University of Florida Thesis Or Dissertation Formatting

BIOLOGY OF THE GREEN TURTLE CHELONIA MYDAS IN THE GALÁPAGOS ISLANDS

PATRICIA M. ZARATE

A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA

2013 1

To my children and my mother

ACKNOWLEDGMENTS

Although I am listed as the sole author of this dissertation, the research presented here and my graduate career have been dependent upon the help and guidance of many people.

My supervisor, Karen Bjorndal, invested much time and effort in my academic career. Although I am grateful for all the things she has done for me and all her support,

I am most indebted to her for the sound training she has provided me in the areas of research and writing and for the trust she put in me during my tenure. My gratitude also goes to Alan Bolten for his invaluable help, advice and guidance during all of the years of my graduate career.

I am also grateful to the other members of my graduate committee: Alan Bolten,

Peter Dutton, Franklin Percival, Jeffrey Seminoff and Brian Silliman. They have all provided me with solid suggestions and advice, and their comments helped to greatly improve and strengthen the final version of this dissertation.

My fellow students, Joe Pfaller, Hanna Vander Zanden, Mariela Pajuelo, Melania

Lopez, Luciano Soares and Robert Johnson, have been valued peers. I am grateful for their time and effort invested in my talks and for their valuable comments on some of the chapters in this dissertation. I am especially grateful to Joe, for the constant motivation and encouragement and the helpful advice and suggestions he gave me each day.

I would like to thank the people from the Department: Karen Patterson, Susan

Spaulding and Tangelyn Mitchell who provided me with assistance on a daily basis, and who were always attentive and ready to answer or explain the numerous questions. To

Ken Albergotti and Boyd Westerman, for always providing quick technical assistance 4

with my countless computer issues during these 5 years. I would also like to thank Peter

Eliazar, for always greeting me with a big smile, with a willingness to help me with what

I needed and for all the helpful advice and suggestions on my research.

I am forever indebted to those people outside of the University of Florida who have helped this project come to fruition. Two people deserve special recognition, and I give my eternal gratitude to Peter Dutton and Jeffrey Seminoff, from NOAA-NMFS, who introduced me to the amazing world of sea turtles thirteen years ago. They provided me with training, knowledge and financial support, but above all, they became colleagues and friends over the years. We shared unforgettable trips around the Galápagos

Islands, long nights of walking on nesting beaches tagging turtles, and many great experiences that have made me a better professional and a better person.

Other sea turtle people I have met along the way who have had a strong influence on my attitude and work in sea turtle conservation include Peter Pritchard,

George Balazs, Derek Green, Mario Hurtado, Neca Marcovaldi, Jeane Mortimer,

Alberto Abreu, Bryan Wallace, Joanna Alfaro, Nelly de Paz, Alexander Gaos, Ingrid

Yañez, Mike Frick, Didiher Chacon, and Alejandro Falabrino. I would also like to thank

Elpidio M. López from the National Mexican Turtle Center in Oaxaca, Mexico, for his insights on beetle predation.

All my love and thanks to my family and friends who helped me through this challenging journey. A special thank you to my amazing daughter and son, Mariantú and Cristóbal, who always gave me words of support, encouragement, and believed in me and joined me in many field trips sharing my passion for wildlife and nature. To my mom, Yolanda, and my sister, Verónica, for always being there for me with their

patience and support, giving me strength and confidence, even from the distance. All my love and a million thank you’s to my Mom Barbara and my sisters, Marie, Tric,

Barby, Karen and Kathy, who have always been so proud of my achievements and never ever had a single doubt I could do this. They have all been there for me. To my friends, René Durandeau, Javier Robayo, Mariana Vera, Macarena Parra, Nicole

Botteri, Mariela Pajuelo, Catalina Pimiento, Bernardo Cardenas, Camila Pizano, Marisol

Quiroz, Joanna Alfaro, Claudia Escobar and Nelly de Paz, who never let me quit or give up, even when the road looked so bumpy and unpleasant to walk on. I do not know how

I could have done this without my family and friends by my side.

My dear friend and colleague, Boyd Lyon, who now rests in peace, is hugely responsible for my decision to enter into the graduate program. I can still remember that day on the beach when we were looking at the basking turtles. He was trying so hard to convince me that graduate school was a great idea, even when we were “a little old”. I will never forget you my dear friend, you have been in my heart and mind during this journey. Every time I felt this was more than I could handle, I thought of our talk at the beach and how your life was taken prematurely, without you fulfilling your dreams.

Boyd, my friend, you were an inspiration to me in life and now in spirit.

Thanks to my cousins, Drs. Rodrigo Bustamante and Ramiro Bustamante. They inspired me and brought me into the biological sciences when I was still very young. I used to listen to them talk about biology and science from a distance with a great interest, but it took many years until they invited me to join their conversation. When I was younger, I wished that I could be like them when I “grew up”. Now, I feel that I am a little closer to this goal.

To Robert Bensted-Smith, Graham Watkins, and Bryan Milstead, my former bosses in the Charles Darwin Foundation. I thank you for helping me become a better professional. You gave me the opportunity to grow my wings and fly. The trust you had in me gave me the confidence to keep reaching higher.

I would also like to give my full gratitude to my research and field assistants,

Macarena Parra, Edison Cadena, Carmen Chasiluisa, Italo Bravo, Agustina Fernie, Nel

Beaumont, Sonia Castillo, Javier Carrión, Mariantu Robles, Flor Gomez, Diego Paez,

Cecilia Angulo, Sigita Cahoon, Edissa palacios, Maria Gonzalez, Manuela Borja,

Zackary Smith and Andres Panezo. You all gave your heart and soul to this project and shared a passion for sea turtles with me. A special recognition to Macarena Parra who has always been there with thoughtful comments and piercing analyses. She has assisted in all aspects of the work we have done together, from fieldwork in nesting and foraging areas to writing papers. She has been supportive of my graduate career, even at the expense of her own work and time.

All my gratitude to all volunteers who were in the field: international, national

(Ecuadorian) and local (Galápagos) students, young professionals, naturalist and diving guides, fishermen, park officers and people from the community who spent long time on the beach, or were part of my team during trips to foraging areas. This research was possible because you dedicated your time and were passionate for sea turtles and the environment. You were the backbone of this project!

I want to thank all the people who helped with collection, identification and transportation of my samples, which were highly valuable to validate this dissertation.

Thanks to Gustavo Jiménez and Macarena Parra, from the Charles Darwin Foundation

(CDF), for taking the time to collect mangrove samples. I thank Patricia Jaramillo for the identification of plant material, and Edissa Palacios and Javier Carrión for algae identification and to Lynn Fowler for sample transport. Thanks to Henri Herrera and

Anamaria Ortega from CDF for rearing flies and to Bradley Sinclair of the Zoologisches

Forschungs institute und Museum Alexander Koenig in Germany for identifying adult flies, I also give my thanks. Thank you to Garret Lemmons (NOOA-NMFS) and Jason

Curtis (University of Florida) for assistance with stable isotope analysis.

I owe my gratitude to all captains, marineros and pangueros in Galápagos who helped not only with transportation to field sites but also for the hard work and friendliness that made every trip a more enjoyable one. My special recognition to

Captain Bernardo Rodriguez and Fausto Lara, to Jorge Suarez, “Cuarto”, Julio Delgado and Roberto Pépolas and the crews of El Beagle, Tiburon Martillo, Guadalupe, Atlántida and Golondrina II. I also want to express my gratitude to the tourism sector and numerous vessels and their crews who provided transportation and food for me and all the volunteers travelling to and from field sites. They provided oases in the middle of the desert for all of us who spent days or months in the field. Special thanks go to my dear friend Eduardo Swinburg and his crew from El Pelicano for invaluable support of this project since its conception. I also thank the Ecuadorian Air Force personnel from Baltra

Airport, for helping with the logistics and the transportation of volunteers to and from camping sites.

Financial assistance for this research was provided by the National Marine

Fisheries Service (NMFS, USA), Conservación Internacional (CI, Ecuador), Ecology

Project International (EPI, USA), National Fish and Wildlife Foundation (NFWF, USA),

Lindblad National Geographic Fund, Galápagos Conservation Trust, Turner Foundation,

Swiss Friends of Galápagos, GAP Adventures, Laboratorio Epidemiología y Patología

Fabricio Valverde (GNP and University of Guayaquil), Charles Darwin Foundation

Canada, United Nation Foundation (UNF), Ocean Foundation (Boyd Lyon Fellowship),

Captain Planet Foundation, Association for Women in Science (Satter Award, AWIS),

Fellowship Grant (UF), GAP Adventures (Planeterra Foundation) and Lerner-Gray Fund for Marine Research.

I would like to express my appreciation to the Galápagos National Park (GNP), particularly to Wacho Tapia for not only providing research permits for this investigation and the collection of samples, but also for his valuable comments. Thanks to the GNP personnel in Isabela, Oscar Carvajal and the park officers who helped with logistics to and from Isabela field sites. Thank you to Drs. Marylin Cruz, Virna Cedeño, and their team from Fabricio Valverde’s lab for their support and collaboration.

Many people from the CDF helped me along the way. Many thanks to administration, finance, logistics, quarantine and inspection, sciences, volunteer and comisariato areas and their staff at the Charles Darwin Foundation for their invaluable support and assistance with logistic, supplies, paperwork, permits, and volunteers.

TABLE OF CONTENTS

page

ACKNOWLEDGMENTS ...... 4

LIST OF TABLES ...... 13

LIST OF FIGURES ...... 14

LIST OF ABBREVIATIONS ...... 16

ABSTRACT ...... 17

CHAPTER

1 SEA TURTLES AND ISLANDS ...... 19

Ecology of Sea Turtles at Oceanic and Continental Islands ...... 19 Sea Turtle Nesting Biology ...... 20 Migratory Patterns and Foraging Ecology ...... 21 Biology of Sea Turtles at Foraging Grounds ...... 21 Approach in this Dissertation ...... 22

2 OFFSHORE OASIS: ECOLOGY OF SEA TURTLES AT OCEANIC ISLANDS OF THE EASTERN PACIFIC ...... 25

Introduction ...... 25 Oceanic Islands and Archipelagos in the Eastern Pacific ...... 25 Galápagos Archipelago, Ecuador ...... 26 Sea turtle research prior to 2000 ...... 27 Recent monitoring work ...... 29 Oceanic Islands Systems ...... 32 Revillagigedos Archipelago, Mexico ...... 32 Clipperton Island, France ...... 33 Cocos Island, Costa Rica ...... 35 Easter Island, Chile ...... 37 Island Systems on the Continental Shelf ...... 37 Tres Marías Islands, México ...... 37 Coiba Island, Panamá ...... 38 Malpelo Island, Colombia ...... 38 Gorgona Island, Colombia ...... 39 Challenges and Advances in Island Conservation: a Case Study of the Galápagos Archipelago ...... 40 Coastal Zonation Scheme Implementation ...... 42 Longlining Banned within the Galápagos Marine Reserve ...... 42 Quarantine and Inspection System and Eradication Programs Implemented... 43

International Conservation Efforts for Island Systems in the EP ...... 45

3 HATCHING AND EMERGENCE SUCCESS OF GREEN TURTLE (Chelonia mydas) NESTS IN THE GALÁPAGOS ISLANDS ...... 49

Introduction ...... 49 Material and Methods ...... 51 Study sites ...... 51 Data collection ...... 52 Statistical Analyses ...... 55 Results ...... 56 Discussion ...... 60 Variation in Hatching Success and Comparisons with other Sea Turtle Populations ...... 60 Unknown Sources of Mortality ...... 64 Management Actions and Recommendations ...... 66

4 UNDERSTANDING MIGRATORY PATTERNS AND FORAGING ECOLOGY OF GREEN TURTLES Chelonia mydas IN THE GALÁPAGOS ISLANDS THROUGH STABLE ISOTOPES ...... 87

Introduction ...... 87 Materials and Methods...... 90 Study Sites ...... 90 Sample Collection and Analyses ...... 91 Results ...... 93 Discussion ...... 96 Isotopic Characterization of Galápagos Turtles on Foraging Grounds ...... 96 Isotopic Characterization of Galápagos Turtles on Nesting Beaches ...... 98 Distinguishing between Resident and Migrant Nesting Females ...... 101

5 GROWTH OF GREEN TURTLES AND HAWKSBILLS IN THE GALÁPAGOS ISLANDS ...... 117

Introduction ...... 117 Materials and Methods...... 118 Study sites ...... 118 Analyses ...... 120 Results ...... 121 Discussion ...... 123 Effect of Body Size on Growth Rates ...... 124 Temporal and Spatial Variation in Growth Rates ...... 126 Effect of Morph on Growth Rates ...... 127 Comparisons with Other Green Turtle Populations ...... 127 Growth Rates for Hawksbill Turtles in Galápagos ...... 128

6 CONCLUSIONS AND FURTHER RESEARCH ...... 140

Island Ecology and Sea Turtles ...... 140 Threats to Incubating Embryos ...... 141 Understanding Migratory Patterns and Foraging Ecology through Stable Isotopes ...... 142 Somatic Growth Rates of Sea Turtles ...... 144 Directions for Future Research ...... 146 Nest Survival ...... 146 Nesting Trends and Reproductive Output ...... 147

LIST OF REFERENCES ...... 149

BIOGRAPHICAL SKETCH ...... 172

LIST OF TABLES

Table page

3-1 Hatching and emergence success from natural nests of green turtles ...... 69

3-2 Physical features of nesting beaches in the Galápagos Islands...... 76

3-3 Hatching success in Galápagos green turtles. Summary of binomial general additive regression analysis with fixed effects...... 77

3-4 Variables measured for female green turtles and nests from 2004 through 2007...... 78

3-5 Mean hatching and emergence success of green turtle nests by year and beach at four nesting beaches during years 2004 through 2007...... 79

3-6 Percentages of nests affected by each source of mortality, and percentages of successful nests by beach and season in the Galápagos Islands...... 80

3-7 Percentages of embryos in each nest assigned to each source of mortality by beach and year in the Galápagos Islands...... 81

3-8 Percentages of nests and eggs affected by fungus by beach and year in the Galápagos Islands...... 82

4-1 Mean values and standard deviation values for 13C, 15N, CCL (cm) for green turtles Chelonia mydas by year and site collected at foraging and nesting grounds in the Galápagos Islands...... 103

4-2 Isotopic values of 13C and 15N of algae and mangrove specimens collected at Bahía Elizabeth in 2004...... 104

4-3 Recapture data for 10 female green turtles tagged in the Galápagos Islands between 2002 -2005 and recaptured within Galápagos waters to date...... 105

4-4 Recapture data for 45 turtles tagged in the Galápagos Islands between 1970 -2012 and recaptured outside of Galápagos waters to date...... 106

5-1 Summaries of three general additive regression models ...... 130

5-2 Growth rates (cm/yr) for 10 cm size classes of green turtles from the Galápagos Islands...... 132

5-3 Growth rates (cm/yr) for 10-cm carapace length size classes of green turtles from other foraging grounds...... 133

5-4 Growth rates (kg/yr) for 10 kg mass classes of green turtles from Galápagos. 134

LIST OF FIGURES

Figure page

2-1 Location of the islands in the eastern Pacific Ocean included in this chapter. .... 47

2-2 Yellow morph of Chelonia mydas captured at Galápagos foraging grounds...... 48

3-1 Map of the Galápagos Islands showing green turtle nesting beaches used in this study...... 83

3-2 Graphical summary of GAM analysis of hatching success covariates...... 84

3-3 Hatching and emergence success for the 1039 nests examined in this study at key nesting beaches from 2003-2007 in the Galápagos Islands...... 85

3-4 The relation of day of oviposition and percentage of embryos killed in individual nests by the three mortality factors that changed across the season . 86

4-1 Map of 3 foraging grounds and 4 nesting beaches where green turtles were sampled...... 109

4-2 Isotopic values of 13C and 15N of individual green turtles at foraging grounds in the Galápagos Islands ...... 110

4-3 Stable isotope mean and individual values for green turtles (not corrected for trophic discrimination) and mean isotope values for potential prey at Bahía Elizabeth...... 111

4-4 Values of 13C and 15N of individual green turtle nesting females at nesting grounds of the Galápagos Islands...... 112

4-5 Mean 13C and 15N values for green turtles from foraging grounds and females from nesting beaches of the Galápagos Archipelago...... 113

4-6 Convex polygons representing 13C and 15N values of individual green turtles on nesting and foraging grounds in Galápagos...... 114

4-7 Mean 13C and 15N values for green turtles from all Galápagos nesting grounds and local foraging grounds and, from foraging areas in the eastern Pacific Ocean...... 115

4-8 Convex polygons representing 13C and 15N values of individual green turtles on Galápagos nesting and foraging areas and individual foraging areas in the eastern Pacific Ocean...... 116

5-1 Location of the foraging-ground study sites for sea turtles in the Galápagos Marine Reserve...... 135

5-2 Size class distribution of black and yellow morph from four study sites in the Galápagos Marine Reserve...... 136

5-3 Graphical summaries of general additive regression analyses of straight carapace length (SCL) growth covariates for black and yellow turtles combined...... 137

5-4 Graphical summaries of general additive regression analyses of straight carapace length (SCL) growth covariates for black turtles only ...... 138

5-5 Graphical summaries of general additive regression analyses of mass growth covariates for black and yellow turtles...... 139

LIST OF ABBREVIATIONS

ANOVA Analysis of variance

BB Bahía Barahona

BE Bahía Elizabeth

CCL Curve carapace length

CCW Curve carapace width

CD Caleta Derek

CI Cocos Island

FGs Foraging grounds

GAM Generalized additive model

GD Golfo Dulce

GI Gorgona Island

GPS Global Position System

HWM High water mark

LB Las Bachas

LS Las Salinas

NGs Nesting grounds

PAR Paracas

PE Punta Espinoza

POC Oceanic waters off Perú

PN Punta Núñez

QP Quinta Playa

SCL Straight carapace length

SD Standard deviation

Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy

BIOLOGY OF THE GREEN TURTLE CHELONIA MYDAS IN THE GALÁPAGOS ISLANDS

Patricia M. Zárate

December 2013

Chair: Karen A. Bjorndal Major: Zoology

I present here an investigation of several aspects of the biology of the green turtle Chelonia mydas in the Galápagos Islands. The Galápagos Archipelago is one of the most important rookeries for green turtles in the eastern Pacific Ocean, but it also provides important foraging grounds for the species. Therefore, I had an excellent opportunity to conduct research on different developmental stages and habitats of green turtles.

First, I examined sea turtle natural history around the oceanic and continental islands in the eastern Pacific Ocean. I found that sea turtle populations inhabiting these islands are impacted by human induced threats, particularly by invasive species and fisheries interactions. Next, I examined hatching and emergence success of green turtle nests in the Archipelago. I found relatively low values of hatching and emergence success compared to those of other green turtle populations in the world, due to the combination of predation by beetles, feral pigs, and nest destruction by nesting females.

I examined foraging ecology and migratory patterns of green turtles within and among foraging and nesting grounds through the use of stable isotope analysis. I found substantial variation in 13C and 15N values of sea turtle skin within each foraging

ground; the data suggested that green turtles in Galápagos are not exclusively herbivorous. I tested whether stable isotope analysis could be used to discriminate between resident and migrant females in Galápagos. However, I found no distinctive groups within the nesting aggregation that could be interpreted as representing different foraging strategies.

I also evaluated growth rates of green turtles and hawksbills captured at foraging grounds in Galápagos. I confirmed that growth rates of green turtles in Galápagos are the slowest ever reported for green turtles anywhere in the world. Growth rates in

Galápagos are significantly different for the two morphs, and significantly affected by body size, and foraging site.

Together, this research has improved our knowledge of the green turtle in the

Galápagos Islands by focusing on aspects of their biology at different developmental stages and on critical habitats. The information provided here will help managers of the

Galápagos National Park to effectively protect and conserve sea turtles and their habitats.

CHAPTER 1 SEA TURTLES AND ISLANDS

Ecology of Sea Turtles at Oceanic and Continental Islands

Islands are oases of marine life and terrestrial biodiversity, and their isolation has resulted in unique flora and fauna, and in the distant past, more limited anthropogenic threats were present compared to mainland areas. Thus, it should be no surprise that sea turtles are attracted to these characteristics of marine areas around islands. These remote natural systems have evolved a unique and delicate balance that often differs greatly from those on the closest mainland, and thus are particularly sensitive to impacts (Rolett & Diamond 2004).

Most island environments are characterized by significant detrimental human impact, beginning with initial colonization by humans (Mairs 2007). A common theme for island systems are introduced species (Mulungoy et al. 2006), including plants, but also vertebrates, such as pigs, dogs, livestock, and rodents that can have from mild to very severe impacts on the sea turtle rookeries and on islands ecosystem in general

(Nogales et al. 2004, Campbell & Donlan 2005, Cruz et al. 2005, Howald et al. 2007,

Parkes & Panetta 2009). Native and endemic species that have evolved without contact with these new organisms are often unable to compete or defend themselves. Species invasions have contributed to the extinction of many species on islands (Sax et al.

2002). Anthropogenic impacts also affect the marine environment with direct effects on sea turtle populations, particularly from artisanal and industrial fishing fleets. Fisheries interactions with sea turtles and other marine organisms are a widespread problem around island systems in the Pacific Ocean (Aylesworth 2009).

Sea Turtle Nesting Biology

Sea turtles like most marine organisms spend most of their lives in the ocean and emerge only for a fraction of time on available beaches to lay their eggs (Miller 1997). In spite of their limited time spent in the terrestrial habitats, turtles on beaches provide a good opportunity to examine different aspects of their nesting biology and, most studies of sea turtle biology and ecology have been conducted on nesting beaches. Studies of sea turtle population dynamics have been possible in some species from long term monitoring studies on nesting females (e.g., Bjorndal et al. 1999, Balazs & Chaloupka

2004a). These long term series of data on nesting beaches have revealed dangerous declines and encouraging trends in different sea turtle species (e.g., Reina et al. 2002,

Troëng et al. 2004).

Determining hatching and emergence success of sea turtle nests also provides fundamental information for the conservation and management of sea turtles. These data are essential because they help to understand how suitable a beach is as an incubating environment for sea turtle eggs. Hatching and emergence success can also provide information on the demographic stability of the population (Miller 1997).

The interactions of numerous abiotic and biotic factors experienced by sea turtle embryos during incubation can influence hatching and emergence success values.

Embryonic development can be affected by changes in the nest conditions due to temperature (Matsuzawa et al. 2002, Segura & Cajade 2010), moisture (Ackerman

1980, Mortimer 1982), sand structure and composition (Mortimer 1990), and salinity

(Ackerman 1980). Nest location and its microhabitat or surrounding environment

(Whitmore & Dutton 1985, Bjorndal & Bolten 1992, Hays & Speakman 1993), as well as sand compaction by human activity (Kudo et al. 2003) and predation (Stancyk 1982) 20

can affect hatching and emergence success of sea turtle nests. Hatching success also varies among species and populations of sea turtles (Hirth 1980, Van Buskirk &

Crowder 1994).

Migratory Patterns and Foraging Ecology

Migratory patterns can include turtles that are resident and show strong fidelity to a specific foraging area, while other turtles temporarily visit a series of areas during their development before finally settling in a specific area. As mature adults, females migrate periodically between breeding and foraging grounds during breeding seasons (Miller

1997), in some cases travelling several thousand kilometers (Limpus et al. 2002,

Benson et al. 2011). Migration distance between the foraging and the breeding grounds can affect reproductive output, as measured by parameters including remigration intervals, number of clutches per breeding season and eggs per clutch (Bjorndal 1982,

Troëng & Chaloupka 2007, Zbinden et al. 2010, Hawkes et al. 2011).

Green turtle nesting aggregations are comprised of individuals from multiple foraging locations (Harrison & Bjorndal 2006), and the ability to identify these locations is challenging, but it is a fundamental component of effective management and conservation. Because sea turtles migrate long distances through habitats under the authority of multiple countries at various times throughout their life, international efforts are required for an effective protection.

Biology of Sea Turtles at Foraging Grounds

Foraging grounds play an important part in the sea turtle life cycle. After hatchlings hatch and emerge from nests and make it safely to the sea, they swim to oceanic habitats via major ocean currents, and begin a period termed the “lost years”

(Carr 1987) before recruiting to neritic foraging areas. Green turtles undergo

ontogenetic shifts when moving to neritic areas, often initiating drastic dietary changes

(Bjorndal 1997).

Developmental habitats are important for the survival of juvenile marine turtles

(Bjorndal et al. 2003) and the quality of the foraging habitats play a critical role in determining the optimal body condition required for successful reproduction (Tiwari &

Bjorndal 2000, Broderick et al. 2001a). Each of the habitats where sea turtles grow and develop has different environmental parameters, such as food availability and temperature that will influence growth rates of sea turtles.

Knowledge of somatic growth rates of sea turtles is critical for our understanding of habitat quality and demography of these endangered species. Green turtle growth rates may be affected by a combination of factors including diet, habitat quality, rate of ingestion, season, genetic and physiological factors, water temperature, and density- dependent effects (Boulon & Frazer 1990, Collazo et al. 1992, Bjorndal et al. 2000,

Balazs & Chaloupka 2004b, Chaloupka et al. 2004). Despite the great importance of growth rate dynamics, we know little about the growth and time to maturity of green turtles in the eastern Pacific.

Approach in this Dissertation

The focus of my research has been to enhance our understanding of the biology of green turtles by analyzing different developmental stages and critical habitats in an island system – the Galápagos Islands – that corresponds to one of the most important rookeries for the species in the eastern Pacific Ocean (Seminoff 2004).

In Chapter 2, I focused on sea turtle natural history around the oceanic and continental islands in the eastern Pacific Ocean. I identified threats to sea turtle populations and conservation efforts with emphasis on the Galápagos. I concentrate on 22

the Galápagos because of their global recognition and the history of conservation in this region, which has provided relatively safe haven for green turtles and other sea turtle species, as well as countless other flora and fauna species. Although information from other islands in the region is relatively scarce, I found they provide other examples of ocean oases, where sea turtles thrive in relatively pristine marine habitats and nesting beaches.

In Chapter 3, I determined hatching and emergence success of green turtle

(Chelonia mydas) nests on four key beaches in the Galápagos Islands and identified the factors that influence these values by the use of binomial generalized additive models

(GAM) with fixed effects. I analyzed causes of variation and compared hatching and emergence success of green turtles in the Galápagos with those of other green turtle populations around the world.

In Chapter 4, I collected skin samples from green turtles at four nesting beaches and three foraging grounds to evaluate migratory patterns and foraging ecology through the use of stable isotope analysis. I compared 13C and 15N values of green turtles from foraging grounds to potential prey items to establish dietary composition and trophic level of turtles at foraging and nesting grounds in the Galápagos. I also compared my results with stable isotope values available in the literature for green turtles in other eastern Pacific foraging areas to determine whether we could identify individual green turtles nesting in the Galápagos as either residents or migrants.

In Chapter 5, I examined the growth rate of green turtles at four different foraging grounds and assessed factors influencing growth rates for two different morphs of green turtles encountered in the Galápagos by the use of generalized additive models. I

compared my results with earlier studies and with growth reported for green turtles in other regions. Additionally, I provided information on growth rates for hawksbill turtles at one foraging ground in the islands. This represents the first information on growth rates of hawksbills turtles for the eastern Pacific Ocean.

In the final chapter (Chapter 6), I review how this work provides new insights into sea turtle biology in the eastern Pacific, and how future research efforts might be directed to help our understanding of the ecology of this endangered species.

CHAPTER 2* OFFSHORE OASIS: ECOLOGY OF SEA TURTLES AT OCEANIC ISLANDS OF THE EASTERN PACIFIC

Introduction

Oceanic Islands and Archipelagos in the Eastern Pacific

The Galápagos Archipelago is certainly the most famous island group in the eastern Pacific Ocean (hereafter EP), but other island formations in the region share similar traits. These small islands surrounded by vast oceans are oases for marine as well as terrestrial biodiversity. Ocean currents -- carrying nutrients, oxygen, heat and other ingredients necessary to create marine food webs -- swirl around and run into these islands, creating concentrated areas of high productivity that support abundant marine life. Large aggregations of whales, hammerhead sharks, seabirds, and other migratory fauna bear testimony to the special conditions offered by these islands, many of which enjoy some form of national or international recognition as protected areas or

UNESCO World Heritage Sites. Anthropogenic threats to marine ecosystems tend to be limited compared to threats occurring closer to mainland areas due to the islands’ relative isolation. This isolation has resulted in unique animal and plant life on these islands. As Charles Darwin learned during his voyage on the HMS Beagle, oceanic islands act as “nature’s laboratories,” where animals and plants are separated from their mainland source populations, subject to natural processes in relatively isolated settings.

They are also highly susceptible to threats alien to their native environments. Several islands in the region are home to penal colonies or military installations.

*Chapter 2 has been published in a slightly modified form: Zárate P. 2012. Offshore oasis. Ecology of sea turtles at oceanic islands of the eastern Pacific. Pp. 64-87. In: Seminoff. J.A. and B.P. Wallace (eds). Sea turtles of the eastern Pacific: advances in research and conservation. The University of Arizona Press. Tucson. ISBN 978-0-8165-1158-7. xxiii, 376 pp. Reprinted here with permission.

Other oceanic islands in the EP include Revillagigedos, Guadalupe, and Rocas

Alijos Islands (Mexico), Clipperton Island (overseas holding of France), Cocos Island

(Costa Rica), and Easter Island (Chile) (Fig. 2-1). Several other islands, located not in the open ocean but on the continental shelf, function similarly to their oceanic counterparts as important habitats for unique flora and fauna; among these are Islas

Tres Marías (México), Coiba Island (Panamá), Malpelo Island and Gorgona Island

(Colombia), and Easter Island (Chile). Like the Galápagos, all of these sites host sea turtles, and although information from these areas is relatively scarce, they provide other examples of ocean oases, where sea turtles thrive in relatively pristine marine habitats and nesting beaches. Given the preponderance of information available from the Galápagos as compared to other island formations in the EP, this chapter focuses on current knowledge of sea turtle natural history and recent conservation efforts in the

Galápagos Archipelago, but also recognizes these other oceanic and continental islands and their local sea turtle populations.

Galápagos Archipelago, Ecuador

The oceanographic conditions surrounding the Galápagos Archipelago – located along the equator roughly 1000 km west of mainland Ecuador – have created extreme biogeographic isolation and the greatest level of vertebrate endemism in the entire EP.

The Galápagos Archipelago, volcanic in origin, comprises 13 major islands (total area >

10 km2), 5 of a medium size (area between 1 – 10 km2), and 215 islets (<1 km2)

(Parque Nacional Galápagos 2006). Because of its uniqueness and incredible beauty, the Galápagos Archipelago was a declared Biosphere Reserve (1984) and a World

Heritage Site (1978; 2001). Its breathtaking Marine Reserve is considered one of the top sites in the world for diving (Sammon 1992, Scuba Diving Magazine 2010). 26

Sea turtle research prior to 2000

The Galápagos Islands have been the primary island system for sea turtle research in the eastern Tropical Pacific, as several ‘generations’ of researchers have studied both nesting and foraging areas in the archipelago. The first scientific endeavour was the Joseph R. Slevin Expedition (California Academy’s Scientific

Expedition in 1905 – 1906), during which biologists sacrificed numerous green turtles, taking flipper measurements and recording stomach contents (Fritz 1981). However, it was not until 1970 that focused research targeting green turtles commenced, initially with Peter Pritchard’s exploratory surveys along the coasts of most islands to determine the extent of green turtle nesting in the archipelago (Pritchard 1971, 1972), and later with a flipper tagging program performed by Pritchard, Miguel Cifuentes, and Judy

Webb to study green turtle nesting in the islands.

During the nearly seven decades of research inactivity between these expeditions, sea turtles were harvested as a food source by sailors and island inhabitants. In fact, some of the only accounts we have of sea turtles in the Galápagos during this period come from a canning operation on the islands which relied on local green turtles, and from sailors passing through the area that landed green turtles for food (Hoff 1985). By the 1970s, commercial exploitation of sea turtles was common because they were abundant, large (over 130 kg), and easy to obtain (Pritchard 1971).

However, Japanese longline fishermen had been operating in the islands for almost a decade, and their activity increased in the beginning of the 1970s, including exploitation of sea turtles. Turtles were caught by local fishermen and frozen onboard the Japanese vessels (Lundh 2004). The last official report of commercial exploitation of sea turtles at

Galápagos Islands occurred in 1971 and 1972, when the Japanese vessel “Chikuzen 27

Marou” caught 2,000 to 3,000 turtles, most of which were adult female green turtles, but also included juveniles and adult males (Green 1978, Lundh 2004).

Historically as well as today, green turtles Chelonia mydas are the only sea turtle species that nests in the Galápagos, and is by far the most common, occurring in great abundance in the marine habitats of virtually every island in the archipelago (Fig. 2-1).

The Galápagos nesting population is one of two major rookeries for the species in the

EP region totalling more than 1,000 nesting females per year, the other being Playa

Colola, Michoacán, México (Seminoff 2004, Delgado-Trejo & Álvarado-Díaz 2012).

Although green turtles in the EP are depleted relative to past levels due to the aforementioned human consumption of eggs and meat, numbers in recent years have been stable and perhaps increasing (Seminoff 2004).

The first exhaustive nesting beach and foraging habitat assessments in the

Galápagos was performed by Derek Green from 1975 to 1980. During that time, Green tagged over 2,300 green turtles and a few hawkbills at foraging areas, and tagged over

4,000 turtles at nesting sites. This research resulted in a seminal paper describing the long-distance migrations of green turtles tagged on Galápagos beaches recaptured in

Central and South America, from Costa Rica to Perú, demonstrating an important linkage between the Galápagos and the rest of the region (Green 1984a). Another influential paper described the growth of green turtles in foraging areas – growth so slow that Green suggested some turtles might take up to 50 years to reach maturity

(Green 1993).

Green also reported an interesting dichotomy among green turtles at Galápagos foraging grounds that had been mentioned first by Joseph R. Slevin during his

expedition (Slevin 1931) and later by Archie Carr (Carr 1967): the presence of a dark morph of turtle that nested and foraged locally, as well as a lighter morph known as the

“yellow turtle,” which was present in feeding areas but was never seen nesting. In addition to differences in coloration, these researchers described the relatively underdeveloped reproductive organs of yellow males and females compared to those of darker morph turtles of a similar size. In addition, the yellow turtle was fattier, yielding six to eight times more oil than the dark turtle. Green suggested that only 1% of green turtles in the Galápagos were of the yellow morph, which recent findings have confirmed

(see below).

For several years during Green’s tenure on the islands, he often worked closely with Mario Hurtado, an Ecuadorian scientist who continued investigating the reproductive activity of green turtles (Hurtado 1984). These studies yielded an estimate of 1,400 females nesting annually from 1970 to 1983 and a total of nearly 9,000 females tagged on Galápagos beaches during those years (Hurtado 1984). It was during these efforts, helped in part by Pritchard’s earlier studies, that beaches of Quinta Playa and

Bahía Barahona on southern Isabela, Las Salinas on Baltra, Las Bachas on northern

Santa Cruz, and Espumilla on Santiago were recognized as the most important nesting sites in the archipelago (Green 1994). However, 1983 marked the last year of this research, and not until 2000 did nesting beaches again become the focus of scientific investigation.

Recent monitoring work

Today, the conservation status of the green turtle nesting population in the

Galápagos is positive, and the annual number of nesting females stable. Although feral animals such as cats, dogs and pigs, exist on some beaches, their numbers are 29

controlled by Galápagos National Park Guard’s exotic species eradication program (see below). After successfully monitoring 8 years of nesting activity at key sites beginning in

2001, more than 10,000 females have been tagged.

In addition to the nesting beach work, there also has been considerable research effort in foraging areas throughout the Archipelago. In February 2003, an expedition was launched to revisit the same sites that Green had assessed during his five years of research to provide a comparison between past and present. A research team consisting of Peter Dutton and Jeffrey Seminoff from NOAA, the author, and several very enthusiastic local and international volunteers set off on an 8-day trip to the western side of the Archipelago.

The team boarded a CDRS research vessel boat called The Beagle and travelled to Green’s exact research sites, which probably had not been visited by humans for at least a decade. While approaching the first stop at Punta Espinoza, green turtles were observed mating along the shoreline of the nesting beaches. At most of the sites visited, green turtles were in great abundance – some of them feeding on green algae (Ulva sp.), others resting on the bottom of lagoons or shallow ponds, or basking on sea surface – making them very easy to capture by hand. However, the most exciting event was encountering the first “yellow turtle” documented since Green’s time. A juvenile of

47.4 cm in length, it had a brightly colored carapace with white, orange and brown streaks radiating from bright orange spots at the centers of each scute. The head was black with bright orange borders on facial scutes, the flippers were black with a narrow orange band along the outer and inner margins, and the plastron was uniformly light yellow (Fig. 2-2; Zárate 2007). Of nearly 1,000 individuals of Chelonia mydas tagged at

foraging grounds in Galápagos Archipelago from 2003 to 2007, 10% have been of the yellow morph. While it appears that they originate from green turtle rookeries in the

Indo-Pacific (Dutton & Zárate, unpubl. data), their biology, behavior, and life cycle all remain mysteries.

Green turtles nesting in the Galápagos Archipelago may represent a distinct genetic stock (Dutton & Zárate, unpubl. data), but whether turtles belonging to this stock mix with turtles from other nesting stocks at foraging areas was unknown until recently.

Seminoff et al. (2008) tracked the post-nesting movements of 12 adult female green turtles within and away from the Galápagos Islands. The researchers identified multiple post-nesting behavior patterns, including occupancy of oceanic habitats in the southeastern Pacific, long-distance migration to neritic habitats in Central America, and residential movements of some individuals that did not leave the Archipelago. Thus, just as the Galápagos receives juvenile green turtles from multiple stocks, Galápagos nesting turtles appear to share multiple habitats with turtles from other nesting stocks.

Besides green turtles, hawksbills, Eretmochelys imbricata, olive ridleys,

Lepidochelys olivacea, and leatherbacks, Dermochelys coriacea also have been recorded occasionally in the Galápagos Islands. Six hawksbills were captured among the nearly 1,000 green (and yellow) turtles in marine habitats from 2003 to 2007. Olive ridleys were reported several times in the past and captured by Slevin’s team in 1906

(Slevin 1931), and others have been reported as victims of boat strikes and bycatch in artisanal longline gear (Murillo et al. 2004). Leatherbacks were recorded three times from 1970 to 1983 (Green 1994) and once in 2003 when an individual was incidentally captured in an artisanal longline (Murillo et al. 2004). Satellite telemetry research has

demonstrated that leatherbacks migrate through and around the Galápagos Archipelago en route between nesting beaches in Mexico and Costa Rica to feeding areas in the southeastern Pacific (Eckert & Sarti 1997, Shillinger et al. 2008, Bailey et al. 2012).

The global recognition and history of strong conservation programs make the

Galápagos Archipelago a relative safe-haven for abundant green turtles and other sea turtle species, as well as countless other flora and fauna species. Although anthropogenic threats to sea turtles persist and still require conservation action (see below), the Galápagos will continue to provide a home for sea turtles in the foreseeable future.

Oceanic Islands Systems

Revillagigedos Archipelago, Mexico

The Revillagigedos Islands are located 400 nautical miles southwest of the southern tip of Baja California, Mexico (Everett 1988). This oceanic archipelago encompasses a total area of 157.81 km² including four volcanic islands: San

Benedicto, Socorro, Roca Partida y Clarión (see regional Map). Socorro and Clarión both host stations of the Mexican Navy, with a population of 250 (staff and families) in the south of Socorro and a small garrison with approximately 10 men on Clarión

(Brattstrom 1982, Awbrey et al. 1984, Everett 1988). However, other than this low- density military presence, the islands are uninhabited by humans. Thus, the islands host several endemic vertebrate and plant species, important seabird rookeries and other marine megafauna. Furthering the protection of the wildlife in Revillagigedos, the

Mexican Government established the islands as a Biosphere Reserve on the 1994.

As in the Galápagos, the green turtle is the only marine turtle species that nests in Revillagigedos, with relatively sparse nesting on Clarión and Socorro Islands 32

(Brattstrom 1982, Awbrey et al. 1984; Fig. 2-1). On Clarion Island, Sulphur Beach along the southern coast is the most important nesting site for green turtles, accounting for about 70% of nesting at Revillagigedos (Awbrey et al. 1984, Everett 1988). Nesting occurs year-round but increases seasonally from July to March, with peak nesting in

October and November (Juárez et al. 2003). An average of 86 nests was deposited on

Sulphur Beach during nesting seasons from 1999 to 2001.

Hawksbills, olive ridleys and leatherbacks are also reportedly found in coastal waters of the Revillagigedos Islands, but the only scientific survey information available is from research by Arturo Juárez, Laura Sarti, and colleagues (Juárez et al. 2003), who most frequently observed green turtles at sea around Socorro and Clarion Islands.

Green turtles captured along the coasts of the islands were predominantly adults ranging in curved carapace length from 80.0 - 108.8 cm.

As with Galápagos and other island systems, natural systems in the

Revillagigedos have been impacted by introduced animals, such as sheep, cats, and pigs, which have caused declines in marine and terrestrial bird populations. It is unclear whether these invasive animals have impacted sea turtles, but known threats to sea turtles in waters around the Revillagigedos are predation by sharks and illegal fisheries.

Clipperton Island, France

Clipperton Island also known as Ile de la Passion is located in the eastern Pacific

Ocean at 510 nautical miles southeast of Socorro Island in the Revillagigedo

Archipelago (Mexico) (Fig. 2-1). It is the only atoll of the North East Pacific and its basement forms a seamount rising above the sea floor at 3000 m (Glynn et al. 1996,

Jost & Andrefouet 2006). Volcanic remnant is comprised by an isolated and

conspicuous 29 meter-high rock, other than that peak the highest elevation above sea level is 4 m (Jost & Andrefouet 2006, Lorverlec et al. 2009).

The ring-shaped atoll is of approximately 9 km² and completely encloses a freshwater lagoon that was connected by two channels to the open ocean. However, but because of a hurricane sometime between 1839 and 188, the lagoon was isolated from the ocean and became a brackish system (Sachet 1960, Lorvelec & Pascal 2006,

Lorvelec et al. 2009).

From the 1890s until the 1910s human settlement took place on the island for mining activities. At that time, coconut trees and pigs were introduced and have had an evident impact on the island ecosystem. Reports from those days mentioned that the island was totally deserted with no vegetation cover, along with a huge abundance of crabs (Jost & Andrefouet 2006). The island is currently uninhabited but sporadically visited by crews of fishing boats and tourists. The flora and fauna in the Clipperton atoll has been characterized as low diversity (Jost & Andrefouet 2006).

The only record of sea turtles nesting on Clipperton Island comes from the notes of Benjamin Morrell (Morrel 1832) in which he mentions that green turtles come to the island to lay their eggs. However, there is no indication where he saw the turtles actually nesting or found evidence such as tracks from nesting activities or eggshells or eggs on the beach. The presence of nesting activity based on Morrell’s comments and the species identification as well has been questioned because of a lack of description

(Lorvelec & Pascal 2006). If nesting was effectively occurring at the time of Morrel’s observation it is possible that predation of eggs and adult turtles by humans between

1893 and 1917 or the destruction of nests by the high abundance of pigs on the island

during the first half of the XX century have caused the disappearance of the sea turtle population on Clipperton’s Island (Lorvelec & Pascal 2006). Inventories carried out on the island record sea turtles (Cheloniidae) as native species that have disappeared from the island that were first described on August of 1825, and with no further confirmation of reproduction on the island after that date (Lorvelec & Pascal 2009).

Lorvelec et al. (2009) visited the island on the 2004 and recorded the presence of stranded turtles at different sites along the shoreline of the island. Of the nine carcasses they found five corresponded to Lepidochelys olivacea and in the remaining four species identification was not possible because the cadavers were too decomposed or were reduced to just bones. The death of these strandings was certainly attributed to longline fisheries and to purse seine tuna fishermen to a lesser extent.

The origin of these strandings has been speculative and based on the distribution of nesting grounds in the region (Brown & Brown 1982, Fritts et al. 1982, López - Castro

1999, Alava et al. 2007, Eguchi et al. 2007) and on the current information on migration undertaken by olive ridleys in the region (Parker et al. 2003) the strandings found on

Clipperton Island could come from any of the nesting population within the region

(Lorvelec et al. 2009).

Cocos Island, Costa Rica

Cocos Island is an oceanic island of both volcanic and tectonic origin located approximately 340 nautical miles from mainland Costa Rica (Fig. 2-1). It is surrounded by deep waters and rich ocean currents that attract iconic aggregations of hammerhead sharks, rays, dolphins and other large marine species – as well as SCUBA divers. It is the only oceanic island in the eastern Pacific region topped by dense tropical forests

and their characteristic flora and fauna (Sinergia 69 2000). The island was never linked to a continent, so the island is home to a high proportion of endemic species.

No information in peer-reviewed literature exists to date on sea turtles at Cocos

Island. Sightings of sea turtles were first documented during XVIII and XIX centuries (M.

Montoya, personal communication), and over the past 20 years, divers visiting the island have documented (in photographs and videos) the presence of hawksbills turtles, greens, olive ridleys and leatherbacks. Sightings of sea turtles at sea are frequent around the island, but no records of nesting exist.

In recent years, the Programa Restauración de las Tortugas Marinas

(PRETOMA) has led research expeditions to capture and track sea turtles and sharks around Cocos Islands. To date, satellite transmitters have been deployed on five green turtles and one hawksbill turtle, and movement patterns have demonstrated individual variability, with some turtles staying close to the Island and one making a long distance migration toward mainland Panama before the transmitter ceased to function (R. Arauz, pers. comm.).

Cocos Island was declared a National Park by Executive Decree in 1978, and later was designated a World Heritage Site by UNESCO in 1997. In addition, Cocos is home to a "Wetland of International Importance" as defined by the RAMSAR

Convention. The only persons allowed to live on Cocos Island are Costa Rican Park

Rangers. Tourists are allowed ashore only with permission of island rangers, and are not permitted to camp, stay overnight or collect any flora, fauna or minerals from the island (Montoya 2007). Threats to Cocos ecosystems include invasive rodents (Ratus ratus and Mus musculus) and feral pigs (Sus scrofa), as well as illegal fishing.

Easter Island, Chile

Easter Island, or Rapa Nui in the island people’s indigenous language, is a

Polynesian island of volcanic origin and one of the world's most isolated inhabited islands, located more than 2,000 nautical miles from Chile (Fig. 2-1). Famous for its monumental statues – or moai – Easter Island’s palm forest was systematically deforested by native Easter Islanders in the process of erecting their statues (Hunt

2006). Chile first declared the island a National Park in 1935, and UNESCO designated it a World Heritage Site in 1996.

Little information exists regarding marine turtles around Easter Island, but leatherbacks and green turtles have been documented (M. Donoso, pers. comm.); green turtles have even been satellite tracked within their foraging grounds on the

Easter Island (P. Dutton, unpubl. data). Leatherbacks have been satellite tracked from nesting beaches in Costa Rica to waters nearby Easter Island (Shillinger et al. 2008), and they have been caught around the islands by the Chilean artisanal swordfish fleet.

Island Systems on the Continental Shelf

Tres Marías Islands, México

The Tres Marías Islands are located just 65 nautical miles off the west coast of

México (Fig. 2-1). These islands have been known since early in the history of the New

World, and were first named as Las Islas de la Magdalena. The Tres Marías group comprises four islands: San Juanito, María Madre, María Magdalena, and María Cleofa.

Since 1905, the Tres Marías Islands Federal Prison has been home to some of the most infamous and dangerous criminals in México.

References regarding sea turtles are very scarce, but Stejneger (1899) reported the existence of nesting around May and June by green turtles and hawksbill, and

Parsons (1962) reported a large number of hawksbills nesting on beaches of Tres

Marías. Nesting activity of hawksbills on the islands has not yet been reconfirmed.

Coiba Island, Panamá

Coiba Island, the largest uninhabited tropical forested island in the Americas, is included in Coiba National Park (CNP), which is comprised of over 2,700 km2 of islands, forests, beaches and mangroves (Fig. 2-1). The island is ringed by one of the largest coral reefs on the Pacific Coast of the Americas (Cortés 1997). The remarkable preservation of Coiba Island is largely due to its use as a penal colony since 1920; the prisoners have served as a strong deterrent to colonization by peasants and to the extraction of the island's abundant resources (Castrellón 2008). Due to the pristine nature of the island and its surrounding oceans, it was declared a National Park by the

Panamanian government in 1992, and UNESCO declared the entire Coiba National

Park a "World Heritage Site" in July 2005.

The Indo-Pacific current through the Gulf of Chiriquí provides a unique environment for marine life and, by extension, for recreational diving. The warm current carries tropical marine species from the other side of the Pacific, and larger animals such as humpback whales, sharks, whale sharks, orcas, among others, are also regular visitors (Aguilar et al. 1997). Regarding sea turtles, very little information exists, but olive ridleys, hawksbills, and leatherbacks have been recorded to nest on the island

(Castrellón 2008).

Malpelo Island, Colombia

Malpelo Island is an oceanic island of a volcanic origin emerging from the sea bottom at about 4 km of depth, roughly 270 nautical miles from the coast of Colombia

(Fig. 2-1). It is uninhabited except for a small military post manned by the Colombian

Army, which was established in 1986, and civilian visitors need a written permit from the

Colombian Ministry of the Environment. It was declared a Flora and Fauna Sanctuary in

1995 and a World Heritage Site by UNESCO in 2006. Malpelo Island is a very popular diving location, as hundreds of hammerhead sharks and silky sharks are frequently seen by diving expeditions.

The marine environment is strongly influenced by the marine currents in the area, which create very productive habitats. These conditions make the island an important habitat for many migratory species, including marine mammals, schools of large pelagic fish and sharks, and sea turtles (Birkeland et al. 1975). Five species of marine turtles have been observed feeding around Malpelo Island, including hawksbills, green turtles, olive ridleys, leatherbacks, and loggerheads. However, research surveys carried out in

2006 by the Fundación Malpelo and the Centro de Investigación para el Manejo

Ambiental y el Desarrollo (CIMAD) of Colombia only recorded green turtles, all of them subadults in apparently good health conditions and associated to coral reefs habitats.

This first survey represented the first step in the implementation of the Sea Turtle

Sighting Program at Malpelo Island (Pavía & Amorocho 2006).

Gorgona Island, Colombia

Home to a now defunct, but once notoriously harrowing prison, this island (and its smaller sister island, Gorgonilla) was christened in the 16th Century by Francisco

Pizarro, who, after losing dozens of his men to venomous snake bites, likened the place to the mythical Gorgon sisters. Since the prison closed in 1984 and the Island was named a National Park the following year, the only humans on the island are temporarily stationed Park rangers and visiting tourists.

Like other islands in the region, Gorgona is a refuge for marine and terrestrial biodiversity. The island is a popular tourist destination for whale watching, as female humpback whales pass close to shore with their newborn calves in tow every year, and its rich coral reef habitats draw divers year-round. Among the inhabitants of Gorgona’s fringing reefs, relatively abundant juvenile green turtles, as well as less abundant hawksbills, have been observed during an extensive mark-recapture study conducted since 2003 by CIMAD. During this period, the research group has hand-captured nearly

500 free-swimming green turtles (<10 hawksbills and olive ridleys) during night dives around Gorgona (Amorocho 2009). In addition, low-density olive ridley nesting occurs on sandy beaches on the island (Camayo & Amorocho 2008). Like other known foraging areas for juvenile green turtles in the eastern Pacific, Gorgona appears to host a mixed stock of juvenile turtles, comprised of individuals reflecting genetic haplotypes from different rookeries from the region, as well as individuals of the yellow morph observed in Galápagos that exhibit haplotypes from western Pacific green turtle stocks

(Amorocho 2009, Amorocho et al. 2012).

As consistent monitoring efforts have shown in Gorgona (and other sites), islands in the eastern Pacific often represent important feeding areas for individuals from distinct rookeries in the region, which highlights the importance of protecting these areas to ensure persistence of multiple breeding populations of green turtles in the region.

Challenges and Advances in Island Conservation: a Case Study of the Galápagos Archipelago

Despite the isolation of islands from mainland areas and their associated anthropogenic effects, human-induced threats to island ecosystems certainly exist, as

mentioned previously. These remote natural systems have evolved a unique and delicate balance that often differ greatly from those on the closest mainland, and thus are particularly sensitive to impacts from other environments. In particular, a common theme for island systems in the EP and elsewhere are introduced species, including plants, but also vertebrates, such as pigs, dogs, livestock, and rodents.

Among all the islands in the region, Galápagos represents the most complex system of critical biophysical, socioeconomic and cultural resources, which have a profound impact on the archipelago’s natural resources and biodiversity. The number of visitors has increased 9% annually over the last 25 years, and the resident population in

Galápagos more than doubled from 1990 to 2006, now topping 20,000 inhabitants.

Population growth is increasing pressure on natural resources and the demand for improved public services, motor vehicles, commercial flights, fuel consumption, and electricity, among others. Increased food demand for the growing Galápagos human population has been reflected in the decline of marine resources such as lobster, sea cucumber, and cod.

Major causes of concern regarding sea turtles at Galápagos Archipelago are related to the increasing tourism activity, artisanal fisheries within the Galápagos Marine

Reserve (GMR) and the National Park, and introduced mammal predators. Intensive marine traffic and illegal fishery practices in the GMR has been linked to observations of dead and injured sea turtles. Additionally, feral pigs are voracious predators of sea turtle eggs and hatchlings.

Despite the challenges and problems the Archipelago is facing, Galápagos is the only oceanic archipelago with 95% of its original biodiversity still intact, which is due to a

strong legal framework for conservation and the achievements of the conservation institutions in Galápagos (CDF, GNP and INGALA. 2008). However, a strong commitment among all Galápagos stakeholders is necessary to ensure sustainable co- habitation between humans and nature. In recent years, management entities of the

Galápagos have implemented several measures to address these threats, which might serve as models for other island systems in the region facing similar threats.

Coastal Zonation Scheme Implementation

In 2000, a coastal zonation scheme was established to regulate the human exploitation of natural resources within the GMR, to avoid conflicts between stakeholders, and to protect high biodiversity sites. In some areas, fishing and other activities are permitted, in other areas fishing is prohibited but tourism is allowed, and in others only research and management activities are permitted. The CDF’s marine research team is carrying out systematic biological surveys to provide a baseline for future evaluation (Watkins et al. 2008). Zonation is an extremely important management tool, but has been very difficult to implement due to stakeholder resistance; e.g., fishermen were very reluctant to accept the idea of “no-take areas.” The zonation scheme is to be re-evaluated in terms of both socioeconomic impacts and preliminary ecological impacts, but many of the benefits of no-take areas will only become apparent with time (Novy 2000, Heylings et al 2002, WWF-USAID 2006).

Within the zonation scheme, full protection has not been established to include criticial habitats for sea turtles in the Galápagos Marine Reserve.

Longlining Banned within the Galápagos Marine Reserve

Cold, hot and warm marine currents come together in the waters of the GMR generating a wide diversity of animal life especially around submarine volcanoes whose

peaks nearly reach the surface. These areas are important for both fishermen and tourism because they host a wide variety of commercial fishes as well as sharks, sea lions, sea turtles and dolphins, among others (Oviedo 1999, Banks 2002). Although industrial fishing is forbidden within the GMR, local fishermen have used these areas for targeting tunas and swordfish using longline gear (Zárate & Dutton 2002, Murillo et al.

2004, Galápagos National Park, unpubl. data). Considering the high bycatch associated with this fishing gear, the CDF did a study in 2003 to determine if small-scale longlining of yellowfin tuna and swordfish should be permitted in the reserve. The researchers found that most of the catch was composed by non-target species, mostly sharks but also the four sea turtle species recorded in the Archipelago (Murillo et al. 2004). As a result, longlining was banned in Galápagos waters in 2005 (Registro Oficial 2006).

Quarantine and Inspection System and Eradication Programs Implemented

Since the New World discovery of the Galápagos Archipelago by Bishop Tomás de Berlanga in 1535, humans have introduced exotic (i.e., non-native) species to the islands, some intentionally, including goats, pigs, cats, and both ornamental and food plants (vegetables and fruits), and some accidentally, including rodents, insects, and weedy plants (Watkins et al. 2008). Herbivores, like goats, compete for the little available food with tortoises and land iguanas making it so there is not enough food to support the native creatures, while introduced plants compete with the native plants for scarce nutrients in depauperate Galápagos soil. Pigs and goats destroy nests and eat bird and reptile hatchlings and eggs.

Immigration and tourism in recent decades to the Galápagos has increased the risk of introduced species entry through various pathways such as cargo boats and airplanes. To prevent the entry and spread of potentially threatening exotic species, the 43

Galápagos inspection and quarantine system (SICGAL) was established in 2000

(Zapata 2008). Trained SICGAL inspectors now search incoming cargo shipments from boats and planes, as well as luggage carried by tourists and residents (Zapata 2008). It is much more cost-effective to prevent the arrival of introduced species as the costs of implementing mitigating activities after their arrival can be high and continuous.

Although the quarantine and inspection programs can prevent new biological invasions, eradication programs have been established by the Galápagos National Park to address invasive species already present in the Archipelago. Successful eradication programs include: a program to eradicate feral cats (Felis catus) from the island of

Baltra (Phillips et al. 2005); the largest removal of an insular goat population using ground-based methods, from Pinta island (Campbell et al. 2004); and the multi-year, multi-million dollar Isabela Project, which resulted in complete eradication of goats and donkeys from Santiago and most of Isabela islands (Carrión et al. 2006).

Most important for sea turtles, feral pigs (Sus scrofa) on Santiago Island have been responsible for a near zero recruitment rate of giant tortoises and green turtles

(Calvopiña 1985, Green 1979). Like the goat eradication efforts, the eradication of pigs from Baltra island is considered the largest insular pig removal to date: Over 18,000 pigs were removed during a 30-year eradication campaign (Cruz et al. 2005). As of

2007, several islands and islets in the Archipelago are now free of cats, goats, pigeons, donkeys, and pigs. Introduced species are more abundant and have a greater incidence on the inhabited islands, all of which are considered high priority for control and eradication efforts in the coming years.

International Conservation Efforts for Island Systems in the EP

Oceanic and continental shelf islands play an important role as developmental refugia for sea turtles – especially green turtles – in the EP region. They act as juvenile nursery and foraging areas where individuals from multiple genetic stocks mix, and provide reproduction sites for adult turtles. Because these island systems not only share function for sea turtle life cycles and natural history, but also share individual turtles and turtle populations, international conservation strategies have begun to address islands as a network of important habitats. An important framework for sea turtle conservation in the eastern Tropical Pacific is the Marine Corridor (CMAR) Initiative, which is a voluntary multilateral agreement among the governments of Costa Rica, Panamá,

Colombia, and Ecuador to work towards integrated, sustainable use and conservation of marine resources in these countries’ waters. A related program, the Eastern Tropical

Pacific Seascape (ETPS) Initiative managed by Conservation International, supports inter-institutional, cooperative scientific research and marine management among the same four countries. The Comisión Permanente del Pacífico del Sur (CPPS, or the

Lima Convention), has developed an Action Plan for Sea Turtles in the Southeast

Pacific among signatory countries Panamá, Colombia, Ecuador, Perú, and Chile

(Seminoff & Zárate 2008). The Inter-American Tropical Tuna Commission (IATTC) and its bycatch reduction efforts are globally recognized to be among the world’s finest for regional fisheries management organizations. The Inter-American Convention for the

Protection and Conservation of Sea Turtles (IAC) is another policy instrument designed to decrease impacts on sea turtles from fisheries and other human impacts. Clearly, the region benefits from having several strong, complementary conservation instruments

and organizational structures in place to promote and enhance sustainable resource use and biodiversity protection.

Nonetheless, sea turtle conservation in the EP requires successful implementation and greater integration among the region’s international instruments and accords. New legislation and enforcement of existing laws that curb unsustainable exploitation of sea turtle products in the region’s coastal communities is also necessary.

Hopefully, coordinated management efforts will provide habitat protection that extends from nesting beaches to marine habitats for sea turtles and other species within and among the island oases of the EP.

Tres Marías Is., MEXICO Mexico

Revillagigedos Archipelago, México

Cocos Is., Costa Rica Clipperton Is., Coiba Is., French Overseas Territory Panamá COLOMBIA Malpelo Is., Colombia Gorgona Is., Galápagos Is., Colombia Ecuador ECUADOR

Easter Is., Chile

Figure 2-1. Location of the islands in the eastern Pacific Ocean included in this chapter.

B C

Figure 2-2. Yellow morph of Chelonia mydas captured at Galápagos foraging grounds. A) Lateral view, B) Dorsal view, C) Coloration of the head (photos courtesy of Peter Dutton).

CHAPTER 3* HATCHING AND EMERGENCE SUCCESS OF GREEN TURTLE (Chelonia mydas) NESTS IN THE GALÁPAGOS ISLANDS

Introduction

The importance of hatchling survivorship for long- term sea turtle conservation has been clearly demonstrated in a series of both empirical (Dutton et al. 2005,

Marcovaldi & Chaloupka 2007) and theoretical (Chaloupka 2002, Mazaris et al. 2006) studies. Hatchling survivorship is key for maintaining stable age structure and population size and essential for adult recruitment (National Research Council 2010).

Two metrics, hatching and emergence success are used to measure survival during this life history stage in sea turtles (Miller 1999). Hatching success is the proportion of eggs from which hatchlings emerge in the nest chamber. Emergence success is the proportion of eggs from which hatchlings emerge from the nest chamber and reach the surface of the beach. Usually emergence success is slightly lower than hatching success because not all hatchlings reach the beach surface.

Although hatching and emergence success are direct and simple measurements, surprisingly few data are available for nests left in situ (Table 3-1), given the hundreds of sea turtle nesting beaches that are monitored worldwide each year. Many studies of hatching and emergence success refer to artificial hatchery operations (Hirth 1997) or experimentally manipulated clutches of eggs (Ackerman 1980) that may not reflect natural survival rates (Wyneken et al. 1988, Abella et al. 2007).

* Chapter 3 has been accepted for publication and the citation is: Zárate P, Bjorndal KA, Parra M, Dutton PH, Seminoff JA, Bolten AB (2013). Hatching and emergence success of green turtle (Chelonia mydas) nests in the Galápagos Islands. Aquatic Biology. Vol.19: 217–229. Reprinted here with permission.

Hatching success depends upon the interaction of numerous abiotic and biotic factors and varies among species and populations of sea turtles (Hirth 1980, Van

Buskirk & Crowder 1994). Temperature (Matsuzawa et al. 2002, Segura & Cajade

2010), moisture (Ackerman 1980, Mortimer 1982), sand structure and composition

(Mortimer 1990) and salinity (Ackerman 1980) can affect embryonic development by altering nest conditions. Hatching success can be affected by the nest location and its microhabitat or surrounding environment (Whitmore & Dutton 1985, Bjorndal & Bolten

1992, Hays & Speakman 1993). Human activities on nesting beaches resulting in sand compaction can decrease hatching success (Kudo et al. 2003). Predation of sea turtle eggs and hatchlings by a wide range of predators can have major effects; both native and introduced animals can substantially reduce hatching and emergence success

(Stancyk 1982).

Clutches deposited earlier in the season can be subsequently destroyed by females digging egg chambers later in the season. The probability of this mortality source is highly dependent on nest density. As the density of nesting females increases, the probability of one female excavating another nest increases (Bustard & Tognetti

1969, Tiwari et al. 2006, Honarvar et al. 2008).

In the eastern Pacific Ocean, green turtles, Chelonia mydas, have been heavily affected by human exploitation, and globally green turtles are considered endangered

(IUCN 2012). The Galápagos Islands hosts one of the most important rookeries for green turtles in the eastern Pacific Ocean. The population appears to be stable with more than 40% of the nesting green turtles in the region (Seminoff 2004, 2007).

Green turtle nesting in Galápagos coincides with the warm and rainy season from December to May, with peak nesting in February and March (Green & Ortiz-

Crespo 1982, Zárate & Dutton 2002). Earlier studies on nest predation in Galápagos green turtles (Green & Ortiz-Crespo 1982, Hurtado 1984) found that hatching success varied among beaches. Whereas mean hatching and emergence success of about 70-

80% were found on beaches where no egg depredation or nest flooding occurred, low mean hatching and emergence values of about 40% were found on nesting beaches where nest depredation was caused by feral pigs (Sus scrofa) and beetles (Omorgus suberosus). These studies were conducted decades ago; further investigation is needed because of the important contribution of Galápagos to the regional green turtle population.

The aim of this study was to determine the hatching and emergence success of natural green turtle nests in the Galápagos and to evaluate the effects of beach, year, day of oviposition, size of female, nest position, nest habitat, chamber depth, and depredation impacts. Understanding the hatching and emergence success and impacts on different beaches are important for nesting beach management and will help to improve strategies for the protection and conservation of these critical habitats for green turtles in the Galápagos Archipelago. This modeling approach can be applied to nesting beaches around the world.

Material and Methods

Study sites

The study was conducted on four nesting beaches (Fig. 3-1) – Quinta Playa

(1.00° S, 91.08° W) and Bahía Barahona (0.98° S, 91.03° W) on Isabela Island, Las

Bachas (0.49° S, 90.33° W) on Santa Cruz Island, and Las Salinas (0.47° S, 90.29° W)

on Baltra Island – that have the highest nesting activity in the Galápagos (Zárate &

Dutton 2002).

The four study beaches vary considerably in length, intertidal zone distance, beach slope, nesting zone width, beach area, and open access from the ocean (Table

3-2). The supralittoral vegetation area of Quinta Playa is a wide dense band mostly composed of buttonwood (Conocarpus erectus) and to a lesser extent by black mangroves (Avicennia germinans). Dune (open beach) vegetation consists mostly of sea purslane (Sesuvium portulacastrum), beach morning glory (Ipomoea pescaprae), and saltworts (Batis maritima). Bahía Barahona’s supralittoral vegetation consists mainly of white (Laguncularia racemosa) and red (Rhizophora mangle) mangroves, buttonwoods, and, to a lesser extent, black mangroves. Dune vegetation is very similar to Quinta Playa. Las Bachas has greater plant diversity including several endemic species. Supralittoral vegetation is composed of white and black mangroves and palo santo trees (Bursera graveolens), desert-thorn (Lycium minimum), and shrubs

(Maytenus octogona). Dune vegetation is mainly composed of saltbushes

(Cryptocarpus pyriformis), sea purslanes, and quail plants (Heliotropium curassavicum).

A few patches of desert-thorn, saltworts, and sea purslane can be found on the dune area of Las Salinas.

Data collection

Surveys were conducted every night throughout the nesting season on the four beaches during four consecutive nesting seasons from 2003/04 through 2006/07

(December-June). Hereafter, each nesting season will be referred as using the second year in sequence (e.g., the 2003/04 season is referred to as 2004). Tags with an identification code and return address were attached to each nesting turtle on each front 52

flipper (Style 681 Inconel tags from National Band and Tag Company, Newport,

Kentucky). Curved carapace length (CCL) from the nuchal notch to the tip of the longer supracaudal scute, and curved carapace width (CCW) at the turtle’s widest point were measured (Bolten 1999). Numbers of eggs with and without yolks (hereafter referred to as eggs and yolkless eggs, respectively) in each clutch were also recorded. Yolkless eggs are easily distinguished from yolked eggs by much smaller size and non-spherical shape. Clutch size always refers to the number of yolked eggs. Eggs were counted using a hand tally counter as they fell from the females during oviposition without been handled. The eggs were left in situ to develop under natural conditions. All nests were marked by placing a wooden stick with coded tag in the sand about 10 cm in front of the edge of the clutch, and nest location was recorded by GPS and mapped along with reference points so the nests could be identified after emergence. Marked nests were checked daily for disturbance by predators, wave action, nesting activity by other turtles, and/or human activity. Causes of nest destruction or depredation as well as the number of nests and eggs affected were recorded.

Nest location was assigned based on the zone where the clutch was laid: 1. intertidal, 2. beach slope, 3. open beach (dune), or 4. supralittoral vegetation. The slope represents the natural inclination of the sand on the beach face, which is the zone of highest wave action. The supralittoral vegetation zone can either be a dense band of vegetation or small patches of vegetation behind the open beach.

Nest habitat was classified according to the immediate surrounding environment of each nest: a. bare sand, b. creeping vegetation, c. small bushes, or d. large bushes

and trees. These nest environment categories were assigned independently of the zone in which the clutches were laid.

Egg chamber depth was measured with a steel measuring tape or meter stick from the bottom of the nest to the bottom of the body pit (a pit dug with the front flippers in which the turtle lies while digging the nest chamber). This measurement was taken by an observer lying on the sand behind the turtle just before oviposition. The distance from the nest to the beach high water mark (HWM) was measured by a 100- meter measuring tape. Nest density was calculated as the number of nests divided by the beach area (km2) and expressed as nests/10m2 by each beach and year.

Nests were excavated by hand 70 days after oviposition, thus allowing completion of the natural emergence process (mean incubation period = 55.0 ± 4.9 days; n = 160). Not all clutches deposited over the course of each nesting season were included in this study because of time constraints. Nests were sampled to ensure even spatial and temporal coverage. Unhatched eggs and hatchlings remaining in the nest chamber were counted. Unhatched eggs were opened to assess the extent of embryonic development according to the following characteristics adapted from Miller

(1999): UD = no visible embryonic development (either early embryonic mortality or infertile); UH1 = embryos without pigmentation; UH2 = pigmented embryo; UH3 = full term embryo with small amount of external yolk material; ND = embryo that could not be assigned to a developmental stage because of deterioration. All hatchlings found in the nest chamber were either dead or moribund with a low probability of survival and were all counted as dead. Hatching success was determined using the following formula:

((total eggs - unhatched eggs)/total eggs) x 100. Emergence success was determined by the formula: ((total eggs - unhatched eggs - dead hatchlings)/total eggs) x 100.

Stage of embryonic mortality was recorded unless egg contents were too decomposed. For predation events, if the predator could be identified either by its presence in the nest or by characteristic eggshell damage, the number of embryos and hatchlings killed by each type of predator was recorded. When both fly larvae and beetle were found at the same time, only the beetke was considered as the cause of mortality due to its ability to break through the eggshell. Overlap was most common between beetle larvae and fly larvae, and predation was assigned to beetle larvae based on their higher mortality impact. Predators found in the egg chamber were identified to the species level; fly larvae were reared for identification. Fungi were not identified. Percentages of eggs and nests affected by each mortality factor were calculated by beach and year and also for all beaches in all years for general comparison to other studies.

Statistical Analyses

To evaluate the extent to which various parameters affected hatching and emergence success, a binomial generalized additive model (GAM) with fixed effects was used. Parameters considered in the GAM were beach, year, day of oviposition, number of yolkless eggs, carapace length and width of female, nest position, nest habitat, chamber depth, and distance to the HWM. Analysis of deviance was used to compare models and select the best model; F-tests were used because of overdispersion. Non-independence of data (successive clutches from some individual females) was not addressed in the model. GAM analyses were conducted with S-PLUS

software (version 8.2.0, TIBCO Spotfire Software, Inc.). Results were considered significant at the 0.05 level.

Mean hatching and emergence success were calculated by beach and year. All means are reported  standard deviation.

Results

The study was based on 1039 nests. Because clutch size was not correlated with hatching success (df = 1038, F = 1.60, P = 0.2055) or emergence success (df = 1038, F

= 1.98, P = 0.1598), a binomial generalized additive models (GAM) with fixed effects that did not include clutch size as a parameter was used. In the first model, independent variables were beach, year, day of oviposition, number of yolkless eggs, CCL and CCW of female, nest location, nest habitat, chamber depth, and distance to the HWM (n =

621). Chamber depth and distance to HWM were not significant, so a second model was run without those parameters and with an increased sample size (n = 1,031). Only four parameters – beach, year, nest habitat, and day of oviposition – were significant; number of yolkless eggs, carapace length and width of female, and nest position were not significant. We repeated the model dropping all non-significant parameters.

Comparison of the two models with analysis of deviance revealed no significant difference (df = 17.83, deviance = 506, F = 0.973, P = 0.489). Thus, the model with four parameters was the best fit, although the model only accounts for 13.3% of the variation in hatching success (Table 3-3). Mean values and ranges for all variables measured on the nesting females and nests are presented in Table 3-4.

Variation in hatching and emergence success was significant among years and beaches (Table 3-5), so data could not be combined for analyses. Hatching success at

Las Bachas and Las Salinas was significantly higher than those at Isabela beaches, and significantly lower hatching success was found in 2006 compared to 2004 and 2005

(Table 3-5, Figs. 3-2A and 3-2B). Nests covered by large bushes and trees (d in Fig.3-

2C) had significantly higher hatching success than clutches laid in bare sand (a in Fig.3-

2C). Day of oviposition had a significant nonlinear effect; clutches deposited early in the season had significantly lower hatching success (Table 3-3, Fig. 3-2D). Although it appears that hatching success declined at the end of the season, the wide confidence limits indicate that the decline is not significant.

Overall mean hatching and emergence success for the 1039 nests was 46.0% 

33.4 and 45.6%  33.4, respectively. Hatching success was significantly lower in beaches where nest density was higher (Bahía Barahona and Quinta Playa) and significantly higher in beaches with low nest density (Las Bachas and Las Salinas;

Table 3-5).

Emergence success is very similar to hatching success in Galápagos green turtle nests (Table 3-5, R2 = 0.99; Fig. 3-3) with the exception of 5 nests. Dead hatchlings (6 -

60 hatchlings) were found in those nests, primarily from predation by fly larvae (73.8%) and unknown causes (26.2%). Because the model results for emergence success are almost identical to those of hatching success, only model results for hatching success are presented in this paper.

Embryo mortality was due to many factors including predation, nest destruction by other nesting females, tidal inundation (erosion and submergence), and invasion by plant roots. We observed predation by the native scarabeid beetle (Omorgus suberosus), the feral pig (Sus scrofa), native ghost crab (Ocypode gaudichaudii), and fly

larvae species either introduced (Oxisarcodexia bakeri, Peckia chrysostoma,

Sarcodexia lambens) or endemic (Galopagomyia inoa) (Tables 3-6 and 3-7). In some cases the entire clutch was destroyed, whereas in others only some of the embryos were killed.

Beetles affected 688 nests (66.2 %) and killed 23,361 embryos (31.6%; Tables 3-

6 and 3-7). Adult beetles burrow down to the egg chamber where they reproduce. Both larvae and adults feed on the egg contents after chewing through the shell. In most cases, it was impossible to determine the stage of embryonic mortality from beetles because of decomposition. Beetles attacked very few live or dead hatchlings (n < 10).

Mortality from beetles varied substantially among beaches. Beetles appear to have killed higher percentages of embryos in Bahía Barahona and Quinta Playa (27 – 44 %) than in Las Bachas and Las Salinas (0.8 – 22%) (Tables 3-6 and 3-7). Beetle depredation was recorded throughout the season (Fig. 3-4A) and in all nest habitats.

Feral pigs destroyed 77 nests (7.4%) and killed 5471 embryos (7.4%; Tables 3-6 and 3-7). Mortality from pigs varied greatly by island (pigs do not occur on Las Bachas or Las Salinas) and by year. Feral pigs were observed digging out nests with freshly laid eggs or with pre-emergent hatchlings (hatchlings not yet emerged from the nest) and feeding on hatchlings moving to the sea. However, no information regarding stage of development of the embryos on nests destroyed by pigs was collected. Pigs preyed upon nests in all habitats except under large bushes and trees, and their impact appears to have been greater on clutches deposited early and late in the season (Fig.

3-4B).

Ghost crabs, although abundant in the study beaches, affected only 56 nests

(5.4%) and killed 591 embryos (0.8%; Tables 3-6 and 3-7). Crab burrows were often found around green turtle nests, and occasionally crabs were found in the egg chamber during excavation. Predation by crabs was identified by distinctive cuts in the eggshell.

Predation of sea turtle embryos by ghost crabs occurred on all beaches except Las

Salinas and was more common in clutches laid in areas of bare sand or creeping vegetation.

Fly larvae were found in eggs in 23 nests (2.2%) and killed 148 embryos (0.2%;

Tables 3-6 and 3-7); they mainly fed on hatchlings in the nest, either alive or dead. Adult flies were observed on the surface of the beach over turtle clutches depositing larvae in the sand, which then burrowed down to the egg chamber. Larvae enter hatchlings through the yolk sac, cloaca, mouth, and eyes and consume internal organs and muscles. Fly larvae found in nests on Las Bachas and Las Salinas belonged to the

Sarcophagidae family and included three introduced species (Oxisarcodexia bakeri,

Peckia chrysostoma and Sarcodexia lambens) and one endemic species

(Galopagomyia inoa). Impact of each species on turtle eggs was not determined because fly larvae could not be identified in the field. Depredation by flies was observed in all beaches except Bahía Barahona.

Nesting female green turtles destroyed 28 nests (2.7%) and killed 1996 embryos

(2.7%; Tables 3-6 and 3-7). Nest destruction by nesting females was only recorded on

Isabela beaches and had the greatest effect in 2006. Nest destruction by turtles was observed in all habitats except under large bushes and trees and had a greater effect on clutches deposited early in the season (Fig. 3-4C).

Wave action and flooding only destroyed 17 nests (1.6%) and killed 1183 embryos (1.6%; Tables 3-6 and 3-7). All embryos from these nests were washed away or appear to have drowned in the nest. Impact was greater on nests in Las Salinas and

Quinta Playa. Of these nests, 76% were destroyed in the second half of the nesting season. No information regarding stage of development of the embryos on these nests was collected.

Plant roots invaded only 5 nests (0.5%) and killed 74 embryos (0.1%; Tables 3-6 and 3-7), the lowest values among the known causes of mortality. Three of these nests

(60%) were located in areas with creeping vegetation and small bushes. Root invasion was recorded only in 2005 at Bahía Barahona and Las Salinas and only in 2007 at

Quinta Playa.

A total of 7097 embryos (9.6%) in 592 nests (57%) (Tables 3-6 and 3-7) died from undetermined causes at all beaches, but mostly at Las Bachas and Las Salinas.

Unknown causes of embryonic failure were observed in all nest habitats and throughout the season.

Fungi infested 744 nests (71.6%) and 21,069 (29.7%) of the eggs (Table 3-8). I could not determine whether fungus was a source of mortality, but it was present in more than 50% of nests at each beach and year (Table 3-8). Nest infestation was recorded in all nest habitats and throughout the season.

Discussion

Variation in Hatching Success and Comparisons with other Sea Turtle Populations

Mean hatching success and emergence success values found in this study are relatively low compared to other green turtle populations where most values are over

70% (Table 3-1). Low hatching success at other beaches is usually associated with intensive predation pressure (Brown & Macdonald 1995, Turkozan et al. 2011) or very poorly sorted substrates (Mortimer 1990). The lowest hatching and emergence success for green turtles were recorded at Espumilla Beach on Santiago Island, Galápagos. This beach was severely infested by feral pigs resulting in a hatching success of 1.8%

(Green & Ortiz-Crespo 1982). Pigs have since been eradicated on Santiago Island

(Cruz et al. 2005).

Lower hatching and emergence success were recorded on Quinta Playa and

Bahía Barahona than in Las Bachas and Las Salinas. Three characteristics of Bahía

Barahona and Quinta Playa had strong influences on the lower hatching and emergence success on those beaches: presence of beetles and pigs, and higher turtle nest density. Compared to earlier years (Green & Ortiz-Crespo 1982, Hurtado 1984), values of this study for hatching and emergence success at Quinta Playa and at Las

Salinas were similar, but for Bahía Barahona and Las Bachas lower values were obtained (Table 3-1).

The beetle Omorgus suberosus, which was the major known source of mortality for embryos in this study, had been reported to prey on green turtle eggs on Quinta

Playa, Bahía Barahona, and La Picona (Floreana Island) (Algoewer 1980, Green &

Ortiz-Crespo 1982, Hurtado 1984). In this study, beetle predation in Quinta Playa was similar to earlier studies (~30%), but beetles killed twice the number of embryos in

Bahía Barahona compared to earlier data (18.9%; Allgoewer 1980). Differences among years probably result from variation in beetle abundance or rainfall. A relation among turtle nest density, beetle density per nest, and destruction rate has been established

(Allgoewer 1980, Halffter et al. 2009). The beetles reproduce only in wet weather

(López et al. 1994), so the low levels of beetle depredation during 2006 in Quinta Playa and Bahía Barahona might be explained by low rainfall during that year (Charles Darwin

Foundation 2012). Prior to this study, beetles had not been reported in green turtle nests on Las Salinas and Las Bachas. The low impact of beetles on green turtle hatching and emergence success on these two nesting beaches could be due to the low turtle nest density on these beaches.

The only other record of depredation by the beetle Omorgus suberosus on sea turtle eggs is at La Escobilla beach, Oaxaca, Mexico, where the beetles infest olive ridley (Lepidochelys olivacea) nests (Ocana 2011) and are the major cause for nest failure and low hatching success. These results are very similar to those from La

Escobilla, where most nests show evidence of beetle depredation (Ocana 2011), but all eggs in the nest are not always affected.

Pigs are commonly found on Isabela Island, but depredation by pigs on Isabela beaches was restricted to specific periods in some years. Although feral pigs are primarily herbivores, they feed opportunistically on a wide range of food items including sea turtle eggs and hatchlings (Coblentz & Baber 1987, Cruz et al. 2005). Pigs are generally restricted to high elevation habitats in Galápagos, where abundant and succulent forage is available most of the year (Coblentz & Baber 1987). However, in dry years, feral pigs move down from highland to coastal areas in search of food (Calvopiña

1985). The increase in predation by pigs observed in 2006 on Isabela beaches coincides with low levels of precipitation during that year (Charles Darwin Foundation

2012). Pigs are a major cause of leatherback egg mortality in Papua, Indonesia

(Hitipeuw et al. 2007, Tapilatu & Tiwari 2007) where percentage of nest destruction by pigs varies from 5% to 40% of total nests in a season (Starbird & Suarez 1994). Lower destruction percentages in this study possibly result from smaller pig populations due to long term management actions in Galápagos.

Pig depredation is most common at the beginning and at the end of the season and tracks the within-season day-of-oviposition pattern revealed by the GAM analyses.

Visual and olfactory cues used by feral pigs for prey detection (Hayes et al. 1996) are more effective when nest density is low. Because digging is energetically costly, pigs will dig out nests when there is a higher chance of success (Leighton et al. 2009). Other mammalian predators such as dogs in Tortuguero, Costa Rica, follow a similar pattern with increasing predation at the end of the season when nest density is low (Tiwari et al.

2006).

Nest destruction by nesting females on Isabela beaches varied among years and across seasons. This type of nest destruction is a density-dependent source of mortality

(Bustard & Tognetti 1969, Cornelius et al. 1991, Tiwari et al. 2006, Honarvar et al.

2008). With an increase in the number of nesting females, the probability of a female destroying an earlier nest while digging her own nest chamber increases. The higher nest density observed during 2006 in Quinta Playa and Bahía Barahona resulted in an increase in the proportion of nests destroyed by turtles digging nest chambers suggesting density-dependent effects. The lower hatching and emergence success for clutches laid earlier in the season may be a result of most early nesting occurring on beaches with higher nesting activity such as in Quinta Playa and Bahía Barahona.

Nesting begins in early December on Bahía Barahona and Quinta Playa, and about a

month later on Las Bachas and Las Salinas. Early nests are more vulnerable to subsequent destruction from other nesting turtles.

Nest destruction by later nesting sea turtles has been observed in high nest density populations such as in green turtles from Tortuguero, Costa Rica (Tiwari et al.

2006) and the southern Great Barrier Reef, Australia (Bustard & Tognetti 1969, Limpus et al. 2003), in leatherbacks from French Guiana (Girondot et al. 2002), and olive ridleys in Costa Rica (Honarvar et al. 2008). Nest destruction rate from nesting females in

Tortuguero, Costa Rica, is four times higher (Tiwari et al. 2006) than the estimates from

Bahía Barahona and Quinta Playa, which probably reflects differences in population density.

In this study, the habitat directly around the nest did not have an effect except for clutches laid under large bushes and trees that had higher hatching and emergence success than those in other habitats. Most of these nests (95%) were found on Bahía

Barahona and Quinta Playa where pigs and nesting females are major causes of mortality. However, mammal depredation and nesting females were never recorded as a source of mortality in this nest habitat, which could explain the higher hatching and emergence success. Most nests found under large bushes and trees were located in the open beach zone where shade may lessen loss of moisture and buffer temperatures

(Foley et al. 2006). At other nesting beaches, low hatching success of nests located in vegetated areas may result from higher rates of predation by forest-dwelling predators

(Bjorndal & Bolten 1992, Caut et al. 2006).

Unknown Sources of Mortality

Only 13.3% of the variation in hatching success was explained by GAM analysis.

The proportion would undoubtedly have been higher if more variables were quantified 64

for each beach in each year, such as pig and beetle abundance, changes in nest density throughout the seasons, rainfall, and physical parameters of the beach substrate.

Physical parameters of the beach substrate, such as gas exchange, sand moisture, and temperature are important factors for the survival of sea turtle embryos and can affect hatching and emergence success (Mrosovsky & Yntema 1980, Mortimer

1990). Seasonal changes in sand temperature resulting in temperatures outside of the viable range can induce seasonal changes in mortality. Embryos die from hyperthermia in nests with temperatures above 33- °C for an extended period of time (Matsuzawa et al. 2002). High nest temperatures can reduce emergence success by limiting the ability of hatchlings to reach the surface (Matsuzawa et al. 2002). Amount of rainfall affects hatching success of green turtles at Raine Island, Australia, where drier years have lower rates of hatching and nesting success (Limpus et al. 2003).

Another important aspect of temperature that deserves attention in the

Galápagos is the effect on sea turtle hatchling sex ratios with potential wider implications for the survival of the population. Katselidis et al. (2013), studying long- term variation of hatchling sex ratios from loggerhead turtle nests at Zakynthos, Greece, showed that males and females were produced at different times within a season and that some beaches were responsible for male production while females were produced at other beaches. Understanding the range of male versus female offspring production within a rookery may be critical for specific management actions at each nesting beach.

Global climate change may shift hatchling production on tropical beaches to a single sex (Witt et al. 2010).

The role of fungi in sea turtle nests is poorly understood and deserves greater attention. Fungus infestation has been described in all sea turtle species around the world in eggshells, embryonic tissues, and sand surrounding nests (Peters et al. 1994,

Phillott & Parmenter 2001, Güçlü & Sahiner 2010). However, the actual effect of fungus on embryonic mortality is difficult to establish. The infestation and dispersion of the fungi throughout a clutch is thought to be opportunistic; an egg that is already decaying will be invaded by soil mycobiota (Phillott & Parmenter 2001). Güçlü et al. (2010) found that hatching success in loggerhead nests in Turkey was negatively correlated with the total number of isolated fungi genera. In this study, fungi were present in more than 70% of nests, but I could not determine whether it was a source of mortality.

Management Actions and Recommendations

An important management question is whether the current management plan will succeed in protecting green turtles at key nesting beaches in Galápagos and what specific conservation actions should be undertaken based on threats identified here. I have confirmed that beetles and feral pigs are major threats to turtle nests in Bahía

Barahona and Quinta Playa. I have also identified destruction of nests by nesting females as a new important threat to Isabela beaches.

The Galápagos Archipelago has the greatest level of vertebrate endemism among all islands in the eastern Pacific Ocean (Plan de Manejo del Parque Nacional

Galápagos 2005). Control and management strategies such as eradication or elimination of invasive species have been established by the Galápagos National Park

Service (GNPS) to protect endemic and native species. The eradication of pigs on

Santiago Island after an intensive and expensive campaign was a major victory (Cruz et al. 2005). Since then, the hatching success of green turtle nests on that island has 66

increased (Zárate 2003). A feral pig eradication program that includes the Isabela beaches has been underway since the 1980s. This program keeps pig populations at low levels and should be maintained as a high priority.

With the exception of feral pigs, major factors influencing hatching and emergence success in the Galápagos Islands are of natural origin. Thus, the elimination of the native scarabeid Omorgus suberosus from green turtle beaches is not an option.

Predation by beetles deserves attention, particularly at Isabela beaches where hatching and emergence values are already very low. Our new records of this beetle in Las

Salinas and Las Bachas are of great concern and could represent a serious risk for green turtles on these beaches in the future. Beetle reproduction is influenced by climatic conditions and changes in weather associated with El Niño events or climate change could increase the impact of O. suberosus on green turtle nests. Further research on this species is encouraged to better understand the ecological role of beetle predation, the factors that determine which turtle nests are infested, and whether human activities transport beetles among beaches.

No direct threats from human activities such as pedestrian traffic, egg poaching or turtle capture were recorded during this study, but they do occur to some extent.

Isabela beaches and Las Salinas frequently have unauthorized visitors who use the beach as a recreational site. Las Salinas and Las Bachas are located in the vicinity of a major tourist center formed by the main airport and port on Baltra Island and the Itabaca

Canal. There is concern about the increased tourism activity at Las Bachas during the past decade.

Conservation measures implemented solely on nesting beaches may not be effective when in-water threats are present. The categories currently assigned to study beaches under the Galápagos Marine Reserve allow different activities at sea and along the coast of the islands that affect sea turtles. As a consequence of that, major threats to sea turtles in Galápagos waters are boat strikes, fishing interactions, and direct capture. All of these aspects are of great concern but are difficult to resolve in the short term. The process of management of the Galápagos Marine Reserve requires the participation of all stakeholders at the Participatory Management Board (Plan de Manejo de Conservación y Uso Sustentable para la Reserva Marina de Galápagos 1999).

These increasing threats at sea reinforce the need to keep impacts on nesting beaches at minimum levels as a high conservation priority, particularly at Isabela beaches that have the highest level of green turtle nesting activity in the islands (Hurtado 1984,

Green 1994, Zárate & Dutton 2002).

Results from this study will help managers in the Galápagos National Park

Service to formulate management strategies to protect green turtle critical habitats.

Furthermore, these results are essential for sea turtle demography and population modeling. Hatching and emergence success as key demographic parameters can be used to determine how quickly a population might recover from population perturbations. In addition, these results provide a baseline for studies on climate change and its implications for future impacts.

Table 3-1. Hatching and emergence success from natural nests of green turtles. If only one value is given for hatching or emergence success, it is the mean value. Standard deviations (SD) and ranges are presented when available. Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Pacific/Indian Ocean Revillagigedo Is., Mexico 89.7(16.9) - 61 Juárez-Cerón et al. (2003) Bahía Barahona, Galápagos 74.2 72.9 1979 69 Green & Ortiz-Crespo Is.,Ecuador (1982) Bahía Barahona, Galápagos Is., 41.2(30.5) 41.0(30.5) 2004- 345 This study Ecuador 0-100 0-100 2006 Las Bachas, Galápagos Is., 80.4 78.4 1979 22 Green & Ortiz-Crespo Ecuador (1982) Las Bachas, Galápagos Is., 62.3(281) 61.8(28.4) 2004- 102 This study Ecuador 0-100 0-100 2005 Las Salinas, Galápagos Is., 72.1 69.7 1976 94 Green & Ortiz-Crespo Ecuador (1982) Las Salinas, Galápagos Is., 52.2 49.7 1977 21 Green & Ortiz-Crespo Ecuador (1982) Las Salinas, Galápagos 71.0 69.8 1978 38 Green & Ortiz-Crespo Is.,Ecuador (1982) Las Salinas, Galápagos Is., 71.1 69.9 1979 22 Green & Ortiz-Crespo Ecuador (1982) Las Salinas, Galápagos Is., 71.5(28.9) 71.1(29.1) 2004- 89 This study Ecuador 0-100 0-100 2005 Quinta Playa, Galápagos Is., 38.6 37.8 1976 120 Green & Ortiz-Crespo Ecuador (1982) Quinta Playa, Galápagos Is., 43.7 40.5 1977 101 Green & Ortiz-Crespo Ecuador (1982)

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Quinta Playa, Galápagos Is., 43.5 41.2 1978 40 Green & Ortiz-Crespo Ecuador (1982) Quinta Playa, Galápagos Is., 48.7 47.7 1979 67 Green & Ortiz-Crespo Ecuador (1982) Quinta Playa, Galápagos Is., 41.4(33.9) 41.0(33.9) 2004- 503 This study Ecuador 0-100 0-100 2007 Espumilla, Galápagos Is., 1.9 1.9 1979 122 Green & Ortiz-Crespo Ecuador (1982) Bartolomé, Galápagos Is., 50 47.2 1979 15 Green & Ortiz-Crespo Ecuador (1982) La Picona, Galápagos Is., 60.9 66.5 1982 30 Hurtado (1984) Ecuador French Frigate Shoals, Hawaii, - 70.8 - 40 Balazs (1980) USA French Frigate Shoals, Hawaii, 78.6 71.1 1986- 428 Niethammer et al. USA 1991 (1997) Raine Is., Australia 85.5(13.1) 83.9(13.3) 1983 16 Limpus et al. (2003) Raine Is., Australia 79.5(14.9) 78.6(15.2) 1984 162 Limpus et al. (2003) Heron Is., Australia 55 - - - Moorhouse (1933) Heron Is., Australia - 88 1966-7 26 Bustard (1972) Heron Is., Australia - 85 1967-8 40 Bustard (1972) Long Is., Papua New Guinea - 89 - 1 Spring (1983) Mak Kepit, Pulau Redang Is., - 81.4(22.3) 2002 214 Ali & Ibrahim (2002) Malaysia Wan-an Is., Taiwan 72.2(30.2) 47(39.1) 1997- 242 Cheng et al. (2008) 2006 Lanyu Is., Taiwan 80.7(27.8) 64.1(39.7) 1997- 166 Cheng et al. (2008) 2006

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Baguan Is., Philippines 87.1 85.7 - 146 Trono (1991) Bearu Archipelago, Indonesia 81.9(6.6) - - 7446 Reischig et al. (2012) Mangrol-Porbandar, India 79 76 2000- 194 Venkatesan et al. 2002 (2004) Karan Is., Saudi Arabia - 81.7 - 4 Miller (1989) 60.9-95 Abdul Wadi, Yemen - 48 - 1 Hirth & Carr (1970) South Coast, Kenya 32 - 1997 1 Okemwa et al. (2004) Mombasa, Kenya 82 - 1997 51 Okemwa et al. (2004) Mombasa, Kenya 79 - 1998 10 Okemwa et al. (2004) Mombasa, Kenya 95 - 1999 35 Okemwa et al. (2004) Mombasa, Kenya 84 - 2000 60 Okemwa et al. (2004) Kiunga, Kenya 66 - 1997 15 Okemwa et al. (2004) Kiunga, Kenya 63 - 1998 45 Okemwa et al. (2004) Kiunga, Kenya 79 - 1999 10 Okemwa et al. (2004) Kiunga, Kenya 77 - 2000 74 Okemwa et al. (2004) Watamu, Kenya 81 - 1998 17 Okemwa et al. (2004) Watamu, Kenya 81 - 1999 92 Okemwa et al. (2004) Watamu, Kenya 77 - 2000 7 Okemwa et al. (2004) Mozambique 85.1(21.1) 80.5(24.2) - 321 Silva et al. (2008) Reunion Is., France 95.8(4) 77.4(9.9) 2004- 5 Ciccione & Bourjea 2005 (2006) Europa Is., France - 84 - 5 Servan (1976) 71-96 Aride Is., Republic of Seychelles 94(7) 91(8) 1982- 10 Dugdale (2001) 2000

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Atlantic Ocean Melbourne, Florida, USA - 61.6(33.9) - 25 Witherington & Ehrhart (1989) Melbourne, Florida, USA 54.3 53.4 1991 99 Johnson & Ehrhart (1995) Broward County, Florida, USA - 61.8 - 12 Broward County Erosion Prevention district (1987) Archie Carr National Wildlife 65.8(5.3) - 2006 185 Balfour (2010) Refuge, Brevard County, Florida, USA Canaveral National Seashore, 62( 5) - 1985- >1000 Antworth et al. (2006) Florida, USA 2003 El Cuyo, Mexico - 86.5 - 15 Rodríguez & Zambrano (1991) El Cuyo, Mexico 92 87 2002 165 Xavier et al. (2006) El Cuyo, Mexico 89 87 2003 75 Xavier et al. (2006) El Cuyo, Mexico 86 84 2004 35 Xavier et al. (2006) Guanahacabibes Peninsula, Cuba >70 - 2001- - Azanza et al. (2006) 2003 Tortuguero, Costa Rica - 83.1 1977 134 Fowler (1979) Tortuguero, Costa Rica - 51.1(5.4) 1986 49 Horikoshi (1992) Tortuguero, Costa Rica - 49.1(4.2) 1988 88 Horikoshi (1992) Tortuguero, Costa Rica - 66.9(3.7) 1989 113 Horikoshi (1992) Tortuguero, Costa Rica 63.5 61.2 1998- 1416 De Haro et al. (2008) 2005 Tortuguero, Costa Rica 86 96 2000 28 Segura & Cajade (2010)

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Boka Manzalina, Curacao 71 - 1993 1 Debrot & Pors (1995) Suriname - 84 - 57 Schulz (1975) Krofajapasi, Suriname - 80.4(1.5) - 80 Whitmore & Dutton (1985) Matapica, Suriname 85.5 - 2000 44 Hilterman (2001) Baboensanti, Suriname 84.1 - 2000 17 Hilterman (2001) Trindade Is., Brazil 84.4(21.5) - 313 Almeida et al. (2011) 0-100 - Atol das Rocas, Brazil 72 1993 94 Bellini et al. (2012) 0-100 - Atol das Rocas, Brazil 78.6 1994 87 Bellini et al. (2012) 0-100 - Atol das Rocas, Brazil 74.1 1995 76 Bellini et al. (2012) 0-99.2 - Atol das Rocas, Brazil 70 1996 38 Bellini et al. (2012) 69-100 - Atol das Rocas, Brazil 70 1997 131 Bellini et al. (2012) 0-100 - Ascension Is., Great Britain - 54.4 - 1208 Carr & Hirth (1962) English Bay, Ascension Is., Great 76.3 63.8 1977- 6 Mortimer (1990) Britain 1978 Hanny, Ascension Is., Great 50.6 45.4 1977- 9 Mortimer (1990) Britain 1978 Long beach, Ascension Is., Great 85.8 84.1 1977- 17 Mortimer (1990) Britain 1978 North East Bay, Ascension Is., 74.3 72.1 1977- 13 Mortimer (1990) Great Britain 1978

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Pebbly Wesr, Ascension Is., Great 20.2 17.4 1977- 6 Mortimer (1990) Britain 1978 Porpoise Pt 1, Ascension Is., 94.5 91.6 1977- 4 Mortimer (1990) Great Britain 1978 South West Bay, Ascension Is., 84.2 71.4 1977- 14 Mortimer (1990) Great Britain 1978 South West Bay, Ascencion Is., 57(0.2) - 1998- 12 Broderick et al. Great Britain 82(0.2) 1999 9 (2001b) Long Beach, Ascencion Is., Great 85(0.2) - 1998- 12 Broderick et al. Britain - 1999 (2001b) North East Bay, Ascencion Is., 1998- Broderick et al. Great Britain 1999 (2001b) Poilao, Bijagos Archipelago, 93.6 - 2000 58 Catry et al. (2002) Guinea-Bissau 69-100

Mediterranean Sea Akyatan, Turkey 10.8 - 1993 10 Brown & Macdonald (1995) Akyatan, Turkey 39.8-68.9 - 2006- 1094 Turkozan et al. (2011) 2009 Samandag, Turkey 77.7(9.6) - 2001- 471 Yalçin-Özdilek (2007) 2005 Kazanli, Turkey 87.7 - - - Durmus (1998) Kazanli, Turkey 83.7 - - - Aureggi (2001) Alagadi, Cyprus - 85.3 - 34 Godley & Broderick (1993) 84.2 - 1992- 897 Broderick & Godley Alagadi, Cyprus 1995 (1996)

Table 3-1. Continued Location Hatching Emergence Year Number References success success of nests Mean(SD) Mean(SD) Range Range Alagadi, Cyprus - 70.2(27) 1997 9 Glen et al. (2005) 1.2-97.4 Alagadi, Cyprus - 73.8(30.2) 1998 29 Glen et al. (2005) 1.5-100 75.3 - 2002 67 Ozdemir & Turkozan (2006)

Table 3-2. Physical features of nesting beaches in the Galápagos Islands. Intertidal zone is the distance between high and low tide. Beach slope represents the incline of the foreshore or beach face. Range of nesting zone represents the potentially usable nesting zone width in the dune zone and is measured from the high tide line to littoral vegetation or to the transition between sand and solid soil. Beach area is the product of the beach length and mean range of nesting zone. Open access corresponds to the percentage of the length of the beach free of obstacles in the intertidal zone. Intertidal zone and beach slope are represented by mean values  standard deviation. Length Intertidal Beach Range Beach Open Beaches (km) zone slope () of area access distance (m) nesting (km2) (%) Quinta Playa 2 60.4  10.3 3  0.5 3zone-40 7.4 80 (m) Bahía Barahona 1.2 46.7  18.3 5  0.9 2-30 6.8 60 Las Bachas 0.96 5.9  2.1 8.9  1.4 12-80 9.6 40 Las Salinas 0.84 7.3  1.3 13.7  2.9 6-40 6.6 30

Table 3-3. Hatching success in Galápagos green turtles. Summary of binomial general additive regression analysis with fixed effects (logit link, cubic smoothing splines). P(F) reported for analysis of deviance test. A significant nonparametric F means that the covariate is nonlinear; this test is only relevant for significant continuous model covariates [P(F)]. Nonlinear effects

(nonparametric) Parameter Df Deviance Residual df Residual P(F) df F P deviance 4 parameter model* Null 1030 40659 Beach 3.00 3299 1027 37360 <0.0001 Year 3.00 1396 1024 35964 <0.0001 Nest habitat 3.00 323 1021 35640 0.0114 Day of oviposition 4.00 373 1017 35267 0.0124 3 22525 <0.0001 * R2 = (null deviance – residual deviance)/null deviance = 0.133

Table 3-4. Variables measured for female green turtles and nests from 2004 through 2007. N is number of nests; HWM is high water mark. Variable N Mean St Dev Min Max Female CCL (cm) 1037 85.0 5.5 69 110 Female CCW (cm) 1037 81.7 4.9 68 103 Yolked eggs 1039 71.2 18.3 21 127 Yolkless eggs 1039 1.7 2.9 0 23 Chamber depth (cm) 679 37.4 7.6 16.5 75 Nest to HWM (m) 690 3.5 3.4 0 35

Table 3-5. Mean hatching and emergence success of green turtle nests by year and beach at four nesting beaches during years 2004 through 2007. Beaches and years with (*) represent lower hatching and emergence success values relative to other beaches and years, respectively. Beach Year Total Nest density Total Hatching success (%) Emergence success (%) nests (nests/10m2) eggs Mean St dev Range Mean St dev Range BB* 2004 88 0.7 6566 48.8 29.8 0-100 48.8 29.8 0-100 BB* 2005 127 0.3 8901 44.5 27.7 0-100 44.1 27.8 0-100 BB* 2006* 130 1.4 9133 32.8 31.8 0-100 32.8 31.8 0-100 QP* 2004 78 1.0 5889 47.4 36.5 0-100 47.4 36.5 0-100 QP* 2005 139 0.5 9713 46.3 30.3 0-100 45.7 30.3 0-100 QP* 2006* 121 1.4 8602 30.1 32.0 0-100 29.6 31.9 0-100 QP* 2007 165 1.6 1143 42.8 35.2 0-100 42.2 35.2 0-100 LB 2004 55 0.2 4108 62.7 27.6 0-100 62.4 27.6 0-100 3 LB 2005 47 0.1 3212 61.9 29.0 0-100 61.1 29.5 0-100 LS 2004 40 0.2 2775 83.6 19.4 0-100 83.4 19.4 0-100 LS 2005 49 0.1 3594 61.7 31.7 0-100 61.1 31.8 0-100 All beaches All years 1039 0.7 7392 46.0 33.4 0-100 45.6 33.4 0-100 BB = Bahía Barahona; QP = Quinta Playa; LB = Las Bachas; LS = Las Salinas.

Table 3-6. Percentages of nests affected by each source of mortality, and percentages of successful nests by beach and season in the Galápagos Islands. A successful nest is a nest that produced at least one hatchling that emerged on the surface of the beach. Beach Year Total Beetles Feral Nesting Crabs Flies Wave Plant Unknown Successful nests pigs females action/ roots mortality nests flooding sources BB 2004 88 85.2 1.1 3.4 1.1 0 0 0 36.4 94.3 BB 2005 127 87.4 0 2.4 0 0 0.8 1.6 56.7 97.6 BB 2006 130 66.9 20.8 6.9 0.8 0 0 0 46.2 67.7 QP 2004 78 64.1 16.7 1.3 0 0 0 0 33.3 80.8 QP 2005 139 77.0 5.0 3.6 0.7 2.2 0.7 0 53.2 87.1 QP 2006 121 54.5 24.0 5.8 1.7 0.8 1.7 0 57.9 66.1 QP 2007 165 70.9 0 0 27.9 2.4 3.6 0.6 55.8 93.9 LB 2004 55 81.8 0 0 9.1 3.6 0 0 89.1 96.4 LB 2005 47 48.9 0 0 0 6.4 2.1 0 87.2 91.5 LS 2004 40 0 0 0 0 15.0 0 0 90.0 100.0 LS 2005 49 14.3 0 0 0 8.2 12.2 4.1 81.6 87.8 All beaches All years 1039 66.2 7.4 2.7 5.4 2.2 1.6 0.5 57.0 85.9 BB=Bahía Barahona; QP=Quinta Playa; LB=Las Bachas; LS=Las Salinas.

Table 3-7. Percentages of embryos in each nest assigned to each source of mortality by beach and year in the Galápagos Islands. Standard deviations are in parentheses. Wave Unknown Total Feral Nesting Plant Beach Year Beetles Crabs Flies action/ mortality eggs pigs females Roots flooding source BB 2004 6566 40.7 1.2 3.4 0.3 0 0 0 5.6 (26.9) (10.7) (18.3) (3.1) (13.1) BB 2005 8901 44.2 0 2.7 0 0 0.8 0.4 7.4 (28.6) (15.2) (8.9) (2.1) (18.0) BB 2006 9133 31.8 20.8 6.9 0.8 0 0 0 6.9 (32.2) (40.7) (25.5) (8.8) (13.8) QP 2004 5889 31.3 16.7 1.3 0 0 0 0 3.3 (33.1) (37.5) (11.3) (8.0) QP 2005 9713 36.3 5.0 3.7 0.4 0 0.8 0 7.5 (29.6) (21.9) (18.7) (3.0) (8.5) (18.2) QP 2006 8602 27.2 24.0 5.8 0.9 0 1.7 0 10.3 (34.0) (42.9) (23.4) (9.0) (12.8) (20.1) QP 2007 11433 44.4 0 0 2.9 0 3.7 0.01 7.3 (34.7) (6.8) (18.8) (0.2) (15.1) LB 2004 4108 22.5 0 0 1.1 0.4 0 0 14.4 (21.9) (5.9) (1.7) (20.5) LB 2005 3213 9.1 0 0 0 0.6 2.5 0 25.9 (14.9) (1.7) (14.6) (26.0) LS 2004 2775 0 0 0 0 0.7 0 0 15.7 (2.3) (18.0) LS 2005 3594 0.8 0 0 0 0.5 12.2 1.1 23.7 (2.9) (2.3) (33.1) (5.6) (22.9) All All 73926 31.6 7.4 2.7 0.8 0.2 1.6 0.1 9.6 beaches years (32.1) (26.2) (16.2) (5.6) (2.6) (12.7) (1.4) (18.1) BB = Bahía Barahona; QP = Quinta Playa; LB = Las Bachas; LS = Las Salinas.

Table 3-8. Percentages of nests and eggs affected by fungus by beach and year in the Galápagos Islands. Standard deviations are in parentheses. Beach Year Nests Eggs Bahía Barahona 2004 69.3 22.5 (26.9) Bahía Barahona 2005 87.4 40.4 (29.1) Bahía Barahona 2006 69.2 36.8 (33.9) Quinta Playa 2004 56.4 17.4 (25.1) Quinta Playa 2005 59.7 14.2 (21.3) Quinta Playa 2006 62.0 34.4 (34.4) Quinta Playa 2007 73.3 41.0 (34.8) Las Bachas 2004 89.1 30.7 (24.8) Las Bachas 2005 80.9 27.5 (25.3) Las Salinas 2004 82.5 15.1 (19.4) Las Salinas 2005 79.6 23.7 (23.4) All beaches All years 71.6 29.7 (30.7)

Pinta

Genovesa Ecuador Marchena

Pacific Ocean

Santiago Fernandina Las Salinas Baltra Las Bachas

Santa Cruz

Isabela Santa Fé

San Cristóbal Bahía Barahona Quinta Playa

Floreana Española

Figure 3-1. Map of the Galápagos Islands showing green turtle nesting beaches used in this study. Star symbols represent settlements on each island.

Nesting beach B A Year

) 0.4 1.0

2005 0.8

LB LS 0.2 200 7 0.6 2004

-0.0

0.4

2006 0.2 -0.2 BB QP

-0.0

-0.4

-0.2 GAM response function, hatching success hatching function, GAMresponse

-0.6

C D 1.0

0.5 d 0.8

0.0 0.6

0.4 b

c -0.5

0.2 a

-0.0

-1.0 GAM response function, hatching success hatching function, GAMresponse -0.2 Nest habitat 0 50 100 150 Day of oviposition

Figure 3-2. Graphical summary of GAM analysis of hatching success covariates in Table 3-1. A) nesting beach, B) year, C) nest habitat, D) day of oviposition. All are significant. The response variable (hatching success) is shown on the y- axis as a centered smoothed function scale to ensure valid pointwise 95% confidence bands. The covariate is shown on the x-axis. For A), B), and C), width of the mean covariate response is proportional to sample size with the 95% confidence interval shown by cross bars. In D), the solid curve is the cubic smoothing spline fits for day of oviposition conditional on all other covariates in the GAM model. Dashed curves are pointwise 95% confidence curves around the fits. BB = Bahía Barahona, QP = Quinta Playa, LB = Las Bachas, LS = Las Salinas. For nest habitat, a = Bare sand, b = creeping vegetation, c = small bushes, d = large bushes and trees. For day of oviposition, day 1 is 15 December and day 150 is 13 May.

100

40 Hatching success (%)

0 0 20 40 60 80 100

Emergence success (%)

Figure 3-3. Hatching and emergence success for the 1039 nests examined in this study at key nesting beaches from 2003-2007 in the Galápagos Islands. Each open circle represents a single nest (y = 0.9984x + 0.6597, R2 = 0.9883).

A 100

60 n = 685

Percentage of mortality Percentage 20

0 0 30 60 90 120 150 B 100

60 n = 77

Percentage of mortality Percentage 20

0 0 30 60 90 120 150 C 100

60 n = 28

Percentage of mortalityPercentage 20

0 0 30 60 90 120 150 Day of year Day of oviposition Figure 3-4. The relation of day of oviposition and percentage of embryos killed in individual nests (n = 1039) by the three mortality factors that changed across the season A) beetles, B) feral pigs and C) nesting females. N values are the numbers of nests affected by each factor; circles are values for each nest; lines are cubic smoothing splines with df = 4. Day 1 is 15 December and day 150 is 13 May

CHAPTER 4 UNDERSTANDING MIGRATORY PATTERNS AND FORAGING ECOLOGY OF GREEN TURTLES Chelonia mydas IN THE GALÁPAGOS ISLANDS THROUGH STABLE ISOTOPES

Introduction

Green turtles (Chelonia mydas) are highly migratory species that regularly move between their foraging grounds and breeding areas (Bolten 2003) with distances up to thousands of kilometers (Limpus et al. 1992, Luschi et al. 1998). Sea turtles are capital breeders, while on their foraging grounds, both males and females must store sufficient fat to provide energy for migrations to and from the breeding grounds as well as for reproductive activities including production of eggs and construction of nests (Bjorndal

1982, Plot et al. 2013).

Migration distance between the foraging and the breeding grounds can affect reproductive output, as measured by parameters including remigration intervals, number of clutches per breeding season and eggs per clutch (Bjorndal 1982, Troëng &

Chaloupka 2007, Zbinden et al. 2010, Hawkes et al. 2011). Turtles that forage at greater distances from their breeding grounds, and thus have higher migration costs, may require longer periods of time to acquire sufficient nutrients resulting in longer intervals between breeding seasons (remigration intervals).

The Galápagos Islands, located 1000 km from mainland Ecuador, hosts one of the most important rookeries for green turtles in the East Pacific Ocean (Green 1994,

Zárate & Dutton 2002, Seminoff 2007). It is one of the few places in the world where a sea turtle nesting aggregation comprises both resident and migrant turtles (Green

1984b, 2003, Zárate 2007, Seminoff et al. 2008). Galápagos green turtles present a mosaic of migration strategies including residency in the Galápagos, north-bound

migration to Central America, east-bound migration to South America, and dispersal to oceanic waters southwest of the Galápagos (Green 1984b, Seminoff et al. 2008).

Galápagos nesting aggregations include individuals from multiple foraging grounds, often separated by hundreds or thousands of kilometers, similar to other green turtle populations (Green 1984b, Harrison & Bjorndal 2006).

The mechanisms that cause the intrapopulation variation in the choice to remain on foraging grounds in the Galápagos or migrate to areas out of the archipelago are unknown. A potential stimulus to migrate to distant foraging areas could be nutrient limitation in local foraging areas (Green 1984a, Zárate 2007). Growth rates of immature green turtles on Galápagos foraging grounds (Green 1993) are very slow compared to growth rates in similar–sized green turtles in other areas (e.g., Zug & Glor 1998,

Seminoff et al. 2002, Balazs & Chaloupka 2004b, Zárate et al. in prep) or the foraging grounds for Galápagos nesters may be a result of current-mediated dispersal

(Blumenthal et al. 2009, Gaspar et al. 2012).

In Galápagos, both resident males and females travel distances less than 300 km between their breeding and foraging grounds (Green 1984b, Zárate 2007), whereas green turtles migrating from Central to South American foraging grounds to breen in the

Galápagos must travel up to 2500 km (Green 1984b, Seminoff et al. 2008).

Considerably higher energetic costs accompany such long-distance migrations compared to those of resident turtles in Galápagos foraging grounds. Would resident turtles have higher reproductive output as a result? If residents and migrants turtles could be distinguished, green turtles in Galápagos would provide an excellent study site

for the effect of migration costs on the relative energetics and life history consequences for these two strategies.

Stable isotope analysis is a very useful tool for assessing migratory behavior of species with wide geographical ranges (Peterson and Fry 1987, Rubenstein & Hobson

2004). Foraging locations in marine ecosystems can be revealed by 13C values because of predictable variation that occurs along several gradients between inshore and offshore habitats, between benthic and pelagic habitats, and over latitudes. Values of 15N can be used to evaluate trophic levels as well as geographic location (Vander

Zanden et al. 2013a). In addition, different oceanographic processes can affect baseline values for both carbon (13C) and nitrogen (15N) in marine food webs resulting in isotope variation among locations within and among ocean basins (Ishibashi et al. 2000,

Takai et al. 2000, Wallace et al. 2006, Pajuelo et al. 2010, Seminoff et al. 2012, Vander

Zanden et al. 2013a). Therefore, baseline values for carbon (13C) and nitrogen (15N) in food webs is critical when studying migratory organisms that use widely disperse foraging areas (Vander Zanden et al. 2013a). Knowledge of diet-tissue discrimination factors, the offsets that occur between isotope values of food sources and the consumer, is also essential (Vander Zanden et al. 2012).

Stable isotopes have been used successfully to distinguish between sea turtles that leave nesting beaches and migrate to different locations. These studies include leatherbacks (Dermochelys coriacea) in Papua, Indonesia (Seminoff et al. 2012); loggerheads (Caretta caretta) in Japan (Hatase et al. 2010), and in the Northwest

Atlantic (Reich et al. 2010, Ceriani et al. 2012, Pajuelo et al. 2012a,b).

Based on the success of earlier studies that distinguished between various migration destinations, I wanted to evaluate the use of stable isotope values of 13C and

15N to distinguish between migrant and resident nesting females in Galápagos. For this approach to work, the stable isotope signatures of the different foraging ground destinations, which would be incorporated into sea turtle tissues, must be different. In this study, I collected skin samples from green turtles at four nesting beaches and three foraging grounds, as well as putative prey species from one foraging ground, in the

Galápagos, and analyzed all samples for 13C and 15N. The results were compared with stable isotope values available in the literature for green turtles in other eastern

Pacific foraging areas to determine whether we could identify individual nesting green turtles as residents or migrants. If residents and migrants females could be identified, the Galápagos nesting aggregation would provide an excellent case study for the effects of migration costs on reproductive output.

Materials and Methods

Study Sites

The study was carried out on three foraging grounds during 2004 and at four nesting beaches during 2003/04 nesting season (Fig.4-1). The foraging grounds were

Punta Espinoza (PE; 0.26° S, 91.44° W), and Bahía Elizabeth Lagoon (BE; 0.59° S,

91.07° W) and Caleta Derek Canal (CD; 0.64° S, 91.09° W). The nesting beaches were

Las Bachas (LB; 0.49° S, 90.33° W), Quinta Playa (QP; 1.00° S, 91.08° W), Bahía

Barahona (BB; 0.98° S, 91.03°W), and Las Salinas (LS; 0.47° S, 90.29° W).

The foraging sites of Bahía Elizabeth Lagoon and Caleta Derek Canal are only

5.4 km apart and both open onto the main Bahía Elizabeth (= Elizabeth Bay). Both sites

are characterized by calm shallow waters. Green turtles at these two feeding grounds exhibit a similar diurnal pattern of behavior; some turtles remain throughout the day to feed, whereas others leave in the early morning to feed along the more open coastal areas of Bahía Elizabeth, returning in the late evening to rest (Green 2003). Punta

Espinoza is a very exposed area facing strong water currents and tidal surge. Turtles at this site are commonly seen actively feeding all along the coast. In all three sites, juveniles, sub-adults and adults are present (Green 2003, Zárate 2007).

Of the four beaches studied, Quinta Playa has the highest green turtle nesting activity in the Archipelago (Green 1994, Zárate & Dutton 2002) hosting about 700 nesting females each year. Bahía Barahona, Las Bachas and Las Salinas usually have on average 470, 280 and 175 annual nesting females, respectively. For a more detailed site description of the nesting beaches see Zárate et al. (2013).

Sample Collection and Analyses

At foraging grounds, 106 green turtles were captured by hand and in entanglement nets (100 x 4 m, mesh size=50cm stretched) between February and

November 2004. A tag (Style 681 Inconel tags from National Band and Tag Company,

Newport, Kentucky) was applied to the proximal trailing edge of each front flipper.

Curved carapace length (CCL; ±0.1 cm) was measured from the nuchal notch to the posterior-most edge of the marginal scutes using a flexible measuring tape (Bolten

1999). Turtles were released at site of capture within 4 hrs. Only data for the black morph of green turtles is included in this study. Data for the yellow morph of green turtles found in the foraging grounds with black morph turtles (Green 1994, Zárate 2012) will be presented elsewhere.

At nesting beaches, 117 adult females were examined. Beaches were monitored every night for the entire nesting season (December-May). We double- tagged each turtle and measured CCL as described above.

We collected skin tissue from the dorsal surface of the neck of each turtle with a sterile 6-mm biopsy punch. Skin samples were frozen and later stored in 75% ethanol until preparation and analysis. Prior to analysis, skin samples were rinsed in distilled water, dried to constant weight for 48 h at 60C, and the epidermis layer was finely diced with a scalpel blade. Lipids were extracted from dried skin samples on a Soxhlet apparatus with a 1:1 solvent mixture of petroleum ether and ethyl ether for at least two

10-h cycles. Samples then were dried at 60 °C for 24 h to remove any residual solvent.

Approximately 1 mg of tissue was loaded into pre-cleaned tin capsules. Algae and red mangrove (Rhizopora mangle) samples were collected during 2004 at Bahía Elizabeth, dried at 60°C for 24 h, and homogenized to <1 mm using a Wiley mill; samples of 2.0 –

10.0 mg were loaded into tin capsules. All samples were combusted in a Costech ECS

4010 elemental analyzer interfaced via a ConFlo III device to a ThermoFinnigan Delta

Plus XL (Bremen, Germany) isotope ratio mass spectrometer. Sample preparation was performed in the Stable Isotope Laboratory at Southwest Fisheries Science Center

NOAA-NMFS at La Jolla, California. Elemental concentrations (%C, %N) as well as

13C and 15N analyses were performed at the Stable Isotope Laboratory in the

Department of Geology at the University of Florida, Gainesville.

Stable isotope ratios are expressed in delta () notation, defined as parts per thousand (‰) relative to the standard as follows:  = [(Rsample/Rstandard) – 1] x

(1,000), where Rsample and Rstandard are the corresponding ratios of heavy to light

isotopes (13C/12C and 15N/14N) in the sample and international standard, respectively.

13 Vienna Pee Dee Belemnite was used as the standard for C, and atmospheric N2, for

15N. The reference material USGS40 (L-glutamic acid) was used to normalize all results.

The standard deviation of the reference material was 0.11‰ for 15N and 0.08‰ for

13C.

The 13C and 15N values for green turtle skin tissue were compared among foraging areas, among nesting sites, and among all sites using one-way ANOVAs. If a significant difference was detected among sites, we used Tukey post-hoc comparisons to determine which sites were significantly different. To evaluate the effect of body size on isotopic values within foraging and nesting sites, we used Spearman’s rank- correlation coefficient or linear regression whenever sample size allowed. Convex hull polygons were drawn for foraging and nesting 13C and 15N values to visualize overlap and determine contribution from foraging grounds to nesting beaches. All results are presented as the mean  standard deviation. Statistical analyses were conducted using

JMP (Pro 9.0.2 64-bit Edition, SAS Institute Inc.) with an α level of 0.05.

The 13C and 15N values for plant material were averaged when more than one specimen of the same species was collected. Mean 13C and 15N values  SD were calculated by phylum. For red mangroves, individual values for stems, leaves and propagules from the same plant were obtained.

Results

On the foraging grounds, the skin 13C values of green turtles (n = 106) ranged from -24.8 to -12.1‰ (mean = -14.8 ± 2.6‰), and 15N ranged from 8.5 to 16.2‰ (mean

= 11.8 ± 1.3 ‰) (Fig. 4-2 and Table 4-1). Green turtles from Bahía Elizabeth and Caleta

Derek had greater ranges of 13C and 15N values than those found in Punta Espinoza

(Fig. 4-2 and Table 4-1). No significant differences were found in 15N values among foraging grounds (F2,103 = 2.7, P = 0.07), although the difference between Punta

Espinoza and Caleta Derek approached significance. Significantly higher values of 13C were found in Punta Espinoza compared to Caleta Derek and Bahía Elizabeth (F2,103 =

92.3, p < 0.001) (Fig. 4-2 and Table 4-1). There was no effect of body size (CCL) on

13  C in green turtles at any site (Spearman rank correlation, Bahía Elizabeth: rs = -0.3,

N = 32, P = 0.07; Caleta Derek: rs = -0.2, N = 33, P = 0.2; Punta Espinoza: rs = -0.2, N =

41, P = 0.3), and only turtles from Caleta Derek had a significant negative correlation

15 between body size and  N (Spearman: rs = -0.4, N = 33, P = 0.01; regression coefficient: r2 = 0.20, P = 0.01). None of the turtles examined at the foraging grounds appeared to be reproductively active; there were no fresh mating scars or mating activity. Four of the green turtles captured on foraging grounds had previously been tagged while nesting on Galápagos beaches.

Samples from 15 algae species were collected at Bahía Elizabeth in 2004. One red mangrove sample was collected from the site in 2011. Algal 13C values ranged from -28.3 to –8.7‰, and 15N values ranged from 5.2 to 7.2‰ (Table 4-2). No

13 significant differences were found in  C values among classes of algae (F2,12 = 3.5, P

= 0.06), although the difference between red algae and green algae approached significance. Mean 15N values among the three classes of algae were not significantly

13 different (F2,12 = 1.5, P = 0.3). Mangrove tissues tended to have lower values of  C and higher values of 15N, compared to those in algae (Table 4-2). All of these species

have been recorded in the diet of green turtles in the Galápagos (Green and Ortiz-

Crespo 1982, Carrión-Cortez et al. 2010, Zárate unpubl. data).

Isotopic values of algae, red mangrove, and green turtles from Bahía Elizabeth are presented in Figure 4-3. Mean 13C values of algae were similar to green turtle values. Compared to green turtles, red mangrove 13C values were ~11‰ lower. Mean

15N values of green turtles are 5.6‰, 6.3‰ and 5.6‰ higher than green, brown and red algae values from Bahía Elizabeth, respectively (mean difference is 5.7‰). (Tables

4-1 and 3; Fig. 4-3)

The nesting aggregation in Galápagos exhibited a large range in skin 13C and

15N values. Female 13C values ranged from -24.4 to -11.6‰ (mean = -16.2 ± 1.8 ‰) and 15N values ranged from 9.4 to 18.4‰ (mean = 12.7 ± 1.9 ‰) (Fig. 4-4 and Table 4-

1). No significant differences were found for 13C or 15N values among the beaches

13 15 ( C: F3,114 = 2.0, P = 0.1;  N: F3,114 = 1.7, P = 0.2, Fig. 4). Female body size was not

13 15 13 15 correlated with  C or  N ( C: rs = -0.02, N = 118, P = 0.8;  N: Spearman, rs =

0.14, N = 118, P = 0.1).

Significant differences were found in 13C and 15N among green turtles from

13 foraging grounds and females from nesting beaches ( C: F1,222 = 22.5 , P < 0.0001;

15 13  N: F1,222 = 15.2 , P = 0.0001). For  C values, turtles from the foraging ground of

Punta Espinoza had significantly higher values than females at all nesting grounds

15 (F6,323 = 67.3 , P < 0.0001; Fig. 4-5). Significantly higher  N values were found in

Quinta Playa compared to the three foraging grounds, and Bahía Barahona had higher

15  N values than Caleta Derek (F6,323 =6.5 , P < 0.0001, Fig. 4-5). There is great overlap of 13C and 15N values for nesting and foraging grounds represented by convex hull 95

polygons (Fig. 4-6). However, there are three areas where there is no overlap of the nesting polygon with the foraging polygons (Areas 1, 2 and 3). Area 1 (Punta Espinoza) and Area 2 (Caleta Derek) of the foraging polygons are not represented in the nesting population. Of all nesting females, 91.5 % are contained within the area of the foraging polygons. Females whose values did not fall within the foraging polygons (Area 3) were from three of the nesting beaches: Las Bachas (1.7%), Bahía Barahona (3.4%), and

Quinta Playa (3.4%).

Discussion

This is the first study to report stable isotopes values of 13C and 15N of green turtles at nesting and foraging grounds and their potential prey items in the Galápagos.

This study provides information on the foraging ecology of green turtles by the isotopic characterization of green turtles at three important foraging grounds and in four key nesting beaches in the Archipelago.

Isotopic Characterization of Galápagos Turtles on Foraging Grounds

The isotopic values in skin from turtles at the three foraging sites were similar except that 13C values were significantly higher at Punta Espinoza. These high 13C values may result from Punta Espinoza turtles consuming different species than the turtles on other foraging grounds or from consuming the same species that differ in isotopic values. Oceanographic conditions at Punta Espinoza, which is greatly impacted by upwelling (Alava 2009), could result in high 13C values of prey species. Upwelling produces phytoplankton blooms that decrease dissolved CO2 concentration. This

13 decrease in dissolved CO2 tends to reduce discrimination against  C during photosynthesis leading to higher 13C values (France 1995). Higher stable carbon

signatures have also been found in adult and juvenile Galápagos sea lions in areas affected by upwelling (Jeglinski et al. 2012).

Substantial variation was found in 13C and 15N values within each foraging ground. This variation may reflect individual dietary specialization of turtles at these sites, either in the diet items consumed or habitat differences (Vander Zanden et al.

2013a, 2013b). Although sea turtle aggregations at Bahía Elizabeth and Caleta Derek exhibit a high degree of site fidelity (Green 2003, Zárate 2007), they undertake daily movements in and out of these locations so they could be feeding in other areas as well and using these sites mainly as resting areas.

At the Bahía Elizabeth foraging ground, where both sea turtle skin tissue and plant material were analyzed, results obtained suggest that although algae and mangroves are extremely abundant in the bay, green turtles are not exclusively herbivorous. Because green turtles consuming marine algae and/or mangrove would be one trophic step from baseline primary producers, green turtle skin tissues theoretically should reflect one trophic level of enrichment in 15N (~4.0‰; Vander Zanden et al.

2012). Given that mean 15N of green, brown and red algae and mangroves in Bahía

Elizabeth are 6.4‰, 5.6‰, 6.3‰ and 6.8‰ respectively, green turtle skin 15N should be roughly 9.6‰ to 10.8‰ if they are exclusively herbivorous. However, the range for green turtles in Bahía Elizabeth was 10.2‰ to 16.2‰; thereby suggesting that some turtles are consuming higher-trophic-level foods. These results should be interpreted with caution because we are using a discrimination factor obtained from a different green turtle population on a different diet. Since discrimination factors may vary with species, tissue type, diet, and growth rate (Seminoff et al. 2006, Vander Zanden et al.

2012) appropriate discrimination factors in dietary reconstructions and trophic-level estimations for Galápagos green turtles are needed.

The conclusion that green turtles are not exclusively herbivorous is consistent with earlier studies. Based on esophageal contents, Galápagos green turtles feed primarily on about 30 different algae species and on the leaves and bark of red mangrove (Green 1994; Carrión-Cortez et al. 2010), but they do consume animal matter. Esophageal contents of green turtles analyzed from Bahía Elizabeth, Caleta

Derek and Punta Núñez in 2006 revealed 8.8% (by volume) of animal matter (Carrión-

Cortéz et al. 2010) represented by siphonophores (Hydrozoa), sea jellies (Sciphozoa), roundworms (Nematoda), polychaetes (Annelida), snails (Gastropoda) and amphipods

(Hyperiidae). Sea jellies have also been observed in gut contents in other years (Zárate unpubl. data). This finding is not surprising; green turtles have been known to feed on animal matter for many years, particularly in the eastern Pacific (references in Bjorndal

1997, Jones & Seminoff 2013).

Isotopic Characterization of Galápagos Turtles on Nesting Beaches

We found no significant differences among nesting beaches for either 13C or

15N values. Similar to the findings in foraging areas, a wide range of 13C and 15N isotopic values was found at nesting beaches. In addition to differences in diet, a probable explanation for the large variation of 13C and 15N is the variability in isotope baseline values of the various foraging grounds at which nesting females resided prior to their nesting. Baseline differences due to spatial variation in the primary producer greatly influence green turtle 13C and 15N values. Because females nesting in

Galápagos use foraging areas within and outside the Galápagos, the isotopic values

could reflect the location of the foraging area rather than differences in their diet. For example, the range of nitrogen isotopic values was 9.0 ‰ among nesting turtles (Table

4-1), broader than that expected for a specialist consumer. However, similarly a broad range in 15N values for green turtles nesting at Tortuguero, Costa Rica, resulted from geographic variation in stable isotope baselines among the foraging grounds rather than feeding across trophic levels (Vander Zanden et al. 2013a).

Isotopic composition of green turtles overlapped considerably between

Galápagos nesting beaches and foraging grounds, as expected. The use of Galápagos foraging grounds by Galápagos nesting females (residents) has been recorded in previous studies (Green 2003, Zárate 2007, Seminoff et al. 2008, Zárate unpubl. data)

(Table 4-3). In this study, we recorded two nesting females from Las Bachas foraging in

Caleta Derek, and one from Bahía Barahona and another from Quinta Playa foraging both in Punta Espinoza (Table 4-3).

The low representation of Punta Espinoza turtles in the nesting beach polygon

(Area 1; Fig. 4-6) could result from three causes. Punta Espinoza turtles (1) nest at a

Galápagos nesting beach not included in this study, 2) nest at beaches outside the

Galápagos, 3) move to other foraging grounds prior to nesting Punta Espinoza and, (4) turtles are all adults that move to other foraging grounds prior to nesting. The few beaches in the vicinity of Punta Espinoza have not been monitored due to their low nesting activity. Turtles travel up to 300 km between foraging grounds and nesting beaches within the Archipelago (Green 2003) so Punta Espinoza turtles could nest on beaches at considerable distances from Punta Espinoza. Of the 190 beaches in

Galápagos 56% are known to have nesting activity (Pritchard 1975, Zárate pers. obs.).

Nesting by Punta Espinoza turtles on beaches outside Galápagos is less probable. No foraging turtles tagged within Galápagos have ever been reported nesting outside the

Archipelago. The movement of many turtles away from Punta Espinoza to other foraging grounds for a sufficient period of time prior to nesting to lose the Punta

Espinoza isotope signature is also unlikely. Punta Espinoza turtles range in size from

53.5 to 99.5 cm of CCL (Table 4-1), including immatures and adults. Tag and recapture of turtles feeding at Punta Espinoza have shown that there is a high degree of fidelity

(Green 2003, Zárate 2007), and of the 166 green turtles tagged at Punta Espinoza, none has been recaptured at another foraging site (Zárate unpubl.data). Site fidelity to their foraging grounds has also been observed in other green turtle populations such as those from Southeast Queensland, Australia (Arthur et al. 2008), and Cyprus (Broderick et al. 2007).

Based on the isotope polygons, some of the foraging turtles from Caleta Derek fell below the 15N values of the nesting population in Galápagos, which was a result of three outliers (Area 2; Fig. 4-6). This is also suggesting that some of the turtles that forage in Caleta Derek are nesting in beaches not sampled on this study. With more sampling on the nesting beaches, the nesting polygon may well expand to encompass all of the foraging ground polygons.

Most nesting females (92%) examined in this study had isotopic values within the range found for turtles in foraging areas. The area of the nesting beach polygon that does not overlap with the foraging ground polygon (Area 3; Fig. 4-6) either represents foraging grounds within the Galápagos that we have not sampled, or turtles that come from foraging grounds outside of Galápagos to nest in Galápagos.

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Distinguishing between Resident and Migrant Nesting Females

Although some green turtles that nest in the Galápagos are residents on foraging grounds within the Archipelago, other Galápagos nesters forage in other areas. Based on flipper tags (Hays-Brown & Brown 1982, Green 1984b, Aranda & Chandler 1989,

Bello et al. 2001, Paniagua 2013), satellite telemetry (Seminoff et al. 2008), we know that some Galápagos green turtles travel thousands of kilometers to reach neritic foraging areas along the coasts of Central and South America from Nicaragua to

Ecuador. Genetic analysis suggests that Galápagos green turtle can also be found in northern Chile and in Colombia. Some turtles foraging at Mejillones, Chile and Gorgona

Island, Colombia originate from Galápagos, based on the presence of unique haplotypes identified in the female nesting population from the Archipelago (Amorocho et al. 2012, Donoso & Dutton 2002, Dutton et al. unpubl. data). Tagging sites recorded in Table 4-4 are nesting beaches except Turtle Cove, a small lagoon in the vicinity of several nesting beaches, where tagged individuals were found copulating (Green

1984b). In addition to these neritic foraging sites, satellite telemetry revealed that some females that nest in Galápagos may forage in oceanic habitats (Seminoff et al. 2008).

Stable isotope values were available for green turtles from five foraging areas in the eastern Pacific (Fig. 4-7). The mean 13C and 15N values from each site falls within the range of values recorded for green turtles on Galápagos foraging grounds. This similarity of values is confirmed by the convex hull polygons for the three foraging grounds for which we had individual data (Fig. 4-8). Because of this extensive overlap, I conclude that stable isotope values cannot be used to distinguish between resident and migrant nesters in Galápagos. In addition, a scatter plot of stable isotope values for all

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nesting turtles in Galápagos reveals no clear clusters as has been found in other nesting beach populations with bi-modal foraging strategies (Hatase et al. 2010, Reich et al. 2010, Zbinden et al. 2010, Seminoff et al. 2012).

Although this study has provided valuable knowledge about green turtle isotopic composition in foraging and nesting grounds of the Galápagos Islands, additional studies integrating stable isotope analysis with long term foraging ecology and movement data (satellite telemetry or flipper tagging) are recommended to increase our understanding of turtle foraging ecology, population dynamics, and functional roles.

Distinguishing between resident and migrant nesters in Galápagos remains an important goal for understanding the relative energetics and life history consequences for these two strategies. Other techniques to make this distinction, such as trace elements (López-Castro et al. 2013), should be tested.

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Table 4-1. Mean values and standard deviation values for 13C, 15N, CCL (cm) for green turtles Chelonia mydas by year and site collected at foraging and nesting grounds in the Galápagos Islands. See Fig. 1 for Location. FGs = foraging grounds; NGs = nesting beaches. 13C (‰) 15N(‰) CCL (cm) Location Year Site N Mean(SD) Range Mean(SD) Range Mean(SD) Range FG 2004 BE 32 -16.2(1.3) -18.7 to -12.6 11.9(1.2) 10.2 to 16.2 67.5(11.5) 46.5 to 87.9 FG 2004 CD 33 -16.7(2.1) -24.8 to -12.1 11.4(1.7) 8.5 to 14.5 70.7(12.4) 47.3 to 94.5 FG 2004 PE 41 -12.3(1.1) -15.7 to -10.7 12.1(0.8) 9.6 to 13.9 71.4(9.5) 53.5 to 99.5 All FGs 2004 All FGs 10 -14.8(2.6)) -24.8 to -10.7 11.8(1.3) 8.5 to 16.2 70.0(11.1) 46.5 to 99.5 NG 2003/04 BB 436 -16.3(1.4) -20.4 to -12.4 12.5(1.9) 10.1 to 17.7 82.5(4.2) 75.5 to 94.0 NG 2003/04 LB 8 -17.5(3.3) -24.4 to -14.9 12.6(2.8) 9.4 to 16.2 86.2(5.1) 82.9 to 94.4 NG 2003/04 LS 19 -16.3(1.4) -20.6 to -13.1 12.1(0.9) 10.0 to 13.5 82.1(4.3) 75.7 to 90.0 NG 2003/04 QP 48 -15.9(1.8) -21.8 to -11.6 13.1(2.1) 9.5 to 18.4 85.6(6.1) 71.7 to 98.0 All NGs 2003/04 All NGs 11 -16.2(1.8) -24.4 to -11.6 12.7(1.9) 9.4 to 18.4 83.9(5.3) 71.7 to 98.0 8

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Table 4-2. Isotopic values of 13C and 15N of algae and mangrove specimens collected at Bahía Elizabeth in 2004. Values are presented as mean (SD). Specie Phylum n 13C (‰) 15N (‰) Caulerpa racemosa Chlorophyta 1 -17.5 6.7 Chaetomorpha sp. Chlorophyta 1 -8.7 6.1 Codium sp. Chlorophyta 1 -11.6 6.2 Enteromorpha sp. Chlorophyta 1 -12.7 7.0 Ulva lactuca Chlorophyta 1 -11.6 6.0 All Chlorophyta 5 -12.4(3.2) 6.4(0.4) Dictyota sp. Phaeophyta 1 -14.2 5.8 Padina sp. Phaeophyta 1 -12.6 5.7 Sargassum sp. Phaeophyta 1 -16.8 5.2 All Phaeophyta 3 -14.5(2.1) 5.6(0.3) Ceramium sp. Rhodophyta 1 -14.9 7.2 Cryptopleura sp. Rhodophyta 1 -28.3 6.2 Gymnogongrus sp. Rhodophyta 1 -16.8 7.1 Halopteris sp. Rhodophyta 1 -19.4 5.1 Hypnea sp. Rhodophyta 1 -14.6 7.2 Polysiphonia sp. Rhodophyta 1 -23.8 6.2 Scinaia sp. Rhodophyta 1 -17.5 5.2 All Rhodophyta 7 -19.3(5.0) 6.3(0.9) Rhizophora mangle (stems) Tracheophyta 1 -27.3 5.8 Rhizophora mangle (leaves) Tracheophyta 1 -27.1 6.3 Rhizophora mangle (propagules) Tracheophyta 1 -27.5 8.4 *Red mangrove sample was collected on 2011.

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Table 4-3. Recapture data for 10 female green turtles tagged in the Galápagos Islands between 2002 -2005 and recaptured within Galápagos waters to date. See Fig. 1 for Tagging Site codes. Year of Year of Tagging site Tag # Recovery site Reference tagging recovery BB LP491 2003 Punta Espinoza, Fernandina Is. 2004 This study BB LP206 2003 Punta Espinoza, Fernandina Is. 2004 Zárate (2007) LB 866J 2002 Caleta Derek, Isabela Is. 2004 This study LB 716K 2002 Caleta Derek, Isabela Is. 2004 This study LB J649 2002 Punta Núñez, Santa Cruz Is. 2006 Zárate (2007) LS LR431 2003 Punta Núñez, Santa Cruz Is. 2005 Zárate 2007 LS LR780 2004 Bahía Elizabeth, Isabela Is. 2008 Zárate unpubl. data QP LP850 2003 Punta Espinoza, Fernandina Is. 2004 This study QP LO783 2005 Northern Santa Cruz Is. 2005 Seminoff et al. (2008) QP LO849 2005 Floreana Is. 2005 Seminoff et al. (2008) Turtle Cove, LN104 2003 Las Bachas, Santa Cruz Is. 2003 (Zárate 2007) Santa Cruz Is.

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Table 4-4. Recapture data for 45 turtles tagged in the Galápagos Islands between 1970 -2012 and recaptured outside of Galápagos waters to date. See Fig. 1 for Tagging Site codes. Year of Year of Tagging site Tag # Sex Recovery site Reference tagging recovery BB A1964 F 1973 Golfito, Costa Rica 1974 Green (1984b) Z1948 Hays-Brown & Brown BB F 1978 Pisco, Perú 1979 (1982) Z2047 Hays-Brown & Brown BB F 1978 Pisco, Perú 1979 (1982) BB Z3901 F 1979 De la Plata Is., Ecuador 1979 Green (1984b) BB LO908 F 2005 Gulf of Chiriquí, Panamá 2005 Seminoff et al. (2008) BB GAL636 F 2009 Jiquilisco Bay, El Salvador 2010 Paniagua (2013) GAL1885 FCD/Velez-Suazo (pers F El Ñuro, Perú 2012 BB 2010 comm) DC235 FCD Bulletin/WWF LB F 2004 Off Gulf of Panamá, Panamá 2007 (pers. comm) LS 6282 F 1975 Coronado Bay, Costa Rica 1975 Green (1984b) LS Z978 F 1976 Canal del Morro, Ecuador 1978 Green (1984b) LS Z1541 F 1977 San Lorenzo Is., Perú 1979 Green (1984b) Z1582 Hays-Brown & Brown LS F 1977 Pisco, Perú 1979 (1982) Z2482 Hays-Brown & Brown LS F 1978 Pisco, Perú 1978 (1982) Z2739 Hays-Brown & Brown LS F 1978 Pisco, Perú 1979 (1982) LS Z2587 F 1978 Gulf of Panamá, Panamá 1978 Green (1984b) 3578 Hays-Brown & Brown Northern Santa Cruz Is. F 1970 Pisco, Perú 1978 (1982) QP Z145 F 1976 Coiba Is., Panamá 1978 Green (1984b)

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Table 4-4. Continued Year of Year of Tagging site Tag # Sex Recovery site Reference tagging recovery QP Z88 F 1976 Puerto Bolivar, Ecuador 1978 Green (1984b) QP Z1006 M 1977 925 km off Perú 1979 Green (1984b) QP Z1293 F 1977 Coiba Is., Panamá 1979 Green (1984b) QP Z1005 F 1977 Coiba Is., Panamá 1978 Green (1984b) QP Z1087 F 1977 Punta Galera, Ecuador 1977 Green (1984b) QP Z1088 F 1977 Santa Rosa, Ecuador 1978 Green (1984b) Z2298 Hays-Brown & Brown QP F 1978 Pisco, Perú 1979 (1982) Z2228 Boca de Buenaventura, QP F 1978 1978 Green (1984b) Colombia QP GF616 F 2005 Gulf of Panamá, Panamá 2005 Seminoff et al. (2008) QP LO879 F 2005 Gulf of Fonseca, Nicaragua 2005 Seminoff et al. (2008) QP GAL2339 F 2010 Jiquilisco Bay, El Salvador 2010 Paniagua (2013) * FCD/Chacón QP F 2010 Costa Rica 2010 (pers.comm) Turtle Cove, Santa Cruz Z1831 M 1977 San Andrés, Perú 1979 Green (1984b) Is. Turtle Cove, Santa Cruz Z1716 Gulf of Papagayo, Costa M 1977 1978 Green (1984b) Is. Rica * * F * San Andrés, Perú 1980 IMARPE (pers. comm) * * F * San Andrés, Perú 1980 IMARPE (pers. comm) Hays-Brown & Brown * 376 M * Pisco, Perú 1979 (1982) * * * * Callao, Perú 1979 IMARPE (pers. comm) Zone between Quilca and * * * * 2001 Bello et al. (2001) Canana, Perú

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Table 4-4. Continued Year of Year of Tagging site Tag # Sex Recovery site Reference tagging recovery x x x x Callao, Perú 1979 IMARPE (pers. comm.) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) x Aranda & Chandler x x x Piura, Perú 1989 (1989) * information not available but these turtles were tagged between 1970 and 1979 by Derek Green. x information not available, these turtles were captured by Peruvian fishermen. FCD=Charles Darwin Foundation (Galápagos Islands, Ecuador). WWF= World Wildlife Fund, Ecuador. IMARPE=Instituto del Mar del Perú (Peruvian Seas Institute).

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Pinta Caribbean Sea

Marchena

Ecuador

Santa Cruz Pacific Ocean

PE Isabela Santiago

Fernandina LS Baltra LB

BE CD

Santa Fé BB San Cristóbal QP

Española Floreana

Figure 4-1. Map of 3 foraging grounds (circles) and 4 nesting beaches (stars) where green turtles were sampled. Algae and mangrove samples were collected at the Bahía Elizabeth foraging ground. BE=Bahía Elizabeth, CD=Caleta Derek, PE=Punta Espinoza, BB = Bahía Barahona, LB = Las Bachas, LS = Las Salinas, QP = Quinta Playa.

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A 20 BE 18 n=32

16 N(‰)

15 14  12

8 -26 -24 -22 -20 -18 -16 -14 -12 -10

13C(‰) B 20 CD 18 n=33

16 N(‰)

15 14  12

8 -26 -24 -22 -20 -18 -16 -14 -12 -10

C 13C(‰)

20 PE 18 n=41

16 N(‰)

15 14  12

8 -26 -24 -22 -20 -18 -16 -14 -12 -10

13C(‰) Figure 4-2. Isotopic values of 13C and 15N of individual green turtles at foraging grounds in the Galápagos Islands. A) Bahía Elizabeth (BE), B) Caleta Derek (CD), and C) Punta Espinoza (PE).

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green turtle Rhodophyta Mean green turtle Phaeophyta Chlorophyta Tracheophyta-stems Tracheophyta-leaves Tracheophyta-propagules 18

16 N(‰)

15 14 

4 -30 -26 -22 -18 -14 -10 -6

13C(‰) Figure 4-3. Stable isotope mean and individual values for green turtles (not corrected for trophic discrimination) and mean isotope values for potential prey at Bahía Elizabeth. 13C and 15N values for stems, leaves and propagules of red mangrove (Tracheophyta) correspond to the same plant. Bars represent standard deviation.

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A B

C D

Figure 4-4. Values of 13C and 15N of individual green turtle nesting females at nesting grounds of the Galápagos Islands. A) Las Salinas (LS), Las Bachas (LB), Bahía Barahona (BB), and Quinta Playa (QP).

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Figure 4-5. Mean 13C and 15N values for green turtles from foraging grounds (solid symbols) and females from nesting beaches (open symbols) of the Galápagos Archipelago. Bars represent standard deviation. BE=Bahía Elizabeth, CD=Caleta Derek, PE=Punta Espinoza, BB = Bahía Barahona, LB = Las Bachas, LS = Las Salinas, QP = Quinta Playa.

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Figure 4-6. Convex polygons representing 13C and 15N values of individual green turtles on nesting (dashed black line) and foraging grounds (colored lines) in Galápagos. BE=Bahía Elizabeth, CD=Caleta Derek, PE=Punta Espinoza.

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Figure 4-7. Mean 13C and 15N values for green turtles from all Galápagos nesting grounds (NGs, open circle) and local foraging grounds (open symbols) and, from foraging areas in the eastern Pacific Ocean. FG-BE= Bahía Elizabeth foraging ground; FG-CD= Caleta Derek foraging ground; FG-PE= Punta Espinoza foraging ground; GD=Golfo Dulce and CI=Cocos Islands, Costa Rica (Heidemeyer et al. unpubl. data); GI=Gorgona Island, Colombia (Seminoff & Amorocho unpubl. data), PAR=Paracas, Perú (Seminoff & de Paz unpubl. data); POC=Oceanic, Perú (Kelez 2011). Bars represent 1 standard deviation.

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Figure 4-8. Convex polygons representing 13C and 15N values of individual green turtles on Galápagos nesting (dashed black line) and foraging areas (solid black line) and individual foraging areas in the eastern Pacific Ocean (colored lines). GI=Gorgona Island, Colombia; PAR=Paracas, Perú; POC=Oceanic, Perú.

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CHAPTER 5 GROWTH OF GREEN TURTLES AND HAWKSBILLS IN THE GALÁPAGOS ISLANDS

Introduction

Knowledge of somatic growth rates of sea turtles is critical for our understanding of habitat quality and demography of these endangered species. Growth rates are a valuable estimate of the quality of areas in which sea turtles occur because growth integrates such factors as temperature and diet quality and quantity (Wood & Wood

1981, Bjorndal 1985, Diez & Van Dam 2002), population density (Bjorndal et al. 2000,

Balazs & Chaloupka 2004b, Kubis et al. 2009), predation pressure (Heithaus et al.

2007), and disease status (Chaloupka & Balazs 2005).

Age at sexual maturity was identified by the National Research Council (2010) as one of the most critical demographic parameters needed to improve assessment of sea turtle populations. Because age at sexual maturity in sea turtles is most often estimated from growth rates (Avens & Snover 2013, Bjorndal et al. 2013), improving our understanding of growth is essential.

In the Galápagos Islands, the green turtle Chelonia mydas is the most abundant sea turtle species and is the only turtle species that nests on the islands (Green 1994,

Zárate 2012). Two distinctive morphs of C. mydas co-exist on foraging grounds: the typical dark form, or “black turtle,” and a rare “yellow turtle” form with orange-brownish carapace and yellow-orange plastron (Pritchard 1971, Fritts 1981). While the black morph represents a distinct genetic stock for the Galápagos Islands (Dutton & Zarate unpubl. data), the yellow morph is from rookeries in the Indo-Pacific (Amorocho 2009,

Dutton & Zárate, unpubl data). The hawksbill turtle, Eretmochelys imbricata, although

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not abundant in the Galápagos Islands, is the second most common sea turtle species found at foraging grounds (Green 1994, Zárate 2007).

Growth rates of green turtles (Chelonia mydas) in the waters of the Galápagos

Archipelago reported by Green (1993) are among the slowest ever reported for immature green turtles. Green’s study was based on a relatively small sample size, included growth intervals as short as 8 months, and discarded negative growth rates. As part of a larger study of the ecology of green turtles in the Galápagos, we were able to collect additional growth data from 2003 through 2008 for both color morphs (black and yellow) of green turtles.

In this study, the effect of color morph, body size, recapture interval, year and site of captures on growth rates were evaluated. Growth rate results were compare with the earlier results of Green (1993) and with growth rates reported for green turtles in other regions and discuss possible causes of the slow growth rates in Galápagos green turtles. Finally, we present a few data for growth in hawksbills.

Growth rates can be used as a good indicator of overall turtle population health and provide a baseline with which to compare the quality of, or change in the foraging habitat condition. Growth rates are also essential information for conservation management plan.

Materials and Methods

Study sites

This analysis is part of an ongoing study of sea turtles at four foraging grounds in the Galápagos Marine Reserve, located about 1000 km from mainland Ecuador (Plan de Manejo de Conservación y Uso Sustentable para la Reserva Marina de Galápagos

1999). The foraging grounds were Punta Espinoza (PE; 0.26° S, 91.44° W), Bahía

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Elizabeth Lagoon (BE; 0.59° S, 91.07° W), Caleta Derek Canal (CD; 0.64° S, 91.09° W) and Punta Núñez (PN; 0.74° S, 90.25° W) (Fig. 1).

At each foraging ground between December 2000 to December 2008, turtles were captured by hand and in entanglement nets (100 x 4 m, mesh size=50cm stretched). A tag (Style 681 Inconel tags from National Band and Tag Company,

Newport, Kentucky) was placed on the proximal trailing edge of each front flipper.

Straight carapace length (SCL; ±0.1 cm) was measured from the nuchal notch to the posterior-most edge of the marginal scutes (Bolten 1999) with calipers. Body mass (kg) was also recorded for each turtle. Turtles were released at site of capture.

Bahía Elizabeth lagoon is comprised of a series of inner connected channels or small lagoons that opens by a narrow channel to Elizabeth Bay, located in the central western coast of Isabela Island (Fig. 5-1). The lagoon is surrounded by vegetation, mainly red mangroves Rhizophora mangle. Inner channels have a depth less than 10 m and a muddy bottom where green turtles can be observed resting. The adjacent coastal area of Elizabeth Bay is mainly rocky and covered with the green alga Ulva spp. and other turf algae (eg, Polysiphonia sp.).

Caleta Derek canal is located in the central western coast of Isabela Island (Fig.

5-1) (surrounded by lava rock with almost no vegetation on its borders. It is a long (650 m) and narrow canal (15 m) that leads to a small pond (ca. 500m2) not deeper than 5 m.

Caleta Derek canal has a rocky bottom with small patches of green and red algae; adjacent coastal areas have vast underwater platforms with a greater diversity and abundance of Ulva spp. and macroalgae. The terminal pond is comprised of rocks with

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almost no vegetation where sea turtles can be found on the bottom resting throughout the day.

Punta Núñez is a small bay (1500 m2) of calm and shallow waters not deeper than 15 m in the southeast of Santa Cruz Island (Fig. 5-1). The entrance of the bay is exposed to strong currents and wave action. The vegetation that surrounds the bay is composed of small patches of red and white (Laguncularia racemosa) mangroves, arid- adapted vegetation, and the cacti Opuntia. The bay has mixed patches of algae; the most abundant and common is the green alga Caulerpa occidentalis in association with red algae such as Hypnea sp., Gelidium sp., and other filamentous red algae. Turtles at this site are always feeding and in constant movement.

Punta Espinosa is a foraging area of approximately 700 m2 just off the northeast coast of Fernandina Island (Fig. 5-1). Turtles aggregate to feed all along the rocky bottom that has strong surge and wave action. Water depth ranges from 5 to 20 m. The seafloor is covered with the green algae Ulva spp., abundant patches of Sargassum spp., and other macroalgae species. Punta Espinoza’s shoreline has dense stands of red and white mangroves. Turtles actively feed and swim in this area.

Growth rates values were obtained for both black and yellow morphs at Bahía

Elizabeth and Caleta Derek. Growth rates were obtained only for the black morph at

Punta Espinoza and only for the yellow morph at Punta Núñez. Hawksbill turtles were only captured at Punta Núñez.

Analyses

Growth rates were calculated only for recapture intervals > 11 months to minimize errors in growth rate estimation (Chaloupka & Musick 1997). Negative growth rates, which almost certainly result from measurement error or carapace damage, were

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included in the analyses. We used a mixed longitudinal sampling design (sampling with partial replacement) with 6 of the 47 individual turtles recaptured twice. As with most sea turtle studies, age of the turtles was not known, thus year and cohort effects are confounded. Year was included as a covariate despite the confounding of environmental and cohort effects.

We modeled somatic growth statistically using generalized additive models

(GAM). Our models have 1 response variable (somatic growth rate, either SCL or mass) and 5 potential growth covariates. Three covariates are continuous (mean body size

[either SCL or mass], year, and recapture interval) and two are factors (turtle morph

[black or yellow] and capture site. Mean body size is the arithmetic mean of either SCL or mass at initial capture and recapture. Year is assigned as the calendar year of the midpoint of the recapture interval. Recapture interval is number of days between captures.

The GAM had an identity link, a quasilikelihood error function, and cubic smoothing splines. In GAM analyses, each covariate is conditioned on all other covariates. The significance of the contribution of each covariate to the overall model fit was evaluated with t ratio statistical inference. Significant covariates were evaluated for nonlinearity using a nonparametric F ratio test. The value of R2 was calculated as (null deviance – residual deviance)/null deviance.

We used S-Plus software (TIBCO Spotfire S+ Version 8.2.0) for GAM analyses.

We used alpha = 0.05 for all analyses.

Results

A total of 1065 green turtles were captured at foraging grounds during this study. Size distribution at all foraging grounds included juveniles and adults (Fig. 5-2) but

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differences in number and size ranges were found when comparing among black and yellow morphs. SCL of black and yellow morph turtles range from 40.7 to 98.5 (63.1±10; n = 850) and from 39.0 to 95.7 (63.9±16.4; n = 85), respectively. Black morph turtles were more abundant than yellow morph turtles at all sites except at Punta Núñez (Fig.

5-2).

We measured 41 growth increments in SCL for black morph turtles and 12 for yellow morph turtles. Forty growth increments in mass were measured for black morphs and 10 for yellow morphs. Mean min and max growth rates for black morph turtles were

0.03±0.4 cm/yr and 0.4±0.5 cm/yr, while in yellow morph turtles, mean min growth rate was 0.8±0.4 cm/yr and mean max growth rate was 1.5±0.6 cm/yr (Table 5-2).

When black and yellow morphs were analyzed together for SCL growth, the model accounted for 73.1% of the variation (Table 5-1a, Fig. 5-3). The only significant covariates for SCL growth were morph and site, with turtles at Punta Espinoza having significantly higher growth rates than the other sites. Mean SCL approached significance (t = -1.928, critical value of t = 2.028 for alpha of 0.5).

Because of the strong effect of morph on the SCL growth function, we repeated the analysis with only data for the black morph (Table 5-1b, Fig. 5-4). This model accounted for 59.8% of the variation in black morph turtle SCL growth rates. When considering only black morph turtle SCL growth rates, mean SCL was a significant, linear covariate and site was again significant with high values for turtles at PE. Neither of the SCL models was overdispersed.

For mass growth rates (Table 5-1c, Fig. 5-5), the GAM accounted for 59.0% of the variation in black and yellow turtle morph growth rates and was overdispersed.

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Although there was a trend for yellow morphs to grow more rapidly than black morphs, the difference was not significant, which was surprising given the strength of the effect on SCL growth. Mean mass was a significant, linear covariate. Two sites (Punta

Espinoza and Punta Núñez) were significantly higher than the other sites.

Six hawksbill turtles were captured during the study period, and growth rate values were measured for three hawksbill turtles each captured two times at Punta

Núñez. Growth rate values for individuals with a mean SCL of 46.9, 63.6 and 70.7 cm were 7.9, 2.4 and 4.4 cm/yr, respectively. Growth rates for individuals with a mean mass of 15.0, 29.6 and 40.0 kg were 2.7, 4.6 and 0 kg/yr, respectively.

Discussion

The present study is the first to evaluate the effect of several variables on the somatic growth rate of green turtles in the Galápagos Islands. In addition, this study provides first information on growth rate of hawksbill turtles for the eastern Pacific

Ocean.

Five major findings are derived from this study of sea turtle growth rates within the Galápagos Archipelago. First, for black and yellow morph combined, size did not have a significant effect on SCL growth rates but it did have a significant effect on mass growth rates.For black morph alone, size had a significant linear effect on SCL growth rates. Second, significant spatial variability in green turtle growth rates is revealed among foraging areas. Third, yellow morphs grew significantly faster than black morphs in length but not in mass. Fourth, findings of Green (1993), showing that green turtles in

Galápagos exhibit the slowest growth rates recorded for similar-sized green turtles anywhere in the world, were confirmed. Fifth, hawksbills, based on only 3 individuals, grow considerably faster than green turtles of the same size in Galápagos.

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Effect of Body Size on Growth Rates

Mean body size had a significant linear effect on SCL growth in black morphs, but not on black and yellow morphs combined. Although growth in black turtles appears to increase with SCL in small and large black turtles (<55 cm mean SCL and >70 cm mean SCL; Fig. 5-5A) the only significant part of the size-specific growth function is the declining growth from 55 to 70 cm mean SCL thus revealing a monotonic pattern of growth. The small sample sizes and the great variation in growth rates in this study underscore the need for further research. In particular, additional growth data for small and large size classes are needed to evaluate the growth function over the entire size range.

Green (1993) observed a similar growth function for SCL in green turtles on the same foraging areas in Galápagos as in this study. Growth rates reported by Green

(1993) are either similar to or higher than those we report. The decline in reported growth rates could result from changing conditions or because Green (1993) overestimated his growth rates by excluding negative growth rates. If negative growth rates are removed from the analyses, the mean growth rates for black morphs increase to 0.5, 0.2 and 0.2 cm/yr for 51 - 60 cm, 61 - 70 cm and 71 - 80 cm size classes, respectively. These values are similar to those reported by Green (1993).

Non-monotonic patterns with a single maximum growth rate appear to be characteristic of green turtle populations in the Pacific Ocean. Seminoff et al (2002) showed that growth rates of green turtles from Bahía de Los Angeles increase with increasing carapace length from around 55 cm SCL to maximum values between 80-90 cm SCL, before declining to negligible growth in the large adult classes. Australian

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green turtles from the Great Barrier Reef present a same pattern, but they peaked at smaller sizes (ca. 60-70 cm CCL; Chaloupka et al. 2004). Balazs & Chaloupka (2004) reported non-monotonic growth rate functions that reflect an immature growth spurt for green turtles on Hawaiian foraging grounds. Additional data for the Galápagos, particularly for turtles smaller than 50 cm SCL, are needed to determine if growth spurt is also present on Galápagos green turtles.

Body mass has a significant linear effect (monotonic function) on growth of green turtles in the Galápagos. Growth rate decreases with increasing body mass and then levels off at sexual maturity (ca. 70 kg). In green turtles from Culebra, Puerto Rico, body mass increased at a mean annual rate of 4.65±0.68 kg with larger increments in larger turtles (Collazo et al. 1992). A non-monotonic growth function for green turtles in the southern Bahamas (Bjorndal et al. 2000) and in Hawaii (Balazs & Chaloupka 2004) was found. Mass-specific growth rates of green turtles in both the Bahamas and Hawaii are greatest at similar body mass. An inmmature growth spurt at 20 kg and at ca. 23-35kg was observed in the Bahamas and in Hawaii foraging grounds, respectively before declining to negligible growth approaching the onset of sexual maturity. In other sea turtles species, such as in hawksbills from Mona and Monito Is., Puerto Rico, mass growth rates exhibited a monotonous rise until dipping slightly around 50 cm SCL with a less consisten patterns shown in larger turtles (Diez & vanDam 2002). Mean growth mass rates of green turtles from the Bahamas, Hawaii and Puerto Rico, and from hawksbill turtles in Puerto Rico, were faster than the ones found in green turtles from

Galápagos on this study.

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Temporal and Spatial Variation in Growth Rates

Ulva spp. and red mangroves (leaves and/or propagules) are always present in the diet of turtles in all four sites. However, the proportions at which these prey items are consumed differ substantially among sites. Ulva spp. and red mangrove represent

26.1% and 4.8% of the stomach content volume of green turtles at Bahía Elizabeth,

79.5% and 0.1% at Caleta Derek, 81% and 0.2% at Punta Espinoza and, a 9.6% and

0.5% at Punta Núñez, respectively (Carrión -Cortez 2008, Zárate unpubl. data).

Although diet algae proportions differ between Bahía Elizabeth and Caleta Derek, growth rates are similar, perhaps due to the presence of the same algae species in the diet of green turtles at both sites (Carrión -Cortez et al. 2010) and the close proximity

(ca. 5km) of the two sites. Diets of turtles from these two sites are composed mainly of

Ulva spp, Polysiphonia spp. and Gelidium spp. (Carrión-Cortez et al. 2010). The main diet components at Punta Espinoza are Ulva spp., Gelidium galapagensis, Sargassum spp., and Ceramium spp. (Zárate unpubl. data). Green turtle diet at Punta Núñez is primarily Hypnea spp., Caluerpa racemosa and Dictyota spp. Differences in growth rates among foraging grounds could be explained by the nutritional quality and the available quantity of the algae consumed by turtles. Further research on this topic is needed.

Spatial variation in somatic growth rates in green turtle populations have also been observed in Hawaii (Balazs & Chaloupka 2004) and Australia (Chaloupka et al.

2004) and Florida, USA (Kubis et al. 2009). In all three studies, spatial variation was believed to result from differences in green turtle population density and availability and quality of resources.

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Effect of Morph on Growth Rates

Growth rates in SCL, but not mass, were significantly different between black and yellow morphs.Yellow morph turtles grow in length at significantly faster rates than black morphs. While the black morphs examined on this study included juvenile (59%) and adult turtles (41%), the yellow morph is represented by juvenile turtles only (100%).

Yellow morphs are of Indo-Pacific origin (Amorocho et al. 2012, Dutton & Zárate unpubl. data) and from stocks that mature at a larger size than the black morph from the

Galápagos. Negligible growth after sexual maturity is observed in sea turtles (Carr &

Goodman 1970; Price et al. 2004) thus the more rapid SCL growth rates of yellow morph may result from a larger asymptotic body size. Yellow turtles will grow faster and larger to reach the size at which somatic growth has either stopped completely or become negligible.

Available information on the feeding ecology of green turtles in Galápagos foraging grounds suggests that there may be differences in the dietary contents among black and yellow morphs (Carrión -Cortez 2008). However, this information deserves further study due to the small sample size of esophageal contents analysed.

Comparisons with Other Green Turtle Populations

The black morph of green turtles in the Galápagos Islands has the slowest growth rates (Table 5-2) reported for any aggregation of green turtles in the Pacific and

Atlantic oceans (Table 5-3). Why does the black morph in Galápagos grow so slowly?

Green turtle growth rates may be affected by a combination of factors including diet, habitat quality, rate of ingestion, season, genetic factors, water temperature, and density-dependent effects (Boulon & Frazer 1990, Collazo et al. 1992, Bjorndal et al.

2000, Balazs & Chaloupka 2004, Chaloupka et al. 2004). The Galápagos Archipelago

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has been long protected from sea turtle harvesting and overexploitation (UNESCO

1978), the population is stable (Charles Darwin Foundation unpubl. data), and green turtles are abundant in the Archipelago. Possibly, high green turtle densities, with resulting low food availability or availability of lower quality foods, are responsible for slow growth rates. In Hawaii, the recovery of the green turtle population has been suggested as the cause of decreasing juvenile growth rates there (Balazs & Chaloupka

2004).

Growth Rates for Hawksbill Turtles in Galápagos

Little can be concluded from growth increments for three hawksbills from the

Punta Núñez foraging ground. However, in comparison with growth rates reported for hawksbills in other areas of the world, hawksbills in the Galápagos have rapid growth rates (Chaloupka & Limpus 1997, Mortimer et al. 2003, Bell & Pike 2012, refs in

Bjorndal & Bolten 2010 for the Atlantic). This rapid growth indicates that the slow growth in Galápagos green turtles is not a result of environmental conditions, such as low temperatures, that would not support rapid growth in a sea turtle.

There is a lack of information on the ecology of hawksbills at foraging areas in the eastern Pacific Ocean. In Galápagos, hawksbill turtles are usually associated but not limited to coral reefs areas and feed on sponges, cnidarians and barnacles (P.

Zárate pers. obs, Galápagos diving guides pers. obs.). Differences in growth rates of hawksbill at two different foraging areas in Puerto Rico were attributed to habitat and aggregation density. Lower growth rates of hawksbill turtles were found in sites with a more limited range of food resources and food availability, and high turtle density (Diez

& vanDam 2002). In the southern Bahamas, Bjorndal et al. (2000) found evidence for an inverse relation between aggregation density and growth rates. Possibly, in Galápagos

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faster growth rates can be explained by high nutritional quality and food availability, and low density of hawksbill turtles at foraging grounds.

Collecting additional growth data on hawksbill turtles should be considered a high priority for the research and management institutions in the Galápagos Islands.

In summary, results of this study confirm the findings of Green (1993) for somatic growth rates of green turtles in the Galápagos Islands and significantly extends that study to address the factors influencing growth rates. Somatic growth in Galápagos green turtles is very slow and is significantly affected by morph (or genetic factors), body size, and spatial variation (foraging site). This is the first study to provide information on growth rates for hawksbills turtles in Galápagos providing a start point for further research and comparison to other populations. Growth rates can be used to evaluate changes in populations and provide a baseline with which to compare the quality of, or change in, foraging habitat condition. In addition, growth rate data are an essential component of population models currently being used as conservation management tools.

129 G A M reGAM response function, spannual growth on se Table 5-1. Summaries of three general additive regression models (identity link, robust quasi-likelihood error function, fu cubic smoothing splines). ASE is asymptotic standard error, mean size is the mean of the straight carapace nc lengths (SCL) or masses at the beginning and end of the growth increment, year is the midpoint of the growth tio n, increment, duration is interval between capture and recapture, morph is black or yellow turtle, and site is an capture site (PE = Punta Espinoza, PN = Punta Núñez). nu Nonlinear effects (non parametric) al gr Parameter Estimate ASE t-ratio Prob(t) df F p o wt a. SCL growth for black and yellow turtles † h Constant 201.91 101.44 -1.990 Mean SCL -0.0101 0.0052 -1.928 NS 3 2.716 0.0594 Year 0.1011 0.0506 1.997 NS 3 0.268 0.8459 Duration 0.00003 0.0001 0.284 NS 3 0.240 0.8658 Morph 1.1848 0.1653 7.166 < 0.001 Site (PE) 0.6549 0.1773 3.695 < 0.001

b. SCL growth for black turtles only ‡ Constant -202.36 99.93 -2.025 Mean SCL -0.0141 0.0054 -2.613 < 0.05 3 2.435 0.0880 Year 0.1014 0.0498 2.034 NS 3 0.715 0.5504 Duration 0.0001 0.0001 0.446 NS 3 0.357 0.7831 Site (PE) 0.6840 0.1633 4.187 < 0.001

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Table 5-1. Continued Nonlinear effects (non parametric) Parameter Estimate ASE t-ratio Prob(t) df F p c. Mass growth for black and yellow turtles § Constant -314.36 661.46 -0.475 Mean mass -0.0394 0.0177 -2.219 < 0.05 2 1.029 0.3907 Year 0.1579 0.3300 0.478 NS 3 0.268 0.0096 Duration -0.0017 0.0010 -1.768 NS 2 0.240 0.2117 Morph 1.2353 1.0132 1.219 NS Site (PE) 3.0572 1.2848 2.380 < 0.05 Site (PN) 5.3642 1.8570 2.889 < 0.01 Notes: Probabilities (P) reported for F values are based on nonparametric df and residual deviance df. A significant nonparametric F means that the covariate was nonlinear. If the t test for a covariate is not significant (NS) then the nonparametric F test for nonlinearity is irrelevant. R2 = (null deviance – residual deviance)/null deviance. † Null deviance = 18.99, null df = 52, residual deviance = 5.10, residual df = 36.10, robust quasi-likelihood dispersion parameter = 0.124, R2 = 0.731 ‡ Null deviance = 7.80, null df = 40, residual deviance = 3.13, residual df = 26.10, robust quasi-likelihood dispersion parameter = 0.101, R2 = 0.598 § Null deviance = 578.81, null df = 49, residual deviance = 237.54, residual df = 33.16, robust quasi-likelihood dispersion parameter = 5.040, R2 = 0.590

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Table 5-2. Growth rates (cm/yr) for 10 cm size classes of green turtles from the Galápagos Islands. All values are expressed as mean ± SD(n). Galápagos black Galápagos yellow Galápagos black Galápagos yellow Size morpha morpha morphb morphb class Mean±SD(n) Range Mean±SD(n) Range Mean±SD(n) Range Mean±SD(n) Range 41-50 0.3±0.3(3) 0.0-0.5 1.5±0.6(4) 0.9-2.2 0.4(2) 0.3-0.5 - - 51-60 0.4±0.5(14) -0.4-1.6 - - 0.5±0.5(11) 0.0-1.6 1.6±1.1(4) 0.3-2.9 61-70 0.03±0.4(13) -1.0-0.5 1.3±0.2(2) 1.2-1.4 0.14 - - - 71-80 0.03±0.3(10) -0.5-0.4 0.7(1) - 0.1(34) - - - 81-90 0.2(1) - 0.8±0.4(5) 0.3-1.3 0.1(18) - - aThis study; bGreen (1993)

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Table 5-3. Growth rates (cm/yr) for 10-cm carapace length size classes of green turtles from other foraging grounds. All are based on straight carapace length except Australia is based on curved carapace length. All are based on mark-recapture studies except Hawaii and US Atlantic coast are based on skeletochronology. All values are expressed as mean ± SD(n). Size Gulf of Hawaiian Australiac US Atlantic Sebastian Florida, Great Culebra, class California Is., USb coastd Inlet reef, USf Inagua, Puerto USa Floridae Bahamasg Ricoh 41-50 - 2.1±1.2(67) 0.8±0.6(4) 2.5±2.2(54) 2.4±0.7(18) 2.6±0.9(25) 4.9±2.0(40) 6.0±0.6(9) 51-60 1.0±0.1(2) 2.3±1.0(53) 0.9(1) 2.7±2.1(34) 3.0±0.3(10) 2.7±0.7(7) 3.1±1.6(67) 3.8±0.5(4) 61-70 1.4±1.2(4) 2.2±0.9(62) 1.4±2.0(14) 3.3±2.6(16) 2.5±0.7(3) - 1.8±1.4(22) 3.9±2.0(30) 71-80 1.2±0.6(6) 2.1±1.0(21) 1.5±0.7(15) 2.4±2.1(21) - - 1.2±0.9(9) - 81-90 1.9±1.1(7) 1.3±0.5(12) 1.1±1.1(11) 2.6±3.8(16) - - - - aSeminoff et al. (2002); bZug et al. (2002); c Limpus & Walter (1980) presented as curve carapace length; dGoshe et al. (2010); eKubis et al. (2009); fBresette & Gorham (2001); gBjorndal & Bolten (1988); hCollazo et al. (1992).

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Table 5-4. Growth rates (kg/yr) for 10 kg mass classes of green turtles from Galápagos. Mass class Mean±SD(n) Range 11-20 1.0±1.0(6) 0.0 to 2.9 21-30 -0.4±3.0(16) -9.6 to 3.5 31-40 -0.1±4.6(6) -7.2 to 8.4 41-50 1.3±3.5(8) -3.5 to 7.6 51-60 3.6±2.5(3) 1.3 to 7.1 61-70 -0.6±0.4(3) -1.1 to -0.5 71-80 -2.1±5.1(4) -9.6 to 4.8 81-90 - - 91-100 1.4(1) - 101-110 1.5±0.5(3) 1.1 to 2.2

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Caribbean Sea Pinta

0° 30’ -

Marchena Ecuador

0° 00’ - Pacific Ocean

PE Santiago Fernandina Baltra

0° 30’ - BE Santa Cruz CD PN Isabela Santa Fé

San Cristóbal - 1° 00’ -

Floreana Española

- 91° 30’ - 91° 00’ - 90° 30’ - 90° 00’ - 89° 30’

Figure 5-1. Location of the foraging-ground study sites for sea turtles in the Galápagos -1° 30’ - Marine Reserve. PE = Punta Espinoza; BE = Bahía Elizabeth; CD = Caleta Derek; PN = Punta Núñez.

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A B

C C

Figure 5-2. Size class distribution of black and yellow morph from four study sites in the Galápagos Marine Reserve. A) Bahίa Elizabeth (BE), B) Caleta Derek (CD.), C) Punta Espinoza (PE), and D) Punta Núñez (PN).

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A B 1 2 C BE CD PE PN

1.5

1.0

1.0 0.5

0.5 0.5

0.0 0.0 0.0

-0.5 -0.5 -0.5

growth annual function, response GAM

50 60 70 80 90 Black Yellow BE CD PE PN Morph Site Mean SCL (cm) Figure 5-3. Graphical summaries of general additive regression analyses of straight carapace length (SCL) growth covariates for black and yellow turtles combined of A) mean SCL (not significant), B) turtle morph (significant), and C) site (significant). The response variable (annual SCL growth rate) is shown on the y-axis as a centered smoothed function scale to ensure valid pointwise 95 % confidence bands. For A), the solid line is the cubic smoothing spline fit conditioned on all other covariates in the analyses (Table 5-1). Dashed lines are pointwise 95 % confidence lines around the fits. Open circles are residuals. For B) and C), width of the mean covariate response is proportional to sample size with the 95% confidence interval shown by cross bars.

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BE CD PE A B

1.0 1.0

0.5 0.5

0.0

response function, annual growth annual responsefunction, -0.5

-0.5

GAM

BE CD PE 50 60 70 80 Mean SCL (cm) Site

Figure 5-4. Graphical summaries of general additive regression analyses of straight carapace length (SCL) growth covariates for black turtles only of A) mean SCL and B) site; both are significant. The response variable (annual SCL growth rate) is shown on the y-axis as a centered smoothed function scale to ensure valid pointwise 95 % confidence bands. For A), the solid line is the cubic smoothing spline fit conditioned on all other covariates in the analyses (Table 5-1). Dashed lines are pointwise 95 % confidence lines around the fits. Open circles are residuals. For B), width of the mean covariate response is proportional to sample size with the 95% confidence interval shown by cross bars

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1 2

A B C BE CD PE

6 4 4

4 2

2 2

0 0

-2

-2 -2

-4 ponse function, annual growth annual function, ponse

-4

res -4

-6 -6

GAM

-6 -8 PN 20 40 60 80 100 Black Yellow BE CD PE

Mean mass (kg) Morph Site Figure 5-5. Graphical summaries of general additive regression analyses of mass growth covariates for black and yellow turtles of A) mean mass (significant), B) morph (not significant), and C) site (significant). The response variable (annual SCL growth rate) is shown on the y-axis as a centered smoothed function scale to ensure valid pointwise 95 % confidence bands. For A), the solid line is the cubic smoothing spline fit conditioned on all other covariates in the analyses (Table 5-1). Dashed lines are pointwise 95 % confidence lines around the fits. Open circles are residuals. For B) and C), width of the mean covariate response is proportional to sample size with the 95% confidence interval shown by cross bars.

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CHAPTER 6 CONCLUSIONS AND FURTHER RESEARCH

Island Ecology and Sea Turtles

Remote islands around the world have some of the most unique flora and fauna in the world. Some have species of plants and animals that are not found anywhere else and have evolved in a specialized way. Because these islands provide a shelter from the fierce competition that species face on the mainland, species will develop that take advantage of these rare conditions. As a legacy of a unique evolutionary history, these ecosystems are irreplaceable treasures of nature. The characteristics of size, shape and degree of isolation make many of these islands ecologically and culturally unique.

However these same characteristics also make islands fragile and vulnerable ecosystems (Rolett & Diamond 2004).

In Chapter 2, I examined sea turtle ecology on the oceanic and continental islands of the eastern Pacific Ocean, and identified threats to sea turtle populations. I have also described sea turtle studies and conservation efforts with emphasis on the

Galápagos Islands. I found that sea turtle populations inhabiting these islands are impacted by human induced threats. Invasive species and fisheries interactions were common impacts to sea turtle populations in most islands of the region.

I also discovered that the Galápagos Islands face many more challenges than the rest of the islands of the region due to the high level of immigration, tourism and fisheries activities, and the presence of introduced animals. The strong legal framework of conservation in Galápagos today has successfully led to the implementation of several conservation measures that are helping to protect island original biodiversity to a great extent. However, sea turtles are still indirectly and directly impacted at sea and

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on nesting beaches by marine traffic, visitors on nesting beaches, fisheries practices, and introduced animals.

Threats to Incubating Embryos

Hatching and emergence success are good indicators of the suitability of a particular beach to act as an incubating system and the general health of a nesting population. Therefore, these two parameters provide fundamental information for the conservation and management of sea turtles (Miller 1997). Significant changes through time in these parameters are often indicators of changes in the physical conditions of the beach and/or predation.

Factors influencing hatching and emergence success of sea turtles nests are temperature (Matsuzawa et al. 2002, Segura and Cajade 2010), moisture (Ackerman

1980, Mortimer 1982), sand structure and composition (Mortimer 1990), salinity

(Ackerman 1980), nest location and its microhabitat or surrounding environment

(Whitmore & Dutton 1985, Bjorndal & Bolten 1992, Hays & Speakman 1993), human activities on nesting beaches (Kudo et al. 2003), and predation (Stancyk 1982). I investigated some of these factors in Chapter 3. I determined hatching and emergence success of nests on four major nesting beaches in the Galápagos Islands, and identified factors influencing them. I found relatively low values compared to those of other green turtle (Chelonia mydas) populations in the world, due to the combination of beetles, feral pigs, and nest destruction by nesting females. I found that beaches without pigs and beetles and with low nesting activity had higher hatching and emergence success compared to those beaches with higher nesting activity, pigs, and higher abundance of beetles. Lower hatching success due to predators has being found in other nesting

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population as well (Brown & Macdonald 1995) confirming that predation can have high impacts on sea turtle nests.

I observed differences in embryo survival among years that could be due to different environmental conditions among years, such as rainfall, and how these differences could be linked to predator abundance. Beetle reproduction can be stimulated by rainfall periods, and low rainfall results in higher numbers of pigs on the beach preying on green turtle nests.

This research has contributed to a better understanding of the impacts and sources of embryo mortality at the main nesting sites in the Galápagos. My results highlight the importance of establishing long term studies to monitor status of the rookery. This information is useful to managers to formulate management strategies to protect green turtles at this life stage and in this critical habitat.

Understanding Migratory Patterns and Foraging Ecology through Stable Isotopes

The use of stable isotopes, a non-invasive technique, provides insights for determining trophic level, identifying food sources, and assessing migratory behavior of species with wide geographical ranges (Peterson and Fry 1987, Hobson and Clark

1992, Rubenstein and Hobson 2004). Stable isotopes have successfully been used to assess trophic status and foraging ecology of sea turtles species (Jones and Seminoff

2013).

In Chapter 4, I examined foraging ecology of green turtles at four foraging grounds within the Galápagos Islands by analyzing stable isotope ratios of carbon

(13C) and nitrogen (15N) in turtle skin samples and potential food items. In addition, I

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evaluated if stable isotopes analysis could be useful to distinguish resident from migrant females in Galápagos.

I found substantial variation in 13C and 15N values within each foraging ground.

However, I was unable to distinguish between diet and habitat as the causes of these differences, because prey items were not collected at each foraging ground. In spite of this limitation of the data, mean 15N values from potential prey items collected from one site and the wide range on 15N skin values suggested that some turtles may be consuming higher-trophic-level foods.

These results should be interpreted with caution because I used discrimination factors obtained from a different green turtle population on a different diet. Since discrimination factors may vary with species, tissue type, diet, and growth rate

(Seminoff et al. 2006, Vander Zanden et al. 2012) appropriate discrimination factors in dietary reconstructions and trophic-level estimations for Galápagos green turtles are needed.

Based on my results, I concluded that green turtles in Galápagos are not exclusively herbivorous, and this result was supported by earlier studies on esophageal contents. Green turtles are known to consume animal matter in other areas, particularly in the eastern Pacific (Jones & Seminoff 2013).

Nesting females from Galápagos use foraging areas within and outside

Galápagos (Table 4-3 and Table 4-4). I have been intrigued by the fitness consequences of these two migratory strategies, as they may pose different energetic trade- offs that could be reflected in their reproductive output. Females that have different migration destinations and use distinctive foraging areas, such as loggerheads

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from the Mediterranean Sea, have shown to differ in body size and clutch size (Zbinden et al. 2011).

I expected that because females nesting in Galápagos use foraging areas within and outside the Galápagos, the isotopic values would reflect the location of the foraging area. However, I found no distinctive groups or clusters within the nesting aggregation that could be interpreted as different foraging strategies. In addition, I compared 13C and 15N values at different locations throughout the eastern Pacific, which revealed extensive overlap of values among regions. Mean 13C and 15N values from Costa

Rica (Golfo Dulce and Cocos Is.), Colombia (Gorgona Is.), and Perú (Paracas and oceanic waters) fall within the range of values recorded for Galápagos foraging grounds. Therefore I could not use stable isotope values to distinguish between migrant and resident nesting females in Galápagos.

This study has provided valuable knowledge about green turtle isotopic composition in foraging and nesting grounds of the Galápagos Islands. Little information exists to date regarding the marine isoscape pattern for the East Pacific region.

Baseline studies in the region and elsewhere are needed for a more accurate interpretation of stable isotopes in the study of sea turtle ecology.

Somatic Growth Rates of Sea Turtles

Knowledge of somatic growth rates of sea turtles is critical for our understanding of habitat quality and demography of these endangered species. Growth rates of green turtles are affected by a combination of factors including diet, habitat quality, rate of ingestion, season, genetic composition, water temperature, and density-dependent effects (Boulon & Frazer 1990, Collazo et al. 1992, Bjorndal et al. 2000, Balazs &

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Chaloupka 2004, Chaloupka et al. 2004). Differences in growth rates for green turtles have been found among Pacific and Atlantic populations; the latter are usually higher than those in the Pacific (Table 5-3) possibly due to differences in abundance and quality of the available forage supply (Bjorndal et al. 2000).

An earlier study showed that growth rates of green turtles in Galápagos are among the slowest ever reported for immature green turtles anywhere in the world

(Green 1993). In Chapter 5, I evaluated more recent data for growth rates of green turtles and hawksbills captured at foraging grounds in Galápagos and assessed factors influencing growth rates for black and yellow morphs of green turtles. I confirmed earlier findings for somatic growth of green turtles in Galápagos and found that growth rate is significantly affected by morph, body size, and foraging site.

Two morphs of green turtles co-exist in Galápagos foraging areas but correspond to different stocks. The yellow morph is from rookeries in the Indo-Pacific (Amorocho

2009, Dutton & Zárate unpubl. data) while the black morph nests on beaches in

Galápagos and throughout the East Pacific. I found that yellow morph turtles grew faster than black morph turtles in length, perhaps because the yellow morph has a larger asymptotic body size. The differences I found in growth rates of green turtles among foraging grounds could be explained by the nutritional quality and the available quantity of the algae consumed by turtles. The reasons why black turtles grow so slowly in

Galápagos compared with other turtle population are not well understood. Possibly, the lack of sea turtle harvesting and overexploitation, leading to high density of green turtles in Galápagos and resulting in low food availability or availability of lower quality foods, are responsible for such slow growth rates. Further research on this topic is needed

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This research extends earlier studies by addressing factors influencing growth rates of green turtles on the islands. A significant effect of body size, morph and site on growth rate was found in this study. In addition, the study also provides the first information on growth rates of hawksbill turtles in Galápagos as a start point for further research and comparison to other populations. Information provided here can be used to evaluate changes in populations and provide a baseline with which to compare the quality of, or changes in, foraging habitat condition.

Directions for Future Research

The studies I conducted demonstrate how our understanding of sea turtle biology and ecological roles can be enhanced by focusing on the analysis of different developmental stages and critical habitats and have improved our understanding of green turtles in this important island system. I would like to emphasize some additional topics and potential directions for future research.

Nest Survival

Additional research on the factors influencing embryo survival should consider the inclusion of physical parameters as well as predator population density.

Measurements of temperature, humidity and the determination of substrate characteristic across the beach profile and on particular sectors of the beach could improve understanding of unknown sources of mortality presented in Chapter 3. As evident from my results, other factors influence hatching and emergence success of green turtle nests.

Heavy nest predation can have long- term demographic impacts (Heppell et al.

1996). Therefore, continued monitoring of hatching success on nesting beaches is critical. This monitoring can reveal increases in specific threats, for example an

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increased risk of nest predation on beaches by mammalian predators or the emergence of new threats. Recently, predation by feral cats on green turtle nests has been observed for the first time on Galápagos beaches (M. Parra pers. comm.).

Studies that evaluate sand temperature and other physical parameters on major nesting beaches on the islands are also needed. Sand temperature data were collected for several years on Galápagos nesting beaches by the author and collaborators.

Preliminary results revealed that substantial variation in sand temperatures among beaches. Although preliminary, these results highlight the importance of monitoring beach temperatures to evaluate how global warming could affect sex ratios and nest survival in the future. Hatchling sex ratios may be skewed towards a predominantly female ratio, and eggs may be consistently exposed to temperatures that exceed thermal mortality thresholds (Fuentes et al. 2009). Consequently, understanding the rates at which sand temperatures are likely to change represents an immediate priority.

Nesting Trends and Reproductive Output

Monitoring trends in sea turtle populations is critical to assess population status and to develop and assess conservation strategies. In addition to providing population estimates, nesting beach data also provide information regarding the abundance of nesting females and reproductive or nesting parameters such as fecundity, remigration interval and nesting site fidelity, among others (Heppell et al. 2003).

An analysis of the nesting ecology of green turtles in the Galápagos Islands is highly recommended. Along with growth, reproductive traits are central to understanding animal life histories.

Distinguishing between resident and migrant nesters in Galápagos remains an important goal for understanding the relative energetics and life history consequences

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for these two strategies (Chapter 4). A combination of analytical tools such as satellite tracking, lead (Pb) stable isotopes, and trace elements should be considered to provide new insights on this question.

In summary, I have improved our knowledge of green turtles in Galápagos by focusing on aspects of their biology at different developmental stages and on critical habitats. However, more research is needed to have a better understanding of the ecological roles that green turtles have in the Archipelago ecosystems. I am confident that information provided here will help managers of the Galápagos National Park to effectively protect and conserve sea turtles and their habitats.

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BIOGRAPHICAL SKETCH

Patricia M. Zárate was born in Chile. Since she was young, she has been passionate about animals and nature, constantly engaging in any activity that involved working with animals and trips to the field. At 19, she became a free diver. This was a decisive moment in her life, as the underwater world inspired her enormously. She received her B.A. degree in marine sciences in 1994 and earned the designation of marine biologist from Universidad Católica del Norte, Chile in 1997. As an undergraduate student, she was vice-president of the student government, a teaching assistant for ichthyology for 5 years, and Head of Vertebrate Collections for 3 years. For her undergraduate thesis, she studied the reproductive biology of the swordfish Xiphias gladius in Chilean waters, which was later used to establish minimum size at capture for the Chilean swordfish fisheries. For this research, she also received an award for best undergraduate student paper at the XVI Marine Sciences National Congress, Chile.

She dedicated the first years of her professional career to the study and evaluation of management areas along the central Chilean coast, working closely with fishermen associations and the Instituto de Fomento Pesquero (Fisheries Development

Institute). During this time, she also worked as a scientific diver and was an instructor for several workshops organized to educate fishermen.

In 2000, she moved to the Galápagos Islands, Ecuador, and became part of the staff at the Charles Darwin Foundation, where she was the coordinator and principal investigator of the sea turtle research. For eight years, she coordinated projects at the nesting beaches and foraging grounds. She actively participated in many diving expeditions designed to monitor the benthic resources, fishes and megafauna of the

Galápagos Islands. She was also the biological inspector for the Prosecutor’s Office,

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where she identified shark species from confiscated fins that were illegally harvested in the Galápagos Marine Reserve. Her investigations had an important outreach component, as she worked closely with the local community, as well as local, national and international students. She supervised several student projects and theses during this time.

Patricia has also been deeply involved in shark research and bycatch issues.

She served as the Ecuador delegate for the Scientific Committee of the Inter-American

Convention for the Protection and Conservation of Sea Turtles and the Permanent

Commission for the South Pacific, for the Convention on International Trade in

Endangered Species, and as the technical adviser at Galápagos Marine Reserve management meetings. She is a member of the IUCN Marine Turtle Specialist Group and a scientific collaborator of the Charles Darwin Foundation.

She began her Ph.D. degree with Karen Bjorndal in the Archie Carr Center for

Sea Turtle Research at the University of Florida in 2008. She worked as a teaching assistant for biological sciences, animal physiology and functional vertebrate anatomy, as well as served as an online instructor for the Introduction to biology course. She received her Ph.D from University of Florida in the fall of 2013.

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