Pelagic Food Web Connectivity in the North Pacific

PELAGIC FOOD WEB CONNECTIVITY IN THE NORTH PACIFIC

SUBTROPICAL GYRE: A COMBINED PERSPECTIVE FROM

MULTIPLE BIOCHEMICAL TRACERS AND DIET

A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI`I AT MĀNOA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY

OCEANOGRAPHY

DECEMBER 2013

C. Anela Choy

Dissertation Committee: Jeffrey C. Drazen, Chairperson Brian N. Popp Jeffrey J. Polovina Erica Goetze Gregory E. Ravizza, Outside member

Keywords: micronekton, pelagic fishes, stable isotopes, mercury, amino acid compound specific isotope analysis, mesopelagic, stomach content analysis, Hawaii longline fishery

ii ABSTRACT

Long-term shifts in the abundances of open ocean fishes have been observed over the period of 1996-2011 in the North Pacific Subtropical Gyre (NPSG). Fishery data indicate that large, high trophic position fishes such as tunas, billfishes, and sharks, have been decreasing in relative abundance, while smaller, mid-trophic position fishes such as alepisaurids and gempylids have been increasing. Some of these species are of great commercial importance, and recent calls for ecosystem-based fishery management require accurate characterization of predator-prey relationships supporting biomass production at the top of the food web. The broad goal of this study was to elucidate pelagic food web structure within the NPSG, focusing on the links formed by understudied mid-trophic level animals (micronekton and their predators), and how energy is transferred through feeding interactions between these animals inhabiting different vertical habitats. Four distinct but complementary approaches were employed: stomach content analysis, bulk stable isotope analysis, compound-specific nitrogen isotope analysis of individual amino acids (AA-CSIA), and total mercury concentrations.

Stomach content analysis revealed that pelagic fish species that have been increasing in abundance have distinct diets relative to adult tuna and billfishes. Unique components of the micronekton community were exploited by alepisaurids, gempylids, and lamprids, including hyperiid amphipods, the little-known cephalopod Walvisteuthis youngorum, and mesopelagic fishes (Anoplogaster cornuta, Sternoptyx spp.), and the polychaete Vanadis nans. Despite shared vertical habitat and unique diets, AA-CSIA indicated that both groups of fishes have similar trophic positions. Thus, shifts in

ix abundances could be the result of predation release since tunas and billfishes feed upon

smaller size classes of alepisaurids and gempylids.

Biochemical metrics of trophic position (bulk tissue δ15N values, total mercury

concentrations, and AA-CSIA data) were strongly related to animal size for diverse food

web components ranging from zooplankton to micronekton to large pelagic fishes.

Distinct increases in the δ15N values of glycine, serine, and phenylalanine were observed with micronekton fish depth of capture, suggesting a separation in food resources across epipelagic, mesopelagic, and upper bathypelagic habitats. Broadly, this study established that the pelagic food web of the NPSG is structured by size-based interactions and the influence of vertical habitat.

x TABLE OF CONTENTS

ACKNOWLEDGMENTS ...... V ABSTRACT ...... IX LIST OF TABLES ...... XIV LIST OF FIGURES ...... XV CHAPTER 1 - INTRODUCTION AND RESEARCH RATIONALE ...... 1 1.1. INTRODUCTION...... 1 1.2. UTILITY OF BIOCHEMICAL MARKERS IN ECOSYSTEM STUDIES ...... 5 1.3. RESEARCH OBJECTIVES AND STRUCTURE ...... 8 1.4. REFERENCES ...... 11 CHAPTER 2 - THE DIETS OF FIVE IMPORTANT PREDATORY MESOPELAGIC FISHES OF THE CENTRAL NORTH PACIFIC ...... 18 2.1. ABSTRACT ...... 18 2.2. INTRODUCTION...... 19 2.3. MATERIALS AND METHODS ...... 22 2.3.A. SAMPLE COLLECTION AND PROCESSING ...... 22 2.3.B. HARD PARTS ...... 25 2.3.C. DATA ANALYSIS ...... 25 2.4. RESULTS ...... 27 2.4.A. GENERAL DIET COMPOSITION ...... 27 2.4.B. CEPHALOPOD PREY DIFFERENCES ...... 29 2.4.C. PREY FUNCTIONAL GROUPS & DEPTH DIFFERENCES ...... 31 2.4.D. SIZE-BASED INTRASPECIFIC DIET COMPARISONS ...... 32 2.4.E. INTERSPECIFIC DIET COMPARISONS ...... 33 2.5. DISCUSSION ...... 33 2.5.A. DIETS OF BIG-EYE OPAH AND SMALL-EYE OPAH ...... 33 2.5.B. DIET OF SNAKE MACKEREL ...... 35 2.5.C. DIET OF LANCETFISH ...... 37 2.5.D. ECOLOGICAL NICHE PARTITIONING AMONGST PELAGIC PREDATORS ...... 39 2.6. ACKNOWLEDGMENTS ...... 43 2.7. LITERATURE CITED ...... 44 CHAPTER 3 - PLASTIC FOR DINNER? OBSERVATIONS OF FREQUENT DEBRIS INGESTION BY LARGE PREDATORY FISHES FROM THE CENTRAL NORTH PACIFIC ...... 68 3.1. ABSTRACT ...... 68 3.2. INTRODUCTION...... 69 3.3. MATERIALS AND METHODS ...... 70 3.4. RESULTS ...... 73 3.5. DISCUSSION ...... 74 3.6. ACKNOWLEDGMENTS ...... 80 3.7. LITERATURE CITED ...... 80

xi CHAPTER 4 - GLOBAL TROPHIC POSITION COMPARISON OF TWO DOMINANT MESOPELAGIC FISH FAMILIES (MYCTOPHIDAE, STOMIIDAE) USING AMINO ACID NITROGEN ISOTOPIC ANALYSES ...... 91 4.1. ABSTRACT ...... 91 4.2. INTRODUCTION...... 92 4.3. MATERIALS AND METHODS ...... 95 4.3.A. SAMPLE COLLECTION AND PREPARATION ...... 95 4.3.B. BULK TISSUE STABLE ISOTOPE ANALYSIS ...... 96 4.3.C. TPS FROM BULK STABLE N ISOTOPE DATA ...... 96 4.3.D. STABLE N ISOTOPE ANALYSIS OF INDIVIDUAL AAS ...... 97 4.3.E. TPS FROM CSIA DATA ...... 98 4.4. RESULTS ...... 98 4.4.A. BULK TISSUE ISOTOPIC ANALYSES ...... 98 4.4.B. STABLE N ISOTOPE ANALYSIS OF AMINO ACIDS & TP ESTIMATES ...... 99 4.5. DISCUSSION ...... 100 4.6. ACKNOWLEDGMENTS ...... 104 4.7. REFERENCES ...... 104 CHAPTER 5 - CHANGES IN PELAGIC FISH TROPHIC STRUCTURE WITH DEPTH IN THE NORTH PACIFIC SUBTROPICAL GYRE ECOSYSTEM ...... 120 5.1. ABSTRACT ...... 120 5.2. INTRODUCTION...... 121 5.3. MATERIALS & METHODS ...... 125 5.3.A. SAMPLE COLLECTION ...... 125 5.3.B. LABORATORY ANALYSIS ...... 127 5.3.C. TROPHIC POSITION DESIGNATIONS ...... 129 5.3.D. DATA ANALYSIS ...... 131 5.4. RESULTS ...... 132 5.4.A. BULK TISSUE δ15N AND δ13C VALUES ...... 132 5.4.B. AMINO ACID δ15N VALUES ...... 133 5.4.C. TROPHIC POSITIONS ESTIMATED FROM AA-CSIA ...... 134 5.4.D. BROAD GROUPINGS AND DEPTH-RELATED PATTERNS ...... 135 5.4.E. SIZE-BASED DIFFERENCES ...... 138 5.5. DISCUSSION ...... 139 5.5.A. ISOTOPIC VARIABILITY WITH DEPTH ...... 139 5.5.B. TROPHIC STRUCTURE OF THE PELAGIC FISH ASSEMBLAGE ...... 144 5.5.C. ECOLOGICAL NICHE PARTITIONING WITHIN THE PELAGIC FISH ASSEMBLAGE . 146 5.6. ACKNOWLEDGMENTS ...... 149 5.7. REFERENCES ...... 150 CHAPTER 6 - MERCURY DISTRIBUTIONS IN THE PELAGIC FOOD WEB ECOSYSTEM OF THE NORTH PACIFIC SUBTROPICAL GYRE ...... 168 6.1. ABSTRACT ...... 168 6.2. INTRODUCTION...... 169 6.3. MATERIALS & METHODS ...... 171 6.3.A. SAMPLE COLLECTION ...... 171

xii 6.3.B. TOTAL MERCURY & METHYLMERCURY ANALYSES ...... 172 6.3.C. STABLE ISOTOPE ANALYSIS ...... 173 6.3.D. DATA ANALYSIS ...... 173 6.4. RESULTS & DISCUSSION...... 174 6.4.A. TOTAL MERCURY CONCENTRATIONS IN LARGE PELAGIC FISHES ...... 174 6.4.B. TOTAL MERCURY CONCENTRATIONS IN MICRONEKTON AND ZOOPLANKTON 175 6.4.C. MONOMETHYLMERCURY CONCENTRATIONS ...... 176 6.4.D. BIOMAGNIFICATION OF MERCURY IN THE PELAGIC FOOD WEB ...... 177 6.4.E. INFLUENCES OF HABITAT DEPTH AND FEEDING ...... 178 6.5. ACKNOWLEDGMENTS ...... 181 6.6. REFERENCES ...... 182 CHAPTER 7 - CONCLUSIONS AND FUTURE DIRECTIONS ...... 199 7.1. RESEARCH SYNTHESIS ...... 200 7.2. FUTURE RESEARCH ...... 207 7.3. REFERENCES ...... 210

xiii