased substantially between 1971 and 1975 and then remained

steady until 1995 (core-top date). The 1971-1975 time interval was marked by a drastic

1995

1992

1990 Figure 2.5. Stratigraphic variations in the proportions of Bolivina lanceolata (left) 1988 f £ and Bolivina albatrossi (right) in the foraminiferal assemblage of D80 in the 1985 l | past two decades.

1983

1981 0 0.1 0 2 0 3 0 0.05 0.1

1995 — 1 I

1945 Figure 2.6. Stratigraphic variations in the proportion o f Elphidium gunteri in the foraminiferal assemblage o f G40 from 1853 to 1995.

1895

1853 0 0.05 0.1

reduction in the relative abundance o f Epistominella vitrea , Nonionella basiloba, and

Brizalina lowmani. The reduction in Epistominella vitrea may be related to diminishing

G-W transport processes and/or environmental changes in the Mississippi River plume

area.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1995

1989

1981

1974

1967

1960

Figure 2.7. Stratigraphic variations in the proportions of Buliminella morgani (A.), Epistominella vitrea (B.), Nonionella basiloba (C.) and Elphiditm gunteri/excavatum (D.) in the foraminiferal assemblage of F35 in the past four decades.

The Ammonia-Elphidium Index

Ammonia parkinsoniana and Elphidium gunteri/excavatum, common

foraminiferal species of continental shelves, may be facultative anaerobes (Kitazato,

1994), but the dominance of A. parkinsoniana over E. gunteri/excavatum in nearshore

surface sediments of the Gulf of Mexico during maximum hypoxia (Sen Gupta et al.,

1996) indicates a higher tolerance of the former to oxygen depletion. An Ammonia-

Elphidium (or A-E) index, given by (NA X 100)/(Na + Ne) whose distribution in the

surface sediments of Louisiana Bight correlates well with the abundance of total organic

carbon, was proposed as a proxy measure for paleohypoxia by Sen Gupta et al. (1996).

Because significant proportions of living Ammonia and Elphidium are typical only of

marginal marine and inner shelf habitats, the reliability of this index is reduced beyond a

water depth of about 30 m. This is evident in Figure 2.8. The increase of A-E index

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. correlates well with the overall rise in oxygen stress on Louisiana continental shelf in

water depths o f20-30 m, but this index is more variable in greater depths, especially at A. B. no 100 F20 E30

I9S0 1970 19901930 1950 I960 1970 1980 1995 Year Year

C. 12 G40 10 8 X •o4) .5 6 cdt < 4 2 0 1853 1895 1945 1995 Year

Figure 2.8. A-E index recorded in cores from different water depths: A, 30 m (Core E 30, Sen Gupta et al., 1996), B, 20 m (this study), and C, 40 m (this study).

the margins of the area affected by spring/summer hypoxia (Figure 2.1). Nevertheless,

hypoxia is most frequently recorded between bottom-water depths of 5 and 30 m

(Rabalais et al., 1996), and the lack of a trend in the A-E index in deeper waters may

indicate a much reduced frequency, or an absence, of severe oxygen depletion.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CONCLUSIONS

1. Many species of benthic Foraminifera survive under seasonal hypoxia on the

Louisiana continental shelf. This finding is consistent with field and laboratory

investigations of previous workers on foraminiferal tolerance of severe oxygen depletion.

At any given location, the composition of the present foraminiferal community is

particularly dependent on water depth, distance from the Mississippi River plume, and

dissolved oxygen at the sediment-water interface and in pore water (which was not

measured).

2. Judging by their microhabitat preferences and dominances within living

foraminiferal assemblages, several species are microaerophilitic or facultative anaerobes.

The most notable are Buliminella morgani and Brizalina lowmani.

3. The Ammonia-Elphidium index (based on species proportions in core samples)

is a sensitive proxy for paleohypoxia in water depths less than about 30 m. In greater

depths, the reduced abundances of both genera diminish the reliability of this proxy, but

the high variability of the A-E index here may be related to a decrease in the frequency of

hypoxia.

4. On the basis of the present data, progressively restrictive environmental

conditions (related to the intensity of seasonal hypoxia) are suggested by a decrease of

foraminiferal density from 1981 to 1990 at the deepest (80 m) site and from 1958 to 1994

at the shallowest (35 m) site.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 2.1

Common benthic Foraminifera of the Louisiana Bight (All scale bars represent 100 pm)

I, 2 ,3 . Nonionella basttoba Cushman and McCulloch

4 ,5 . Bolivina albatrossi Cushman

6 ,7. Epistominella vitrea Parker

8. Elphidium gunteri/excavatum Cole/(Terquem)

9. Uvigerina laevis G5es

10,16,17. Fursenkoina pontoni (Cushman)

II,1 3 . Brizalina lowmani (Phleger and Parker)

12. Buliminella morgani Andersen

14,15. Ammonia parkinsoniana (d’Orbigny)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 2.1

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 3

TWENTIETH-CENTURY CHANGES IN THE BENTHIC FORAMINIFERAL COMMUNITY OF THE LOUISIANA CONTINENTAL SHELF

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

The historical record of foraminiferal assemblages from the northwestern Gulf of

Mexico demonstrates a progressive increase of oxygen stress during the twentieth century

(Sen Gupta et al, 1996). A decrease in the abundance of Quinqueloculina spp. (Rabalais

et al., 1996), an increase of Buliminella morgani (Blackwelder et al., 1996), and a

positive trend in the relative dominance of the more tolerant Ammonia parkinsoniana

over the less tolerant Elphidium excavatum (Sen Gupta et al., 1996; Platon and Sen

Gupta, in press) are all thought to be triggered by the strong seasonal oxygen depletion

that affects Louisiana and Texas coastal waters.

Factors such as water stratification and high inputs of organic matter trigger the

formation of hypoxic (O 2 < 2 mg/l =1.4 ml/1) bottom waters (Rabalais et al. 1991). The

freshwater discharged by the Mississippi River System at two sites, the Mississippi

birdfoot delta and the mouth of the Atchafalaya River, initiates the density stratification

restricting the bottom water reoxygenation. Stratification is easily broken down when

winds are strong enough to cause vertical mixing within the water column (Wiseman et

al., 1992). This usually takes place during winter when intense wind mixing is controlled

by cold air outbreaks and frontal passages (Rabalais et al., 1994).

The high nutrient input, regeneration and favorable light conditions (Rabalais et

al., 1994,1996) promote increased biological productivity in the immediate and extended

plume of the Mississippi River (Sklar and Turner, 1981; Lohrenz et al., 1990).

Subsequent carbon accumulation at the seabed provides enough organic matter to deplete

the lower water column of oxygen within shorter (days) or longer (months) periods of

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. time (Turner and Allen, 1982; Dortch et al., 1994). One-hundred-year changes in river-

born nutrient (dissolved phosphate, nitrate, and silicate) concentrations (Rabalais et al.,

1996) are linked to anthropogenic activity in the Mississippi River watershed (Turner and

Rabalais, 1994; Blackwelder et al., 1996). The application of artificial fertilizer in the

Mississippi River drainage basin, in particular, has led to the seaward transportation of

increasing amounts of agricultural byproducts during the last several decades

(Blackwelder et al., 1996).

Since 1985, seasonal bottom-water hypoxia in coastal waters of the Gulf of

Mexico has been monitored and documented over extensive areas of the Louisiana

continental shelf (Rabalais et al., 1991,1992,2000). Low dissolved oxygen concentration

may occur as early as late February and continue through early October (Rabalais et al.,

1999,2000). The areal distribution of hypoxia can extend from shallow nearshore waters

(4 to 5 m) to waters as deep as 60 m water depth (Rabalais et al., 1999), and cover up to

20,000 km2 (Rabalais et al., 2000).

Coastal hypoxia in the northern Gulf of Mexico has been directly studied through

measurements of water quality only for a short period. Thus, little is known about the

century long evolution of the shelf ecosystem in the context of reduced bottom water

oxygen concentrations. Nevertheless, inferences about hypoxia prior to mid 1980s have

been made based on records of water quality data for the lower Mississippi River that go

back to the early 1900s (Rabalais et al., 1996), the sedimentary records of biogenic silica

concentrations (Turner and Rabalais, 1994), glauconite concentrations (Nelsen et al.,

1994), and foraminiferal assemblages (Nelsen et al., 1994; Rabalais et al., 1996;

Blackwelder et al., 1996; Sen Gupta et al., 1996; Platon and Sen Gupta, in press).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The historical data of foraminiferal species distribution in Core 10 of Nelsen et al.

(1994) and Blackwelder et al. (1996) suggests that over the last century “a more diverse,

less hypoxia tolerant community has been replaced by a more stress-tolerant population”

(Blackwelder et al., 1996). Sen Gupta et al. (1996) found that the relative proportions of

more tolerant Ammonia and less tolerant Elphidium (Ammonia-Elphidium index) is a

useful proxy for present and past hypoxia, and the stratigraphic trend of the A-E index

provides a historical record of paleohypoxia on the shelf. The density reduction of some

genera such as Ammonia (Blackwelder et al., 1996) and the disappearances of some taxa

such as Quinqueloculina (Rabalais et al., 1996) and Pyrgo nasutus (Blackwelder et al.,

1996) were noted in cores from nearshore locations (-30 m water depth). Seemingly

tolerant species such as Buliminella morgani, Epistominella vitrea, and Nonionella

basiloba show increasing and/or steadily high relative abundances in sediment cores from

several locations within a water depth range from 30 to 80 m (Blackwelder et al., 1996;

Platon and Sen Gupta, in press).

The focus of this chapter is an assessment of the historical trends in common

benthic foraminiferal species preserved in the stratigraphic record of the last 100 years in

the area most frequently affected by seasonal hypoxia (S to 30 m water depth) and also at

the outer edge of this zone (60 m water depth). Locations from which foraminiferal data

have been analyzed are shown in Figure 3.1. Parameters such as individual taxa (species

and/or higher level) distribution, species richness (number of species), species diversity

(Shannon-Wiener function), univariate and multivariate responses, as well as

microbiostratigraphic signals are examined. A brief overview of worldwide occurrence of

coastal hypoxia is provided.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ^Y0<* ----- BL10 29° 00' ^F35

ass

28° 30' 28° 30’

89° 30'

Figure 3.1. Core locations; F3S and E60 locations sampled in spring 1997; BL10 = Core 10 of Blackwelder et al. (1996); some foraminiferal data from G27 were published in Rabalais et al. (1996) and Sen Gupta et al. (1996).

METHODS

Sediment core samples from two stations located on the Louisiana continental

shelf (Louisiana Bight), as well as published foraminiferal data from cores taken in 29 m

(Blackwelder et al., 1996) and 27 m (Rabalais et al., 1996) water depths, were analyzed

for this study (see Figure 3.1). Box cores were collected in April 1997 from 35 and 60 m

water depths (stations F35 and E60). After retrieval, each box core was examined for

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. disturbance, and was recognized as undisturbed if the overlying water was clear and

surface tracks and open burrows were visible. Subsamples from each box core were

obtained with 7-cm diameter plastic tubes and sliced at 1-cm intervals. Approximately

half of these 1-cm slices became the primary samples for this study. Selected samples

were washed over a 63 pm sieve and dried. The resulting residuum was split with a

microsplitter to provide an aliquot of approximately 300 shells of benthic Foraminifera.

All of these specimens were picked and identified to the specific level.

Species diversity was assessed through two measures computed from the

foraminiferal counts: (I) species richness (S), i.e., the number of species present in the

sample or aliquot, and (2) Shannon Wiener Index given by the equation H(S) = -Zpilnpi,

where pt is the proportion o f the i**1 species. Simple linear regression (SLR) and

multivariate analyses (Cluster analysis, Principal Component Analysis) of foraminiferal

data were performed in order to better understand the historical changes of the

composition of the benthic foraminiferal community. Absolute ages of samples were

estimated based on rates of accumulation calculated through 210Pb dating techniques (R.

E. Turner, personal communication). A few characteristics of sediments in Louisiana

Bight make the 210Pb analysis a reliable technique for determining the accumulation rates.

(1) high deposition rates (> 1 mm/yr); (2) shallow mixed surface zone (< IS cm); (3)

increased proportions of silt and clay (> 40%). The effect of bioturbation is negligible;

the benthic community identified at a 20-m water station in the Louisiana Bight was

dominanted by small, opportunistic polychaetes, rather than mature, deep-burrowing

organisms (Rabalais et al., in press; personal communication). Thus, in all 2t0Pb profiles,

an extended radioactive decay region, found between the surface mixed area and the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. lower region of background activities, allowed the determination of sediment

accumulation rates (R. E. Turner, personal communication).

BACKGROUND: WORLDWIDE COASTAL AND OPEN SHELF HYPOXIA

Hypoxic and anoxic environments are not recent phenomena (Diaz and

Rosenberg, 1995) and they have an extensive occurrence in the marine realm (Bernhard

and Sen Gupta, 1999). Virtually all marine sediments lack oxygen at some depth below

the sediment-water interface. In fine grained coastal sediments, the thickness of the

aerobic zone underneath this interface may vary seasonally as a result of changes in

bottom water oxygen concentration and organic matter supply but will not exceed a few

centimeters (Rasmussen and Jorgensen, 1992 [in Moodley et al., 1998b]). Oxygen

profiles in the substrate of the southern North Sea and the northwestern Adriatic Sea

show that the oxygen penetration does not exceed 2 cm and 1 cm, respectively (Moodley

et al., 1998b).

Laterally extensive dysoxic environments exist in silled basins and fjords where

efficient water renewal is prevented by one or more sills that separate them from the open

ocean. Poor water circulation of Norwegian fjords seems to be the main factor controlling

hypoxia and anoxia in these areas where the most critical oxygen levels are reached

during November (Rygg et al., 1985 [in Diaz and Rosenberg, 1995]). Silled fjords are

highly sensitive to high organic inputs that favor a high level of biologic activity which in

turn may trigger an excessive oxygen consumption. When oxygen consumption exceeds

the supply, especially during the warm summers, bottom water oxygen concentration

may become critical for sustaining life. Thus, periodic seasonal or even permanent

hypoxia may occur. A decline of the yearly minimum oxygen concentrations in fjordic

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. areas of western Sweden has been directly measured and/or inferred on the basis of

fauna! changes (reductions of total mean abundance and biomass, abundance and biomass

of mollusks and abundances of suspension feeders and carnivores) (Josefson and

Rosenberg, 1998; Josefson and Widbom, 1988, Leppakoski, 1968; Rosenberg, 1977 [in

Diaz and Rosenberg, 1995]).

The foraminiferal record of sediment cores from Drammensfjord and Frierfjord,

southern Norway, was studied in the context of a long-term development of anoxic

bottom waters triggered by increased supplies of waste products and domestic sewage

(Alve, 1991). In both areas, naturally oxygenated waters of the past are indicated by high

foraminiferal abundances, whereas gradually decreasing species diversity is correlated

with progressive depletion of oxygen concentration in the bottom waters (Alve, 1990,

1991, 1995b). The most abundant foraminiferal species found in DrammensQord,

Spiroplectammina biformis (agglutinated taxon), seems to tolerate low oxygen

concentrations (< 2 ml/1 = 2.86 mg/1) in the southern part of the fjord. Its widespread

distribution, however, is indicative of a wide environmental tolerance range (salinity: 20-

31.2 “/«,; temperature 3-16 °C; oxygen < 0 .5 -7 ml/1 (= 0.7 - 10 mg/1) (Alve, 1990). An

assemblage restricted to the oxygen depleted (< 2 ml/1 = 2.86 mg/l) waters in the middle

and southern parts of Drammensfjord is dominated by the hyaline species Stainforthia

fusifomis. S. jusifomis is virtually the only living taxon found in the black, H 2 S smelling,

organic-rich surface sediments ofFriefjord (Alve, 1990). Low foraminiferal species

diversity, especially in the proximity of the redox cline, was recorded in both living

populations and total assemblages. The analysis of agglutinated-calcareous species

relationship revealed that extremely oxygen deficient environments, with salinities

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. exceeding 30 °/00f support assemblages dominated by thin shelled calcareous forms,

whereas the combination of low pH-values and reduced salinity (< 20°/oo) seems to

prevent the development of calcareous assemblages in the shallowest parts of the

Drammensfjord (Alve, 1990).

In formerly anoxic environments of Drammensfj ord, it took more than one year

after reoxygenation before the area became suitable for new foraminiferal colonization

(Alve, 1995a). At this time, the foraminiferal standing crop doubled and four new species

appeared in the habitat. The first species that successfully recolonized the previously

anoxic areas was the hyaline Stainforthia fusifomis (Alve, 1995a).

Seasonal or periodic hypoxia has also been documented in coastal areas that

include estuaries and open continental shelves. Well known examples of such areas are

those of New York Bight, Long Island Sound, Chesapeake Bay, Gulf of Mexico, Adriatic

Sea, and Orinoco Paria Shelf (Boesch and Rabalais, 1991; Malone, 1991; van der Zwaan

and Jorissen, 1991; Welsh and Eller, 1991 [in Bernhard and Sen Gupta 1999]).

Worldwide increase of eutrophication associated with riverine input of sediments,

nutrients and organic detritus “has a profound effect and may lead to anoxic or dysoxic

conditions even at great distances from fresh water sources” (van Der Zwaan and

Jorissen, 1991).

Intense and widespread hypoxic events are rare in the New York Bight area,

which experiences frequent, but spatially limited hypoxia (Boesch and Rabalais, 1991).

However, an area of about 7000 km2 was affected by bottom water hypoxia in water

depths ranging from 18 to 50 m during the period June through September 1976

(Swanson and Sinderman, 1979). For two months, low dissolved oxygen concentrations

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (near zero) and the presence of H 2 S were common characteristics of the bottom waters

along the inner shelf of central New Jersey.

Chesapeake Bay is probably one of the best documented hypoxic areas, with

regard to spatial extent, controlling factors, and historical development A combination of

factors, including meteorology and the amount of fresh water runoff, controls the

magnitude of primary production and the stratification of water column, and through

these, the variable spatial extent and the severity of hypoxia and anoxia in the bay

(Officer et al., 1984; Seliger et al., 1985). Like the northern Gulf of Mexico, the

Chesapeake Bay receives a significant freshwater inflow with a high nutrient content that

has increased over time. Consequently, the spatial extent of hypoxia has increased, with

the intrusion of hypoxic waters onto shallower bottoms (Officer et a., 1984, Seliger et al.,

1985; Seliger and Boggs, 1988). Hypoxic and anoxic conditions in Chesapeake Bay exist

every year from May through September, and are most severe during August. The

Susquehanna River discharges half of the freshwater entering the bay, and is responsible

for 70% of the nitrogen and 60% of the phosphorus loadings. High accumulations of

phytoplankton biomass during spring season trigger oxygen depletion and summer anoxia

(Malone, 1992).

Several indicators recorded in dated sediments from Chasepeake Bay were used

for reconstructing a long-term history of anoxia and eutrophication in the bay. Increased

sedimentation rates, anoxic conditions, and eutrophication were suggested by variations

in pollen, diatoms, organic carbon, nitrogen, sulfur, and an estimate of the degree of

pyritization of iron (Cooper and Brush, 1991,1993). A significant environmental change

recorded for the post European settlement period (from the early I ? 111 to early 18th

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. century) suggested anthropogenic influences on the watershed (Cooper and Brush,

1993). Deforestation was indicated by an incresae in ragweed pollen in sediments. A

large increase in sedimentation rates, increased amounts of organic carbon, nitrogen, and

sulfur in sediments, and a change in diatom species abundance and diversity documented

the shift to agricultural land use. More severe hypoxia and anoxia after about 1940 were

indicated by an increase of sulfur and the degree of pyritization of iron (Cooper and

Brush, 1993).

The historical record of benthic Foraminifera from Chesapeake Bay reveals a

significant change in the relative abundances of the species Ammonia parkinsoniana.

From being absent prior to the late 17th century, Ammonia parkinsoniana became the

most abundant species (80-90%) beginning in the early 1970s (Karlsen et al., 2000). y Deformed tests of A. parkinsoniana were found in samples representing the last three

decades of the century (Karlsen et al., 2000). The foramininferal record suggests that

limited oxygen depletion may have existed in Chesapeake Bay prior to the late 17th

century. Dysoxic and perhaps anoxic conditions have occurred during the last 200 years

and severe (spatially and temporally extended) anoxic conditions characterized the most

recent interval beginning in the early 1970s (Karlsen et al., 2000).

Long Island Sound is another well documented and large estuary characterized by

a pronounced seasonal water stratification in its western part (Riley, 19S6,1959;

Koppelman et al., 1976; Gordon, 1980). In contrast to the northern Gulf of Mexico and

the Chesapeake Bay, the stratification here is driven by summer temperature differences

rather than by salinity differences (Welsh and Eller, 1991). However, as in the Gulf of

Mexico and Chesapeake Bay, significant nitrogen and phosphorus loadings, mainly

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. discharged by East River, trigger algal blooms. During the summer season, western

waters become hypoxic with a severity peak in July-August, when thermal stratification

is most pronounced (New York State Department of Environmental Conservation and

Connecticut Department of Environmental Protection, 1999 [in Thomas et al., 2000]).

Historical trends of benthic foraminifera as related to the evolution of hypoxia

within Long Island Sound have been assessed by Thomas et al. (2000). The comparison

of total foraminiferal data collected in 1996 with those in Parker (1952) and Buzas (1965)

revealed a significant assemblage change. A decrease in the relative abundance of

Elphidium excavation clavatum towards western Long Island correlates well with a

strong increase in the relative abundance o f Ammonia beccarii. Also significant is the

decreasing trend of total assemblage species diversity as well as that of the relative

abundance of Eggerella advena. However, since the relative abundance of Eggerella

advena changed over the full east-west extent of Long Island Sound, a clear link between

this trend and hypoxia does not exist (Thomas et al., 2000).

The northern Adriatic Sea is under the influence of the freshwater discharge of the

Po River, the second largest river in Europe (Justic et al., 1995). High amounts of

nutrients and organic detritus supplied by the river into this shallow basin (< 50 m) fuel

significant algal blooms during the spring and summer seasons. Subsequently, especially

during the summer season when the water column is strongly stratified, the

decomposition of phytoplankton causes severe oxygen depletion (van der Zwaan and

Jorissen, 1991). There is a good correlation between the number of benthic Foraminifera

within the sediment and the oxygen concentration in the bottom waters (Jorissen et al.,

1992; Barmawidjaja et al., 1992). Opportunistic foraminiferal taxa, such as Bulimina,

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Valvulmeria, and Nonionella , can tolerate low oxygen concentration and thus, profit from

the high food availability (van der Zwaan and Jorissen, 1991).

SEDIMENTS AND BENTHIC FORAMINIFERA

The distribution of benthic foraminifera is intimately related to the sediments that

host them. Thus, the type of substrate, the amount and type of food in the substrate, the

types of material the sediment might provide for constructing tests, are all significant

factors. Important aspects of sediments are the relative amounts of clay, silt and sand; the

mobility of the substrate; the rate of accumulation; and the amount and composition of

organic detritus (Poag, 1981b). The major source of siliciclastic sediments in the Gulf of

Mexico is the Mississippi River, whose load, rich in silt, clay, and organic detritus,

reaches a very large portion of the Gulf that includes the deep water area (Mississippi

Fan), Sigsbee and Florida plains and the eastern half of the Texas-Louisiana shelf (see

Davies and Moore, 1970; Davies, 1972). A distinctive muddy substrate covers the eastern

Texas-Louisiana shelf, including our study area

Rates of sedimentation influence both living foraminifers and the preservation of

their tests after death. Very high rates of accumulation of muddy sediments are associated

with increased turbidity, which, by reducing the amount of light, reduces photosynthesis,

and thus may affect calcareous foraminifers that have symbiotic algae and all benthic

species that feed on and/or attach to marine plants. High rates of sedimentation, however,

ensure a rapid burial of foraminiferal tests after the death of the living organisms and

thus, contribute to a better preservation of the foraminiferal assemblage. Due to abundant

supply from the Mississippi River, the accumulation of sediments on the inner to middle

parts of the central Louisiana shelf and western areas reaches the maximum rates within

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the entire Gulf of Mexico (Curray, 1960). Lead 210 data from several cores in the area

affected by seasonal hypoxia yield rates of accumulation between a few millimeters and a

few centimeters per year (R. E. Turner, personal communication).

The rates of accumulation also influence our research strategy as well as the

interpretation of the fossil assemblages. In the northern Gulf of Mexico, the

extraordinarily high amounts of annual sediment accumulation facilitate detailed

microbiostratigraphic studies in which foraminiferal populations of even a single season

can be analyzed. Infaunal foraminifers populating the Louisiana continental shelf are

capable of surviving as deep as IS cm within the sediment (Platon and Sen Gupta, in

press). However, the number of living specimens (detected by Rose Bengal stain) found

below the depth of 7 cm becomes statistically insignificant when compared to the rest of

the assemblage. The downcore live/dead ratios varies with the sediment depth, whereas

station to station live/dead ratio can be correlated with the sedimentation rates and

perhaps the water depth. In addition, the correlation between the live/dead ratios and

sedimentation rates is influenced by the benthic foraminiferal life span that varies

between several months and two years (Lee and Anderson, 1991).

In a core located in 35 m water depth (F35), the average live/dead ratio for the top

7 cm of sediment is 0.12 with a maximum value of 0.23 reached at the depth of 2 cm, and

a minimum of 0.01 recorded for the deepest sample (7 cm). Figure 3.2 shows how many

new specimens will be added to a foraminiferal assemblage during the burial down to a

depth of 7 cm if, the live/dead ratios and the rate of sedimentation (0.71 cm/year - R. E.

Turner, personal communication) are those of F35 core, and foraminiferal life span is one

year.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Thus, changes of foraminiferal distribution patterns cannot be interpreted as being

exactly contemporaneous with the deposition of the sediments that contain the

assemblage. In most cases, depending primarily on sedimentation rates and foraminiferal

life span, these bioevents will be a few years younger than the age of the substrate.

Obviously, the lower the clastic sedimentation rates the greater the proportions of

foraminiferal tests that would represent populations younger than the encompassing

sediments. On the other hand, low sedimentation rates would negatively affect the test

preservation and thus obscure trends within the minor components.

Due to the lack of live/dead foraminiferal data in all the analyzed cores, I could

not determine the time gap between the sediment ages and those of the bioevents. Thus,

Dead + live specimens Time (years ago) — 9.9 80+20 — 8.5 mi 100+30 < 2 — 7.0 3 130+10 BS — 5.6 140+27 — 4.2 I 167+13 2.8 180+14 - l - 1.4 192+2

Figure 3.2. Dead and Live individuals during assemblage burial down to a depth of 7 cm (Station F35); Each box represents a foraminiferal assemblage accumulated within a 1 cm thick sediment layer. Almost 50% of Foraminifera in an assemblage retrieved from 7 cm below the sediment-water interface consist of individuals that have been added after the sediment deposition.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the ages for foraminiferal changes noticed in the data are considered the same as the

sediment 2t0Pb ages. However, I suggest that future studies concerned with short-term

foraminiferal changes may consider the proportions of live individuals in the computation

of bioevent ages.

SPECIES DIVERSITY

Plots of species richness for samples collected from 60 and 35 m water depth

locations are depicted in Figure 3.3 (A and B, respectively). Three intervals can be

distinguished within the distribution of species richness at the 60 meter station. During

the first interval, 1915-1936, a relatively high number (27-29) of benthic foraminiferal

species populated the habitat. Then species richness decreased steadily from 27 in 1936

to 12 in 1970 and remained somewhat constant at values that averaged 10.6 for the rest of

the investigated time interval (1970-1997). The decreasing trend of the number of

benthic foraminiferal species at station E60 was tested with simple linear regression

(SLR). This statistics, performed at 95 % confidence, explained 92% of the data

variability (correlation coefficient, r = 0.92) and showed that the species richness

increased with the core depth with a P (slope) value of 0.47. In the F35 core, species

richness decreased from 23 to 7 from 1943 to 1948 and remained somewhat constant with

an average of 8 during the subsequent period (1948-1997). The SLR for F35 could

explain only 30% of the data variability (species richness against depth). Thus, the

decreasing trend in species richness is not as evident as in core E60. In core F35,

however, the value recorded for the year 1943 stands clearly above values of all

subsequent years.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 35

30 J

2 5 -| (0 CO «> CM 20 cnoo a>f- 0 3 a0 3 0 3 15 0 3 in

10 inCM 5 0 3

10 20 30 40 50 Sample Depth (cm)

CO CO o 15 o>CO a. CM 0 3 CO 0 3 0 3 0 3

0 10 1520 2530 35 405 Sample Depth (cm) Figure 3.3. Species richness distribution through time; A: E60 core; B: F35 core.

Shannon-Wiener Index plots for E60 and F3S (Figure 3.4) show similar trends to

those noticed within the distributions of species richness. In 60 m of water the diversity

index decreased steadily from 2.29 in 1915 to 0.81 in 1997, whereas at the shallower

location (35 m) the value changed from 1.74 in 1943 to 1.31 in 1948, with a noticeable

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. minimum value around 1973. This drop in the Shannon-Wiener Index is due to a

significant reduction in the number of minor components. The regression analysis of E60

data showed with 95% confidence that diversity index increased downcore. The SLR’s

“best fit” explained 92% of the response variable. No significant pattern of diversity

change can be deciphered from the SLR analysis performed on the data from core F35.

2.5 I

00 CM 2J a>N- 0> a* x | s S » CO •5 -I o> O) 0» o>

e oo cm 1 0> I 0.5

10 20 30 40 50 Sample Depth (cm)

10 20 25 30 35 4015 Sample Depth (cm) Figure 3.4. Species diversity index (Shannon-Wiener) distribution through time; A: E60 core; B: F35 core.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. SPECIES DISTRIBUTION

Dom inant Species

Plots of the distribution of the most dominant species, Buliminella morgani,

Nonionella basiloba, and Epistominella vitrea, are depicted in Figure 3.5.

0> 0>CO 0.7 1 co M o> e o S o a Q. a a .

0.1

0 10 20 30 40 50 1-2] B

0.8 ^ tt e o o C o CL & a. 0.4 J

0.2 -

0 5 10 15 20 2530 35 40 Sample Depth (cm)

Legend: — N_basil — a— B_morg — E_vitr - a — All three

Figure 3.5. Dominant species distribution through time; A: E60 core; B: F35 core.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The sum of proportions of the most abundant species in the E60 ranges between 0.62 and

0.94 with an average of 0.86. An increasing trend of this sum is evident especially

between 1915 and 1945. A significant increase of the relative abundance of the species

Buliminella morgcmi between 1988 and 1997 is also noticeable. In F35, the sum of the

relative abundances of Buliminella morgani, Epistominella vitrea, and Nonionella

basiloba show an increasing trend between 1943 and 1955. Two somewhat significant

drops interrupt the plot of this sum in 1970 and 1976. During the second half of the

century, the three hyaline species make, on average, as much as 91% of the foraminiferal

assemblages in both of the cores.

Ammonia and Elphidium

The temporal distribution of Ammonia-Elphidiwm index (given by NA/(NA +

NE)X100, Sen Gupta et al., 1996) is provided in Figure 3.6. for core F35. No particular

120 n o>

100 h 0 5 0 5 CO 0 5 CO 0 5 0 5 0 5 CO oX 0 5 ■o 0 5 0 5 e 0 5 ^T 60 n T 0 5 111 to CO i < 0 5 'TCO CO 0 5 fx- CM 40 4 0 5 CO to 0 5 0 5 TTCO IO 0 5 to 0 5 20 -

0 5 10 1520 2530 35 40 Sample Depth (cm) Figure 3.6. Temporal distribution of Ammonia - Elphidium Index in Core F35; A-E index takes maximum values (100) in samples where no ElDhidium was found.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. trend of this index can be distinguished in core F35, except for nearly consistent high

values (p. 80%) since 1979. The index reaches maximum values (100) in several samples

towards the top of the core due to the lack of Elphidium specimens. Where both Ammonia

and Elphidium were absent, values are shown as zero. Only two specimens of Ammonia

parkinsoniana were found in the E60 core; there was no Elphidium.

Minor Components

Some species of benthic Foraminifera in E60 have low relative abundances but

they occur in a significant number of samples. The plot in Figure 3.7 shows the relative

abundance distributions of Bulimina marginata, Ccmcris sagra, Fursenkoina pontoni,

0.06

0.05

0.04 o>

£ 0.03 to 0.02

0.01

0 0 10 20 30 40 50 Sample Depth (cm) Legend: Uv_h_c -e-F_pont -*-B_marg

C_sagra —e—Sac. Drfi

Figure 3.7. Temporal distribution of the relative abundances of the species Bulimina marginata, Cancris sagra, Fursenkoina pontoni, Saccammina diflugiformis, and Uvigerina hispido-costata; E60 Core.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Saccammina diflugiformis, and Uvigerina hispido-costata. It is evident that the relative

abundances of all these species decreased especially between 1915 and 1945.

The distributions of the relative abundances of the species Bolivina lowmani and

Bulimina marginata from F35 core are plotted in Figure 3.8. These proportions are highly

variable through time.

0.12 i

0.08 -1 COo> * 0.06 i

0.04 j CO

0.02 i

0 5 10 1520 25 3035 40 Sample Depth (cm)

Legend: — BolJow -e — Bul_marg

Figure 3.8. Temporal distribution of the relative abundances of the species Bulimina marginata and Bolivina lowmani; F35 Core.

Quinqueloculina

A pronounced decline of the relative abundance of the porcelaneous genus

Quinqueloculina was observed in the core E60 (Figure 3.9). At this 60-m site, the

proportions of Quinqueloculina dropped from about 0.03 in 1915 to 0.0 in 1943.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.03

0.025 o>

0.02 « o> 0e 0.015 1 ao 0> 2 0.01 a. oo CM COCO a t 0.005 CM o>a> a» a> a>m

-0.005 Sample Depth (cm)

Figure 3.9. Distribution change in relative abundance of Quinqueloculina; Core E60.

0.04 n

0.035 -

0.03 -

CO 2 0.025

0.02 iS

o- 0.015 4 ata> 0.01 j a t 0> at a t 0.005 -i

0 5 10 15 20 25 30 35 40 Sample Depth (cm)

Figure 3.10. Distribution change in relative abundance Quinqueloculina; Core F35.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. At the shallower F3S station, Quinqueloculina is sporadically present, reaching a

proportion of about 0.03 in 1943 and proportions between 0.003 and 0.01 in the post

1975 period; it was absent in the 1948-1975 time interval (Figure 3.10).

DISTRIBUTION OF AGGLUTINATED AND PORCELANEOUS GROUPS

Agglutinated (Astrorhizida, Lituolida, Textulariida) and porcelaneous (Miliolida) orders

0.09 -

0.08

0.07 a> 0.06 n CM a> | 0.05

I 0.04

0.03 CM

0 10 20 30 40 50 Sample Depth (cm)

Figure 3.11. Distribution of agglutinated Foraminifera in core E60.

living in water depths between 35 and 60 m, suffered a noticeable decline, or even

disappeared, during the past century. In 60 meters of water, the proportions of

agglutinated species dropped from 0.08 in 1915 to 0.006 in 1943 (Figure 3.11), whereas

those of porcelaneous ones declined from 0.06 to 0.003 during the same time span

(Figure 3.12). During the subsequent period, up to 1997, both groups were very poorly

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. represented and they disappeared during the last few decades of the century. Even though

the historical record of benthic Foraminifera at the 35 m station is shorter than the one in

E60, reduced proportions of agglutinated and porcelaneous taxa are still apparent

(Figures 3.13. and 3.14). The relative abundance of agglutinated taxa was 0.06 in 1943

and 0.00 during the last decade of the century, whereas that of porcelaneous was about

0.04 in 1943 and, with one exception, 0.00 for the most part of the last decade of the

century.

0.07 -j

0.06 i

0.05 ]

o 0.04 J

2 0.03 -!

0.02 a t

o .o i i 5 a t CD

0 10 20 30 40 50 Sample Depth (cm)

Figure 3.12. Distribution change in relative abundance of porcelaneous species, Core E60.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0.07 i

0.06

0.05

o 0.04

g 0.03

CO 0.02 - a>GO CO O) oo a> 0.01 -I a> o>w O)o> ! ^ A 0 5 10 15 20 25 30 35 40 Sample Depth (cm) Figure 3.13. Distribution change in relative abundance of agglutinated species; Core F35.

0.03

0.025 f m

0.02 i CO o>CO § 0.015 a. oo

0.01 a t 52 0.005i 8 a t £ in

0 5 10 15 20 2530 35 40 Sample Depth (cm)

Figure 3.14. Distribution change in relative abundance of porcelaneous species; Core F35.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. COMMUNITY CHANGE

Foraminiferal data from the cores E60 and F3S were analyzed with the aid of

Cluster Analysis (CA). In addition, Principal Component Analysis (PCA) was used in the

analysis of the data set for the E60 core. In this core, three main clusters are apparent

(Figure 3.15). They correspond to the intervals 1915-1936, 1938-1978 and 1970-1997

that correlate well with the three time periods distinguished in the species richness

distribution plot. Major shifts in the benthic foraminiferal assemblage at this location

took place sometime within the 1936-1938 and 1978-1979 intervals.

- 1995-1997 1979-1981 I 1988-1990 J 1934-1936 1923-1925 — h i------1915-1917 III 1976-1978 1943-1945 1961-1963 1952-1954 1970-1972 I 1 1 1938-1940 z n — 0.0 0.2 0.4 0.6 0.8 1 Linkage Distance

Figure 3.15. Cluster analysis of E60 data; tree diagram for 12 cases; linkage procedure: Ward’s Method; correlation coefficient: Euclidean distance.

The CA for F35 core data (Figure 3.16) shows no meaningful grouping of the

sample collection. Nevertheless, at a closer look, one can notice that temporally

successive samples representing the 1970-1975 time interval belong to an isolated cluster

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. whose distance from the other groups is relatively high. This, once again, is due to a very

low representation of minor components in the corresponding samples.

0.0 0.5 0.1 1.5 2.0 2.5 Linkage Distance

Figure 3.16. Cluster analysis of F35 data; tree diagram for 33 cases; linkage procedure: Ward’s Method; Correlation coefficient: Euclidean distance The arrow points to the core bottom sample whose species richness differentiates it from the rest of the sample collection.

The core bottom sample whose species richness makes it different from the rest of

the sample collection has a somewhat isolated placement within the dendrogram. The

similarity between this sample and the group to which it was linked (1959,1960,1977) is

given by the absence of certain species rather than by a very similar taxonomic content It

is evident that the lack of any meaningful clustering of the foraminiferal data of F35 is

due to the shorter time interval covered by the analyzed samples. However, as shown by

the species richness, a possible shift of the benthic foraminiferal content could have taken

place prior to 1948. A longer foraminiferal record is needed in order to better determine

when such a shift occurred.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The scree plot of eigenvalues for E60 core data (Figure 3.17) reveals two

significant factors that account for 64.7% of the total variance. However, given the

relatively high proportion of variance (14.8%) explained by a third factor, it too was

considered. As seen in Table 3.1, factor 1 accounts for almost half of the total variance

(46.7%) and its “major parameters” (Table 3.1) are Nonionella basiloba, Uvigerina

hispido costata, Fursenkoina pontoni, Cancris sagra, agglutinated foraminifer

6.5 6.0 5.5 5.0 4.5 4.0 3.5 § I 2.5 2.0 1.5 1.0 0.5 0.0 0 1 2 3 4 56 7 8 9 10 11 12 13 Number of Eigenvalues

Figure 3.17. Scree plot for the eigenvalues for E60 core data. Arrow denotes the significant number of factors (points to level where curve’s slope change significantly).

Table 3.1. Eigenvalues for E 60 data; Extraction: Principal components.

Factor Eigenval Variance Eigenval % 1 5.6070398 46.725332 5.6070398 46.725 2 2.1608055 18.006713 7.7678454 64.732 3 1.7773271 14.811059 9.5451724 79.543

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. species (agglutinated), and Pyrgo and other porcelaneous taxa including Quinqueloculina

and Triloculina (Q/T - ina). Factor 2 accounts for 18% of total variance. Significant

loadings onto factor 2 are those of Buliminella morgani and Epistommella vitrea. Within

factor 3, Bulimina marginata, Bolivina lowmani, and other species o f Bolivina (B. spp),

show significant loadings (Table 3.2). Thus, most of the variability in the data set is due

Table 3.2. Factor loadings for 12 foraminiferal taxa in E60 core; Rotation: Varimax Normalized; Extraction: Principal components.

Taxa Factor Factor Factor 1 2 3 N. basiloba -0.71051 0.3475779 0.0676453 E. vitrea 0.1329909 0.7868568 -0.250877 B. morgani -0.066129 -0.947769 -0.102249 U. hispido costata 0.7395553 0.1880553 0.5665451 F. pontoni 0.7402202 0.2667797 -0.219597 B. marginata 0.0028491 0.4325385 0.7023258 C. sagra 0.9486338 -0.040595 0.0333846 B. lowmani -0.026707 0.2134872 -0.770596 B. spp. 0.3590785 -0.281262 0.7904396 Agglutinated 0.8520473 0.2180553 0.3812768 Pyrgo 0.7512396 0.1741379 0.5153114 Q/T - ina 0.8778652 0.0941215 0.3418745 Expl.Var 4.7123098 2.1449108 2.6879519 Prp.TotJ 0.3926925 0.1787426 0.223996

to changes in historical distribution of agglutinated, porcelaneous, and a few hyaline taxa.

It is noticeable that in E60, Buliminella morgani, perhaps the most opportunistic species

in the area of seasonal hypoxia of northwestern Gulf of Mexico (Blackwelder et al., 1996;

Platon and Sen Gupta, in press), has a significant loading onto factor 2 which accounts

for 18% of the total variance. Plots of loadings onto factor 1,2, and 3 (Figures 3.18 and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 3.3. Factor scores for 12 samples in E60 core.

Obs. Factor Factor Factor 1 2 3 1 -0.048191 -3.023071 -0.121067 2 -0.368304 0.8202798 -1.051938 3 -0.520913 0.6882466 -0.465986 4 -0.85864 -0.016316 0.2509972 5 -0.12036 -0.152501 -1.422886 6 -0.670037 0.141852 -0.56499 7 -0.840622 -0.160083 1.1244943 8 -0.68357 0.1101386 0.4775404 9 -0.211689 0.7416906 0.9235517 10 1.6443484 0.3358802 -1.535607 11 0.2702164 0.5065064 1.2350393 12 2.4077612 0.0073767 1.1508508

3.19) reveal similar behavior of the Fursenkoina pontoni, Cancris sagra, Uvigerina

hispido-costata, agglutinated species group, Quinqueloculina-Triloculina group and

Pyrgo. Their behavior is opposite to that of Nonionella basiloba.

1.2

0.8 e _ vttr

0.4 N.BASIL B_LOW UV_H_C

CM QJSAORA %a u. BOL_SPP

-0.4

- 0.8 m

- 1.2 - 1.0 - 0.6 - 0.2 0.2 0.6 1.0 1.4 Factor 1 Figure 3.18. Factor loadings; Factor l/Factor2; E60 core

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. without prohibited reproduction Further owner. copyright the of permission with Reproduced

Factor 3 Factor 3 - • 0.2 0.6 1.0 1.0 - Figure 3.19. Factor loadings; Factor l/Factor3 (A) and Factor Factor and (A) l/Factor3 Factor loadings; Factor 3.19. Figure 2/Factor 3 (B); E60 core. E60 (B); 3 2/Factor 12 08 04 . 04 . 1.2 0.8 0.4 0.0 -0.4 -0.8 -1.2 1.0 . ORG B.M B N_BASIL • - 0.6 - 0.2 BOL_SPP BJMORQ LOW B * B.MARG B.MARG * Factor 1 Factor TR IT V _ E C.SAQ RA N_BASIL N_BASIL RA C.SAQ Factor 2 • 72 t q BOL_SPP A° .A _ • PYRQO VHC • UV_H_C B.LOW F_PONT • l q • 0.6 PONT N O _P F SAGRA C e _ 1.0 tr it v • 1.4 Figure 320 depicts the temporal distribution of factor scores of factor 1 and factor

2 (data in Table 3.3). A change from positive to negative values of the scores of factor 1

took place in the later part of the fourth decade of the century, e.g. alter 1938. This trend

is related to the reduced abundances or even disappearance of taxa with positive scores in

younger sediments (Table 3.2). The scores of factor 2 vary less in time. However, a very

negative value of the score calculated for the top core sample is due to the high

abundance of Buliminella morgani associated with reduced proportions of Epistominella

vitrea and Nonionella basiloba . ,______2QQQ______, 1990 , 1980 .1 9 7 0 ai . 1960 E i— 1950 • 1940 1930 1920 • ______1910 -1.5 -1 -0.5 0 0.5 1 1.5 2 2.5 3 Factor scores

2000 _____ B 1990 1980 1970.* e 1960 E i— 1950 a 1940 » 1930 ' 1920 1910 * -3-2-1 0 1 Factor scores Figure 3.20. Plots of factor scores against time; E60 core, A. Factor 1; B. Factor 2.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ADDITIONAL DATA

Published and unpublished foraminiferal data (Blackwelder et al., 1996; Rabalais

et al., 1996) from two other nearshore cores (BL10 and G27) in the study area (water

depth 29 m and 27 m, respectively) were analyzed with the aim of better understanding

the foraminiferal response to seasonal hypoxia. Figure 3.21 depicts the temporal

distribution of the relative abundance of the genus Quinqueloculina in the G27 core (raw

data provided by Dr. B. K. Sen Gupta). The historical decline of this taxon and its

disappearance in the 1890s suggest progressively worsened environmental condition on

the Louisiana continental shelf. Trends similar to those observed in the data from E60

and G27 cores have also been noticed by Blackwelder et al. (1996). In the upper part

0.16

h 0.14

0.12

o 0.06 £

- 0.02

2000 1950 1900 1850 1800 1750 1700 1650 - 0.02 Time Figure 3.21. Distribution change in relative abundance of genus Quinqueloculina; core G27

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of their core (BL10 here), the miliolid species, Pyrgo nasutus, shows a decreasing trend

followed by disappearance. An upcore decrease of proportions of agglutinated species

was also noted.

Raw foraminiferal data of Blackwelder et al. (1996) were subjected to

multivariate analyses (C A and PCA). Results of Cluster analysis are depicted in

Figure 3.22. Two major clusters, placed at a relatively high linkage distance one from

1987 1973

1940 "U 19381931193819 V 1934.5 -> n 1933 -n 1929 1922 -n —1 1927.5 - J ‘1926 -r

0 5 10 15 20 25 30 35 40 Linkage

Figure 3.22. Cluster analysis of BL10 core data; tree diagram for SI cases; linkage procedure: Ward’s Method; correlation coefficient: Euclidean distance. 75

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. another, reveal a major microfaunal shift that took place sometime during the fifth decade

o f the 20th century.

Successive runs of PCA against foraminiferal data from BL10 core revealed the

existence of four factors that explain 68.32% of the total variance (Table 3.4). According

to the scree plot of eigenvalues (Figure 3.23), however, the first two factors, accounting

for 50.26% of total variance, are the most significant. Given some significant loadings on

the third and fourth factors, however, we chose to pay attention to these factors as well.

2 1

0 0 1 2 3 4 5 8 7 8 9 10 11 12 13 14 15 16 17 18 19 Number of Eigenvalues

Figure 3.23. Scree plot for the eigenvalues for the data from BL10 core (data from Blackwelder et al., 1996); Arrow denotes the significant number of factors.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 3.4. Eigenvalues for BL10 core data (data from Blackwelder et al., 1996); Extraction: Principal components.

Factor Eigenval % total Cumul. Cumul. Variance Eigenval % 1 6.975127 38.75071 6.975127 38.75071 2 2.071704 11.50947 9.046831 50.26017 3 1.659239 9.217992 10.70607 59.47817 4 1.591264 8.840354 12.29733 68.31852

Table 3.S. Factor loadings for 18 foraminiferal species from BL 10 core (data from Blackwelder et al., 1996); Rotation: Varimax Normalized; Extraction: Principal components.

Species Factor Factor Factor Factor 1 2 3 4 B. morgani -0.64443 -0.67949 -0.04239 -0.09684 E. vitrea 0.008331 -0.69939 -0.60564 0.023484 E. gunteri 0.218805 0.47532 0.55822 0.041476 B. lowmani -0.14123 0.337416 -0.58652 0.040451 A. parkinsoniana 0.220137 0.820384 -0.18493 0.132664 N. opima -0.85387 0.161868 0.02265 0.179732 A. pauciloculata 0.281875 0.696989 0.051267 0.031923 N. atlantica -0.05035 0.761433 0.122944 -0.0019 H. concentrica 0.239366 0.15558 0.762594 0.039075 A. parkinsoniana typica -0.13212 -0.22732 0.392379 -0.6875 Q. tanagos 0.803254 0.232209 0.123191 -0.00185 P. nasutus 0.523701 0.67358 0.1062 -0.11404 Q. bicarinata 0.398886 0.527317 0.05401 -0.31529 Q. poeyanum 0.138989 0.331983 -0.03012 -0.66056 8. irregularis 0.729607 0.156321 0.258504 0.194536 T. mayori 0.714906 0.423283 0.329993 0.099306 D. compressa 0.199352 0.164346 0.378003 0.652702 Q. horrida 0.658773 0.355881 0.294589 0.267591 Expl.Var 4.032517 4.384495 2.247846 1.632476 Prp.Totl 0.224029 0.243583 0.12488 0.090693

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 3.6. Factor scores for 49 samples in BL10 core (data from Blackwelder et al., 1996).

Factor 1 Factor 2 Factor 3 Factor 4 1 -0.48122 -1.08324 -111119 -0.08323 2 -1.67203 -0.16628 -0.33482 -1.43318 3 -0.42282 -0.97421 -1.76984 0.009264 4 -1.40853 0.21381 -0.26748 -0.12035 5 -1.53036 -0.36407 0.591225 -0.77603 6 0.181671 -1.34876 -2.48464 -1.38348 7 -1.30655 -0.08608 -0.41935 0.692406 8 -1.41997 -0.14399 -0.3072 -0.50098 9 -0.68901 -0.5705 -0.47208 0.405213 10 -1.3192 -0.08 2.116699 -2.44198 11 -1.51448 0.39729 -0.4136 0.642855 12 -1.04796 -0.04447 0.742137 1.135192 13 -1.72386 -0.34678 0.58157 0.938308 14 -0.48878 -1.36507 0.978647 0.181291 15 -2.13605 0.168625 0.244512 -0.82407 16 -0.35472 -1.1742 -1.18195 0.600629 17 -0.61035 -0.99993 -0.10784 -0.19373 18 -0.68481 -0.84634 0.24758 -0.12746 19 -0.27682 -0.61058 0.810591 0.907395 20 0.090429 -0.6559 1.41446 1.831858 21 -0.37714 -0.43625 -0.5132 0.643231 22 0.684288 -0.65607 -0.47642 0.223092 23 -0.0677 0.148944 1.373853 -0.21142 24 0.742861 -1.10498 0.124675 0.367363 25 0.572107 -1.0469 0.320976 0.262355 26 0.885904 -0.36226 -0.16871 0.967205 27 1.891137 -1.25614 0.511665 -0.23981 28 1.782352 -1.0635 0.114132 0.104459 29 1.353399 -0.70162 1.570027 -0.21255 30 1.726832 -1.23569 0.261685 0.339893 31 1.138749 -0.53175 0.570417 0.268557 32 1.041035 -0.03209 -1.57777 -1.71329 33 0.836588 -0.0158 0.700937 0.988924 34 0.527275 1.136862 -1.70006 -0.58794 35 0.541232 0.799493 -0.92688 0.488483 36 0.688044 -0.06644 1.22701 -1.78784 37 0.89621 0.071353 0.855234 0.412464 38 0.027184 1.836092 0.356473 0.341922 39 -0.23034 1.686524 1.493817 0.737099 40 0.196358 1.531756 1.059462 0.682319 41 0.310973 1.483433 -0.57999 1.095502 (Table 3.6 continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 42 0.689159 0.918724 0.932401 -0.27179 43 -0.29699 1.686597 0.027225 -0.74207 44 1.373385 1.536641 0.6165 -3.50543 45 0.245668 0.140052 -1.00889 -1.0039 46 0.511454 2.480361 -1.35689 0.784564 47 0.103366 1.414932 -0.8069 1.280516 48 0.43289 1.535738 -0.28962 0.464566 49 0.58913 0.182699 -1.56859 0.363617

1.0 AMM PARK NON ATL IV 0.6 ELPH_EXC # j BRIZ LOW 5•r ® d \ \ Q_TANA 0.2 HANZ CON BIG IR t

CM ok— TS u.co I/I P TV - 0.2 • /

- 0.6 BULL.MOI E P IS T J/l' m

- 1.0 - 1.0 - 0.6 - 0.2 0.2 0.6 1.0 F a c to r 1 Figure 3.24. Factor loadings; Factor 1/Factor 2; core E60.

Factor 1, the most significant one, accounts for 38.75% of the total variance

whereas factor 2 accounts for 11.51 % of the variance. Less significant factors, 3 and 4,

account for 9.22 % and 8.84 %, respectively, of the total variance (Table 3.4). Important

high loadings of considered variables (foraminiferal species) onto factor 1 are those of

Buliminella morgani, Nonionella opima , Quinqueloculina tanagos, Bigenerina

irrelgularis, Textularia mayori, and Quinqueloculina horrida (Table 3.5.). Among

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. loadings onto factor 2, those of Buliminella morgani, Epistominella vitrea, Ammonia

parkinsoniana, A. pauciloculata, Nonionella atlantica, and Pyrgo nasutus show

significant (> 0.6) values. The next two sets of loadings comprise few meaningful loads,

-2096-

0 E

-3 -2 -1 0 1 2 3 Factor Scores

------2 0 0 0 —|------B 1 • •

• % e • A IflfiA ...... e...... e V;* e

** e • i s ...... m......

1 < v v k

------4 8 8 0 - •2-10 1 2 3 Factor Scores Figure 3.2S. Plots of factor scores against time; A. Factor 1; B. Factor 2; Core BL10.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Epistominella vitrea, Hanzawaia concentrica (factor 3), and. Ammonia parkinsoniana-

typica (factor 4). [Taxonomic note: “ Ammonia pauciloculatcT of Blackwelder et al.

(1996) may have been included within yl. parkinsoniana in this study, because the

distinction is subtle and controversial. However, this question cannot be answered

without comparing specimens or illustrations (B.K. Sen Gupta, personal

communication).]

Blackwelder et al. (1996), noticed that historical changes of the foraminiferal

relative abundances in core BL10, including an increasing trend of the species

Buliminella morgani, match the increased use of the fertilizer in the United States, which

can be related to the seasonal hypoxia. Considering these observations and the high

(negative) loading of B. morgani, we infer that the factor I measures differences in

60 -

40 - 1 i 30 ^ £

1880 1900 1920 1940 1960 1980 2000 Time

Figure 3.26. U.S. fertilizer application (tons x 106) (data from SAUS 1991-1975; Berry and Hargett, 1997 [inNelsen et al., 1994])

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the data set that are controlled by environmental change mainly driven by the bottom

water oxygen content. This is also supported by the temporal distribution of scores of

factor 1 (Figure 3.25; data in Table 3.6) which matches that of fertilizer use in the United

States. Factor score values dropped significantly (from 1.76 to 0.78) in the early 1940s

and became negative in the mid 1950s. A rapid increase of fertilizer use begun in the late

1930s to early 1940s (see Figure 3.26).

The second meaningful factor, factor 2, may be related to oxygen depletion but

also to factors other than hypoxia. Long term environmental changes behind this factor

are suggested by the upcore trend of factor scores. Overall, these scores take positive

values for the first four decades of the century and most of them fall below zero in the

subsequent time interval. Abundant Epistominella vitrea specimens have been found

mainly in the Mississippi plume area (Blackwelder et al., 1996). The association of

Epistominella vitrea with areas characterized by high sediment loads is assumed to reflect

the capability of this species to tolerate rapid burial (Blackwelder et al., 1996). Thus, it is

possible that high loadings of Epistominella vitrea onto factor 2 may indicate that

changes in the data set distinguished in this projection can be related to the evolution of

the Mississippi River plume.

Factor 3 and factor 4, as mentioned earlier, explain less variance than factor 1 and

factor 2 explain. The data set variation measured by these two factors is perhaps related

to small scale environmental changes as well as to circumstances related to sample

collection and processing.

The fine structure of the data discussed herein can be analyzed on plots of factor

loadings. The plot in Figure 3.24 reveals the existence of a few foraminiferal groups that

have different behaviors along factor 1 and factor 2 axes. Group I ( Buliminella morgani

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and Nonionella opima) and group II ( Quinqueloculina tanagos, Quinqueloculina horrida,

Bigenerina irregularis, and Textularia mayori) have opposite behaviors along factor I

whereas group m ( Buliminella morgani and Epistominella vitrea) and group IV

(Nonionella atlantica, Ammonia parkinsoniana, A. pauciloculata, and Pyrgo nasutus) are

placed at the extreme ends of factor 2 axis. A fifth group is made of some hyaline and

porcelaneous species ( Brizalina lowmani, Ammonia parkinsoniana typica,

Quinqueloculina bicarinata, Q. poeyanum, Elphidium gunteri, Discammina compressa,

and Hanzawaia concentrica ) whose variations along both of the two axes are less

significant

HISTORICAL RECORD OF FORAMINIFERA: IMPLICATIONS REGARDING HYPOXIA

Species Richness and Diversity

Since most benthic Foraminifera are adapted to normal marine salinities, the

general trend of foraminiferal assemblages in modem shallow water is an increasing

species diversity along increasing salinity gradients and with increasing environmental

stability (Sen Gupta and Kilboume, 1974; Locklin and Maddoks, 1982; Alve, 1995b).

Low species diversities, i.e., assemblages consisting of few species that occur in large

numbers, generally indicate unstable environments (Lankford, 1959; Walton, 1964;

Gibson, 1966; Murray, 1971). Changes of species diversity as consequences of

environmental changes are frequently reported in the literature (Bandy et al., 1964a;

1964b; Alve, 1990,1995b; Nelsen et al., 1994; Blackwelder et al., 1996; Jannink et al.,

1998). It has been documented that certain hyaline taxa such as Bolivina , Bulimina,

Buliminella, Epistominella , Nonionella , Stainforthia, Valvulineria, and Uvigerina do

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. better than most of the other species within an assemblage under conditions of high

organic flux that may be accompanied by oxygen depletion (Alve, 1995a, 1995b; van der

Zwaan and Jorissen, 1991; Jorissen et al., 1992; Rathbum and Corliss, 1994, Blackwelder

et al., 1996).

The temporal distribution of two measurements of species diversity, Simpson

Index (B = I p 2 where pt = proportion of the community represented by species i) and

Shannon-Wiener Index, revealed an upcore decreasing trend in BL10 core (Blackwelder

et al., 1996). Three significant intervals were distinguished: (1) high values prior to the

mid 1930s, (2) consistently decreasing values from the mid 1930s to the mid 1950s, (3)

consistant low values for the post 1960 time interval.

Both species richness and Shannon-Wiener Index decreased upcore in samples

from E60 and F35 locations. Somewhat similarly to results in BL10, temporal

distribution of species diversity recorded in E60 can be divided into three intervals that

are characterized as follows: (1) relatively high diversity prior to the mid 1930s; (2)

decreasing species richness but relatively steady species proportions from the mid 1930s

to the early 1970s; (3) low and relatively steady species diversity from early 1970s up to

1997. In samples from F35 only one significant change of species diversity was recorded

for the interval 1943-1948. Species diversity was low and rather constant in the 1948-

1997 interval.

As noticed by Blackwelder et al. (1996), a relationship exists between

foraminiferal species diversity in core BL10 and fertilizer consumption in the U.S.

This suggests that the observed foraminiferal trends are direct responses to seasonal

hypoxia whose intensity became more critical after the 1940s. Furthermore, the

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. resemblance between the distributional pattern of species diversity in E60 and BL10 core

suggest that oxygen depletion extended over areas of deeper (60 meters) waters, although

less frequently.

Taxon Distribution

Dominant Species

Some of the taxa commonly reported from the northern Gulf of Mexico seem to

tolerate oxygen deficiency, and prefer organic rich sediments in other marine areas. Such

taxa are Bulimina marginata (Bandy et al., 1964b), Uvigerina peregrina (Miller and

Lohman, 1982; Lutze, 1980; van der Zwaan et al., 1986), Bolivina lowmani (Bizon and

Bizon, 1984), Fursenkoina (Seiglie, 1968,1971), Nonionella (Seiglie, 1968; Sen Gupta

and Machain-Casdllo, 1992), Cancris (Seiglie, 1968; Jonkers, 1984; van der Zwaan,

1983), Epistominella (Verhallen, 1987), and Buliminella (Bandy et al., 1964a, b, 1965).

In a previous study (Platon and Sen Gupta, in press), we showed that Buliminella

morgani dominates living assemblages of benthic Foraminifera from the sediment-water

interface down to a sediment depth of 5-10 cm, possibly in severely dysoxic, or even

anoxic, microhabitats. Given this adaptation, it is expected that the biostratigraphical

record would reveal an increasing trend in relative abundances of Buliminella morgani as

a consequence of progressive hypoxia

At stations G27 (Rabalais et al., 1996) and BL10 (Blackwelder et al., 1996), an

overall increase of the foraminiferal species Buliminella morgani [cited as Fursenkoina

pontoni in Rabalais et al. (1996)] has been related to the progression of the seasonal

hypoxia (Blackwelder et al., 1996; Rabalais et al., 1996; B.K. Sen Gupta, personal

communication). Three hyaline species, Buliminella morgani, Nonionella basiloba , and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Epistominella vitrea, dominate the foraminiferal assemblages throughout the cores F35

and E60 (see Figure 3.5). Furthermore, the sum of their relative proportions increased

steadily during the twentieth century, which probably reflects an opportunistic response

to progressive hypoxia on the Louisiana continental shelf.

Minor Components

The distribution of relative abundances of several foraminiferal species ( Bulimina

marginata, Cancris sagra, Fursenkoina pontoni, Saccammina diflugiformis, and

Uvigerina hispido-costata) identified from 60-m water-depth (station E60; see Figure

3.7) suggests a limited tolerance of these taxa to environmental changes that affected this

area of the Gulf. Most of these taxa have been identified in organic-rich, oxygen-deficient

environments in other marine areas. Their individual abundances of 2-5% before the

early 1940s dropped to less than 2% after 1945 and less than 1% in the last decade of the

century, perhaps because of their inability to compete with the opportunistic species

Buliminella morgani, Nonionella basiloba , and Epistominella vitrea.

Porcelaneous and Agglutinated Taxa Density Distribution

As seen so far, two major groups of benthic Foraminifera, agglutinated and

porcelanoeus, underwent significant historical changes at stations within the area of

present-day chronic hypoxia (G27, F35), but also in areas where direct water

measurements indicate a less intense oxygen depletion (E60). [Agglutinated foraminifera

construct their test with foreign particles selected by the organisms from the environment.

Porcelaneous foraminifers have the ability to secrete an imperforate calcific wall. In

* contrast, the hyaline taxa secrete a perforate calcific test]

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. On the continental shelf of Gulf of Mexico, abundant porcelaneous taxa exist

within what was called “miliolid predominance facies” (Poag, 1981b), and they are

widespread on the West Florida Shelf and Campeche Shelf (Poag, 1981b; Culver and

Buzas, 1981). An isolated strip of miliolid predominance facies occurs near the shelf

edge off Cape San Bias (Poag, 1981b). Species such as Quinqueloculina agglutinans, Q.

bicarinata, Q. bicostata forma typica , and Q. compta are abundant in this facies but are

also common in other facies with abundant miliolids, whereas other species such as Q.

bicostata forma garrettii, Q. collumnosa forma excavata, Q. crassa forma subcuneata, Q.

horrida , Q. parkeri forma occidentalism Spiroloculina antillarum forma crenulata, S.

soldanii forma dentata, S. soldanii forma typica , Triloculina tricarinata, T. trigonula, and

T. variolata are rare to common in the miliolid predominance facies and absent or rare

elsewhere (Poag, 1981). Agglutinated taxa such as Ammobaculites and Saccammina are

abundant in the “Saccammina-A mmobaculites predominant facies“ of Texas-Louisiana

shelf (Poag, 1981). Ammotium and Haplophragmoides are rare to common in shallow

waters on the continental shelf, whereas Goessela can be found only in the vicinity of the

Mississippi delta, where it is abundant and predominant in Goesella predominance facies

(Poag, 1981b). So, except for Saccammina and Ammobaculites, both agglutinated and

miliolid foraminifera are rare on the Texas-Louisiana shelf, which instead is populated by

abundant hyaline species.

Field and laboratory studies have demonstrated foraminiferal sensitivity to

changes in environmental conditions. In an area close to Puerto Jobos, Puerto Rico,

polluted by sewage outfalls, Ammonia tepida population has increased on account of

pollution, while Quinqueloculina rhodiensis has decreased (Seiglie, 1971). Living Q.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. rhodiensis represent 3% of the total living foraminiferal population, while living and

dead individuals of this species constitute 30% of the total assemblage (Seiglie, 1971).

Agglutinated foraminifers dominate the sediments of the silled and partially hypoxic

Drammensfj ord, where primitive taxa such as Ammodiscus, Astrammina,

Psammosphaera seem to endure the combined effect of strong river flow and easily

degradable organic matter (Alve, 1990). Spiroplectammina biformis, the most abundant

species in the area, can tolerate substantially reduced oxygen concentration (< 2 ml/1 =

2.86 mg/1). Nevertheless, a thin shelled, hyaline species, Stainforthia Jusiformis,

dominates the foraminiferal population closest to the redox cline (Alve, 1990). The

agglutinated species Eggerella adverta is able to compete with Elphidium excavatum

close to the Chesapeake-Elizabeth sewage outfall (Bates and Spencer, 1979). At Laguna

Beach and Hyperion outfalls, California, an increased dominance of hyaline species from

dead to live assemblages has been related to the augmented nutrient supplies (Bandy et

al., 1964a, 1964b, 1965). Furthermore, an overall increase in foraminiferal density was

recorded in the vicinity of the sewer outfalls as compared with other areas on the shelf

(Bandy etal., 1964a, 1964b, 1965).

Laboratory experiments on foraminiferal subsurface activity under oxygen-stress

conditions suggest that the miliolid species Quinqueloculina seminulum does prefer oxic

environments and has the ability of moving away from the anoxic sediment layers

(Moodley et al., 1998a). Another miliolid, Quinqueloculina impressa, used in an

experiment meant to measure the rate of vertical movement under different burial depths,

seems to move relatively fast in contrast to the other species present in the substrate

(Severin and Erskian, 1981). This can be seen as an adaptation of this species to escape

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. oxygen stressed microenvironments. Significant reduction of total assemblage densities

with time was recorded in laboratory experiments testing the tolerance of benthic

Foraminifera to prolonged H 2S exposure (Moodley et al., 1998b). Taxa such as

Textularia, Reophax, Quinqueloculina, Bolivina, and Bulimina were all negatively

affected by the sulfidic conditions, whereas densities of other genera, Staintforthia and

Hopkinskia , decreased to a lesser degree (Moodley et al., 1998b).

A decreasing trend of the genus Quinqueloculina followed by its disappearance

was recorded in both the area frequently affected by hypoxia (G27, F3S) and at the outer

edge of this zone (E60). The disappearance occurred between 1938 and 1945 in

60-m water depth and in the 1890s in 27 m of water. In 35 m of water, however,

Quinqueloculina was present in small proportions even after 1945. A relationship exists

between the disappearance of Quiqueloculina (important component of Recent

assemblages from only well-oxygenated environments) and the progression of the

seasonal hypoxia. Thus, at station G27 (Rabalais et al., 1996), the hypoxia sensitive

Quinqueloculina, whose highest proportion before 1900s reached 16% of the total

assemblage, was unable to compete with the hyaline taxa (favored by increasing carbon

fluxes to the seabed) and/or to cope with even slightly diminished oxygen concentrations

that might have existed at this location in the late 1800s and early 1900s. Possible

hypoxia in nearshore waters of Louisiana continental shelf prior to the 1900s was

suggested by the temporal trend of Ammonia-Elphidium Index in a few sediment cores

from the Louisiana continental shelf (Sen Gupta et al., 1996) The historical trends of the

relative abundance of genus Quinqueloculina observed at G27 and E60 stations suggest a

time gap o f40-50 years between seemingly similar biological events that took place in

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. both shallow and relatively deeper waters. Thus, it can be inferred that increased nutrient

amounts and oxygen depletion became critical for some foraminiferal species at station

E60 during the fifth decade of the twentieth century.

Even though Quinqueloculina disappeared at the location of E60 around 1944,

another miliolid ( Pyrgo) was present at this site for two more decades, thus making the

miliolid disappearance a two-stage event The distribution of the relative abundance of

the agglutinated Foraminifera in E60 and F3S agrees with that of the miliolid taxa in the

same cores. In E60, the decreasing trend recorded for 1915-1940 intensified during 1940-

1946, reducing the abundance of agglutinated foraminifera to almost zero for the rest of

the time span recorded in the core (until 1997). The pattern in the upper half of the E60

core is repeated in.the F35 core in which the samples represent a shorter time interval

(1943-1997). It can be thus inferred that both agglutinated and porcelaneous Foraminifera

responded to the progressive environmental change that included increased carbon fluxes

to the seabed and bottom-water hypoxia.

Assemblage Structure and Its Changes

Results of the two multivariate analysis procedures on foraminiferal assemblages

not only support the inferences made so far, but also bring further insight into

foraminiferal responses to progressive oxygen depletion in the northern Gulf of Mexico.

Three and two strati graphically-separated assemblages were found in cores E60 and

BL10 (Blackwelder et al., 1996), respectively. In E60, a more diverse and less dominated

foraminiferal assemblage is replaced by a more dominated one in the late 1930s - early

1940s, which in turn is followed by a high-dominance assemblage after the late 1970s.

This pattern matches the three stage foraminiferal evolution suggested by Blackwelder et

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. al. (1996) for the BL10 core and proves that similar environmental changes influenced

the foraminiferal composition at station E60. In the BL10 core, cluster analysis of

published data (Blackwelder et al., 1996) revealed a significant change in foraminiferal

composition that seems to have taken place in the middle of the twentieth century.

As seen before, the temporal pattern of faunas could be identified by Principal

Components Analysis. In 60 m water depth (station E60), significant loadings onto the

first factor (which apparently explains hypoxia-related variability in our data set) are

those of Nonionella basiloba, Uvigerina hispido-costata, Fursenkoina pontoni, Cancris

sagra, agglutinated species, Pyrgo, and the Quiqueloculina-Triloculina pair (Table 3.2).

The second axis (factor 2) is positively loaded by Epistominella vitrea and negatively

loaded by Buliminella morgani. The opposite trends of Buliminella morgani and

Epistominella vitrea (according to their loadings onto factor 2) may be environment-

related responses, but, to some extent, may as well be an artifact of sample processing.

Nevertheless, the overall increasing trend of the opportunistic B. morgani is inferred to

have resulted from changes of water quality (oxygen depletion). Five foraminiferal

groups are apparent in a factor 1/factor 2 plot (Figure 3.18). Group I consists of

Nonionella (N. basiloba ), group II of hypoxia -sensitive Uvigerina hispido-costata,

Fursenkoina pontoni, Cancris sagra, agglutinated species, Pyrgo and the

Quinquloculina-Triloculina pair, group HI of Buliminella morgani, group IV of

Epistominella vitrea, and group V of Bulimina marginata, Bolvvina lowmani, and

Bolivina spp. It is evident that most of the changes in the foraminiferal distribution

pattern at station E60 are due to increasing trends of the opportunistic species Nonionella

basiloba and Buliminella morgani and decreasing trends of miliolids, agglutinateds, and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. some sensitive hyaline forms such as Fursenkoina pontoni, Cancris sagra, and

Uvigerina hispido-costata. Taxa of group V are less affected by the environmental

changes.

As shown by scores of the first factor (Figure 3.20), the main turnover in the

historical record of foraminiferal assemblages in the E60 core takes place in the late

1930s, and is perhaps the result of an intensification of hypoxia at this station. No other

.significant change of factor score values can be distinguished post 1940, which is perhaps

due to the low-frequency occurrence of hypoxia in deeper-water areas.

The analysis of data from the BL10 core (Blackwelder et. al., 1996) showed that

the first axis is negatively loaded by Buliminella morgani, Nonionella opima, and

positively loaded by the miliolid species Quinqueloculina tanagos and Q. horrida, and

the agglutinated species Bigenerina irregularis and Textularia mayori. The main loadings

on the second axis were negative for Epistominella vitrea and positive for Ammonia

parkinsoniana, A. pauciloculata, and Nonionella atlantica. Thus, five foraminiferal

groups that responded differently to the environmental changes could be distinguished

(see Figure 3.24). Group I is made of two opportunistic species ( Buliminella morgani and

Nonionella opima ) that progressively replaced species belonging to group II

(Quinqueloculina tanagos, Q. horrida, Bigenerina irregularis, and T. mayori) when

oxygen depletion became critical at this station. Group m (.Buliminella morgani and

Epistominella vitrea) and group IV (Ammonia parkinsoniana, A. pauciloculata,

Nonionella atlantica , and Pyrgo nasatus) have opposite trends on the factor 2, which

perhaps is controlled by temporal changes of the Mississippi River plume as well as by

bottom water oxygen content The intermediate group V (Ammonia parkinsoniana

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. typica, Brizcdina lowmani, Discammina compressa, Elphidiim excavation, Hanzawaia

concentrica, Quinqueloculina bicarinata, and Q. poeyanum) consist of foraminifers

whose response to the major environmental controlling factor, bottom water oxygen

content, is less significant. Considering the suggested environmental importance of

Ammonia and Elphidium, it should be mentioned that the overall loadings of Ammonia

parkinsoniana and Elphidium gunteri (we consider this taxon to be synonymous with E.

excavation) indicate that the former taxon suffered a less severe temporal decline than the

latter. This supports an earlier conclusion of Sen Gupta et al. (1996), i.e., Ammonia is

more tolerant to hypoxia than Elphidium. The temporal distribution of factor 1 scores

(Figure 3.21) is similar to that obtained for the E60 data set Thus, a major drop in score

values occurred in the late 1930s, which perhaps indicates a change in hypoxia severity.

Results of PCA on the Blackwelder et al. (1996) data support our findings in E60 core.

Thus, it is evident that the relative proportions of the few major hyaline components

([Buliminella, Nonionella, and Epistominella) responded positively to the environmental

changes affecting both the shallower (about 30 m) and the deeper (60 m) waters in the

northern Gulf of Mexico. Furthermore, some agglutinated and porcelaneous taxa suffered

a significant decline during the last 100 years.

Foraminiferal Indicators of Hypoxia

It has been shown that some foraminifer species might be facultative anaerobes.

Among them, Ammonia parkinsoniana and Elphidium excavation may survive in anoxic

conditions, at least for a very short time (Moodley and Hess, 1992; Kitazato, 1994).

Moreover, the abundant occurrence o f Ammonia parkinsoniana in polluted, organic rich

sediments in Puerto Rican bays and lagoons correlated with the absence of Elphidium

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Seiglie, 1975), and the dominance of A. parkinsoniana over £ excavation in the surface

sediments of the shallow Gulf of Mexico dining maximum hypoxia (Sen Gupta et al.,

1996) suggests a better adaptation of the former species as compared to the latter one.

The Ammonia-Elphidium index was proposed as a proxy measure for hypoxia by Sen

Gupta et al. (1996). Three characteristics of Ammonia and Elphidium make the A-E index

a valuable hypoxia indicator: (1) both survive hypoxic conditions; (2) one ( Ammonia ) is

more tolerant than the other ( Elphidium ); and (3) both are common in shallow waters of

the continental shelf (see Poag, 1981b). However, the use of these two taxa as hypoxia

markers in waters deeper than 30 meters becomes unreliable because of their sparseness.

As mentioned before, only two specimens of Ammonia and none of Elphidium were

found in E60 core. Nevertheless, given the trends we have seen so far, two major groups

of benthic Foraminifera, i.e., agglutinated and porcelaneous taxa, may constitute

indicators of oxygen depletion in waters deeper than 30 meters. Plots of the sum of the

abundances of these two groups in cores from E60, F35, and BL10 stations show a

decreasing trend of what may be termed the Agglutinated-Porcelaneous Index (A-P

Index = % A + % P) (Figure 3.27).

The distribution of A-P index in BL10 core coincides with the distribution of

glauconite concentrations (clay mineral associated with anoxic environments in shelf

settings) (Nelsen et al., 1994) and that of the use of the fertilizer in the United States. The

decrease of A-P index throughout the twentieth century also parallels the rise in the

concentrations of biogenic silica (BSi) (a good indicator of in situ diatom production)

recorded in dated sediments from several locations in Louisiana Bight (27,50,35, and 60

m water depths) (Turner and Rabalais, 1994; Rabalais et al., 1996). It can be thus

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. inferred, that the severe decrease of A-P index after the early 1940s is related to the

oxygen depletion at the three analyzed stations.

18 30 16 14 25 5 12 20 ■g 10 15 ? ® 6 < CO 10 o>. 4 5 2 0 0 Time Time

CO T"3

X O) ■oc Q. < 4 o> * a> o>

Time

Figure 3.27. A-P index at stations BL10 (A), E60 (B) and F35 (C);

Model of Foraminiferal Response to Progressive Hypoxia in the Northern Gulf of Mexico

Historical data of foraminiferal distribution in four cores from the northern Gulf

of Mexico in water depths between 27 and 60 m [G27, BL10 (Blackwelder et al., 1996),

F35, and E60] allowed us to construct a model of the foraminiferal response to

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. progressive hypoxia (Figure 3.28). In this three-stage model that focuses on the last one

hundred years of foraminiferal change, we distinguish an early-hypoxia, a mid-hypoxia,

and a Iate-hypoxia period. The above terms are intended to reflect the placement of the

three periods within the twentieth century. As shown by previous studies (Rabalais et al.,

1996, Sen Gupta et al., 1996), some foraminiferal trends suggest the existence of hypoxia

prior to the 1900s. Relatively stable foraminiferal assemblages consisting of hyaline,

porcelaneous, and agglutinated taxa in proportions of about 80-90%, 5-10%, and 5%,

respectively, characterize the first four decades of the twentieth century. During the next

three to four decades, a progressive increase of hyaline taxa at the expense of

porcelaneous and agglutinated groups appears to be related to an increase of hypoxia in

the northern Gulf of Mexico. Stable but impoverished foraminiferal assemblages, highly

dominated by hyaline taxa (mainly Nonionella , Buliminella, and Epistominella),

characterize the end of the century when direct measurements of the bottom water

oxygen content proved the existence of a severe hypoxia (e.g., Rabalais et al., 1990,

1991). In shallow waters, the Ammonia-Elphidium Index increased throughout the

century.

Although the overall pattern of foraminiferal change in shallow waters (29

meters) is similar to that in deeper waters (60 meters), some differences regarding relative

abundances of all foraminiferal groups are evident Water depth and different hypoxia

frequencies seem to be the major factors responsible for these differences.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 3.28. One-hundred-year foraminiferal change in the northern Gulf of Mexico; curves represent overall trends of: Ammonia-Elphidium Index (red), Agglutinated - Porcelaneoues Index (green), hyaline taxa abundances (purple); SEM micrographs indicate species richness distribution.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CONCLUSIONS

1. On the Louisiana continental shelf, the change in the intensity of hypoxia in the

late 1930s and early 1940s, as well as its further development are suggested by the

distribution pattern of species diversity index, species richness, and relative abundances

of agglutinated and porcelaneous taxa, and by the changes of the total assemblage

structure. The temporal distribution of species diversity recorded in samples from 60 m

water depth can be divided into three intervals: (1) relatively high diversity prior to the

mid-1930s; (2) decreasing species richness but somewhat steady species proportions from

the mid 1930s to the early 1970s; (3) low and relatively steady species diversity from the

early 1970s up to 1997. Relative abundances of agglutinated and porcelaneous groups

diminished severely in the last one hundred years. Several stratigraphically-separated

assemblages demonstrate the overall change of the foraminiferal composition in Recent

sediments from the northern Gulf of Mexico. Overall, the foraminiferal decline recorded

in the Louisiana Bight follows the increasing trend of nitrogen and phosphorus fertilizer

use this century in the United States (see Turner and Rabalais, 1991) and that of nitrogen

concentrations in the Mississippi and Atchafalaya Rivers (Rabalais et al., 1991). Long

term changes in proportions of nutrients in the Gulf of Mexico coastal waters resulted in

“an almost perfectly balanced nutrient composition” (Rabalais et al., 1996) that seem to

have favored an increase of overall productivity of the ecosystem which led to more

severe depletion of the bottom water oxygen (Rabalais et al., 1996).

2. Some hyaline taxa, mainly Nonionella , Buliminella and Epistominella , cope

well with the progressive oxygen depletion in the northern Gulf of Mexico, showing an

opportunistic behavior when abundances of agglutinated and porcelaneous foraminifers

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. are strongly diminished. The disappearance of Quinqueloculina (mainly known from well

oxygenated modem environments) seems to be related to the progression of the seasonal

hypoxia. Furthermore, the historical distribution of the genus Quinqueloculina suggests

that critical oxygen levels reached nearshore waters (station G27) towards the end of the

1800s, whereas similar conditions affected relatively deeper waters (station E60) only in

the mid 1900s. Several foraminiferal components such as Bulimina marginata, Cancris

sagra, Fursenkoina pontonim, Saccammina diflugiformis, and Uvigerina hispido-costata

show a limited tolerance to hypoxic conditions.

3. The similarity between the foraminiferal pattern recorded at 60-m water depth

and that recorded at 30-m water depth (BL10 core of Blackwelder et al., 1996) suggests

that hypoxia has worsened in the past century even near the outer edge of the present-day

zone of seasonal oxygen depletion. Foraminiferal trends observed at these two stations

match the temporal distribution of the fertilizer use in the U.S., showing the

anthropogenic contribution to progressive hypoxia in the last six decades of the twentieth

century.

4. The distribution pattern of the summed relative abundances of agglutinated and

porcelaneous groups (A-P Index) indicates an overall rise in oxygen stress (increasing

hypoxia) on the Louisiana continental shelf in water depths from 30 to 60 meters. The A-

P trends suggest a potential use of higher level taxa in tracing recent and ancient

hypoxia. Nevertheless, the reliability of the A-P index as a hypoxia marker should be

tested further. Future studies may attempt to correlate A-P distribution with that of

parameters such as %BSi and/or organic carbon.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 5. Results of this study demonstrate the utility of the foraminiferal record in

assessing the historical evolution of hypoxia on continental shelves and thus their

potential in deciphering similar but ancient phenomena. However, for gaining further

insight into changes of foraminiferal pattern and their relationships with hypoxia in the

northern Gulf of Mexico, longer stratigraphic records should be examined.

too

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX

Species Abundance Data for F35 and E60 Cores

F35 - Raw Data

Depth 0-1 cm 1-2 cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm 8-9 cm 9-10 cm Am m_park 5 1 3 8 4 4 10 7 6 A m tjsa ls 0 B o ljo w 13 12 6 24 15 11 2 12 14 16 B ig jtm g 0 Bol_venez Boijalb 2 Bol. sp 1 1 Bol_cf_frag B uljacul Bul_marg 3 3 2 1 12 2 6 1 2 B uljm oig 97 104 67 86 81 55 123 92 101 47 Cancris C a ssjsu b Dorothia 1 E lphjaxc 1 Elph_p Epist_vitr 55 77 162 81 163 80 99 96 105 85 F jaleg F ursjpont 5 1 1 3 2 H a n z jx n c Lagena Lent MUtojsp 1 Mil_warr 2 2 Non_basil 50 38 39 86 72 35 86 60 70 P yrgojobf Pull_bull Q Jam ark 1 1 Q jstr Q _ cfja m Q _sp1 Q _sp_And 2 R ect_adv S ip h ja tr 1 Sacc_difl Spirotoc 1 Sfgm oJB n Slq_dlst 1 Text_cand T Jrig 1 U Ja evis 1 8 1 2 1 U_peragr (F35 - Raw Data continued)

101

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 10-11 cm 11-12 cm 12-13 1 3 -1 4 1 4 -1 5 1 5 -1 6 1 6 -1 7 1 7 -1 8 1 8 -1 9 cm cm cm cm cm cm cm Am m_park 3 8 8 8 7 4 12 A m t_sals B o ljo w 3 14 12 12 6 1 1 4 B ig jrreg Bol_venez B oljolb Bol. sp B ol_cfJrag 1 B uljacul 1 1 Bul_marg 2 9 1 1 1 1 2 Bul_morg 80 136 123 123 117 9 138 228 229 Cancris C a ssjsu b 1 Dorothia E lphjB xc 1 2 2 3 5 Elph_p E p istjritr 73 106 130 130 138 5 23 20 F_eleg 4 4 Furs_pont 1 1 H am _conc Lagana 1 Lent M iliojsp Mtt_warr 2 Non_basll 65 66 47 97 3 3 42 22 Pyrgo_obl Pull_bull 1 Q Jam ark 1 Q jstr Q jsfJ a m Q _sp1 Q _sp_And R ect_adv Siph_aff Sacc_difl 1 2 Spiroloc Slgm oJU n S iq jB s t Taxt_cand T Jrig U Ja evis 1 1 1 U jx r o g r 1 (F35 - Raw Data continued)

102

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 19-20 cm 20-21 cm 2 1 -2 2 cm 22 - 23 cm 2 3 -2 4 cm 2 4 - 2 5 cm 25 - 26 cm 2 6 -2 7 cm Am m_park 6 7 1 1 5 3 A m t_sals B o tjo w 2 1 8 17 46 28 26 B ig jn e g Bot_venez 1 1 1 Bof_alb B o L sp 1 1 Bol_cf_ftag B uljacul B u ljn a tg 4 2 2 1 3 Bul_morg 2 47 87 81 188 264 187 177 Cancris C a ssjsu b Dorothia E lphjaxc 1 18 2 1 2 1 Elph _p Eplst_vitr 6 35 21 76 135 244 249 208 F ja leg 1 3 Furs_pont 1 2 H a m jso n c Lagena Lent m to js p Mil_warr Non_basil 11 62 113 90 144 75 96 75 Pyrgo_obl PuB_bull Q Jam ark Q jstr Q _ cfja m Q js p l Q _sp_And R act_adv 1 S lp h ja ff 1 1 Sacc_dif1 1 2 1 Spiroioc Sigm oJIin S lg jiis t T extjsa n d T Jrig U Ja evis 2 2 U_peregr (F35 - Raw Data continued)

103

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 27 - 28 cm 2 8 -2 9 cm 2 9 -3 0 cm 31 • 32 cm 34 - 35 cm 37 - 38 cm A m m ja r k 1 6 4 10 A m t_sals 3 1 B o ljo w 6 6 4 3 8 5 B ig jrreg 2 2 Bol_yenez 6 B oljalb So/, sp 1 1 1 B o IjsfJra g B uljacui 1 B u tjn a rg 1 1 1 1 B u ljn o rg 98 136 123 184 93 159 Cancris 1 C a ssjsu b Domthfa E lphjaxc 4 1 6 Elph_p 1 E p istjritr 78 97 100 79 65 167 F jateg 1 Furs_pont 1 2 H a m jso n c S Laguna Lent 1 2 M ttiojsp MH_warr Non_basil 61 62 38 52 28 69 Pyrgo_obl 2 Pull_bull Q Jam ark 4 Q jstr 1 Q jcfJa m 1 Q js p l 5 Q _sp_And R a ctja d v S lp h ja tf 1 5 S a c c jB fl 1 1 Spim loc Slgm oJBn 5 S ig jU st T extjsan d 1 17 T Jrig U Jaavis U jx r e g r

104

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. F35 - Relative Proportions

Depth 0-1 cm 1-2 cm 2-3 cm 3-4 cm 4-5 cm 5 -6 cm 6-7 cm 7-8 cm Amm_park 0.0226244 0.0042017 0.0107143 0.0276817 0.011396 0.0203046 0.0307692 0 Am t_sals 0 0 0 0 0 0 0 0 B o ljo w 0.0588235 0.0504202 0.0214286 0.083045 0.042735 0.0558376 0.0061538 0.0444444 B lg jrreg 0 0 0 0 0 0 0 0 B ol_vanez 0 0 0 0 0 0 0 0 B oljalb 0 0 0 0 0 0 0 0 Bot-sp. 0 0 0 0 0 0 0.0030769 0.0037037 Bol_cf_ftag 0 0 0 0 0 0 0 0 B uljacui 0 0 0 0 0 0 0 0 B u tjn a rg 0 0.012605 0.0107143 0.0069204 0.002849 0.0609137 0.0061538 0.0222222 B u ljn o rg 0.438914 0.4369748 0.2392857 0.2975779 0.2307692 0.2791878 0.3784615 0.3407407 Cancris 0 0 0 0 0 0 0 0 C a ssjsu b 0 0 0 0 0 0 0 0 Dorothla 0 0 0 0.0034602 0 0 0 0 E lphjaxc 0.0045249 0 0 0 0 0 0 0 Elphj> 0 0 0 0 0 0 0 0 E plstjritr 0.2488688 0.3235294 0.5785714 0.2802768 0.4643875 0.4060914 0.3046154 0.3555556 F jaleg 0 0 0 0 0 0 0 0 F u rsj)o n t 0 0 0 0 0.014245 0 0.0030769 0.0037037 H anzjBonc 0 0 0 0 0 0 0 0 Laguna 0 0 0 0 0 0 0 0 Lent 0 0 0 0 0 0 0 0 M iliojsp 0 0 0 0 0 0 0 0 Mil_warr 0 0.0084034 0 0 0.005698 0 0 0 Non_basil 0.2262443 0.1596639 0.1392857 0.2975779 0.2051282 0.177665 0.2646154 0.2222222 Pyrgojabl 0 0 0 0 0 0 0 0 Pull_bull 0 0 0 0 0 0 0 0 Q Jam ark 0 0 0 0 0 0 0 0.0037037 Q jstr 0 0 0 0 0 0 0 0 Q jriJ a m 0 0 0 0 0 0 0 0 Q_sp1 0 0 0 0 0 0 0 0 Q _sp_And 0 0 0 0 0 0 0 0 Rect_adv 0 0 0 0 0 0 0 0 S lp h jr if 0 0 0 0 0 0 0 0 S a ccjd ifi 0 0 0 0 0 0 0 0 Slroloc 0 0.0042017 0 0 0 0 0 0 S ig m o jttn 0 0 0 0 0 0 0 0 S ig jd ist 0 0 0 0 0 0 0.0030769 0 Taxt_cand 0 0 0 0 0 0 0 0 T Jrig 0 0 0 0 0 0 0 0 U Jaevis 0 0 0 0.00346020.022792 0 0 0.0037037 U jperegr 0 0 0 0 0 0 0 0 (F35 - Relative Proportions continued)

105

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13cm 13-14cm 14-15 cm 15-16 cm Amm_park 0.0228013 0.0368098 0.012987 0.0234604 0.0284698 0.0243161 0.0188679 0.25 Am t_sals 0 0 0 0 0 0 0 0 B o ljo w 0.0456026 0.0981595 0.012987 0.0410557 0.0427046 0.0364742 0.0161725 0 B lg jrreg 0 0 0 0 0 0 0 0 B ol_venez 0 0 0 0 0 0 0 0 Bol_aIb 0.0065147 0 0 0 0 0 0 0 Bobsp. 0 0 0 0 0 0 0 0 Bol_cf_frag 0 0 0.004329 0 0 0 0 0 B uljacui 0 0 0 0 0.0035587 0.0030395 0 0 B u ljn a rg 0.0032573 0.0122699 0.008658 0.026393 0.0035587 0.0030395 0.0026954 0 B u ljn o rg 0.3289902 02883436 0.3463203 0.398827 0.4377224 0.3738602 0.3153639 0.5625 Cancris 0 0 0 0 0 0 0 0 C a ssjsu b 0 0 0 0 0 0 0 0 Dorothia 0 0 0 0 0 0 0 0 E lphjB xc 0 0 0 0.0029326 0.0071174 0.006079 0.0080863 0 E lp h j 0 0 0 0 0 0 0 0 E pistjrttr 0.3420195 0.5214724 0.3160173 0.3108504 0.4626335 0.3951368 0.3719677 0 F j l e g 0 0 0 0 0.01423490.0121581 0 0 F u r s jx n t 0.009772 0.0122699 0.004329 0 0 0 0 0 H anzjconc 0 0 0 0 0 0 0 0 Lagena 0 0 0 0 0 0 0 0 Lent 0 0 0 0 0 0 0 0 M iltojsp 0 0.006135 0 0 0 0 0 0 Mil_warr 0 0 0.008658 0 0 0 0 0 N o n jia sll 0.228013 0 0.2813853 0.1935484 0 0.1428571 0.2614555 0.1875 P yrgojabl 0 0 0 0 0 0 0 0 Pulljaull 0 0 0 0 0 0 0 0 Q Jam ark 0.0032573 0 0 0 0 0 0.0026954 0 Q jstr 0 0 0 0 0 0 0 0 Q jcfJa m 0 0 0 0 0 0 0 0 Q _sp1 0 0 0 0 0 0 0 0 Q _sp_And 0 0.0122699 0 0 0 0 0 0 R ect_adv 0 0 0 0 0 0 0 0 S l p h j f f 0 0.006135 0 0 0 0 0 0 S a c c jS b 0 0 0 0 0 0 0 0 Slroloc 0 0 0 0 0 0 0 0 S fg m o jlln 0 0 0 0 0 0 0 0 S lg jB s t 0 0 0 0 0 0 0 0 T extjaand 0 0 0 0 0 0 0 0 T Jrig 0.0032573 0 0 0 0 0 0 0 U Ja evis 0.0065147 0.006135 0.004329 0 0 0.0030395 0.0026954 0 U ja te g r 0 0 0 0.0029326 0 0 0 0 (F35 - Relative Proportions continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 1 6 - 1 7 cm 17-18 cm 18-19cm 19-20 cm 20-21 cm 21-22 cm 22-23 cm 2 3 -2 4 cm A m m jaark 0 0 0.0408163 0.2068966 0.0397727 0.0044444 0 0 A m tjsa ls 0 0 0 0 0 0 0 0 B o ljo w 0.0067114 0.0033333 0.0136054 0.0689655 0 0.0044444 0.0307692 0.0349076 B igjirreg 0 0 0 0 0 0 0 0 B ol_venez 0 0 0 0 0 0 0 0 Bol_alb 0 0 0 0 0 0 0 0 BoFsp. 0 0 0 0 0 0 0 0 Bol_cf_frag 0 0 0 0 0 0 0 0 B uljacui 0 0 0 0 0 0 0 0 Bul_marg 0 0.0033333 0.0068027 0 0.0227273 0 0.0076923 0.0041068 B u ljn o rg 0.9261745 0.76 0.7789116 0.0689655 0.2670455 0.3866667 0.3115385 0.386037 Cancris 0 0 0 0 0 0 0 0 C ass_sub 0 0.0033333 0 0 0 0 0 0 Dorothia 0 0 0 0 0 0 0 0 E lphjaxc 0 0 0.0170068 0.0344828 0.1022727 0.0088889 0.0038462 0 Elphj> 0 0 0 0 0 0 0 0 Epist_vitr 0.033557 0.0766667 0.0680272 0.2068966 0.1988636 0.0933333 0.2923077 0.2772074 F jaleg 0 0 0 0 0 0 0 0 Furs_pont 0.0067114 0 0 0 0 0 0 0 H a n z jx n c 0 0 0 0 0 0 0 0 Lagena 0 0.0033333 0 0 0 0 0 0 Lent 0 0 0 0 0 0 0 0 M lllojsp 0 0 0 0 0 0 0 0 Mil_warr 0 0 0 0 0 0 0 0 N on_basll 0.0201342 0.14 0.0748299 0.3793103 0.3522727 0.5022222 0.3461538 0.2956879 P yrgojabl 0 0 0 0 0 0 0 0 Pull_bull 0 0.0033333 0 0 0 0 0 0 Q Jam ark 0 0 0 0 0 0 0 0 Q jstr 0 0 0 0 0 0 0 0 Q jsfJ a m 0 0 0 0 0 0 0 0 Q_sp1 0 0 0 0 0 0 0 0 Q _sp_And 0 0 0 0 0 0 0 0 R ect_adv 0 0 0 0 0.0056818 0 0 0 S lp h ja ff 0 0 0 0 0 0 0 0.0020534 S a c c jM 0.0067114 0.0066667 0 0.0344828 0.0113636 0 0 0 Slroloc 0 0 0 0 0 0 0 0 Sigm oJIin 0 0 0 0 0 0 0 0 Sig_dist 0 0 0 0 0 0 0 0 T extjcan d 0 0 0 0 0 0 0 0 T Jrig 0 0 0 0 0 0 0 0 U Ja evis 0 0 0 0 0 0 0.0076923 0 U jie re g r 0 0 0 0 0 0 0 0 (F35 - Relative Proportions continued)

107

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 2 4 -2 5 cm 2 5 -2 6 cm 26 - 27 cm 2 7 -2 8 cm 28 - 29 cm A m m jp atk 0.0015699 0.0087413 0.0060241 0 0 A m tjsa ls 0 0 0 0 0 B o tjo w 0.0722135 0.048951 0.0522068 0.0242915 0.0197368 B iqjrrag . * 0 0 0 0 B ol_venez 0.0015699 0.0017483 0.002008 0 0 Bol_alb 0 0 0 0 0 Bol-sp. 0.0015699 0.0017483 0 0.0040486 0.0032895 B o ljiJ m g 0 0 0 0 0 B uljacul 0 0 0 0 0 B u ljn a rg 0 0.0017483 0.0060241 0.0040486 0.0032895 B u ljn o rg 0.4144427 0.3269231 0.3554217 0.3967611 0.4473684 Cancris 0 0 0 0 0 C a ssjsu b 0 0 0 0 0 Dorothia 0 0 0 0 0 E lphjBxc 0 0.0034965 0.002008 0 0 Elph_p 0 0 0 0 0 Epist_vitr 0.3830455 0.4353147 0.4176707 0.3157895 0.3190789 F_aleg 0.0015699 0 0.0060241 0.0040486 0 F u rsjx in t 0.0015699 0.0034965 0 0 0 H anzjconc 0 0 0 0 0 Lagena 0 0 0 0 0 Lent 0 0 0 0 0.0032895 M llb jsp 0 0 0 0 0 Mil_warr 0 0 0 0 0 Non_basil 0.1177394 0.1678322 0.1506024 0.2469636 0.2039474 Pyrgo_obl 0 0 0 0 0 P uIIJhjII 0 0 0 0 0 Q Jam atk 0 0 0 0 0 Q _str 0 0 0 0 0 Q _ cfja m 0 0 0 0 0 Q_sp1 0 0 0 0 0 Q jsp_A nd 0 0 0 0 0 R e c tja d v 0 0 0 0 0 Slph_aff 0 0 0.002008 0 0 Sacc_difl 0.0015699 0 0 0.0040486 0 Sirofoc 0 0 0 0 0 S lg m o jlin 0 0 0 0 0 Sigu& st 0 0 0 0 0 Text_cand 0 0 0 0 0 T Jrig 0 0 0 0 0 (JJaevis 0.0031397 0 0 0 0 U_peregr 0 0 0 0 0 (F35 - Relative Proportions continued)

108

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 29 - 30 cm 3 1 -3 2 cm 3 4 - 3 5 cm 37 - 38 cm Amm_park 0.0037175 0.0178042 0.0197044 0.0211416 Am t_sals 0 0 0.0147783 0.0021142 B o ljo w 0.0148699 0.0089021 0.0394089 0.0105708 B ig jn a g 0 0.0059347 0 0.0042283 Boi_venez 0 0 0 0.012685 Boljalb 0 0 0 0 Bol-sp. 0.0037175 0 0 0 Bol_cfJrag 0 0 0 0 B uljacul 0.0037175 0 0 0 B utjn arg 0.0037175 0 0 0.0021142 B u ljn org 0.4572491 0.5459941 0.4581281 0.3361522 Cancris 0 0 0 0.0021142 C a ssjsu b 0 0 0 0 Dorothia 0 0 0 0 B p h ja x c 0 0.0118694 0.0049261 0.012685 Elph_p 0 0 0 0.0021142 Epist_vitr 0.3717472 0.2344214 0.320197 0.3530655 F jaleg 0 0 0 0 F u rsjx jn t 0 0.0029674 0 0.0042283 Hanz_conc 0 0.0148368 0 0 Lagena 0 0 0 0 Lent 0 0 0 0.0042283 M iliojsp 0 0 0 0 Mil_warr 0 0 0 0 Non_basil 0.1412639 0.1543027 0.137931 0.1458774 Pyrgo_obl 0 0 0 0.0042283 Pull_butl 0 0 0 0 Q Jam ark 0 0 0 0.0084567 Q jstr 0 0 0 0.0021142 Q _ cfjam 0 0 0 0.0021142 Q_sp1 0 0 0 0.0105708 Q_sp_And 0 0 0 0 R ectja d v 0 0 0 0 S ip h ja ff 0 0.0029674 0 0.0105708 Sacc_dift 0 0 0 0.0021142 Sirotoc 0 0 0 0 Sigm oJIin 0 0 0 0.0105708 Sig_dist 0 0 0 0 Taxt_cand 0 0 0.0049261 0.0359408 TJrig 0 0 0 0 U Jaevis 0 0 0 0 U_peregr 0 0 0 0

109

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. E60-Raw Data

Depth 0-1 cm 4-5 cm 9-10 cm 11-12 cm 14-15 cm 19-20 cm N. basil 10 90 86 138 74 159 Ev#r 20 208 205 111 98 192 S. morgani 121 62 64 76 75 95 B. sp 1 1 0 0 0 0 U v.h-c 1 2 2 2 1 0 F .p o n t 4 4 4 3 4 B. marg 3 4 3 0 0 C. sagra 1 1 0 0 1 0 B. low 1 12 7 4 17 9 Un. 1 1 0 0 0 1 B. fragllls 1 1 8 6 9 7 B. striat 8 0 2 12 0 6 Sac. Dill 0 1 0 1 0 Fisa. E60 0 1 0 0 0 Bol.105 0 0 1 0 0 T ext sp. 0 0 1 0 0 T extcand 0 0 0 1 0 Fiss44 0 0 0 0 1 Palmula 0 0 0 0 1 L e n tsp 1 0 0 0 0 1 Pyr. c fo b l 0 0 0 0 1 P yr.P hlg 0 0 0 0 0 Am. c fp rk 0 0 0 0 0 M ag. Sp 0 0 0 0 0 Un. 2 1 0 0 0 0 0 U. bellula 0 0 0 0 0 Tritaxia 0 0 0 0 0 R ecto, adv 0 0 0 0 0 B ulsp. 0 0 0 0 0 Q .lam aick. 0 0 0 0 0 Ang. b eta 0 0 0 0 0 Am. Slsum 0 0 0 0 0 £. c f. Incart 0 0 0 0 0 S p iro kx 0 0 0 0 0 S ip h o a ff 0 0 0 0 0 A m m b. t 0 0 0 0 0 H am . 0 0 0 0 0 SlgschL 0 0 0 0 0 Fis. sp 2 0 0 0 0 0 B olbar 0 0 0 0 0 T trig 0 0 0 0 0 Q sp A n 0 0 0 0 0 Q cm pta 0 0 0 0 0 L e n sp A n 0 0 0 0 0 PsdClav mex 0 0 0 0 0 B o lsp 1 0 0 0 0 0 B o ls p 2 0 0 0 0 0 T ricsp 1 0 0 0 0 0 T rilsp 2 0 0 0 0 0 (E60 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. A m park 0 0 0 0 0 S ip h c fa ff 0 0 0 0 0 Q. cfv u tg 0 0 0 0 0 T rilsp 2 0 0 0 0 0 Q. un. 0 0 0 0 0 Slgm fBntii 0 0 0 0 0 Pmo 0 0 0 0 0 (E60 - Raw Data continued)

ill

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Depth 24-25 cm 29-30 cm 32-33 cm 34-35 cm 40-41 cm 45-46 cm N. basil 200 127 70 62 73 22 E. vitr 110 124 85 162 263 106 B. morgani 100 72 55 76 76 46 B .s p 0 2 1 U v.h-c 7 4 5 8 15 10 F .p o n t 8 2 3 19 3 9 B. marg 7 4 9 1 10 4 C. sagra 1 2 1 8 3 7 B. tow 0 1 7 12 Un. 1 0 B .fragilis 23 1 2 1 15 B .striat 14 12 8 7 28 29 Sac. Din 0 1 6 8 11 6 Fiss. E60 1 5 1 1 Bol.105 0 0 0 0 0 T extsp. 0 1 T axtcand 0 1 1 2 1 Fiss44 0 1 Palmula 0 1 4 1 L en tsp 1 0 P yr.cfo b l 0 2 2 3 5 P yr.P hlg 1 1 1 1 1 Am . cfp rk 1 Marg. Sp 1 1 U n.2 1 U. bellula 0 Tritaxla 0 1 R ecto, adv 0 1 1 B ulsp. 0 1 Q. tamarck. 0 0 1 1 3 2 Ang. balla 0 0 2 Am . Slsum 0 0 3 4 5 12 E. c f. Incart 0 0 1 1 1 Splrotoc 0 0 1 S tp fio a ff 0 0 0 2 3 2 A m m b . t 0 0 0 2 H am. 0 0 0 1 5 5 S ig schl. 0 0 0 1 F is .s p 2 0 0 0 1 Bol bar 0 0 0 1 T trig 0 0 0 1 3 4 Q sp A n 0 0 0 1 1 4 Q cm pta 0 0 0 3 L a n sp A n 0 0 0 1 PsdClav max 0 0 0 0 2 B o tsp 1 0 0 0 0 2 B o ts p 2 0 0 0 0 1 T ricsp 1 0 0 0 0 1 T rilsp 2 0 0 0 0 1 Am park 0 0 ■ 0 0 0 2 S lp h c fa ff 0 0 0 0 0 1 (E60 - Raw Data continued)

112

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Q .c fv u lg 0 0 0 0 0 1 TrH sp2 0 0 0 0 0 2 Q. u n 0 0 0 0 0 1 Slgm fRntii 0 0 0 0 0 1 Pyrgo 0 0 0 0 0 1

113

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. E60 - Relative proportions

Sample 0-1 cm 4-5 cm 9-10 cm 11-12 cm 14-15 cm 19-20 cm N. basil 0.0606061 0.2337662 0.2239583 0.3854749 0.2642857 03333333 £ vllr 0.1212121 0.5402597 0.5338542 0.3100559 0.35 0.4025157 B. morgani 0.7333333 0.161039 0.1666667 0.2122905 0.2678571 0.1991614 B. sp 0.0060606 0.0025974 0 0 0 0 Uv. h-c 0.0060606 0.0051948 0.0052083 0.0055866 0.0035714 0 F .p o n t 0 0.0103896 0.0104167 0.0111732 0.0107143 0.0083857 B. marg 0 0.0077922 0.0104167 0.0083799 0 0 C. sagra 0.0060606 0.0025974 0 0 0.0035714 0 B. k m 0.0060606 0.0311688 0.0182292 0.0111732 0.0607143 0.0188679 Un. 1 0 0.0025974 0 0 0 0.0020964 B. fragilis 0.0060606 0.0025974 0.0208333 0.0167598 0.0321429 0.0146751 B .stria t 0.0464848 0 0.0052083 0.0335196 0 0.0125786 Sac. Dill 0 0 0.0026042 0 0.0035714 0 F lss.E 6 0 0 0 0.0026042 0 0 0 Bol.105 0 0 0 0.0027933 0 0 T extsp . 0 0 0 0.0027933 0 0 T ext cand 0 0 0 0 0.0035714 0 Fiss44 0 0 0 0 0 0.0020964 Palmuta 0 0 0 0 0 0.0020964 L ent sp 1 0 0 0 0 0 0.0020964 Pyr. c fo b l 0 0 0 0 0 0.0020964 P yr.P hlg 0 0 0 0 0 0 Am. c fp rk 0 0 0 0 0 0 Marg. Sp 0 0 0 0 0 0 Un. 2 0.0060606 0 0 0 0 0 U. bellula 0 0 0 0 0 0 Tritaxia 0 0 0 0 0 0 R ecto, adv 0 0 0 0 0 0 B u lsp . 0 0 0 0 0 0 Q. lamarck. 0 0 0 0 0 0 Ang. balla 0 0 0 0 0 0 Am. Slsum 0 0 0 0 0 0 £ cf. Incett 0 0 0 0 0 0 Spkoloc 0 0 0 0 0 0 S fp h o a ff 0 0 0 0 0 0 A m m b . t 0 0 0 0 0 0 H am . 0 0 0 0 0 0 S ig scht. 0 0 0 0 0 0 F is .s p 2 0 0 0 0 0 0 Bo! bar 0 0 0 0 0 0 T trig 0 0 0 0 0 0 Q s p A n 0 0 0 0 0 0 Q cm pta 0 0 0 0 0 0 L en s p An 0 0 0 0 0 0 P sdC tavm ex 0 0 0 0 0 0 B o lsp 1 0 0 0 0 0 0 B o ls p 2 0 0 0 0 0 0 T ricsp 1 0 0 0 0 0 0 (E60 - Relative Proportions continued)

114

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. T rilsp 2 0 0 0 0 0 0 A m park 0 0 0 0 0 0 S ip h c fa lf 0 0 0 0 0 0 Q .c fvu lg 0 0 0 0 0 0 T rilsp 2 0 0 0 0 0 0 Q. un. 0 0 0 0 0 0 Sigmflintii 0 0 0 0 0 0 Pyrgo 0 0 0 0 0 0 (E60 - Relative Proportions continued)

115

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sample 24-25 cm 29-30 cm 32-33 cm 34-35 cm 4041 cm 4 5 4 6 c m N. basil 0.4210526 0.3547486 0.2651515 0.156962 0.1367041 0.0763889 £ vitr 0.2315789 0.3463687 0.3219697 0.4101266 0.4925094 0.3680556 B. morgani 0.2105263 0.2011173 0.2083333 0.1924051 0.1423221 0.1597222 B. sp 0 0.0055866 0 0 0.0018727 0 Uv. h-c 0.0147368 0.0111732 0.0189394 0.0202532 0.0280899 0.0347222 F .p o n t 0.0168421 0.0055866 0.0113636 0.0481013 0.005618 0.03125 B. marg 0.0147368 0.0111732 0.0340909 0.0025316 0.0187266 0.0138889 C. sagra 0.0021053 0.0055866 0.0037879 0.0202532 0.005618 0.0243056 B. low 0 0.0027933 0.0265152 0.0303797 0 0 Un. 1 0 0 0 0 0 0 B. ftagiUs 0.0484211 0.0027933 0.0075758 0.0025316 0.0280899 0 B .striat 0.0294737 0.0335196 0.030303 0.0177215 0.0524345 0.1006944 Sac. DU 0 0.0027933 0.0227273 0.0202532 0.0205993 0.0208333 Fisa. E60 0.0021053 0 0 0.0126582 0.0018727 0.0034722 Bel. 105 0 0 0 0 0 0 T extsp. 0 0 0 0 0 0.0034722 T extca nd 0 0 0.0037879 0.0025316 0.0037453 0.0034722 Flss44 0 0 0.0037879 0 0 0 Palmula 0 0.0027933 0 0.0101266 0.0018727 0 L e n ts p l 0 0 0 0 0 0 Pyr. c fo b l 0 0 0.0075758 0.0050633 0.005618 0.0173611 P yr.P hlg 0.0021053 0.0027933 0.0037879 0 0.0018727 0.0034722 Am. c fp rk 0.0021053 0 0 0 0 0 Marg. Sp 0.0021053 0.0027933 0 0 0 0 Un. 2 0.0021053 0 0 0 0 0 U. bellula 0 0 0 0 0 0 Tritaxia 0 0.0027933 0 0 0 0 R ecto, adv 0 0.0027933 0 0 0 0.0034722 B u lsp . 0 0.0027933 0 0 0 0 Q .lam arck. 0 0 0.0037879 0.0025316 0.005618 0.0069444 Ang. betta 0 0 0.0075758 0 0 0 Am . Slsum 0 0 0.0113636 0.0101266 0.0093633 0.0416667 £ cf. Incart 0 0 0.0037879 0 0.0018727 0.0034722 Spiroloc 0 0 0.0037879 0 0 0 S lp h o a ff 0 0 0 0.0050633 0.005618 0.0069444 A m m b. t 0 0 0 0.0050633 0 0 H am . 0 0 0 0.0025316 0.0093633 0.0173611 Sig sch l. 0 0 0 0.0025316 0 0 F is .s p 2 0 0 0 0.0025316 0 0 Bo! bar 0 0 0 0.0025316 0 0 T trig 0 0 0 0.0025316 0.005618 0.0138889 Q s p A n 0 0 0 0.0025316 0.0018727 0.0138889 Q cm pta 0 0 0 0.0075949 0 0 L e n sp A n 0 0 0 0.0025316 0 0 P sdC lavm ex 0 0 0 0 0.0037453 0 B o lsp 1 0 0 0 0 0.0037453 0 B o ts p 2 0 0 0 0 0.0018727 0 Trie sp 1 0 0 0 0 0.0018727 0 T tU sp2 0 0 0 0 0.0018727 0 Am park 0 0 0 0 0 0.0069444 S ip h c fa ff 0 0 0 0 0 0.0034722 (E60 - Relative Proportions continued)

116

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Q .cfvu lg 0 0 0 0 0 0.0034722 Trilsp2 0 0 0 0 0 0.0069444 Q. un. 0 0 0 0 0 0.0034722 Sigm ffintii 0 0 0 0 0 0.0034722 Pyrgo 0 0 0 0 0 0.0034722

117

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 4

FORAMINIFERAL COLONIZATION OF HYDROCARBON-SEEP BACTERIAL MATS AND UNDERLYING SEDIMENT, GULF OF MEXICO SLOPE*

*Barun K. Sen Gupta, Emil Platon, Joan MJternhard, and Paul Aharon; Published Journal of Foraminiferal Research, v. 27, no. 4 [p. 292 - 300], October 1997

118

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

Hydrocarbon seeps and vents of the Gulf of Mexico support unusual bathyal

biotas, including the large mat-forming bacterium Beggiatoa and chemosynthesis-based

communities of mussels, clams, and tubeworms (e.g., Brooks et al., 1987; MacDonald et

al., 1990; Sassen et al., 1993; Carney, 1994). Benthic foraminifers have been recorded

from microhabitats associated with these organisms (Sen Gupta and Aharon, 1994),

notwithstanding the severe depletion or absence of 02, and possible H 2 S toxicity,

immediately below the sediment-water interface. In addition, the initial distribution data,

restricted to surface sediments, indicated that among the seep-related habitats,

undisturbed bacterial mats support the denser and the most diverse foraminiferal

communities. The present study, based mainly on habitat observation and sampling in

Green Canyon in November 1995, is an inquiry into the vertical distribution and

adaptation of live Foraminifera in and under Beggiatoa mats.

SAMPLE COLLECTION, ON-BOARD PROCESSING, AND LABORATORY TECHNIQUES

The samples used for foraminiferal census and ultrastructure study (Table 4.1)

were collected from Beggiatoa mats and underlying sediments by coring at six dive sites

from the submersible Johnson Sea-Link II. Both box cores and push cores were taken at

the dive sites (Figure 4.1). The 15-cm wide and 18-cm high square coring box was

divided into four equal compartments, and designed to retrieve four undisturbed cores;

each of these cores (subcores in this report) had a 7-cm x 7-cm cross-section. Two kinds

of push cores, with inner diameters of 6.4 cm and 8.9 cm, were used.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The stabie-isotope data came from a different set of Green Canyon samples collected in

1989 and 1991 (Sen Gupta and Aharon, 1994).

Figure 4.1. Dive sites, indicated by Johnson Sea-Link dive numbers. See Table 3.1 for sample locations.

Table 4.1. Dive and sample information. Bsc = box subcore (sample volume 49 cc); pc = smaller push core (sample volume 32.2 cc); PC = larger push core (sample volume 62.2 cc); N = Number of foraminiferal specimens staining with Rose Bengal. Samples whose portions were removed for the ultrastructure study are indicated by asterisks. Sample 1l- 0 was used only for ultrastructure study. Dive No. Sample Coordinates Water Depth (m) Core Type Substrate depth N No. (N/W) (cm)

JSL2635 4-0* 27°44.259791018.012’ 587 Bsc 0-1 5 JSL2635 4-1 Same Same Bsc 1-2 21 JSL2635 4-2 Same Same Bsc 2-3 0 JSL2635 5-0 Same Same Bsc 0-1 21 JSL2635 6-0 Same Same Bsc 0-1 51 JSL263S 6-1 Same Same Bsc 1-2 28 JSL2635 6-2 Same Same Bsc 2-3 0 JSL2635 11-0* Same Same pc 0-1 - JSL2636 16-0 27°44.477'/91019.056’ 569 Bsc 0-1 19 JSL2636 16-1 Same Same Bsc 1-2 6 JSL2636 16-2 Same Same Bsc 2-3 15 JSL2636 16-3 Same Same Bsc 3-4 1 JSL2636 16-4 Same Same Bsc 4-5 3 JSL2636 17-0 Same Same Bsc 0-1 16 JSL2639 25-0* 27°44.519791°19.076' 568 Bsc 0-1 9 JSL2639 26-0 Same Same Bsc 0-1 22 JSL2639 26-1 Same Same Bsc 1-2 25 JSL2639 26-2 Same Same Bsc 2-3 1 (Table 4.1 continued) 120

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. JSL2639 26-3 Same Same Bsc 3-4 0 JSL2639 26-4 Same Same Bsc 4-5 0 JSL2639 28-0 Same Same Bsc 0-1 29 JSL2639 28-1 Same Same Bsc 1-2 13 JSL 2639 28-2 Same Same Bsc 2-3 14 JSL2639 28-3 Same Same Bsc 3-4 4 JSL 2639 28-4 Same Same Bsc 4-5 0 JSL 2639 35-0* 27°44.513’/91°19.10r 569 pc 0-1 15 JSL 2644 39-0* 27°44.515791°19.06T 570 Bsc 0-1 5 JSL 2644 40-0 Same Same Bsc 0-1 17 JSL 2644 40-1 Same Same Bsc 1-2 30 JSL 2644 40-2 Same Same Bsc 2-3 24 JSL 2644 40-3 Same Same Bsc 3-4 0 JSL 2644 40-4 Same Same Bsc 4-5 0 JSL 2644 42-0 Same Same Bsc 0-1 7 JSL 2644 49-1 Same Same pc 1-2 0 JSL 2647 52-0* 27°46.962’/91 °30.512’ 543 PC 0-1 5 JSL 2647 53-0 Same Same pc 0-1 35 JSL 2647 56-0* Same Same Bsc 0-1 9 JSL 2647 56-1 Same Same Bsc 1-2 28 JSL 2647 56-2 Same Same Bsc 2-3 2 JSL 2647 56-3 Same Same Bsc 3-4 0 JSL 2647 56-4 Same Same Bsc 4-5 0 JSL 2647 57-0* Same Same Bsc 0-1 5 JSL 2648 64-0 27°44.419791°19.189' 583 PC 0-1 59 JSL 2648 64-1 Same Same PC 1-2 14 JSL 2648 64-2 Same Same PC 2-3 3 JSL 2648 64-3 Same Same PC 3-4 4 JSL 2648 64-4 Same Same PC 4-5 0

Foraminiferal Census

The surface (0-1 cm) samples used for foraminiferal census were preserved in a

saturated solution of Rose Bengal in ethanol. The subsurface (below 1 cm) portions of the

box subcores and push cores were kept frozen until sectioned (in 1-cm slices) in the

laboratory, down to the 5th centimeter level, and stained with Rose Bengal. The samples

were washed through a 63 pm sieve. All stained specimens present in the samples were

identified and counted.

Ultrastructure

The ultrastructure of eight species (12 individuals) of Foraminifera was examined

as an independent means to distinguish live from dead specimens. From a number of

121

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. core-top samples, small splits, about 10 cc in volume, were removed on board shortly

after core retrieval. Within 5 minutes, they were fixed in chilled 3% glutaraldehyde in

0.1M cacodylate buffer (final concentration; pH 7.2) and kept at 5°C until further

processing. Once in the laboratory, Foraminifera were prepared for electron microscopy

using standard techniques (e.g., Bernhard and Reimers, 1991; Bernhard, 1993). Briefly,

specimens were removed from fixed sediment samples, rinsed three times in 0.1M

cacodylate buffer, decalcified in 0.1 M EDTA, post-fixed in 0.5% 0 s0 4 , rinsed with

distilled water, dehydrated in a serial sequence of ethanol, cleared with propylene oxide,

and embedded with Epon-Araldite. After polymerization, specimens were sectioned and

examined with a Philips 301 transmission electron microscope.

Stable Isotope Analysis

Stable carbon and oxygen isotope analyses were performed on calcific benthic

foraminiferal tests found in previously collected surface sediment from 11 seep sites (16

samples; see Sen Gupta and Aharon, 1994, Table 4.2); these sites cover a bathymetric

range o f216-694 m. The analytical methods are described in Sen Gupta and Aharon

(1994). Each foraminiferal sample consisted of two to five monospecific tests that were

Table 4.2. Mean abundance variations of dominant Foraminifera, six cores (Bsc 6, Bsc 16, Bsc 26, Bsc 28, Bsc 40, PC 64), 0-2 cm: Density (individuals in 30 cc of sediment) and percentage of assemblage.

Substrate depth Gavelinopsis Bolivina Trifarina Bolivina Osangularia translucens ordinaria bradyi albatrossi Rugosa

0-1 cm 5.3,31.6% 5.1,25.3% 2.8, 15.7% 1.1,5.5% 0.9,3.6% 1-2 cm 0.9,7.0% 2.1,14.3% 1.3,9.3% 2.4,16.7% 0.0%

carefully screened under the binocular microscope for traces of carbonate encrustations.

Because of the scarcity of Rose-Bengal-stained specimens in the chosen seep-sediment

122

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. samples, only unstained tests (> 250 pm) were analyzed. Most of the analyses were

performed on Uvigerina peregrina, except for two samples each of B olivina

subaenariensis and Lenticulina sp. We note, however, that none of these species was

dominant in Green Canyon samples taken in 1995 for foraminiferal census.

BACKGROUND: ANOXIA IN BEGGIATOA MATS

Beggiatoa, a large, motile, filamentous, chemolithotrophic, sulfide-oxidizing

bacterium, forms white, yellow, or orange mats around hydrocarbon seeps and vents in

the Gulf of Mexico, including the Green Canyon continental slope. The larger Beggiatoa

mats may be several meters wide (Sassen et al., 1993), but even the easily recognizable

(i.e., apparently well established) mats are no more than a few mm thick, and frequently

less than one mm thick. The exceptions are the network-like B eggiatoa mats that follow

fissures in hardground, and are 1 mm to 3 cm thick (Larkin et al., 1994). None of our

samples, however, were from this type of mat; they were all obtained from round patches

of mats (1-2 m across) overlying a mud substrate. When the cores were examined before

freezing, matted strands of Beggiatoa were visible to the naked eye within only the top 1-

2 mm layer. We did not measure the amount of 02 present in, or under, our sampled

substrates. However, excellent documentation exists that a critical oxic-anoxic boundary

zone is present within Beggiatoa mats, with H 2 S present in the underlying sediment

(because of sulfate-reducing bacteria), but 02 in overlying water (e.g., Jorgensen, 1977;

Spies and Davis, 1979; Larkin and Strohl, 1983). Microelectrode measurements in both

laboratory-grown and natural Beggiatoa mats have demonstrated this oxic-anoxic

interface even within very thin mats (e.g., Jorgensen, 1977,1982; Nelson et al., 1986). For

example, in a Beggiatoa mat growing on Iagoonal mud (and further developed in the

123

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. laboratory), the disappearance of 0 2 and the appearance of H 2 S were detected within a

0.05-mm thick transition layer whose top was less than 0.1 nun below the mat surface;

both 0 2 and H 2 S concentrations were extremely low (a few micromoles per liter) in the

microenvironment that supported living Beggiatoa (Jorgensen and Revsbech, 1983).

Thus, we surmise that in our cores from Green Canyon mats, an oxic-anoxic

boundary zone was present within about 1 mm from the core top. Although in situ

measurement of O 2 or H 2 S was not done in Green Canyon Beggiatoa mats, pore-water

H2 S was measured in some cores that were retrieved from Beggiatoa-mat environments

but not used in the foraminiferal study. The H 2 S content was very high at all stratigraphic

levels, but the shallowest level from which pore water could be analyzed was about 3 cm

below the core top, because of the preset spacing between ports on the pore-water

squeezer (Fu Baoshun, personal communication).

FORAMINIFERAL ABUNDANCE AND SPECIES DISTRIBUTION

Sediment-Water Interface

Forty two species were identified among the foraminiferal tests stained by Rose

Bengal and those examined for ultrastructure (Table 4.3). Excluding samples from which

a part was removed for ultrastructure study, the simple species diversity (species count)

in the unsplit core-top samples varied from 5 to 18. The assemblage sizes, however,

were small. The highest number of stained individuals recovered from a core-top sample

was 59, that from any downcore sample 30. The density distribution of the stained

foraminiferal assemblage in these surface samples showed considerable variability (Table

4.1), although all our sampling stations were within a very small area of Green Canyon

124

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 43. Identified species. Species illustrated in PI. 1 are marked by asterisks.

Alfredosilvestris levinsorti Andersen Angulogerina sp. *Bolivina albatrossi Cushman *Bolivina ordinaria Phleger and Parker B olivina sp. c£ B. spinata Cushman B olivina sp. *Bulimina aculeata d'Orbigny *Bulimina alazanensis Cushman Cassidulina sp. c£ C. australis Phleger and Parker *Cassidulina neocarinata Thalmann Cassidulina curvata Phleger and Parker Cassidulina subglobosa Brady Cassidulina sp. C ibicides sp. D entalina sp. Ehrenbergina trigona Go€s Epistominella exigua (Brady) Epistominella vitrea Parker F issurina sp. Fursenkoina compressa (Bailey) *Gavelinopsis translucens (Phleger and Parker) G landulina sp. Gyrodinoides altiformis (Stewart and Stewart) Gyrodinoides umbonatus (Silvestri) Hoeglundina elegans (d'Orbigny) Islandiella sp. Lagena mexicana Andersen Lenticulina clericii (Fomasini) Lenticulina orbicularis (d'Orbigny) Lenticulina rotulata (Lamarck) Lenticulina c£ L. serpens (Sequenza) Lenticulina sp. Marginulina sp. Neoeponides regularis (Phleger and Parker) Nonionella opima Cushman *Osangularia rugosa (Phleger and Parker) *Planulina ariminensis d'Orbigny P ullenia subcarinata (d'Orbigny) Saracenaria sp. *Trifarina bradyi Cushman Triloculina trigonula (Lamarck) Uvigerina peregrina Cushman

125

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. (Figure 4.1), and within the narrow depth range o f543-587 m. In the 10 unsplit core-top

samples (Table 4.1), the numbers of Rose-Bengal-stained foraminifers in 30 cc of surface

(0-1 cm) sediment have a range of 4-31 (x = 14.5, s. d. = 8 .6 ). Even the highest value of

foraminiferal density is a small fraction of the typical density observed in the Beggiatoa

mats of Santa Barbara Basin, California, in a water depth of about 580 m (Bernhard and

Reimers, 1991). Using the species distribution data from all unsplit core-top samples

except 42-0 (which contained only seven stained specimens), the ranking of frve

dominant species and their mean proportions (in nine samples) were as follows: ( 1 )

Gavelinopsis translucens (32.7%); (2) Bolivina ordinaria (19.0%); (3) Trifarina bradyi

(13.2%); (4) Bolivina albatrossi (5.4%); (5) Osangularia rugosa (3.1%). These and four

other commonly occurring species, Bulimina aculeata, B. alazanensis, Cassidulina

neocarinata, and Planulina ariminensis, are illustrated in PI. 4.1. Cassidulina

neocarinata and Bulimina alazanensis are much more abundant (~10%) in two samples

previously described from about the same depth (~585 m) in Green Canyon (Sen Gupta

and Aharon, 1994). However, the dominance of Gavelinopsis translucens and Bolivina

ordinaria is persistent; their mean proportions in these two samples were 29.5% and

21.2%, respectively. All of the above species are known to be commonly present in Gulf

of Mexico sediments in water depths of 500-600 m. In particular, >10% mean

proportions (for total assemblages in 16 samples) have been reported for Gavelinopsis

translucens and Bolivina ordinaria (Denne, 1990). This supports an earlier conclusion

(Sen Gupta and Aharon, 1994) that the foraminiferal species inhabiting Gulf of Mexico

hydrocarbon-vent habitats are not exotic taxa, but recruits from the vent-free surrounding

area. There is, however, at least one species whose distribution record is ambiguous.

126

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Epistominella exigua, known for its association with abyssal phytodetritus aggregates in

the North Atlantic (Gooday, 1988, 1993), is commonly present at 500-600 m water depth

in the surface sediment of the northwestern Gulf, but only one individual has been

identified among the Rose-Bengal-stained specimens in our sample set This may be a

species with little tolerance to the presence of H 2 S or petroleum at the sediment-water

interface.

Subsurface Layers

We examined the vertical distribution of Rose-Bengal-stained foraminiferal tests

in five box subcores and one push core (Figure 4.2). Foraminifera with cytoplasm (i.e.,

Rose-Bengal-stained) were exceedingly rare below the 3rd cm level, but it is noteworthy

that in Bsc 28 (JSL 2639), four such individuals were found in a 49-cc sample from the

3-4 cm layer (black sediment). A high concentration of H 2 S ( - 8 millimoles/1 total

dissolved sulfide) has been recorded from this layer in a push core taken from the same

site (Fu Baoshun, personal communication). In spite of some anomalously high

foraminiferal densities in subsurface samples, the overall trend is one of a pronounced

decrease from the surface layer (containing the B eggiatoa mat) to the subsurface layers.

The mean densities computed for 30 cc of sediment in the six cores are as follows:

0-1 cm, 19; 1-2 cm, 12; 2-3 cm, 6 ; 3-4,1.

All of the relatively common species (illustrated in Plate 4.1) were present in the

1-2 and 2-3 cm layers of one or more cores. Of the five dominant foraminifers of

Beggiatoa mats (Gavelinopsis translucens, Bolivina ordinaria, Trifarina bradyi, Bolivina

albatrossi, and Osangularia rugosa), four show a sharp decline in both absolute and

relative abundances from the 0-1 to the 1-2 cm layers. The exception is B olivina

127

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. albatrossi, which shows an opposite trend. For the six selected cores mentioned above

(Table 4.3), its mean population density (in 30 cc of sediment) increases downcore from

1.1 in the uppermost cm to 2.4 in the next The corresponding increase in the relative

abundance of B. albatrossi is even more pronounced— from 5.5% to 16.7%, because of

the population reduction in all other common species.

JSL 2636 Bsc 16 JSL 2635 Sac 6 JSL 2639 Bsc 26

5-4 cm p | _____ | 5-4 cm J _____ 0 10 20 0 20 40 0 10 20 Spetimens/30 cc Spsdmsns/30 cc Specimsns/30 cc

JSL 2639 Bsc 28 JSL 2644 Bsc 40 JSL 2648 Bsc 64

0-1 cm

g- 2-3 cm

0 10 20 0 20 40 0 10 20 Spscimsns/30 cc Spsclmsns/30 cc Spscimsns/30 cc

Figure 4.2. Surface to subsurface variations in foraminiferal assemblage density (number of Rose-Bengal-stained individuals in 30 cc of sediment). Dive and core numbers shown on each plot Bsc = box subcore; PC = large push core

ULTRASTRUCTURE

Twelve specimens, collected from four sampling sites, were examined for

ultrastructural characteristics (Table 4.4). Specimens had cytoplasm that was degraded to

varied degrees. Identifiable organelles were not observed in the cytoplasm of ten

specimens. The cytoplasm of one Gavelinopsis translucens appeared only partially

degraded (Figure 4.3A), allowing identification of some organelles such as mitochondria,

food vacuoles, and lipid vesicles (Figure 4.3B). A specimen of Cassidulina neocarinata

12S

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. also had identifiable lipid stored in some chambers. This specimen had a thick organic

lining veiling the inner test wall (Figure 4.3C). The organic lining, which appeared

laminated, did not occlude pore plugs (Figure 4.3D).

Table 4.4. Foraminiferal specimens collected from Beggiatoa mats and examined for ultrastucture. See Table 3.1 for coordinates.

Dive and sample Depth Species (and number of specimens)

JSL 2635,4-0 587 m Gavelinopsis translucens (3) Fursenkoina compressa (1)

JSL 2635, ll-O 587 m Dentalina sp. (1)

JSL 2639,35-0 589 m Cassidulina neocarinata (2) Gavelinopsis translucens (2) Bolivina ordinaria (1) Cibicides sp. (1)

JSL 2647,52-0 543 m Fursenkoina compressa (1)

Overall, ultrastructural observations showed that specimens had degraded

cytoplasm, suggesting that all examined individuals were dead at the time of fixation. It is

possible that live specimens inhabit the sediments influenced by the seeps, but only

specimens with degraded cytoplasm were observed in this study. The decay rate of

foraminiferal cytoplasm is unknown, but foraminiferal cytoplasm can remain in the test

after death for weeks (Bernhard, 1988). Thus, it is uncertain when the observed

specimens died. In other words, we cannot say if the Foraminifera died before or after

hydrocarbon seep activity affected their immediate environment.

While it is likely that all 12 specimens examined were dead, it is possible that the

two specimens with mildly-degraded cytoplasm were living at the time of collection.

Their degraded cytoplasm might have resulted from poor fixation due to time, pressure,

or temperature constraints. Alternatively, the Cassidulina neocarinata specimens might

129

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. not have fixed well because the thickness of their organic lining could inhibit exchange

with surrounding liquids.

The fact that the laminated and thickened organic lining did not occlude the pore

Figure 4.3. Transmission electron micrographs. A, B. 250-nm-thick section of Gavelinopsis translucens. A. Low-magnification view showing cytoplasm distributed throughout test p, proloculus. B. Higher-magnification view showing degraded cytoplasm, in particular the ruptured membranes of a mitochondrion (m). C, D. 120-nm-thick sections of Cassidulina neocarinata. C. Low- magnification view showing thick organic lining vesting inner surfaces of all chambers, including the prolocuhis (p). Note intact lipid droplets (1)> hut otherwise test is nearly devoid of cytoplasm. Also visible is matrix template for calcite test (M). D. Higher-magnification view showing laminated appearance of organic lining (OL). Also note that pore plug is not obstructed by OL. M, calcite matrix template. Scale bars, A, C = 10 pm, B, D = 1 pm.

130

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. plugs of C. neocarinata suggests that the organic lining was formed by the foraminfer,

and not as a post-mortem artifact. It is possible that the foraminifer responded to

hydrocarbon seep activity by creating the thickened lining to seclude its cytoplasm from

the surrounding environment. This thickened lining might be a visible indicator of

dormancy, which is suspected to occur in Foraminifera (e.g., McGee-Russell, 1974;

Linke et al., 1995). It must be noted, however, that the thickness of the organic lining in

C. neocarinata specimens from non-seep areas has not been examined. If indeed the

thickened lining is a manifestation of dormancy, we would expect to see thinner linings

in specimens from more "normal" environments.

The census of Rose-Bengal-stained individuals (Table 4.1) shows that compared

to the Foraminifera living in the extensive Beggiatoa mats of the Santa Barbara Basin at

comparable depths (Bernhard and Reimers, 1991), the putative living foraminiferal

populations in our samples were small. Thus, a strong possibility exists that the 10-cc

subsamples used in the ultrastructure study were too small for an assured recovery of live

individuals, even if they were present in the habitat.

STABLE ISOTOPE COMPOSITIONS

The carbon and oxygen isotope compositions of the analyzed foraminiferal tests

(Uvigerina peregrina , Bolivina subaenariensis , and Lenticulina sp.) are plotted in Figure

4.4. In general, the 8 ^ 0 values are enriched in the isotope, and show a relatively

narrow range of values ( 0 .8 % o to 1 .8 °/oo); two samples showing particularly heavy

5 I 8 0 values of 2.6°/oo and 2.8°/oo stand out The carbon isotopes show a spread of

values (0.4% o to -3.6%o) greater than that of the oxygen isotopes.

131

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. We argue, on the basis of the evidence discussed below, that the stable isotope

values graphed in Figure 4.4 record the specific habitats of the Foraminifera in the

context of seeps.

Figure 4.4. Carbon and oxygen isotope compositions of benthic foraminifera from seeps. Vertical bars show the range of S^C values (Aharon et al., 1992) in bathyal Gulf of Mexico bottom water away from seeps (GOMbw), and in C02 plumes enveloping seeps and derived from methane oxidation by free-living methanotrophs (Seep CO2 plumes). Triangles, U vigerina peregrina; squares, Bolivina subaenariensis; circles, Lenticulina sp.

0 1 2 3

8"0 (%«. PDB)

The seep sites from which foraminiferal tests were obtained for stable-isotope

analysis are located on the upper slope of the northern Gulf of Mexico where there is a

consistent downslope decline in the bottom water temperature (Aharon and Sen Gupta,

1994). Foraminifera depositing their calcite tests in isotopic equilibrium with the bottom

seawater are expected to record the site temperatures and the downslope temperature

decline in their oxygen isotopes. For example, the water temperature difference between

150 m and 370 m is 6 °C, which corresponds to an ^O-enrichment of 1.4%o (i.e., 6 °C

x 0-23°/oo). The measured 8 ^ 0 values of Foraminifera sampled at these water depths

are 0 .8 % o and 1 .8 % o, respectively, yielding an isotope contrast of 1 .0 % o that agrees

132

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. well with the values predicted from the water-temperature data under isotope equilibrium

conditions. In addition, two samples from middle bathyal seeps at 585 and 694 m yield

the heaviest 8 ^ 0 values (2.6°/oo and 2.8°/oo for a temperature of about 7 °C; Figure

4.4), as expected if the ambient water temperature exerts the primary control on the 8 ^ 0

values of the foraminiferal tests. No relation can be discerned in our data between 8 ^ 0

and S^C values (Figure 4.4), suggesting that the two isotope systems are controlled by

independent factors.

Regarding the carbon isotopes, the primary controlling factors are the 8 ^ C

composition of the dissolved inorganic carbon (DIC) in the ambient seawater-derived

fluids that serves as the primary source for carbon in the calcite tests of Foraminifera and

the so-called "vital effects." Three sources of DIC accessible to benthic Foraminifera can

be distinguished in the context of hydrocarbon seeps: ( 1 ) pore fluids below the

sediment/water interface; (2) overlying bottom water directly affected by seeps, and (3)

bottom waters unaffected by seeps. Pore-fluid chemistry studies of seeps indicate highly

elevated DIC levels (as much as 10 times higher than those at seep-free sites; et al., 1992;

Aharon, in press), with S^C negative anomalies in the range of -1 l°/oo to -38% o

(Graber et al., 1990; Aharon, in press). The high DIC levels in seeps are attributed to

microbial processes involving sulfate reduction and hydrocarbon oxidation (Roberts and

Aharon, 1994), which impart anomalously depleted ^ C values. Another bacterial

hydrocarbon oxidation process typical of seeps occurs in the water column, where C02

plumes derived from oxidation of methane by free-living methanotrophs (LaRock et al.,

1994) and diluted with normal bottom waters display anomalously negative S ^C values

133

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of up to -4.5% o (Aharon et al., 1992). Away from seeps, the Gulf of Mexico bathyal

DIC displays 8 ^ C values (0.4% o to -0.9%o, Figure 4.4) that are typical of "normal”

oxic oceans (Shackleton, 1977; Grossman, 1987).

Foraminiferal species exhibiting "vital effects" yield S ^C values that depart from

the isotope compositions of the ambient DIC, but these departures do not exceed 2°/oo

(Grossman, 1987). According to Grossman's study, species of Uvigerina and B olivina

precipitate their tests in isotopic equilibrium with their source. Because our samples (with

the exception of two Lenticulina samples) consist of Uvigerina peregrina and B olivina

subaenariensis, we conclude that their 8 ^ C values are likely to be controlled by the

ambient DIC.

Two groups ofS13C values can be discerned in the data plotted in Figure 4.4: (1)

foraminiferal tests compatible with a carbon source in bathyal DIC unaffected by seeps

(0.4% o to -0.8% o), and (2) those compatible with the seep C02 plumes (-1.3%o to -

3.6% o). The first group may include tests formed during time of seep quiescence and/or

allochthonous tests transported into the seepage sites by bottom currents. The second

group, preserving the imprints of hydrocarbon oxidation effects, suggests that carbon

from seep environments is utilized in some foraminiferal test construction and that

multiple foraminiferal species may have adapted to the dysoxia or anoxia associated with

advecting hydrocarbons. Foraminiferal S ^C depletions do not necessarily require the

influence of hydrocarbon seeps, since a similar range of negative values was obtained by

McCorkle et al. (1990) and Rathbum et al. (1996) from other taxa in non-seep settings.

The key factor supporting a hydrocarbon seep effect on the benthic Foraminifera studied

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. here is that large 5^C differences are discerned in tests of the same taxon and previous

studies have found little variation in 5 ^ C values within same species. However, for any

of the three species studied for carbon isotopes, a permanent habitation in seeps cannot be

invoked from the present isotope data because of the absence of anomalously negative

8 ^ C values such as those documented from seep pore-fluid DIC (-11°/oo to -38°/oo;

Graber et al., 1990; Aharon, in press). It needs to be emphasized here that none of the

dominant species from microhabitats in or under Beggiatoa mats in deep-bathyal Green

Canyon (e.g., Bolivina albatrossi , B. ordinaria, Gavelinopsis translucens , and Trifarina

bradyi) has been studied yet for carbon-isotope composition.

DISCUSSION AND CONCLUSIONS

Our present conclusions on the occurrence of living Foraminifera are based solely

on Rose-Bengal staining of cytoplasm in tests, because the very small subsamples fixed

for the ultrastructure study seem unreliable for the recovery of Foraminifera with

undegraded cytoplasm. Although complete post-mortem loss of cytoplasm in tests may

require considerable time (Bernhard, 1988; Corliss and Emerson, 1990), judging by the

quality of the internal staining and the number of stained specimens obtained from

processed samples (Table 4.1, Figure 4.2), we infer that living Foraminifera were present

in the B eggiatoa mats and (in many cases) in the underlying sediments at the time of

collection. Within the mats, 02 and H 2 S may coexist in small concentrations, and the

Foraminifera may not necessarily be facultative anaerobes; they may be microaerophiles

(see Bernhard, 1996). However, many individuals of several species recovered from

under the Beggiatoa mats were stained well by rose Bengal (Figure 4.2); some of these

were found at a sediment depth where the concentration of H 2 S was high, and, by

135

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. inference, 02 was absent Apparently, these species, including Bolivina albatrossi,

Bolivina ordinaria , Cassidulina neocarinata , Gavelinopsis translucens, Osangularia

rugosa, and Trifarina bradyi , are facultative anaerobes. They, however, are not exotic

imports to the sites of hydrocarbon seeps, but are common species of northern Gulf of

Mexico in mid-bathyal depths.

Our observations on dysoxia or anoxia tolerance of hydrocarbon-seep benthic

Foraminifera are supported by similar observations from other continental shelves and

slopes, especially from silled basins (see Sen Gupta and Machain-Castillo, 1993;

Bernhard, 1996). Overall, in benthic marine habitats, the Foraminifera withstand hypoxia

better than other meiofauna (Josefson and Widbom, 1988). In the central Santa Barbara

Basin, living Foraminifera (as determined by ATP assay) with intact organelles (as

determined by electron microscopy) have been found in anoxic pore waters 3 cm below

B eggiatoa mats. However, even such species (including Nonionella Stella) do not tolerate

anoxia indefinitely. Present information indicates that when the bottom water becomes

truly anoxic, Foraminifera do not survive in the Santa Barbara Basin (Bernhard and

Reimers, 1991); apparently, no "real anaerobic species" are known among the

Foraminifera (Fenchel and Finlay, 1995). On such evidence, it is likely that the survival

of most Foraminifera under the Beggiatoa mats of Gulf of Mexico hydrocarbon vents is a

short-term phenomenon. The 8 13c values recorded in unstained tests of Uvigerina

peregrina , Bolivina subaenariensis, and Lenticulina sp. are those of seep CO 2 plumes,

and not of pore fluids, which indicates that these species can invade anoxic layers under

Beggiatoa mats, but are unable to construct tests in such environments. No carbon-

isotope data, however, are available for the dominant foraminiferal species of Beggiatoa

136

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. mats of deep-bathyal Green Canyon. Thus, whether a species such as Bolivina albatrossi

and B.ordinaria may not only survive, but secrete calcite tests in a sulfidic environment

2-3 cm under a Beggiatoa mat is still an open question.

Compared to the isobathyal but much more extensive Beggiatoa mats of the silled

Santa Barbara Basin, those of the Green Canyon hydrocarbon seeps support much

smaller foraminiferal populations. This discrepancy can be explained by (a) the size

difference of the mats in the two areas, and (b) the inherently ephemeral nature of the

Green Canyon mats, whose occurrence is controlled by the shifting point sources of sea-

floor hydrocarbon emission. Such shifts are connected with the complex interplay of

various geological and geochemical factors, such as locations of hydrocarbon (methane

and petroleum) reservoirs, faulting, erosion, and sedimentation (Roberts and Aharon,

1994).

The foraminiferal species that arguably makes the best use of the trophic

resources of Green Canyon Beggiatoa mats is a small Bolivina , B. albatrossi. Its

population size actually increases from the sediment-water interface to the substrate

depth of 1-2 cm, indicating its H 2 S tolerance. Such small, infaunal, H 2 S tolerant,

opportunistic species (e.g., Stainforthia fusiformis ; see Alve, 1994) are generally regarded

as r-strategists. However, in view of the rapid turnovers in population densities of

protozoans (resulting from very short life cycles) and the variable roles of abiotic and

biotic factors, a protozoan species does not have a fixed place on the r-K continuum

(Layboum-Parry, 1984).

One potential source of stress for the Foraminifera of Green Canyon Beggiatoa

mats is the liquid and gaseous petroleum present in the bottom water and the sediments.

137

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. We, however, could not detect any effect of these natural pollutants on the structure of

the foraminiferal community. Samples with an extraordinary amount of oil were not

barren of Foraminifera, and did not contain deformed individuals, as reported for a

gigantic oil spill from a tanker (Venec Peyre, 1981), or for environments polluted with

heavy metals (e.g., Yanko et al., 1994; Alve, 1995). A parallel is seen in the meiofaunal

community that survives in a shallow-marine petroleum seep off California, because the

"stressful effects are more than offset by dynamic trophic processes associated with the

fringes of spots of active seepage" (Montagna and Spies, 1985). Tolerance data are not

available on foraminiferal species, but laboratory experiments on metazoan meiofauna

indicate an adaptation to increased levels of petroleum hydrocarbons, if the natural

environment of the community is one of chronic contamination by such chemicals

(Carman et al., 1995).

138

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 4.1

Scanning electron micrographs (scale bars = 100 pm)

1A Cassidulina neocarinata Thalmann; 3,4, Planulina ariminensis d'Orbigny;

5,6, Gavelinopsis translucens (Phleger and Parker); 7,8, Osangularia rugosa (Phleger and Parker);

9, Bolivina ordinaria Phleger and Parker;

1 0 , Bolivina albatrossi Cushman;

1 1 , Bulimina aculeata d'Orbigny;

1 2 , Trifarina bradyi Cushman;

13, Bulimina alazanensis Cushman.

139

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 4.1

140

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 5

BENTHIC FORAMINIFERA OF HYDROCARBON SEEPS OF THE NORTHERN GULF OF MEXICO: MICROHABITATS AND HISTORICAL TRENDS

141

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

About two decades ago, direct observations (submersible missions) of the ocean

floor resulted in the discovery of the hydrothermal vents and vent fauna at deep-sea

spreading centers (Corliss et al., 1979; Ballard, 1984; Jonhson et al., 1988). Similar

chemosynthetic communities were later found in areas of cold hydrocarbon seeps and

vents along convergent plate boundaries (Kulm et al., 1986; Juniper and Sibuet, 1987)

and also passive continental margins (Pauli et al., 1989; Kennicutt et al., 1985).

In the Gulf of Mexico, especially on the Louisiana continental slope, hydrocarbon

seeps cover extensive areas. In contrast to hydrothermal vents, hydrocarbon seeps occur

at relatively shallow depths and are characterized by ambient bottom-water temperatures.

The most evident emissions released at cold seeps are both in liquid (crude oil) and

gaseous forms (LaRock et al., 1994). The diapirism of the Jurassic salt in the Gulf of

Mexico (see Figure 5.1) plays an important role in the development of growth-fault

network through which fluids and hydrocarbons are transported to the sea floor (e.g.,

Roberts et al., 1992b).

Mounded carbonates Gas hydrate Figure 5.1. Schematic mounds figure showing the relationship between salt, sediments, faults P[*l«loc»n« and vent-seep-related features (modified from Roberts and Carney, 1997).

lkoc«n* :*>>>«*«

142

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Abundant benthic fauna of mussel and clam bivalves, gastropods and tube worms

that use chemosymbiosis to derive energy and nutrients (Jannash and Mottl, 1985;

Kennicutt et al., 1985; Tunniclife, 1992) have been found in the seemingly inhospitable

hydrothermal and hydrocarbon venting areas. Observations from submersibles revealed

that venting sites of cold vent domain are also associated with active deposition of

carbonates, sulfides, and sulfates of varied morphologies and complex mineralogies

(Commeau et al., 1987; Kulm and Suess, 1990; Roberts et al., 1992a; Fu et al., 1994).

It has been suggested that the release of methane from marine environments is

linked with global climate change both as a causal mechanism and as a consequence of

temperature changes (Rathbum et al., 2000). This inference was prompted by large shifts

in the stable isotope composition of benthic Foraminfera during climate change in the

Quaternary (Wefer et al., 1994; Kennett et al., 1996) and Late Paleocene (Dickens et al.,

1995,1997). During cold episodes of the climate cycle, sea level drops because water is

trapped in glaciers and polar ice caps, but mostly from thermal contraction of ocean

water. Under these conditions, reduced hydrostatic pressure favors the release of

enormous amounts of methane into the water column and atmosphere. Furthermore, this

process affects climate change by shortening the extent of glaciation during a given cycle

(MacDonald, 1990; Pauli et al., 1991; Kvenvolden, 1993). Carbon isotope studies of

foraminiferal shells from sediment cores retrieved from cold methane seeps on the

northern California margin suggest that these SI3C values reflect methane seepage and

can indicate temporal variations in seep activity (Rathbum et al., 2000).

The relationship between vent-seep features, biotic communities, and

hydrocarbon delivery rates in the Gulf of Mexico, was summarized by Roberts and

143

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Camey (1997). One or more types of flux rates (rapid, transitional, and slow) may occur

at a given site in environments with hydrocarbon emissions. (1) Rapid flux-rate

environments are associated with “mud-prone features” such as mud volcanoes, mud

flows, and gas expulsions. Under conditions of unstable substrate, only bacterial mats

survive in active areas. However, lucinids, vesycomyids, and pogonophorans may be

locally present in areas with more stable substrate. (2) Gas hydrate areas are typical of

transitional sites where gas hydrate mounds, isolated authigenic carbonate, and small

scale gas-fluid expulsion represent dominant features. Bathymodiolid mussels,

vestimentiferan tube worms, and Beggiatoa bacteria populate the hard substrate of

authigenic carbonate, whereas lucinid and vesycomyid clams and pogonophoran tube

worms can be found in mud substrates. Intra-annual emission activity at gas hydrate sites

is seemingly related to intrusions of warm-cored eddies from the Loop Current that

trigger short-term episodic releases by changing the temperature equilibrium. The long

term frequency of emissions at transitional sites is controlled by hydrostatic loading and

unloading generated by the sea level change. (3) Abundant authigenic carbonates

(nodules, crusts, hardgrounds, slabs, and mounds) characterize areas of slow flux rates. In

these areas, the sparsely distributed biota consists of bathymodiolid mussels,

vestimentiferan tube worms, and small bacterial mats. Lucinid and vesycomyid clams

and pogonophoran tube worms can be found on muddy bottoms surrounding the hard

substrate sites (Roberts and Camey, 1997).

Communities of benthic Foraminifera (living individuals detected by Rose Bengal

staining) are found in hydrocarbon seep areas from the northern Gulf of Mexico in

association with the chemolithotrophic, sulfide oxidizing bacterium Beggiatoa (Sen

144

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Gupta et al., 1997). Individuals belonging to the species Bolivina albatrossi , B olivina

ordinaria, Cassidulina neocarinata, Gavelinopsis translueens, Osangularia rugosa , and

Trifarina bradyi were found a few centimeters below the Beggiatoa mat under conditions

o f high H 2 S concentrations and consequent lack of O 2 (Sen Gupta et al., 1997). These

benthic Foraminifera from hydrocarbon seeps endure three major environmental

stressors: oxygen deficiency, H 2S toxicity, and oil toxicity.

Foraminiferal response to environmental stressors similar to those of hydrocarbon

seeps have been studied through both field and laboratory observations. Casey et al.

(1980) investigated the impact of the Ixtoc I and Burmah Agate oil spills on living

benthic Foraminifera and microzooplankton in the Gulf of Mexico. They concluded that

an increase in benthic foraminiferal standing crop and the appearance of the species

Bolivina lowmani were connected with oil sedimentation. The authors surmised these

community characteristics were actually related to the increase of sedimentary organic

content, but they did not rule out the possibility that the increased fallout of planktonic

organisms killed by the oil contributed to the higher standing crop of benthic

Foraminifera.

Some relevant laboratory data on H 2S tolerance are available. Some species can

survive short term (21 days) exposure to sulfidic conditions (dissolved H 2S = 6.66 pM)

but a significant reduction of total foraminiferal densities occurs after a prolonged

exposure (66 days) to higher concentrations (dissolved H 2 S = 12 pM) (Moodley et al.,

1998b). Furthermore, none of the genera in this experiment proliferated under sulfidic

conditions. In contrast, reproduction was visible when the experiment was conducted

under just anoxic conditions (Moodley et al., 1998b).

145

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The present study focuses on enhancing our understanding of foraminiferal ** ** * distribution in cold seep areas of northern Gulf of Mexico and assessing the potential use

of these benthic microorganisms in determining the temporal evolution of seeps.

MATERIAL AND METHODS

Samples used in this study were collected in August 1995 and August 1997 from

several locations in Green Canyon (Figure 5.2, Table 5.1). Box cores and push cores were

taken from the submersible Johnson Sea-Link I I at the dive sites. The coring box was

divided into four equal compartments that allowed retrieval of four undisturbed subcores

with a cross-section of 7-cm X 7-cm and a length of 18 cm. Push cores with an inner

diameter of 7 cm were used. After retrieval, the top 1 cm sediment from all the cores (box

subcores and push cores) was removed, stained with Rose Bengal, and kept in plastic jars

until it was processed. Also, one subcore from each box core was sectioned in I-cm slices

down to a depth of 8 cm, and each resulting subsample was stained with Rose Bengal.

The rest of the material was kept frozen until it was processed in the laboratory.

Specimens for the census of living Foraminifera were wet picked. All Rose-Bengal

stained specimens (bright red internal coloration) found in the top 8 cm of each core were

picked. Foraminiferal assemblages used for historical reconstruction were obtained from

a push core (PC2; length = 24 cm) retrieved during the JSL 2900 dive from block 232 in

Green Canyon (5.2). Mathew Hackworth (Ph.D. candidate at LSU), who performed a

suite of analyses on sediments from this push core provided data on % total carbon,

radiocarbon ages, stable isotope values of carbonate nodules, and proportions of fine and

coarse sediment fractions. Dr. Paul Aharon supervised the foraminiferal stable isotope

analysis, which was performed by Dr. Christopher Wheeler in the LSU Department of

146

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Geology and Geophysics stable isotope laboratory. For this analysis, I picked about 30

specimens of B olivina (mainly B. ordinaria and B. albatrossi) and about 10 specimens of

Globigerinoides ruber from each of the 24 samples of the core.

Table 5.1. Sample information. Samples from PC2 from JSL 2900 dive were analyzed for historical trends; all other samples were studied for the content of living Foraminifera.

MMS Dive no. Core Lat. Long. Water Block (N) (W) depth(m)

232 JSL2639 PC2 27°44.519’ 91°19.076’ 569 same same PC3 same same same same JSL 2900 EP9 24°44.64’ 91°19.05’ 567 same same EP10 same same same same same EPll same same same same same PC2 same same same same JSL 2893 EPl 27°46.9360’ 91°30.4999’ 541

Data analysis included several measures of species diversity: (1) species richness

(S), i.e., the number of species present in the sample, and (2) Shannon Wiener Index

given by the equation H(S) = -Ipilnpi, where pi is the proportion of the i* species,

Figure 5.2. Dive sites, indicated by Johnson Sea-Link dive numbers; Cores taken: Site 2693: PC2, PC3; Site 2893: EPl; Site 2900: Ep9, EplO, E pll, PC2.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. and (3) equitability given by E’ = e H(S)/S. Principal Component Analysis (PCA) of

species distribution data was performed in order to better understand the intimate

structure of the data set and its temporal variation. Since the number of variables that can

be introduced into PCA cannot exceed the number of observations (samples), selected

taxa (species and genera) were used. The goal of PCA is to detect the structure within the

variance-covariance of a multivariate data collection. The method is very efficient in

determining the number of linear independent vectors that exist in a matrix and thus can

measure the redundancy in the original set of variables (Davis, 1973). PCA allowed us to

determine covarying parameters even with high variances in the data set.

BENTHIC FORAMINIFERA AT COLD SEEPS

Earlier Work

There is a rather limited body of literature dealing with Foraminifera from

hydrothermal vent and cold seep environments in which researchers distinguished living

from dead specimens. Sen Gupta and Aharon (1994) and Sen Gupta et al. (1997)

described the distribution of living species around Gulf of Mexico hydrocarbon seeps;

live Foraminifera were recognized through the use of non-vital Rose-Bengal stain.

Furthermore, Sen Gupta et al. (1997) examined cytoplasmatic ultrastructure in order to

unequivocally demonstrate that Foraminfera live at seeps, but results, due to probably

poor fixation as well as the rather limited number of analyzed individuals, failed to

clearly confirm that Foraminifera were alive at the sampling time. However, in

ultrastructural studies combined with adenosine triphosphate (ATP) assays performed on

Foraminifera from Santa Barbara Basin, California, living Foraminfiera with intact

organelles were found 3 cm below the Beggiatoa mat (Bernhard and Reimers, 1991).

148

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Several field and laboratory observations have shown that Foraminifera can cope

with severely reduced oxygen concentration and even anoxia. A comprehensive review of

this work is provided by Bernhard et al. (in press). As mentioned before, benthic

Foraminifera found at cold seeps of northern Gulf of Mexico are present both within the

B eggiatoa mat and a few centimeters below it The development of Beggiatoa needs the

presence of O 2 in the overlying water and H 2S in the underlying sediment (Jorgensen,

1977; Spies and Davis, 1979; Larkin and Strohl, 1983). This is why an oxic-anoxic

interface exists within the very thin mats of the Gulf. Since H 2 S at these sites is

intimately related to hydrocarbon emissions with shifting point sources, it is expected that

Beggiatoa mats are ephemeral. Below the Beggiatoa mat, Foraminifera endure not only

anoxic conditions but also H 2S and perhaps oil toxicity (Sen Gupta et al., 1997).

Sen Gupta et al. (1997) identified 42 species of benthic Foraminifera that

apparently survive extreme environmental conditions at sites of cold seeps in Green

Canyon. Among these, species with high proportions in the assemblage (within the top 1

cm sediment layer) were: Gavelinopsis translucens (32.7%), Bolivina ordinaria (19.0%),

Trifarina bradyi (13.2%), Bolivina albatrossi (5.4%), and Osangularia rugosa (3.1%).

The examination of foraminiferal distribution within the subsurface layer revealed that all

the above mentioned species but Bolivina albatrossi show a sharp decline in both the

absolute number and relative abundances from 0-1 to the 1-2 cm layers. The mean

densities of living Foraminifera counted in the six analyzed cores dropped from 19 in 0-1

cm layer to 1 at a depth of 4 cm below the sediment-water interface. Plots of the

formaniferal density downcore distribution revealed that, in two out of the six cases, the

maximum density of living benthic Foraminifera was present in the 1-2 cm. Species

149

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. showing maximum density at this level were Bolivina albatrossi, B. sp., Bulim ina

alazanensis , and Trifarina bradyi (Sen Gupta et al., 1997).

Recent foraminiferal data from cold methane seep areas of the northern

Californian margin revealed unusual subsurface density peaks for several species

(Rathbum et al., 2000). Since these trends are isolated, it is believed that Foraminifera do

not try to avoid surface predation but rather benefit by enhanced food supplies, probably

linked to burrows or favorable chemical conditions (Rathbum et al., 2000). Foraminifera

from cold seeps of Monterey Bay, California (900-1000 m water depth) were analyzed by

Bernhard et al. (in press). Two independent vital methods ([ATP], cellular ultrastructure)

and conventional Rose Bengal (rB) staining were used to determine if Foraminifera

inhabit methane-rich or sulfide rich cold seeps in this region (Bernhard et al., in press).

Samples assayed for both rB and ATP showed little difference between the results of the

two procedures. In general, rB-stained specimens were also deemed living by ATP assay.

However, Rose Bengal stained specimens of Globobulimina from one sample were

determined to be dead by the ATP. Abundances of a few species were higher in seep

samples than in non-seep samples, and many rB-stained specimens found in seep samples

belonged to small-sized taxa. Prokaryote ectosymbionts were found in pores of one

specimen o f Uvigerina peregrina (Bernhard et al., in press)

Present Data

In this study, samples collected from several locations in Green Canyon (see

Figure 5.2) were analyzed for their foraminiferal content with the aim of better

understanding the microhabitat distribution within and under Beggiatoa mats. Although

living benthic Foraminifera were recorded in top and subsurface samples at some of these

ISO

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. stations (Table 5.2), samples with very pungent EfeS smell and high oil and carbonate

nodule content were void of benthic Foraminifera.

The pattern of vertical distribution of living Foraminifera collected from a hydrate

mound in Green Canyon (27° 44.46’ N, 91°19.05’ W) is consistent with previous findings

* (Sen Gupta et al., 1997). The three sediment cores (two push cores [PC] and one box core

[Bsc]) were retrieved from an orange Beggiatoa mat (Bsc EP9), a white Beggiatoa mat

Table 5.2. Locations of cores whose analysis revealed the existence of living Foraminifera.

MMS Dive no. Core Lat. Long Water Block (N) (W) depth (m) 232 JSL 2900 EP9 24°44.64’ 91°19.05’ 567 same same EPIO same same same same same E P ll same same same

(PC EPl 1), and at a location where no bacterial mat was visible (EPIO; five meters away

from EP9) in an attempt to compare seep with non seep populations. Nevertheless, both

carbonate nodules and oil droplets found in samples of in EPIO push core indicated that

even though no bacterial mat was visible on the surface, the sampled spot was still

located within the hydrocarbon seep. The maximum number of living Foraminifera was

found in the core tops at all these three stations (mean = 19.33 individuals in 30 cc of

sediment). Common species in the top 1-cm-thick layer were Bolivina albatrossi, B.

ordinaria, Cassidulina neocarinata, Fursenkoina compressa, and Trifarina bradyi. As

seen in Figure 5.3, foraminiferal density drops rapidly below the depth of 1 cm in two of

the cores and becomes zero below 1 cm in EPIO. The disappearance of living

Foraminifera in EPIO below I-cm level and the decrease of foraminiferal density in other

151

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. JSL 2900 Bsc EP9 JSL 2900 PC EP10 0 5 10 15 20 10 20 30

=•2 ? 2 CL

W . 0 O 4 Q 4

Individuals Individuals

JSL 2900 PC EP11 0 10 20

Individuals

Figure 5.3. Downcore variations in foraminiferal assemblage density (number of living individuals in 30 cc of sediment). Dive and core numbers shown on each plot. Bsc = box subcore; PC = push core).

cores coincide with increased amounts of oil droplets (only qualitatively determined) and

H2S (indicated by progressively stronger H 2 S smell). Thus, one potential source of stress

for the Foraminifera of Green Canyon Beggiatoa mats is the liquid and gaseous

petroleum present in the bottom water and the sediments (Sen Gupta et al., 1997).

Although we found Rose Bengal stained Foraminifera in sediments containing oil and no

deformed individuals, as reported for a gigantic oil spill from a tanker (Venec Peyre,

1981), an apparently negative relationship exists between foraminiferal density and the

152

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. amount of petroleum present in the sediment at hydrocarbon seeps. In petroleum-free

environments where oxygen deficiency is the major environmental stressor, living

Foraminifera may be found at levels as deep as 15 cm below the sediment-water

interface, whereas at hydrocarbon seep sites (where petroleum and H 2S are additional

stressors) living species have been found only as deep as 5 cm below the surface (see

Figure 5.3).

The data examined so far (Sen Gupta et al., 1997; this chapter) indicates that

certain foraminiferal species of slope environments can survive limited amounts of both

oil and H 2 S, but it is unclear if any of the species takes advantage of these compounds.

Apparently, most of the living species found at hydrocarbon seep sites in Green Canyon

are survivors rather than opportunists. As noted in Sen Gupta et al., 1997, however, the

mean density o f Bolivim albatrossi may increase downcore, indicating that at least one

species may show opportunistic behavior.

Remarks: Adaptation to Vent Habitats

The census of Rose-Bengal-stained Foraminifera from the cores analyzed in this

study supports our previous findings, i.e., some benthic Foraminifera live in Beggiatoa

mats and in the underlying sediments. As noted by Sen Gupta et al. (1997), given the

small concentrations of O 2 and H 2S o f the Beggiatoa layer, Foraminifera inhabiting the

mat may be microaerophiles (Bernhard, 1996) rather than facultative anaerobes. Below

the Beggiatoa mats living Foraminifera have to cope with a harsh environment

characterized by lack of oxygen, and H 2S and oil toxicity. As mentioned before, some

live specimens were found in these habitats but sediment samples with conspicuous

amounts of oil droplets and pungent H 2S smell were void of Foraminifera. We infer from

153

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the species census that foraminiferal taxa with high tolerance in these environments are:

Bolivina albatrossi, B. ordinaria , Cassidulina neocarinata , Fursenkoina compressa,

Osangularia rugosa, and Trifarina bradyi .

We have very little knowledge of foraminiferal adaptive strategies for survival in

the seemingly inhospitable environments of hydrocarbon seeps. Nevertheless, some

inferences regarding foraminiferal adaptations to such environments can be made. Many

foraminiferal assemblages collected from oxygen depleted, non-seep environments are

dominated by small-sized species such as Nonionella Stella (Bernhard et al., 1997),

StaninforthiaJusiformis (Alve, 1990,1994,1995b), Epistominella spp. (Ingle et al., 1980;

Jorissen et al., 1992; Platon and Sen Gupta, in press), and Buliminella morgani (Platon

and Sen Gupta, in press). This pattern supports the suggestion that small Foraminifera are

better adapted to these environments than large-sized species are, because of their

diminished oxygen needs (Phleger and Soutar, 1973). Some studies suggest that pore size

and pore density of foraminiferal species from oxygen-depleted environments are higher

than those of species from well-oxygenated environments (Perez-Cruz and Machain-

Castillo, 1990; Moodley and Hess, 1992). Since pores seem to facilitate the intake of

oxygen (Berthold, 1976), larger and more numerous pores may help the foraminifers to

acquire more oxygen. However, as Bernhard (1999) noted, low-oxygen habitats are also

populated by species with very small pores and by the poreless agglutinated species.

Furthermore, concentrations of mitochondria (respiratory organelles) have been noticed

not only beneath the pore plugs but also in apertural cytoplasm and pseudopods

(Bernhard, 1999).

154

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Bernhard (1993) suggested that possible physiological strategies that allow

Foraminifera to survive anoxia include: metabolic dormancy, encystment, or

incorporation of bacterial endosymbionts. Rod-shaped bacteria were found in association

with the pore plugs of the infaunal taxon Globocassidulina in reducing environments of a

shallow Antarctic bay (Bernhard 1993). It is possible that these symbionts oxidize H 2 S

and thus detoxify this pore-water constituent (Bernhard, 1993,1999). Recent

ultrastructural observations on Foraminifera from cold seeps of Monterey Bay,

California, revealed not only that Foraminifera inhabit these environments but also that

Uvigerina peregrina harbor prokaryotic ectosymbionts associated with its pore plugs

(Bernhard et al., in press). It was assumed that such ectosymbionts enable Foraminifera to

live in these microxic or anoxic environmental conditions (Bernhard et al., in press). Sen

Gupta and Aharon (1994) suggested that Beggiatoa may represent a significant food

source for the Foraminifera that inhabit the hydrocarbon seeps of the Gulf. Remains of

this bacterium were found in food vacuoles of Chilostomella ovoidea that inhabits

oxygen-depleted environments of Santa Barbara Basin, California (Bernhard and Reims,

1991). Furthermore, no living Foraminifera were found a few meters away from a

Beggiatoa mat in the northern Gulf of Mexico, whereas, seven species with living

individuals were identified in a sample collected from a Beggiatoa mat (Sen Gupta and

Aharon, 1994).

Survival and Reproduction under Sulfidic Conditions

Experimental studies intended to assess the foraminiferal survival in anoxic,

sulfidic conditions (Bernhard, 1993; Moodley, 1998b) have demonstrated that some

species tolerate such environmental conditions. Under moderate H 2S concentrations (500

155

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. aM), the ATP concentrations of Foraminifera did not differ much from those of

Foraminifera kept in oxygenated conditions (observations were made after 30 days of

incubation; Bernhard, 1993). Under conditions of higher H 2S concentrations (S pM), life

signs were noticed after 21 days but no specimen was alive after 42 days of experiment,

when H 2 S concentrations were as high as 12 pM (Moodley, 1998b). Furthermore,

Moodley (1998b) noticed that reproduction took place under anoxic conditions but no

Foraminiferal proliferation was noticed under sulfidic conditions. Considering this, it is

reasonable to assume that benthic Foraminifera populating the cold vents of northern

Gulf of Mexico perhaps reproduce at and/or very close to the surface where more oxygen

is available and reduced amounts of H 2S and oil do not interfere with this process.

Another possibility would be that they reproduce away from seeps and travel into the

seep areas for reasons that might include predation and food availability. Nevertheless,

highly negative carbon isotope compositions measured on benthic foraminiferal tests

from a Green Canyon hydrocarbon mound (to be discussed in the second part of this

chapter) indicate that test biomineralization takes place on and/or within sediments

deposited in these environments. We infer that the few foraminiferal species that live in

hydrocarbon seep environments of the Gulf of Mexico reproduce, grow, and attain

maturity in these microhabitats.

STRATIGRAPfflC DISTRIBUTION

The historical distribution of foraminiferal assemblages from the hydrocarbon

seep habitats was analyzed in a core retrieved from a white Beggiatoa mat in MMS block

232, Green Canyon (JSL2900-PC2; see Figure 5.2). Stable isotope measurements were

1S6

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. performed (by Paul Aharon and Christopher Wheeler) on both benthic and planktonic

foraminiferal tests collected from this core.

The micropaleontological analysis of the 24 subsamples of JSL2900-PC2 resulted

in the identification of over 70 species of benhtic Foraminifera (Table 5.3). The

maximum number of species, 46, was recorded in the bottom sample (24 cm below the

top), whereas the minimum number of species was counted for a sample 9 cm below top,

i.e., the sediment-water interface (Figure 5.4). Decreasing trends of species richness were Number of species Shannon Wiener Index 0 20 40 60

Eo 9 11

13 E IB 15 (0 17

Figure 5.4. Species diversity distribution in JSL2900-PC2; (A) Species richness; (B) Shannon Wiener Index.

recorded within the 22-20 cm,16-13 cm, and 12-9 cm intervals. The distribution of

Shannon Wiener Index (Figure 5.4) can be divided into a few intervals. A decrease of this

157

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. measure is observed in the 24-19 cm and 17-9 cm intervals, whereas increases can be

noted in the 19-17 and 9-0 cm intervals. More pronounced trends are those of equitability

(Figure 5.5). The average values for the equitability are 0.45 for the 24-21 cm interval,

Equitability specimens/1 g of sediment 0 0.5 1 0 2000 3000

9 < ► oE 11 S CL a. 13 Q 13 ► a. mE CO 17

Figure 5.5. JSL2900-PC2; Distribution of equitability (A) and number of specimens per 1 gram of dry sediment (B).

0.63 for the interval between 20 cm and 15 cm, and 0.74 for the subsequent interval up to

the top of the core. A noticeable trend is that of the number of specimens found in one

gram of dry sediment (foraminiferal density) throughout the core (Figure 5.5). Thus,

foraminiferal density decreases severely in the 24-15 cm interval, stays at very low values

up to the 7 cm level, and slightly increases in the top six cm of the core. Both the

158

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. depleted number of species and much reduced population densities in the upper two

thirds of the core result in a more uniform distribution of species within foraminiferal

assemblages (see equitability plot; Figure 5.5). Therefore, increasing trends of

equitability in this particular data set are due to the low number of specimens and species

found in the upper core samples. Furthermore, this trend suggests a lack of foraminiferal

opportunistic behavior as a response to the environmental change.

Table 5.3. Foraminiferal species identified in JSL2900-PC2

Species name Species name Amphicoryna sp. Hyalinonetrion sp. Bolmna albatrossi Karreriella bradyi B. barbata Lagena laevigata B.fragilis L. sp. B. lanceolata Laticarinina pauperta (?) B. lawmani Lenticulina difflugiformis (?) B. ordinaria Lenticulina sp. 2 B. ordinaria var. 1 Lenticulina sp. 3 B. subanaraensis Lenticulina sp. 4 Bolmna sp. Lentticulina sp. 1 Bulimina aculeata Marginulina sp. 1 Bulimina alazanensis Marginulina sp. 2 Bulimina mexicana Miliolinella circularis (?) Bulimina sp. Necrosbyia minuta Cibicidoides incrassatus Neolenticulina sp. 1 C. to Nonion sp. C. neocarinata Oolina sp. C. nodosa Osangularia rugosa C. pachydermus P.faveolata C. reg (?) Planulina ariminensis Cassidulina curvata Pofymorphina sp. C. subglobosa Pseudononion sp. Epistominella exigua Pullenia buloides EL sp. Pullenia subsphaerica Eponides regularis Pyrgo murchina Fissurina cf. sp. F. bicostata Quinqueloculina sp. 1 F. hspdC?) Q. sp.2 F. sp. 1 Q. sp. 3 F. sp.2 e-sp.4 F. sp. 3 Sigmoilinasp. Gavelinopsis translucens Stanforthia (?) (Table 5.3 continued)

159

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Globocassidulina affirtis Syphonina bradyana G. laevigatus Trifarina brady G. sp. 1 Triloculina sp. G. sp.2 T. sp. 1 Hansenisca soldani Uvigerina peregrina Hoeglundina elegcms Vabmlineria mexicana

Species frequently occurring throughout the core are Bolmna albatrossi, B.

ordinaria, Bulimina alazanensis, Bulimina aculeta, Cassidulina neocarinata,

Epistominella exigua, Gavelinopsis translucens, Osangularia rugosa, Siphonina

bradyana, Trifarina brady, and Uvigerina peregrina. As determined by Rose Bengal

staining, all species were found alive at hydrocarbon seep sites in the northern Gulf of

Mexico (Sen Gupta et al., 1997; this study). It should be noted, however, that living U.

peregrina is very rare in these environments (Sen Gupta and Aharon, 1994). Among taxa

that occur in more than 50% of the analyzed samples, Bolm na shows the highest relative

abundance. Figure 5.6 shows the temporal distribution of the main genera: Bolm na (B.

albatrossi, B. ordinaria, B. lowmani, B. translucens, B.fragilis), Bulimina (B.

alazanensis, B. mexicana, B. marginata, B. aculeata), Cassidulina (C. neocarinata, C.

subglobosa, C. curvata, C. nodosa), Gavelinopsis (G. translucens), Osangularia (O.

rugosa), Plamtlina (P. ariminensis, P.faveoloata), Siphonina (S. bradyana), Trifarina (71

bradyi ), and Uvigerina (C/1 peregrina). In terms of relative abundance, one of the three

genera - Cassidulina, Gavelinopsis, or Bulimina - is the second-ranking taxon at different

levels of the core. A major component of foraminiferal assemblages in JSL2900-PC2 is

Bolmna ordinaria. Its average relative abundance of about 15% falls within the normal

relative abundances of this species in the Gulf in water depths of about 570 m (Denne,

1990). Similarly, B. albatrossi, B. aculeata, G. translucens, and Uvigerina peregrina

160

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.

T_bnly - Os_rug - Planul -Total e U_per -X--- -A— Siph_brd -A— » Bol » Total ... A* * ■ Total Cassld Total ■ * ...A* -- -x- Gav_.tr —e—Total Bulim —e—Total Sample (cm) Depth Sample (cm) Depth * 1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

0 0.1 0.1 0.4 0 3 Figure 5.6. Vertical distribution ofselected foraminiferal taxa in JSL2900-PC2. 0.02 0.01 0.09 0.08 0.35 0.05 g 0.04 O 0.05 O 0.25 c 0.07 «, «, O. 0.03 :§ 0.06 !« | 0.15 o\

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. seem to have normal relative abundances for this water depth. Also very close to normal

values are the relative abundances of Bolmna lowmani and Bulimina alazanensis .

However, the abundances of Cassidulina species are an order of magnitude below those

recorded by Denne (1990) from surface sediments in normal marine environments.

Multivariate Analysis

Principal Component Analysis was performed with the aim of better

understanding the relationships among the parameters measured in JSL2900-PC2

3.5

3.0

2.5

2.0 s ><5 1.5

1.0

0.5

0.0 0 1 2 34 56 7 8 9 10 11 12 Number of Eigenvalues

Figure 5.7. Scree plot of eigenvalues for Principal Components Analysis; Arrow denotes the significant number of components.

samples. The scree plot in Figure 5.7 shows that three principal components have

significant values. Altogether, they explain 60.3% of the data set total variance of (Table

5.4). As shown in table 5.5, high loadings onto factor 1 are those o f the foraminiferal taxa

162

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 5.4. Eigenvalues; Extraction: Principal Components.

Factor Eigenval % total Cumul Cumul ______Variance Eigenval % 1 3.084458 28.04052 3.084458 28.04052 2 2.138493 19.44084 5.22295 47.48137 3 1.411908 12.83553 6.634858 60.31689

Table 5.5. PCA. Factor loadings for 21 variables obtained from the analysis of JSL2900- PC2 data; Rotation: Varimax Normalized; Extraction: Principal components.

Parameter Factor Factor Factor 1 2 3 B ALB -0.75484 0.136042 0.258111 B ORD -0.2593 -0.66932 -0.2813 BUL ALAZ -0.25847 0.670927 0.061928 T BULIM 0.70015 -0.01595 0.085384 CASS NC 0.016978 -0.0171 0.711357 GAV TR 0.039623 0.535923 -0.54344 OS RUG 0.701156 0.398988 -0.07707 T PLANUL 0.196068 0.435926 0.616123 SYPH BRD -0.70245 -0.20698 -0.03247 T BRDY 0.344614 0.873828 0.007428 U PER -0.29159 0.139351 0.69808 Expl.Var 2.423185 2.379464 1.832209 Prp.Totl 0.22029 0.216315 0.166564

Bolmna albatrossi., Bulimina, Osangularia rugosa, and Siphonina bradyana. The second

most significant factor explains about 19% of the total variance and is strong loaded by

three parameters: Bolivina ordinaria, Bulimina alazanensis, and Trifarina bradyi.

Cassidulina neocarinata, Plartulina, and Uvigerina peregrina have loadings onto factor

three that explains about 18% of the total variance.

163

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Plots of factor scores (Table 5.6) against sample depth are depicted in Figure 5.8.

The temporal distribution of the scores (Figure 5.8A) reveals a clear change of the

parameters with high loadings onto factor 1 that, as seen in Table 5.4, explains about 28%

Table 5.6. PCA on data from JSL2900-PC2: Factor scores; Rotation: Varimax normalized; Extraction: Principal components.

Factor Factor Factor 1 2 3 1 -0.27647 1.781693 -1.47866 2 0.551534 0.9946 1.737601 3 1.029147 1.540698 0.804318 4 0.767544 0.205289 -1.21692 5 1.133113 0.722043 2.110527 6 1.499338 0.846097 -0.07745 7 -0.52231 1.899486 -0.84634 8 1.854784 0.103018 -1.4166 9 0.100576 -1.18795 0.040608 10 1.374948 -2.17385 -0.60749 11 -0.6706 -0.39991 -1.07087 12 0.965698 -0.3098 -0.53156 13 1.03721 -1.09909 1.235006 14 -1.15674 -0.49655 0.642162 15 -0.62641 0.040949 0.155518 16 -1.18318 -0.29722 0.903835 17 -0.15496 -0.67884 0.180177 18 -1.47468 0.139744 0.42574 19 0.198211 -0.80021 -0.0248 20 -0.92868 0.207539 -0.84651 21 -0.83132 -1.0758 -0.23809 22 -0.84207 0.619356 -0.89567 23 -0.78995 -0.90448 -0.38642 24 -1.05474 0.32319 1.401875

of the total variance of the analyzed data set. A significant break in the temporal

distribution of factor 1 scores takes place between 13 and 14 cm below the sediment-

water interface. The average score value for the interval 14-24 cm is -0.80, whereas

above the 14 cm level, the average is 0.68. The distribution pattern of factor 2 scores

(Figure 5.8B) is mainly controlled by Bolmna ordinaria , Bulimina alazanenis, and

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Trifarina bradyi . A continuous increase of factor 2 score values from -2.17 to 1.89 can be

seen between 10 cm and 7 cm below the surface. Factor 3 scores show a highly variable

distribution, and a large-scale pattern could not be distinguished.

Scores S cores -2 -1 o 1 -2 o

-O h ------B e e !e 10 10 E E e o e o e e e e o 15 -j • 15 e Q e a e • i o a E E a e 20 i a 20 (0 0)

25 25

30 J 30

Figure 5.8. Plots of factor scores of (A) factor 1 and (B) factor 2.

Plots of factor loadings are depicted in Figures 5.9 through 5.10. In the factor 1

vs. factor 2 plot, a similar behavior of the parameters of Trifarina bradyi , Osangularia

rugosa, Bulimina alazanensis , Gavelinopsis translucens , and Bulimina is noticeable. An

opposite trend is shown by the parameters of Bolivina albatrossi, B. ordinaria , and

Siphonina bradyana. Two other groups show opposite trends along factor 3 axis (see

Figure 5.10). One consists of Uvigerina peregrina , Cassidulina neocarinata and

Planulma, whereas the other is represented by only Gavelinopsis translucens.

165

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1.0 T.BRDY 0.8 BULJUAZ

0.6 GAV_.TR

T.PLANUL OS.RUG 0.4

cm B.ALB U.PER

CASS.NC T.BUUM

SYPH.BRO

-0.4

• 0.6 B.ORD

- 0.8 - 1.0 -0.6 0.6 1.0 Factor 1 Figure 5.9. Plots of factor loadings for foraminiferal data in JSL2900-PC2; Factor 1 vs. Factor 2; Rotation: Varimax normalized; Extraction: Principal components. 0.8 U.PER CASS.NC T.PLANUL 0.6

0.4

B.ALB

T.BUUM

CO T.BRDY SYPH.BRO % OS.RUG u.a -02 BORO

-0.4

GAV.TR

• 0.6

- 0.8 - 1.0 - 0.6 0.6 1.0 Factor 1 Figure 5.10. Plots of factor loadings for foraminiferal data in JSL2900-PC2; Factor 1 vs. Factor 3; Rotation: Varimax normalized; Extraction: Principal components.

166

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. STABLE ISOTOPE RECORDS OF BENTfflC FORAMINIFERAL TESTS

Previous Work on Stable Isotope Composition of Cold Seep Benthic Foraminifera

Carbon isotope composition of a foraminiferal shell, acquired during the test

secretion, is a function of the ambient chemistry and vital effects (e.g. McCorkle et al.,

1990,1997; Rathbum et al., 2000). A correspondence exists between the foraminiferal

microhabitat preference and the test isotopic composition (McCorkle et al., 1990,1997;

Rathbum et al., 1996,2000), but different species of benthic Foraminifera living at the

same time may differ in 8I3C values by as much as 3°/oo or 4°/oo (McCorkle, 1990,1997;

Rathbum, 1996).

The primary source for carbon in the calcite test of Foraminifera is the dissolved

inorganic carbon (DIC) from pore fluids below the sediment-water interface, overlying

bottom water directly affected by seeps, and bottom waters unaffected by seeps (Sen

Gupta et al., 1997). Thus, 8l3C values of epifaunal species reflect the Sl3C of the bottom-

water dissolved inorganic carbon, whereas the S13C signature of the infaunal taxa is

closely related to the more negative carbon isotope values of subsurface pore waters

(McCorkle et al., 1990,1997). Highly elevated DIC levels with 8l3C values between

-1 l°/oo and -38°/oo were revealed by pore-fluid chemistry studies of seeps (Graber et al.,

1990). These increased levels of DIC are attributed to microbial processes involving

sulfate reduction and hydrocarbon oxidation (Aharon et al., 1992; Roberts and Aharon,

1994). In the water column above the seeps, CO 2 produced by the activity of methane

oxidizing free-living methanotrophic bacteria (LaRock et al. 1994) is diluted with that

from normal bottom waters. However, anomalously negative SI3C values of up to

167

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. -4.57oo were recorded in the water column CO 2 at hydrocarbon seep sites (Aharon et al.,

1992). In areas unaffected by seeps, “normal” values for DIC 813C are 0.4°/oo to

-0.9 °/oo (Shackleton, 1977; Grossman, 1987).

The published data for stable isotope composition of living foraminiferal

carbonate associated with hydrocarbon seeps is rather limited. As reported by Sen Gupta

and Aharon (1994) and Sen Gupta et al. (1997), 8I3C signature of Uvigerina peregrina

and Bolivina subaenarensis related to seep CO 2 can be as negative as -1.3 °/oo to -3.6 °/oo,

whereas isotopic values obtained from tests of the same species in non-seep environments

are 0.4 °/oo to -0.8 °/oo. A comparison between living and fossil Foraminifera associated

with cold methane seeps on the northern California margin revealed that fossil

Foraminifera have carbon isotope values 4.10 (C/1 peregrina) and 3.60 ( B. subargentea)

more negative than 8,3C values recorded for living species (Rathbum et al., 2000).

Isotope Compositions of Selected Foraminiferal Species

Stable carbon isotope analyses were performed on calcitic benthic {Bolivina

albatrossi and B. ordinaria) and planktonic ( Globigerinoides ruber) foraminiferal tests

found throughout a 24 cm long push core (JSL2900-PC2). The isotope analysis was

guided by Dr. Paul Aharon and performed by Dr. Christopher Wheeler in the LSU

Department of Geology and Geophysics stable isotope laboratory. As mentioned before,

sizeable populations of Bolivina albatrossi and B. ordinaria were found living at seep

sites in Green Canyon (Sen Gupta et al., 1997; this study). Because of this finding and

their high relative abundances in JSL2900-PC2, Bolivina albatrossi and B. ordinaria

were the preferred species for the isotope analysis. Foraminiferal samples prepared for

the isotopic analysis were collected from each 1 cm interval along the entire core. [Due to

168

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the relative paucity of tests in some sampling intervals, however, some samples had to be

combined (see Table 5.7 for details; C. Wheeler, personal communication). The two

benthic species, Bolivma albatrossi and B. ordinaria, were mixed in each of these

artificial samples in a proportion that reflected their distribution in the natural samples.]

In order to facilitate interpretation of the isotopic values obtained for the species

from the hydrocarbon seep core, specimens of B. ordinaria, B. albatrossi (mixed in

proportions similar to those in JSL2900-PC2), and the planktonic Globigerinoides ruber

from non-seep sites were analyzed for 8l3C. These control samples were obtained from

sites located in the western Gulf of Mexico. Isotopic data and sample water depths are

provided in Table 5.7. Plots of data from Table 5.7 and Table 5.8 are depicted in Figure

Table 5.7. Stable isotope values (SI3C ) of planktonic and benthic Foraminifera. JSL2900-PC2; Source: P. Aharon (personal communication).

Globigerinoides Bolivina Depth 813C Depth 813C (PDB1______(PDB)

1 cm -3.42 1 cm -7.90 2 cm -4.54 2 cm -8.27 3 cm -6.16 3 cm -8.94 4cm -4.63 4cm -8.80 5cm -6.68 5 cm -8.36 6 cm -3.31 6+7 cm -9.11 7 cm -4.04 7+8 cm -9.72 8 cm -5.33 9cm -6.37 9+10 cm -9.79 10cm -6.90 11 cm -3.10 11+12 cm -8.54 12 cm -3.61 13 cm -2.36 13+14 cm -10.15 14 cm -5.44 14+15 cm -9.70 15cm -3.37 16 cm -2.91 16 cm -7.60 (Table 5.7 continued)

169

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 17cm -5.34 17 cm -8.52 18 cm -5.77 -7.49 19 cm -4.53 19 cm -8.23 20 cm -3.25 20 cm -7.23 21 cm -3.98 21cm -6.40 22 cm -0.28 22 cm -4.16 23 cm -0.09 23+24 cm -2.72 24 cm 0.26

5.11. Very large excursions (6-7 °/oo) in carbon isotope signature occur in both Bolivina

and Globigerinoides. The isotope trends in Globigerionoides suggest diagenetic changes

of the test geochemistry. As with all planktonic Foraminifera, Globigerinoides secretes

its test in isotopic equilibrium with the upper part of the water column and its “normal”

§13C values, as determined through isotopic measurements on non-seep specimens,

range between -.022 and 1.36 (see Table 5.8). Therefore, it is reasonable to assume that

the recorded negative shifts of Globigerinoides carbon isotope values reflect

hydrocarbon-seep bottom- and pore-water chemistry and they resulted through diagenetic

processes (carbonate overgrowths). The test biomineralization of Bolivina and other

benthic Foraminifera living in hydrocarbon seep environments takes place

Table 5.8. Stable isotope values (S13C ) of planktonic and benthic Foraminifera from control samples in the western Gulf of Mexico; Source: P. Aharon (personal communication).

Water Depth Sample GlobigerinoidesBolivina (m) 813C 813C (PDB) (PDB) 564 207 1.05 -1.67 579 211 -0.22 -2.08 579 213 1.12 -1.17 549 214 0.61 -1.58 595 597 1.36 -1.07

in isotopic equilibrium with the pore fluids below the sediment-water interface and

overlying bottom water directly affected by seeps (Sen Gupta et al., 1997). Therefore, it

170

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. is expected that their original isotopic composition would reflect seep activity.

Postdepositional changes of the isotopic composition of Globigerinoides tests (inferred

from seep vs. non-seep values) suggest that diagenesis too might have affected Bolivina.

Judging by the fact that the isotope departures from normal values are higher in Bolivina

than they are in Globigerinoides (Figure 5.11), we argue that the recorded 5I3C of

Bolivina represents both isotope composition acquired during test secretion and

diagenetic additions.

The vertical distribution of 8l3C in Bolivina (Figure 5.11) matches well the

distribution of percent carbonate and that of fine fraction/coarse fraction ratio (Figure

513C ( ° / o o PDB) -12.0 -10.0 -8.0 -6.0 -4.0 -2.( 0.0 1 2 3 Bolivina 4 5 6 7 8 atCO 3 9 o 10 o 11 «a Globigerinoides 12 13 o 14 3 15 16 17 18 19 20 21 22 23 L_u 24

Figure 5.11.8I3C vertical distribution; stripes to the right represent normal 5l3C values for Bolivina (left) and Globigerinoides (right); Source: P. Aharon (personal communication).

171

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 5.12). Progressively negative carbon isotope values of foraminiferal tests coincide with

increased percent of total carbonate and carbonate nodules. This shows that after some

point in time, more carbonate with negative carbon isotope signatures was available for

foraminiferal test building and/or diagenetic transformations.

% Total Carbonate Fine/Coarse Ratio a 10 20 30 40 50 60 70 80 0 s 10 15 20 25 30 35 40 45

Figure 5.12. Vertical distribution of % total carbonate (left) and fine fraction/large fraction ratio (right); based on raw data from M. Hackworth (personal communication).

Scanning electron microscope (SEM) analysis of selected specimens of Bolivina

albatrossi, B. ordinaria, and Globigerinoides ruber (Figure 5.13 through 5.16) confirm

the existence of diagenesis within both benthic and planktonic foraminifers. However,

well preserved foraminiferal tests (with little or no visible addition of secondary material)

were very common among the analyzed individuals.

172

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.13. Globigerinoides ruber, aragonite (?) spicules grown within the aperture.

173

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.14. Authigenic carbonate growth on Bolivina ordinaria; A. carbonate grains cover almost entirely the specimen test; B. transition from smooth surface (top) to carbonate growths (base).

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.15. Bolivina albatrossi; A. well preserved specimens: (A.1) whole specimen; (A.2) highly magnified portion of the test showing the smooth surface of a “clean” specimen; B. heavily altered specimens: (B.l) whole specimen; (B.2) highly magnified surface showing carbonate grains entirely covering the specimen surface and its pores.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 5.16. Globigerinoides ruber: (A) clean test surface; (B) carbonate grains grown on the surface and within the pores.

176

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Diagenetic and Biogenic Isotopic Signature

As mentioned before and supported by the SEM analysis, the collection of B.

albatrossi and B. ordinaria analyzed for the 5I3C content bore a mixed biogenic-

diagenetic isotope signature. On the other hand, the negative isotope exclusions in the

planktonic species, Globigerinoides ruber , reflect diagenetic processes rather than

biomineralogic composition. Carbonate overgrowths on Globigerinoides test are

responsible for isotope negative departures as high as - 6 °/00. We assume that if only

diagenesis had affected both Bolivina and Globigerinoides , and the carbonate in

foraminiferal test had been completely replaced in the two taxa, their isotopic signatures

would be similar and equal to the values for the authigenic carbonate, i.e., -14°/oo (M.

Hackworth, personal communication). Furthermore, if the replacement had not been

complete but similar proportions of biogenic carbonate had been replaced by authigenic

carbonate it would be reasonable to assume that departures from the isotopic values

recorded in the control samples would be similar in the two foraminiferal groups.

Analysis of the plots in Figure 5.11 indicates that not only the carbon isotope values for

Bolivina and Globigerinoides are different, but their departures from non-seep isotopic

signatures are different too.

We subtracted the Globigerinoides isotope departures (mean value of S13C in

control samples minus SI3C in samples throughout JSL2900-PC2) from Bolivina carbon

isotope values to find out how much of the 8l3C composition represents the biogenic

signal in Bolivina. Since the signal in Globigerinoides tests is rather noisy, we fitted a

second order polynomial regression curve to the Globigerinoides isotopic data and used

this new curve for obtaining the departures from control 8I3C values (Figure 5.17). A plot

177

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.

5 UC 8UC from which 8,3C data in •8.00 -6.00 -4.00 -2.00 0.00 2.00 have been subtracted; Bolivina R2 -R2 0.4774 y y - 0.0189x2 • 0.3178x • 3.8413 Globigerinoides Globigerinoids

0.00 0 25 8 ,JC •4.00 -2.00 Figure 5.17. (A) Vertical distribution of carbon isotopic departures in (B) Polynomial regression fitJSL2900-PC2. to A o , E a . a E

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. o f S13C that approximates the biogenic isotopic signature of Bolivina is depicted in Figure

5.17. These carbon isotope values become more negative upcore, between the bottom

sample (24 cm) and the sample situated 19 cm below the sediment surface

(-4.39°/oo).Between this latter level and the core top, the most negative 8l3C

(•4.687oo) occurs in the combined 14-13 cm sample and a slight trend towards more

positive values is apparent

We infer that a correspondence exists between the temporal distribution of the

original §t3C in Bolivina tests and that of some parameters that characterize the

foraminiferal assemblages. Thus, progressively negative 813C recorded in the bottom five

samples (Figure 5.11) matches the severe decrease in assemblage density (number of

specimens found in one gram of sediments; Figure 5.5), the decrease of species richness

(Figure 5.4), and the increase of species equitability (Figure 5.5). The 14-13 cm interval,

where the most negative 8I3C composition was recorded, is characterized by very low

species richness and assemblage density and the highest average of species equitability.

In the upper 7 cm of the core, all Bolivina 8l3C composition, species richness, and

assemblage density show increasing trends. Overall, species equitability increases

between 7 and 2 cm below the surface and drops drastically in the surface sediments

(lcm level).

DISCUSSION

Historical Record of Seep Foraminifera

The temporal distribution of foraminiferal diversity and density measures show

trends that can be related to environmental changes taking place at the JSL2900-PC2 site.

Thus, the lower part of the core is characterized by a severe reduction of foraminiferal

179

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. density (number of specimens/1 gram of sediment) and an increasing trend of species

equitability (E’). In the upper half of the core, low and relatively steady values were

recorded for foraminiferal density and species richness. Slightly increased values of these

two parameters are noticeable in the top few centimeters of the core. Species equitability

has relatively high values in much of the upper half of the core but decreases severely in

the surface sample. The distributional pattern of Shannon Wiener Index, another diversity

measure, shows changes that generally match those of the parameters already mentioned.

However, due to its sensitivity to minor components, H(S) seems less reliable in

describing the major changes of foraminiferal assemblages in JSL2900-PC2.

The foraminiferal record at JSL2900-PC2 station shows that several foraminiferal

taxa, such as Bolivina barbata , Bolivina translucens , Bulimina mexicana, Cibicidoides,

Gyroidinoides , Laticarinina, Pyrgo, and some species of Lenticulina and

Quinqueloculina, decline and disappear through time. Most of these taxa have low

relative proportions in the lower part of the core. Their disappearance from the

foraminiferal assemblages, and the decline of relative proportions of Bolivina are

associated with more balanced species distributions in the upper part of the core (see E’;

Figure 5.5). Although Bolivina declines in the upper 14 cm of the core and two major

drops of its relative proportions were recorded at 12 and 5-8 am levels, this taxon retains

its dominance above the 20 cm level. The temporal distribution of foraminiferal diversity

and density measures agrees with that of carbon isotope in Bolivina. Furthermore, a

relation between the distribution patterns of these parameters and those of percent total

carbonate and fine/coarse sediment fraction (M. Hackworth, personal communication)

can be noticed.

180

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Carbon Isotope Record

As already mentioned, I assume that isotope values of benhtic foraminiferal test,

wholly or partly reflect pore-water conditions. Thus, isotope changes in pore-water

chemistry will trigger changes in foraminiferal test isotope signature. At cold seep sites,

increased levels of DIC (Roberts and Aharon, 1994) with negative 5L3C signatures are

available for foraminiferal test secretion. “A wide range of carbon isotope values of

foraminiferal carbonate might be expected in methane seep subenvironments because

probable spatial heterogeneity in seepage. The variability of subenvironments and the

range of 8t3C values would be expected to increase with the activity of the seep”

(Rathbum et al., 2000).

Based on the estimated 13.4 cm/ky sedimentation rate (M. Hackworth, personal

communication), JSL2900-PC2 covers a time range of about 1.8 ky. The distribution of

the Bolivina S13C data in JSL2900-PC2 suggests that seepage activity at this site is less

than 1.8 ky old. The values o f the carbon isotope turn from normal (-1.51 ± 0.41 °/oo

PDB) at the bottom of the core (24-23 cm) into progressively negative values up to 13 cm

below the surface, and then turn slightly towards more positive values up to the surface.

We have seen so far that the carbon isotope measured in Bolivina was acquired

during both test secretion and diagenesis. Diagenesis was suggested by the upcore trend

of 513C measured in the planktonic species Globigerinoides ruber and by the carbonate

growths observed on some specimens of both Bolivina and Globigerinoides. A

relationship exists between the trend of Globigerinoides 8l3C in JSL2900-PC2 (Figure

5.11) on one side and the trend of % total carbonate and that of the fine over coarse

181

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. sediment fraction ratio (Figure 5.12) on the other side. A greater concentration of

carbonate, mainly in the form of carbonate nodules in the upper 20 cm of the core, must

be related to the existence of increased DIC. We assume that increased levels of DIC

(with 8l3C composition reflecting the hydrocarbon seep activity) not only influence the

isotopic composition acquired by benhtic Foraminifera during test secretion but also play

a role in the diagenetic changes that take place in tests of both benthic and plantktonic

Foraminifera. Since the increased DIC concentration is attributed to microbial processes

involving sulfate reduction and hydrocarbon oxidation (Roberts and Aharon, 1994), it is

expected that carbonate nodule formation as well as the diagenetic processes (carbonate

overgrowths) responsible for isotope change of foraminiferal tests take place mainly in

near surface sediments. Once buried to a certain depth (> 2-3 cm?) foraminiferal tests

may preserve an unaltered isotopic signature even though the hydrocarbon emissions

remain active over extended periods of time. This interpretation is supported by the

upcore trends of SI3C in Globigerinoides , % total carbonate and fine/coarse fraction ratio.

If hydrocarbon emissions had influenced the isotopic composition of foraminiferal tests

all along during the burial, one should expect a downcore increasing trend of S13C in

Globigerinoides. Similarly, the amount of carbonate nodules should increase with depth

if they had formed at any depth while the emissions were active. The S13C signals,

however, show both increasing and decreasing trends along the length of the core. This is

why they may be solely controlled by the intensity of seep activity.

S13C measured on fossil specimens collected at methane-influenced environments

(Sen Gupta and Aharon, 1994; Wefer et al., 1994; Kennet et al., 1996; Rathbum et al.,

2000) show a range of values up to 5 ° /q q . Measurements performed for this study (P.

182

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Aharon, personal communication) revealed a high of 8.26 %) 513C departure from

normal values, corresponding to the most negative value (-10.15 °/oo) so far recorded in

these environments. However, eliminating the diagenetic effect, the residual values

(maximum departure = -3.57 °/oo; most negative value = -5.46 °/oo) fall within limits

found in previous studies.

Significant Biological Trends

The severe reduction of both species richness and foraminiferal density (number

of specimens) in the lower part of the analyzed core reflects the biological response of

these microorganisms to a progressively deteriorating microenvironemnt. However, since

carbonate nodules incorporate foraminiferal tests (both planktonic and benthic), a portion

(probably minor) of the upcore reduction of foraminiferal density is due to diagenetic

processes. Several species present in the bottom sample (23-24 cm) disappear shortly

after this level; this change probably indicates a severe environmental change, i.e.,

initiation of seepage. The rapid disappearance of these species coincides with an

increased relative proportion of the genus Bolivina immediately above 24-cm sample,

showing that this taxon can better cope with the harsh environmental conditions of

hydrocarbon seeps. Nevertheless, as our data show, all foraminiferal taxa, including

Boltvina , decline rapidly due to continual hydrocarbon emission. The PC A performed on

selected foraminiferal data (discussed earlier) revealed a significant change in loadings of

Boltvina, Trifarina brady, Gavelinopsis translucens , and Osangularia rugosa within

factor 1. As shown by the temporal distribution of factor 1 scores (Figure 5.8), most of

this change takes place in the upper 8 cm of the core where a slightly reduced seep

activity is suggested by the reduced trend of % total carbonate and increased fine/coarse

183

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. sediment fraction (M. Hackworth personal communication), and somewhat less negative

S13C o f Bolivina tests.

Our results show that all species previously identified within living foraminiferal

populations at hydrocarbon seep in the Gulf (Sen Gupta et al., 1997) are present in most

of the core samples and that they tolerate the stressful environmental conditions

associated with seeps. Species of Bolivina were frequently reported from severely

oxygen-depleted environments (see Bernhard’s review, 1999) including hydrocarbon

seeps (Akimoto et al., 1994; Sen Gupta and Aharon, 1994; Sen Gupta et al., 1997;

Rathbum et al., 2000; Bernhard et al., in press). Given its high relative proportions

through most of the core, we infer that Bolivina is the most tolerant taxon in JSL2900-

PC2 assemblages. Furthermore, taxa such as Cassidulina, Bulimina, Epistominella , and

Uvigerina peregrina are reported from seeps in other marine areas including the Gulf

(Akimoto et al., 1994; Sen Gupta et al., 1997; Jones, 1993; Sen Gupta and Aharon, 1994;

Bernhard et al., in press). However, differences in foraminiferal compositions exist

between seep environments located in different areas. They may be related to common

limiting factors (depths, temperature etc.) but also, as Bernhard et al. (in press) noted, to a

different nature of the hydrocarbon emission.

The presence of Bolivina and other major survivor taxa {Bulimina, Gavelinopsis,

Cassidulina, Trifarina, Osangularia) before the seepage initiation at JSL2900-PC2 (see

Figure 5.2) supports previous observations according to which calcareous taxa living at

cold seeps are not exotic, they are recruits from the surrounding normal habitats (Sen

Gupta and Aharon, 1994 - Gulf of Mexico; Kitazato, 1996 - Sagami Bay, Japan; Sen

Gupta et al., 1997 - Gulf of Mexico; Bernhard et al., in press - Monterey Bay, California).

184

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Although no species seems to live solely at the seep sites, some are more abundant at

seeps than they are in the non-seep surroundings (Bernhard et. al., in press; Akimoto et

al., 1994). This observation and the organic rich nature of hydrocarbon seeps lead to the

suggestion that foraminiferal species are attracted to seep environments (Rathbum, 2000).

Our results, however, show that the abundance of all species declines in response to

hydrocarbon emissions. Thus, it seems that the few species living at hydrocarbon seep

sites in the Green Canyon sites do not really benefit from the increased food supplies

available in these environments.

CONCLUSIONS

Several species of benthic Foraminifera live within the top few centimeters at

hydrocarbon seep sites in Green Canyon. The common species are Bolivina albatrossi, B.

ordinaria, Cassidulina neocarinata, Osangularia rugosa, Fursenkoina compressa, and

Trifarina bradyi. Furthermore, it seems that Bolivina has a higher tolerance than other

taxa to the harsh conditions associated with seeps. The data we examined so far indicate

that certain foraminiferal species of slope environments can survive limited amounts of

both oil and H 2 S but none of the species apparently benefits from these compounds.

Our results show that the isotopic signatures of benthic foraminiferal species are

good indicators of hydrocarbon releases and can be used in historical reconstruction of

seep activity. In the analyzed core, temporal distribution of the isotopic composition of

Bolivina tests suggests that seep activity begun about 1600 years ago. A better

understanding of the relationship between foraminiferal isotopic signatures and methane

seepage will result from additional work on isotopic composition of species that currently

185

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. live at active seep sites. Other species living in these environments, especially those

common in some other areas of the world, should be included in future isotopic analysis.

Negative carbon isotope excursions in the genus Bolivina associated with

biomineralization constitute additional proof that these organisms grow and live in

sediments of hydrocarbon seeps. We infer that benthic foraminifera populating the cold

vents of northern Gulf of Mexico reproduce at and/or very close to the surface where

more oxygen is available and prevalent amounts of H 2S and oil do not interfere with this

process.

A severe decline of species richness and foraminiferal density represents the

major foraminiferal response to environmental changes that affected the JSL2900-PC2

site. The presence of survivor species before seepage initiation supports the previous

observation that living Foraminifera at seeps sites are not endemic.

186

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPENDIX

Species Abundance Data for JSL2900-PC2 Core

JSL2900 - PC2 - Raw Data

Sp/Depth 0-1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm Ammod. Amph 1 1 1 Am phy02 Angulo A stacolus B_alb 7 3 3 2 2 1 1 B_barb B_cap B Jra g 1 5 3 B_otd 10 4 13 2 9 3 2 B Jra n s B J o w 4 1 1 B_ord_tap 2 1 4 B_sub B_und 9 3 13 2 4 1 0 Bul_marg 1 B_ella 1 Bol B uljalaz 5 1 3 2 2 2 B u ljn e x Bul_ac 1 6 5 4 6 12 3 Bulim? C a rib jm x C ass_curv 1 1 C ass_nc 1 3 5 1 7 6 1 C a ssjsu b 1 1 C ass_nod G b jn c r G b jo b 1 1 C ib ja g G b_rot G b jo Gb_pah 3 1 Chil_ool G avulina 1 Dentalina 1 Egg 1 Ep_ax 1 1 EpisK?) E p ja g G av_tr 18 4 5 9 4 9 3 2 Gfob_aff (JSL2900 - PC2 - Raw Data continued)

187

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 0-1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm G yr Gyro_Lae 1 Gyro44 Gym H oegfjai Hyato 1 1 Hyalo-str F iss 1 1 1 1 6 2 F issJB nt F iss J a a v 1 1 FissB 2 F is s jis p d Fis_big Fiss_bi 1 F issjsp B H ansjso ld 1 2 3 1 Karr_brdy LentOI L a g jn e x Lagena 1 L a g ja e v Lat_pau L ent_cak 1 1 Lent02 1 1 Lent? 1 L entjsm tt LentD iff 1 MilltoBdes 10 4 4 M rgjna Margin 1 M il_drc 2 1 Nonion N c rjn in N eoLnt Oof 0 rkUimb O s_m g 5 1 6 5 4 7 2 O s_culter P sdN onja Pijarim 1 1 2 2 1 P lja v 1 1 1 2 Poly Pul_bul

(JSL2900 - PC2 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 0-1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm P u IJw l P uljsub 1 Pyr_obl Pyr_m Qj B t 8 4 5 Q Jam arck Q sp . 1 SlgmjBlttpt Staint S yphjM d 1 T b r d y 6 2 7 2 4 5 2 1 Tritoc 1 U_per 3 4 3 2 5 2 1 Valv_mex sp_1 sp_2 sp_3 sp_4 sp_5 sp_6 sp_7 sp_8 sp_9 1 sp_10 1 sp_11 1 sp_12 1 sp_13 1 sp_14 1 sp_15 1 sp_16 1 sp_17 sp_18 1 sp_19 sp_20 sp_20 sp_21 sp_22 sp_23 sp_24 sp_25 sp_28 sp_27 sp_28 (JSL2900 - PC2 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13 cm 13-14 cm 14-15 cm 15-16 cm Ammod. 1 Am ph 1 1 1 1 Am phy02 Anguto A stacolus 1 B_alb 1 3 2 1 7 8 25 B_barb B_cap B_frag 1 4 1 B_ord 6 6 5 18 6 12 9 38 B Jra n s 1 B Jo w 1 1 3 4 B jx d J a p 4 B jsu b 1 B_und 6 2 2 7 2 8 1 B u ljn a rg 4 B j b IIb So/ 1 B uljalaz 2 2 1 8 Bul_m ex 1 4 1 1 B u lja c 3 5 7 7 1 Bulim? Carib_mex 1 C a s s jx u v 1 3 C ass_nc 2 4 3 3 7 15 C ass_sub 3 C ass_nod C ib jn c r Cib_rob 1 2 C ib ja g C lb jo t C ib jo Cib_pah 1 5 ChiljDol 1 Clavulina Dentalina Egg 1 E p ja x 1 1 Epist(?) E p ja g G a v jr 1 4 6 3 1 7 7 G lo b jstf (JSL2900 - PC2 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13 cm 13-14 cm 14-15 cm 15-16 cm G yr 1 6 Gyro_Lae Gyro44 2 G ym H oegljal 1 Hyato 1 H yalo-str F iss 2 3 F IssJB nt F iss J a e v FissB 1 F iss_hspd Fis_big Fiss_bi F Issjsp B 1 H a nsjsold 1 2 1 1 2 Karr_bnfy LentOI 1 L a g jn e x Lagena 1 L a g ja a v 2 Lat_pau 1 4 Lent_calc 1 2 Lent02 1 Lent? L entjsm ll 1 1 LentDHf MUHoOdes 1 6 1 M rgjna Margin 1 M lljdrc 2 1 Nonion N c rjn in N eoLnt Ool 1 Orid-umb O s_rug 4 1 1 3 2 O s_cultar 1 PsdNon_a P ljarim 1 P lja v 1 Poly 3 Pul_bul (JSL2900 - PC2 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. S p/Depth 8-9 cm 9-10 on 10-11 an 11-12 an 12-13 an 13-14 an 14-15 a n 15-16 a n P uljsub P yrjobl 1 1 Pyr_m 1 Q J a t 4 5 Q Jam arck 1 1 1 Q Sigmjallipt 1 1 Staint 1 S y p h ju ri 1 1 1 1 6 T_brtfy 1 1 1 Tribe U_par 1 4 4 2 11 Valv_mex sp_1 sp_2 sp_3 sp_4 sp_5 sp_6 sp_7 1 sp_8 1 sp_9 sp_10 sp_11 sp_12 sp_13 sp_14 sp_1S sp_18 sp_17 sp_18 sp_19 1 sp_20 1 sp_20 1 sp_21 1 sp_22 1 sp_23 1 sp_24 1 sp_25 sp_26 sp_27 sp_28 (JSL2900 - PC2 - Raw Data continued)

192

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 16-17 an 17-18 an 18-19 an 19-20 an 20-21 an 21-22 a n 22-23 a n 23-24 a n Ammod. 1 Am ph 2 1 1 1 Am phy02 1 Angulo 1 A stacolus B jalb 1 11 6 2 1 23 8 36 B_baib 1 2 1 B_cap 1 B Jra g 1 3 3 4 2 3 B_ord 1 39 4 33 56 24 23 B Jra n s 1 1 2 B Jo w 1 2 6 11 5 B jo rd J a p 26 25 B jsu b 2 B_und 4 2 2 Bul_marg 2 3 2 1

B j b IIs So/ Bul_alaz 1 4 2 2 9 3 B u l_ m x 1 1 3 2 B u lja c 2 3 4 Bulim? 1 C a ribjn ex Cass_curv 1 2 2 C ass_nc 7 6 9 2 6 3 3 8 C a ssjsu b 3 1 1 1 C a ssjn o d 1 C ib jn cr 1 C ib jo b 1 Cib_mg 1 Cib_rot 1 C ib jo 1 Cib_pah 1 4 2 1 2 2 4 Chil_ool 1 1 3 Clavullna Dentalina 1 1

S g g Ep_ax 2 2 1 2 2 8 9 7 Epist(?) 1 Ep_teg 1 G a v jr 10 8 7 5 9 19 6 7 G lobjB ff 1 (JSL2900 - PC2 - Raw Data continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 16-17 cm 17-18 cm 18-19 cm 19-20 cm 20-21 cm 21-22 cm 22-23 cm 23-24 cm G yr 1 6 Gyro_Lae G ym 44 2 Gyro H oegl_el 1 Hyato 1 Hyalo-str F iss 2 3 F is s jtn t F is s ja a v FissB 1 Fiss_hspd Fls_blg Fiss_bi F issjsp B 1 H an sjso ld 1 2 1 1 2 Karr_bnty LantOI 1 L a g jn a x Lagena 1 L a g ja a v 2 Lat_pau 1 4 Lant_cafo 1 2 Lent02 1 Lent? L en tjsm ll 1 1 LantDiff MUBoBdas 1 6 1 M rgjna Margin 1 M ilja'rc 2 1 Nonion N c rjn in NaoLnt Oo/ 1 Orid-umb Os_rug 4 1 1 3 2 O s_culter 1 PsdNon_a Pljarim 1 P!_fav 1 Poly 3 P uIJ m I (JSL2900 - PC2 - Raw Data continued)

194

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 16-17 cm 17-18 cm 18-19 cm 19-20 cm 20-21 cm 21-22 cm 22-23 cm 23-24 cm P u ljsu b 1 1 Pyr_obl P y r jn 1 1 Q J a t Q Jam arck Q Sigmjalllpt 1 1 Staint 1 S y p h jm l 1 5 1 5 3 2 3 T_brdy 3 2 1 5 1 5 Triloc U_per 2 7 2 1 8 7 4 17 V a tifjn ex 2 sp_1 2 sp_2 1 sp_3 1 sp_4 1 sp JS 1 sp JS 1 sp_7 sp_8 sp _ 9 sp_10 sp_11 sp_12 sp_13 sp_14 sp_15 sp_16 sp_17 sp_18 sp_19 sp_20 sp_20 sp_21 sp_22 sp_23 sp_24 sp_25 1 sp_26 1 sp_27 1 sp_28 1

195

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1ST .2900 - PC2 - Relative Proportions

Depth 0-1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm Am m od. 0 0 0 0 0 0 0 0 Am ph 0 0 0 0 0 0 0 0 Am phy02 0 0 0 0 0 0 0 0 Angulo 0 0 0 0 0 0 0 0 A stacolus 0 0 0 0 0 0 0 0 B jalb 0.07292 0.07317 0.04478 0.04255 0.02941 0.01333 0.04167 0 B_baib 0 0 0 0 0 0 0 0 B _cap 0 0 0 0 0 0 0 0 B_frag 0.01042 0.12195 0 0 0.04412 0 0 0 B _ofd 0.10417 0 0.0597 0.2766 0.02941 0.12 0.125 0.09524 B J ra n s 0 0 0 0 0 0 0 0 B J o w 0 0 0.0597 0 0 0.01333 0 0.04762 B _ordJap 0.02083 0 0 0.02128 0.05882 0 0 0 B jsu b 0 0 0 0 0 0 0 0 B ju n d 0.09375 0.07317 0.19403 0.04255 0 0.05333 0.04167 0 Bul_marg 0.01042 0 0 0 0 0 0 0 B jalla 0 0 0 0 0 0 0 0.04762 B ol 0 0 0 0 0 0 0 0 Bul_aJaz 0.05208 0.02439 0.04478 0 0.02941 0.02667 0.08333 0 B ul_m ex 0 0 0 0 0 0 0 0 B u lja c 0.01042 0.14634 0.07463 0.08511 0.08824 0.16 0 0.14286 Bu«m? 0 0 0 0 0 0 0 0 C a tib jn e x 0 0 0 0 0 0 0 0 C ass_curv 0.01042 0 0 0 0 0.01333 0 0 C ass_nc 0.01042 0.07317 0.07463 0.02128 0.10294 0.08 0.04167 0 C a ssjsu b 0.01042 0 0 0 0 0.01333 0 0 C ass_nod 0 0 0 0 0 0 0 0 C ib jn c r 0 0 0 0 0 0 0 0 Cib_mb 0 0 0 0.02128 0.01471 0 0 0 G b je g 0 0 0 0 0 0 0 0 Cib_rot 0 0 0 0 0 0 0 0 C lb jo 0 0 0 0 0 0 0 0 Clb_pah 0 0 0.04478 0 0 0.01333 0 0 Chil_ool 0 0 0 0 0 0 0 0 Clavulina 0 0 0 0 0 0 0 0.04762 Dentalina 0 0.02439 0 0 0 0 0 0 Egg 0 0 0 0 0 0 0 0.04762 E p ja x 0 0 0 0 0 0.01333 0 0.04762 Epist(?) 0 0 0 0 0 0 0 0 E p je g 0 0 0 0 0 0 0 0 G a v jr 0.1875 0.09756 0.07463 0.19149 0.05882 0.12 0.125 0.09524 G fo b ja ff 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

196

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 0-1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm Gyr 0 0 0 0 0 0 0 0 Gym_Lae 0.01042 0 0 0 0 0 0 0 Gyro44 0 0 0 0 0 0 0 0 G ym 0 0 0 0 0 0 0 0 H oegljal 0 0 0 0 0 0 0 0 Hyafo 0.01042 0 0 0 0 0.01333 0 0 Hyalo-str 0 0 0 0 0 0 0 0 F iss 0.01042 0.02439 0.01493 0.02128 0.08824 0 0 0.09524 F issJIint 0 0 0 0 0 0 0 0 F is s ja e v 0 0 0 0.02128 0.01471 0 0 0 FissB 0.02083 0 0 0 0 0 0 0 F is s jis p d 0 0 0 0 0 0 0 0 F lsjiig 0 0 0 0 0 0 0 0 F ls s jji 0 0 0 0 0 0.01333 0 0 F fssjspB 0 0 0 0 0 0 0 0 H ansjsold 0 0 0 0.02128 0.02941 0.04 0.04167 0 Kair_brdy 0 0 0 0 0 0 0 0 LentOI 0 0 0 0 0 0 0 0 L a g jn e x 0 0 0 0 0 0 0 0 Lagena 0.01042 0 0 0 0 0 0 0 L a g ja e v 0 0 0 0 0 0 0 0 Lat_pau 0 0 0 0 0 0 0 0 Lent_calc 0 0.02439 0 0.02128 0 0 0 0 Lent02 0.01042 0 0 0 0 0 0.04167 0 Lent? 0 0 0 0 0 0.01333 0 0 L entjsm ll 0 0 0 0 0 0 0 0 LantDiff 0 0 0.01493 0 0 0 0 0 im o B d e s 0 0 0 0 0.14706 0 0.16667 0.19048 M rgjna 0 0 0 0 0 0 0 0 Margin 0 0 0 0 0 0 0.04167 0 M iljdrc 0.02083 0 0 0 0 0 0.04167 0 Nonion 0 0 0 0 0 0 0 0 N c rjn in 0 0 0 0 0 0 0 0 NeoLnt 0 0 0 0 0 0 0 0 Oo/ 0 0 0 0 0 0 0 0 OrkPumb 0 0 0 0 0 0 0 0 Os_rug 0.05208 0.02439 0.08955 0.10638 0.05882 0.09333 0 0.09524 O s_cultar 0 0 0 0 0 0 0 0 PsdNon_a 0 0 0 0 0 0 0 0 Pljarim 0.01042 0.02439 0.02985 0 0.02941 0.01333 0 0 P lja v 0 0.02439 0.01493 0.02128 0.02941 0 0 0 Pofy 0 0 0 0 0 0 0 0 Pul_bul 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

197

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 0*1 cm 1-2cm 2-3 cm 3-4 cm 4-5 cm 5-6 cm 6-7 cm 7-8 cm P uljsub 0 0 0 0 0 0 0.04167 0 P yrjobl 0 0 0 0 0 0 0 0 P yrjm 0 0 0 0 0 0 0 0 Q J a t 0.08333 0.09756 0 0 0 0.06667 0 0 Q J a n w c k 0 0 0 0 0 0 0 0 Q 0.01042 0 0 0 0 0 0 0 SigmjBlOpt 0 0 0 0 0 0 0 0 Staint 0 0 0 0 0 0 0 0 S y p h jm t 0 0 0 0 0 0.01333 0 0 T_brdy 0.0625 0.04878 0.10448 0.04255 0.05882 0.06667 0.08333 0.04762 Triloc 0.01042 0 0 0 0 0 0 0 U j m 0.03125 0.09756 0.04478 0.04255 0.07353 0.02667 0.04167 0 Vatv_mex 0 0 0 0 0 0 0 0 sp_1 0 0 0 0 0 0 0 0 sp_2 0 0 0 0 0 0 0 0 sp_3 0 0 0 0 0 0 0 0 sp_4 0 0 0 0 0 0 0 0 sp_S 0 0 0 0 0 0 0 0 s p jS 0 0 0 0 0 0 0 0 sp_7 0 0 0 0 0 0 0 0 sp_8 0 0 0 0 0 0 0 0 sp_9 0.01042 0 0 0 0 0 0 0 sp_10 0.01042 0 0 0 0 0 0 0 sp.,11 0.01042 0 0 0 0 0 0 0 sp_12 0.01042 0 0 0 0 0 0 0 sp_13 0 0 0.01493 0 0 0 0 0 sp_14 0 0 0 0.02128 0 0 0 0 sp_1S 0 0 0 0.02128 0 0 0 0 sp_16 0 0 0 0.02128 0 0 0 0 sp_17 0 0 0 0 0 0 0 0 sp_18 0 0 0 0 0.01471 0 0 0 sp_19 0 0 0 0 0 0 0 0 sp_20 0 0 0 0 0 0 0 0 sp_20 0 0 0 0 0 0 0 0 sp_21 0 0 0 0 0 0 0 0 sp_22 0 0 0 0 0 0 0 0 sp_23 0 0 0 0 0 0 0 0 sp_24 0 0 0 0 0 0 0 0 sp_25 0 0 0 0 0 0 0 0 sp_26 0 0 0 0 0 0 0 0 sp_27 0 0 0 0 0 0 0 0 sp_28 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

198

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13 cm 13-14 cm 14-15 cm 15-16 cm AmmotL 0 0 0 0 0 0.02174 0 0 Am ph 0 0 0 0 0 0 0 0 Am phy02 0 0 0 0 0 0 0 0 Angulo 0 0 0 0 0 0 0 0 A stacolus 0 0 0.03571 0 0 0 0 0 B_alb 0.04 0 0.10714 0.02532 0.02439 0.15217 0.12903 0.15723 B_barb 0 0 0 0 0 0 0 0 B_cap 0 0 0 0 0 0 0 0 B Jra g 0 0 0 0 0.02439 0.08696 0 0.00629 B_ord 0.24 0.33333 0.17857 0.22785 0.14634 0.26087 0.14516 0.23899 B Jra n s 0 0 0 0 0 0 0 0.00629 B Jo w 0.04 0.05556 0 0 0 0 0.04839 0.02516 B jx d J a p 0 0 0 0.05063 0 0 0 0 B jsu b 0 0 0 0 0 0 0 0.00629 B ju n d 0.24 0 0.07143 0.02532 0.17073 0.04348 0.12903 0.00629 Bul_marg 0 0 0 0 0 0 0 0.02516 B jslla 0 0 0 0 0 0 0 0 Bol 0 0 0 0.01266 0 0 0 0 B uljalaz 0 0 0 0.02532 0 0.04348 0.01613 0.05031 Bul_mex 0 0.05556 0 0.05063 0 0 0.01613 0.00629 B u lja c 0 0.16667 0.17857 0.08861 0.17073 0.02174 0 0 Buttm? 0 0 0 0 0 0 0 0 C a rib jn ex 0 0 0 0 0 0 0 0.00629 Cass_curv 0 0 0 0.01266 0 0 0 0.01887 C ass_nc 0.08 0 0 0.05063 0.07317 0.06522 0.1129 0.09434 C a ssjsu b 0 0 0 0.03797 0 0 0 0 C ass_nod 0 0 0 0 0 0 0 0 C ib jn c r 0 0 0 0 0 0 0 0 O b_m b 0 0 0 0 0.02439 0.04348 0 0 C ib_ng 0 0 0 0 0 0 0 0 Cib_rot 0 0 0 0 0 0 0 0 C ib jo 0 0 0 0 0 0 0 0 C ibjpah 0 0 0 0.01266 0 0 0.08065 0 C hiljool 0 0 0 0 0 0 0 0.00629 Clavullna 0 0 0 0 0 0 0 0 Dantallna 0 0 0 0 0 0 0 0 Egg 0 0.05556 0 0 0 0 0 0 Ep_ex 0.04 0 0.03571 0 0 0 0 0 Epistf?) 0 0 0 0 0 0 0 0 Ep_reg 0 0 0 0 0 0 0 0 Gav_tr 0.04 0 0.14286 0.07595 0.07317 0.02174 0.1129 0.04403 G lob_aff 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13 cm 13-14 cm 14-15 cm 15-16 cm Gyr 0 0 0 0.012658 0 0 0 0.037736 Gyro_Lae 0 0 0 0 0 0 0 0 Gym44 0 0 0 0 0 0 0 0.012579 Gym 0 0 0 0 0 0 0 0 H oegljal 0 0 0 0 0 0 0 0.006289 Hyalo 0 0 0.035714 0 0 0 0 0 H yatostr 0 0 0 0 0 0 0 0 F iss 0 0.111111 0 0.037975 0 0 0 0 FissJU nt 0 0 0 0 0 0 0 0 F iss J a w 0 0 0 0 0 0 0 0 FissB 0 0 0 0 0 0 0 0.006289 F is s jis p d 0 0 0 0 0 0 0 0 F isJ)ig 0 0 0 0 0 0 0 0 Fiss_bi 0 0 0 0 0 0 0 0 Fiss_spB 0 0.055556 0 0 0 0 0 0 H ansjsold 0 0.055556 0 0.025316 0 0.021739 0.016129 0.012579 K a rrjm ty 0 0 0 0 0 0 0 0 LentOI 0 0 0 0.012658 0 0 0 0 L a g jn e x 0 0 0 0 0 0 0 0 Lagena 0 0 0.035714 0 0 0 0 0 L a g ja e v 0 0 0 0 0 0 0 0.012579 L a tjx u 0 0 0 0 0 0.021739 0 0.025157 Lent_catc 0 0 0 0 0 0.021739 0 0.012579 Lent02 0 0 0 0.012658 0 0 0 0 Lent? 0 0 0 0 0 0 0 0 Lent_smll 0.04 0 0 0 0 0 0.016129 0 LentDiff 0 0 0 0 0 0 0 0 Milliolides 0 0 0.035714 0 0.146341 0 0 0.006289 M rgjna 0 0 0 0 0 0 0 0 Margin 0 0 0 0 0 0 0 0.006289 M tijarc 0.08 0 0 0 0 0.021739 0 0 Nonion 0 0 0 0 0 0 0 0 N c rjn in 0 0 0 0 0 0 0 0 NaoLnt 0 0 0 0 0 0 0 0 Oo/ 0 0 0 0.012658 0 0 0 0 Orid-umb 0 0 0 0 0 0 0 0 Os_rug 0 0 0 0.050633 0.02439 0.021739 0.048387 0.012579 O sjcuttar 0 0 0 0 0 0 0 0.006289 PsdNon_a 0 0 0 0 0 0 0 0 Pl_arim 0 0 0 0 0 0 0 0.006289 P lja v 0 0 0 0 0 0 0 0.006289 Poly 0 0 0 0 0 0 0.048387 0 P u IJw l 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

200

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 8-9 cm 9-10 cm 10-11 cm 11-12 cm 12-13 cm 13-14 cm 14-15 cm 15-16 cm P uljsub 0 0 0 0 0 0 0 0 Pyr_obl 0 0.05556 0 0 0 0.02174 0 0 Pyr_m 0 0 0 0 0 0 0 0.00629 QJ a t 0.16 0 0 0.06329 0 0 0 0 Q Jam arck 0 0.05556 0.03571 0 0 0.02174 0 0 Q 0 0 0 0 0 0 0 0 SigmjBlOpt 0 0 0 0 0.02439 0 0 0.00629 Staint 0 0 0 0.01266 0 0 0 0 Syph_brd 0 0 0.03571 0.01266 0 0.02174 0.01613 0.03774 T_bnfy 0 0 0 0.01266 0 0 0.01613 0.00629 T rikx 0 0 0 0 0 0 0 0 U_per 0 0 0.03571 0 0.09756 0.08696 0.03226 0.06918 Valv_mex 0 0 0 0 0 0 0 0 sp_1 0 0 0 0 0 0 0 0 sp_2 0 0 0 0 0 0 0 0 sp_3 0 0 0 0 0 0 0 0 sp_4 0 0 0 0 0 0 0 0 sp_5 0 0 0 0 0 0 0 0 sp_6 0 0 0 0 0 0 0 0 sp_7 0 0 0 0.01266 0 0 0 0 sp_8 0 0 0 0.01266 0 0 0 0 spJB 0 0 0 0 0 0 0 0 sp_10 0 0 0 0 0 0 0 0 sp_11 0 0 0 0 0 0 0 0 sp_12 0 0 0 0 0 0 0 0 sp_13 0 0 0 0 0 0 0 0 sp_14 0 0 0 0 0 0 0 0 sp_15 0 0 0 0 0 0 0 0 sp_16 0 0 0 0 0 0 0 0 sp_17 0 0 0 0 0 0 0 0 sp_18 0 0 0 0 0 0 0 0 sp_19 0 0.05556 0 0 0 0 0 0 sp_20 0 0 0 0 0.02439 0 0 0 sp_20 0 0 0 0 0.02439 0 0 0 sp_21 0 0 0 0 0 0.02174 0 0 sp_22 0 0 0 0 0 0.02174 0 0 sp_23 0 0 0 0 0 0.02174 0 0 sp_24 0 0 0 0 0 0 0 0.00629 sp_2S 0 0 0 0 0 0 0 0 sp_26 0 0 0 0 0 0 0 0 sp_27 0 0 0 0 0 0 0 0 sp_28 0 0 0 0 0 0 0 0 (JSL2900 - PC2 - Relative Proportions continued)

201

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/D epth 16-17 cm 17-18 cm 18-19 cm 19-20 cm 20-21 cm 21-22 cm 22-23 cm 23-24 cm Ammod. 0 0 0 0 0 0.00578 0 0 Am ph 0.02273 0 0 0 0 0 0 0 Am phy02 0.02273 0 0 0 0 0 0 0 Angulo 0.02273 0 0 0 0 0 0 0 A stacolus 0 0 0 0 0 0 0 0 B_alb 0.02273 0.11 0.06522 0.06897 0.0098 0.13295 0.11268 0.19459 B_barb 0 0 0.01087 0 0 0.01156 0 0.00541 B_cap 0 0 0 0 0 0.00578 0 0 B Jrag 0 0.01 0.03261 0.10345 0.03922 0.01156 0 0.01622 B_ord 0.02273 0 0.42391 0.13793 0.32353 0.3237 0.33803 0.12432 B Jra n s 0 0.01 0 0 0 0 0.01408 0.01081 B Jo w 0.02273 0.02 0.06522 0 0.10784 0.0289 0 0 B_ord_tap 0 0.26 0 0 0 0 0 0.13514 B_sub 0 0 0 0 0.01961 0 0 0 B ju n d 0 0 0 0.13793 0 0.01156 0 0.01081 Butjm arg 0.04545 0 0.03261 0 0 0.01156 0.01408 0 BjBlla 0 0 0 0 0 0 0 0 Bol 0 0 0 0 0 0 0 0 B uljalaz 0.02273 0.04 0.02174 0 0.01961 0.05202 0 0.01622 B u ljn e x 0.02273 0.01 0 0 0 0 0.04225 0.01081 B u lja e 0 0.02 0 0 0.02941 0 0 0.02162 Bullm? 0.02273 0 0 0 0 0 0 0 Carib_mex 0 0 0 0 0 0 0 0 Cass_curv 0 0 0 0.03448 0 0.01156 0.02817 0 C ass_nc 0.15909 0.06 0.09763 0.06897 0.05882 0.01734 0.04225 0.04324 C a ssjsu b 0 0 0.03261 0 0.0098 0 0.01408 0.00541 C ass_nod 0 0 0 0 0.0098 0 0 0 C lb jn c r 0 0 0 0 0 0 0 0.00541 Clb_rob 0.02273 0 0 0 0 0 0 0 Cib_reg 0 0 0 0 0 0 0 0.00541 Cib_m t 0.02273 0 0 0 0 0 0 0 C ib jo 0 0 0 0 0 0 0 0.00541 Cib_pah 0.02273 0.04 0.02174 0.03448 0.01961 0.01156 0 0.02162 Chil_ool 0.02273 0 0 0.03448 0 0.01734 0 0 Clavulina 0 0 0 0 0 0 0 0 Dentalfna 0 0 0.01087 0 0 0.00578 0 0 Egg 0 0 0 0 0 0 0 0 E p ja x 0.04545 0.02 0.01087 0.06897 0.01961 0.04624 0.12676 0.03784 Epist(?) 0 0 0 0 0.0098 0 0 0 Ep_reg 0 0 0 0 0 0 0 0.00541 Gav_tr 0.22727 0.08 0.07609 0.17241 0.08824 0.10983 0.08451 0.03784 Glob_aff 0 0 0 0 0 0 0 0.00541 (JSL2900 - PC2 - Relative Proportions continued)

202

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 16-17 cm 17-18 cm 18-19 cm 19-20 cm 20-21 cm 21-22 cm 22-23 cm 23-24 cm Gyr 0 0 0 0 0 0 0 0.00541 Gym_Lae 0 0 0 0 0 0 0 0 Gyro44 0.02273 0 0.02174 0 0.0098 0.01156 0 0 Gyro 0 0 0 0.03448 0 0 0 0 Hoegl_el 0 0.01 0 0 0 0 0 0 Hyak) 0.02273 0 0 0 0 0.00578 0 0 H ya to -st 0 0 0 0 0 0.00578 0 0 F iss 0.02273 0 0 0 0 0.00578 0 0.00541 FissjfBnt 0 0 0 0 0 0.00578 0 0 F is s ja e v 0 0 0 0 0 0 0 0 FissB 0 0 0 0 0 0 0 0 Fiss_hspd 0 0.01 0 0 0 0 0 0 F is jiig 0 0.01 0 0 0 0 0 0 Fiss_bi 0 0 0 0 0 0 0 0 Fiss_spB 0 0 0 0 0 0 0 0 H ans_sold 0.02273 0 0.01087 0 0.01961 0.01156 0 0.00541 Karr_brdy 0 0 0 0 0.0098 0 0 0 LentOI 0 0 0 0 0 0.00578 0 0 L a g jn e x 0 0 0 0 0 0.00578 0 0 Lagena 0 0 0 0 0 0 0 0 L a g ja e v 0 0 0 0 0.0098 0 0 0 Lat_pau 0 0 0 0 0.0098 0.01734 0.01408 0 Lant_calc 0 0 0.01087 0 0 0 0.01408 0 Lent02 0 0 0 0 0 0 0 0 Lent? 0 0.01 0 0 0 0 0 0 L antjsm ll 0 0.01 0 0 0 0 0 0 LentD iff 0 0 0 0 0 0 0 0 MBHottdes 0 0 0 0 0 0 0 0 M rgjna 0 0 0 0 0 0 0 0.00541 Margin 0 0 0 0 0 0 0.01408 0.01622 M iljarc 0 0 0 0 0 0 0 0.00541 Nonion 0 0 0 0 0 0 0 0.00541 N c rjn in 0 0 0 0 0 0 0 0.00541 NeoLnt 0 0 0 0 0 0 0 0.00541 Oo/ 0 0 0 0 0.0098 0 0 0 0 rid-umb 0 0 0 0 0 0.00578 0 0 Os_rug 0 0 0.01087 0 0 0.00578 0.01408 0.01081 Os_cultar 0 0 0 0 0 0 0 0 P sdN onja 0 0 0 0 0.0098 0 0 0 Ptjarfm 0.04545 0.03 0 0 0 0.00578 0 0.00541 Pl_fav 0.02273 0 0 0 0 0.00576 0 0.01081 Poly 0 0.04 0 0 0 0 0 0 Pul_bul 0 0 0 0 0.0098 0 0 0.00541 (JSL2900 - PC2 - Relative Proportions continued)

203

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Sp/Depth 16-17 cm 17-18 cm 18-19 cm 19-20 cm 20-21 cm 21-22 cm22-23 cm 23-24 cm P u ljsu b 0 0 0 0 0.0098 0 0.01408 0 P y r jM 0 0 0 0 0 0 0 0 Pyr_m 0.02273 0 0 0 0 0 0 0.00541 Q J a t 0 0 0 0 0 0 0 0 Q Jam a K k 0 0 0 0 0 0 0 0 Q 0 0 0 0 0 0 0 0 Stgmjslllpt 0 0.01 0 0 0 0 0 0.00541 Staint 0 0 0 0 0.0098 0 0 0 Syph_brd 0.02273 0.05 0 0.03448 0.04902 0.01734 0.02817 0.01622 T J u d y 0 0.03 0.02174 0.03448 0 0.0289 0.01408 0.02703 TMoc 0 0 0 0 0 0 0 0 U_per 0.04545 0.07 0.02174 0.03448 0.07843 0.04046 0.05634 0.09189 Vatv_mex 0 0.02 0 0 0 0 0 0 sp_1 0 0 0 0 0 0 0 0.01081 sp_2 0 0 0 0 0 0 0 0.00541 sp_3 0 0 0 0 0 0 0 0.00541 sp_4 0 0 0 0 0 0 0 0.00541 sp_S 0 0 0 0 0 0 0 0.00541 s p jS 0 0 0 0 0 0 0 0.00541 sp_7 0 0 0 0 0 0 0 0 spJB 0 0 0 0 0 0 0 0 sp_9 0 0 0 0 0 0 0 0 sp_10 0 0 0 0 0 0 0 0 sp_11 0 0 0 0 0 0 0 0 sp_12 0 0 0 0 0 0 0 0 sp_13 0 0 0 0 0 0 0 0 sp_14 0 0 0 0 0 0 0 0 sp_1S 0 0 0 0 0 0 0 0 sp_16 0 0 0 0 0 0 0 0 sp_17 0 0 0 0 0 0 0 0 sp_18 0 0 0 0 0 0 0 0 sp_19 0 0 0 0 0 0 0 0 sp_20 0 0 0 0 0 0 0 0 sp_20 0 0 0 0 0 0 0 0 sp_21 0 0 0 0 0 0 0 0 sp_22 0 0 0 0 0 0 0 0 sp_23 0 0 0 0 0 0 0 0 sp_24 0 0 0 0 0 0 0 0 sp_2S 0.02273 0 0 0 0 0 0 0 sp_2 S 0 0 0 0 0 0.00578 0 0 sp_27 0 0 0 0 0 0 0.01408 0 sp_28 0 0 0 0 0 0 0.01408 0 (JSL2900 - PC2 - Relative Proportions continued)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Species Abundance Data for EP9, EP10 and EP11 Locations

Location EPS EP10 EP11

Sp/Depth 0-1 cm 1-2 cm 2-3 cm 0-1 cm 0-1 cm 1-2 cm 2-3 cm 3-4 cm B jalb 4 2 1 1 B jx ti 3 B_cf_ord 3 B jacul 1 3 Buljala 3 B jsp 1 1 F_pont(?) 1 F jsom pr 3 Cas_neoc 3 1 Dent 1 1 G a vjra n sl 1 1 1 1 G ym jsp 1 G yrojalt 1 2 Hapl 1 1st 1 L e n tjo w 1 Lent_sp2 1 Lent 1 1 1 M argglabr 2 miBoBtis 8 1 N onjgrate 1 O jv g 3 Pjarim i 1 Trf_Brd 3 1 1 U_peregr 2 2 1 sp_1 1 1 sp_2 1 sp_3 1

2 0 5

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER 6

BENTHIC FORAMINIFERA FROM LOW-OXYGEN SHELF AND SLOPE ENVIRONMENTS OF THE NORTHERN GULF OF MEXICO: TAXONOMIC SUMMARY

206

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION

This chapter is a census of benthic foraminiferal species living in oxygen depleted

environments of the northern Gulf of Mexico, i.e., in the zone of seasonal hypoxia on the

continental shelf and in habitats around hydrocarbon vents on the slope. It includes both

dead and live specimens. The Rose Bengal staining technique for recognition of the

living Foraminifera was used for samples collected from the sediment-water interface

down to 15 cm sediment depth on the continental shelf, and down to 7 cm on the

continental slope. With few exceptions, total foraminiferal assemblages were assessed for

each I-cm interval of sediment in the core from the sea floor (zero) level to a maximum

depth of 10-47 cm.

SPECIES DOMINANCE

Continental Shelf (Hypoxia Study)

On the continental shelf, few species of benthic Foraminifera show very high

abundances; the majority of the identified species are rare to very rare. The “rare to very

rare” species may occur in a few samples or in many samples.

At stations located in water depths between 35 and 80 meters (samples of the

hypoxia study), foraminiferal assemblages are strongly dominated by Epistominella

vitrea (the most abundant), Buliminella morgani, and Nonionella basiloba. These three

species may make up more than 90% of the total assemblages. However, this community

changes in shallower waters (< 20 m) were the most dominant species, Buliminella

m organi, is followed by Ammonia parkinsoniana, Epistominella vitrea, Bolivina

lowmani, and Elphidium excavatum. Although rare and very rare in terms of numerical

abundance, species such as Ammonia parkinsoniana , Ammotium salsum, Bolivina

207

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. albatrossi, B.fragilis, B. lanceolata, B. lowmani, B. striata , Bulimimlla elegantissima,

Elphidium excavation , Fursenkoina pontoni , Hanzawaia concentrica, Miliolinella

circularis, Pyrgo cf. P. oblonga, P. phlegeri, Quinqueloculina lamarckiana , Saccammina

diflugiformis, Sagrinopsis advena, Textularia candeiana, and Uvigerina laevis, are

commonly present in many of the analyzed cores.

The living populations of Foraminifera are, with some exceptions, dominated by

Buliminella morgani. This dominance is maintained throughout the entire length of most

analyzed cores. The exceptions involve the dominance of Bolivma lowmani , which is the

most abundant species from the core top down to IS cm below the sediment-water

interface at a station located in 11 m water depth in the proximity of the Mississippi River

mouth. Furthermore, this species dominates the living population below 7 cm at a station

located in 35 m of water.

Continental Slope (Hydrocarbon Seeps Study)

Living populations of Foraminifera identified in samples collected from locations

that cover a bathymetric range o f216-694 m in areas of hydrocarbon seeps and vents on

the continental slope (MMS lease blocks in Green Canyon; see maps in chapters 1,4, and

5), show low species richness.

These populations are dominated by species such as: Bolivina albatrossi , B.

ordinaria, Gavelinopsis translucens, Osangularia rugosa, and Trifarina bradyi . Other

commonly occurring species are: Bulimina aculeata, B. alazanensis, Cassidulina

neocarinata , and Planulina ariminensis. Rose-Bengal stained foraminifers have been

found as deep as 5 cm below the sediment water interface. A relatively homogenous

distribution of benthic Foraminifera was observed in a Green Canyon core. B olivina

208

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ordinaria, Bulimina alazanensis , Cassidulina neocarinata, Siphonina bradyana,

Trifarina bradyi, and Uvigerina peregrina were fairly common in the assemblages

identified throughout this 24 cm long core.

TAXONOMY

The classification scheme adopted herein is from Loeblich and Tappan (1987 and

1992) as modified by Sen Gupta (1999). Thus, the lower taxonomic level separations

(genus, subfamily, family) have been determined according to the classification of

Loeblich and Tappan (1987), whereas the higher taxonomic groupings (superfamilies,

orders) follow Loeblich and Tappan (1992), with minor changes introduced by Sen Gupta

(1999). The overall distribution of each identified species is provided. In these

summaries, “shelf’ and “slope” refer only to those areas on the continental shelf and

slope that we sampled. Thus, shelf samples are restricted to environments placed between

10 and 80 m water depth on the Louisiana continental shelf and the slope samples are

restricted to hydrocarbon seeps and vents in 216 to 694 m water depths in Green Canyon

and Garden Banks. The comments on distribution relate only to surface sediments. The

terms “very rare”, “rare”, “common” and “abundant” refer to the average relative

abundance of species as follows: very rare < 5%, rare = 5-10%, common = 10-15%,

abundant = 15-20%, very abundant > 20%. All illustrations are scanning electron

micrographs. Taxonomic references for taxa included in this summary can be found in

Loeblich and Tappan (1987) and Ellis and Messina Catalogue (1940 and supplement).

Alphabetical lists of these shelf and slope species are given below.

209

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Shelf Species

Alfredosilvestris levinsoni Andersen

Ammobaculites sp.

Ammonia parkinsoniana (d’Orbigny)

Ammotium salsum (Cushman and Brdnnimann) forma dilatatum (Cushman and

Brfinnimann)

Angulogerina bella Phleger and Parker

Bigenerina irregularis Phleger and Parker

Bolivina albatrossi Cushman

Bolivina barbata Phleger and Parker

Bolivina lanceolata Napoli

Bolivina lowmani Phleger and Parker

Bolivina ordinaria Phleger and Parker

Bolivina striatula Cushman var. spinata Cushman

Bolivina translucens Phleger and Parker

Bolivina venezuelana Sellier de Civrieux

Bulimina marginata d’Orbigny

Buliminella elegantissima (d’Orbigny)

Buliminella morgani Andersen

Cancris sagra (d’Orbigny)

D entalm a sp.

Elphidium excavatum (Terquem)

Elphidium poyeamim (d’Orbigny)

210

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Epistominella vitrea Parker

Epistominella exigua (Brady)

Fursenkoina pontoni (Cushman)

G uttulina sp. cf. G. pulchella d’Orbigny

Hanzawaia concentrica (Cushman)

Haplophragmoides sp.

Haplophragmoides sp. cf. H. pianissimo Cushman

Lagena mexicana Andersen

Lagena sp. cf. L. perlucida (Montagu)

Lagena striata (d’Orbigny)

Lagena sp.

Lenticulina sp. cf. L. sp. "F" Andersen

Lenticulina sp.

Lenticulina sp. “B” Andersen

Miliolinella circularis (Bomeman)

Miliolinella sp.

Miliolinella warreni Andersen

Neoeponides antillarum (d’Orbigny)

Nonionella basiloba Cushman and McCulloch

N onionella sp. cf. N. basiloba Cushman and McCulloch

Pandaglandulina sp.

Procerolagena purii (Andersen)

Pseudoclavulina mexicana (Cushman)

211

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Pyrgo carinata (d’Orbigny)

Pyrgo oblonga (d’Orbigny)

Pyrgo phlegeri Andersen

Quirtqueloculina auberiana d’Orbigny

Quinqueloculina crassa (Heron-Alien and Earland) forma subcuneata Cushman

Quinquelocidina lamarckiana d’Orbigny

Quinqueloculina linneiana (d’Orbigny)

Quinqueloculina sp. cf Q. compta Cushman

Quinqueloculina sp. cf. Q. tropicalis Cushman

Quinqueloculina sp. 1

Quinqueloculina sp. 2

Reussella miocenica Cushman

Saccammina comprima (Phleger and Parker)

Saccammina difflugiformis (H.B. Brady)

Sagrinopsis advena (Cushman)

Sigmoilopsis Jlintii (Cushman)

Siphotextularia affinis (Fomasini)

Textularia candeiana d’Orbigny

Textularia porrecta (Brady)

Triloculina sp.

Uvigerina laevis G8es

Uvigerina sp.

Uvigerina sp. cf. U. parvula Cushman and Thomas

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Slope Species

Amphicoryna hispida (d’Orbigny)

Angulogerina bella Phleger and Parker

Angulogerina sp.

A stacolits sp.

Astrononion tumidum Cushman and Edwards

Bolivina albatrossi Cushman

Bolivina hastata Phleger and Parker

Bolivina barbata Phleger and Parker

Bolivina ordinaria Phleger and Parker

Bolivina striatula Cushman var. spinata Cushman

Bolivina subaenariensis mexicana Cushman

B olivina sp. cf. B. ordinaria Phleger and Parker

B olivina sp. cf. B. peirsonae Uchio

Bulimina aculeata d’Orbigny

Bulimina alazanensis Cushman

Bulimina mexicana Cushman

Cassidulina curvata Phleger and Parker

Cassidulina neocarinata Thalmann

Cassidulina nodosa Stewart and Stewart

Cassidulina subglobosa Brady

Cibicidoides incrassatus (Fichtel and Moll)

Cibicidoides io (Cushman)

213

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Cibicidoides umbonalus (Phleger and Parker)

Cribrolagena sp.

Ehrenbergina trigona Go€s

Epistominella exigua (Brady)

Eponides sp. cf. E. regularis Phleger and Parker

F issurina sp. “B " Andersen

Fursenkoina compressa (Bailey)

Gavelinopsis translucens (Phleger and Parker)

G landulina sp.

Gyroidinoides altiformis (Stewart and Stewart)

Gyroidinoides sp. cf. G. rodundimargo (Stewart and Stewart)

H ansenisca sp. cf. H. soldanii (d’Orbigny)

Hoeglundina elegans d’Orbigny, 1826

Hyalinonetrion sp. cf. H. sahulense Patterson and Richardson

Lenticulina clericii (Fomasini)

Lenticulina gibba (d’Orbigny)

Lenticulina orbicularis (d’Orbigny)

Lenticulina rotulata (Lamarck)

Lenticulina sp. cf. L serpens (Sequenza)

Lenticulina sp.

M arginulina glabra d’Orbigny

Marginulinopsis marginulinoides (Goes)

Neocrosbyia minuta (Parker)

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Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Neolenticulina peregrina (Schwager)

N onion sp.

Osangularia rugosa (Phleger and Parker)

Planulina ariminesis d’Orbigny

Planulina faveolata (Brady)

Pyrgo sp. cf. P. murrhina (Schwager)

Rzehakina sp.

Siphonina bradyiana Cushman

Stainforthia complanata (Egger)

Trifarina bradyi Cushman

Uvigerina hispido-costata Cushman and Todd

Uvigerina peregrina Cushman

Uvigerina peregrina dimpta Todd

U vigerina sp. cf. U. parvula Cushman and Thomas

Uvigerina sp. cf. U. peregrina Cushman

Virgulopsoides razaensis McCulloch

Class FORAMINIFERA d’Orbigny, 1826

Order ASTRORHIZIDA Lankester, 1885

Superfamily ASTRORH3ZACEA Brady, 1881

Family SACCAMMINIDAE Brady, 1884

Subfamily SACCAMMININAE Brady, 1884

Genus SACCAMMINA Carpenter, 1869

2 1 5

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Saccammina comprima (Phleger and Parker)

= Proteonina comprima Phleger and Parker, 1951

Plate 6.1, figs. 1,2

Distribution: Continental shelf: very rare.

Saccammina difflugiformis (H.B. Brady)

= Reophax difflugiformis H.B. Brady, 1879

Plate 6.1, figs. 3,4

Distribution: Continental shelf: very rare.

Order LITUOLIDA Lankester, 1885

Superfamily RZEHAKINACEA Cushman, 1933

Family RZEHAKINIDAE Cushman, 1933

Genus RZEHAKINA Cushman, 1927

R zehakina sp.

Plate 6.1, fig. 24

Remarks: Test relatively compressed, oval in side view, periphery rounded; sutures

indistinct; aperture indistinct; wall finely agglutinated.

Distribution: Continental slope: very rare.

Plate 6.1, fig. 24

Superfamily LITUOLACEA de Blainville, 1827

Family HAPLOPHRAGMODIDAE Maync, 1952

Genus HAPLOPHRAGMOIDES Cushman, 1910

Haplophragmoides sp. cf. H . pianissim o Cushman, 1927

Plate 6.1, fig. 8

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.1

Saccamminidae, Rzehakinidae, Haplophragmodidae, Lituolidae, Textulariidae, and Hauerinidae (All scale bars represent SO pm)

l, 2. Saccammina comprima (Phleger and Parker)

3 ,4 . Saccammina diflugiformis (H.B. Brady)

5,6 . Ammotium salsum (Cushman and Brdnnimann) forma dilatatum

(Cushman and Brdnnimann)

7. Haplophragmoides sp.

8. Haplophragmoides sp cf. H. pianissimo Cushman

9. Ammobaculites sp.

10-12. Textularia candeiana d’Orbigny

14,15 Textularia porrecta Brady

13,16-18. Siphotextularia affinis (Fomasini)

19-23. Bigenerina irregularis Phleger and Parker

24. R zehakina sp.

25. Sigmoilopsisflin tii (Cushman)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.1

\ ■-I ? 1 I 18

218

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission Remarks: The specimens have a slightly larger umbilicus than those described by

Cushman.

Distribution: Continental shelf: very rare.

Haplophragmoides sp.

Plate 6.1, fig. 7

Remarks: Test relatively large, circular, periphery rounded; chambers and sutures

indistinct; umbilicus large, occupies 1/3 of the diameter.

Distribution: Continental shelf: very rare.

Family LITUOLIDAE de BlainviUe, 1827

Subfamily AMMOMARGINULININAE Podobina, 1978

Genus AMMOBACULlTES Cushman, 1910

Ammobaculites sp.

Plate 6.1, fig. 9

Remarks: Test broad and compressed, slightly uncoiled, periphery lobulate; umbilicus

relatively narrow.

Distribution: Continental shelf: very rare.

Genus AMMOTIUM Loeblich and Tappan 1953

Ammotium salsum (Cushman and Br6nnimann) forma dilatatum (Cushman and

Brdnnimann)

=Ammobaculites dilataus, Cushman and Brdnnimann, 1948

Plate 6.1, figs. 5,6

Distribution: Continental shelf: very rare.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Order TEXTULARDD A Lankester, 1885

Superfamily TEXTULARIACEA Ehrenberg, 1838

Family TEXTULARHDAE Ehrenberg, 1838

Subfamily TEXTULARIINAE Ehrenberg, 1838

Genus TEXTULARIA Defiance, 1824

Bigenerina irregularis Phleger and Parker, 1951

Plate 6.1, figs. 19-23

Distribution: Continental shelf: very rare.

Textularia candeiana d’Orbigny, 1839

Plate 6.1, figs. 10-12

Distribution: Continental shelf: very rare.

Textularia porrecta Brady

= Textularia agglutinans d’Orbigny, var. porrecta Brady, 1884

Plate 6.1, figs. 14,15

Distribution: Continental shelf: very rare.

Subfamily SIPHOTEXTULARHNAE Loeblich and Tappan, 1985

Genus SIPHOTEXTULARIA Finlay, 1939

Siphotextularia affinis (Fomasini)

= Sagrina affinis Fomasini, 1883 ft Plate 6.1, figs. 13,16-18

Distribution: Continental shelf: very rare.

Family PSEUDOGAUDRYINTDAE Loeblich and Tappan, 1985

Subfamily PSEUDOGAUDRYININAE Loeblich and Tappan, 1985

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Pseudoclavulina mexicana (Cushman)

- Clavulina humilis H.B. Brady, var. m exicana Cushman, 1922

Not illustrated

Distribution: Continental shelf: very rare.

Order MILIOLIDA Lankester, 1885

Superfamily MILIOLACEA Ehrenberg, 1839

Family HAUERINIDAE Schwager, 1876

Subfamily SIPHONAPERTINAE Saidova, 1975

Genus QUINQUELOCULINA d’Orbigny, 1826

Quinqueloculina auberiana d’Orbigny, 1839

Plate 6.2, fig. 23

Distribution: Continental shelf: very rare.

Quinqueloculina crassa (Heron-Alien and Earland) forma subcuneata Cushman

[Quinqueloculina crassa = Miliolina crassa Heron-Alien and Earland]

Plate 6.2, fig. 17

Distribution: Continental shelf: very rare.

Quinqueloculina sp. cf. Q. com pta Cushman, 1947

Plate 6.2, fig. 14

Remarks: Our specimens lack the short neck described for the species by Cushman.

Distribution: Continental shelf: very rare.

Quinqueloculina lamarckiana d’Orbigny, 1839

Plate 6.2, figs. 1-3,6

Distribution: Continental shelf: very rare.

221

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.2

Hauerinidae, Nodosariidae, and Vaginulinidae (All scale bars represent SO pm)

1-3,6. Quinqueloculina lamarkiana d’Orbigny

4. Miliolinella warreni Andersen

5. Quinqueloculina sp. cf. Q. tropicalis Cushman

7-9. Miliolinella circularis (Bomeman)

10. Miliolinella sp.

11. Quinqueloculina linneiana d’Orbigny forma com is Bandy

12. Triloculina sp.

13,22. Quinqueloculina sp. 1

14. Quinqueloculina sp. cf. Q. compta Cushman

15,16. Pyrgo phlegeri Andersen

17. Quinqueloculina crassa (Heron-Alien and Earland)

forma subcuneata Cushman

18. Pyrgo carinata (d’Orbigny)

19. Pyrgo murhina (Schwager)

20,21. Pyrgo oblonga (d’Orbigny)

23. Quinqueloculina auberiana d’Orbigny

24. Quinqueloculina sp. 2

25. Alfiedosilvestri levinsoni Andersen

26. Pandaglandulina sp.

27. Lenticulina sp.

222

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 28. Lenticulina sp. “B” (Andersen)

29. Lenticulina clericii

30. Lenticulina orbicularis

223

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.2

224

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Quinqueloculina linneiana (d’Orbigny), 1839

Plate 6.2, fig. 11

Distribution: Continental shelf: very rare.

Quinqueloculina sp. cf. Q. tropicalis Cushman

Plate 6.2, fig. 5

Remarks: Less elongate than Q. tropicalis as described by Cushman.

Distribution: Continental shelf: very rare.

Quinqueloculina sp. 1

Plate 6.2, figs. 13,22

Remarks: Somewhat similar with Q. compta Cushman. However, our specimens lack the

short neck and have a smooth wall surface.

Distribution: Continental shelf: very rare.

Quinqueloculina sp. 2

Plate 6.2, fig. 24

Remarks: The test shape, the bluntly rounded periphery and the somewhat rounded spine

resemble the features of Q. apicula Cushman. However, our specimens have a slightly

rougose surface texture.

Distribution: Continental shelf: very rare.

Subfamily MILIOLINELLINAE Vella, 1957

Genus MILIOLINELLA Wiesner, 1931

Miliolinella circularis (Borneman)

= Triloculina circularis Borneman, 1855

Plate 6.2, figs. 7-9

225

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental shelf: very rare.

Miliolinella warreni Andersen, 1961

Plate 6 2 , fig. 4

Distribution: Continental shelf: very rare.

Miliolinella sp.

Plate 6.2, fig. 10

Remarks: Test elongate, oval outline, triloculine chamber arrangement; chamber

triangular in cross section; aperture with a semilunate toothplate.

Distribution: Continental shelf: very rare.

Genus PYRGO Defiance, 1824

Pyrgo carinata (d’Orbigny)

= Biloculina carinata d’Orbigny, 1839

Plate 6.2, fig. 18

Distribution: Continental shelf: very rare.

Pyrgo sp. cf. P. murrhina (Schwager)

= Biloculina murrhina Schwager, 1866

Plate 6.2, fig. 19

Remarks: It has less distinct distal notches than the species described by Schwager.

Distribution: Continental slope: very rare.

Pyrgo oblonga (d’Orbigny)

= Biloculina oblonga d’Orbigny, 1839

Plate 6.2, figs. 20,21

Distribution: Continental shelf: very rare.

226

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Pyrgo phlegeri Andersen, 1961

Plate 6.2, figs. 15,16

Distribution: Continental shelf: very rare.

Genus TRILOCULINA d’Orbigny, 1826

Triloculina sp.

Plate 6.2, fig. 12

Remarks: Test relatively large, triangular; sutures distinct, surface smooth; aperture

crescentiform without a neck.

Distribution: Continental shelf: very rare.

Subfamily SIGMOILOPSINAE Vella, 1957

Genus SIGMOILOPSIS Finlay, 1947

Sigmoilopsisflin tii (Cushman)

= Sigm oilina flin tii Cushman, 1946

Plate 6.1, fig. 25

Distribution: Continental shelf: very rare.

Order LAGEN1DA Lankester, 1885

Superfamily NODOSARIACEA Ehrenberg, 1838

Family NODOSARHDAE Ehrenberg, 1838

Subfamily NODOSARHNAE Ehrenberg, 1838

Genus Alfiredosilvestri Andersen, 1961

Alfredosilvestris levinsoni Andersen, 1961

Plate 6.2, fig. 25

Distribution: Continental shelf: very rare.

227

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Genus DENTALINA Risso, 1826

D entalina sp.

Plate 6.3, fig. 18

Remarks: Test free, elongate; chambers increasing gradually in size as added; sutures

distinct, curved; wall calcareous, surface smooth; aperture radiate, terminal.

Distribution: Continental shelf: very rare.

Genus P AND AGLANDULINA Loeblich and Tappan, 1955

Pandaglanduiina sp.

Plate 6.2, fig. 26

Remarks: Test free, fusiform, elongate, uniserial; sutures straight; wall calcareous,

hyaline, smooth; aperture terminal, radiate, slightly produced.

Distribution: Continental shelf: very rare.

Family GLANDULINIDAE Reuss, 1860

Subfamily GLANDULININAE Reuss, 1860

Genus GLANDULINA d’Orbigny, 1839

G landulina sp.

Plate 6.3, fig. 15

Remarks: Test fusiform; chambers in the early portion biserial, later uniserial, and

overlapping; sutures distinct, in early portion straight, later curved; aperture terminal,

radiate; entosolenian tube present

Distribution: Continental slope: very rare.

228

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.3

Nodosariidae, Glandulinidae, Vaginulinidae, Lagenidae, Polymorphinidae, Ellipsolagenidae, Epistominidae, and Bolivinidae (All scale bars represent 50 pm)

1. Lenticulina rotulata (Lamarck)

2. Lenticulina cf. L . serpens (Sequenza)

3. L enticulina gibba d’Orbigny

4. Lenticulina sp. cf. Z. sp. ”F ” Andersen

5,6. M arginulina glabra d’Orbigny

7. Marginulinopsis marginulinoides (Gogs)

8. A stacolus sp.

9. Neolenticulina peregrina (Schwager)

10,11,14. Procerolagena purii (Andersen)

12. Lagena mexicana Andersen

13. Lagena sp. cf. L. perlucida (Montagu)

15. G landulina sp.

16. Cribrolagena sp.

17. Lagena striata (d’Orbigny)

18. D entalina sp.

19. Ampkicoryna hispida (d’Orbigny)

2 0 . G uttulina cf. G, p ulch ella d’Orbigny

21. F issurina sp. “5 ” Andersen

22. Lagena sp.

23. Hoeglundina elegans d’Orbigny, 1826

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 24,29. Bolivina barbata Phleger and Parker

25. Hyalinonetrion sp cf. H. sahulense Patterson and Richardson

26,27. B olivina sp. cf. B. ordinaria Phleger and Parker

28. Bolivina striatula Cushman var. spinata Cushman

230

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.3

A •' 1 9 10 12 7 8

13 14 1 3 18 \ 'X

20 21 19 o o

25 26 27 28 29

231

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Family VAGENULINIDAE Reuss, I860

Subfamily LENTICULININAE Chapman, Parr, and Collins, 1934

Genus LENTICULINA Lamarck, 1804

Lenticulina clericti (Fomasini)

- Cristelaria clericti Fomasini, 1895

Plate 6.2, fig. 29

Distribution: Continental slope: very rare.

Lenticulina gibba (d'Orbigny)

= Cristelaria gubba d’Orbigny, 1839

Plate 6.3, fig. 3

Distribution: Continental slope: very rare.

Lenticulina orbicularis (d'Orbigny)

= Robulina orbicularis d'Orbigny, 1826

Plate 6.2, fig. 30

Distribution: Continental slope: very rare.

Lenticulina rotulata (Lamarck)

= Lenticulites rotulata Lamarck, 1804

Plate 6.3, fig. 1

Distribution: Continental slope: very rare.

Lenticulina sp. cf. L. sp. "F" Andersen, 1961

Plate 6.3, fig. 4

Remarks: L. sp. “F", not a formal species name, was chosen by Andersen to describe

specimens of Lenticulina somewhat similar to L. oblongus Coryell and Rivero. Our

2 3 2

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. specimens have a less distinct keel when compared with specimens o f L sp. "F”.

Distribution: Continental shelf: very rare.

Lenticulina sp. cf. L . serpens (Sequenza)

= Robulina serpens Sequenza, 1880

Plate 6.3, fig. 2

Remarks: The specimens we found have a more rounded outline than those originally

described by Sequenza.

Distribution: Continental slope: very rare.

Lenticulina sp. “B” (Andersen), 1961

Plate 6.2, fig. 28

Remarks: Lenticulina sp. "B ” is not a formal species name. Andersen finds that these

forms o f Lenticulina resemble L. clericii. However, L. sp. “B ” does not have the

“cribrate aperture attributed to L. clericir.

Distribution: Continental shelf: very rare.

Lenticulina sp.

Plate 6.2, fig. 27

Remarks: Test free, relatively small, lenticular, planispiral and involute; 5 to 6 chambers

in the last formed whorl; periphery acute and carinate; sutures curved; aperture face

relatively large with a radiate aperture. Differs from L. calcar by lacking the peripheral

spines and having a rather elongated contour spines; differs from L. orbicularis by having

a more elongated test

Distribution: Continental shelf: very rare.

Genus MARGINULINOPSIS A. Silvestri, 1904

233

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Marginulinopsis marginulinoides (Gogs)

- Cristellaria aculeata d’Orbigny var. marginulinoides Gogs, 1896

Plate 6.3, fig. 7

Distribution: Continental slope: very rare.

Genus NEOLENTICULINA McCulloch, 1977

Neolenticuiina peregrina (Schwager)

= Cristellaria peregrina Schwager, 1866

Plate 6.3, fig. 9

Distribution: Continental slope: very rare.

Subfamily MARGINULININAE Wedekind, 1937

Genus AMPHICORYNA Schlumberger, 1881

Ampkicoryna hispida (d’Orbigny)

= Nodosaria hispida d’Orbigny, 1846

Plate 6.3, fig. 19

Distribution: Continental slope: very rare.

Genus ASTACOLUS de Montfort, 1808

A stacolus sp.

Plate 6.3, fig. 8

Remarks: Test free, large, relatively compressed; periphery subacute with a relatively

narrow dorsal keel; chambers elongated, sutures distinct, depressed, slightly curved; wall

calcareous, surface smooth; aperture radiate at the dorsal angle.

Distribution: Continental slope: very rare.

Genus MARGINULINA d’Orbigny, 1826

234

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Marginulina glabra d’Orbigny, 1826

Plate 6.3, figs. 5,6

Distribution: Continental slope: very rare.

Family LAGENIDAE Reuss, 1862

Genus HYALINONETRION Patterson

Hyalinonetrion sp. cf. H. sahulense Patterson and Richardson, 1988

Plate 6.3, fig. 25

Remarks: The only specimen we found lacks the phialine lip surrounding the apertural

end; however, the specimen may not be completely preserved.

Distribution: Continental slope: very rare.

Genus CRIBROLAGENA Sellier de Civrieux and Dessauvagies, 1965

Cribrolagena sp

Plate 6.3, fig. 16

Remarks: Test free, single chambered, elongated with a long neck; wall calcareous,

surface smooth; aperture terminal and cribrate.

Distribution: Continental slope: very rare.

Genus LAGENA Walker and Jacob, 1798

Lagena mexicana Andersen, 1961

Plate 6.3, fig. 12

Distribution: Continental shelf: very rare.

Lagena striata (d’Orbigny)

= Oolina striata d’Orbigny, 1839

Plate 6.3, fig. 17

235

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental shelf: very rare.

Lagena sp. cf. L. perlucida (Montagu)

= Vermiculum perlucidum Montagu, 1803

Plate 6.3, fig. 13

Remarks: Our specimens differ from V. perlucidum (Montagu) in having a more

elongated test

Distribution: Continental shelf: very rare.

Lagena sp.

Plate 6.3, fig. 22

Remarks: Test free, calcareous, unilocular, almost spherical in shape; surface with strong

longitudinal striations; aperture at the end of a tubular neck

Distribution: Continental shelf: very rare.

Genus PROCEROLAGENA Puri, 1954

Procerolagena purii (Andersen)

=Amphorina purii Andersen, 1961

Plate 6.3, figs. 10,11,14

Distribution: Continental shelf: very rare.

Superfamily POLYMORPHINACEA Wedekind, 1937

Family POLYMORPHIN1DAE d’Orbigny

Subfamily POLYMORPHININAE d'Orbigny, 1839

Genus GUTTULINA d’Orbigny, 1839

G uttulina sp. cf. G. pulchella d’Orbigny, 1839

Plate 6.3, fig. 20

236

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Remarks: Our specimens differ from G. pulchella d’Orbigny in having less elongated

tests.

Distribution: Continental shelf: very rare.

Family ELLIPSOLAGENIDAE A. Silvestri, 1923

Subfamily ELLIPSOLAGENINAE A. Silvestri, 1923

Genus FISSURINA Reuss, 1850

F issurina sp. “B ” Andersen, 1961

Plate 6.3, fig. 21

Remarks: F. sp "B ” is not a formal species name. Andersen used the name for describing

specimens of F issurina that resemble F. laevigata Reuss but from which differs in having

a less rounded cross section.

Distribution: Continental slope: very rare.

ORDER ROBERTINIDA Mikhalevich, 1980

Superfamily CERATOBULIMINACEA Cushman, 1927

Family EPISTOMINIDAE Wedekind, 1937

Subfamily EPISTOMININAE Wedekind, 1937

Genus HOEGLUNDINA Brotzen, 1948

Hoeglundina elegans d’Orbigny, 1826

Plate 6.3, fig. 23

Distribution: Continental slope: very rare.

Order BULIMINIDA Fursenko, 1958

Superfamily BOLIVINACEA Glaessner, 1937

Family BOLIV1NEDAE Glaessner, 1937

2 3 7

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Genus BOLIVINA d’Orbigny, 1839

Bolivina albatrossi Cushman, 1922

Plate 6.4, figs. 16,17

Distribution: Continental slope: abundant among Rose Bengal stained specimens. It

seems to be better adapted to live within the sediment between 1 and 3 cm depth.

Bolivina hastata Phleger and Parker, 1951

Plate 6.4, fig 21.

Distribution: Continental slope: very rare.

Bolivina barbata Phleger and Parker, 19S1

Plate 6.3, figs. 24,27;

Plate 6.4, fig. 19

Distribution: Continental shelf: very rare.

Continental slope: very rare.

Bolivina capitata Cushman, 1933

Plate 6.4, fig. 13

Distribution: Continental shelf: very rare.

Bolivina lanceolata Napoli, 1952

Plate 6.4, figs. 6-9,14

Distribution: Continental shelf: rare to common on the continental shelf. Living

specimens were found from the top sample down to 10 cm below sediment-water

interface.

Bolivina lowmani Phleger and Parker, 1951

Plate 6.4, figs. 1-3

2 3 8

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.4

Bolivinidae and Cassidulinidae (All scale bars represent 50 pm)

I -3. Bolivina lowmani Phleger and Parker

4,5,10-12. Bolivina ordinaria Phleger and Parker

6-9,14. Bolivina lanceolata Napoli

13. Bolivina capitata Cushman

15. Bolivina translucens Phleger and Parker

16,17. Bolivina albatrossi Cushman

18. Bolivina venezueleana Sellier de Civrieux

19. Bolivina barbata Phleger and Parker

20. Bolivina sp. cf. B. peirsonae Uchio, 1960

21. Bolivina astata Phleger and Parker

22. Bolivina striatula Cushman var. spinata Cushman

23,24. Cassidulina curvata Phleger and Parker

25,26. Cassidulina neocarinata Thalmann

239

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.4

240

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental shelf: common to abundant on the continental shelf. Sometimes,

it dominates microhabitats located deep within the sediment (13-15 cm below sediment-

water interface).

Bolivina ordinaria Phleger and Parker, 1952

Plate 6.4, figs. 4,5,10-12

Distribution: Continental slope: very abundant. Lives both on and within the sediment

and dominates the populations from the top sediment down to a depth of 2 cm. Living

specimens of B. ordinaria were found as deep as 5 cm below the sediment-water

interface.

Bolivina striatula Cushman var. spinata Cushman, 1936

Plate 6.3, fig. 29

Plate 6.4, fig. 22

Distribution: Continental shelf: very rare.

Continental slope: very rare.

Bolivina subanaraensis mexicana Cushman, 1922

Not illustrated

Distribution: Continental slope: very rare.

Bolivina translucens Phleger and Parker, 1951

Plate 6.4, fig. 15

Distribution: Continental shelf: rare.

Continental slope: common to abundant

Bolivina venezuelana Sellier de Civrieux, 1976

Plate 6.4, fig. 18

241

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental shelf: very rare to rare.

B olivina sp. cf. B. ordinaria Phleger and Parker, 1952

Plate 6.3, figs. 26,27

Remarks: Very small specimens having relatively large pores distributed exclusively

along the sutures. Differs from B. ordinaria in having a very small test with a more

tapered shape.

Distribution: Continental slope: very rare.

B olivina sp. cf. B. peirsonae Uchio, 1960

Plate 6.4, fig. 20

Remarks: Chambers have less distinct spines at the outer posterior angle.

Distribution: Continental slope: very rare.

Superfamily CASSIDULINACEA d’Orbigny, 1839

Family CASSIDULINIDAE d’Orbigny, 1839

Subfamily CASSIDULININAE d’Orbigny, 1839

Genus CASSIDULINA d’Orbigny, 1826

Cassidulina curvata Phleger and Parker, 1951

Plate 6.4, figs. 23,24

Distribution: Continental slope: very rare.

Cassidulina neocarinata Thalmann, 1950

Plate 6.4, figs. 25,26

Distribution: Continental slope: common to abundant Living specimens were found from

the top sediment down to a depth of 3 cm below the sediment-water interface.

Cassidulina nodosa Stewart and Stewart, 1930

242

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Plate 6.5, fig. 1

Distribution: Continental slope: very rare.

Genus GLOBOCASIDULINA Voloshinova, 1960

Globocassidulina subglobosa (Brady), 1881

Plate 6.5, fig. 2

Distribution: Continental slope: very rare.

Subfamily EHRENBERGININAE Cushman, 1927

Genus EHRENBERGINA Reuss, 1850

Ehrenbergina trigona Goes, 1896

Plate 6.5, fig. 3

Distribution: Continental slope: very rare. Living specimens were found between 1 and 2

cm below sediment-water interface.

Superfamily TURRILINACEA Cushman, 1927

Family STAINFORTHIIDAE Reiss, 1963

Genus STAJNFORTHIA Hofker, 1956

Stainforthia complanata (Egger)

= Virgulina schreibersiana Czjzek var. complanata Egger, 1893

Plate 6.5, fig. 20

Distribution: Continental slope: very rare.

Genus V1RGULOPSOIDES McCulloch, 1977

Virgulopsoides razaensis McCulloch, 1977

Plate 6.5, fig. 4

Distribution: Continental slope: very rare.

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.5

Cassidulinidae, Stainforthiidae, Siphogenerinoididae, Buliminidae, and Uvigerininidae (All scale bars represent 50 pm)

1. Cassidulina nodosa Stewart and Stewart

2. Cassidulina subgtobosa Brady

3. Ehrenbergina trigona Gogs

4. Virgulopsoides razaensis McCulloch

5-7. Sagrinopsis advena (Cushman)

g, 9. Buliminella elegantissima (d’Orbigny)

10,11. Buliminella morgani Andersen

12-14, Bulimina marginata d’Orbigny

15. Bulimina aculeata d’Orbigny

16. Bulimina mexicana Cushman

17. U vigerina sp.

18,19,26 Uvigerina laevis Ehrenberg

20. Stainforthia complanata (Egger)

21.22. Uvigerina hispido-costata Cushman and Todd

23. Bulimina alazaensis Cushman

21.22. Uvigerina hispido-costata Cushman and Todd

24,27. U vigerina sp. cf. U. parvula Cushman

25. Uvigerina sp. cf. U. peregrina Cushman

28,31,33,34. Uvigerina peregrina Cushman

29,30. Angulogerina bella Phleger and Parker

32. Uvigerina peregrina dirupta Todd

244

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.5

245

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Superfamily BULIMINACEA Jones, 1875

Family SIPHOGENERINOIDEDAE Saidova, 1981

Subfamily TUBULOGENERININAE Saidova, 1981

Genus SAGRINOPSIS SeUier de Civrieux, 1969

Sagrinopsis advena (Cushman)

= Siphogenerina advena Cushman, 1922

Plate 6.5, figs. 5-7

Distribution: Continental shelf: very rare to rare.

Family BULIMINIDAE Jones, 1875

Genus BULIMINA d’Orbigny, 1826

Bulimina aculeata d’Orbigny, 1826

Plate 6.5, fig. 15

Distribution: Continental slope: common. Living specimens were found as deep as 3-4

cm below sediment water interface.

Bulimina alazanensis Cushman, 1927

Plate 6.5, fig. 23

Distribution: Continental slope: rare to common.

Bulimina marginaia d’Orbigny, 1826

Plate 6 J, figs. 12-14

Distribution Continental shelf: very rare to rare. Living specimens have been found as

deep as 11 cm below sediment water interface.

Bulimina mexicana Cushman

= Bulimina striata d’Orbigny, var. mexicana Cushman, 1922

246

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Plate 6.5, fig. 16

Distribution: Continental slope: very rare.

Genus BULIMINELLA Cushman, 1911

Buliminella elegantissima (d’Orbigny)

= Bulimina elegantissima d’Orbigny, 1839

Plate 6.5, figs. 8,9

Distribution: Continental shelf: very rare.

Buliminella morgani Andersen, 1961

Plate 6.5, figs. 10,11

Distribution: Continental shelf: very abundant. Living specimens were found from the

top sediment down to a depth of 10 cm.

Family UVIGERININIDAE Haeckel, 1894

Subfamily UVIGERININAE Haeckel, 1894

Genus UVIGERINA d’Orbigny, 1826

Uvigerina hispido-costata Cushman and Todd, 1945

Plate 6.5, figs.21,22

Distribution: Continental slope: very rare.

Uvigerina laevis G6es

= Uvigerina auberiana d’Orbigny, var. laevis Gdes, 1896

Plate 6.5, figs.18,19,26

Distribution: Continental shelf: very rare.

Uvigerina peregrina Cushman, 1923

Plate 6.5, figs. 28,31,33,34

247

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental slope: very rare.

Uvigerina peregrina dirupta Todd, 1929

Plate 6.5, fig. 32

Distribution: Continental slope: very rare.

U vigerina sp. cf. U. parvula Cushman and Thomas, 1923

Plate 6.5, figs. 24,27

Remarks: Our specimens differ from U parvula described by Cushman and Thomas in

having the surface of last chamber ornamented by fine spines.

Distribution: Continental shelf: very rare.

Continental slope: very rare.

U vigerina sp. cf. U. peregrina Cushman

Plate 6.5, fig. 25

Remarks: The ornamentation shows no spinose or irregular portions toward the base and

the apertural end of the test as U. peregrina was described by Cushman.

Distribution: Continental slope: very rare.

U vigerina sp.

Plate 6.5, fig. 17

Remarks: Test elongate, early stage triserial, later loosely triserial and finally somewhat

irregularly uniserial, chambers inflated, sutures depressed; wall calcareous, perforate,

surface with longitudinal costae that are not continuous over the sutures; aperture

rounded, at the end o f a short neck.

Distribution: Continental shelf: very rare.

Subfamily ANGULOGERININAE Galloway, 1933

248

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Genus ANGULOGERINA Cushman, 1927

Angulogerina bella Phleger and Parker, 1951

Plate 6.5, figs. 29,30

Plate 6.6, figs. 1,2

Distribution: Continental shelf: rare. Living specimens were found as deep as 10 cm

below sediment-water interface.

Angulogerina sp.

Plate 6.6, figs. 3

Remarks: Differs from Angulogerina bella Phleger and Parker in having a more

elongated test with not as sharply undercut chambers; differs from Angulogerina

angulosa Chapman & Parr in having a heavier ornamentation (short blunt spines in the

initial portion of the test followed by interrupted costae in the later stages).

Distribution: Continental slope: very rare.

Genus TRIFARINA Cushman, 1923

Trifarina bradyi Cushman, 1923

Plate 6.6, figs. 5,6

Distribution: Continental slope: abundant. One of the most abundant living species found

on the continental slope.

Family REUSSELLIDAE Cushman, 1933

Geuns REUSSELLA Galloway, 1933

ReusseUa miocenica Cushman, 1933

Plate 6.6, figs. 9,10

Distribution: Continental shelf: very rare.

249

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.6

Uvigerininidae, Reussellidae, Fursenkoinidae, Bagginidae, Eponididae, Discorbidae, Rosalinidae, Siphoninidae, and Parrelloididae (All scale bars represent 50 pm)

1,2. Angulogerina bella Phleger and Parker

3. Angulogerina sp.

4 ,7 . Fursenkoina pontoni (Cushman)

5 ,6 . Trifarina bradyi Cushman

8. Fursenkoina compressa (Bailey)

9, 10. Russella miocenica Cushman

11,12. Gavelinopsis translucens (Phleger and Parker)

13,14. Neoeponides antillarum (d’Orbigny)

15-17. Cancris sagra (d’Orbigny)

18,23. Siphonina bradyana Cushman

19,20. Neocrosbyia minuta (Parker)

21,22. Cibicidoides incrassatus (Fichtel and Moll)

24,25. Eponides sp. cf. E. regularis Phleger and Parker

26,27. Cibicidoides umbonatus (Phleger and Parker)

2 5 0

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.6

251

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission Superfamily FURSENKOINACEA Loeblich and Tappan, 1961

Family FURSENKOINIDAE Loeblich and Tappan, 1961

Genus FURSENKOINA Loeblich and Tappan, 1961

Fursenkoina compressa (Bailey)

= Bulimina compressa Bailey, 1851

Plate 6.6, fig. 8

Distribution: Continental slope: very rare.

Fursenkoina pontoni (Cushman)

= Virgulina pontoni Cushman, 1932

Plate 6.6, figs. 4, 7

Distribution: Continental shelf: very rare.

Order ROTALIIDA Lankester, 1885

Superfamily DISCORBACEA Ehrenberg, 1838

Family BAGGINIDAE Cushman, 1927

Subfamily BAGGININAE Cushman, 1927

Genus CANCRIS de Montfort, 1808

Cancris sagra (d’Orbigny)

= Rotalia sagra d’Orbigny, 1839

Plate 6.6, figs. 15-17

Distribution: Continental shelf: very rare. Living specimens were found as deep as 3 cm

below sediment-water interface.

Genus NEOCROSBYIA McCulloch, 1977

Neocrosbyia minuta (Parker)

252

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. = Valvulineria minuta Parker, 1954

Plate 6.6, figs. 19,20

Distribution: Continental slope: very rare.

Family EPONIDIDAE Hofker, 1951

Genus EPONIDES de Montfort, 1808

Eponides sp. cf. E regularis Phleger and Parker, 1951

Plate 6.6, figs. 24,25

Remarks: Not as biconvex as E. regularis specimens figured by Phleger and Parker.

Distribution: Continental slope: very rare.

Family DISCORBIDAE Ehrenberg, 1838

Genus NEOEPONIDES Reiss, 1960

Neoeponides antillarum (d’Orbigny)

- Rotalina antiUarum d’Orbigny, 1839

Plate 6.6, figs. 13,14

Distribution: Continental shelf: very rare.

Family ROSALINIDAE Reiss, 1963

Genus GAVELINOPSIS Hoefker, 1951

Gavelinopsis translucens (Phleger and Parker)

= Rotalia translucens, Phleger and Parker, 1951

Plate 6.6, figs. 11, 12

Distribution: Continental slope: common. Living specimens were found as deep as 4 cm

within the sediment

Superfamily SIPHONINACEA Cushman, 1927

253

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Family SIPH0NIN1DAE Cushman, 1927

Genus SIPHONINA Reuss, 1850

Siphonina bradyana Cushman, 1927

Plate 6.6, figs. 18,23

Distribution: Continental slope: common.

Superfamily DISCORBINELLACEA, Sigal, 1952

Family PARRELLOIDIDAE Hofker, 1956

Genus CIBICIDOIDES Thalmann, 1939

Cibicidoides incrassatus (Fichtel and Moll)

= Nautilus incrassatus Fichtel and Moll, 1798

Plate 6.6, figs. 21,22

Distribution: Continental slope: very rare.

Cibicidoides (Cushman)io

= Cibicides pseudoungeriana (Cushman) var. io Cushman, 1931

Plate 6.7, figs. 1,2

Distribution: Continental slope: very rare.

Cibicidoides umbonatus (Phleger and Parker)

= Cibicides umbonatus Phleger and Parker, 1951

Plate 6.6, figs. 26,27

Distribution: Continental slope: very rare.

Family PSEUDOPARRELLIDAE Voloshinova, 1952

Subfamily PSEUDOPARRELLINAE Voloshinova, 1952

Genus EPISTOMINELLA Husezima and Maruhasi, 1944

254

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.7

Parrelloididae, Pseudoparrellidae, Planulinidae, Nonionidae, and Gavelinellidae (Ail scale bars represent 50 pm)

1,2. Cibicidoides (Cushman)io

3,4. Planulina ariminesis d’Orbigny

5,6. Planulina faveolata (Brady)

7,16,17. Epistominella exigua (Brady)

8-10. NonioneUa basiloba Cushman and McCulloch

11,12. Epistominella vitrea Parker

13-15. Nonionella sp. cf. N. basUoba Cushman and McCulloch

18. Pullenia (?) sp.

19. Nonionion sp.

20. Astrononion tumidum Cushman and Edwards

22,23. Gyroidinoides cf. G. rodundimargo (check the author)23,

24. Gyroidinoides altiformis (Stewart and Stewart)

255

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.7

256

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Epistominella exigua (Brady)

= Putvinulina exigua Brady, 1884

Plate 6.7, figs. 7,16,17

Distribution: Continental slope: rare. Living specimes were found from the water

interface down to a depth of 2 cm.

Epistominella vitrea Parker, 1953

Plate 6.7, figs. 11,12

Distribution: Continental shelf: very abundant. E. vitrea is of the most abundant species

found on the continental shelf. It dominates the foraminiferal populations within and in

the vicinity of the Mississippi River plume. In water depths between 35 and 80 m, living

specimens were commonly found down to a depth of 4-5 cm below the sediment-water

interface. It seems to prefer the 3-5 centimeter interval where it dominates the living

population of Foraminifera.

Superfamily PLANORBULINACEA Schwager, 1877

Family PLANULINIDAE Bermuda, 1952

Genus PLANULINA d’Orbigny, 1826

Planulina ariminesis d’Orbigny, 1826

Plate 6.7, figs. 3,4

Distribution: Continental slope: rare to common.

Planulinafaveolata (Brady)

= Anomalina faveolata Brady, 1884

Plate 6.7, figs. 5,6

Distribution: Continental slope: very rare.

2 5 7

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Superfamily NONIONACEA Schultze, 1854

Family NONIONIDAE Schultze, 1854

Subfamily NONIONINAE Schultze, 1854

Genus NONION, de Montfort, 1808

N onion sp.

Plate 6.7, fig. 19

Remarks: Test free, involute, bilaterally symmetrical, somewhat longer than broad,

periphery subacute, outline somewhat serrate; sutures distinct, depressed and curved; wall

calcareous, surface smooth.

Distribution: Continental slope: very rare.

Genus NONIONELLA Cushman, 1926

Nonioneiia basiloba Cushman and McCulloch, 1940

Plate 6.7, figs. 8-10

Distribution: Continental shelf: very abundant. Living specimens were commonly found

down to a depth of 6-7 cm within the sediment; a few were found even at depths of 11-12

cm.

N onioneiia sp. cf. N. basiloba Cushman and McCulloch, 1940

Plate 6.7, figs. 13-15

Remarks: These specimens slightly differ from N. basiloba in having a less inflated last

chamber.

Distribution: Continental shelf: rare.

Subfamily ASTRONONIONINAE Saidova, 1981

Genus ASTRONONION Cushman, 1937

2 5 8

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Astrononion tumidum Cushman and Edwards

Plate 6.7, figs. 20

Distribution: Continental slope: very rare.

Superfamily CHILOSTOMELLACEA Brady, 1881

Family OSANGULARHDAE Loeblich and Tappan, 1964

Genus OSANGULARIA Brotzen, 1940

Osangularia rugosa (Phleger and Parker)

= Pseudoparella rugosa (?) Phleger and Parker, 1951

Plate 6.8, figs. 1,2

Distribution: Continental slope: rare to common. Living specimens were found from the

top sediment to a depth of 3 cm below sediment-water interface.

Family GAVELINELLIDAE Hofker, 1956

Subfamily GYROIDINOIDINAE Saidova, 1981

Genus GYROIDINOIDES Brotzen, 1942

Gyroidinoides sp. cf. G. rodundimargo (Stewart and Stewart)

= Gyroidina soldanii d’Orbigny, var. rotundimargo Stewart and Stewart, 1930

Plate 6.7, figs. 22,23

Remarks: Our specimens differ from G. rotundimargo (Stewart and Stewart) in having

less chambers.

Distribution: Continental slope: very rare.

Gyroidinoides aitiformis (Stewart and Stewart)

= G yroidina so ld a n ii d’Orbigny, var. aitiformis, Stewart and Stewart, 1930

Plate 6.7, figs. 23,24

259

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. PLATE 6.8

Osangulariidae, Gavelinellidae, Rotaliidae, and Elphidiidae (All scale bars represent 50 pm)

1,2. Osangularia rugosa (Phleger and Parker)

3 ,4. Hansenisca sp. cf. H. soldanii (d’Orbigny)

5-9. Hanzawaia concentrica (Cushman)

10,11. Ammonia parkinsoniana (d’Orbigny)

12-16. Elphidium excavatum (Terquem)

17. Elphidium poyeanum (d’Orbigny)

260

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261

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Distribution: Continental slope: very rare.

Subfamily GAVELINELLINAE Hofker, 1956

Genus HANSENISCA Loeblich and Tappan, 1988

Hansenisca sp. cf. H. soldanii (d’Orbigny)

= Gyroidina soldanii d’Orbigny, 1826

Plate 6.8, figs. 3,4

Remarks: our specimes have less numerous chambers and do not have a depressed spiral

side.

Distribution: Continental slope: very rare.

Genus Hanzawaia Asano, 1944

Hanzawaia concentrica (Cushman)

= Truncatulina concentrica Cushman, 1918

Plate 6.8, figs. 5-9

Distribution: Continental shelf: very rare.

Superfamily ROTALIACEA Ehrenberg, 1839

Family ROTALIIDAE Ehrenberg, 1839

Subfamily AMMONHNAE Saidova, 1981

Genus AMMONIA Briinnich, 1772

Ammonia parkinsoniana (d’Orbigny)

= Rosalina parkinsoniana d’Orbigny, 1839

Plate 6.8, figs. 10,11

Distribution: Continental shelf: abundant. Abundant live specimens were found on the

continental shelf in waters shallower than 30 m. Living specimens were commonly found

262

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. from top sediments down to 10 cm below the sediment-water interface in these shallow

waters.

Family ELPHIDIIDAE Galloway, 1933

Subfamily ELPHEDIINAE Galloway, 1933

Genus ELPHIDIUM de Montfort, 1808

Elphidium excavatum (Terquem)

= Polystomella excavata Terquem, 1875

Plate 6.8, figs. 12-16

Distribution: Continental shelf: rare to common.

Elphidium poyeanum (d’Orbigny)

= Polystomella poeyana d’Orbigny, 1839

Plate 6.8, fig. 17

Distribution: Continental shelf: rare.

Unknown Genus and Species

Plate 6.7, fig. 18

Remarks: Test free, planispiral, involute, somewhat globular; wall calcareous, surface

smooth; aperture a small interiomarginal opening.

Distribution: Continental slope: rare.

263

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SUMMARY AND CONCLUSIONS

264

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. In this study I documented the foraminiferal microhabitat distribution and

temporal variation of species richness, species diversity, and abundances of foraminiferal

species on two areas on the continental margin of the Gulf of Mexico. (1) Spatial and

temporal variations of foraminiferal communities/assemblages were investigated in the

context of seasonal changes in oxygen content of Louisiana continental shelf bottom

waters. (2) On the continental slope, living and fossil Foraminifera were analyzed with

the aim of better understanding foraminiferal distribution and adaptation in and under

cold seep Beggiatoa mats as well as to evaluate their potential for historical

reconstruction of hydrocarbon emissions. Significant findings of this work are

summarized in the conclusions listed below.

1. Many species of benthic Foraminifera exist under seasonal hypoxia on the

Louisiana continental shelf. This finding is consistent with field and laboratory

investigations of previous workers on foraminiferal tolerance of severe oxygen depletion.

At any given location, the composition of the present foraminiferal community is

particularly dependent on water depth, distance from the Mississippi River plume, and

dissolved oxygen at the sediment-water.

2. Judging by their microhabitat preferences and dominances within living

foraminiferal assemblages, several species are microaerophilitic or facultative anaerobes.

The most notable are Buliminella morgani, Nonioneiia basiloba , and Bolivina lowmani.

3. The Ammonia-Elphidium index (based on species proportions in core samples)

is a sensitive proxy for paleohypoxia in water depths less than about 30 m. In greater

depths, the reduced abundances of both genera diminish the reliability of this proxy.

2 6 5

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 4. On the Louisiana continental shelf, the change in the intensity of hypoxia in the

late 1930s and early 1940s, as well as its further development are suggested by the

distribution pattern of species diversity index, species richness, and relative abundances

of agglutinated and porcelaneous taxa, and by the changes of the total assemblage

structure. Temporal distribution of species diversity recorded in samples from 60 m water

depth can be divided into three intervals: (I) relatively high diversity prior to mid-l930s;

(2) decreasing species richness but somewhat stable species proportions from mid 1930s

to early 1970s; (3) low and relatively stable species diversity from early 1970s up to

1997. Relative abundances of agglutinated and porcelaneous groups diminished severely

in the last one hundred years on the Louisiana continental shelf. Several stratigraphically-

separated assemblages demonstrate the overall change of the foraminiferal composition

in Recent sediments from the northern Gulf of Mexico.

5. Some hyaline taxa, mainly Nonioneiia, Buliminella, and Epistominella , cope

well with the progressive oxygen depletion in the northern Gulf of Mexico, showing an

opportunistic behavior when abundances of agglutinated and porcelaneous foraminifers

are strongly diminished. The disappearance of Quiqueloculina (mainly known from well

oxygenated modem environments) seems to be related to the progression of the seasonal

hypoxia. Furthermore, the historical distribution of the genus Quinqueloculina suggests

that critical oxygen levels reached nearshore waters (station G27) towards the end of the

1800s whereas similar conditions affected relatively deeper waters (station E60) only in

the mid 1900s.

6. The similarity between the foraminiferal pattern recorded at 60-m water depth

and that recorded at 30-m water depth (BL10 core of Blackwelder et al., 1996) suggests

266

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. that hypoxia has worsened in the past century even near the outer edge of the present-day

zone of seasonal oxygen depletion. Foraminiferal trends observed at these two stations

match the temporal distribution of the fertilizer use in the U.S., showing the

anthropogenic contribution to progressive hypoxia in the last six decades of the twentieth

century.

7. The distribution pattern of the summed relative abundances of the agglutinated

and porcelaeous groups (A-P index) indicates an overall rise in oxygen stress (increasing

hypoxia) on the Louisiana continental shelf in water depths from 30 to 60 meters. The

A-P index trends suggest potential use of higher level taxa in tracing recent and ancient

hypoxia. Nevertheless, the reliability of the A-P index as a hypoxia marker should be

further tested. Future studies may attempt to correlate the A-P index distribution with that

of parameters such as %BSi and/or organic carbon.

8. Results of this study demonstrate the utility of the foraminiferal record in

assessing the historical evolution of hypoxia on continental shelves and thus their

potential in deciphering similar but ancient phenomena. However, for gaining further

insight into changes of foraminiferal pattern and their relationships with hypoxia in the

northern Gulf of Mexico, longer stratigraphic records should be examined.

9. Several species of benthic Foraminifera live within the top few centimeters of

sediment at hydrocarbon seep sites in Green Canyon. The common species are Bolivina

albatrossi, B. ordinaria, Cassidulina neocarinata , Osangularia rugosa, Fursenkoina

compressa, and Trifarina bradyi. Furthermore, it seems that Bolivina has a higher

tolerance than the other taxa to the harsh conditions associated with seeps. The data I

examined so far indicate that certain foraminiferal species of slope environments can

267

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. survive limited amounts of both oil and H 2 S but none of the species apparently benefits

from these compounds.

10. Our results show that the isotopic signatures of benthic foraminiferal species

are good indicators of hydrocarbon releases and can be used in historical reconstruction

of seep activity. In the analyzed core, temporal distribution of the isotopic composition of

Bolivina tests suggests that seep activity at this spot began about 1600 years ago. A better

understanding of the relationship between foraminiferal isotopic signatures and methane

seepage will result from additional work on isotopic composition of species that currently

live at active seep sites. Other species living in these environments, especially those

common in some other areas of the world, should be included in future isotopic analysis.

11. Negative carbon isotope excursions in the genus Bolivina associated with

biomineralization constitute additional proof that these organisms grow and live in

sediments of hydrocarbon seeps. We infer that benthic Foraminifera populating the cold

vents of northern Gulf of Mexico perhaps reproduce at and/or very close to the surface

where more oxygen is available and prevalent amounts of H 2S and oil do not interfere

with this process.

12. A severe decline of foraminiferal density represents the major foraminiferal

response to environmental changes that affected the JSL2900-PC2 site. The presence of

survivor species before seepage initiation supports the previous observation that living

Foraminifera at seeps sites are not endemic.

Numerous species of benthic Foraminifera live in oxygen depleted environments

of the northern Gulf of Mexico, i.e., in the zone of seasonal hypoxia on the continental

shelf and in habitats around hydrocarbon vents on the slope. Besides oxygen reduction,

268

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. H2S and gaseous and/or liquid petroleum are additional environmental stressors in the

hydrocarbon seep habitats. Changes in the structure of benthic foraminiferal assemblages

from these habitats allow us to assess the areal distribution and temporal evolution of

these stressed environments.

269

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. REFERENCES

Aharon, P., 1994. Geology and biology of modem and ancient submarine hydrocarbon seeps and vents: An introduction. Geo-Marine Letters, v. 14, p. 69-73

, in press. Microbial processes and products fueled by hydrocarbons in submarine seeps. In: Riding, R., and Awramik, S. M. (eds.), Microbial Sediments, Springer- Verlag, Berlin.

, Graber, E. R., and Roberts, H. H., 1992. Dissolved carbon and 8^C anomalies in the water column caused by hydrocarbon seeps on the northwestern Gulf of Mexico slope. Geo-Marine Letters, v. 12, p. 33-40

, and Sen Gupta, B. K., 1994. Bathymetric reconstructions of the Miocene-age "calcari a Lucina” (Northern Apennines, Italy) from oxygen isotopes and benthic foraminifera. Geo-Marine Letters, v. 14, p. 219-230

, Schwarcz, H.P. and Roberts, H.H., 1997. Radiometric dating of submarine hydrocarbon seeps in the Gulf of Mexico. Geological Society of America Bulletin, v.109 (5) p. 568-579

Akimoto, K., Tanaka, T., Hattori, M., and Hotta, H., 1994. Recent benthic foraminiferal assemblages from cold seep communities - A contribution to the methane gas indicator. In: Tsuchi, R. (ed.), Pacific Neogene Events in Time and Space, University of Tokyo Press, Tokyo, p. 11-25

Alve, E, 1990. Variations in estuarine foraminiferal biofacies within diminishing oxygen conditions in Drammensfjord, SE Norway. In: Hemleben, C., Kaminski, M., Kuhnt, W., and Scott, D. B. (editors), Paloecology, Biostratigraphy, and Taxonomy of Agglutinated Foraminifera, Kluwer, Dordrecht, p. 661-694

, 1991. Benthic Foraminifera in sediment cores reflecting heavy metal pollution in Sorfjord, western Norway. Journal of Foraminiferal Research, v. 21, p. 1-19

, 1994, Opportunistic features of the foraminifer Stainforthia Jusiformis (Williamson): Evidence from Frierfjord, Norway. Journal of Micropalaeontology, v. 13, p. 24

, 1995a. Benthic foraminiferal distribution and recolonization of formely anoxic environments in Drammensfj ords, southern Norway. Marine Micropaleontology, v. 25, p. 169-186

, 1995b. Benthic foraminiferal responses to estuarine pollution: A review. Journal of Foraminiferal Research, v. 25, p. 190-203

2 7 0

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , and Bernhard, J. M., 1995. Vertical migratory response of benthic Foraminifera to controlled decreasing oxygen concentrations in an experimental mesocosm. Marine Ecology Progress Series, v. 116, p 137-151

Ballard, R. D., 1984. The exploits of Alvin and Angus: Exploring the East Pacific Rise. Oceanus, v. 27, no. 3, p. 7-14

Bandy, O. L., 1954. Distribution of some shallow-water Foraminifera in the Gulf of Mexico. U. S. Geological Survey Professional Paper, v. 254 F, p. 125-141

, 1956. Ecology of Foraminifera in northeastern Gulf of Mexico. U. S. Geological Survey, Professional Paper, v. 274-G, p. 179-206

, Ingle, J. C. Jr., and Resig, J. M., 1964a. Foraminiferal trends, Laguna Beach outfall area, California. Limnology and Oceanography, v. 9, p. 112-123

, Ingle, J. C. Jr., and Resig, J. M., 1964b. Foraminifera, Los Angeles County outfall area, California. Limnology and Oceanography, v. 9, p. 9124-137

, Ingle, J. C. Jr., and Resig, J. M., 1965. Foraminiferal trends, Hyperion Outfall, California. Limnology and Oceanography, v. 10, p. 314-322

Bates, J. M., and Spencer, R. S., 1979. Modifications of foraminiferal trends by the Chesapeake-Elizabeth sewage outfall, Virginia Beach, Virginia. Journal of Foraminiferal Research, v. 9, p. 125-140

Barmawidjaja, D. M., Jorrisen, F. J., Puskaric, S., and van der Zwaan, G. J., 1992. Microhabitat selection by benthic Foraminifera in the northern Adriatic Sea. Journal of Foraminiferal Research, v. 22, p. 137-151

Bernhard, J. M., 1988. Postmortem vital staining in benthic foraminifera: Duration and importance in population and distributional studies. Journal of Foraminiferal Research, v. 18, p. 143-146.

, 1989. The distribution of benthic foraminifera with respect to oxygen concentration and organic carbon levels in shallow-water Antarctic sediments. Limnology and Oceanography, v. 134, p. 1131-1141

, 1993. Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Marine Micropaleontology, v. 20, p.203-213.

, 1996. Microaerophilic and facultative anaerobic benthic foraminifera: A review of experimental and ultrastructural evidence. Revue de Paleobiologie, v.15, p. 261- 275

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , and Alve, E., 1996. Survival, ATP pool, and ultrastructural characterization of benthic foraminifera from Drammmensfjord (Norway): response to anoxia. Marine Micropaleontology, v. 28, p. 5-17

, Buck, K. R., and Barry J. P., in press. Monterey Bay cold-seep biota: Assemblages, abundance, and ultrastructure of living foraminifera. Deep-Sea Research

, and Reims, C. E., 1991. Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin. Biogeochemistry, v. 15, p. 127-149

, and Sen Gupta, B. K., 1999. Foraminifera of oxygen depleted environments. In: B. K. Sen Gupta (ed.), Modem Foraminifera, Kluwer Academic Publishers, Dordrecht, p. 201-216

, Sen Gupta, B. K., and Bome, P. F., 1997. Benthic foraminiferal proxy to estimate dysoxic bottom-water oxygen concentrations: Santa Barbara Basin, U. S. Pacific continental margin. Journal of Foraminiferal Research, v. 27, p. 301-310

Berthold, W. U., 1976. Ultrastructure and function of wall perforations in Patellina corrugata Williamson, Foraminiferida. Journal of Foraminiferal Research, v. 6 p. 22-29

B izon, G. and Bizon, J. J. 1984. Distribution des foraminif&res sur le plateau continental au large du Rhone. In: Bizon, J. J and Burollet, P. F (eds.), Ecologie des microorganismes en M6diteranee occidentale ‘ECOMED’. Association Franfais des Techniciens du Pdtrole, Paris, p. 84-94

Blackwelder, P., Hood, T., Alvarez-Zarikian, C., Nelsen, T. A., and McKee, B., 1996. Benthic Foraminifera from the NECOP study area impacted by the Mississippi River plume and seasonal hypoxia. Quaternary International, v. 31, p. 19-36

Boesch, D. F., and Rabalais, N. N., 1991. Effects of hypoxia on continental shelf benthos: Comparison between the New York Bight and die northern Gulf of Mexico. In: Tyson, R. V., and Pearson, T. H. (eds.), Modem and ancient continental shelf anoxia: Geological Society of London, special Publication, v. 58, p. 27-34

Brooks, J. M., Kennicutt, M. C., Fisher, C. R., Macko, S. A., Cole, K., Childress, J. J., Bidigare, R. R., and Vetter, R. D., 1987. Deep-sea hydrocarbon seep communities: Evidence for energy and nutritional carbon sources. Science, v. 238, p. 1138-1142

Buzas, M. A., 1965. The distribution and abundance of Foraminifera in Long Island Sound. Smithsonian Institution Miscellaneous Collection, v. 149 (1), p. 1-88

272

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , and Gibson, T. G., 1969. Species diversity: Benthonic Foraminifera in western North Atlantic. Science, 163, p. 72-76

Carman, K. R., Fleeger, J. W., Means, J. C., Pomarico, S. M., and McMillin, D. G., 1995. Experimental investigation of the effects of polynuclear aromatic hydrocarbons on an estuarine sediment food web. Marine Environmental Research, v. 40, p. 289-318

Camey, R. S., 1994. Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents. Geo-Marine Letters, v. 14, p. 149-159

Childress, J. J., Fisher, C. R., Brooks, J. M., Kennicutt II. M. C., Bidigare. R., and Anderson, A., 1986. A metanotrophic molluscan (Bivalvia: Mytillidae) symbiosis: mussels fheled by gas. Science, v. 233, p. 306-1308

Commeau, R. F., Pauli, C. K., Commeau, J. A., and Poppe, L. J., 1987. Chemistry and mineralogy of pyrite-enriched sediments at a passive margin sulfide brine seep: abyssal Gulf of Mexico. Earth and Planetary Science Letters, v. 82, p. 62-74

Cooper, S. R. and Brush, G. S., 1991. Long-term history of Chesapeake Bay anoxia. Science, v. 254, p. 992-996

, and Brush, G. S., 1993. A 2,500-year history of anoxia and eutrophication in Chesapeake Bay. Estuaries, v. 16, no. 3B, p. 617-626

Corliss, B. H., and Emerson, S. R., 1990. Distribution of Rose Bengal stained deep-sea benthic Foraminifera from the Nova Scotia continental margin and Gulf of Maine. Deep-Sea Research, v. 37, p. 381- 400

, and Fois, E., 1991. Morphotype analysis of deep-sea bethic Foraminifera from the northwest Gulf of Mexico. Palaios, v. 5, p. 589-605

Corliss J. B., Dymond, J., Gordon, L. I., Edmond, J. M., Von Herzen R. P., Ballard, R. D., Green, K., Williams, D., Brainbridge, A., Crane, K., and Van Andel, T. H., 1979. Submarine thermal springs on the Galapagos rift. Science v. 203, p. 1073- 1083

CWPPRA. Atchafalaya Basin [Online], 6 paragraphs. Available: http://www.lacoast.gov/Programs/CWPPRA/Projects/atchafaIaya/ atch_basdyn.html

CWPPRA. Mississippi River Delta Basin [Online], 9 paragraphs. Available: http://www.lacoast.gov/Programs/CWPPRA/Projects/mississippi/Index.htni

27 3

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Culver, S. J., and Buzas, M. A., 1981. Foraminifera distribution of provinces in the Gulf of Mexico. Nature, v. 290, p. 328-329

Curray, J. R., I960. Sediments and history of Holocene transgression, continental shelf, northwestern Gulf of Mexico. In Shepard, F. P. (ed.), Recent Sediments, northwestern Gulf of Mexico, American Association of Petroleum Geologists, Tulsa, Okla., pp. 221-266

Davies, D. K., 1972. Deep sea sediments and their sedimentation, Gulf of Mexico. American Association of Petroleum Geologists Bulletin, v. 56, p. 2212-2239

Davies, D. K., and Moore, W. R., 1970. Dispersal of Mississippi sediment in the Gulf of Mexico. Journal of Sedimentary Petrology, v. 40, p. 339-353

Davis, J. C., 1973. Statistics and Data Analysis in Geology. New York, Wiley, 550 p.

Denne, R. A., 1990. Late Quaternary Foraminifera of the Northwestern Gulf of Mexico: Ph. D. dissertation, Louisiana State University, Baton Rouge, 488 p.

, and Sen Gupta, B. K., 1991. Association of bathyal Foraminifera with water masses in the northwestern Gulf of Mexico. Marine Micropaleontology, v. 17, p. 173-193

, and Sen Gupta, B. K., 1993. Matching of benthic foraminiferal depth limits and water-mass boundaries in the northwestern Gulf of Mexico. Journal of Foraminiferal Research, v. 23, p. 108-117

Diaz R. J. and Rosenberg R., 1995. Marine benthic hypoxia: A review of its ecological effects and behavioural responses of benthic macrofauna. Oceanography and Marine Biology: an Annual Review, v. 33, p. 245-305

Dickens, G. R., Castillo, M. M., and Walker, J. C. G., 1997. A blast of gas in the latest Paleocene: Simulating first-order effects of massive dissociation of oceanic methane hydrate. Geology, v. 25 p. 259-262

Dickens, G. R., O’Neil, J. R., Rea, D. K., and Owen, R. M., 1995. Dissociation of oceanic methane hydrate as a cause of the carbon isotope excursion at the end of the Paleocene. Paleoceanography, v. 10, p. 965-971

Dortch, Q., Rabalais, N. N., Turner, R. E., and Rowe, G. T., 1994. Respiration rates and hypoxia on the Louisiana shelf. Estuaries, v. 17, p. 862-872

Ellis, B. F., and Messina, A. R., 1940 and later. Catalogue of Foraminifera. American Museum of Natural History, New York

274

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Engen, S., 1979. Some basic concepts of ecological equitability, in Ecological Diversity In: Grassle, J. F., Patil, G. P., Smith, W., and Taillie, C. (eds.) Theory and Practice. International Cooperative Publishing House, Fairland, Maryland, p. 37- 50

Epstein, S., Buchsbaum, R., Lowestam, H. A., and Urey, H. C., 1953, Revised carbonate- water isotopic temperature scale. Geological Society of America Bulletin, v. 64, p. 1315-1326

Fenchel, T., and Finlay, B. J., 1995. Ecology and Evolution in Anoxic Worlds, Oxford University Press, Oxford, 276 p.

Fisher, C. R., Childress, J. J., Oremland, R. S., Bidigare, R. R., 1987. The importance of methane and thiosulfate in the metabolism of the bacterial symbionts of two deep- sea mussels, Marine Biology, v. 96, p. 59-71

Fu, B., Aharon. P., Byrely, G. R., and Roberts, H. H., 1994. Barite chimneys on the Gulf of Mexico slope: Initial report on their petrography and geochemistry. Geo- Marine Letters, v.14, p. 81-87

Gaston, G. R., 1985. Effects of hypoxia on macrobenthos of the inner shelf off Cameron, Louisiana. Estuarine, Coastal and Shelf Science, v. 20, p. 603-613

Gibson, L. B., 1966. Foraminiferal species diversity distribution, eastern Gulf of Mexico (abs.). American Association of Petroleum Geologists Bulletin, v. 50, p. 614-615

Gooday, A. J., 1988. A response by benthic foraminifera to the deposition of phytodetritus in the deep sea. Nature, v. 332, p. 70-73

, 1993. Deep-sea benthic foraminiferal species which exploit phytodetritus: Characteristic features and controls on distribution. Marine Micropaleontology, v. 22, p. 187-205

Gordon, R. B., 1980. The sedimentary system of Long Island Sound. Advances in Geophysics, v. 22, p. 1-39

Gore, R. H., 1992. The Gulf of Mexico, Pineapple Press, Inc., Sarasota, 384 p.

Graber, E. R., Aharon, P., and Roberts, H. H., 1990. Pore water chemistry from hydrocarbon vents on the Gulf of Mexico slope. Geological Society of America Abstracts with Programs, v. 22, p. A 208

Grossman, E. L., 1987. Stable isotopes in modem benthic foraminifera: A study of vital effect Journal of Foraminiferal Research, v. 17, p. 48-61

27 5

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Hunt, A. S., and Corliss, B. H., 1993. Distribution and microhabitats of living (stained) benthic foraminifera from the Canadian Arctic Archipelago. Marine Micropaleontolgy, v. 20, p. 321-345

Ingle, J. C., Keller, G., and Kolpack, R. L., 1980. Benthic foraminiferal biofacies, sediments and water masses of the southern Peru-Chile Trench area, southeastern Pacific Ocean. Micropaleontology, v. 26, p. 113-50

Iwama, G. K., 1998. Stress in fish. In: Csermely, P. (ed.), Stress of Life from Molecules to Man, Annals of the New York Academy of Science, New York, p. 304-310

Jannash, H. W., and Mottl, M. J., 1985. Geomicrobiology of deep-sea hydrothermal vents. Science, v. 229, p. 717-725

Jannink., N. T., Zachariasse, W. J., and van der Zwaan, G. J., 1998. Living (Rose Bengal stained) benthic Foraminifera from Pakistan continental margin (northern Arabian Sea). Deep-Sea Research, v. 145, p. 1483-153

Johnson, K. S., Childress, J. J., Hessler, R. R., Sakamoto-Amold C. M., and Beehler, C. L., 1988. Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep-Sea Research, v. 35, p. 1723-1744

Jones, P., 1987. Differences in microhabitat, abundances, biomass and body size between oxybiotic and thiobiotic free-living marine nematodes. Oecologia (Berlin), v. 71, p. 564-567

, 1993. Preliminary observations on benthonic Foraminifera associated with biogenic gas seep in the North Sea. In: Jenkins, D. G. (ed.), Applied Micropaleontology, Kluwer Academic, p. 69-91

Jonkers, H. A. 1984. Pliocene benthic Foraminifera from homogenous and laminated marls on Crete. Utrecht Micropaleontological Bulletins, v. 31, p. 1-179

Jorgensen, B. B., 1977. Distribution of colorless sulfur bacteria (Beggiatoa spp.) in a coastal marine sediment. Marine Biology, v. 41, p. 19-28

, 1982. Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Philosophical Transactions, Royal Society of London, v. B298, p. 543-561

, and Revsbech, N. P., 1983. Colorless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in 02 and H2S microgradients. Applied and Environmental Microbiology, v. 45, p. 1261-1270

Jorissen, F. J., 1987. The distribution of benthic Foraminifera in the Adriatic Sea. Marine Micropaleontology, v. 12, p. 21-48

276

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , 1999. Benthic foraminiferal microhabitats below the sediment-water interface, In: B. K. Sen Gupta (ed.), Modem Foraminifera, Kluwer Academic Publishers, Dordrecht, p. 161-180

, Barmawidjaja, D. M., Puskaric, S., and van der Zwaan, G. J., 1992. Vertical distribution of benthic Foraminifera in the northern Adriatic Sea: The relation with the organic flux. Marine Micropaleontology, v. 19, p. 131-146

Josefson, A. B., and Widbom, B., 1988. Differential response of benthic meiofauna and macrofauna to hypoxia in the Gullmar Fjord basin. Marine Biology, v. 100, p. 31 - 40

Juniper, S. K. and Sibuet, M., 1987. Cold seep benthic communities in Japan: spatial organization, trophic strategies, and evidence for temporal evolution. Marine Ecology Progress Series, v. 40, p. 115-126

Justic, D., Rabalais, N. N„ Turner, R. E., and Dortch, Q., 1995. Changes in nutrient structure of river-dominated coastal waters: Stoichiometric nutrient balance and its consequences. Estuarine, Coastal and Shelf Science v. 40, p. 339-356

Kennett, J. P., Hendy, I. L., and Behl, R. J., 1996. Late Quaternary foraminiferal carbon isotopic record in Santa Barbara Basin: Implications for rapid climate change. Eos, Transactions American Geophysical Union v. 77 no.46 p. 294

Kennicutt, M. C., Brooks, J. M., Bidigare, R. R., Fay, R. R., Wade T. L., and McDonald, T. J., 1985. Vent type taxa in a hydrocarbon seep region on the Louisiana slope. Nature v. 317, p. 351-353

Kitazato, H., 1994. Foraminiferal microhabitats in four marine environments around Japan. Marine Micropaleontology, v. 24, p. 29-41

, H., 1996. Benthic Foraminifera associated with cold seepages: Discussion of their faunal characteristics and adaptations. Fossils, v. 60, p. 48-52

Karlsen, A.W., Cronin, T. M., Ishman, S.E., Willard, D. A., Kerhin, R., Holmes, C. W., and Marot, M., 2000. Historical trends in Chesapeake Bay dissolved oxygen based on benthic Foraminifera from sediment cores. Estuaries, v. 23, p. 488-508

Kvenvolden, K. A., 1993. Gas hydrates-geological perspective and global change. Reviews in Geophysics, v. 31, p. 173-187

Koppelman, L. E., Weyl, P. K., Grant Gross, M., and Davies, D. S., 1976. The Urban Sea: Long Island Sound. New York: Praeger Publishers, 223 p.

277

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Kulm, L. V. D., Suess, E., 1990. Relationship between carbonate deposits and fluid venting: Oregon accretionary prism. Journal of Geophysical Research, v. 95 (B6) p. 8899-8915

Kulm, L. V. D., Suess, E., Moore, J. C., Carson, B., Lewis, B. T., Ritger, S. D., Kadko, D. C., Thornburg, T. M., Embley, R. W., Rugh, W. D., Massoth, G. J., Langseth, M. G., Cochrane, G. R., and Scamman, R. L., 1986. Oregon subduction zone: Venting, fauna, and carbonates. Science, v. 231, p. 561-566

Lankford, R., R., 1959. Distribution and ecology of the foraminifera from East Mississippi Delta margin. American Association of Petroleum Geologists Bulletin, v. 43, p. 2068-2099

Larkin, J. M., Aharon, P., and Henk, M. C., 1994. Beggiatoa in microbial mats at hydrocarbon vents in the Gulf of Mexico and Warm Mineral Springs, Florida. Geo-Marine Letters, v. 14, p. 97-103.

, and Strohl, W. R., 1983. Beggiatoa, Thiothrix, and Thioploca. Annual Review of Microbiology, v. 37, p. 341-367.

LaRock, P. A., Hyun J-H., and Bennison, B. W. 1994: Bacterioplankton growth and production at the Louisiana hydrocarbon seeps. Geo-Marine Letters, v. 14, p. 104- 109.

Layboum-Parry, J., 1984. A Functional Biology of Free-Living Protozoa, University of California Press, Berkeley, 218 p.

Lee, J. J., and Anderson, O. R., 1991. Biology of Foraminifera, Academic Press, San Diego, 380 p.

Linke, P., Altenbach, A.V., Graf, G., and Heeger, T., 1995. Response of deep-sea benthic Foraminifera to a simulated sedimentation event. Journal of Foraminiferal Research, v. 25, p. 75-82

Locklin, J. A., and Maddocks, R. F., 1982. Recent Foraminifera around petroleum production platforms on Southwest Louisiana Shelf. Gulf Coast Association of Geological Societies, Transaction, v. 32, p. 377-397

Lohrenz, S. E., Dagg, M. J., and. Whitledge, T. E., 1990. Enhanced primary production at the plume/oceanic interface of the Mississippi River. Continental Shelf Research, v. 10, p. 639-664

Loeblich, A. R., and Tappan, H, 1987. Foraminiferal Genera and Their Classification, v. 1-2, Van Nostrand Reinhold, New York

278

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Loeblich, A. R., and Tappan, H, 1992. Present status of foraminiferal classification. In: Takayanagi, Y., and Saito, T. (eds.), Studies in Benthic Foraminifera, Proceedings of the Fourth International Symposium on Benthic Foraminifera, Sendai, 1990 (Benthos ’90), Tokai University, Press, Tokyo, Japan, p. 93-102

Lowman, S. W., 1949. Sedimentary facies in Gulf Coast. American Association of Petroleum Geologists Bulletin, v. 33, p. 1939-1997

Lutze, G. F. 1980. Depth distribution of benthic foraminifera on the continental margin offNW Africa. ‘Meteor’ Forschungs-Ergebnisse, Reihe C, 32, p. 31-80

Lynts, G. W., 1962. Distribution of recent Foraminifera in upper Florida bay and associated sounds. Contributions from the Cushman Foundation for Foraminiferal Research, v. 16, p. 67-69

, 1965. Observation on some recent Florida Bay Foraminifera. Contributions from the Cushman Foundation for Foraminiferal Research, v. 16, p. 67-69

, G. W., 1966. Variation of foraminiferal standing crop over short lateral distances in Buttonwood Sound, Florida Bay. Limnology and Oceanography, v. 11, pp. 562-566

MacDonald, G. T., 1990. Role of methane clathrates in past and future climates. Climate Change, v. 16, p. 247-281

MacDonald, I. R., Callender, W. R., Burke, R. A., Macdonald, S. J., and Carney, R. S., 1990. Fine scale distribution of methanotrophic mussels at a Louisiana cold seep. Progress in Oceanography, v. 24, p. 15-24

Malone, T.C., 1991. River flow, phytoplankton production and oxygen depletion in Chesapeake Bay. In: Tyson, R.V. and T.H. Pearson (eds.), Modem and Ancient Continentintal Shelf Anoxia.Geological Society special publication no. 58. London: The Geological Society, p. 83-93

,1992. Effects of water column processes on dissolved oxygen, nutrients, phytoplankton and zooplankton. In: Smith, D.E., Leffler, M., and Makieman, G. (eds.), Oxygen dynamics in Chesapeake Bay: A synthesis of recent research. College Park, MD: Maryland Sea Grant College Program, p. 61-112

Milliaman, J. D., and Meade, R., 1983. World-wide delivery of river sediment to ocean. Journal of Geoloy, v. 91, p. 1-21

McCorkle, D.C., Corliss, and B. H., Famham, C., 1997. Vertical distribution and isotopic compositions of live (stained) benthic Foraminifera from the North Carolina and California continental margins. Deep-Sea Research, v. 44, pp. 983-1024

279

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. McCorkle, D. C., Keigwin, L. D., Corliss, B. H., and Emerson, S. R., 1990. The influence of microhabitats on the carbon isotopic composition of deep-sea benthic Foraminifera. Paleoceanography, v. 5, p. 161-185

McGee-Russell, S.M., 1974. Dynamic activities and labile microtubutles in cytoplasmic transport in the marine foraminiferan Allogromia. Symposium of the Society for Experimental Biology, v. 28, p. 157-189

Miller, K. G. and Lohmann, G. P. 1982. Environmental distribution of Recent benthic Foraminifera on the northeast United States continental slope. Geological Society of America Bulletin, v. 93, pp. 200-206

Moodley, L, and Hess, C., 1992. Tolerance of infaunal benthic Foraminifera for low and high oxygen concentrations. Biological Bulletin, v. 183, p. 94-98

, Schaub, B. E. M., Van Der Zwaan, G. J., and Herman, P. M. J., 1998b. Tolerance of benthic Foraminifera (Protista: Sarcodina) to hydrogen sulphide. Marine Ecology Progress Series, v. 169, p. 77-86

, van der Zwaan, G. J., J. Herman, P. M., Kempers, L., and van Bruegel, P., 1997. Differential response o f benthic meiofauna to anoxia with special reference to Foraminifera (Protista: Sarcodina). Mar. Ecol. Prog. Ser., 158, p. 151-163

, van der Zwaan, G. J., Rutten, M. W., Boom, R. C. E., and Kempers, L., 1998a, Subsurface activity of benthic Foraminifera in relation to porewater oxygen content: laboratory experiments. Marine Micropaleontology, 34, p. 91-106

Moore, W. E., 1957. Ecology of recent Foraminifera in the northern Florida Keys. American Association of Petroleum Geologists Bulletin, v. 41. pp. 727-741

Montagna, P. A., and Spies, R. B., 1985. Meiofauna and chlorophyll associated with Beggiatoa mats of a natural submarine petroleum seep. Marine Environmental Research, v. 16, p. 231-242

Morrison, J. M., and Nowlin, W.D., 1977. Repeated nutrient, oxygen, and density sections through the Loop Current Journal of Marine Research, v. 35, p. 105-128

Murray, G. E., 1961. Geology of the Atlantic and Gulf Coastal Province of North America. Harper and Brothers, New York, 692 p.

Murray, J. W., 1971. Living foraminiferids of tidal marshes, A review. Journal of Foraminiferal Research, v .l, p. 153-161

Murrell, M. C., and Fleeger, J. W., 1989. Meiofauna abundance on the Gulf of Mexico continental shelf affected by hypoxia. Continental Shelf Research, v. 9, no. 12, p.1049-1062

280

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Nelsen, T. A., Blackwelder, T. H., McKee, B., Romer, N., and Metz, S., 1994. Time- based correlation of biogenic, lithogenic and authigenic sediment components with anthropogenic inputs in the Gulf of Mexico NECOP Study Area. Estuaries, v. 17, no. 4, p. 873-885

Nelson, D. C., Revsbech, N. P., and Jorgensen, B. B., 1986. Microoxic-anoxic niche of Beggiatoa spp.: Microelectrode survey of marine and freshwater strains. Applied and Environmental Microbiology, v. 52, p. 161-168

Officer, C.B., Biggs, R.B., Taft, J.L., Cronin, L.E., Tyler, M., and Boynton, W.R., 1984. Chesapeake Bay anoxia: Origin, development, and significance. Science, v. 223, p. 22-27

Parker, F. L., 1952. Foraminiferal distribution in the Long Island Sound - Buzzards Bay area. Bulletin Museum Comparative Zoology, Harvard College, v. 106, no. 10, p. 428-473

, 1954. Distribution of the Foraminifera in northeastern Gulf of Mexico. Bulletin Museum Comparative Zoology, Harvard College, v. 111, p. 453-588

Pauli, C. K, Martens, C. S., Chanton, J. P., Neumann, A. C., Coston, J., Jull, A. J. T., and Toolin, L. J., 1989. Old carbon in living organisms and young CaC 0 3 cements from abyssal brine seeps. Nature, v. 342, p. 166-168

, Usseler, W., HI, and Dillon, W. P., 1991. Is the extent of glaciation limited by marine gas hydrates? Geophysical Research Letters, v. 18, p. 432-434

Perez-Cruz, L. L., and Machain-Castillo, M. L., 1990. Benthic Foraminifera of oxygen minimum zone, continental shelf of the Gulf of Tehuantepec, Mexico. Journal of Foraminiferal Research, v. 20, p. 312-325

Phleger, F. B., 1951. Ecology of Foraminifera Northwest Gulf of Mexico, part I. Geological Society of America Memoir, v. 46, p. 1-88

, 1954. Ecology of Foraminifera and associated microorganisms from Mississippi Sound and environs. American Association of Petroleum Geologists Bulletin, v. 38. p. 584-647

, 1955. Ecology of Foraminifera in southeastern Mississippi Delta area. American Association of Petroleum Geologists Bulletin, v. 39, p. 712-752

, 1960. Ecology and Distribution of Recent Foraminifera. Johns Hopkins Press, Baltimore, 297 p.

, and Parker F. L., 1951. Ecology of Foraminifera Northwest Gulf of Mexico, part II. Geological Society of America Memoir, v. 46. p. 1-88

281

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , and Soutar, A., 1973. Production of benthic Foraminifera in three east Pacific oxygen minima. Micropaleontology, v. 19, p. 110-15

Platon, E., and Sen Gupta, B. K., in press. Foraminiferal communities of oxygen-stressed environments on the Louisiana continental shelf. In: Rabalais, N. N. and Turner, R. E. (eds.), Coastal Hypoxia: Consequences for Living Resources and Ecosystems. Coastal and Estuarine Studies 58, American Geophysical Union, Washington, D.C.

Platon, E., Sen Gupta, B. K., Turner, R. E., and Overton, E. B., 1997. Influence of the Mississippi River plume on the distribution of modem benthic Foraminifera on the Louisiana continental shelf. Geological Society of America, 1997 Annual Meeting, Abstracts with Programs, p. A95.

Poag, C. W., 1978. Paired foraminiferal ecophenotypes in Gulf Coast estuaries: ecological and paleoecological implications. Gulf Coast Association of Geological Societies Transactions, v. 28, p. 395-421

, 1981a. Living foraminifers of West Flower Garden Bank, northernmost coral reef in the Gulf of Mexico. Micropaleontology, v. 27, no. 1, p. 31-70

, 1981b. Ecologic atlas of benhtic Foraminifera of the Gulf of Mexico, Marine Science International, Hutchinson Ross Publishing Company, Woods Hole, Massachusetts, 174 p.

, 1984. Distribution and ecology of deep-water benthic Foraminifera in the Gulf of Mexico. Palaeogeogeography, Palaeoclimatology, Palaeoecology, v. 48, p. 25-37

, and Sweet, W. E. Jr., 1972. Claypile Bank, Texas continental shelf. In: Rezak, R., and Henry, V. J. (eds.), Contributions on the Geological and Geophysical Oceanography of the Gulf of Mexico, Texas A&M University Oceanography Series, v. 3, p. 223-261

Rabalais N. N., and, Harper, Jr., D. E., 1992. Studies of benthic biota in areas affected by moderate and severe hypoxia, p. 150-153 In: Nutrient Enhanced Coastal Ocean Productivity, proceedings of a Workshop, Louisiana Universities Marine Consortium, October 1991, Publ. No. TAMU-SG-91 -109, Texas A&M University Sea Grant College program, College Station, Texas.

, Turner, R. E., Justic, D., Dortch, Q., Wiesman, W. J. Jr., and Sen Gupta, B. K., 1996. Nutrient changes in the Mississippi River and system responses on the adjacent continental shelf. Estuaries, v. 19, p. 386-407

, Turner, R. E., Justic, D., Dortch, Q., Wiseman, W. J. Jr.. and Sen Gupta, B. K., 2000. Gulf of Mexico biological responses to nutrient changes in the Mississippi

282

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. River. In: Hobbie, John, E. (ed.), Estuarine Synthesis. A Synthetic Approach to Research and Practice, Island Press, Washington, p. 241-268

, Turner R. E., and Wiseman, W. J. Jr., 1999. Hypoxia in the northern Gulf of Mexico: Linkages with the Mississippi River. Pages 297-322 in H. Kumpf, K. Steidinger and K. Sherman (eds.), The Gulf of Mexico Large Marine Ecosystem, Assessment, Sustainability, and Management, Blackwell Science, Malden, Massachusetts, 697 p.

, Turner, R. E., Wiseman, W. J Jr., and Boesch, D. F., 1991. A brief summary of hypoxia on the northern Gulf of Mexico continental shelf: 1985-1988, in: Tyson, R. V., and Pearson, T. H. (eds.), Modem and ancient continental shelf anoxia: Geological Society of London, special Publication, no. 58. p. 35-46

, Wiseman, W. J. Jr., and Turner, R. E., 1994. Comparison of continuous records of near-bottom dissolved oxygen from the hypoxia zone along the Louisiana coast Estuaries, v. 17. p. 850-861

Rathbum, A. E. and Corliss, B. H., 1994. The ecology of living (stained) deep-sea Foraminifera from Sulu Sea. Paleoceanography, v. 9 (1) p. 87-159

, Corliss, B. H., Tappa, K. D., and Lohmann, K. C., 1996. Comparisons of the ecology and stable isotopic compositions of living (stained) benthic Foraminifera from the Sulu and South China Seas. Deep-Sea Research, v. 43, p. 1617-1646

, Levin, L. A., Held, Z., and Lohmann, K.C., 2000. Benthic foraminifera associated with cold methane seeps on the northern California margin: Ecology and stable isotopic composition. Marine Micropaleontology, v. 38, pp.247-266

Roberts, H. H., and Aharon, P., 1994. Hydrocarbon-derived carbonate buildups of the northern Gulf of Mexico continental slope: A review of submersible investigations. Geo-Marine Letters, v. 14, p. 135-148.

, Aharon, P., and Walsh, M. M., 1992 a. Cold-seep carbonates of the Louisiana continental slope to basin floor. In Rezak R. and Lavoie D. (eds.), Carbonate Microfabrics. Spring-Verlang, Berlin, p. 95-104.

, and Camey, R. S., 1997. Evidence of episodic fluid, gas, and sediment venting on northern Gulf of Mexico continental slope. Economic Geology, v. 92, p. 863-879

, Cook, D. J., and Sheedlo, M. K., 1992 b. Hydrocarbon seeps of the Louisiana continental slope: seismic amplitude signature and sea floor response. Gulf Coast Association of Geological Societies Transactions, v. 42, p. 349-362

Riley, G. A., 1956. Oceanography of Long Island Sound, 1952-1954. Bulletin of the Bingham Oceanographic Collections, v. 15, p. 15-46

283

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Riley, G. A., 1959. Oceanography of Long Island Sound, 1954-1955. Bulletin of the Bingham Oceanographic Collections, v. 17, p. 9-29

Sassen, R., Roberts, H. H., Aharon, P., Larkin, J., Chinn, E. W., and Carney, R., 1993. Chemosynthetic bacterial mats at cold hydrocarbon seeps, Gulf of Mexico continental slope. Organic Geochemistry, v. 20, p. 77-89

Schafer, C. T., 1973. Distribution of Foraminifera near pollution sources in Chaleur Bay. Water, Air, and Soil Pollution, v. 2, p. 219-233

Seigiie, G. A., 1968. Foraminiferal assemblages as indicators of high organic carbon content in sediments and of polluted waters. American Association of Petroleum Geologists Bulletin, v. 52, no 11, p. 2231-2241

, G. A., 1971. A preliminary note on the relationships between foraminifers and pollution in two Puerto Rican bays, Caribbean Journal of Science, v. 11 no. 1-2, p p .93-98

, G. A., 1975. Foraminifera of Guyanilla Bay and their use as environmental indicators. Revista Espagnola de Micopalaleontologia, v. 7, p. 453-587

Seliger, H. H., and Boggs, J. A., 1988. Long-term pattern of anoxia in the Chesapeake Bay. In: Lynch, M. P., and Krome, E. C. (eds.), Understanding the estuary: advances in Chesapeake Bay research, p. 570-83. Chesapeake Research Consortium Publication 129, Solomons, Maryland.

, Boggs, J. A., and Biggley, W. H., 1985. Catastrophic anoxia in Chesapeake Bay in 1984. Science, v. 228, p. 70-73

Sen Gupta, B. K., 1999. Systematics of modem Foraminifera. In: Sen Gupta, B. K. (ed.), Modem Foraminifera, Kluwer Academic, Dordrecht, p. 7-36

, and Aharon, P., 1994. Benthic Foraminifera of bathyal hydrocarbon vents of the Gulf of Mexico: Initial report on communities and stable isotopes. Geo-Marine Letters, v. 14, p. 88-96.

, and Kilboume, R. T., 1974. Depth distribution of benthic Foraminifera on the Georgia continental shelf. In: Schafer, C. T., and Pelletier, B. R. (eds.), First International Symposium on Benthic Foraminifera of Continental Margins, Part A: Ecology and Biology, Maritime Sediments, Special Publication no. 1, p. 25-38

, and Machain-Castillo, M. L., 1993. Benthic Foraminifera in oxygen-poor habitats. Marine Micropaleontology, v. 20, p. 83-201

, Platon, E., Bernhard, J. M, and Aharon, P., 1997. Foraminiferal colonization of hydrocarbon-seep bacterial mats and underlying sediment, Gulf of Mexico. Journal of Foraminiferal Research, v. 27, no. 4, p. 292-300

284

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , Turner, R. E., and Rabalais, N. N., 1996. Seasonal oxygen depletion in continental shelf waters of Louisiana: Historical record of benthic foraminifers. Geology, v. 24 p. 227-230

Severin, K. P. and Erskian, M. G., 1981. Laboratory experiments on the vertical movements of Quirtqueloculina impressa Reuss through sand. Journal of Foraminiferal Research, v. 11, p. 133-136

Shackleton, N. J., 1977, Carbon-13 in Uvigerina: Tropical rainforest history and the equatorial Pacific carbonate dissolution cycles, In: Andersen, N. R., and Malahoff, A. (eds.): The Fate of Fossil Fuel CO 2 in the Oceans: Plenum Press, New York, p. 401-427

Shifflett, E., 1961. Living, dead and total foraminiferal faunas, Heald Bank, Gulf of Mexico. Micropaleontology, v. 7, no. I, p. 45-54

Sklar, F. H. and Turner, R. E., 1981. Characteristics of phytoplankton production off Barataraia Bay in an area influenced by Mississippi River. Contributions in Marine Science, v. 24, p. 93-106

Spencer, R. S., 1992. Quantified intraspecific variation of common benthic Foraminifera from the Northwest Gulf of Mexico: a potential paleobathymetric indicator. Journal of Foraminiferal Research, v. 22, no. 3, p. 274-292

Spies, R. B., and Davis, P. H., 1979. The infaunal benthos of a natural oil seep in the Santa Barbara Channel. Marine Biology, v. 50, p. 227-237

Swanson, R.L., and Sindermann, C.J., 1979. Oxygen depletion and associated benthic mortalities in New York Bight, 1976. NOAA Professional Paper no. 11, Washington, DC: NOAA. 345 p.

Thomas, E., Gapotchenko, T., Varekamp, J. C., Mecray, E. L., and Buchholz Ten Brink, M. R., 2000. Benthic Foraminifera and Environmental Changes in Long Island Sound. Journal of Coastal Research v. 16, p. 641-655

Tunnicliffe, V., 1992. Hydrothermal-vent communities of the deep sea. American Scientist, v. 80, p. 336-349

Turner, R. E. and Allen, R. L., 1982. Planktonic respiration rates in the bottom waters of the Mississippi River Delta Bight. Contributions in Marine science, v. 25, p. 109- 120

, and Rabalais, N. N, 1991. Changes in Mississippi River water quality this century. Implications for coastal food webs. BioScience, v. 41, p. 140-147

285

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. , and Rabalais, N. N., 1994. Coastal eutrophication near Mississippi river delta. Nature v. 368, p. 619-621

Uchupi, E, 1975. Physiography of the Gulf of Mexico and Caribbean Sea. In: Naim, A. E. M. and Stehli, F. G. (eds.), The Ocean Basins and Margins, v. 3, The Gulf of Mexico and the Caribbean, Plenum Press, New York, p. 1-64

van der Zwaan, G. J., 1983. Paleoecology of the Late Miocene Mediterranean foraminifera. Utrecht Micropaleontological Buletins, v. 25., p. 1-202

, G. J., Jorissen, F. J., Verhallen, P. J. J. M, and Von Daniels, C. H., 1986. Uvigerina from the eastern Atlantic, North Sea basin, Paratethys and Mediterranean. In: van der Zwaan, G. J., Jorissen, F. J., Verhallen, P. J. J. M and Von Daniels, C. H. (eds.), Atlantic-European Oligocene to Recent Uvigerina. Utrecht Micropaleontological Bulletins, v. 35, p. 7-20

, G. J., and Jorissen, F. J., 1991. Biofacial patterns in river-induced shelf hypoxia. In: Tyson, R. V., and Pearson, T. H. (editors), Modem and Ancient Continental Shelf Anoxia. Geol. Soc. Spec. Pub., 58, p. 65-82

Verhallen, P. J. J. M., 1997. Epistominella tricarinata , a new species from sapropelitic layers in the Upper Pliocene of Italy. In: Proceedings Koninklijke Nederlandse Akademie van Wetenschappen, series B. v. 90, p. 307-313

Venec-Peyre, M.-T., 1981. Les foraminif&res et la pollution: gtude de la microfaune de la Cale du Dourduff (embrochure de la rivigre de Morlaix). Cahiers de Biologie Marine, v. 22, p. 25-33

Walton, W. R., 1964. Recent foramininferal ecology and paleocology. In: Imbrie, J., and Newell, N. (eds.), Approaches to paleontology, John Wiley and sons, Inc., pp. 151-237

Watkins, J.,G., 1961. Foraminiferal ecology around Orange County, California, ocean outfall. Micropaleontology, v. 7, p. 199-206

Wefer, G., Heinze, P.-M., Berger, W. M., 1994. Clues to ancient methane release. Nature v. 369, p. 282

Welsh, B. L. and Eller, F. C., 1991. Mechanisms controlling summertime oxygen depletion in western Long Island Sound. Estuaries, v. 3, p. 265-268

Wiseman, Jr., W. J., Bierman, Jr. V.J., Rabalais, N. N., Turner, R. E., 1992. Physical structure of theLouisiana shelf hypoxic region, pp. 21-26 in Nutrient Enhanced Coastal Ocean Productivity. Publ. no. TAMU-SG-92-109, Texas Sea Grant College Program, Galveston, Texas.

286

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Whitcomb N., 1977. Effects of oil pollution on selected species of benthic Foraminifera. Unpublished Master’s Thesis, Duke University.

Yanko, V., Kronfeld, J., and Flexer A., 1994. Response of benthic foraminifera to various pollution sources: Implication for pollution monitoring. Journal of Foraminiferal Research, v. 24, p. 1-17

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Cushman Foundation for Foraminiferal Research MRC-121 Department o f Paleobiology. National Museum o f Natmal History, Ufcafcngtnn. DC 20560-0121 Phone (202) 357-1390 iatfJ/atAConrnt nhi cda Fax (202) 7*6-2*32

January 23,2001

Emil Platon Energy & Geoscience Instiyute University of Utah Research Park 423 Wakara Way, Suite 300 Salt Lake City. Utah 84108-1242

Dear Mr. Platon.

Thank you very much for your request for permission to use the article "Foraminiferal colonization of hydrocarbon-seep bacterial mats and underlying sediment. Gulf of Mexico slope". B. K. ScnGupta. E. Platon. J. M. Bernhard and P. Aharon. 1997. Journal of Foraminiferal Research, v. 27 no. 4. You are welcome to use the material, providing it is properly cited in the publication.

We would be grateful if you would send an reprint of the paper, when it is published, for our library.

Jennifer A.'Jett Secretary/Treasurer Cushman Foundation for Foraminiferal Research [email protected]

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Emil Platon:

We are pleased to grant peonW oa ibe the use of tbs materiii requested fee inclusion in your thesis, mchriing microfilm editions thereof:

I h ^ B M Biiiiiftn l PnmimiiiM in Otygen TVpteed Enuimmnants of tha Lmneime P u ittiBHHf l Shelf* nP CES 58; Coastal Hypoxia: Consequences for Living Resources and Ecosystems, Naacy N. Rabalais sad R. Eugene Tamer

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Emil Platon, the second son of loan and Maria Platon, was bom on April 26,

1958, in Oradea, Romania. He graduated from loan Neculce High School in Bucharest,

Romania, in June 1979. He passed the admission exam for entering the college at the

University of Bucharest in July 1979. After the mandatory military service, Emil Platon

began working on his college degree at the University of Bucharest, in October 1980,

where he meet his future wife, Roxana Florescu, whom he married in October 1984. He

was awarded the highest scholarship at that time in Romania, Bursa Republicans, in

1984. He graduated from the University of Bucharest in June 1985, with a “Diploma”

degree in geological and geophysical engineering. Between 1985 and 1994, Emil Platon

worked with the Enterprise for Drilling and Special Mining Works (1985-1987) and the

Geological Institute of Romania (1987-1994). He also worked as an academic visitor

with the University College London in the spring of 1992. Emil Platon was admitted as a

graduate student at Louisiana State University, Department of Geology and Geophysics

in 1994 and began working on a doctoral degree in the fall semester of that year. In 1997

he received the Cushman Foundation Student Award in recognition for his scientific

work. He was admitted in a master’s program in the Department of Computer Science

also at LSU in 1997 and graduated from that department in the summer o f2000. Emil

defended his dissertation on December 1st, 2000 and is currently finalizing the editorial

work on his dissertation.

2 9 0

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Candidates Emil Platon

M&jor Field: Geology

Title of Dissertation: Benthic Foraminifera in Two Stressed Environments of the Northern Gulf of Mexico

Approved:

Majpm.Professor add Chairman

EXAMINING COMMITTEE:

/ /

Date of Kraminations

I; 3-frrt>

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