Movements and behavior of the East Pacific Green ... - CORE

Movements and Behavior of the East Pacific Green Turtle

(Chelonia mydas) from Costa Rica

A Dissertation

Submitted to the Faculty

of

Drexel University

by

Gabriela S. Blanco

in partial fulfillment of the

requirements for the degree

of

Doctor of Philosophy

October 2010

© Copyright 2010

Gabriela S. Blanco

All Rights Reserved

ii

Dedication

To all the people that walk sea turtle beaches every night.

Para la gente que todas las noches patrulla playas de tortugas.

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Acknowledgments

First of all, I would like to thank three of my professors and friends who have

been crucial during the process of my Ph.D. I could never thank enough my advisor, Dr.

James R. Spotila for giving me the opportunity to be part of his lab at Drexel and who,

through all these years, has guided me to become a “real” scientist and conservationist.

Dr. Frank Paladino “my other boss” who trusted and allowed me to do what will always

be one of the most challenging, educating and rewarding experiences of my career:

Running the Leatherback Project. I am grateful to him for his best lesson: “You can sit

here and see how all the poachers take the eggs or you can go there and get your Ph.D.

done”. Finally, Dr. Stephen Morreale has not just taught me all I know about telemetry,

mapping, and science. He guided me step by step during field work, data analysis and

manuscript preparation, but most importantly he taught me how to “Think Big”. Steve,

Jim, and Frank have been incredibly patient and supportive during all these years and I

am truly honored for being part of their team. I am grateful to the other members of my

committee: Dr Jeffrey Seminoff, who greatly improved many aspects of this thesis,

manuscript preparation, and data analysis and gave me great advice in the field. In

addition, I thank Dr. Harold Avery who always reminded me that there are other than sea

turtles out there and Dr. Susan Kilham from whom I learned the true meaning of ecology.

I am indebted to Dr. Kenneth Lacovara for bringing me to Drexel. Without him none of

this would have ever happened. I am grateful to Dr. “Bob” George for all his help with

ultrasound and to Dr. Helen Bailey for her help with SSSM.

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In Philadelphia

I am extremely grateful to my husband, Lucio for his constant support and

encouragement. But most importantly, I want to thank him for not divorcing me after my

never- ending field seasons in Costa Rica. I am especially thankful to my family in

Philly: Lucio, Bibi (Dr. Santidrián Tomillo), Eugenia Zandonà and Marcelo Weksler for

their support and wonderful friendship. Euge and Bibi have been by my side during all

the process of my Ph.D. They are the best friends, family and colleagues one could ever

wish to have (grazie mille!). In addition, I would like to thank all the students that went

through the Ecology lab during my time at Drexel especially Carlos Mario Orrego,

Kimberly Magrini, Jack Suss, Steve Pearson, Shaya Honovar and Annette Sieg. Finally, I

am especially grateful to Laurie Spotila and Rebecca Schneider who made me feel at

home in USA. Thanks to the Morreale family for hosting and making me feel at home so

many times.

In Costa Rica:

I could never thank enough the Chacón Family for letting me be one of them and

take care of me while in Playa Grande. Also, Bibi was the person who first introduced me

to the “sea turtle world” and taught me the real meaning of sea turtle conservation

(Gracias Bibi!). I would like to thank Rotney Piedra and Elizabeth Velez for showing me

their beach, Nombre de Jesús and inviting me to work there. I am especially thankful to

Rotney for many hours of turtle discussion and advice. I can’t express my gratitude

enough to all the Park Rangers at Las Baulas for their help in the field, their friendship

and for letting me share the “tico” culture. I give special thanks to Carlos Díaz and Bernal

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Cortés for their priceless help in many ways. Thanks to the tour guides for their support

and for making the best of the long hours on the beach. I am extremely grateful to my

field assistant Wilder Méndez Montes for countless hours on the beach without losing his

enthusiasm, dedication and commitment with conservation. I would like to thank all the

people that helped me in the field with data collection and transportation of the “portable”

ultrasound scanner: Will, Eddy M., Wilverth V., Fabricio A., Sharon U., Carlos O., Sam

F, Tom B, Luca M., Jonah M., Celine C., Nathan R., Sara V., Tera D., Johnna H, and

MINAET and Earthwatch volunteers. I want to thank all the assistants of the leatherback

project for their tremendous dedication to the turtles and because of all I have learned

from them; especially the “Dream Team” Tera, Rebecca, Nikki and Sara and “The

Family” Tom, Sam, Johnna, Sara and Abby.

Finally and most importantly, I am sure I could not have gone through my last

field season without the help and support of Steve Morreale, Carlos Díaz, Bernal Cortés

and Wilder Mendes, Mil gracias por todo!

In Argentina

I want to thank my parents for always encouraging me to follow my passion, and

always being there for me and my sisters (and best friends) through everything. Thanks to

my Argentinean friends for not forgetting me - especially María Laura, Celina and

Graciela.

vi

Funding opportunities

I want to express gratitude for funding to The Betz Chair Endowment of Drexel

University, Earthwatch Institute, Wildlife Conservation Society (WCS), and The

Leatherback Trust. Special thanks to the Goldring Marine Biology Station at Playa

Grande and its staff. Thanks to Lucas Moxey (from NOAA OceanWatch-LAS) for all his

assistance and expertise obtaining oceanography data.

vii

TABLE OF CONTENTS

LIST OF TABLES………………………………………………………………………. ix

LIST OF FIGURES………………………………………………………………….........x

ABSTRACT………………………………………………………………………….......xv

CHPTER1: Introduction to sea turtles……………………………………………………1

CHAPTER 2: Diving behavior and movements of the east Pacific green turtle

(Chelonia mydas) during internesting in Costa Rica…………………………………….13

ABSTRACT…………………………………………………………………......13

INTRODUCTION………………………………………………………………15

MATERIALS AND METHODS……………………………………………......17

RESULTS……………………………………………………………………….23

DISCUSSION…………………………………………………………………...27

REFERENCES…………………………………………………………………..33

CHAPTER 3: Reproductive Output and Ultrasonography of an Endangered Population

of the East Pacific Green Turtle……………………………………………………….....51

ABSTRACT…………………………………………………………………......51

INTRODUCTION………………………………………………………………53


RESULTS……………………………………………………………………….60

DISCUSSION…………………………………………………………………...61

REFERENCES…………………………………………………………………..68

viii

CHAPTER 4: Post-nesting Movements and Foraging Areas of the East Pacific Green

Turtle (Chelonia mydas) from Costa Rica……………………………………………….77

ABSTRACT…………………………………………………………………......77

INTRODUCTION………………………………………………………………79


RESULTS………………………………………………………………………..87

DISCUSSION…………………………………………………………………...91

REFERENCES………..……………………………………………………….103

CHAPTER 5: Dispersion of East Pacific Green Turtle hatchlings emerging from Nombre

de Jesús, Costa Rica…………………………………………………………………….128

ABSTRACT………………………………………………………………….....128

INTRODUCTION……………………………………………………………...130

MATERIALS AND METHODS…………………………………………….....133

RESULTS………………………………………………………………………136

DISCUSSION…………………………………………………………………..138

REFERENCES………...……………………………………………………….143

CHAPTER 6: Conclusions…………………………………………………………….170

VITA……………………………………………………………………………………173

ix

LIST OF TABLES

2.1 Attachment data for 13 eastern pacific green turtles (Chelonia mydas) during

the nesting season in Costa Rica. All individuals included in the study were in

their internesting interval. *Transmitters recovered after premature

release………………………………………………………………………………..39

3.1 East Pacific green turtles selected from the database from which there was a

complete record of their reproductive status through ultrasound; turtles were

scanned every time they came to the beach during the period of study. ECFU is the

effective clutch frequency + the number of clutches left calculated from

ultrasonography………………………………………………………………………73

4.1 Post-nesting movements of East Pacific green turtles (Chelonia mydas) with

satellite transmitters attached from Nombre de Jesús, Costa Rica. Track length is

total distance moved of the turtle during migration. Length of migration is the

calculated number of days the turtles took to reach the foraging areas. Total tracking

includes the total duration of the satellite

transmitters………………………………………………………………………….112

4.2 MCPs of East Pacific green turtles (Chelonia mydas) on the foraging grounds.

The MCPs were created based on all locations of the turtles in the foraging areas.

Foraging (tracking days) refers to the time spent on the foraging grounds………...113

5.1 Mean magnitude (cm/sec) of currents in the Eastern Tropical Pacific Ocean that

transported a model hatchling for one year for all years analyzed.…………...147

x

LIST OF FIGURES

2.1 Satellite transmitter attachment to an East Pacific green turtle. a)

posterior marginal scute. b) upper plastic button. c) flexible lanyard (400 lb

monofilament fishing line). d) corrosive link with metallic crimps and swivel.

e) Satellite transmitter (Mk 10 PAT tag, programmed for opportunistic

transmissions)……………………………………………………………….40

2.2 Fixed Kernel density analysis. Internesting areas occupied by East

Pacific green turtles. Areas highly used are Nombre de Jesús (NJ),

Zapotillal (Z), the Bay of Playa Brasilito (PB) and, Playa Conchal (PC).

PNMB: Parque Nacional Marino las Baulas, PL: Playa Langosta.

Utilization Distribution (UD) 25% = 1.57 (red), 50% = 4.5 (orange),

75% = 9.4 (light green) and 95% = 53.9 km2 (dark green). Scale (from white

to blue) represents depth (meters) Insert shows location on map of Costa

Rica.…………………………………………………………………………41

2.3 a) Percentage of dives culminating at specific depth intervals during

internesting for 13 East Pacific green turtles from satellite data obtained

through Argos and summarized in bins. We calculated the average at depth in

relation to the total dives for each turtle. b) Percentage of duration

intervals of dives during internesting for 13 East Pacific green turtles from satellite data obtained through Argos and summarized into bins.

We calculated the average duration in relation to the total dives for each

turtle…………………………………………………………………………42

2.4 Proportion of U-dives of East Pacific green turtles in Costa Rica ending

at different depth intervals during internesting. The proportion of U-dives

at depth was calculated in relation to the total U-dives for each turtle taken

from data logged in the transmitter….……………………………………...43

2.5 Duration intervals of U-dives of East Pacific green turtles during the

internesting. The duration of U-dives was calculated in relation to the total

number of U-dive for each turtle. Complete data were taken from satellite

transmitters recovered from turtles…….……………………………………44

xi

2.6 Regression of dive depth and dive duration including all dive types for

East Pacific green turtles during internesting (p < 0.01). Turtle 1: r² =

0.215, Turtle 2: r² = 0.213, Turtle 3: r² = 0.455 and, Turtle 4: r² = 0.01. Data

recovered from satellite transmitters. ………………………………………45

2.7 Dive profiles for East Pacific green turtles. Black lines represent depth and

gray lines represent light levels. Elevated light levels represent daytime and

low light levels represent nighttime. Turtle 2: Dives performed during day

and night. Turtle 3: dives mainly performed during the day with prolonged

time at surface during the night……………………………………………46

2.8 Difference between surface times of East Pacific green turtles during day

and night. Day represents the 12 hours of light in the tropics. Days 1 to 4

includes 4 individuals; days 5 to 9 include 3 individuals. Day 1: first day

after successful nesting (transmitter attachment). The percentage of time at

the surface was calculated in relation to the total surface time during the 12

hour of light or darkness each day.………………………………………….47

2.9 a) Surface time and U-dives during the internesting for 4 East Pacific

green turtles. The shaded areas represent night (12 dark hours). Each data

point represents an interval of 2 hours. b) Proportion of time spent at the

surface and U-dives performed at different times of the day for 4 East

Pacific green turtles. Total represents the sum of the proportion of time

spent at surface and the proportion of U-dives performed by the turtles. Each

data point represents an interval of hours………………………………48-49

2.10 Correlation between the total time spent at the surface during the night

and the total U-dives performed during the internesting by East Pacific

green turtles (p < 0.05, r² = 0.930). U-dives were calculated in relation to the

total number of U-dives performed by each turtle during the internesting.

Surface time was calculated in relation to the total time spent at the surface at

night during the internesting..……………………………………………….50

3.1 Ultrasonographic image of an ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. The ovary was filled

with vitellogenic follicles (vf). The turtle had at least two more clutches to

lay during the nesting season.……………………………………………….74

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3.2 Ultrasonographic image of the ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. Ovary in late

preovulatory stage. The turtle had one more clutch to lay during the nesting

season. In this stage we observed vitellogenic follicles (vf), atretic follicles

(af) and some coleomic (empty) space..…………………………………….74

3.3 Ultrasonographic image of the ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. The depleted ovary

indicated that the turtle had completed the nesting season and would start

migrating. We considered an ovary depleted when we identified fewer than 5

vitellogenic follicles remaining (none in this picture)..…………………….75

3.4 Ultrasonographic image of the oviduct of an East Pacific green turtle

(Chelonia mydas) after a nesting event. The presence of the shelled egg

after oviposition indicates that some kind of disturbance occurred during the

nesting event causing the turtle to stop laying eggs and start covering the

nest. s = shell, a = albumen, y = yolk.……………………………………75

3.5 Percentage of East Pacific green turtles in Costa Rica with depleted

ovaries and late preovulatory staged ovaries by month. The percentages

were calculated in relation to the number of turtles scanned by ultrasound

every month…………………………………………………………….…...76

4.1 Post-nesting movements of east Pacific green turtles nesting on Nombre

de Jesús, Costa Rica that migrated to the area of Santa Elena Bay( a, b),

within the area of Gulf of Fonseca(c) and to the Gulf of Panama (d)...114-115

4.2 Migration routes in relation to geostrophic surface currents (0.5º spatial

grid, monthly composites) of East Pacific green turtles from Nombre de Jesús

that migrated to the area of the Gulf of Fonseca (a, b, c) and to the Gulf of

Panama (d) Scale represents magnitude of currents (cm/sec)………116-117

4.3 Foraging areas of East Pacific green turtles represented by 100% MCP.

Each polygon includes all the locations for the individual turtles during

foraging……………………………………………………………..118-119

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4.4 MCP per week of two east Pacific green turtles whose MCP areas were

higher than 10,000 km2. Each polygon includes locations for 7 days in the

foraging areas……………………………………………………………...120

4.5 Percentage of dives of different durations performed by east Pacific

green turtles during migration and foraging. Migration = 8 turtles,

foraging = 9 turtles……………………………………………………….121

4.6 Percentage of dives at different depths performed by east Pacific green

turtles during migration and foraging. Migration = 8 turtles, foraging = 9

turtles. *Indicates significant differences (ANOVA, p < 0.05) between 5 m

and other depths……………………………………………………………121

4.7 Percentage of dives at different depths of east Pacific green turtles in the

foraging areas. Santa Elena bay includes 4 turtles because of the small

variation between individuals (bars represent SD)…………………...122-123

4.8 Percentage of durations and depths of dives during migration and

foraging of east Pacific green turtles. Each graph includes percentages

corresponding to day (white bars) and night (black bars). M: migration, F:

foraging. Migration = 8 turtles, foraging = 9 turtles………………….124-125

4.9 Monthly MCP in relation to Sea Surface Temperature (SST). SST

(0.1° spatial grid, monthly composites) for each month of study. MCPs

correspond to all locations in a month for each turtle in the foraging

area……………………………………………………………………..…126

4.10 Monthly MCP in relation to Chlorophyll-a (CHL). CHL

(0.05° spatial grid, monthly composites) for each month of study. MCPs

correspond to all locations in a month for individual turtles in the foraging

areas………………………………………………………………………127

xiv

5.1 Location of model hatchlings released 10 km off the coast of Nombre de

Jesús in northwest Costa Rica as calculated by the model every week for all

analyzed years (1992-2009). Each dot represents the new position of the

model hatchling after being transported by a current for a period of 7

days. ……………………………………………………………………….148

5.2 Circulation of currents in the Eastern Pacific Ocean at different times of

the year. Colors represent magnitude (cm/sec) and arrows represent direction

of the currents. Each picture represents the first week of the month referred to

in the legend. We obtained data from NOAA OceanWatch-LAS. The grids

were composited in a 7 day period with 0.5º spatial resolution………149-150

5.3 Movement of model hatchlings released 10 km off the coast of Nombre

de Jesús in northwest Costa Rica as calculated by the model for each year

from 1992 to 2008. Each dot represents the new position of the model

hatchling after being transported by a current for a period of 7 days. Lines

connecting points represent probable trajectories from one week to the

next……………………………………………………………………151-160

5.4 Movement of model hatchlings released 10 km off the coast of Nombre

de Jesús in northwest Costa Rica in comparison with ocean currents as

calculated by the model for each year from 1992 to 2008. Each dot represents

the new position of the model hatchling after being transported by a current

for a period of 7 days. Black dots represent a three month period starting the

same week as the period of the background current image. Grey dots

represent the rest of the locations for the year. Background color represents

the magnitude of the currents (cm/sec) for the first week of the month

referred to in the map………….……………………………………...161-169

xv

ABSTRACT

Movements and Behavior of the East Pacific Green Turtle (Chelonia mydas)

from Costa Rica

Gabriela S. Blanco

Supervisor: James R. Spotila, PhD

I attached satellite transmitters to study the movements and behavior during internesting

and migration of East Pacific green turtles nesting on Nombre de Jesús and Zapotillal.

Prior to transmitter attachment we preformed an ultrasound scan to determine the turtle’s

reproductive status. I obtained information on geostrophic surface currents to simulate the

dispersion of hatchlings emerging from Nombre de Jesús. I determined the Estimated

clutch frequency (ECFU: mean ± SD) 5.13 ± 1.32 using ultrasound, which was an

effective technique to determine the reproductive effort of turtles. Turtles spent the 12

day internesting period in the nearby waters off the nesting beach using mainly an area of

4.5 km2. Depths of dives and depth of water in the area indicated that the turtles dove to

the bottom to rest during the day and rested at the surface during the night. After the

nesting season, some turtles moved to their foraging areas in Gulf of Papagayo and the

Santa Elena Bay, close to the Gulf of Fonseca, and in inshore waters of Panama. During

migration the turtles dove mainly to a depth of 5 m or less. During foraging most of the

dives were between 5 and 10 m depth. I found three different scenarios for possible

hatchling dispersion: 1-hatchlings could be transported offshore and after three months

pushed back closer to the coast, 2- hatchlings could be transported north or south

remaining along the coast and, 3-hatchlings could be transported to waters offshore still

within the Eastern Tropical Pacific (ETP). East Pacific green turtles remained their entire

xvi

life within the waters of the ETP including females, which carry out limited to-long-

distance migrations (5 to 1091 km). The unique characteristics of the area disperse

hatchlings to productive areas providing them with enough resources to grow at the early

life stages and move to adult foraging areas also in the ETP. The coastal nature of their

movements and the high concentration of turtles off the nesting beach make them

vulnerable to artisanal fisheries. That, together with intense poaching that occurs on the

nesting beach indicates that this population may soon face extinction.

1

Chapter 1: Introduction

Sea turtles are widely distributed, occurring in neritic and oceanic environments

around the world, but their nesting beaches are restricted to tropical and subtropical areas

(Pritchard 1997). The seven species of sea turtles share a common generalized life cycle

that includes long periods at sea away from the nesting areas (Carr 1987). Reproductively

active female sea turtles migrate to nesting beaches to lay eggs; this process takes several

months for each individual.

During a single reproductive season turtles nest repeatedly with variable

internesting times between consecutive clutches (Miller 1997). Prior to nesting pre-

ovulatory follicles develop in the ovaries and are then ovulated into the oviductal tract

(Rostal et al. 1990, Rostal et al. 1996) where the sperm is stored and fertilization takes

place (Gist and Congdon, 1998). After this process the albumin layers and the shell are

deposited (Rostal 2007). At the culmination of this phase, turtles emerge onto the nesting

beaches and lay their eggs. Meanwhile in the ovary, there are still enlarged follicles that

will be ovulated and shelled for the following nesting event. The process takes place

during the internesting interval and is repeated until the end of the nesting season when

the eggs are depleted.

In general, during the internesting period sea turtles congregate in areas along the

coast relatively close to the nesting beaches, moving back to the nesting beaches just a

few days prior to the nesting event (Fossette et al. 2007, Schofield et al. 2009, Shillinger

et al. 2010). The behavior of female turtles during internesting is driven by energy

2

optimization due to the high coast of crawling onto the beach and laying eggs (Wallace et

al. 2005); as a result they spend most of the time resting on the seabed (Hays et al. 1999).

After several weeks of incubation hatchlings emerge from the nest, enter the surf

and swim to oceanic areas (Bolten et al. 1998). The oceanic stage of sea turtles has been

referred to as “the lost years” (Carr 1982) a stage that can last for several years. In a later

juvenile stage sea turtles move to the adult foraging areas where they stay and reach

sexual maturity and start to carry out migrations to and from the nesting beaches (Bolten

2003). This is true for all sea turtle species but for the flatback turtle (Natator depressa)

which is the only sea turtle species that lacks an oceanic phase in its life cycle (Walker

and Parmenter 1990) and the leatherback turtle (Dermochelys coriacea) which is pelagic

all its life (Bolten 2003).

Another feature common to all sea turtles is migration. Migration in sea turtles is

driven by the balance of the cost of residing at a given location versus the benefit of

moving (Morreale et al. 2007). For example, turtles in foraging areas need to migrate to

tropical and subtropical beaches to ensure the proper development of eggs and survival of

the hatchlings. However, food availability in the surroundings of the nesting beaches is

not always optimal for adult survival (Hays et al. 1999).

Due to the pelagic habits of sea turtles, studying their migration has been

challenging (Myers et al. 2006). Different methodologies have been applied to determine

the migration of these reptiles. Eckert and Eckert (1988) analyzed time of colonization as

well as the age of the barnacle communities that live on sea turtle’s carapaces. Green

(1984) and Alvarado and Figueroa (1992) used tag return to study the migration of

3

turtles. The mark-recapture technique provided information on movements (point to

point) but no data on migratory pathways (Byles et al. 1995).

Satellite telemetry was used in several studies recovering data on diving behavior

(Hays et al. 2000, Hays et al. 2002, Eckert 2006, Fossette et al. 2007, Blumenthal et al.

2009), and migratory paths (Morreale et al. 1996, Cheng 2000, Eckert 2006, Seminoff et

al. 2008, Shillinger et al. 2008) of sea turtles. More studies are including telemetry

because it gives information on the geographic location of the animal, as well as other

behavioral and environmental information (Tremblay et al. 2006). Therefore, electronic

devices play an important and increasing role in the study of marine turtles (Myers et al.

2006)

Sea turtle migrations can be fairly extensive. Pacific leatherback turtles nesting in

Costa Rica migrate into the South Pacific off Chile and Peru (Morreale et al. 1996,

Shillinger et al. 2008). Green turtles (Chelonia mydas) nesting on Ascension Island travel

to feeding grounds along the coast of Brazil (Hays et al. 2002), and olive ridley turtles

(Lepidochelys olivecea) nesting in northwestern Australia migrate between 180 and 1100

km to their feeding grounds (Whiting et al. 2007). Some juvenile loggerheads (Caretta

caretta) traverse the entire Pacific Ocean during developmental migrations; traveling

from nesting beaches in Japan and Australia to foraging areas in Baja California (Bowen

et al. 1995). When they reach sexual maturity they return to the western Pacific where

they remain the rest of their life (Nichols et al. 2000). In the Eastern Pacific, green turtles

nesting in the Galapagos Islands migrate to the coast of Central America and to oceanic

areas in the Eastern Tropical Pacific (Seminoff et al. 2008).

4

Conservation of sea turtles is vital for marine and terrestrial ecosystems, which

are significantly affected by these reptiles (Bouchard and Bjorndal. 2000). Their

ecological role consists in being consumers, prey, hosts for parasites, substrate for

epibionts, nutrient transporters and modifiers of the landscape (Bjorndal and Jackson

2003, Heithaus et al. 2007). All sea turtle species are in the Red list of threatened species

ranging from vulnerable to critically endangered (IUCN 2010). For several decades,

people have harvested eggs and adults (Seminoff 2004, Santidrián-Tomillo et al. 2008),

these activities continue until today in unprotected areas. In addition, numerous

populations have declined because of several interactions with fisheries, both industrial

and artisanal (Lewison et al. 2004, Spotila et al. 2000, Troëng et al. 2004). One of the

main problems that sea turtles are facing at present is the loss of marine ecosystems and

nesting beaches through pollution, over-fishing and development of nesting sites

(Bjordnal et al. 2003). The new threat faced by sea turtles is global warming, because at

very least an increase in incubation temperatures may lead to female biased populations

and will increase levels of egg mortality (Spotila 2004).

East Pacific green turtles (Chelonia mydas) (also known as black turtles) belong

to distinct breeding populations of this Endangered Species (IUCN 2010) and inhabit

waters in tropical and sub tropical regions throughout the Eastern Pacific (Seminoff et al.

2002b). In general, green turtles forage in coastal areas, estuaries, lagoons (Seminoff et

al. 2002b) and near shore insular habitats (Amorocho and Reina 2007). Their diet is

mainly sea grass and red and green algae. However, in the Pacific they also eat

invertebrates and gelatinous prey (Seminoff et al. 2002a, Seminoff et al. 2006, Quiñones

et al. 2010). In the Eastern Pacific, their range extends from the U.S. West Coast to Chile

5

and the Galapagos Islands. The most important nesting grounds in the eastern Pacific are

reported to be in Michoacán, Mexico (Alvarado and Figueroa 1992) and the Galapagos

Islands, Ecuador (Green 1984). Although green turtles are common along the Pacific

coast of Central America, limited information exists on population characteristics and

number of individuals nesting on those sites (Richard and Hughes 1972, Cornelius 1976).

Although few scientific data are available for East Pacific green turtles in Costa

Rica it appears to host an important population along the coast of Guanacaste on the

Nicoya peninsula (Richard and Hughes 1972, Cornelius 1976). Nesting there occurs

mainly on Nombre de Jesús and Zapotillal beaches and in lower numbers on beaches

along the North of the Nicoya peninsula. Nombre de Jesús and Zapotillal are located

north of Parque Nacional Marino Las Baulas (PNMB), created to protect leatherback

turtles, but these beaches lie just outside its area of protection. Because of the lack of

official status, poaching of eggs, presence of tourists on the beach and small artisanal

vessels fishing in the nearby waters are common.

Both the potential conservation gaps and the potential importance of this

unstudied breeding population motivated the present research. The main focus of this

dissertation was to study the movements and behavior of adults and hatchlings of East

Pacific green turtles from Costa Rica during different stages of their life. Through this

effort I intended to contribute to the general knowledge of sea turtle life cycles and to

identify areas in need of protection.

In Chapter 2, I identified high use internesting areas for turtles nesting on Nombre de

Jesús and Zapotillal beaches. I also determined the diving behavior and vertical habitat

6

use of the turtles. This information allowed me to highlight hot spots for conservation of

sea turtles in Northwestern Costa Rica.

In Chapter 3, I studied the reproductive status of East Pacific green turtles to assess their

clutch frequency and the duration of the internesting period to have a better

understanding of the nesting habits of this population.

In Chapter 4, I described the post nesting movements and behavior, and identified

foraging areas for the Costa Rican green turtles. I also analyzed oceanic characteristics

that may influence the movements and behavior of the turtles.

Finally, in Chapter 5, I estimated the dispersion of hatchlings emerging from Nombre de

Jesús in their post-hatchling stage by modeling currents in the Eastern Tropical Pacific.

7

References

Alvarado, J. and A. Figueroa. 1992. Recapturas post-anidatorias de hembras de tortuga

marina negra (Chelonia agassizii) marcadas en Michoacán, México. Biotropica

24: 560-566.

Amorocho, D. F. and R. D. Reina. 2007. Feeding ecology of the East Pacific green sea

turtle Chelonia mydas agassizii at Gorgona National Park, Colombia. Endangered

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13

Chapter 2: Diving behavior and movements of the East Pacific green turtle

(Chelonia mydas) during internesting in Costa Rica

Abstract

We attached hydrodynamic satellite transmitters by tether to 13 East Pacific green turtles

nesting on Nombre de Jesús and Zapotillal beaches to identify movements and diving

behavior, and to determine high use internesting areas in need of protection in

northwestern Costa Rica. Tracking duration ranged from 5-39 days. A fixed Kernel

density analysis showed that high use areas during internesting periods were close to the

nesting beaches; utilization distribution polygons of 50 and 95% included 4.5 and 53.9

km2 respectively. Turtles performed short dives (2-10 min) mainly in the upper 10 m of

the water column. U-shaped dives were shallow (3-5 m) and their modal duration ranged

from 8 to 23 min. These were probably animals resting at the bottom. Strong diel patterns

occurred in diving behavior during internesting with a significantly larger amount of time

spent at the surface during the night. The proportion of U-dives was negatively correlated

with surface time at night suggesting the turtles were floating at the surface as a resting

strategy and resting at the bottom during the day. The combination of movement and

behavioral data suggested that the turtles were staying near the nesting beach relatively

inactive during the internesting period. The depths of U-dives and depth of water in the

area indicated that the turtles used calm shallow areas to rest between successive nesting

events. This high concentration of nesting turtles and the lack of long distance

movements during internesting indicated the extensive use of the area by resting turtles.

This behavior was probably representative of the behavior of the whole population,

14

which indicated that this small area was of great importance for East Pacific green turtles

and likely a crucial location for conservation of this population.

15

Introduction

Marine animals spend most of their life in the ocean away from shore, which

makes it difficult to obtain direct observations of their behavior. Recently modern

technologies have allowed scientists to collect much more information on the ecology

and natural behavior of marine vertebrates (Wolcott 1995, Cooke et al. 2004, Altmann

and Altmann 2003). In particular, satellite telemetry has been widely used to analyze the

movements, behavior and physiology of marine mammals (Mate et al. 1999), fish (Block

et al. 1998), sea birds (Jouventin et al. 1994) and sea turtles (Morreale et al. 1996, Hays et

al. 2000, Eckert 2002, Seminoff et al. 2008, Shillinger et al. 2010).

Specifically, satellite telemetry and deployment of data loggers have helped us

understand different dive patterns in sea turtles involving depths, durations and ascent

and descent phases. These patterns vary widely within species and their immediate

environments. Several studies indicate that sea turtles display different dive types

associated with different life history phases (Minamikawa et al. 1997, Hays et al. 1999,

Hochscheid et al. 1999, Houghton et al. 2002). Whereas leatherback turtles (Dermochelys

coreacea) dive at an average maximum depth of 108 m during the internesting period off

northwestern Costa Rica (Shillinger et al. 2010) green turtles (Chelonia mydas) in the

Mediterranean only dive as deep as 25 m (Hochscheid et al. 1999) and loggerheads

(Caretta caretta) use an average depth < 20m during the internesting (Houghton et al,

2002). In addition, data loggers have revealed that different dive shapes are related to a

sea turtle’s underwater behavior (Minamikawa et al. 1997, Hays et al. 2000, Houghton et

al. 2002, Seminoff et al. 2006). Six types of dives have been recognized. Type 1 or “U”

16

dives are associated with resting behavior (Houghton et al. 2002, Hays et al. 2000) and

stationary foraging (Seminoff et al. 2006); Type 2 or “V” and Type 6 (W-shaped) dives

indicate underwater exploratory surveys or turtle orientation; Type 4 or “S” dives may

relate to energy savings while returning to the surface using positive buoyancy

(Hochscheid et al. 1999). Finally, Types 3 and 5 have been linked to foraging activity

(Seminoff et al. 2006). Different dive types have been recognized during the internesting

in sea turtles (U-dives, V-dives, S-dives) but the predominant dive during that period is

the U-dive (Hays et al. 1999, Hochscheid et al. 1999, Houghton et al. 2002).

The behavior of turtles during the internesting period appears to be driven by

energy optimization. For example, lack of food availability in some reproductive areas

causes turtles to spend most of the time resting during the internesting period (Hays et al.

1999, Reina et al. 2005). On the other hand, some populations forage during internesting

(Houghton et al. 2002, Fossette et al. 2008, Tucker and Read 2001). These differences

are related to the conditions of the nesting grounds (Hays et al. 2002a).

The green turtle is listed as endangered by the IUCN. In particular the population

in the Eastern Pacific is classified as endangered by the US and considered highly

vulnerable to extinction. The decline in the eastern Pacific was due to harvest of eggs and

adults, habitat degradation at nesting beaches and feeding grounds and by-catch from

fisheries in the ocean (Seminoff 2004)

The objective of this study was to examine the movements and identify the dive

behavior of green turtles during internesting periods, as well as to determine their vertical

habitat use along the Pacific Coast of Costa Rica. To our knowledge, this is the first study

17

on internesting movements and behavior of the East Pacific green turtle. These data will

help elucidate high use internesting areas in need of protection in northwestern Costa

Rica.

Materials and Methods

Study site

To monitor individual East Pacific green turtles, we deployed 13 ARGOS-linked

satellite transmitters from August 2007 to October 2007 and an additional one in

November 2009. The study took place at three nesting beaches on the Nicoya Peninsula

in Northwest Costa Rica. We attached 12 transmitters on turtles on Nombre de Jesús (10°

23’ 30” N; 85° 50’ 07” W), a 1 km stretch of beach and on its neighboring 700 m beach,

Zapotillal (10° 23’48”N; 85°49’48”). These beaches hosted an important aggregation of

nesting green turtles (~15 turtles/night during peak season) and were located just north of

Parque Nacional Marino Las Baulas (PNMB), which was created to protect leatherback

turtles (Dermochelys coriacea), but they were just outside its area of protection.

Therefore, poaching of eggs, presence of tourists on the beach and small artisanal vessels

fishing in nearby waters were common. We also attached one transmitter on a green turtle

on Playa Ventanas a 1.1 km stretch beach in PNMB where green turtles sometimes nest

as well.

18

Turtle measurements

To intercept the turtles we patrolled Nombre de Jesús, Zapotillal and Playa

Ventanas at night. Each turtle encountered on the beach was scanned for a Passive

Integrate Transponder (PIT tag). If they did not have one, we injected a PIT tag into the

right front flipper for later identification. We measured the curved carapace length, CCL

+/- 0.5 mm of every tagged turtle with a flexible meter tape and we checked them for

scars or lesions. Additionally some of the turtles were scanned with ultrasound to assess

their reproductive status, enabling us to see future clutches (Chapter 3)

Satellite transmitter attachment

Sea turtles have a streamlined shape that minimizes hydrodynamic disturbance

when they are moving through the water. This characteristic undoubtedly minimizes

energy expenditure while they swim. Therefore, any disturbance in the shape of the turtle

will cause flow separation increasing drag (Schlichting 1979, Denny 1993), and

consequently increasing energy expended by the turtle (Watson and Granger 1998).

Two different methodologies have been used to attach satellite transmitters to sea

turtles: lying on the carapace and trailing behind the turtle. Commonly for hard-shelled

turtles a rectangular transmitter is attached to the anterior top-most part of the carapace

(Plotkin et al. 1995, Balazs et al. 1996, Papi et al. 1997, Hays et al. 1999). However, this

placement increases drag due to the disturbance of the carapace’s shape potentially

causing a 13% increase in travel time and increasing energy consumption by 13 to 27%

(Watson and Granger 1998). For this method drag is even greater when the transmitter is

placed more anteriorly on the carapace where they are commonly attached (Logan and

19

Morreale 1994). Another method is to attach the transmitters using a tether, a technique

first developed by Standora et al (1982) and modified by Morreale et al (1996) and

Morreale (1999). In this technique the transmitter trails behind the turtle without

disturbing shape and flow across the carapace. The buoyant and hydrodynamic

transmitter follows closely behind the turtle and floats with the antenna out of the water

when the turtle rises to the surface. A further benefit to this technique is that the

attachment can be performed in a short period of time with minimal disturbance of the

turtle’s natural behavior while it is on the beach. The main disadvantage of this technique

is the potential for shorter duration of tracks due to the smaller batteries and the shedding

of the transmitter when the tether breaks. Balancing all of these factors we opted to use

tether transmitters for this study.

When we determined that a turtle was suitable for attachment we cleaned the

marginal posterior scute of the carapace with 70% alcohol, and made a 3 mm diameter

incision with a sterile electric drill bit (battery-powered electric drill). Immediately after

the incision we applied lidocaine and betadine antiseptic solution and inserted sterile

surgical tubing into the small hole through the overhanging edge of the scute. We

positioned plastic buttons with Y shaped holes above and below the carapace to avoid

friction and wearing damage to the carapace. The transmitter was connected to the

buttons on the carapace by a flexible lanyard (monofilament fishing line, 400 lb test) that

passed through the holes and was secured to itself with a corrosive metal crimp. To avoid

entanglement or long-term impediment of the turtles, we placed in line swivels and

crimps that would breakaway with corrosion (Figure 2.1). The attachment process took

20

from 7 to 15 min for all turtles and was performed when the turtle was covering the nest

after laying eggs, thus minimizing the impact on its nesting behavior.

Satellite transmitters

We attached transmitters to 13 female green turtles at Nombre de Jesús, Zapotillal

and Playa Ventanas (Table 2.1) to track their movements and analyze diving behavior.

The satellite transmitters (Wildlife Computers Mk-10 PAT Pop up archival transmitting

tag) were configured to transmit opportunistic transmissions, so we could obtain real time

location data.

We customized the satellite tags with a buoyant case made out of syntactic foam.

Satellite transmitters weighed ~115 g (≈ 0.2 % of the turtle mass), had a hydrodynamic

shape and were tethered behind, all resulting in minimized drag. The transmitter’s

positive buoyancy was 36 g, enough to bring the antenna of the transmitter out of the

water each time the turtle surfaced but very minimal for adult green turtles. We

programmed the tags with duty cycles of 10 h on / 14 h off (0:00-9:00 h/ 10:00-23:00 h

local time) to optimize battery life. The transmitter sampled and summarized dive depth,

dive duration and time at depth data in categorized bins: Dive depth: 5, 10, 15, 20, 25, 30,

35, 40, 45, 50, 75, 100 and 200 m; Dive duration; 2, 5, 10, 15, 20, 25, 30, 40, 50, 60, 70,

80 and 90 min.

Dive and movement analysis

The location of the animals and the summarized satellite messages were

transmitted via the Argos system. To analyze the areas used by the turtles we performed a

21

Kernel Density Analysis using ArcGIS and Home Range Tools for ArcGIS (Rodgers et

al. 2005). We performed a fixed kernel density analysis using the least-squares-cross-

validation method (LSCV) to calculate the smoothing factor. The core areas were

determined by 25, 50, 70 and 95 % Utilization Distribution (UD).

We analyzed the daily displacement of the turtles by calculating the distance between

all points travelled in a given day. We then calculated the total movement in the first 10

days after a successful nesting event. We used 10 days because it was the shortest

internesting time recorded in this study to have a representation during the internesting.

We also compared turtle size (CCL) to the distance covered in 1 and 10 days, to analyze

if the size of the turtle had an influence on displacement.

We analyzed diving behavior of turtles from the summarized dive information

obtained from the Argos messages and from the more detailed data retrieved from

satellite transmitters that were later recovered.

The summarized dive information allowed us to calculate the percentage of dives

accumulated in 4 hour period at different depths for all turtles and the average duration of

dives, although these data did not allow us to determine the specific number of dives that

the turtles performed during the tracking period.

We were able to later retrieve four satellite transmitters, which archived complete

detailed information on the animal’s diving behavior including every dive performed by

the turtle during the tracking period (date, time, water temperature, dive depth, duration,

bottom time, surface time, etc). This allowed us to identify, analyze, count and classify

individual dives.

22

From the retrieved satellite transmitters we analyzed the relation between the total

duration of dives and their depth. Also, we specifically separated the U-dives from the

total dives. These dives were characterized by a steady descent phase followed by a

period of time at a constant depth followed by a steady ascent phase (Hochscheid et al.

1999). U-dives are commonly related to resting behavior, which appears to be the main

activity during the internesting period of sea turtles. To identify U-dives we calculated

the relation between total duration of an individual dive and the time at the bottom. If the

time at the deepest depth was 90% or more of the dive, it was considered a U-dive (Hays

et al. 1999). We calculated the proportion of U-dives at depth and their duration for every

turtle. We calculated the proportion of U-dives in relation to all other dives for individual

turtles. Additionally, we studied the behavior of turtles during the day and night. Based

on the hours of light in the study area 05:30 to 17:30, night corresponded to 17:30 to

05:30. We calculated and compared the surface time for each turtle during day and night

and also compared it to the percentage of U-dives performed by each turtle. All

statistical analyses were performed using SPSS. Data are reported as mean ± SD.

Internesting Interval

From tagged individuals, we calculated the observed internesting period (OIP) as

the number of days between observed successful nesting events (Reina et al. 2002). The

mean reported internesting interval for green turtles is 12 days (ranging from 10-17days)

(Miller 1997) therefore data where the observed interval was higher than 17 days were

excluded from the analysis.

23

Additional observations

We made observations of activity on the beaches including presence of tourists

and illegal egg collectors (poachers). We also recorded the presence of fishing activity in

the area and the occurrence of male and female green turtles near the nesting beaches.

Results

In all, we attached satellite transmitters to 13 turtles with CCL from 82.0 to 89.5

cm (mean ± SD = 84.9 ± 2.5 cm). Duration of satellite attachment for all internesting

turtles ranged from 5 to 39 days (mean ± SD = 19.3 ± 3.2 days) (Table 2.1).

Several transmitters were removed by egg collectors at night and moved to

different localities of Costa Rica. Others were taken by fisherman in the ocean. On two

separate occasions the transmitters were brought to land by artisanal fishing boats. Those

transmitters were transported to a small fishing village, and it was not possible to recover

them. Before transmissions ended we did track one transmitter as it moved around

Guanacaste, but we could not catch up to it for recovery. In general, premature release

was due to the transmitter releasing itself through a failure in the popup emergency

release mechanism and to its removal from the turtle by people.

Internesting areas

Observed internesting periods exhibited a mean of 12 days (range 10-15 days, N = 25.

Internesting areas ranged from north of Brasilito Bay to Playa Langosta in PNMB in the

south (Figure 2.2) both within 15 km of the nesting beach. Turtles spent most of the time

24

in waters even closer to the nesting beaches during internesting, limiting their travel to 1-

4 km off the nesting beaches. Kernel density analysis showed UD polygons of 25, 50, 75

and 95% included 1.6, 4.5, 9.4 and 53.9 km2 respectively (Figure 2.2). Notably

approximately 39% of the 25% UD was contained within the Bay of Nombre de Jesús,

34% corresponded to the Bay of Zapotillal and the remaining 27% was in the southern

part of neighboring Conchal Bay. One of the turtles showed a broader movement

swimming 50 km south of the nesting beach. All the turtles tagged in the present study

were between nesting emergences; we recorded the majority of these turtles nesting at

least once more through satellite locations and direct beach observations. Additionally,

some of these turtles were scanned with ultrasound as part of a different study. This

enabled us to see more future clutches (Chapter 3).

During internesting the mean daily distance travelled by turtles was 4 ± 3 km

Mean distance covered in 10 days was 52 km. There were no significant correlations

between daily displacement of turtles and the CCL (p = 0.119) and the movements in 10

days and CCL (p = 0.233).

Diving behavior

Of all dives, during internesting 69% were performed in the first 5 m of the water

column with an additional 20% to depths between 5 and 10 m (Figure 2.3a). Likewise,

most dives were of short duration, between 2 and 10 min (71%) (Figure 2.3b).

We retrieved four of the satellite transmitters, from which we obtained archival

information on the detailed diving behavior for individuals. The total number of dives for

each turtle was: Turtle 1 = 1375, Turtle 2 = 833, Turtle 3 = 725 and Turtle 4 = 3692.

25

Mean water temperature recorded by the transmitter during internesting was 27.5 ± 1.0

°C.

Even though we recognized different dive types (V-shaped dives, S- shaped dives,

W- shape dives) in the dive profiles of the four turtles, we focused our analysis on U-

dives because they were described as the predominant dive type that sea turtles perform

during the internesting period (Hays et al. 1999, Hoscheid et al. 1999, Houghton et al.

2002) and they were the predominant dive type in our study.

The percentage of dives that were U-dives performed by the turtles were: Turtle

1: 21%, Turtle 2: 31.6%, Turtle 3: 9.9% and Turtle 4: 31.2%. The U-dives were

characterized by shallow ultimate depths with 79.3% (± 9.2) of dives ranging between 3-

5 m (Figure 2.4). The modal durations of dives were 8 min, 11.5 min, 15 min and 23 min

for all four turtles respectively (Figure 2.5).

The relation between depth and duration was weakly explained by a regression for

all four turtles (Figure 2.6). Dives were mainly performed in the first 10 m of the water

column independently of their duration. Turtle 4 performed the deepest dive (110 m) in

10 minutes and the longest dive, 55 min to a depth of 18 m.

During the internesting period green turtles exhibited a strong diel pattern in their

submergence behavior. Dive profiles exhibited that two turtles (1 and 3) spent a

significant amount of time at the surface at night as opposed to turtles 2 and 4 (Figure

2.7) that spent most of their time diving. Overall, we found significant differences when

comparing the surface time during day and night (ANOVA, F = 48.775, df1, 17; p < 0.01)

(Figure 2.8).

26

We also compared the proportion of U-dives performed during the day and night

with the time spent at the surface (Figure 2.9a). Turtles spent more time at the surface at

night and more time performing U-dives during the day. Total time of entire tracking

duration spent involved in those activities together (U-dives and surface time) was 73 %

(± 4.73) (Figure 2.9b), which gave an indication of great amount of time spent resting

during internesting.

Due to the differences in the total of U-dives between individual turtles; we

compared the proportion of U-dives and the total time spent at the surface during the

night (Figure 2.10). We found a strong negative regression despite the small sample size,

between U-dives and surface time during the night (r² = 0.930, p < 0.05, N = 4).

Additional observations

We estimated that 90% of the eggs were taken by illegal egg collectors on

Nombre de Jesús and Zapotillal beaches unless researchers or rangers were on the beach.

We also observed 10 longlines on different occasions and several gill nets set up in the

water within sight of the nesting beaches. Gill nets were set for durations of at least 12 h.

Simultaneously with our study colleagues reported several green turtles hooked on

longlines in the nearby Gulf of Papagayo near the nesting beaches. Male green turtles

also were present in the area and we observed several copulating pairs of green turtles

near the nesting beaches during both day and night.

27

Discussion

Our data indicated that the internesting interval for the East Pacific green turtle

population nesting in Costa Rica was 12 days. It was shorter than the 14 days reported at

Ascension Island by Carr et al. (1974) and at Tortuguero, Costa Rica (Bjorndal and Carr

1989). The internesting period is the time that it takes for the turtle to develop the next

clutch, thus it is a direct representation of the ovulation, fertilization and shelling of the

following clutch (Rostal 2007). Ovulation, fertilization and albumen deposition occur

within the first 3 days after nesting (Wibbels et al. 1992) and in the remaining time the

eggs are shelled in the oviduct.

Egg development is directly affected by temperature in the surrounding

environment (Sato et al. 1998). Standora et al. (1982) reported water temperatures at

Tortuguero between 27.5 and 28.5 ºC and Hays et al (2002b) reported water temperatures

at Ascension Island close to 28ºC. The mean water temperatures from this study varied

between 27.5 and 27.9 ºC. The similarity in the water temperatures of the three areas

indicated that the shorter internesting interval of the green turtles in Costa Rica was not a

result of higher temperatures. We believe that the difference in the duration of

internesting interval may be related to differences in size of the turtles and number of

eggs per clutch (Bjorndal and Carr 1989, Broderick et al. 2003, Wallace et al. 2006).

Internesting Movements

Satellite tracking indicated that the areas of importance during the internesting

period of green turtles that nested on Nombre de Jesús and Zapotillal beaches were the

waters off the nesting beaches in nearby Brasilito Bay (4 km north of the nesting beach).

28

Turtles mainly remained in a particularly small area (4.5 km2- 50% UD) near the nesting

beaches. The turtle that nested on Playa Ventanas used a broader area, but even this was a

relatively small area, ranging from the nesting beach to 12.5 km south along the Nicoya

Peninsula. These limited internesting movements underscore the importance of coastal

waters near the nesting beaches.

Contrary to our findings, green turtles on the Caribbean coast of Costa Rica travel

from 30 to approximately 100 km off shore during internesting (Tröeng et al. 2005). Our

results also differ from the behavior described for leatherback turtles that nest at nearby

PNMB that travel hundreds of kilometers during the reproductive season (Shillinger et al.

2010)

The mean daily distance traveled by the green turtle was 4.6 km. There was little

variation between turtles, and these differences apparently were not related to turtle sizes

as was reported for leatherback turtles (Eckert 2002). In contrast to overall movements,

distances covered in a day for these green turtles were similar to the daily distance

traveled by leatherback turtles at nearby PNMB (Shillinger et al. 2010)

Dive behavior

The binned data obtained from the satellite transmitters indicated that, during

internesting, turtles dive mostly between depths of 2 and 10 m (90% of the dives)

performing mainly short dives. The depth of the majority of the dives corresponded to the

depth in the area where the turtles stayed during the internesting interval indicating that

diving behavior of the turtles was mainly influenced by bathymetry of the internesting

area and turtles mainly dove to the bottom. Along Nombre de Jesús the depth ranged

29

from 0 to 3m in the first 300 m off the coast and depth increased to 10 m at 900 m away

from the coast. Conditions were similar in Brasilito Bay reaching 10 m of depth at 1.3 km

from the coast. The mean dive depth of this population was similar to the mean depth

described for internesting green turtles in Ascension Island (Hays et al. 2000, Hochschied

et al. 1999), and loggerheads in the Mediterranean (Houghton et al. 2002).

Dive data obtained from the transmitters that we recovered indicated that the

predominant depth for U-dives ranged from 3 to 5 m reinforcing the assumption that

these turtles rested mainly on the bottom. Turtles did more U-dives during the day than at

night. U-dives are related to resting behavior because turtles remain at a fixed depth for a

period of time; this depth often is the bottom (Minamikawa et al. 1997, Hays et al. 2000).

U-dives have widely been considered to represent resting activity on the sea floor,

although on occasion some other activities such as foraging or movement along the

bottom may occur (Hochscheid, et al 1999, Seminoff et al. 2006). Although some

populations do not forage due to lack of food in the internesting areas (Hays et al. 2000,

Reina et al. 2005), other sea turtle populations do feed during the breeding season

(Houghton et al. 2002, Fossette et al. 2008, Tucker and Read 2001). We could not

observe our turtles in the water, so we cannot rule out foraging behavior. However, there

is no seagrass, and little algae are present on the bottom in the area near the nesting beach

(Reina et al. 2005, Bernecker and Wehrtmann 2009). Therefore, these turtles were

probably resting at the bottom. Duration of U-dives varied with individual turtles from 8

to 23 min. There was no relationship between dive depth and dive duration for U-dives as

found in other populations (Houghton et al. 2002), although we found a weak relationship

between depth and duration including all dive types. In this study the turtles spent a

30

relatively short proportion of the overall time carrying out U-dives in relation to other

studies (Hays et al. 2000).

Green turtles in our study area spent a large amount of time at the surface and the

majority of the surface time occurred at night. One individual spent the longest

consecutive time at the surface (12 hours at night). A basking sea turtle can increase its

body temperature almost 4 ºC by exposing a substantial portion of the carapace to the sun

(Spotila and Standora 1985). Our study showed that turtles were at the surface at night so

they were not basking, but rather were probably resting. Because floating at the surface

during the day in the warm waters off the beach would cause an increase in their body

temperature (Spotila et al. 1997) the turtles avoiding heating by diving to the bottom to

rest during the day.

U-dives, probably related to resting behavior, mainly took place during the day

and there was a strong tendency for the turtles to go to the surface when the sun set.

There was a negative correlation between the total surface time and the percentage of U-

dives performed during the internesting indicating that the turtles that lay on the surface

more at night invested less time doing U-dives during the day. Combining the time

turtles spent at the surface at night and in U-dives during the day it appeared that east

Pacific green turtles invested 73 % (± 4.73) of their total time during the internesting

interval resting while their eggs are being developed in the oviducts.

During internesting turtles need to save energy to yolk up and shell eggs, crawl to

the beach and lay the eggs several times in the season. Green turtles in this study

remained close to the nesting beach and rested most of the time during the internesting

31

period. These behaviors reduced energy expenditure during the nesting season which

could be a significant cost for reproduction (Wallace et al. 2005). During the reproductive

season sea turtles mainly rely on stored lipids to support metabolism and reproduction

(Hamann et al. 2002) especially in areas where food is not plentiful. The mechanism of

floating at the surface for resting may be less costly in terms of energy than diving. It has

been suggested that one of the adaptations for sea turtles to dive is to avoid predation

(Lutcavage and Lutz 1997). However, by staying close to the beach this Costa Rica green

turtle population may be less exposed to predation than other populations, which would

allow it to rest at the surface for long periods of time at night.

Conservation Implications

Female green turtles spent the internesting period close to the nesting beaches in

Northwestern Costa Rica and used the complete water column, which was very shallow.

Males are present in the waters off the nesting beaches and we often observed mating in

the waters off the beach. Therefore, several parts of the life cycle of this population are

occurring in this small portion of Costa Rica and this area is of great importance for the

conservation of this population. At the same time there was heavy fishing pressure in this

area. On two occasions, transmitters were brought to land by artisanal fishing boats

indicating that turtles were being captured by fisherman during the internesting period. In

addition, we observed turtles caught on longlines nearby. Gill nets were common in the

area.

During the course of this study we estimated that 90% of the eggs were taken in

Nombre de Jesús and Zapotillal by egg collectors, unless biologists or rangers were on

32

the beach and secretly relocated the clutches. Despite the Costa Rican law that prohibits

the egg harvest on every beach in Costa Rica except Ostional (Spotila and Paladino 2004)

poaching of eggs is very common in areas that are not protected within a National Park.

East Pacific green turtles nest along the coast of Guanacaste in low numbers with more

concentration in some beaches like Nombre de Jesús and Zapotillal. Moreover none of

these beaches have law enforcement and there is little or no control over

commercialization of eggs in the area.

At least four sea turtle species nest along the coast of Guanacaste, Costa Rica:

olive ridley turtles (Lepidochelys olivacea), green turtles, leatherback turtles and

hawksbill turtles (Eretmochelys imbricata) (Cornelius 1979). With all these species in

danger of extinction, urgent action must take place in Costa Rica to save these important

populations. The intensive poaching that is taking place on Nombre de Jesús may lead to

a decline in the population as has already happened with the leatherback population in

PNMB (Santidrián Tomillo et al. 2008). Because there is no previous information on the

number of females nesting on these beaches, it will be difficult to determine if the impact

of the egg poaching is already affecting these numbers. Nevertheless, it is essential that

enhanced protection be provided both on the beaches and in the waters of Northwestern

Costa Rica where there is a previously unreported large breeding population of the highly

endangered East Pacific green turtle.

33

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http://www.sciencedirect.com/science?_ob=PublicationURL&_tockey=%23TOC%236808%231992%23999129998%23524750%23FLA%23&_cdi=6808&_pubType=J&view=c&_auth=y&_acct=C000007158&_version=1&_urlVersion=0&_userid=95578&md5=26e05de859c5c68d76539d8a3b733c19

39

Tables

Table 2.1: Attachment data for 13 eastern pacific green turtles (Chelonia mydas)

during the nesting season in Costa Rica. All individuals included in the study were in

their internesting interval. *Transmitters recovered after premature release. #Transmitters

probably removed by fisherman.

ID Attachment

date Beach CCL (cm) CCW (cm) Days of

transmission

1* 26-Aug-07 Zapotillal 87.5 79.0 10 2* 2-Sep-07 Zapotillal 82.0 80.0 8 3* 9-Sep-07 N. Jesús 89.0 84.0 5 4* 22-Oct-07 Zapotillal 82.0 76.0 29

5 25-Aug-07 N. Jesús 89.5 85.9 11 6 22-Oct-07 Zapotillal 86.1 83.0 39 7 22-Oct-07 Zapotillal 82.2 81.8 25 8 24-Oct-07 Ventanas 82.0 ---- 24

9# 27-Oct-07 Zapotillal 86.5 71.5 16 10 27-Oct-07 Zapotillal 85.0 83.5 39

11# 27-Oct-07 Zapotillal ---- ---- 11 12 27-Oct-07 Zapotillal 84.5 78.3 22 13 6-Nov-09 N. Jesús 84.4 82 12

40

Figures

Figure 2.1: Satellite transmitter attachment to an East Pacific green turtle. a)

posterior marginal scute. b) upper plastic button. c) flexible lanyard (400 lb monofilament

fishing line). d) corrosive link with metallic crimps and swivel. e) Satellite transmitter

(Mk 10 PAT tag, programmed for opportunistic transmissions)

41

Figure 2.2: Fixed Kernel density analysis. Internesting areas occupied by East

Pacific green turtles. Areas highly used are Nombre de Jesús (NJ), Zapotillal (Z), the

Bay of Playa Brasilito (PB) and, Playa Conchal (PC). PNMB: Parque Nacional Marino

las Baulas, PL: Playa Langosta. Utilization Distribution (UD) 25% = 1.57 (red), 50% =

4.5 (orange), 75% = 9.4 (light green) and 95% = 53.9 km2 (dark green). Scale (from white

to blue) represents depth (meters). Insert shows location on map of Costa Rica.

PacAme

rshift

Value -10,6

54 - -6,00

0

-5,999.99

9999 - -5

,000

-4,999.99

9999 - -4

,000

-3,999.99

9999 - -3

,000

-2,999.99

9999 - -2

,500

-2,499.99

9999 - -2

,000

-1,999.99

9999 - -1

,500

-1,499.99

9999 - -5

00

-499.999

9999 - -2

50

-249.999

9999 - -1

25

-124.999

9999 - -3

0

-29.99999

999 - -10

-9.999999

99 - 0

0 - 50

50.00000

001 - 125

125.0000

001 - 500

500.0000

001 - 1,0

00

1,000.00

0001 - 2,0

00

2,000.00

0001 - 3,0

00

3,000.00

0001 - 4,0

00

4,000.00

0001 - 5,0

00

5,000.00

0001 - 6,0

00

6,000.00

0001 - 7,0

00

pacamer

shift

VALUE 1; 2;

3; 4; 5; 6

; 7; 8; 9; 1

0

-10; -9; -

8; -7; -6;

-5; -4; -3

; -2; -1

-19; -18;

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; -4,022; -

4,021; -4

,020; -4,0

19; -4,01

8; -4,017

; -4,016; -

4,015; -4

,014; -4,0

13; -4,01

2; -4,011

; -4,010; -

4,009; -4

,008; -4,0

07; -4,00

6; -4,005

; -4,004; -

4,003; -4

,002; -4,0

01; -4,00

0

42

Figure 2.3: a) Percentage of dives culminating at specific depth intervals during

internesting for 13 East Pacific green turtles from satellite data obtained through

Argos and summarized in bins. We calculated the average at depth in relation to the total

dives for each turtle. b) Percentage of duration intervals of dives during internesting

for 13 East Pacific green turtles from satellite data obtained through Argos and

summarized into bins. We calculated the average duration in relation to the total dives for

each turtle.

0

10

20

30

40

50

2 10 20 30 50 70 90

Div

es (

%)

Duration (min)

0 10 20 30 40 50 60 70 80

5

20

35

50

200

Dives (%)

Dep

th (

m)

43

0

10

20

30

40

50

0 5 10 15 20 25 30

U-D

ives

(%

)

Depth (m)

Turtle 3

0

10

20

30

40

0 5 10 15 20 25 30

U-D

ives

(%

)

Turtle 1

0

10

20

30

40

0 10 20 30 40

Depth (m)

Turtle 4

0

10

20

30

40

0 10 20 30 40 50

Turtle 2

Figure 2.4: Percentage of U-dives of East Pacific green turtles ending at

different depth intervals during internesting. The proportion of U-dives at depth

was calculated in relation to the total U-dives for each turtle taken from data logged

in the transmitter.

44

0

3

6

9

12

15

3 9 15 21 27 33 39 45 51Duration (min)

Turtle 4 N = 1152

0

3

6

9

12

15

3 9 15 21 27 33 39 45

Turtle 2N = 263

0

3

6

9

12

15

3 9 15 21 27 33 39 45

U-D

ives

(%

)

Duration (min)

Turtle 3N = 72

0

3

6

9

12

15

3 9 15 21 27 33 39 45

U-

Div

es (

%)

Turtle 1N = 289

Figure 2.5: Duration intervals of U-dives of East Pacific green turtles during the

internesting. The duration of U-dives was calculated in relation to the total number of

U-dive for each turtle. Complete data were taken from satellite transmitters recovered.

45

0

10

20

30

40

0 20 40

Du

rati

on

(m

in)

Turtle 1 N=399

0

10

20

30

40

0 20 40

Du

rati

on

(min

)

Depth (m)

Turtle 3 N = 283

0

10

20

30

40

50

0 10 20 30 40 50 60 70 80

Turtle 2 N = 543

0

10

20

30

0 50 100 150Depth (m)

Turtle 4 N = 2894

Figure 2.6: Regression of dive depth and dive duration including all dive types

for East Pacific green turtles during internesting (p < 0.01). Turtle 1: r²= 0.215,

Turtle 2: r²= 0.213, Turtle 3: r² = 0.455 and, Turtle 4: r² = 0.01. Data recovered

from satellite transmitters.

46

Figure 2.7: Dive profiles for East Pacific green turtles. Black lines represent depth and

gray lines represent light levels. Elevated light levels represent daytime and low light

levels represent nighttime. Turtle 2: Dives performed during day and night. Turtle 3:

dives mainly performed during the day with prolonged time at surface during the night.

0

10

20

0

100

200

300

De

pth

Lig

ht

Turtle 3

Light Level Depth

0

30

60

900

100

200

300

De

pth

Lig

ht

Turtle 2

47

Figure 2.8: Difference between surface times of East Pacific green turtles during day

and night. Day represents the 12 hours of light in the tropics. Days 1 to 4 includes 4

individuals; days 5 to 9 include 3 individuals. Day 1: first day after successful nesting

(transmitter attachment). The percentage of time at the surface was calculated in relation

to the total surface time during the 12 hour of light or darkness each day.

0

20

40

60

80

100

Day 1 Day 3 Day 5 Day 7 Day 9

Tim

e (%

)

Day Night

48

Turtle 1

0

20

40

60

80

100

0:00 6:00 12:00 18:00

Tim

e(%

)

Surface Time U-Dives Time

0

20

40

60

80

100

0:00 4:00 8:00 12:00 16:00 20:00

Turtle 2

0

20

40

60

80

100

0:00 4:00 8:00 12:00 16:00 20:00

Tim

e(%

)

Turtle 1

0

20

40

60

80

100

0:00 4:00 8:00 12:00 16:00 20:00

Tim

e (%

)

Turtle 3

a

Turtle 1

0

20

40

60

80

100

0:00 6:00 12:00 18:00

Tim

e(%

)

Surface Time U-Dives Time

0

20

40

60

80

100

0:00 4:00 8:00 12:00 16:00 20:00

Turtle 4

49

0

20

40

60

80

100

0:00 4:00 8:00 12:00 16:00 20:00

Tim

e (%

)

Surface time U-Dives Total

Figure 2.9: a) Surface time and U-dives during the internesting for 4 East Pacific green turtles. The shaded areas represent night

(12 dark hours). Each data point represents an interval of 2 hours. b) Proportion of time spent at the surface and u-dives

performed at different times of the day for 4 East Pacific green turtles. Total represents the sum of the proportion of time spent at

surface and the proportion of U-dives performed by the turtles. Each data point represents an interval of 2 hours.

b

50

Figure 2.10: Correlation between the total time spent at the surface during the night

and the total U-dives performed during the internesting by East Pacific green turtles

(p<0.05, r² = 0.930). U-dives were calculated in relation to the total number of u- dives

performed by each turtle during the internesting. Surface time was calculated in relation

to the total time spent at the surface at night during the internesting.

Turtle 3

Turtle 1

Turtle 2

Turtle 4

R2 = 0.93050

20

40

60

80

100

0 10 20 30 40

U-Dive %

Surf

ace

tim

e at

nig

ht

(%)

51

Chapter 3: Reproductive Output and Ultrasonography of an Endangered

Population of the East Pacific Green Turtle.

Abstract

Reproductive output is one of the most relevant aspects of life history; the lack of this

information can hinder management plans and conservation efforts. The goal of this

study was to analyze the reproductive output of the endangered East Pacific green turtle

nesting on Nombre de Jesús in Costa Rica; supplementing beach patrols and estimation

of clutch frequency with ultrasonography. Through the ultrasound scans we were able to

classify the reproductive status of females based on the stage of their ovaries in: early

stage (2 or more clutches), late stage (1 more clutch) and depleted ovaries (no more

clutches). We also encountered turtles with shelled eggs returning to the water which

coincided with disturbances on the beach such as egg collectors and/or tourists. We

calculated the ECF (mean ± SD) 3.5 ± 1.8 (N=24) and added the information on the

individual turtle ovaries to obtain the new ECFU (mean ± SD) 5.2 SD = 1.3. This

reproductive output is higher than previously described for East Pacific green turtles. Our

study illustrated that the use of ultrasound as a non-invasive technique was an effective

way to accurately determine the reproductive status and reproductive effort of green

turtles. This key parameter provides knowledge on the number of females, annual

fecundity, hatchling production and it can also influence male’s breeding strategies. On

one side, higher individual output could represent a healthier population; on the other

hand it could decrease number of females previously estimated. Given the need for

52

accurate demographic data on sea turtle populations this technique should be used in

nesting beaches studies. Our data along with the observations of egg poaching and

uncontrolled tourism indicated that there is a great need to protect Nombre de Jesús

because it hosts a high reproductive East Pacific green turtle population.

53

Introduction

Reproductive output is one of the most important aspects of life history; it is

fundamental to understand the reproductive biology of a species, which is essential for

developing effective conservation and management plans for individual populations. For

sea turtles, many key aspects of reproduction have been difficult to study in the wild. As

a result, little information is available regarding mating systems, lifetime reproductive

output, and male and female reproductive strategies. This very lack of knowledge often

hampers conservation efforts.

As a result of some thorough earlier studies, we do know some key steps in the

reproductive biology of sea turtles. In general, mature female sea turtles have a pair of

ovaries where follicles develop and become enlarged prior to mating (Owens 1980,

Rostal et al. 1990). Usually sometime after mating, enlarged follicles are ovulated into

the paired oviducts where they are fertilized and sheathed in albumen and shell material

(Owens 1980). The ovaries and oviducts function synchronously during the reproductive

season (Rostal et al. 2007), in which a single female will deposit anywhere from two to

many clutches of eggs over a period of many weeks. Where and when the different steps

in the female reproductive process occur has direct bearing on both female and male

reproductive strategies. Undoubtedly, these strategies are directly relevant to

conservation plans for individual species and populations of sea turtles; namely, where

and when is it most effective to focus our energies.

For adult female sea turtles, all the energy needed for reproduction is accumulated in

the foraging areas prior to migration. Eight to eleven months prior to the breeding season,

54

they start a period of ovarian recrudescence where lipids are allocated and ovarian

follicles start developing (Hamann et al. 2002). This is the process of vitellogenesis,

which consists of the enlargement of ovaries and follicles before reproduction, and during

which there is an incorporation of yolk proteins in the oocyte within the follicle (Rostal

2007). At this stage the females do not have fully mature follicles, but the ovary has

several size classes of vitellogenic follicles that represent the number of clutches the

turtle will lay during the season (Owens 1980, Etches and Petitte 1990, Rostal et al.

1998). These follicles continue to increase in size during pre-mating and mating periods

(Rostal et al. 1990). For female turtles at the foraging grounds, a drop in estrogen and an

increase in progesterone level may signal the beginning of the migration to distant

nesting beaches (Owens 1997).

As female sea turtles get closer to the nesting season, they become receptive to the

mating advances of males. At this stage the ovaries are completely developed (Rostal et

al. 1998) and the final stages of follicular maturation begin (Owens 1980). Mating

apparently occurs immediately prior to and at the beginning of the nesting season

(Fitzsimmons 1998, Pearse and Avise 2001). It has been suggested that the first

ovulation of the nesting season takes place several weeks after mating in loggerhead

(Caretta caretta) and green turtles (Chelonia mydas) (Fitzsimmons 1998, Owens 1997).

However, Manire et al. (2008) indicated that after successful intromission, ovulation may

occur within a few days. It is the timing of the final stages of the female reproductive

cycle and the mechanism of successful fertilization of the season’s eggs that will greatly

influence the behavior and locations of male sea turtles in the population.

55

There is a possibility that free sperm in the oviducts from the male chelonids can

contribute greatly to the female’s next clutch (Pearse and Avis 2001). Such a mating

system would favor a male that migrates to a nesting area to copulate with pre-ovulatory

females (Owens 1980, Carr et al. 1974). However, many other systems could favor males

that breed in foraging areas prior to female migration, or in courtship or staging areas

along migratory routes, removed from the nesting and feeding areas (Miller 1997, Jessop

et al. 1999; Schroeder et al. 2003, Bowen and Karl, 2007). It is common for chelonid

females to store sperm in the oviducts, sometimes for extended periods (Gist and

Congdon 1998, Fitzsimmons 1998, Uller and Olsson 2008). This mechanism of delayed

fertilization could tip the scales in favor of early mating males, possibly those that breed

prior to female migration. The benefits to early breeding males would be further

enhanced with a mating system that favors the first male that copulates, which may be the

case in sea turtles (Fitzsimmons 1998).

In addition to affecting mating strategy clutch frequency provides invaluable

information for calculating population parameters, such as the number of females in a

population, or estimates of annual reproductive output. Without such information, it is

difficult to establish effective conservation strategies and management plans. Generally,

sea turtles have high clutch frequencies and high seasonal reproductive output during the

years when they nest. Leatherback turtles (Dermochelys coriacea) deposit approximately

seven clutches in a nesting season (Reina et al. 2002), and for green turtles, clutch

frequency in the Atlantic could be as high as six clutches per season (Bjorndal et al. 1999,

Johnson and Ehrhart 1996). It is notable, however, that their conspecific, the East Pacific

green turtle, is reported to have a clutch frequency of three or less for a nesting season

56

(Alvarado-Díaz et al. 2003). Even though there is clutch frequency information for all sea

turtle species, complete information is limited because of incomplete coverage of nesting

areas, loss of tags, loss of individual turtles, etc (Miller 1997). Additionally, for many of

these reasons, the numbers of clutches laid per season may be underestimated for many

populations. This may be the case for East Pacific green turtle populations, yet solid

information on this important life history trait is still rare. Undoubtedly, such low

numbers of clutches reported could help explain the extremely endangered status of these

populations (Alvarado-Díaz et al. 2003), both as a function of low reproductive output,

and as an influence on whether or not males of these populations are more driven to join

females in their extensive breeding migrations.

Information on the reproductive cycle of turtles in the wild is difficult to obtain.

Ultrasound imaging has been used to study reproductive cycles in tortoises (Robeck et al.

1990, Rostal et al. 1994, Casares et al. 1997) fresh water turtles (Kuchling 1989, Shelby

et al. 2000) female sea turtles (Rostal et al. 1990, Rostal et al. 1996, Plotkin et al 1997,

Rostal et al. 1998) and male sea turtles (Pease et al. 2010) and is especially useful to

study the reproductive cycle and physiology of wild and captive animals.

Ultrasoundography allows for the analysis of reptile reproductive status without the use

of anesthesia or other invasive techniques (Rostal et al. 1990). This technique is an

effective modality to repeatedly monitor follicular development and egg production

(Robeck et al. 1990)

The objective of the current study was to analyze the reproductive output of the

endangered East Pacific green turtles (Chelonia mydas) nesting at a beach complex in

57

northwestern Costa Rica. To get accurate numbers, close observation of the entire nesting

beach is needed for the entire season. Alternatively, on beaches where complete coverage

is not possible, estimations can be made (Limpus et al. 2003). In our study we

supplemented our beach patrols, tagging information, and seasonal clutch frequency

calculations with ultrasonography of post-nesting females to enhance our estimates of

seasonal reproductive output.

Study Area

The main nesting beach, Nombre de Jesús (10° 23’ 30” N; 85° 50’ 07” W) is a

high energy sandy beach, approximately 1 km long located in the north of the Nicoya

Peninsula, Guanacaste Province, Costa Rica. Along with its neighboring beach,

Zapotillal, it hosts an important aggregation of nesting East Pacific green turtles, (also

known as black turtles), with approximately 15 turtles per night during peak season.


We patrolled Nombre de Jesús from October 2008 to January 2009 and from July

to November 2009 to intercept nesting female green turtles. After each turtle finished

nesting we set up a portable real-time ultrasound scanner (Aloka SSD-500) behind the

front flippers of the turtle. The scanner was plugged into a portable battery (Eliminator

PowerBox 400 watt), and thus ran without any noise. The turtle was scanned while it was

covering the nest. We used an electronic convex probe, 3.5 MHz, because low wave

length penetrates deeper than 20 cm into tissue and is more effective in larger species of

58

sea turtles (Rostal et al. 1990). The probe was coated with Acuasonic gel (Parker

Laboratories), a coupling gel that enhances imaging. One ovary and oviduct at a time

were scanned by placing the probe in the inguinal region above the hind flipper (Rostal et

al. 1990); every scan was recorded using an attached printer (Sony video graphic printer).

In addition to ultrasound scanning, each turtle was checked for PIT tags with a handheld

PIT tag reader (AVID Identification System). If the turtle was untagged we applied a new

PIT tag in the right front flipper for later identification. This study was approved by the

Animal Care and Use Committee of Drexel University (Protocol 18466) and by the

Ministry of Environment and Telecommunications (MINAET) in Costa Rica (ACT-

PNMB-005-2007; ACT-SASP-PI-195; ACT-OR-D-050)

When turtles were observed during consecutive successful nesting events, we

were able to calculate a mean observed internesting period (OIP), which was simply the

interval in days between observed successful nesting events averaged among all turtles

for which we had this type of data. Turtles observed after an interval greater than 20 days

and less than 6 days were excluded from the analysis following protocol established by

Reina et al. (2002). Similarly, we recorded observed clutch frequency (OCF) as the

number of clutches actually observed during the sampling period for an individual. The

OCF may underestimate the number of clutches per turtle (Frazer and Richardson, 1985,

Steyermark et al. 1996) unless a turtle is seen every time it nests throughout the season,

and therefore the mean OCF is undoubtedly an underestimate of this key population

parameter. To approach a more realistic estimate, we calculated estimated clutch

frequency (ECF) using the first and last date of observation of an individual turtle,

59

dividing it by the OIP and adding 1 for the first oviposition (Reina et al. 2002, Limpus et

al. 2003).

For turtles with complete information on the reproductive status from

ultrasonography, we added 0, 1 or 2 clutches to their ECF based on the reproductive

status they showed the last time they were seen on the beach. In this way we obtained an

even more realistic ECFU estimate (ECF + number of clutches remaining as observed in

the last ultrasound).

To calculate OIP, OCF, ECF and ECFU we used turtles encountered from July to

November 2009 because the beach coverage was higher than in 2008. Although the beach

was not completely covered for the entire season, the effort was high throughout the

season, and there were enough consecutive encounters to provide a solid baseline for

estimates of seasonal reproductive output.

As another benefit to the ultrasound technique, we also were able to calculate the

percentage of turtles with late-stage or depleted ovaries to have a better idea of the timing

of the end of the nesting season for this population, about which little was previously

known. In this analysis we included all the turtles scanned in 2008 and 2009. This was

supplemented with occasional surveys of the nesting beaches in March, April and June to

verify the absence of tracks during those months.

60

Results

We encountered, and scanned with ultrasound, turtles 127 times (96 individuals)

from October 2008 to November 2009. In 100% of the scans we were able to visualize

the ovaries of the turtles. Scanning the ovaries, we were able to differentiate between an

early preovulatory, late preovulatory and a depleted ovary (postovulatory) (Rostal et al.

1996). In the early stages (beginning of the nesting season) the ovaries were filled with

vitellogenic follicles. In the late preovulatory stage we were able to distinguish only when

one clutch was left, due to the presence of fewer follicles, coelomic space and atretic

follicles in some cases. When the ovary was depleted, we observed atretic follicles and

approximately less than 5 follicles, meaning that the clutch just laid was the last clutch of

the season. An accurate estimation of the number of vitellogenic follicles using

ultrasound was not possible; however, we could estimate the following: 1) Ovaries in

early stage (Figure 3.1): turtles will lay at least two more clutches following the present

nesting event, 2) Ovaries in late stage (Figure 3.2): turtles will lay one more clutch

following the present nesting event, 3) Ovaries depleted (Figure 3.3): the turtle will not

lay more clutches during the season.

In four cases we found shelled eggs (Figure 3.4) still in the oviduct when the turtle

was covering the nest. These encounters coincided with the presence of poachers or

tourists around the turtles. We observed that 90% of the eggs were taken on Nombre de

Jesús by poachers except when researchers were on the beach and secretly relocated the

eggs.

61

The OIP (mean ± SD) for this population was 12.0 ± 2.1 days (N = 37 individuals,

98 encounters). The OCF (mean ± SD) was 1.54 ± 0.79 (N = 24) and the ECF (mean ±

SD) 3.53 ± 1.79 (N=24). The newly calculated ECFU (mean ± SD) was 5.13 ± 1.32 (N =

24).

We also calculated the percentage of turtles seen with depleted and late staged

ovaries during the months of August through February (Figure 3.5). There were two

peaks where the greatest number of turtles left the nesting beaches, October-November

and January. Occasional observations in March, April and June indicated the presence of

nesting females on the nesting beaches in very low numbers

Discussion

Contrary to the findings of Cornelius (1976) on Playa Naranjo, Costa Rica and

Alvarado-Díaz et al. (2003) that suggested the East Pacific green turtles nest an average

of three times, our findings using regular tagging data and relocations on the beach

indicated an ECF of 3.7 for this population. By adding the information obtained with the

ultrasound, the new ECFU increased 1.5 nests to 5 nests per season. This number is closer

to the clutch frequency reported by Bjorndal et al. (1999) for green turtles in the Atlantic.

The difference in clutch frequency reported for different populations could be

affected by loss of tags, beach coverage, time of the year, and beach fidelity. This

includes tagging or recapturing turtles a fraction of the night instead of all dark hours or

not covering the complete nesting season. By using the information provided by the

62

ultrasound on the reproductive stage of the turtles through the season, we could estimate

a more accurate clutch frequency for the Costa Rican population. The accuracy of this

type of information, such as clutch frequency and internesting intervals, provides better

knowledge of the number of females in a population, annual fecundity, hatchling

production, etc (Miller 1997). The underestimation of these values could affect

conservation strategies by overestimating the number of females in a population where

number of females is estimated by number of nests. Alvarado-Díaz et al. (2003)

calculated the number of females nesting per year based on OCF = 2.5 and compared it to

the number of females nesting per year obtained by estimating it with ECF = 3.1; the

annual numbers were reduced by 20%. Therefore the estimated number of females in the

population is lower with a higher clutch frequency. If such a key parameter is incorrect it

could lead to a misinterpretation of the status of a population.

The number of clutches a female produces in a single nesting season is also a key

characteristic that could greatly influence a male sea turtle’s breeding strategy (Gist and

Congdon 1998). Stored sperm in the oviducts of chelonids may become much more

advantageous after the first oviposition by a female. The passage of dozens of enlarged

follicles and eggs can greatly distend the oviduct and sweep it clean of any existing free

sperm. The subsequent clutches may then be fertilized mainly by sperm stored in the

submucosal tubules high up in the oviduct. In fact, if mating does not occur shortly after

egg laying, or later in the season, then stored sperm takes on a very important role and the

payoffs for an early breeding male could be rather large, including a whole season’s

compliment of eggs (Fitzsimmons 1998). In conjunction with sperm storage, the number

of clutches for a nesting female during a single season could dictate whether males were

63

favored more heavily to stay in foraging areas or to migrate to breeding areas. With more

clutches laid in a season, the genetic output of males is more important in the overall

hatchling production of that given season. It is probably beneficial for a male to migrate

to the nesting beaches because the concentration of females would be higher than in

foraging areas. But also the migration and competition with other males for a female

requires much energy. In addition, several questions still remain regarding the nature of

sea turtle mating system. For example, if the first copulation yields a higher percentage of

the clutches fertilized this would also favor the earliest breeding males. Indeed, mating at

the foraging areas has been demonstrated through analysis of nDNA (Bowen and Karl

2007). Therefore, there is a possibility that the males that remain in a foraging area will

also contribute to the production of the season by inseminating females before their

migration. This would undoubtedly change the nature of assessment and conservation

strategies.

During the course of this study we did not carry out surveys on the nesting beach all

year around, although occasional observations in March, April and June indicated that the

nesting season for East Pacific Costa Rican green turtles possibly extended all year

around or at least 10 months as indicated by Cornelius (1976). There were two peaks for

migrating turtles (turtles with depleted ovaries) in the months of October-November and

January. Following our findings it appears that green turtles in Pacific Costa Rica take an

average of two months to complete a nesting season. Therefore, turtles leaving the

nesting grounds in October would have started nesting in August and turtles leaving in

January would have started nesting in November. Based on our observations, there may

be turtles arriving at the nesting beaches as early as June and turtles leaving the nesting

64

grounds as late as April. However, in order to have a better understanding of the timing

of the nesting season more observations throughout the year are necessary.

The use of ultrasound is a very successful methodology to understand the

reproductive status of sea turtles. The scanner can be taken to the beach and the

procedure does not require anesthesia or handling the animals and allows the acquisition

of real time images which makes this methodology ideal for the study of wild animals

(Rostal et al. 1990, Pease et al. 2010). The whole process can take between five to ten

minutes. We conducted the scanning after the turtle laid the eggs. Although during the

process the turtles were gently moving the rear flippers, there were times when they

stopped and the scanning was performed with no inconvenience. Additionally the

movement of the flippers allowed us to have a better vision of different portions of the

ovary. Complete visualization of the ovary is not possible through ultrasound (Robeck et

al. 1990) and at the beginning of the nesting season each ovary could have between 50 to

more than 200 follicles (Rostal et al. 1990). That makes it impossible to estimate the

number of eggs the turtle will lay during the season. However, this technique allowed us

to identify the remaining reproductive output of every scanned turtle. At the beginning of

the nesting season the ovaries of most green turtles displayed large quantities of

preovulatory vitelogenic follicles. This characteristic also occurs in leatherback turtles

showing that the reproductive cycle is common for different sea turtle species (Rostal et

al. 1996). Even though the follicles have different sizes (Etches and Petitte 1990) it is

difficult even to estimate the number of clutches the turtle will lay during the season. As

the season progresses and the follicles were ovulated, the ovaries started showing fewer

follicles and the presence of atretic follicles. Atretic follicles have an anechoic line

65

surrounded by an echoic yolk (Rostal et al. 1990, Rostal 2007). The presence of these

types of follicles is known for sea turtles (Rostal et al. 1990, Rostal et al. 1996, Rostal

2007) and tortoises (Robeck et al. 1990, Casares et al. 1997). Atretic follicles are the

result of non-ovulated follicles during the nesting season. Casares et al. (1997) suggested

that in Galapagos tortoises, the follicles go into atresia when conditions such as food

availability and temperature are not favorable. Sea turtles potentially reuse the energy

from the stored yolk by reabsorbing the yolk from the oocyte. The artretic follicle would

be reduced in size leaving a scar (Rostal 2007). In our study turtles with one clutch left

(post ovulatory stage) were followed until their last nesting event. The turtles with

depleted ovaries were part of a different study in which we attached satellite transmitters

to them and followed their migration; therefore we ascertained that the turtles had just

one clutch left when she was scanned in her previous nesting event.

Our study illustrated that the use of ultrasound as a non-invasive technique was an

effective way to accurately determine the reproductive status and reproductive effort of

East Pacific green turtles. Given the need for more detailed demographic data to obtain a

more complete understanding of the demographic status of sea turtle populations

(Bjorndal et al. 2010) this technique should be used routinely in nesting beach studies.

Conservation Implications

The East Pacific green turtle is in danger of extinction (IUCN 2010). Our study

indicated that there was a large and active breeding population on beaches without law

enforcement along the Pacific coast of Costa Rica, where egg collection and unregulated

fishing was a common activity. The poaching taking place on the nesting beaches was

66

undoubtedly causing a decline in the population, as has been documented for leatherback

turtles nearby (Santidrián Tomillo et al. 2007). We observed extensive poaching (90% of

the clutches were taken) and uncontrolled tourism at night on Nombre de Jesús. We

observed that turtles that were disturbed stopped laying eggs and walked away still

carrying shelled eggs.

Even though the turtles are able to hold shelled eggs for long periods of time

(Casares et al. 1997, Plotkin et al. 1997) they generally come back to the nesting beach,

later that night or the following night, to lay the remaining eggs (personal observation).

This caused the turtle to spend more energy than needed for a nesting season compared to

a beach with no human interference. Indeed extra energy spent in unsuccessful nesting

events could impact the overall number of clutches for that female in a season (Hamann

et al. 2002). Additionally, the possibility of hatchlings emerging from very small nests is

very low due to the lack of mutual stimulation and group activity displayed by the

hatchlings digging upwards in the sand to get to the surface (Carr and Hirth 1961, Miller

1997). As a result, those eggs that were not deposited with the main clutch would

probably be lost.

Reproductive output is one of the most important measures for population biology,

conservation and management of sea turtle populations. The information obtained from

this study showed a higher reproductive output than previously described for the East

Pacific green turtle. On the positive side higher individual output could represent a

healthy population with good resources available to foraging adults, which would allow

them to produce more offspring. On the other hand, higher reproductive output could

67

modify previous estimations in number of females in a population, decreasing numbers

previously reported for this species.

Thus, the data collected in this study along with the observations of poaching

activity and uncontrolled tourism indicate that there is a great need to protect Nombre de

Jesús because it is one of the most important nesting beaches hosting a population with

the highest reproductive output reported for East Pacific green turtles.

68

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73

Tables

Table 3.1: East Pacific green turtles selected from the database from which

there was a complete record of their reproductive status through ultrasound; turtles

were scanned every time they came to the beach during the period of study. ECFU is the

effective clutch frequency + the number of clutches left calculated from ultrasonography.

Turtle ID First seen Last seen ECF Clutches left ECFU

1 28-Jul-09 27-Oct-09 8.55 0 8.55

2 3-Aug-09 31-Aug-09 3.32 2 5.32

3 11-Aug-09 1-Sep-09 2.74 2 4.74

4 15-Aug-09 27-Aug-09 2.00 2 4.00

5 18-Aug-09 14-Sep-09 3.24 2 5.24

6 22-Aug-09 23-Oct-09 6.15 0 6.15

7 22-Aug-09 2-Nov-09 6.98 1 7.98

8 25-Aug-09 6-Sep-09 2.00 2 4.00

9 28-Aug-09 9-Oct-09 4.49 0 4.49

10 2-Sep-09 14-Sep-09 2.00 2 4.00

11 9-Sep-09 12-Oct-09 3.74 0 3.74

12 10-Sep-09 13-Nov-09 6.31 0 6.31

13 10-Sep-09 18-Oct-09 4.15 2 6.15

14 15-Sep-09 26-Oct-09 4.40 2 6.40

15 17-Sep-09 22-Oct-09 3.91 2 5.91

16 19-Sep-09 25-Oct-09 3.99 2 5.99

17 10-Oct-09 22-Oct-09 2.00 2 4.00

18 10-Oct-09 23-Oct-09 2.08 2 4.08

19 11-Oct-09 25-Oct-09 2.16 2 4.16

20 12-Oct-09 18-Nov-09 4.07 0 4.07

21 15-Oct-09 25-Oct-09 1.83 2 3.83

22 15-Oct-09 6-Nov-09 2.83 2 4.83

23 17-Oct-09 30-Oct-09 2.08 2 4.08

24 18-Oct-09 11-Nov-09 2.99 2 4.99

Mean 3.67 5.13

SD

1.79

1.32

74

Figures

Figure 3.1: Ultrasonographic image of an ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. The ovary was filled with

vitellogenic follicles (vf). The turtle had at least two more clutches to lay during the

nesting season.

Figure 3.2: Ultrasonographic image of the ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. Ovary in late preovulatory stage.

The turtle had one more clutch to lay during the nesting season. In this stage we observed

vitellogenic follicles (vf), atretic follicles (af) and some coleomic (empty) space.

75

Figure 3.3: Ultrasonographic image of the ovary of an East Pacific green turtle

(Chelonia mydas) after a successful nesting event. The depleted ovary indicated that

the turtle had completed the nesting season and would start migrating. We considered an

ovary depleted when we identified fewer than 5 vitellogenic follicles remaining (none in

this picture).

Figure 3.4: Ultrasonographic image of the oviduct of an East Pacific green turtle

(Chelonia mydas) after a nesting event. The presence of the shelled egg after

oviposition indicates that some kind of disturbance occurred during the nesting event

causing the turtle to stop laying eggs and start covering the nest. s = shell, a = albumen, y

= yolk.

76

Figure 3.5: Percentage of East Pacific green turtles in Costa Rica with depleted

ovaries and late preovulatory staged ovaries by month. The percentages were

calculated in relation to the number of turtles scanned by ultrasound every month.

0

2

4

6

8

10

12

14

Aug Sept Oct Nov Dec Jan Feb

% t

urt

les

Depleted Ovary Late Preovulatory

77

Chapter 4: Post-nesting Movements and Foraging Areas of East Pacific Green

Turtles (Chelonia mydas) from Costa Rica

Abstract

We used satellite transmitters (Mk 10 Pat tags) to study the post-nesting

movements, behavior and, foraging grounds of 10 East Pacific green turtles from Nombre

de Jesús and Zapotillal beaches in Northwest Costa Rica. Some turtles were local

residents in the Gulf of Papagayo; some moved an intermediate distance; and others

moved to Panama or El Salvador. Total length of post-nesting migrations ranged from 5

to 1091 km, with a main daily speed of net travel of 37 km/day. Home range in the

foraging areas varied from 265 km² to 18,260 km2 (being one of the largest areas reported

for this species). During migration turtles showed a bimodal distribution in duration of

dives with majority of durations between 2-5 min and 40-60 min and dive depths mainly

to 5 m or shallower. During foraging, distribution of dive duration was homogeneous,

displaying all dive durations, while most of the dives were to 5-10 m depth. Sea surface

currents did not influence preferred migration routes of the turtles. Nevertheless, some

turtles seemed to benefit from currents by swimming in the same direction to reach the

feeding grounds. The turtles in the present study did not exhibit patterns that would

suggest that their behavior in the feeding grounds was influenced by variations in CHL or

SST. However, all feeding grounds in this study had high primary productivity due to the

oceanography of the area. The oceanic and bathymetric features could be influencing the

general areas where the turtles are, but not their specific movements within the area. Our

study indicated that green turtles that nest in Northwestern Costa Rica spend all their life

78

as adults in coastal areas of Central America. The coastal nature of their movements

makes them vulnerable to many human coastal activities. With the new information

provided by this study we suggest that there is a clear interaction between sea turtles and

artisanal fisheries because they are occupying the same areas. The fact that the turtles are

swimming through different countries makes management more complex and calls for

agreements between nations. More information is needed in order to understand how

severe the impact of coastal fisheries is on this population.

79

Introduction

Animals migrate in response to the need for resources that are not available at

their present site. For example, red knots (Calidris canutus) travel from North America to

winter areas in Argentina (Harrington et al. 1988) and the monarch butterfly (Danaus

plexippus) migrates from eastern North America to over-wintering areas in central

Mexico travelling 3600 km (Brower 1996). In general, whales also display a seasonal

migration from high-latitude foraging areas to low-latitude reproductive grounds

(Corkeron and Connor 1999). Migration is driven by balance of the cost of remaining at

a given location, versus the benefit of moving (Morreale et al. 2007). In areas where food

resources vary temporally or environmental conditions are not optimal all year, migratory

behavior often evolves in the affected animals. For instance, if the conditions are optimal

for adult populations but not for offspring development; the adults may undergo

migrations to reproduce and ensure the survival of their offspring. This is common in

animals such as whales and sea turtles.

Sea turtles are the only reptiles that exhibit long distance migrations (Plotkin

2003). Pacific Leatherback turtles nesting in Costa Rica migrate into the South Pacific off

Chile and Peru (Morreale et al. 1996, Shillinger et al. 2008). Green turtles nesting on

Ascension Island travel to feeding grounds along the coast of Brazil (Carr and Carr 1972,

Hays et al. 2002). Olive ridley turtles nesting in northwestern Australia migrate between

180 and 1100 km to their feeding grounds (Whiting et al. 2007). Juvenile loggerheads

transverse the entire Pacific Ocean during developmental migrations; traveling from

nesting beaches in Japan and Australia to foraging areas in Baja California (Bowen et al.

80

1995); when they reach sexual maturity they return to the western Pacific where they

remain the rest of their life (Nichols et al. 2000).

Sea turtles migrate in open ocean likely using a variety of cues. Hatchlings can

follow light cues to get to the ocean, then orient into waves and also orient to the earth’s

magnetic field (Lohmann and Lohmann 1992). For adults orientation plays an important

role because they show fidelity to a particular nesting beach and foraging area (Carr and

Carr 1972, Nordmoe et al. 2004, Plotkin et al. 1996, Ireland et al. 2003). Adults appear to

have the capability to migrate to a specific location possibly by using the inclination of

the earth’s magnetic field and by having a bicoordinate magnetic map (Lohmann and

Lohmann 1996). Sea turtles also follow environmental features such as bathymetric

contours or currents to help orientation (Morreale et al. 1996, Shillinger et al. 2008).

Green turtles going from Ascension Island to Brazil may follow chemical cues, currents

and magnetic cues collecting this information during the migration to adjust their course

(Luschi et al. 1998).

East Pacific green turtles (Chelonia mydas) (also known as black turtles) belong

to a distinct population of this endangered species inhabiting waters in tropical and sub

tropical regions throughout the Eastern Pacific (Seminoff et al. 2002a). They range from

Baja California to Chile and west to Galapagos Islands. The most important nesting

grounds identified in the Pacific are found at Colola and Maruata in Michoacán (Mexico)

(Alvarado and Figueroa 1992), and in the Galapagos Islands (Green 1984). Although

green turtles are present along the Pacific coast of Central America (Cornelius 1979),

limited information exists on populations nesting there (Richard and Hughes 1972,

Cornelius 1976).

81

Turtles nesting in Michoacán move north and south along the Central American

coast (Alvarado and Figueroa 1992). East Pacific green turtles that nest in the Galapagos

show three different migratory strategies as indicated by flipper tag returns (Green 1984)

and satellite telemetry (Seminoff et al. 2008). Some individual females swim through

open ocean and reach the coast of central America (Green 1984, Seminoff et al. 2008);

others reside among the Galapagos islands; and a third group moves to oceanic waters

and feeds there (Seminoff et al. 2008). For green turtles that nest along the Central

American coast it is not known where they migrate to reach their feeding grounds.

Juvenile and adult green turtles are known to forage in coastal areas, estuaries,

lagoons (Seminoff et al. 2002a) and near shore insular habitats (Amorocho and Reina

2007). Even though it was believed that green turtles only foraged in coastal

environments, recent studies demonstrated they also forage in open waters as adults

(Quiñones et al. 2010). Their diet is mainly sea grass and red and green algae. However,

they also eat invertebrates and gelatinous prey (Seminoff et al. 2002b, Seminoff et al.

2006a). Adult green turtles foraging off shore of Peru have a diet dominated by jelly fish,

mollusks and crustaceans (Quiñones et al. 2010).

The eastern Tropical Pacific offers areas of high productivity as a result of its

particular oceanic features. It is characterized by the presence of coastal and open ocean

upwellings, fronts, eddies and meanders (Lavín et al. 2006). The convergence of the trade

winds of the intertropical convergence zone (ITCZ) produces a low wind area off Central

America where the SST (sea surface temperatures) is higher than elsewhere in the area.

However, the wind blowing from land to sea produces the Tehuantepec, Papagayo and

Panama jets causing eddies that generate productive areas exhibiting a decrease in SST

82

and increase in chlorophyll levels and interrupting the warm low productivity “warm

pool” (Palacios and Bograd 2005, Lavín et al. 2006). Within this region, the Costa Rican

dome is another upwelling region in the eastern Pacific with high primary and secondary

production (Lavín et al. 2006). Centered 300 km off the Gulf of Papagayo between Costa

Rica and Nicaragua, it is produced by costal jets, eddies, the ITCZ and the geostrophic

balance of the thermocline (Fiedler 2002).

In coastal areas, Costa Rica hosts an important population of the East Pacific

green turtle along shore of Guanacaste on the Nicoya peninsula (Richard and Hughes

1972, Cornelius 1976). Little scientific data are available for this population and we do

not know where their foraging grounds are, nor what routes they take to get to them.

Anecdotal information suggests that these turtles are subjected to capture in longlines and

gill nets and it is well known that poaching of eggs is rampant on many beaches in the

area. In order to better protect this highly endangered population of green turtles from

threats in the ocean we need to know their migration routes, foraging grounds and

behavior at sea at the very least. The situation on the nesting beaches and during the

internesting period was discussed in Chapter 2. Here we report the post-nesting

movements, behavior and foraging grounds of green turtles that nest in Guanacaste and

we discuss how they potentially respond to oceanographic conditions. We also discuss

the conservation implications of these data.

83


We used satellite telemetry to study the post-nesting movements and behavior of East

Pacific green turtles nesting on Nombre de Jesús (10° 23’ 30” N; 85° 50’ 07” W) in

Guanacaste Province of Costa Rica. We patrolled the beach at night during the nesting

season to intercept turtles during their last nesting event. We selected turtles with

depleted ovaries for this study. To assess the reproductive status of each turtle and to

verify that we were witnessing its last nest of the season we used an ultrasound

instrument (Aloka SD 500) (Chapter 3). This ensured that the turtles would leave the area

after nesting and not be subjected to poachers on the beach or fisherman near the beach.

Satellite transmitters (Wildlife Computers Mk-10 PAT Pop up archival transmitting tag)

were attached to 10 female green turtles, 1 in October 2006, 1 in August 2007, 2 in

January 2009, 4 in October 2009 and 2 in November 2009 (Table 4.1).The transmitters

were configured to transmit opportunistic transmissions so we could obtain real-time

location data.

Satellite transmitter attachment

We followed a modified methodology used by Morreale et al. (1996) as described

in Morreale (1999) to attach the satellite transmitters to the turtle. We measured the

curved carapace length (CCL) of each turtle with a flexible measuring tape (± 0.5 cm).

We cleaned the marginal posterior scute of the carapace with 70% alcohol and made a 3

mm diameter incision with a sterile electric drill bit (battery-powered electric drill).

Immediately after the incision we applied lidocaine and inserted sterile surgical tubing.

We positioned plastic buttons with Y holes above and below the carapace to avoid

84

friction and consequent damage to the carapace. We connected the transmitter to the

buttons on the carapace by a flexible lanyard (monofilament fishing line, 400 lb test) that

passed through the holes and was secured to itself with a metal crimp. To avoid

entanglement or long-term impediment of the turtles, we placed swivels and crimps

which would break away with corrosion.

The attachment process took 7 to 10 min and was done when the turtle was

covering the nest after laying eggs minimizing the impact on the turtle’s natural behavior.

Satellite transmitters

We customized satellite tags with a buoyant case made out of syntactic foam. Satellite

transmitters weighed ~115g (≈ 0.2 % of the turtle mass), had a hydrodynamic shape and

trailed behind the turtle to minimize drag. The transmitter’s positive buoyancy was 36g,

enough to bring the antenna of the transmitter to the surface when the turtle breathed. We

programmed the tags with duty cycles of 10h/24h (13:00-17:00hs and 18:00-00:00hs) to

optimize battery life. The transmitter sampled and summarized data (dive depth, dive

duration and time at depth) stored in categorized bins: Dive depth: 5, 10, 15, 20, 25, 30,

35, 40, 45, 50, 75, 100 and 200 m; Dive duration; 2, 5, 10, 20, 30, 40, 50, 60 and 90 min.

SSSM Method

We applied a Bayesian switching state-space model (SSSM) developed by Jonsen et al.

(2007) to all of the raw Argos-acquired surface locations for each track (n = 10) resulting

in daily position estimates. This model allowed location estimates to be inferred by

coupling a statistical model of the observation method (measurement equation) with a

85

model of the movement dynamics (transition equation) (Patterson et al, 2008)

The measurement equation accounted for errors in observed satellite locations and

these were based on published estimates (Vincent et al. 2002). Similar priors were placed

on model parameters as in Jonsen et al. (2007). When satellite positions were missing,

linearly interpolated positions were used as initial values (Bailey et al. 2008).

The transition equation was based on a correlated random walk model and

included a process model for each of two behavioral modes (Jonsen et al. 2005).

Behavioral mode 1 was considered to represent transiting and behavioral mode 2

represented foraging (or area-restricted search behavior) (Bailey et al. 2010). Priors were

specified assuming that during transiting turn angles should be closer to 0 and

autocorrelation should be higher than when foraging (Jonsen et al. 2007).

The model was fitted using the R software package (R Development Core Team

2008) and WinBUGS software (Lunn et al. 2000). Two chains were run in parallel, each

for a total of 30,000 Markov Chain Monte Carlo (MCMC) samples. The first 10,000

samples were discarded as a burn-in and the remaining samples were thinned, retaining

every fifth sample to reduce autocorrelation. Thus, posterior distributions for parameter,

state, and behavioral mode estimates were based on 4000 samples from each chain.

We plotted the migration routes on a map using ArcGIS version 9.3 geographic

information system software (www.esri.com). Based on the daily locations obtained with

the SSSM, we calculated distance traveled in one day and the total distance traveled. We

included in this analysis the turtles from which migration was tracked for more than two

days. We compared the size (CCL) of the turtles tagged with the total distance traveled

86

and the daily movements. The longer tracks (> 100 km) were compared against

geostrophic surface currents. Aviso geostrophic surface current (u and v vectors, cm/sec)

were monthly composites, at a 0.5º spatial resolution (NOAA Ocean-Watch-LAS).

Diving behavior

We obtained dive depth and dive duration summarized in bins and transmitted

through the Argos system. We separated dive data into migration and foraging based on

the behavior mode determined with the SSSM model and calculated proportion of dives

at depth and duration for each turtle. We calculated proportion and tested differences

(one-way ANOVA) between depths of dives and duration of dives for all turtles during

migration and foraging and during day and night. We also calculated and compared depth

of dives for the turtles in different foraging areas. Each histogram was summarized in

intervals of 4 hours, which allowed us to compare dive depth and dive duration for day

and night. Statistical analyses were performed using SPSS Inc. Data were transformed

when necessary before analysis to meet the assumption that data were normally

distributed. Statistical significance was accepted at 0.05 level.

Foraging Areas

We estimated areas used for foraging for individual turtles using 100% Minimum

Convex Polygons (MCP) to estimate their home range during foraging using the Hawths

tools extension (Beyer 2004) for ArcGIS. Minimum convex polygon areas are based on

minimum distance of outer locations for each turtle in foraging areas including all

locations for duration of the transmission.

http://gcmd.nasa.gov/KeywordSearch/RedirectAction.do?target=S6cqF6vMwKxGiWs51Zzg%2F0RMqGC4qkbfmX3ALULuAcGvbwqSYGjj9gb38zikCX0Jtu0JJcwrKvA%3D

87

Based on differences in areas of polygons, we divided foraging time in weeks and

preformed MCP calculations for turtles in which overall area of the polygons was higher

than 10,000 km². To analyze use of foraging area in comparison with oceanic

characteristics, we divided locations into months and created monthly MCPs. Oceanic

variables analyzed were surface chlorophyll-a levels, geostrophic surface currents and sea

surface temperatures (SST). These variables were obtained from NOAA OceanWatch-

LAS and NOAA OceanWatch - Central Pacific (http://oceanwatch.pifsc.noaa.gov,

http://las.pfeg.noaa.gov/oceanWatch/oceanwatch). The SST (ºC) grids were monthly

composites with a spatial resolution of 0.1º and surface chlorophyll-a (mg/m-3

) grids were

monthly composites, with a spatial resolution of 0.05º.

Results

Post-nesting movements

Through ultrasonography we identified turtles with depleted ovaries and all turtles

with transmitters started post-nesting movements, without returning to the nesting beach.

The 10 satellite transmitters reported data for 25 to 102 days (mean ± SD = 62.2 ±

28 d). All turtles conducted post-nesting movements to neritic foraging grounds (Figure

4.1). Turtle 2 carried out the longest migration, approximately 1091 km southwards to the

Gulf of Panama (Figure 4.1-d). Three turtles migrated (293, 410 and 425 km) northwards

to the Gulf of Fonseca off El Salvador (Figure 4.1c). Four turtles carried out short

migrations (24, 43, 71 and 152 km) to the Bay of Santa Elena in northern Costa Rica

http://oceanwatch.pifsc.noaa.gov/

http://las.pfeg.noaa.gov/oceanWatch/oceanwatch

88

(Figure 4.1 a-b). The last 2 turtles were local residents in the Gulf of Papagayo

approximately 5 km north of the nesting beach. There was no correlation between the

size of the turtles and the length of their tracks (p = 0.614, N = 6). The mean daily

movement during the migration was 37.03 km ± 8.36 and it was not correlated to CCL (p

= 0.209 N = 6).

Comparing post-nesting movements with geostrophic surface currents indicated

that turtles migrating to the Gulf of Fonseca (Figure 4.2) swam in the same direction as

the prevailing current, the Costa Rica Coastal Current (Kessler 2006). In contrast the

turtle migrating to the Gulf of Panama swam both against and with the current.

Foraging Areas

We identified four coastal foraging areas for this population: Gulf of Fonseca,

Gulf of Panama, Bay of Santa Elena and Gulf of Papagayo (Table 4.1). The daily

movement during foraging was 12.8 ± 3.4 km and was not correlated with the turtle size

(p = 0.838, N = 9). Even though turtles moved to the Gulf of Fonseca area, none of the

turtles foraged inside the gulf. Behaving differently, the turtle that migrated to the Gulf of

Panama resided for the duration of the transmitter life (44 tracking days in the foraging

grounds) near shore in the Gulf of San Miguel. We calculated MCPs for each turtle

including all the locations during foraging (Figure 4.3). Areas used during foraging for

the individuals ranged from 265 to 18,260 km² (Table 4.2). Interestingly, there was no

significant correlation (p = 0.342, N = 9) between the number of days of tracking and the

area of the polygons. Also, we did not find a significant correlation (p = 0.143, N = 9)

when we analyzed the relation between the foraging grounds and the area of the MCP.

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Based on the differences in the areas of the MCP we divided the data to create weekly

polygons. Only the turtles with the largest polygons (turtles 6 and 9) displayed notable

shifts in their foraging areas with time (Figure 4.4).

Diving behavior

There were significant differences between the overall duration of dives (ANOVA) F =

3.125, df = 8, p = 0.003). Bonferroni post hoc multiple comparison test explained these

differences by the difference between 2 and 90 and 40 and 90 min (p = 0.010 and p =

0.011 respectively). There were no significant differences (One-way ANOVA F = 1.218,

df = 8, p = 0.295) between mean duration of dives during migration and foraging.

However, the distribution of dive durations during foraging was more homogeneous with

turtles performing 79% of the dives between 2 and 40 min. During migrations there was a

bimodal distribution of dive duration; between 2 and 5 min (32 %) and between 40 and

60 min (46 %) (Figure 4.5). There were highly significant differences between the depth

at which the dives were performed (ANOVA, F = 11.046, df = 12, p = 0.0001). These

differences were explained by the difference between 5 m and all other depths

(Bonferroni posthoc multiple comparison, p < 0.0001). Overall, the turtles carried out

shallower dives (5 m) during both activities (migration mean ± SD 31.2% ± 5.7; foraging,

mean ± SD 38.8 ± 5.6) (Figure 4.6). There were no significant differences (ANOVA F =

1.23, df = 12, p = 0.273) between the depths of the dives during migration and foraging.

Turtles used different depths even in the same foraging area (Figure 4.7). Turtles foraging

in the Bay of Santa Elena dove to a predominant depth of 5 m (mean ± SD 51.5 ±

11.9%). Turtles foraging in the Gulf of Fonseca used different depths ranging from 5 to

90

80 m; while one turtle did not show a strong tendency to use a certain depth, the other

turtle carried out 52 % of the dives in the first 5 m of the water column. The turtles

foraging in the Gulf of Papagayo also used different depths. One turtle mainly used the

first 15 m of the water column and the other turtle dove mainly to 70 m.

During migration and foraging turtles used similar depths during day and night

(Figure 4.8) (5 and10 m, 49%, 42% respectively). There were no differences in dive

duration between day and night during migration. During foraging there were two

predominant durations of dives at night: short dives (2 min, 22%) and long dives (from

20-40 min, 49%), while during the day the duration of the dives varied widely from 5 to

40 min.

Oceanographic features

We divided all foraging locations monthly for each turtle and created monthly

MCP. We also overlaid the monthly MCPs with SST (Figure 4.9) and chlorophyll-a for

visual comparison (Figure 4.10). The SSTs ranged from 17 to 31 ºC. Turtles occupied

areas ranging from 22 to 31 ºC during October, November, and December. In January the

turtles stayed at temperatures higher than 24º C despite the fact that lower temperatures

were available. Noticeably during January and February 2009, there was a drop in the

SST reaching 22º C in the Gulf of Papagayo but a turtle foraging there did not respond to

this drop and stayed in the same area. Overall, chlorophyll levels were higher closer to

the coast but CHL variations occurred through the course of the study. Even though the

turtles foraged close to the coast (where CHL concentrations were high), they did not

apparently respond to variations. Turtles foraging in Santa Elena Bay experienced higher

91

chlorophyll levels than the turtles foraging elsewhere. In January and February 2009 a

bloom occurred in the areas off Costa Rica and Nicaragua affecting mainly the Gulf of

Papagayo and the Bay of Santa Elena. None of the individuals foraging in those areas

responded to these changes in productivity staying in the same areas. The turtles foraging

near the Gulf of Fonseca did not select places with high primary productivity even though

they were available closer to the Gulf in the period where the turtles were tracked.

Discussion

Post nesting movements

The satellite transmitters sent messages for 25 to 102 days. Even though battery

life for some was less than expected, the short distances moved by the turtles allowed us

to collect information on both post nesting movements and foraging areas for all turtles.

East Pacific green turtles moved between 5 and 1091 km after nesting. Some

turtles were local residents in the Gulf of Papagayo, some moved an intermediate

distance, and others moved to Panama and El Salvador. It appeared that Nombre de Jesús

was an important nesting beach for turtles residing in waters throughout Central America.

Turtles in this population did not undertake oceanic migrations reported for other sea

turtles (Green 1984, Carr 1975, Plotkin et al. 1995, Seminoff et al. 2008). Rather they

stayed within coastal areas even when migrating over 1000 km. Even though it may not

be the shortest distance to the preferred foraging area, it appears that green turtles prefer

to migrate along the coast in shallow waters. Green turtles from Wan- An Island migrate

92

over the continental shelf to mainland China involving detours that increase the final

migration distance (Cheng 2000). Commonly sea turtles from the same nesting area carry

out post-nesting migrations using different routes (Plotkin et al. 1995, Seminoff et al.

2008, Hatase et al. 2006). Some olive ridely turtles nesting on Nancite beach (Gulf of

Papagayo) migrate to coastal neritic environments (Honduras, El Salvador and

Guatemala) whereas others move to oceanic areas in the Eastern Pacific (Plotkin et al.

1995). Green turtles nesting in Galápagos undertake coastal and oceanic migrations to

reach different feeding grounds (Seminoff et al. 2008), as well as green turtles from the

Ogasawara Island in Japan (Hatase et al. 2006). In the present study differences in

migration routes were not related to the size of the turtles as occurred in green turtles

from the Galápagos (Seminoff et al. 2008).

The turtle going to Panama exhibited the longest migration traveling 40 km/day

and covering the distance in 25 days. This turtle migrated following the shoreline until it

reached the Gulf of Panama, which it crossed straight to the Gulf of San Miguel along the

coast.

Two turtles moved to the Gulf of Papagayo 5 km north of the nesting beach,

where they resided for the rest of the tracking duration (25 and 63 days). Residency in

green sea turtles also occurs in turtles nesting in Galápagos Islands. Contrary to the

present study, resident Galapagos green turtles moved at least 75 km (Seminoff et al.

2008) from the nesting beach. Four green turtles moved to Santa Elena Bay; two of them

completed their movement one day after laying the last clutch of the season and remained

there for the rest of the tracking duration. Two turtles took longer (3 days) to reach the

93

foraging area, the longer duration could be related to the turtles foraging on the way

because they traveled across the Gulf of Papagayo where other turtles were foraging; or

stayed after the last nest one or two days in the area close to the nesting beaches.

Of the three turtles that migrated to the Gulf of Fonseca, two moved along the

coast. Turtle 1 was the only one to traverse deeper waters moving outside the continental

shelf. And one turtle stopped north along the Santa Elena Peninsula before continuing the

migration to the Gulf of Fonseca. These three turtles swam through suitable foraging

areas (Gulf of Papagayo and Santa Elena Bay), where turtles from the same nesting beach

were foraging, while continuing on to more distant foraging areas. Hawksbill, olive ridley

and green turtles nesting at other locations stop and forage on the way to their final

destination (Cheng 2000, Cuevas et al. 2008, Whiting et al. 2007) which may reduce the

overall cost of migration (Godley et al. 2002).

Similar behavior occurs in the green turtles foraging along the coast of Brazil

(Hays et al. 2002). The fact that turtles are swimming through zones that may offer the

resources needed before they reach their final destination, raises the question of how the

turtles select their foraging sites. Some discussion in the literature regarding this question

arose when other populations displayed this pattern. The behavior was attributed to food

resource limitation, proximity to over-wintering sites and territorial defense (Broderick et

al. 2007). In the present study, we discard the possibility of the turtles being closer to

overwintering sites for the obvious reason of inhabiting the tropics, we also discard the

resource limitation because there are turtles foraging in all the areas. Additionally, the

length of the migration and, as a result, the foraging sites are not related to turtle size. We

94

suggest that as juveniles or sub-adults these turtles chose these foraging areas as a

consequence of their early dispersal patterns as hatchlings, and as adults kept performing

these migrations in response to fidelity to a specific foraging area (Broderick et al. 2007).

The mean daily speed of travel during migration for this population was

approximately 37 km/day. East Pacific green turtles travelled slower than green turtles in

the Caribbean of Costa Rica who travelled an average of 58 km/day to reach the foraging

grounds (from 400 to 1090 km) north of the nesting beaches (Troëng et al. 2005). Also

green turtles nesting in Taiwan move an average of 43 km/day to the continental shelf of

China (Cheng 2000). These greater speeds of travel may reflect a lack of intervening

foraging habitats or the need to travel greater distances.

Foraging areas

We identified 4 different foraging grounds: Gulf of Panama, Gulf of Papagayo,

Bay of Santa Elena and Gulf of Fonseca. There were remarkable differences in how the

turtles used these areas. Calculated foraging area home ranges varied from 265 km² to

18,260 km². Our findings differ from those for ridleys, loggerheads and other green sea

turtles where the home ranges are smaller in general than the present study (Whiting et al.

2007, Makowski et al. 2006, Seminoff et al. 2002b). Olive ridleys in their foraging

grounds of Australia use areas as large as 1260 km2 (Whiting et al. 2007). Loggerheads in

the Mediterranean use average home ranges of 305 km2 ranging from 3.5 to 1,198 km

2

(Zbinden et al. 2008), while juvenile green turtles in Florida inhabit small reef systems

using home ranges between 0.7 and 5 km2 (Makowski et al. 2006). Seminoff et al

(2002b) reported mean polygon areas of 16.6 km2 for East Pacific green turtles foraging

95

in Mexico. The two turtles that moved the most while foraging were turtle 6 in the Gulf

of Fonseca and turtle 9 in Santa Elena Bay. Turtle 6 used a total area of 14,083 km²,

starting foraging in Nicaragua (south of the Gulf of Fonseca) and continuing until

Guatemala. The weekly MCP showed that this turtle stopped at different places, probably

exploring patchy food resources and was still moving at the end of transmission (80 days

after leaving the beach). At least in two different weeks the turtle in Santa Elena Bay

moved out to oceanic waters reaching areas with depths greater than 2000 meters

covering an overall area of 18,260 km² during the duration of the tracking. In contrast,

the turtle at Panama only foraged in the Gulf of San Miguel using 265 km² in 45 days.

Whereas the turtle in Panama was probably feeding on sea grass and pastures related to

estuarine environments, the turtle off Santa Elena may have been consuming macro algae

and other components of the plankton like jellyfish (Quiñones et al. 2010). Turtles

foraging in Santa Elena Bay displayed greater variations in the use of the area. Overall,

differences in the uses of foraging areas can be due to different foraging strategies, food

availability in each foraging site (Godley et al. 2003) and food availability in the different

sites or within the same area (Seminoff et al. 2002b).

Sea grass and coral reefs provide foraging habitats for sea turtles (Chaloupka and

Limpus 2001, Jackson et al. 2001). Coral reefs are present along the coasts of Guatemala,

El Salvador and Nicaragua and Costa Rica. The coral reef located in the Gulf of

Papagayo is dead and covered with filamentous algae (Glynn 2001). These patches of

coral and their associated species of algae and invertebrates could explain the greater

movements of the turtles foraging near the Gulf of Fonseca in contrast to the turtles

foraging in the Gulf of Papagayo and Santa Elena Bay. In these regions macroalgae are

96

present from 0.5 m until approximately 20 m depth (Bernecker and Wehrtmann 2009,

Fernández and Alvarado 2008). The genus Cladophora and Ulva are the most common

within the green algae populations in the eastern Pacific (Fernández and Alvarado 2008).

Also species such as Gracilaria spp, Gigartina spp and Codium spp.are present along the

Pacific coast of Costa Rica and are part of the diet of the green turtles in Gorgona

(Amorocho and Reina 2007) and Gulf of California (Seminoff et al. 2002a). Sea grasses

(Ruppia maritima and Halophila baillonii) were present in the Gulf of Papagayo but after

a storm destroyed these pastures in 1996 no sea grass has been present along the Pacific

coast of Costa Rica (Cortés 2001).

As a possible explanation for the short migrations of green turtles in the

Caribbean it was proposed that this population spends less energy in migration and more

in reproduction than green turtles elsewhere (Troëng et al. 2005). Our findings suggest

that the East Pacific green turtles spend even less energy in migration reflected in the

short distance traveled, and short distance covered in a day, but they used broader areas

while foraging than many other populations and species. Along the coast of the Central

America the food availably probably is wide spread causing the turtles to spend more

energy in foraging (using larger areas to forage).

Diving behavior

During migration turtles showed a bimodal distribution in duration of dives with

major durations between 2-5 min and 40-60 min. The shorter intervals were associated

with shallow dives and the longer intervals with deeper dives. Depth most used during

migration was 5m. These short shallow dives allow the turtles to swim more efficiently

97

by reducing drag which increases at the surface and decreases when the depth is 2-3

times the body thickness (Hays et al. 2001). It has been reported that shallow dives are

mainly found during movement of turtles when they are swimming towards a specific

destination (Rice and Balazs 2008). During migration the turtles also dived deeper than

during foraging with a mean depth of 40 m and long submergences ranging from 40 to 60

min. The deeper dives during migration may be related to resting behavior (Rice and

Balazs 2008) and avoiding predation (Hays et al. 2001). Also turtles are known to forage

during migration (Cheng 2000, Cuevas et al. 2008, Whiting et al. 2007) and in this study

the coastal movements showed that they swim through other suitable foraging areas

suggesting that these deeper and longer dives are related to foraging on the way to their

final destination.

During foraging the distribution of the dive duration was homogeneous displaying

all dive durations. On the other hand, most of them were performed at 5-10 m depth. In

foraging areas the turtles display different behaviors probably associated with different

foraging strategies. Besides foraging, the turtles are carrying out other activities for

example: resting, moving from patch to patch, exploring the area (Seminoff et al. 2006b)

or even performing self cleaning behavior (Heithaus et al. 2002). It is difficult to

determine what type of behavior the turtle is undertaking when submerging to a certain

depth. Most of their behavior is related to the environmental characteristics of the specific

foraging area and to the food available at the site. In general, green turtles can forage in

benthic environments (3-32 m) or the mid water column (3-5 m) (Seminoff et al. 2006b).

In our study the four turtles foraging in the Gulf of Santa Elena foraged mainly in the first

5 m of the water column. Those shallow dives may be related to the turtles foraging at the

98

bottom of the coastal environment. However, two of the turtles foraging in that area made

excursions to deep water environments suggesting they were also foraging on animals or

floating algae associated with drifting material such as trees or other floatsom. The

variation in the depths used may be associated with the feeding preferences of the

individual turtles. Turtles foraging in the same area commonly show different depths

depending on whether they are planktivores or herbivores (Hatase et al. 2006). Green

turtles inhabit both shallow water and offshore deeper water where they could be resting

or foraging on deep water invertebrates (Seminoff et al. 2006b). In some populations

turtles avoid waters deeper than 10 m due to the lack of food availability and to avoid

predation by sharks (Senko et al. 2010). The turtles foraging in the Gulf of Papagayo

used different depths suggesting they may be using different resources in the same area.

One of the turtles used almost exclusively the first 20 m of the water column while the

other showed a peak at 70 m and the rest of the dives were distributed between 25 and 50

m. Turtles foraging in the Gulf of Fonseca also used different depths with one individual

diving from 15 to 75 m, and the other mainly diving in the upper 5 m of the water column

and at 70 and 100 m. The turtles swimming to 70 m depth were probably swimming to

the ocean floor because that was the depth in the areas where this behavior occurred.

This population did not use extensively the 20 m depth that was suggested as

neutral buoyancy for green turtles (Hays et al. 2000) and the average depth where green

turtles may rest (Hays et al. 2001). However, buoyancy control may not be a unique

strategy for resting sea turtles (Seminoff et al. 2006b). We did not find differences when

we compared depths and durations during day and night during migration. During

foraging there was a peak at 5 m depth during the night with duration of 2 and 20 – 40

99

min dives. The significant proportion of shallow and short dives during the night

indicated that these turtles were not achieving neutral buoyancy to rest but were resting

very close to or at the surface. As indicated for this population during internesting, the

turtles may float at the surface as a resting strategy (Chapter 2). The long duration of

night dives could also be related to vertical migration performed by plankton at night and

the turtles foraging on it as described for green turtles in Japan (Hatase et al. 2006).

Oceanic features

Effect of currents on turtle migrations

Ocean currents may influence differently sea turtle migration. Three turtles

moved in the same direction as the Costa Rica coastal current (CRCC) while migrating to

the Gulf of Foncesca. Sea turtles use currents to minimize energy costs while migrating

(Luschi et al. 2003a), their migratory routes drift as a result of prevailing currents causing

them to deviate from their original trajectory (Luschi et al. 2003b, Shillinger et al. 2008)

and their movements are influenced by oceanographic features like eddies or fronts

because of an increase in food availability (Seminoff et al. 2008). The CRCC is the east

edge of the CRD and continues along the coast until the Gulf of Tehuantepec in Mexico

where it gets cut off and turns offshore feeding the North Equatorial Current (Kessler

2006). Probably the three turtles migrating to the Gulf of Fonseca benefited from this

current while going from the nesting beach to the foraging area. However, the coastal

nature of two of these turtles indicated that they were following the coast independently

of the current. One of the turtles moving north swam farther from the coast suggesting

that the original route may have drifted due to the speed of the current. If these

100

individuals were taking advantage of the CRCC to reach the foraging area they would

have to swim against this prevalent current (that is present all year around) when they

returned to the nesting beach using the same migratory path. As for the turtle migrating to

the Panama Gulf, she swam with and against the prevalent current. The area is affected

by the north equatorial counter current which produces southern flow of the current until

the Gulf where the combination of trade winds and the north flow along the Colombian

coast causes the current to circulate north (Kessler 2006). In general, we suggest the

surface currents did not have an influence on the preferred migration routes of the turtles.

Nevertheless, some turtles may be benefiting from currents by swimming in the same

direction to reach the feeding grounds. The CRCC could have drifted the original

trajectory of one of the turtles.

Effect of currents, SST and CHL in foraging grounds

The turtles in the present study did not exhibit patterns that would suggest that

their behavior in the feeding grounds was influenced by variations in CHL or SST. The

eastern Tropical Pacific is characterized by coastal and open ocean upwellings, fronts and

eddies (Lavín et al. 2006). One of the most important oceanic features of the eastern

Pacific is the Costa Rican Dome (CRD), located off the Coast of Central America and

centered 300 km off the Gulf of Papagayo between Costa Rica and Nicaragua (Fiedler

2002). These characteristics may explain the importance of the Gulf of Papagayo, Bay of

Santa Elena and Gulf of Fonseca as foraging areas for the east Pacific green turtles. Even

though the data did not indicate that the turtles selected the sites with higher CHL; all the

feeding grounds described in this study had high primary productivity due to the

101

oceanography of the area. This could be influencing the general areas where the turtles

are, but not their specific movements within the area. The CHL levels do influence

movements of Galapagos green turtles (Seminoff et al. 2008) and loggerheads foraging in

the transition zone of the North Pacific (Polovina et al. 2001).

The turtles in our study used SSTs ranging from 22 to 31ºC. Even in the Papagayo

and Santa Elena region there was a decrease in the temperature produced by the

Papagayo winds, the turtles during these months did not show variation in their

movements. Although it was suggested that migrating turtles reach a threshold at 25 ºC

(Seminoff et al. 2008) it may be possible that during foraging they could support lower

temperatures.

During January and February 2009 there was an unusual drop in the SST and an

increase in the chlorophyll levels produced by the Papagayo winds. The temperatures

decreased considerably along the coast reaching 22 ºC. This unusual phenomenon did not

produce a change in the foraging area for the turtles which continued in the Papagayo

Gulf.

Conservation implications

The East Pacific green turtle is in danger of extinction (IUCN, 2010). Our study

indicated that green turtles that nest in Northwestern Costa Rica spend all their life as

adults in coastal areas of Central America (Panama, Costa Rica, Nicaragua, Honduras, El

Salvador and Guatemala). The coastal nature of their movements makes them vulnerable

to human activities in those countries. Small and large scale artisanal and commercial

fisheries in Central America use principally longlines, gillnets and trawling nets as

102

fishing gear, that are sources of high bycatch for sea turtle populations (Lewison et al.

2007) . Commercial fisheries target mainly yellowfin tuna, swordfish, dolphin fish and

marlin. Whereas artisanal fisheries in Costa Rica target species like flounder, grouper,

croaker and snapper among others (Obtained from Manual de Especies Comerciales de

Costa Rica).

Different populations of sea turtles had been reported to decline due to bycatch by

fisheries (Lewison et al. 2004, Spotila et al. 2000, Troëng et al. 2004). Based on our

results the East Pacific green turtles are mainly exposed to artisanal fisheries operating in

Central America. Small-scale fisheries have been overlooked over the past years as

researchers focused primarily on commercial large-scale fisheries that affect principally

highly migratory species (Peckham et al. 2007). There is a lack of information about

artisanal fisheries because they operate mainly without management, and their landings

are mostly unreported, as a consequence there is no information on their interaction with

turtles. During the course of this study we observed longlines and gill nets set in the

waters close to the nesting beach, and observed the capture of East Pacific green turtles

and ridley turtles in the Gulf of Papagayo. With the new information provided by this

study we suggest that there is a clear interaction between sea turtles and artisanal fisheries

because they are occupying the same areas. The fact that the turtles are swimming

through different countries makes management more complex and calls for agreements

between nations. More information is needed in order to understand how severe the

impact of coastal fisheries is on this population, which is extremely important to the

species (Chapter 3).

103

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Tables

Table 4.1 Post-nesting movements of East Pacific green turtles (Chelonia mydas) with satellite transmitters attached from

Nombre de Jesús, Costa Rica. Track length is total distance moved of the turtle during migration. Length of migration is the

calculated number of days the turtles took to reach the foraging areas. Total tracking includes the total duration of the satellite

transmitters.

Turtle Attachment CCL Total Tracking Foraging Length of Migration Track length

ID Date (cm) (days) grounds (days) (km)

1 17-Oct-06 77.50 29 Fonseca Gulf 29 430

2 24-Aug-07 91.40 70 Panama Gulf 26 1086

3 16-Jan-09 78.10 54 Fonseca Gulf 17 390

4 24-Jan-09 84.00 63 Papagayo Gulf 0 0

5 9-Oct-09 87.70 89 Santa Elena Bay 3 66

6 23-Oct-09 88.00 80 Fonseca Gulf 10 270

7 25-Oct-09 81.40 25 Papagayo Gulf 0 0

8 27-Oct-09 86.00 26 Santa Elena Bay 3 98

9 13-Nov-09 82.50 84 Santa Elena Bay 1 77.5

10 18-Nov-09 84.40 102 Santa Elena Bay 1 62.5

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Table 4.2 MCPs of East Pacific green turtles (Chelonia mydas) on the foraging

grounds. The MCPs were created based on all locations of the turtles in the foraging

areas. Foraging (tracking days) refers to the time spent on the foraging grounds.

Turtle Foraging Foraging Polygon Polygon

ID ground (tracking days) area (km²) perimeter (km)

2 Panama Gulf 45 265.07 75.24

3 Fonseca Gulf 33 4817.38 353.50 4 Papagayo Gulf 58 1071.60 138.83 5 Santa Elena Bay 84 1168.70 145.54 6 Fonseca Gulf 71 14083.71 823.00 7 Papagayo Gulf 18 602.68 94.40 8 Santa Elena Bay 18 2976.47 241.42 9 Santa Elena Bay 77 18260.10 631.56

10 Santa Elena Bay 89 2472.40 197.04

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Figures

Figure 4.1: Post-nesting movements of east Pacific green turtles nesting on Nombre

de Jesús, Costa Rica that migrated to the area of Santa Elena Bay( a, b), within the area

of Gulf of Fonseca(c) and to the Gulf of Panama (d).

a

b

115

Figure 4.1: Continued

d

c Fonseca Gulf

116

feb20

09ma

gn

<VAL

UE>

0 - 5.

3851

6473

8

5.385

1647

39 - 1

0.049

8752

6

10.04

9875

27 - 1

4.317

8215

14.31

7821

51 - 1

8.681

5414

4

18.68

1541

45 - 2

3.345

2358

2

23.34

5235

83 - 2

8.460

4988

1

28.46

0498

82 - 3

3.615

4708

9

33.61

5470

9 - 38

.6393

5852

38.63

9358

53 - 4

4.598

2055

7

44.59

8205

58 - 5

1.088

1576

5

51.08

8157

66 - 5

7.314

9185

2

57.31

4918

53 - 6

5.253

3493

65.25

3349

31 - 7

4.330

3451

5

74.33

0345

16 - 8

6.977

005

86.97

7005

01 - 1

21.45

7809

4

Figure 4.2: Migration routes in relation to geostrophic surface currents (0.5º spatial

grid, monthly composites) of East Pacific green turtles from Nombre de Jesús that migrated

to the area of the Gulf of Fonseca (a, b, c) and to the Gulf of Panama (d). Scale represents

magnitude of currents (cm/sec).

a b

a

b

117

feb20

09ma

gn

<VAL

UE>

0 - 5.

3851

6473

8

5.385

1647

39 - 1

0.049

8752

6

10.04

9875

27 - 1

4.317

8215

14.31

7821

51 - 1

8.681

5414

4

18.68

1541

45 - 2

3.345

2358

2

23.34

5235

83 - 2

8.460

4988

1

28.46

0498

82 - 3

3.615

4708

9

33.61

5470

9 - 38

.6393

5852

38.63

9358

53 - 4

4.598

2055

7

44.59

8205

58 - 5

1.088

1576

5

51.08

8157

66 - 5

7.314

9185

2

57.31

4918

53 - 6

5.253

3493

65.25

3349

31 - 7

4.330

3451

5

74.33

0345

16 - 8

6.977

005

86.97

7005

01 - 1

21.45

7809

4


c

d

118

Figure 4.3: Foraging areas of East Pacific green turtles represented by 100% MCP. Each polygon includes all the locations for

the individual turtles during foraging.

119


120

Figure 4.4: MCP per week of two east Pacific green turtles whose MCP areas were

higher than 10,000 km2. Each polygon includes locations for 7 days in the foraging

areas.

121

Figure 4.5: Percentage of dives of different durations performed by east Pacific

green turtles during migration and foraging. Migration = 8 turtles, foraging = 9 turtles

Figure 4.6: Percentage of dives at different depths performed by east Pacific green

turtles during migration and foraging. Migration = 8 turtles, foraging = 9 turtles.

*Indicates significant differences (ANOVA, p < 0.05) between 5 m and other depths.

0

5

10

15

20

25

30

2 5 10 20 30 40 50 60 90 >90

Div

es (

%)

Duration (min)

Migration Foraging

0

10

20

30

40

50

5 10 15 20 25 30 35 40 45 50 70 100 200

Div

es (

%)

Depth (m)

*

*

122

Figure 4.7: Percentage of dives at different depths performed by East Pacific green

turtles in the foraging areas. Santa Elena bay includes 4 turtles because of the small

variation between individuals (bars represent SD)

0

10

20

30

40

50

5 15 25 35 45 70

Gulf of Fonseca

turtle 3

0

10

20

30

40

5 15 25 35 45 70

Gulf of Papagayo

turtle 4

0

10

20

30

40

50

60

5 15 25 35 45 70

Div

es (

%)

turtle 6

0

10

20

30

40

5 15 25 35 45 70

turtle 7

Depth (m) Depth (m)

123


0

10

20

30

40

50

60

70

5 15 25 35 45 70 200

Depth (m)

Santa Elena Bay

0

10

20

30

40

5 15 25 35 45 70

Depth (m)

Gulf of Panama

turtle 2

124

Figure 4.8: Percentage of durations (a) and depths of dives (b) during migration and foraging of East Pacific green turtles.

Each graph includes percentages corresponding to day (white bars) and night (black bars). M: migration, F: foraging. Migration = 8

turtles, foraging = 9 turtles.

2 5 10 20 30 40 50 60 90 >90

Duration-F

0

10

20

30

40

2 5 10 20 30 40 50 60 90 >90

Duration-Ma

Duration (min) Duration (min)

Div

es (

%)

125


5 10 15 20 25 30 35 40 45 50 70 100

Depth-F

Day

Night

0

10

20

30

40

50

60

5 10 15 20 25 30 35 40 45 50 70 100

Depth-Mb

Div

es (

%)

Depth (m) Depth (m)

126

Figure 4.9: Monthly MCP in relation to Sea Surface Temperature (SST). SST (0.1°

spatial grid, monthly composites) for each month of study. MCPs correspond to all

locations in a month for each turtle in the foraging area.

127

11509

Feb 2009Value

High : 55.814

Low : 0.025

Figure 4.10: Monthly MCP in relation to Chlorophyll-a (CHL). CHL (0.05°

spatial grid, monthly composites) for each month of study. MCPs correspond to all

locations in a month for individual turtles in the foraging areas.

0.025 55.814

128

Chapter 5: Dispersion of East Pacific green turtle hatchlings emerging from

Nombre de Jesús, Costa Rica.

Abstract

We designed and developed a program to estimate the dispersion of East Pacific

green turtle hatchlings emerging on Nombre de Jesús, Costa Rica. First we created a DOS

program using FWTools and phyton script, then passed the output to a spatially explicit

model we created using ArcInfo Workstation to simulate the trajectory produced by

oceanic surface currents on an ideal planktonic particle. The model simulates a hatchling

drifting with the currents in the uppermost layer of the water column. We tested three

scenarios releasing the hatchling 10 km off: 1-Nombre de Jesús in peak hatchling season

(1st week of December), 2- Nombre de Jesús in non hatchling season (1

st week of June)

and 3-same latitude as the nesting beach, but in the southern hemisphere. Simulated

hatchlings showed a broad dispersion from Nombre de Jesús with the southernmost

location 1º 35’ S off Ecuador, the northernmost location 14º 30’ N off southern Mexico

and 115ºW in the Pacific Ocean. We found three different scenarios in which hatchlings

could be dispersed depending upon the year of emergence. 1- modeled hatchlings were

transported to oceanic waters and after three months were pushed back closer to the coast

2- hatchlings were transported north or south remaining close to the coast for the whole

year and 3- hatchlings were transported to waters off the coast for the whole year but still

within the Eastern Tropical Pacific (ETP). Areas with concentrations of hatchlings concur

with adult foraging areas suggesting that adult feeding grounds are in locations where

hatchlings are naturally deposited by the currents. The magnitude of currents in the

129

southern hemisphere was significantly lower than those near Nombre de Jesús suggesting

that the oceanography in the ETP provides a unique area for hatchling development. The

main oceanic characteristics related to the hatchling dispersal were the Costa Rican Dome

(CRD) associated with the eddies produced by the Tehuantepec, Papagayo and Panama

jets. The eddies and the CRD have associated with them high biological productivity

which would provide hatchlings with the necessary resources for development. This

model was the first attempt to simulate the hatchling dispersion from Pacific Costa Rica

and provided insights into the possible early life stage of the East Pacific green turtles.

130

Introduction

Sea turtles go through different ontogenetic stages in which they inhabit different

habitats. Generally adult foraging areas are neritic environments for all sea turtles species

except leatherbacks (Dermochelys corieacea), which forage in pelagic environments

(Shillinger et al. 2008). From the feeding grounds sea turtles migrate to nesting beaches

to lay eggs. Once these eggs hatch, hatchlings move into the ocean currents, entering

early juvenile nursery areas in oceanic environments (Musick and Limpus 1997). This is

also called the oceanic post-hatchling phase (Carr 1987). After this dispersion phase

turtles move to the later juvenile developmental habitats which commonly are neritic

environments (Musick and Limpus 1997). The flatback turtle (Natator depressus) is the

only sea turtle species that lacks an oceanic phase in its life cycle (Walker and Parmenter

1990).

Sea turtle neonates emerge from the nest, crawl immediately to the ocean and

swim away from shore hyperactively (Musick and Limpus 1997). This active swimming

is called the hatchling frenzy characterized by hatchlings swimming almost continuously

for a period of approximately 24 hours or more (Wyneken and Salmon 1992). This

“frenzy” is crucial for their survival because they swim away from shore where predators

are more abundant (Salmon and Wyneken 1987) and hatchlings also move to the main

offshore currents (Bolten 2003). Post-frenzy activity is the phase where hatchlings swim

during daylight hours and rest by floating at the surface during dark hours (Wyneken and

Salmon, 1992). Hatchlings initially orientate through visual cues following the brighter

oceanic horizon when they are on the beach crawling to sea, then they orient into waves

131

as they swim away from the beach and after that they orient using the earth’s magnetic

field as a cue (Lohmann and Lohmann 1992). During the post hatchling transitional stage

the young turtles start to feed while still in neritic zones and it is at this stage that they

reach the oceanic zone.

East Pacific green turtles (Chelonia mydas) nest in Costa Rica (Cornelius 1979)

with a peak nesting time in October (Chapter 3). Considering that mean incubation period

for green turtles is approximately two months (Fowler 1979), the peak hatchling season

for the turtles nesting on the Pacific coast of Costa Rica occurs at the beginning of

December. The offshore waters of the Eastern Tropical Pacific (ETP) offer unique

characteristics for hatchling dispersal and development.

Some of the most productive waters of the world exist in the ETP (Fiedler et al.

1991). The ETP is located between the subtropical gyres in the North and South Pacific at

23.5º N and S and 140º W. The eastern boundary is the California Current flowing from

the north and the Peru Current flowing from the South, and it is also constrained by the

impact of two equatorial currents (Fiedler and Talley 2006, Pennington et al. 2006). The

ETP is characterized by the presence of coastal and open ocean upwellings, fronts, eddies

and meanders (Lavín et al. 2006). The convergence of the trade winds in the intertropical

convergence zone (ITCZ) produces a low wind area off Central America where the sea

surface temperatures (SST) are higher than elsewhere in the area leaving a “warm pool”

(> 27.5 ºC) west of Mexico and Central America (Lavín et al. 2006, Fielder and Talley

2006). However, the wind blowing from the land to sea produces the Tehuantepec,

Papagayo and Panama jets causing eddies (upwellings) that generate productive areas

132

(with a decrease in SST and increase in chlorophyll levels) interrupting the warm low

productivity “warm pool” (Palacios and Bograd 2005). All the gulf regional winds

enhance euphotic nutrient supply and biological productivity. The jets are highly

seasonal, being stronger from December through April and decreasing or disappearing

after May (Pennington et al. 2006). Another characteristic present in the ETP is the

equatorial cold tongue (centered south of the equator) that is produced by the Peru

Current and equatorial upwelling which extends to 120ºW (Fielder and Talley 2006).

The Tehuantepec bowl (13N, 105W) is a shallow upwelling feature delimited in

the south by the Costa Rican Coastal Current which flows continuously from Costa Rica

to the Gulf of Tehuantepec (Kessler 2006). The Costa Rican dome (CRD) is the biggest

upwelling region of the ETP with high primary and secondary production (Lavín et al.

2006). The CRD is a shoaling of the thermocline of the ETP where the top of the

thermocline is 15 m deep at the dome at the center of the dome and 30 to 40m to the

north and south (Fiedler 2002). The CRD is centered 300 km off the Gulf of Papagayo

between Costa Rica and Nicaragua (9N, 90W); it is associated with the equatorial current

system and with the costal jets, eddies, the ITCZ and the geostrophic balance that occurs

in the thermocline (Fiedler 2002, Fiedler and Talley 2006). The CRD varies in size and

location through the year. In January the dome is far from the coast, there is a shoaling of

the thermocline at the coast (next to the Papagayo Gulf) that increases through March and

during this time the dome remains connected to the coast. During May and June it is

separated from the coast and from July to October the dome increases in size and

extending to the Gulf of Tehuantepec in November, and then decreases in size in

December (Fiedler 2002).

133

All these oceanographic characteristics make the ETP suitable for species that

congregate in this area. For example 29 species of cetaceans (Wade and Gerrodette

1993), 4 sea turtle species (Spotila 2004), numerous sea birds and fish (Greenblat 1979,

Au and Pitman 1986) among many other species inhabiting the ETP.

In this study, we estimated the dispersion of east Pacific green turtle neonates

after hatching on Nombre de Jesús beach on the Nicoya Peninsula of Northwest Costa

Rica in their post-hatchling stage following the currents in the area. The oceanographic

characteristics in the region were assumed to dominate dispersal and determine where

hatchlings would eventually reside and ultimately determine their return to the coast.


We designed and developed a model to simulate the dispersion produced by

oceanic surface currents for an ideal planktonic hatchling released from different

locations in the ETP. Sea turtle hatchlings are carried by ocean currents and act as passive

dispersers, like plankton. A similar approach was used to simulate the dispersal of

loggerhead hatchlings in Greece (Hays et al. 2010).

The currents included in the model were the Aviso geostrophic surface current (u

and v vectors, cm/sec) from years 1992 to 2009 and obtained from NOAA OceanWatch-

LAS (http://oceanwatch.pifsc.noaa.gov/las/servlets/dataset). Aviso was calculated with

the sea surface height anomaly data, merged with sea-surface height climatology and then

converted to current (Niiler et al. 2003). The Grids were netcdf files composited during a

7 day period, 0.5º spatial grid.

134

First we created a DOS program that used FW (Frank Warmerdam,

http://fwtools.maptools.org/) tools, phyton script and the GDAL (Geospatial Data

Abstraction Library, Geospatial Foundation) subpackage to read and convert netcdf files

to u and v layers in ASCII format readable by ArcInfo. Then we wrote a program in

ArcInfo Workstation (http://www.esri.com/software/arcgis/arcinfo) that took the present

grid with magnitude of the current and a model hatchling (assumed as ideal planktonic)

and made it travel along with the speed of the surface current (magnitude and direction)

for a 7 day period. Next the model hatchling moved to the next grid for the following

week and repeated the process for the amount of time indicated. We set the program to

run for every week starting with the first week of December or June until the last week of

November or May of the following year depending upon the conditions simulated.

The initial release point for the model hatchling was situated 10 km off the coast

which accounted for the first day of the frenzy where hatchlings swim away from shore

and would reach and be exposed to the main offshore currents (Bolten, 2003). We ran the

model in three different scenarios extended over 17 separate years 1992-2009 from which

oceanic data was available. First, we set the release point 10 km off Nombre de Jesús

(10° 23’ 30” N; 85° 50’ 07” W), Costa Rica during the first week of December

simulating the peak of hatchling emergence season for East Pacific green turtles and we

modeled it for one year with corresponding oceanography. Second, the release point was

10 km off the nesting beach starting the first week of June simulating the non hatchling

emergence season and we modeled the dispersal for one year. Lastly we ran the model

from an initial release point 10 km off the coast of South America at 10° 23’ 30” S (a

http://www.osgeo.org/

135

mirror image from the latitude of the nesting beach) to simulate the dispersion in the

southern hemisphere.

The model produced possible outputs of latitude and longitude, magnitude of

currents and date for each location where the model hatchling was transported for one

year. This allowed us to statistically compare the magnitude of the current to which

particles were exposed during different years and different months, with differences in

magnitudes between hatchling emergence season and no emergence season incorporating

differences between the currents at the nesting beach as well as differences in the

southern hemisphere.

Based on this information we generated maps using ArcGis version 9.3

geographic information system (GIS) software (www.esri.com/software/ArcGIS) for

visual interpretation. First we plotted the location of the hatchlings for each year, and

then we divided the locations into 3 months periods, overlapping them with the

magnitude of the current in the first week for each period. We also mapped speed and

direction of the currents to analyze oceanic characteristics present during dispersion and

visualized how they varied in the season.

Statistical analyses were performed using SPSS Inc. Statistical significance was

accepted at 0.05 level.

136

Results

Modeled hatchlings transported from Nombre de Jesús showed a broad dispersion

with the southernmost location 1º 35’ S in Ecuador, the northernmost location 14º 30’ N

in the south of Mexico and the westernmost location at 115ºW in the Pacific (Figure 5.1).

There were significant differences (ANOVA, F = 27.72, df = 15, p < 0.001) between the

magnitude of the currents to which the hatchlings were exposed during different years

(Table 5.1). The highest speed was in 1997 (65.86 cm/sec) and the lowest speed was in

2005 (19.36 cm/sec). We mapped the magnitude and direction of the currents in the first

week of December, March, June and September (Figure 5.2 shows one year as an

example). Even though there were no significant differences in overall speeds between

months (ANOVA, F = 1.728, df = 11, p = 0.63) there were obvious differences in speed

of currents in particular locations in the ocean during different months. March was the

month with highest current speeds, followed by December, June and September (mean =

32.99, 30.6, 30.4, 23.8 cm/sec respectively for all years). There was considerable

variation between years resulting in high variance and a lack of overall statistical

significance in the months

Although there were no significant differences in the current speed in which the

hatchlings were transported during emergence season (1st week of December) versus the

non hatchling season (1st week of June), there was a strong trend for hatchlings released

during emergence season to experience higher speeds (Hatchling season, Mean ± SD =

29.16 ± 20.0 cm/sec; Non hatchling season, Mean ± SD = 27.4 ± 20.3 cm/sec) (t-test, t =

1.720 df = 823, p = 0.086). The high variance from year to year reduced the overall

137

statistical significance of the differences. There were significant differences between the

current speeds experienced by the hatchlings released during emergence season from

Nombre de Jesús and the current speeds experienced by the hatchlings released from the

equivalent latitude to Nombre de Jesús in the southern hemisphere (12.51 ± 7.289) (t-test,

t = 21.559, df = 823, p<0.001). Currents near Nombre de Jesús were almost three times

faster than in the southern hemisphere.

In 10 of the 16 years analyzed, we found a similar trajectory for the first month

after the model hatchling was released. Approximately in week 5 hatchlings reached

between 95º and 100ºW and would then be transported to areas closer to the coast (Figure

5.3). Years 1994 and 2000 displayed a different dispersion pattern where the model

hatchlings were transported north staying for the full year south of the Gulf of Fonseca in

Nicaragua (Figure 5.3). In 2005 and 2008, on the other hand, model hatchlings were

transported to the west reaching longitudes between 110º and 115º W (Figure 5.3). These

two years had the lowest mean magnitude in current speeds. In 7 of the modeled years,

towards the end of the year, the model hatchlings transported to the coast of Colombia

and Panama.

The comparison between the geostrophic currents and how the model hatchlings

were transported (Figure 5.4) indicated that there were predominant features controlling

the model hatchling drifting in the ETP. The main characteristic was related to the CRD

which caused the model hatchlings to move to oceanic waters in December and January

and come closer to the coast in March. Also the jets produced by the trade winds

transported hatchlings north and south.

138

Discussion

The “post hatchling transitional stage” refers to the phase when the turtles start

foraging while they are still within the neritic zone and ends when the turtles enter the

oceanic zone initiating the “oceanic juvenile stage” (Bolten 2003). During both these

stages turtles mainly drift with the ocean currents (Carr 1987, Bolten 2003, Musik and

Limpus 1997). For this reason we suggest that the model estimating the movement of a

model hatchling that is being transported by a current represents the movements of green

turtle hatchlings emerging from Nombre de Jesús.

Overall the hatchlings occupied a broad area of the ETP for all years. Main

concentrations were found along the coast of Nicaragua and the coast of Colombia and

Ecuador. There was also an important aggregation of hatchlings along the coast of Costa

Rica. The area in Nicaragua (near the Gulf of Fonseca) is highly used by East Pacific

green turtles as a foraging ground (Chapter 4), which suggests that the location of adult

feeding grounds are the direct result of hatchling dispersion. Contrary to our results

Atlantic loggerhead post-hatchlings are commonly found in the edge of the Gulf Stream

and the loggerheads hatching in Japan transverse the entire Pacific to the coast of

California (Bowen et al. 2005) travelling extensively through the ocean. Our model

suggested that hatchlings emerging in the Pacific coast of Costa Rica may be transported

by currents and “captured” in the oceanographic system of the ETP.

There were statistical differences between the magnitudes of the current between

the years. Even small variations in the characteristics of currents could lead to different

distributions of hatchlings (Collard and Ogren 1990). Based on the results of the model,

139

hatchlings emerging from Nombre de Jesús could disperse following three different

scenarios. The most common trajectory observed in most of the years studied had turtles

leaving the nesting beach with model hatchlings transported to waters off the coast. The

main oceanic feature influencing the dispersion of hatchlings was the Costa Rican Dome

(CRD) which increased in size and was closer to the coast from January through March

(Fiedler 2002). After three months the model hatchling was transported back closer to the

coast, where in some cases it remained in coastal areas and in other simulations it was

transported back to oceanic areas off Panama.

The second scenario that resulted from the simulation had the model hatchling

being transported north or south but, remaining close to the coast for the entire year. This

simulation resulted in hatchlings spending their first year of life in neritic environments

along the coast of Central America north and south from the natal beach (Figure 5.2 years

1994, 1997, 2000, 2007). If the currents are drifting the hatchlings into coastal areas then

(depending on the year of emergence) these turtles may not have an oceanic phase. Even

though in these particular simulations post-hatchlings may be associated with neritic

coastal environments they still inhabit the surface; therefore this hatchling stage is

different than the neritic juvenile stage where juveniles forage on the sea floor (Musick

and Limpus 1997). In the third model scenario hatchlings were transported to the west at

about 10° N, off the coast for the first year in which case the hatchlings would be in areas

of low productivity but still within the ETP (Fiedler et al. 1991).

The magnitude of the currents in the southern hemisphere was significantly lower

than the currents near Nombre de Jesús which suggests that the oceanography in the ETP

140

makes it a unique area for hatchling development. Hatchlings emerging from hypothetical

nesting beaches along the shore of Ecuador, which is 10° S of the equator and a southern

mirror image of the Costa Rican beaches, would not have the same opportunities for

dispersal as do hatchlings from Costa Rica. The simulation and models revealed two

main oceanic features that may be related to hatchling dispersion. First the CRD is

surrounded by currents flowing cyclonically (Fiedler 2002) and even though in December

the dome is separated from the coast, the current off the Nicoya Peninsula transported

model hatchlings towards the dome. The model suggested that the Tehuantepec,

Papagayo and Panama eddies played an important role transporting hatchlings. These

eddies are produced by the winds blowing from land, which intensify during the dry

season (November to April) (Willet et al. 2006). The Tehuantepec and Papagayo eddies

are important transporters of nutrients from the continent to the ocean and cause

upwellings, which also bring nutrients to the surface waters (Palacios and Bograd 2005).

The currents related to these eddies may be the main factor transporting hatchlings to the

ocean. Carr (1987) found post-hatchling turtles associated with floating material and

Witherington (2002) found loggerhead post- hatchlings associated with debris and other

biota in the edge of the Gulf Stream.

The most important characteristic associated with eddies and the dome is their

high biological productivity. The cyclonic circulation associated with the CRD combined

with the strong and shallow thermocline produce an upwelling which makes the CRD a

distinct biological habitat (Ballance et al. 2006). In addition, the Tehuantepec and

Papagayo eddies transport coastal waters (nutrient rich) to the ocean interior that combine

with the process of downwelling during intensification and upwelling as they decay

141

resulting in a high primary and secondary productivity area (Palacios and Bograd 2005).

These high productivity areas should provide the necessary nutrients to produce food for

the hatchlings so that they can develop into juveniles.

The duration of the oceanic stage for Atlantic green turtles is between 2.8-4.6

years (Reich et al. 2007), for Hawaiian green turtles it extends to 6 years (Zug et al. 2002)

and for Atlantic loggerheads as much as 7 years (Bjorndal et al. 2003). The variations in

the duration of the oceanic stage may depend upon the available resources in the

locations where the turtles spend this stage (Bolten 2003). During all these years the

turtles also move actively and considering that turtles are approximately 15-20 cm at one

year of age (Bjorndal et al. 2003, Zug et al. 2002) they may be able to swim and select

places to forage within the same general area. After one year the juvenile turtles from

Costa Rica could be actively swimming in the same oceanic features where they

developed because of the important biological productivity of the Eastern Tropical

Pacific.

This model simulated the drift of a particle based on ocean currents and was an

estimation of the dispersal of sea turtle hatchlings. This model provided insights into the

early life stage of East Pacific green turtles and indicated that they would disperse

throughout the region as currents shifted from year to year. However, the predominant

locations where hatchlings would congregate would be along the Costa Rican coast, off

Panama and Colombia and off Nicaragua. These are some of the same areas to which

adult females migrate after nesting on Nombre de Jesús (Chapter 3), although we did not

find any turtles migrating to Colombia. The model indicated that the driving forces for

142

hatchling dispersal were a unique set of currents, upwellings and other oceanographic

features in the Eastern Tropical Pacific Ocean. This first attempt to simulate green turtle

hatchling dispersion from Costa Rica demonstrates that one of the important reasons for

successful green turtle nesting in Costa Rica is that the oceanic features nearby ensure a

wide dispersion of hatchlings into productive waters where they will thrive and grow to

become juvenile turtles that can navigate and move about by active swimming. By the

time they have entered the free swimming juvenile stage turtles will have experienced a

wide area of the Eastern Pacific Ocean and have a map and memory of conditions in the

region. Considering that the oceanic phase is the least understood in sea turtle life history

(Witherington 2002) more research needs to be focused in this direction. More detailed

modeling coupled with oceanic sampling will refine the initial estimates we derived from

this model. This research also raises a conservation issue. Since oceanic debris and trash

also drift with currents and are influenced by oceanic features such as upwellings and

convergence zones, we can expect that plastics and other waste from human civilization

along the Central American coast accumulate in the same places as the green turtle

hatchlings and are a potential source of mortality for those turtles (McCauley and

Bjorndal 1999).

143

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147

Tables

Table 5.1 Mean magnitude (cm/sec) of currents in the eastern Tropical Pacific

Ocean that transported a model hatchling for one year for all years analyzed.

Year Magnitude

(Mean) SD

1992 18.25 16.404 1993 38.12 21.691

1994 28.58 7.545

1995 21.48 13.419

1996 21.13 13.943

1997 65.86 25.787

1998 22.27 16.839

1999 42.73 21.091

2000 26.06 5.867

2001 22.46 14.803

2002 26.64 13.017

2003 24.73 21.712

2004 25.49 19.020

2005 19.36 10.403

2006 22.13 14.082

2007 34.00 18.021

2008 20.05 12.118

148

Figures

Figure 5.1: Location of model hatchlings released 10 km off the coast of Nombre de

Jesús in northwest Costa Rica as calculated by the model every week for all analyzed

years (1992-2009). Each dot represents the new position of the model hatchling after

being transported by a current for a period of 7 days.

149

Figure 5.2: Circulation of currents in the Eastern Pacific Ocean at different times of the year. Colors represent

magnitude (cm/sec) and arrows represent direction of the currents. Each picture represents the first week of the months referred to in

the legend. We obtained data from NOAA OceanWatch-LAS. The grids were composited in a 7 day period with 0.5º spatial

resolution. Scale represents magnitude of the currents (cm/sec)

Septem

ber 199

5

mag199

5sep

<VALUE

> 0 - 4.472

136021

4.47213

6022 - 8

.246211

052

8.24621

1053 - 1

2.20655

537

12.2065

5538 - 1

6.40122

032

16.4012

2033 - 2

0.61552

811

20.6155

2812 - 2

5.07987

213

25.0798

7214 - 2

9.61418

533

29.6141

8534 - 3

4.40930

176

34.4093

0177 - 3

9.66106

415

39.6610

6416 - 4

5.27692

413

45.2769

2414 - 5

1.31276

703

51.3127

6704 - 5

8.30952

072

58.3095

2073 - 6

6.85057

831

66.8505

7832 - 8

0.23091

888

80.2309

1889 - 1

26.2893

524

150


Septe

mber

1995

mag1

995sep

<VAL

UE> 0 -

4.4721

36021

4.4721

36022

- 8.246

211052

8.2462

11053

- 12.20

655537

12.206

55538

- 16.40

122032

16.401

22033

- 20.61

552811

20.615

52812

- 25.07

987213

25.079

87214

- 29.61

418533

29.614

18534

- 34.40

930176

34.409

30177

- 39.66

106415

39.661

06416

- 45.27

692413

45.276

92414

- 51.31

276703

51.312

76704

- 58.30

952072

58.309

52073

- 66.85

057831

66.850

57832

- 80.23

091888

80.230

91889

- 126.2

893524

Septem

ber 199

5

mag199

5sep

<VALUE

> 0 - 4.472

136021

4.47213

6022 - 8

.2462110

52

8.246211

053 - 12

.206555

37

12.2065

5538 - 1

6.40122

032

16.4012

2033 - 2

0.61552

811

20.6155

2812 - 2

5.07987

213

25.0798

7214 - 2

9.61418

533

29.6141

8534 - 3

4.40930

176

34.4093

0177 - 3

9.66106

415

39.6610

6416 - 4

5.27692

413

45.2769

2414 - 5

1.31276

703

51.3127

6704 - 5

8.30952

072

58.3095

2073 - 6

6.85057

831

66.8505

7832 - 8

0.23091

888

80.2309

1889 - 1

26.2893

524

151

Figure 5.3: Movement of model hatchlings released 10 km off the coast of Nombre de Jesús in northwest Costa Rica as

calculated by the model for each year from 1992 to 2008. Each dot represents the new position of the model hatchling after being

transported by a current for a period of 7 days. Lines connecting points represent probable trajectories from one week to the next.

152


153


154


155


156


157


158


159


160


161

Figure 5.4: Movement of model hatchlings released 10 km off the coast of Nombre de Jesús in northwest Costa Rica in

comparison with ocean currents as calculated by the model for each year from 1992 to 2008. Each dot represents the new position of

the model hatchling after being transported by a current for a period of 7 days. Black dots represent a three month period starting the

same week as the period of the background current image. Grey dots represent the rest of the locations for the year. Background color

represents the magnitude of the currents (cm/sec) for the first week of the month referred to in the map. Scale represents magnitude of

the current (cm/sec)

Color reference

December1993

March 1994

Septe

mber

1995

mag19

95sep

<VAL

UE> 0 -

4.4721

36021

4.4721

36022

- 8.246

211052

8.2462

11053

- 12.20

655537

12.206

55538

- 16.40

122032

16.401

22033

- 20.61

552811

20.615

52812

- 25.07

987213

25.079

87214

- 29.61

418533

29.614

18534

- 34.40

930176

34.409

30177

- 39.66

106415

39.661

06416

- 45.27

692413

45.276

92414

- 51.31

276703

51.312

76704

- 58.30

952072

58.309

52073

- 66.85

057831

66.850

57832

- 80.23

091888

80.230

91889

- 126.2

893524

162

June 1994

September 1994


163

December1995

June 1996

September 1996

March 1996


164

December1997

June 1998

September 1998

March 1998


165

December1999

June 2000

September 2000

March 2000


166

December

1997

March

1998

June

1998

September

1998

December 2001

June 2002

September 2002

March 2002


167

December

1999

March

2000

June

2000

September

2000

December 2003

June 2004

September 2004

March 2004


168

December

2003

March

2004

June

2004

September

2004

December 2005

June 2006

September 2006

March 2006


169

December 2007

March 2008

June 2008

September 2008


170

Chapter 6: Conclusions

The East Pacific green turtle nests in high concentrations on Nombre de Jesús and

Zapotillal. These two beaches represent the most important nesting site for this species in

Northwestern Costa Rica. By using the information obtained with ultrasound scans we

could estimate a more accurate clutch frequency. Turtles nested 5 times in a season, the

highest number reported for green turtles in the Eastern Pacific Ocean. The accuracy of

this information is crucial to calculate population parameters, such as the number of

females in a population, or estimates of annual reproductive output. Also it can give us

insights into mating strategies. Without such information, it is difficult to establish

effective conservation strategies and management plans. During the nesting season, this

population spent the time between clutches in a small area in front of the nesting beach

diving to the bottom, thus using the complete water column, demonstrating the

importance not just of the nesting beach but also of the waters surrounding it for the

conservation of green turtles. During the internesting, the turtles spent most of their time

resting. The strong diel pattern in their diving behavior demonstrated that during the day

the turtles rest by performing U-dives but during the night the turtles float at the surface.

We could estimate through modeling currents and simulating the transport of hatchlings

that once the eggs hatch, the neonates coming from Nombre de Jesús would disperse in

different ways depending on the year. The hatchlings could be transported to the area of

the Costa Rican Dome (CRD) ~300km off the Papagayo Gulf; they could be transported

north and south along the coast and less common they could be transported to waters off

the coast still within the Eastern Tropical Pacific Ocean. Interestingly, hatchlings may be

foraging during their oceanic stage in areas close to the adult foraging areas where

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females go immediately after the nesting season. Adult foraging areas were in the Gulf of

Papagayo, where turtles demonstrated to be resident of the area, the Bay of Santa Elena,

the Gulf of Fonseca and the Gulf of Panama. All the post nesting movements were

coastal. During migration the turtles used mainly the first 5 meters of the water column,

performing short dives (2 min) and long dives (40 min). During foraging the turtles dove

mainly between 5-10 meters, showing variability between foraging areas and between

individuals. The fact that the Pacific green turtle is spending its entire life cycle in the

Eastern Tropical Pacific reveals the unique characteristics that this oceanic region offers

for hatchlings and adults. Despite the fact that adult females did not follow currents to

migrate; seasonal oceanic features make the area rich in nutrients. The main features

affecting the turtles are the CRD and eddies produced by the trade winds blowing from

the Gulf of Papagayo, Panama and Tehuantepec. These produce upwelling areas which

are rich in primary and secondary productivity. The foraging areas in Papagayo and

Santa Elena and Gulf of Fonseca are directly affected by the CRD and by the Papagayo

and Tehuantepec eddies.

The findings of this project have major implications for conservation. First,

number of females nesting per night added to their high reproductive output may indicate

this is a population with good resource availability. Because historic records for this

population do not exist we could not estimate if the intense egg poaching taking place on

the nesting beaches is already affecting these numbers. Urgent action must take place to

protect beaches because this activity is detrimental for sea turtle populations. The habit of

staying within 5 km of the nesting beach during internesting and the consequent presence

of males in the area makes the waters off Nombre de Jesús a hot spot for conservation of

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this species. The coastal habit of these turtles and the fact they are travelling through

waters of Panama, Costa Rica, Nicaragua, Honduras, El Salvador and Guatemala makes

them vulnerable to the human activities in the region. Artisanal fisheries are one of the

mortality sources for sea turtles due to by catch, activity which is common in Central

America. Therefore, it is essential that enhanced protection be provided both on the

beaches and in the waters of Northwestern Costa Rica if the east Pacific green turtle is to

be protected from extinction over the next few years.

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Curriculum Vita

Gabriela S. Blanco

Specialization: Marine Biology, Ecology, Conservation Biology

Major Advisor: James R. Spotila, Ph.D.

Drexel University, Department of Biology

3141 Chestnut Street, Philadelphia, PA 19104

Email: [email protected]

EDUCATION

Ph.D., 2005-present: Drexel University, Philadelphia PA. Dissertation Research: “Movements

and Behavior of the East Pacific Green Turtle (Chelonia mydas) from Costa Rica”. Defense date:

October 2010.

Licenciatura in Biological Sciences, 2005: Universidad Nacional de la Patagonia, SJB,

Comodoro Rivadavia, Argentina. Thesis Research: Uso de la Ría Deseado por parte de la Tonina

Overa (Cephalorhynchus commersonii): Pautas para el manejo y conservación de la especie.

RESEARCH EXPERIENCE

2006- 2010. Principal Investigator. Migration and Behavior of Eastern Pacific green turtles.

2007-2009. Co-Principal Investigator and Field Manager. Leatherback Turtle Project, Playa

Grande, Costa Rica. Earthwatch Institute. Drexel University/Indiana-Purdue University Fort

Wayne.

2006. Research Assistant. Population studies of red-bellied turtles. Drexel University,

Philadelphia, Pennsylvania

TEACHING EXPERIENCE

2006. Teaching Assistant. Cells and Genetics. Bioscience and Biotechnology. Drexel University.

2006. Teaching Assistant. Microbiology. Bioscience and Biotechnology. Drexel University.

2005. Teaching Assistant. Molecular Biology. Bioscience and Biotechnology. Drexel University.

OUTREACH/ INFORMAL TEACHING ACTIVITIES

2008 - Primary schools in Guanacaste, Costa Rica.

2007-2009–Visiting Universities and volunteers. Parque Nacional Marino Las Baulas, and

Goldring Marine Biology Station, Playa Grande, Costa Rica.

PUBLICATIONS

Santidrián Tomillo, M.P.; Suss, J.; Wallace, B. P.; Magrini, K; Blanco, G.; Paladino, F.V.; and

Spotila J. R. 2009. Influence of emergence success on the annual reproductive output of

leatherback turtles. Marine Biology 156: 2021-2031.

Blanco G. S., Morreale, S. J., Vélez, E., Piedra, R., Paladino, F. V. and Spotila, J. R.

Reproductive output and ultrasonography of an endangered population of east Pacific green

turtles. Submitted to Journal of Wildlife Management.

PRESENTATIONS AT SYMPOSIA: 6 presentations at scientific meetings

GRANTS AND AWARDS

2009 Research Fellow Grant. Wildlife Conservation Society.

2010 Travel Grant Biology Department, Drexel University.

2007-2010 Research Fellow. Betz Chair of Environmental Science.

mailto:[email protected]

Movements and behavior of the East Pacific Green ... - CORE

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