physiological status and post-release mortality of sea...

PHYSIOLOGICAL STATUS AND POST-RELEASE MORTALITY OF SEA

TURTLES RELEASED FROM GILLNETS IN THE LOWER CAPE FEAR RIVER,

NORTH CAROLINA

Jessica E. Snoddy

A Thesis Submitted to the

University of North Carolina Wilmington in Partial Fulfillment

of the requirements for the Degree of

Master of Science

Department of Biology and Marine Biology

University of North Carolina Wilmington

2009

Approved by

Advisory Committee

Andrew J. Westgate_______ Thomas E. Lankford ____

_____Amanda L. Southwood_____

Chair

Accepted by

______________________________

Dean, Graduate School

ii

TABLE OF CONTENTS

ABSTRACT ....................................................................................................................... iv

ACKNOWLEDGMENTS ...................................................................................................v

DEDICATION ................................................................................................................... vi

LIST OF TABLES ............................................................................................................ vii

LIST OF FIGURES ......................................................................................................... viii

INTRODUCTION ...............................................................................................................1

Sea Turtle Biology ...................................................................................................1

Nearshore Behavior and Movements .......................................................................2

Fishing Threats.........................................................................................................4

Diving Physiology and Stress of Capture ................................................................6

Project Rationale ......................................................................................................9

CHAPTER 1. BLOOD BIOCHEMISTRY OF SEA TURTLES RELEASED FROM

GILLNETS IN THE LOWER CAPE FEAR RIVER, NORTH CAROLINA, USA ........12

ABSTRACT .......................................................................................................................12

INTRODUCTION .............................................................................................................13

METHODS ........................................................................................................................16

Field Procedures.....................................................................................................16

Blood Analysis .......................................................................................................19

Statistical Analysis .................................................................................................21

RESULTS ..........................................................................................................................22

DISCUSSION ....................................................................................................................23

Management Implications ......................................................................................28

iii

CHAPTER 2. MOVEMENTS OF JUVENILE SEA TURTLES RELEASED FROM

GILLNETS IN THE CAPE FEAR RIVER, NORTH CAROLINA .................................38

ABSTRACT .......................................................................................................................38

INTRODUCTION .............................................................................................................39

METHODS ........................................................................................................................42

Field Procedures.....................................................................................................42

Analysis of Location Data .....................................................................................44

Assessment of Mortality ........................................................................................45

RESULTS ..........................................................................................................................48

Movements and Habitat Utilization .......................................................................48

Post-Release Mortality ...........................................................................................49

DISCUSSION ....................................................................................................................52

CONCLUSIONS................................................................................................................86

REFERENCES ..................................................................................................................89

iv

ABSTRACT

By-catch of sea turtles in the North Carolina coastal gillnet fishery has been

implicated as a significant source of mortality, and numerous management measures have

been taken to either minimize the detrimental effects of capture (gear modification and

attendance requirements) or to reduce or prevent capture of sea turtles in fishing gear

(time and area-based closures). Management decisions regarding sea turtle interactions

and acceptable take levels for this fishery are currently based on analyses of fishing

effort, observed bycatch of sea turtles, sea turtle strandings, and estimates of mortality

rates for sea turtles due to fisheries interactions derived from these data. The purpose of

this study was to directly evaluate the impact that entanglement in gillnets has on the

physiological status and post-release behavior of sea turtles, and to use these data to

refine our estimates of post-release mortality for the gillnet fishery. I conducted physical

examinations and collected blood samples from eighteen sea turtles captured in shallow-

set gillnets in the lower Cape Fear River. Satellite and VHF radio transmitters were

deployed on fourteen of these turtles so that I could monitor their post-release movements

and document mortality events. I found that entanglement in gillnets resulted in severe

disruptions of blood biochemistry. One confirmed post-release mortality and three

suspected post-release mortalities were documented during the course of the study.

Integration of physiology and behavior data with observer and stranding data shows

promise as a means of refining mortality estimates associated with gillnet entanglement.

v

ACKNOWLEDGMENTS

Special thanks go to my family and friends for supporting me through the years.

Many thanks to my advisor, Dr. Amanda Southwood, for the opportunity to be a part of

her lab and this research. I am forever grateful for her guidance and support. I would

like to thank my lab mates, James Casey, Lisa Goshe, and Leigh Anne Harden, for their

advice and the laughs.

Field work would not have been possible without the expertise of Captain Jeff

Wolfe. Many laughs will be remembered from long days on the river. Thanks to

Elizabeth Brandon, Diana Bierschenk, and countless other volunteers in the field.

Catherine McClellan provided valuable information on techniques and problems

associated with tracking juvenile green turtles in nearshore environments, and Theresa

Thorpe gave valuable information on where to find sea turtles in the river.

Jean Beasley, Craig Harms, and Chris Butler provided blood samples from

captive sea turtles. Thanks to David Owens and Gaëlle Blanvillain for help with

corticosterone analysis. I thank Francine Christiano and Marion Landon for assistance

with analyzing blood lactate concentrations. Dr. James Blum assisted with statistical

analysis.

North Carolina Sea Grant provided funding for this research. Finally, I would

like to thank University of North Carolina Wilmington Department of Biology and

Marine Biology, especially my committee members, for their guidance and support

throughout my studies.

vi

DEDICATION

To my family, the Snoddys and the Snobergers, for many years of love and support.

vii

LIST OF TABLES

Table Page

1. Capture data for Kemp’s ridley and green sea turtles entangled in shallow-set

gillnets in the lower Cape Fear River during May - October 2007 .......................30

2. Descriptive statistics for blood parameters measured in juvenile Kemp’s ridley

and sea turtles immediately following removal from gillnets (INITIAL samples).32

3. Results for paired t-test analysis of INITIAL and PRE-RELEASE values of blood

parameters in Kemp’s ridley and green sea turtles ................................................34

4. Mortality classification, total tracking duration and percent of high quality

Transmissions received for all tracked greens and Kemp’s ridley sea turtles .......51

viii

LIST OF FIGURES

Figure Page

1. Blood lactate, LDH, CPK, glucose, phosphorus and corticosterone for sea

turtles entangled in gillnets from 20 – 240 minutes ...............................................35

2. Photograph of satellite and radio tag deployment on Kemp’s ridley turtle Lk 1 ...60

3. Capture locations and 25 and 50% volume contours of all filtered location

data for all turtles captured in the lower Cape Fear River May – October 2007 ...61

4. Percent of each location class transmissions received from all turtles released

from gillnets .........................................................................................................62

5. Map of filtered location data for green turtle Cm 3 ...............................................63

6a. Map of filtered location data for green turtle Cm 13 .............................................64

6b. Expanded view of filtered location data in lower Cape Fear River for green

turtle Cm 13 Lk 2 ...................................................................................................65

7. Map of filtered location data for Kemp’s ridley turtle Lk 2 ..................................66

8. Map of filtered location data for Kemp’s ridley turtle Lk 4 .................................67







15. Map of filtered location data for green turtle Cm 10 .............................................74



18. Map of filtered location data for Kemp’s ridley turtle Lk 1 ..................................77

ix

19a. Transmission pattern of entire track duration for Kemp’s ridley turtle

Lk 2 ........................................................................................................................78

19b. Transmission pattern of entire track duration for Kemp’s ridley turtle

Lk 4 ........................................................................................................................78

19c. Transmission pattern of entire track duration for green turtle Cm 2 .....................79

19d. Transmission pattern of entire track duration for green turtle Cm 3 .....................79

19e. Transmission pattern of entire track duration for green turtle Cm 5 .....................80

19f. Transmission pattern of entire track duration for green turtle Cm 1 .....................80

19g. Transmission pattern of entire track duration for green turtle Cm 4 .....................81

19h. Transmission pattern of entire track duration for green turtle Cm 7 .....................81

19i. Transmission pattern of entire track duration for green turtle Cm 8 .....................82

19j. Transmission pattern of entire track duration for green turtle Cm 10 ...................82

19k. Transmission pattern of entire track duration for green turtle Cm 11 ...................83

19l. Transmission pattern of entire track duration for green turtle Cm 12 ...................83

19m. Transmission pattern of entire track duration for green turtle Cm 13 ...................84

19n. Transmission pattern of entire track duration for Kemp’s ridley turtle

Lk 1 ........................................................................................................................84

INTRODUCTION

Sea Turtle Biology

Sea turtles are long-lived marine reptiles that develop and mature very slowly

(Musick and Limpus, 1997). These characteristics have important implications for

conservation of threatened and endangered sea turtle species. Juveniles that do not

survive to sexual maturity will not reproduce and will not add individuals to the

population, which could eventually cause a population decline. Sea turtles face many

threats to their survival, including loss of nesting beaches and foraging grounds, egg and

hatchling predation, pollution, and other anthropogenic factors such as boat strikes and

interactions with fisheries (Lutcavage et al., 1997). Recently, there has been a growing

concern about mortality associated with entanglement in commercial fishing gear, and the

impact this may have on sea turtle populations (Gearhart, 2001; Griffin et al., 2006).

Coastal fishing operations may have a large impact on juvenile sea turtles in particular, as

they utilize nearshore developmental habitats.

Sea turtles undergo long-distance migrations throughout their life, beginning

with hatchling movements from breeding beach nests to oceanic habitats (Bolten and

Balazs, 1995). The first few years of life at sea are referred to as “the lost years” because

very little is known of sea turtles’ movements and behavior until they recruit into coastal

habitats as juveniles (Bolten and Balazs, 1995). Juvenile sea turtles migrate into North

Carolina’s nearshore waters to forage in the spring when water temperatures (Tw) warm

to approximately 13°C. When Tw begin to drop in the fall, turtles will emigrate from the

North Carolina waters (Coles and Musick, 2000) and move into deeper oceanic or more

2

southerly waters. (Epperly et al., 1995a, Epperly et al., 1995b). These yearly migrations

are largely dictated by sea turtles’ preferred Tw range.

.

Nearshore Behavior and Movements

North Carolina waters serve as an important nursery ground for foraging and

developing juvenile sea turtles, and also provide breeding habitat for adult sea turtles.

The three species of sea turtles most frequently encountered in North Carolina are

loggerheads (Caretta caretta), greens (Chelonia mydas) and Kemp’s ridleys

(Lepidochelys kempii) (Epperly et al., 1995a). Kemp’s ridleys only nest in Rancho

Nuevo, Mexico, but frequent North Carolina as juveniles to feed on crabs and small

benthic invertebrates (Mortimer, 1995). Adult loggerheads nest in coastal North Carolina

(Hawkes et al., 2005), and juveniles of this species feed on benthic invertebrates and fish

(Mortimer, 1995). Adult green turtles also nest in North Carolina, and juvenile greens

feed on algae in the shallow coastal waters (Mortimer, 1995).

Movements of juvenile turtles in the summer months are usually limited to a

small home range (~5 km2) (Seminoff et al., 2002; Makowski et al., 2005). Site fidelity

is based on availability of food and nightly resting spots (Brill et al., 1995; Makowski et

al., 2005). Sea turtles display strong homing behaviors for particular areas and routinely

pinpoint specific foraging sites. They also exhibit strong site fidelity from hundreds of

kilometers away when migrating (Lohmann et al., 1997). Juvenile loggerheads that were

displaced after capture in Pamlico Sound, North Carolina returned to the same capture

location within the same season and in subsequent years (Avens et al., 2003).

3

Sea turtles display predictable daily movement and diving patterns during summer

months. During the morning and late afternoon they are found in shallow waters, but

move into deeper areas when Tw increases around mid-day. Mendonça (1983) found

that juvenile greens utilize shallow seagrass flats for 70% of daylight hours in a Florida

lagoon. It is typical for turtles to return to the same resting spots night after night

(Mendonça, 1983; Southwood et al., 2003). In general, dives are longer during nighttime

resting periods than during daytime foraging. Turtles are most active from dawn to dusk

while foraging and they dive frequently and to shallow depths during those times

(Southwood et al., 2003).

The majority of research on movements and seasonal utilization of coastal North

Carolina waters by sea turtles has focused on the Core and Pamlico Sound region. Aerial

surveys of Pamlico and Core Sounds indicate that there is a seasonal migration of sea

turtles into and out of this region and that nearly all turtles found inshore are juveniles

(Epperly et al., 1995a; Epperly et al., 1995b). Read et al. (2004) found that green turtles

in Pamlico Sound occupy very shallow waters (0-2 m), while loggerheads and Kemp’s

ridleys are found at more variable depths (0-6 m). Turtles were found in Tw of 8º C to

30º C, but spent 90% of the time in Tw greater than 14º C (Read et al., 2004). Juvenile

sea turtles also use the lower Cape Fear River as a seasonal foraging habitat, but very

little is known of their behavior and movement patterns in this area, with most of the

information coming from interactions with fisheries.

4

Fishing Threats

All sea turtles are protected by the Endangered Species Act of 1973, so there is a

federal mandate to minimize the negative impacts of commercial fishing on populations.

Commercial fishing in North Carolina peaks during the summer months, which coincides

with the presence of large numbers of juvenile sea turtles in coastal waters (Gearhart,

2001; Read and Foster, 2004; Price, 2005). Fishing interactions with sea turtles have

become a critical concern for fisheries managers, as several mass stranding events have

occurred during peak fishing season since 1995 (Gearhart, 2001; Price, 2005).

Sea turtles encounter a variety of commercial fisheries while in nearshore habitats, but

encounters with coastal gillnets are thought to be the primary contributor to stranding

events and sea turtle mortality (NC Division of Marine Fisheries, 2005). These fisheries

target mostly monkfish and flounder, but bycatch of sea turtles in gillnets is a common

occurrence (Federal Register, December 2002). A gillnet can be described as a mesh

fence in the water column, usually running perpendicular to the shoreline. A float line is

attached to the top of the net and a weighted lead line pulls the bottom of the net down to

the sea floor. Sea turtles that swim into a gillnet may become entangled, making it

difficult for them to surface to breathe.

The degree of injury and physiological disruption for sea turtles entangled in

gillnets can vary depending on the gear type. Large mesh gillnets (mesh size >5 inches)

(Federal Register, December 2002) are most dangerous to sea turtles, as the holes are

large enough to wrap around the turtle’s head or limbs. Large mesh gillnets were

historically used in fisheries that targeted sea turtles before the establishment of the

Endangered Species Act (Federal Register, December 2002). In Pamlico Sound, North

5

Carolina, large mesh net is prohibited due to the high risk to sea turtles (Federal Register,

December 2002). Small mesh gillnets (mesh size ≤ 5 inches) are considered a lesser

threat to sea turtles because turtles are less likely to become entangled (Federal Register,

December 2002).

The impact of gillnet entanglement on sea turtle physiology and survival may also

depend on the depth at which the gillnet is set and manner in which net is fished.

Shallow-set gillnets are set in waters less than 3 m deep, are typically left to soak

overnight, and range in length from 500 to 2000 yards (Gearhart, 2001; Federal Register,

September 2002; Price, 2005). In contrast, deep-set gillnets are set at depths of 3 m or

greater, may soak for up to 3 days at a time, and range in length from 2,000 – 10,000

yards (Gearhart, 2001; Federal Register, September 2002; Price, 2005). Deep-set gillnets

pose a much larger threat to sea turtles, as the turtles are unable to surface to breathe

while entangled. In-net mortality rates for deep-set gillnets are high (Gearhart, 2001),

and use of this gear is now prohibited (Federal Register, September 2002). The majority

of sea turtles caught in shallow-set nets are released alive (Gearhart, 2001). Lower rates

of in-net mortality for shallow-set gillnets may be due to the fact that turtles have less

difficulty reaching the surface to breathe while entangled, or that they have not been in

the net for a long period of time.

The National Marine Fisheries Service and NC DMF have implemented

numerous mitigation measures to address the problem of sea turtle bycatch in the gillnet

fisheries of Core and Pamlico Sounds, but until recent years the lower Cape Fear River

has received less attention from regulatory agencies. Anecdotal evidence from local

fishermen suggests that there has been an increase in the number of juvenile turtles in the

6

Cape Fear River over the last 5-10 years, which may be due to an increase in algae in the

area (Jeff Wolfe, David Beresoff, pers. comm.). Juvenile greens, loggerheads and

Kemp’s ridleys are incidentally captured in gillnets in the lower Cape Fear River, with

greens being caught most frequently. Incidental capture of sea turtles is highest between

June and September (Thorpe and Beresoff, 2005). Thorpe and Beresoff (2005)

documented 23 green turtles, 4 Kemp’s ridleys and 6 loggerheads captured in 40 gillnet

trips over the course of one summer.

Fisheries managers now recognize that the lower Cape Fear River provides

important seasonal foraging habitat for sea turtles during the summer months, and the NC

DMF has placed restrictions on gillnetting in the lower Cape Fear River between June

and August. Gillnet fisherman are required to attend their nets at all times and remove

any turtles that become entangled, however there are no mesh size or depth restrictions

(Pate, DMF, 2006). Due to this net-attendance restriction, the summer gillnet fishery in

this area has essentially closed because fisherman are unwilling to stay with their nets

throughout the 12 hours of a typical set. Management agencies are eager to learn more

about sea turtle habitat utilization and behavior in this region so that they may refine

mitigation measures.

Diving Physiology and Stress of Capture

Sea turtles can dive for prolonged periods and to great depths voluntarily because

of their low reptilian metabolic rates, efficient blood oxygen transport mechanisms, and

moderate tolerance to hypoxia (Lutcavage and Lutz, 1997). Typical voluntary dive times

vary according to size, species and habitat. Larger turtles are able to stay submerged for

7

longer periods than juveniles, due to the nature of scaling of oxygen stores and metabolic

rate with body size. Oxygen stores scale directly with mass, whereas mass specific

metabolic rate scales in an allometric manner, with an exponent of approximately 0.75

rather than 1. Therefore, larger turtles have larger oxygen stores with relation to mass-

specific metabolic rate than do smaller turtles (Schmidt-Nielsen, 1984). Juvenile

loggerheads routinely dive for 19-30 min, juvenile green turtles typically dive for 9-23

min, and juvenile Kemp’s ridleys normally dive for 12-18 min (Lutcavage and Lutz,

1997).

Studies of natural diving behavior indicate that juvenile turtles typically spend

very little time at the surface (Gitschlag, 1996; Lutcavage and Lutz, 1997). This is likely

due to the fact that, as with most air-breathing diving vertebrates, sea turtles rely

primarily on aerobic metabolism while submerged (Kooyman, 1985). The lung is the

major oxygen store for shallow diving turtles in coastal areas (Lutcavage and Lutz,

1997). For example, loggerheads, store 72% of oxygen in the lungs, and tissue oxygen

stores are minor (Lutz and Bentley, 1985). Oxygen stores are rapidly replenished and

CO2 is eliminated during short surfacing intervals, and the number of breaths increases

with increasing dive time (Lutcavage and Lutz, 1991). Sea turtles will generally surface

for air before oxygen stores run out, but are able to cope with progressively decreasing

blood oxygen stores through high blood oxygen affinity and strong blood buffering

capabilities. Thus, blood pH remains stable and lactate levels also remain low during the

course of routine aerobic dives (Lutcavage and Lutz, 1991; Lutz and Bentley, 1985).

Although sea turtles can stay submerged for 20-180 minutes during voluntary

dives, forced submergence due to net entanglement can be lethal (Lutz and Bentely,

8

1985). Turtles caught in a net will struggle in attempts to escape and surface for air, and

oxygen stores will be rapidly depleted. Tethered adult green sea turtles diving in

attempts to escape depleted their oxygen stores within 15 min (Wood, 1984), and turtles

forcibly submerged in nets for as little as 30 minutes may drown (Lutcavage and Lutz,

1997). Juvenile turtles are more susceptible to drowning than adults, due to their high

mass-specific metabolic rates and relatively small oxygen stores (Berkson, 1966;

Schmidt-Nielsen, 1984). Turtles submerged in nets for longer than an hour have a low

chance of survival (Lutz and Bentley, 1985; Federal Register, 2004).

Forcibly submerged turtles must resort to anaerobic metabolism when there is not

enough oxygen to support aerobic metabolic pathways, and this results in a build-up of

lactic acid and acidification of the blood (Lutz, 1997). Increased CO2 levels (respiratory

acidosis) may also contribute to a drop in blood pH during forced submergence (Stabenau

et al., 1991; Stabenau and Vietti, 2003). Alteration in blood pH can damage proteins,

disrupt cellular function, and affect the ability of blood to coagulate properly (Soslau,

2004). Physiological damage incurred due to net entanglement may affect the turtle’s

behavior and reduce its chances of survival post-release. Previous studies have noted that

forcibly submerged sea turtles spend extended periods of time at the surface, presumably

to recover and restore physiological homeostasis (Stabenau and Vietti, 2003). A sea

turtle’s recovery from lactic acid build up can take over 15 hours, depending on the

severity of the acidosis (Lutz and Dunbar-Cooper, 1987). Lactate must be cleared from

the blood stream and tissues by conversion back to pyruvate and subsequent processing

by aerobic metabolic pathways, so ample oxygen is required to recover from metabolic

9

acidosis. Extended surface intervals would make turtles vulnerable to predators and

increase the danger of being struck by a boat.

Numerous other alterations in blood biochemistry may occur as a result of

enforced submergence. For example, prolonged struggling in a net may result in injuries

and muscle tissue damage, which could result in release of intracellular enzymes such as

lactate dehydrogenase (LDH) and creatine phosphokinase (CPK) into the blood (Aguirre

et al., 1995; Randall et al., 2002; Dahlhoff, 2004; Martínez-Amat et al., 2005; Moyes and

Schulte, 2006). Damaged muscle tissue may also release intracellular ions, such as K+,

Mg2+, and Ca2+ into the blood (Moyes et al., 2006), and the controlled release of

intracellular ions may occur as a counteractive measure against blood acidosis.

Corticosterone concentration may increase in sea turtles that are forcibly submerged, due

to induction of a systemic stress response (Gregory et al., 1996). Assessment of blood

biochemistry at the time a turtle is captured may provide important information regarding

the overall condition of the animal and the likelihood of post-release survival (Dahlhoff,

2004).

Project Rationale

Although most sea turtles are released alive from shallow-set gillnets, there are no

existing data on the physiological condition and ultimate fate of turtles once they are

released. Fisheries impacts on the sea turtle population are thought to be substantial,

which is why bycatch reduction is a hotly debated subject amongst conservationists and

fisheries managers (Magnuson et al., 1990; Griffin et al., 2006). Before 1995, an average

of less than 200 turtles were found stranded on North Carolina’s coasts per year. From

10

2001-2006, an average of 401 turtles per year stranded in North Carolina (North Carolina

Wildlife Resources Commission Sea Turtle Stranding Network Database 2005). The

Pamlico Sound gillnet fishery was identified as the most likely cause of the turtle

stranding events, due to the concentrated fishing effort in that region at the time of the

strandings (Gearhart, 2001). Additionally, stranded turtle carcasses showed visible

injuries consistent with gillnet fishery interactions, such as trauma to flippers and neck,

and necropsies showed that the turtles were in otherwise good nutritional condition

(Boettcher, 2000). Although it was likely that the increase in strandings was due to

gillnet entanglements, other possibilities, such as an overall increase in the turtle

population in this area, could not be discounted.

The Division of Marine Fisheries currently bases sea turtle mortality estimates on

fishing effort, stranding data, and observer coverage (Gearhart, 2001). These are only

estimates of fisheries related mortality, and there is a need for refinement. Current

fisheries management decisions are based on best available estimates and anecdotal

evidence, but there is no direct documentation of the number of turtles that survive after

release from gillnets. An assessment of the impacts of entanglement on sea turtle health

and documentation of post-release mortality rates are necessary so that the current

restrictions on the fishery are correctly justified and the economic impacts on fisherman

are minimized.

There is also a need to conduct basic research of the movement patterns and

behavior of sea turtles in the lower Cape Fear River. There are numerous reports of sea

turtle interactions with gillnets in this area, but little understanding of sea turtle habitat

utilization and the potential for overlap with fishing operations. An understanding of sea

11

turtle movement patterns would allow managers to implement mitigation measures to

reduce or prevent sea turtle interactions in this region.

The overall goal of my research was to refine our understanding of the impacts of

entanglement in gillnets on the physiology, behavior, and survivability of sea turtles. My

specific research objectives were as follows:

1. Analyze blood chemistry of sea turtles released from gillnets to assess

physiological impacts of entanglement.

2. Quantify post-release mortality of sea turtles released from shallow-set gillnets in

the lower Cape Fear River using satellite telemetry.

3. Document seasonal movements of sea turtles in the lower Cape Fear River using

satellite telemetry.

CHAPTER 1. BLOOD BIOCHEMISTRY OF SEA TURTLES RELEASED FROM

GILLNETS IN THE LOWER CAPE FEAR RIVER, NORTH CAROLINA, USA

Accepted for publication in the Journal of Wildlife Management

ABSTRACT

Mortality due to fisheries interactions has been implicated as a contributor to

population decline for several species of sea turtle. The incidental capture of sea turtles

in the coastal gillnet fisheries of North Carolina has received much attention in recent

years, and mitigation measures to reduce sea turtle mortality due to gillnet entanglement

are a high priority for managers and conservationists. Efforts to evaluate the effects of

gillnet entanglement on sea turtle populations are complicated by the lack of information

on health status of turtles released alive from nets and post-release mortality. I obtained

blood samples from green and Kemp’s ridley sea turtles captured in gillnets for 20 - 240

minutes to assess the impacts of gillnet entanglement on blood biochemistry and

physiological status. I measured concentrations of lactate, corticosterone, ions (Na+, K

+,

Cl-, P, Ca

2+), enzymes (LDH, CPK, AST), protein and glucose in the blood and also

performed comprehensive physical examinations of turtles to document external

indicators of health status (injuries, lethargy, muted reflexes). Statistical analyses were

conducted to evaluate the effects of entanglement time on blood biochemistry and to look

for correlations between blood biochemistry and results of the physical examinations. I

observed a significant increase in blood lactate, LDH, CPK, phosphorus, and glucose

with increased entanglement time. Alterations in blood biochemistry were generally

associated with a decline in health status as indicated by results of the physical

13

examination. Although entanglement time plays an important role in determining the

health status of sea turtles upon release from a gillnet, my results suggest that factors such

as the depth and severity of entanglement may also have an effect on health status of

turtles and the probability of post-release survival.

INTRODUCTION

Commercial fishing operations frequently overlap with sea turtle habitat, and

unintended capture of sea turtles in fishing gear has become a problem of increasing

concern for fisheries managers and conservationists (Magnuson et al., 1990; National

Marine Fisheries Service and U.S. Fish and Wildlife Service, 1991; Santora, 2003;

Lewison et al., 2004; Read et al., 2004; Cox et al., 2007). All sea turtles are protected by

the Endangered Species Act of 1973, and the federal government has a mandate to assess

and mitigate the impacts of commercial fisheries interactions on sea turtle populations

(National Marine Fisheries Service and U.S. Fish and Wildlife Service, 1991).

Interactions with gillnet fisheries have been implicated as a major source of mortality for

loggerhead (Caretta caretta), Kemp’s ridley (Lepidochelys kempii) and green (Chelonia

mydas) sea turtles in coastal North Carolina, USA (Gearhart, 2001; Price, 2005).

Throughout spring, summer and fall of 1999, 430 sea turtle carcasses washed up on the

shores of North Carolina, accounting for 19% of the total sea turtle carcass strandings

reported in the United States that year (Boettcher, 2000). Coastal gillnet fisheries were

identified as a primary contributor to the mass sea turtle stranding event, due to the high

14

fishing effort that year and injuries on sea turtle carcasses consistent with gillnet

entanglement (Boettcher, 2000; Gearhart, 2001).

Since the mass stranding events of 1999, North Carolina Division of Marine

Fisheries (NC DMF) and the National Oceanic and Atmospheric Administration (NOAA)

Fisheries have implemented temporal and spatial fisheries closures to avoid interactions

with sea turtles, as well as gear restrictions designed to minimize the impacts of

entanglement on sea turtle health and survival (Federal Register, 2004; Thorpe and

Beresoff, 2005). For example, use of gillnets is now restricted to shallow waters (< 3 m),

as the incidence of in-net mortality for turtles caught in shallow-set gillnets is low

compared with deep-set gillnets (3 - 6 m) (Gearhart, 2001; Price, 2005). Managers

speculate that sea turtles entangled in shallow-set nets are still capable of reaching the

surface to breathe, and therefore the risk of drowning in the nets is reduced (Gearhart,

2001). Although observer data and reports from fishermen indicate that sea turtles caught

in shallow-set gillnets are typically released alive (Gearhart, 2001), the ultimate fate of

these sea turtles is not known. Severe disruptions to normal physiological function and

injuries sustained as a result of entanglement in fishing gear could lead to undocumented

post-release mortality (Lutcavage and Lutz, 1991; Stabenau and Vietti, 2002; Harms et

al., 2003).

Previous studies have shown that sea turtles that experience hypoxia and restraint

stress related to enforced submergence have significant alterations in blood biochemistry

(Berkson, 1966; Stabenau et al., 1991; Gregory et al., 1996). Harms et al. (2003)

observed a decrease in blood pH in loggerhead turtles submerged in trawls for up to 30

minutes. The controlled release of ions into the blood may occur as a counteractive

15

measure against blood acidosis. For example, a significant increase in blood K+

concentration has been observed following capture and restraint in Kemp’s ridley turtles

(Stabenau et al., 1991; Hoopes et al., 2000). It is possible that K+ ions are released by

cells in exchange for H+ ions to buffer changes in blood pH, although a K

+/H

+ exchanger

has not yet been identified in the cells of sea turtles (Rose, 1977; Lutz, 1997; Stabenau

and Vietti, 1999; Hoopes et al., 2000). It is likely that the acidosis experienced by

forcibly submerged sea turtles has both a respiratory and metabolic component. Stabenau

et al. (1991) saw a 6-fold increase in lactate levels of Kemp’s ridleys forcibly submerged

in shrimp trawls for approximately 7.3 min. Kemp’s ridley turtles captured in

entanglement nets and temporarily restrained in holding tanks also experienced an

increase in plasma lactate concentrations and alterations in blood ions indicative of acid-

base adjustments (Hoopes et al., 2000). Increases in blood lactate concentrations and a

concomitant decrease in blood pH suggest a shift towards reliance on anaerobic

metabolic pathways, which could be the result of intense activity associated with escape

attempts or hypoxia due to forced submergence. Prolonged anaerobiosis due to

entanglement in fishing gear or restraint may leave sea turtles exhausted and vulnerable

to other threats upon release from gear. There is also evidence that entanglement in

fishing gear results in induction of a systemic stress response in sea turtles, which may

persist following release depending on the extent of injuries suffered or stress

experienced. Gregory et al. (1996) noted approximately a 3-fold increase above control

values for plasma corticosterone (a hormone indicative of stress) in loggerheads that were

forcibly submerged in a trawl for up to 30 minutes.

16

As with entanglement in trawls and other gear types, sea turtles entangled in

gillnets may experience physiological disturbances related to restricted access to air,

intense struggling, injuries to soft tissues, and induction of a systemic stress response

(Lutz and Dunbar-Cooper, 1987; Stabenau et al., 1991; Gregory et al., 1996; Boettcher,

2000; Jessop et al., 2004). The goals of this study were to 1) investigate the

physiological impacts of gillnet entanglement on juvenile sea turtles, and to 2) determine

if entanglement time would be indicative of the degree of physiological disruption in

gillnet captured juvenile sea turtles. I predicted that the degree of physiological

disruption, as indicated by blood biochemistry, would increase with increased

entanglement time and that severe disruptions in blood biochemistry would be associated

with poor health status as ascertained by a physical examination.

METHODS

Field Procedures

I captured sea turtles in 5.5 inch mesh gillnets set at depths of 1- 2 m in the lower

Cape Fear River, North Carolina during daylight hours (06:00 - 16:00) from May through

October of 2007. This area consists of 3 bays enclosed by marsh to the east and a man-

made rock wall which divides the bays from the river to the west. Average tide height at

this location is approximately 1 m, and the rock wall is partially exposed at low tide.

Gillnets remained in water for a maximum of 6 hours and were attended at all times so

that I could record the time when turtles were captured and the length of time that turtles

spent in the net (entanglement time). I captured 14 green turtles and 4 Kemp’s ridley

17

turtles. Table 1 provides details on capture time and location, entanglement time,

environmental conditions at the capture site, and morphometric data for each turtle.

Turtles were entangled for an average of 82.3 min (range of 20 - 240 min) and I closely

monitored them for signs of distress while in the net. If turtles remained submerged for

greater than 20 minutes or appeared to be in danger of drowning due to airway or

swimming restriction, I immediately removed them from the net.

Upon removal from nets, I brought the turtles on board the boat and restrained

them in a 16 cm × 43 cm padded plastic bin. The turtles were shaded from direct sunlight

and were periodically sprayed with seawater. I immediately obtained a 4 ml blood

sample (INITIAL sample) from the cervical sinus using heparinized vacuum tubes and a

21G x 1.5” needle (BD Vacutainer, Franklin Lakes, NJ, USA) and stored samples on ice

(N = 12 for green turtles, N = 4 for Kemp’s ridley turtles). INITIAL blood samples were

not obtained from 2 of the 14 green turtles that I captured. Using calipers, I measured

straight carapace length notch to notch (SCLnn) and straight carapace width (SCW),and

calculated carapace area (cm2) using the formula for the area of an ellipse: area (cm

2) = ∏

× 1/2 (SCLnn) × 1/2 (SCW). I obtained cloacal body temperature (TB) using a digital

thermometer (model 52 II, Fluke Corp., Everett, WA, USA) with a flexible veterinary

probe at a depth of 4 - 25 cm. A passive induced transponder (PIT) tag was inserted

above the left front flipper of each turtle that I captured for future identification.

I examined turtles for net-inflicted external injuries and assessed reflex responses

and activity levels using a protocol described by Sadove et al. (1998). Injuries were

classified as minor (scrapes to skin or shell), moderate (shallow cuts to skin, bruising of

skin), or severe (deep cuts that exposed muscle). I classified reflex responses to a gentle

18

touch to the tail, nose, and eyelid as good (immediate and strong flinch), delayed (slow or

lethargic flinch), or absent. Activity was classified as “high” if the turtle frequently and

vigorously struggled in attempts to escape. Turtles were classified as having “moderate”

activity levels if they occasionally struggled vigorously with long periods of little to no

movement in between. Activity was classified as “low” if turtles exhibited infrequent

and weak struggling or no movement when onboard. I assigned a physical grade (A, B,

C, D) based on the reflex response level, activity level, and presence/absence and severity

of net-inflicted external injuries to each turtle. The physical grade criteria are as follows:

A. High activity, all reflexes present and good, no injuries

B. Medium activity, all reflexes present and good, minor injuries

C. Medium activity, missing or delayed reflexes, moderate injuries

D. Low activity, missing or delayed reflexes, severe injuries

I assigned each grade based on exhibition of at least two of the three criteria.

Turtles were on board the boat for an average of 57.7 min (range of 10 - 110 min),

and I subsequently released them within 10 meters of the capture site. Immediately prior

to release, I obtained a second 4 ml blood sample (PRE-RELEASE sample) from 7 green

turtles so that I could assess the effect of onboard restraint on blood parameters.

INITIAL and PRE-RELEASE blood samples were stored on ice for 30 - 240 minutes

before centrifuging at 7,000 RPM for 10 minutes using a portable field centrifuge (Zip

Spin, LW Scientific Inc., Lawrenceville, GA, USA). Plasma was stored in cryogenic

tubes on dry ice and ultimately transferred to a −80ºC freezer. I analyzed blood

biochemistry within 4 months of sample collection.

19

All procedures used for this study were approved by University of North

Carolina Wilmington Institutional Animal Care and Use Committee (protocol #2006-12)

and The NOAA Fisheries Office of Protected Resources (permit # 1572).

Blood Analysis

Plasma concentrations of lactate dehydrogenase (LDH), creatine phosphokinase

(CPK), aspartate aminotransferase (AST), Na+, K

+, Cl

-, P, Ca

2+, total protein, albumin,

globulin, uric acid, urea nitrogen and glucose were analyzed by spectrophotometry at a

veterinary diagnostic laboratory (Antech Diagnostics, Southaven, MS). I determined

plasma lactate concentrations using a commercially available two-step lactate reagent kit

(Pointe Scientific Inc., Canton, MI) and standard spectrophotometric techniques (Lambda

25 UV/Vis, PerkinElmer, Waltham, MA). I used lactate standards of 5 mmol·L-1

, 10

mmol·L-1

, 15 mmol·L-1

, and 50 mmol·L-1

to generate a regression equation to describe the

relationship between absorbance and lactate concentration ([Lactate] mmol·L-1

= (abs –

0.0309)/0.0299, r2 = 0.9995). All plasma samples were run in duplicate, and I used the

mean of duplicate absorbance values to estimate plasma lactate concentrations using the

standard regression. Buffer solutions and 15 mmol·L-1

standard solutions were assayed

simultaneously with plasma samples as a quality control measure.

I analyzed corticosterone levels by radioimmunoassay (RIA) as previously

described by Valverde (1996). For each sample, I extracted 25 to 250 µL of plasma with

4 mL of anhydrous diethyl ether, dried the tubes under nitrogen gas, and resuspended

them with 1 mL of gel buffer (pH 7.0). I pipetted two 400-µL aliquots from the 1 mL of

gel buffer, and placed the tubes at 4ºC overnight. The following day, all tubes were

20

incubated in a water bath for 30 minutes at 37ºC. At this point, I prepared tubes

containing 400 µL of corticosterone standard solution with concentrations ranging from

0.0625 to 8 ng·mL-1

in duplicate. Following incubation, I added 100 µL of costicosterone

antibody (# B3-163, lot 163-077, purchased from Esoterix Laboratory Services,

Calabasas Hills, CA) to all tubes (standards and samples), as well as 100 µL of tritiated

corticosterone (~10000 cpm; PerkinElmer Life and Analytical Sciences, Inc, Boston,

MA). The tubes were incubated overnight at 4ºC. The next day, I placed all tubes in an

ice bath, and added 500 µL of dextran-coated charcoal to each assay tube except those

used to determine total counts. All tubes were incubated for 15 minutes at 4ºC, and

centrifuged at 2300 rpm at 4ºC for 15 minutes. I then poured the supernatant into

scintillation vials and added 5 mL of Ecolume scintillation cocktail to each vial. The

vials were counted for 60 seconds with a Wallac 1409 liquid scintillation counter. I then

calculated corticosterone concentrations in ng·mL-1

from the counts using the standard

curve. The values were corrected by multiplying the volume extracted by the extraction

efficiency and the fraction aliquoted from the reconstituted sample (40%). I calculated

the extraction efficiency for each sample individually by extracting the same volume of

plasma used to determine corticosterone concentration as described above (25 - 250 µL),

and by adding 100 µL of tritiated corticosterone (~10000 cpm) prior to the ether-

extraction. Extraction efficiencies ranged 92.4 - 100%. I used a loggerhead sea turtle

control sample and extracted 4 - 5 times to evaluate intra and inter-assay variability,

which was 4.3% and 12.9%, respectively.

21

Statistical Analyses

In order to assess the effects of entanglement time and physical grade on each

blood parameter for the INITIAL samples collected from green turtles, I used analysis of

co-variance (ANCOVA). Only INITIAL samples (N = 12), as opposed to PRE-

RELEASE samples were used for these analyses as this allowed me to assess the

physiological disturbances attributable to gillnet entanglement without the potentially

confounding effects of on-board restraint. Due to a low sample size (N = 4), I did not

perform statistical analyses of Kemp’s ridley data.. I examined the relationship between

each blood parameter and predictors such as TB, TW, carapace area (as an indicator of

body size), and salinity using Pearson’s correlation. For predictors that were determined

to be strongly (r > 0.50) and significantly (P < 0.05) correlated with a particular blood

parameter, I initially included them in the ANCOVA model for that parameter. As a

result, TB was used as a co-variate in the ANCOVA model for LDH, and carapace area

was used as a co-variate in the ANCOVA models for Na+, Cl

-, and glucose. Ultimately,

carapace area contributed significantly to the ANCOVA model for glucose but none of

the other co-variates contributed significantly to ANCOVA models.

I used a paired t-test and applied a Bonferroni correction to compare INITIAL and

PRE-RELEASE values for blood parameters in green sea turtles (N = 7). Significance

was set at P < 0.003 using the Bonferroni correction. I performed all analyses using

Statistical Analysis Software (SAS) version 9.1 (Cary, NC, USA).

22

RESULTS

The majority of turtles that were entangled in gillnets for less than 4 hours were

classified as having physical grades of B and C (Table 1). Of the 18 turtles that I

captured, 17 % of the turtles were classified as physical grade A, 33 % turtles were

classified as physical grade B, 39 % of the turtles were classified as physical grade C, and

11 % of the turtles were classified as physical grade D. Table 2 presents descriptive

statistics and standard deviations (SD) for blood parameters of INITIAL samples from

gillnet-entangled green and Kemp’s ridley turtles. Increased entanglement time and

decreased physical grade accounted for an increase in plasma lactate (F6 = 25.91, P =

0.001) (Fig. 1a), LDH (F7 = 7611.39, P = 0.009) (Fig. 1b), CPK (F5 = 8.53, P = 0.017)

(Fig. 1c), phosphorus (F6 = 10.61, P = 0.010) (Fig. 1d), and glucose (F7 = 8.44, P =

0.028) (Fig. 1e). I also found that entanglement time and physical grade did not account

for trends in plasma albumin (F5 = 5.01, P = 0.051), AST (F6 = 0.25, P = 0.939) , Na+ (F7

= 0.58, P = 0.750), K+ (F6 = 2.41, P = 0.177), Cl

- (F7 = 2.39, P = 0.209), Ca

2+ (F6 = 3.67,

P = 0.088), total protein (F6 = 3.83, P = 0.081), globulin (F6 = 2.11, P = 0.216), uric acid

(F6 = 4.83, P = 0.052), urea nitrogen (F6 = 0.86, P = 0.577), or corticosterone (F6 = 1.34,

P = 0.383). Although the trend in increased corticosterone with increased time in net and

decreased physical grade was not significant, I recorded very high corticosterone in

gillnet entangled turtles (Table 2, Fig. 1f). I did not find any significant trend in any

blood parameter between INITIAL and PRE-RELEASE samples from gillnet entangled

green turtles.

23

DISCUSSION

The main focus of this study was to investigate the effect of gillnet entanglement

time on blood biochemistry and health status of sea turtles. I found that longer

entanglement times resulted in pronounced disruptions in blood biochemistry and were

associated with lower physical grades (Tables 1 and 2). In general, blood parameters that

did not vary significantly with increased gillnet entanglement time fell within the range

of published values for healthy, wild-caught green sea turtles (Bolten and Bjorndal, 1992;

Aguirre et al., 1995; Hasbún et al., 1998), whereas parameters that were significantly

impacted by gillnet entanglement time were in agreement with literature values for sea

turtles exposed to stressors (Lutz and Dunbar-Cooper, 1987; Aguirre et al., 1995;

Gregory et al., 1996; Hoopes et al., 2000; Jessop et al., 2002; Harms et al., 2003; Jessop

et al., 2004; Jessop and Hamann, 2005).

Entanglement times of as little as 30 minutes resulted in elevated plasma lactate.

The highest lactate value recorded in my study (50.6 mmol·L-1

) was 2 – 8 times higher

than maximum values for blood lactate reported in other studies of sea turtle

entanglement in fishing gear (6.2 – 20 mmol∙L-1) (Lutz and Dunbar-Cooper, 1987;

Hoopes et al., 2000; Harms et al., 2003). The average blood lactate concentration for

green turtles in our study (30.6 ± 3 mmol∙L-1, N = 12) was 9 times higher than average

blood lactate concentration of rehabilitated captive green turtles not exposed to a stress

protocol and just prior to release (3.4 ± 1.1 mmol∙L-1, N = 10) (C. Harms and J. Beasley,

unpublished data). Although sea turtles have a high aerobic capacity to support sustained,

long-distance swimming (Butler et al., 1984), they resort to anaerobic pathways during

24

intense burst activity. Intense struggling and forced submergence during entanglement

likely result in a shift from aerobic to anaerobic metabolic pathways due to an imbalance

between oxygen supply and demand. Increased reliance on glycolysis and lactic acid

fermentation results in lactate accumulation in blood and tissues.

Oxygen is required in order for lactate to be metabolized and cleared from the

bloodstream. Previous studies have noted that sea turtles subjected to enforced

submergence may require extended periods of time at the surface to rest, recover, and

repay the oxygen debt incurred while forcibly submerged (Lutz and Bentley, 1985;

Stabenau and Vietti, 2003). Extended time at the surface may leave recovering sea turtles

vulnerable to other threats, such as boat strikes or shark predation. Studies investigating

lactate loads and clearance rates for sea turtles captured in trawls or restrained in in-water

cages have demonstrated that lactate clearance rates can vary between 0.25 – 3.3 mmol·L-

1·hr

-1 for blood lactate concentrations of 5 – 14 mmol·L

-1 (Lutz and Bentley, 1985;

Stabenau and Vietti, 2003). If sea turtles in my study cleared lactate at the fastest rates

documented in the literature, it would take 4 – 15 hours to remove accumulated lactate

from the bloodstream. It is likely that full clearance of the high lactate loads I observed

would actually require more time, as clearance rates tend to decline with declining blood

lactate concentrations. Lutz and Dunbar-Cooper (1987) calculated that clearance of only

3 – 4 mmol·L-1

blood lactate could take as long as 20 hours due to the decline in

clearance rates at low blood lactate concentrations.

Although low to moderate levels of circulating lactate (< 5 mmol·L-1

·hr-1

) may not

impose a great physiological challenge to sea turtles, this situation may be problematic

for turtles that experience repeat captures in fishing gear. The limited home range of

25

juvenile green and Kemp’s ridley sea turtles in nearshore, coastal waters (Mendonca,

1983; Brill et al., 1995; Avens et al., 2003; Avens and Lohmann, 2004; Makowski et al.,

2006) predisposes them to multiple encounters with fishing gear set within their home

range. Additional enforced submergence events greatly increase the chance of in-net or

post-release mortality, particularly if the turtle has not fully recovered from the

physiological disruptions of the first entanglement. Stabenau and Vietti (2003) noted

severe metabolic disturbances in juvenile loggerhead turtles forcibly submerged in trawls

multiple times, and found that a surface recovery interval of 42 minutes following the

first submergence was inadequate for blood lactate clearance.

Although the ANCOVA model to assess the effects of entanglement time and

physical grade on blood corticosterone levels was not statistically significant, I feel this

blood variable warrants further comment given the widespread effects that corticosterone

may have on the physiology of sea turtles (Gregory et al., 1996; Jessop et al., 2002;

Jessop et al., 2004; Jessop and Hamann, 2005). Corticosterone is a glucocorticoid that is

released into the blood by the adrenal glands as a response to various stressors. The

release of corticosterone triggers behavioral and physiological adjustments to promote

survival, while curtailing other non-essential processes preferentially partition energy

stores towards survival (Jessop, 2001; Jessop et al., 2002). Continued stress associated

with injuries sustained during entanglement or behavioral alterations may delay clearance

of corticosterone and impact post-release survival, but I was not able to address this

possibility in our study.

I recorded a maximum corticosterone concentration of 51.8 ng·ml-1

for INITIAL

samples from green turtles (Table 2), and levels I observed were as high as or higher than

26

values reported in the literature for stressed turtles (2 – 25 ng·ml-1

) (Gregory et al., 1996;

Jessop et al., 2002; Jessop et al., 2004; Jessop and Hamann, 2005). Previous studies of

induction of the stress response in sea turtles demonstrated that maximum concentrations

of blood corticosterone were reached within 60 – 180 minutes of stress exposure (Jessop,

2001; Jessop et al., 2004; Jessop and Hamann, 2005). In my study, corticosterone

appeared to level off at maximum concentrations within 60 – 120 minutes of capture

(Fig. 1f). This may explain why the ANCOVA model, which covered entanglement

times that ranged from 20 – 240 minutes, failed to detect a significant effect of

entanglement time on blood corticosterone concentrations.

The trend towards increased corticosterone with increased time in net was

accompanied by an increase in blood glucose concentration, a classic signature of

induction of a systemic stress response. Elevated blood glucose has been documented in

previous studies of sea turtles exposed to capture and handling stress (Aguirre et al.,

1995; Hoopes et al., 2000). Blood glucose levels of juvenile green turtles in my study

ranged from 89 – 192 mg·dL-1

( X ± SD = 136.3 ± 34.9 mg·dL-1

), which is consistent with

levels noted by Aguirre et al. (1995) for green turtles exposed to a capture stress protocol

(87 – 195 mg∙dL-1

).

The physiological stress response induced by gillnet entanglement may be

exacerbated by injuries incurred while in the net. The significant increases in plasma

LDH and CPK seen in gillnet-entangled turtles are indicative of muscle or tissue damage,

as these enzymes may leak from ruptured cells into the blood stream (Aguirre et al.,

1995; Killen et al., 2003; Morrissey et al., 2005). Several of the turtles in this study

incurred soft tissue damage from the nets, as documented during the physical

27

examination, and possible cardiac muscle damage due to struggling and overexertion. I

found average LDH in juvenile green turtles of 897.8 U·L-1

, which was approximately 7

times the amount noted by Aguirre et al. (1995) in juvenile green turtles exposed to acute

capture and handling stress for up to 4 hours.

It is important to note that the significant increase in CPK and LDH with

increased entanglement time and decreased physical grade is largely driven by values of

green turtles with physical grade D (N = 2). These turtles had very high plasma CPK and

LDH concentrations. When I removed these two turtles from the analysis, the ANCOVA

model testing the effects of entanglement time and physical grade on LDH concentration

was still statistically significant (P = 0.039), but the model for CPK concentrations was

not significant (P = 0.915).

The high concentrations of phosphorus in the blood that I observed may also

indicate tissue damage, as inorganic phosphates leak out of damaged cells into the

bloodstream (Bishop et al., 2004). Increased blood phosphorus may also indicate

decreased kidney function and filtration. Previous studies on rabbits (Nastuk, 1947) and

rats (Goranson et al., 1948) have shown an increase in blood inorganic phosphate levels

associated with shock, potentially the result of an increase in the rate of high energy

phosphate bond hydrolysis in the face of increased energy demands (McShan et al., 1945;

Nastuk, 1947).

Although my study focused on the effects of entanglement time on health status

of sea turtles, other factors may also contribute to physiological stress during gillnet

entanglement. For example, turtles entangled at the bottom of the gillnet (depths > 0.5

m) or turtles that have net tightly wrapped around their neck or flippers may be prevented

28

from reaching the surface to breathe and experience severe respiratory and metabolic

disruptions after only a short entanglement time. Green turtle Cm 9 was entangled in the

net for only 70 minutes, but at a depth greater than 0.5 m, which made it difficult to reach

the surface. This turtle had a physical grade of C, very high lactate levels

(38.2 mmol·L-1

), and the highest corticosterone levels observed in our study

(51.8 ng·ml-1

). In contrast, green turtle Cm 12 was lightly entangled for 212 minutes at

the top of the net (< 0.5 m). Although this turtle had one of the longest entanglement

times in the study, it had a physical grade of B and low lactate (15.0 mmol·L-1

) and

corticosterone (7.0 ng·ml-1

) levels compared to other turtles entangled for similar

amounts of time. Turtles entangled at the top of the net, or only lightly entangled, may be

able to endure long entanglement times with only mild to moderate disruptions in blood

biochemistry due to relatively unimpeded access to air.

Management Implications

Currently, the North Carolina Division of Marine Fisheries enforces a mandatory

gillnet attendance regulation on gillnet fisheries in the lower Cape Fear River, North

Carolina during the summer months in an effort to minimize sea turtle entanglements and

mortalities. This has essentially closed the fishery during this time, as fishermen are

unlikely to remain with their nets during the typical soak period of 12 hours or more. I

was hopeful that our investigation of the effects of entanglement time on the physiology

of sea turtles would allow us to determine a maximum unattended gillnet soak time that

could be implemented that would minimize the impacts on sea turtles that are captured.

Due to the fact that there are variables other than entanglement time that contribute to the

29

severity of the impact of entanglement, it is very difficult to propose a “safe” soak time

that would reliably minimize detrimental effects of entanglement on captured turtles.

However, the health status of turtles at the time of removal from the net can be easily

assessed using the on-board protocol described in this paper. Physical examinations to

assess behavior, injuries and reflexes provided valuable insight into the physiological

impacts of entanglement on sea turtles. Data obtained through a simple physical

examination may help determine whether to release a turtle or take it to a rehabilitation

facility following a gillnet encounter, thereby minimizing the potential for post-release

mortality.

30

Table 1: Descriptive information for Kemp’s ridley (Lk) (N=4) and green (Cm) (N=14) turtles captured in gillnets in the lower Cape

Fear River, North Carolina from May - October 2007.

Turtle

ID

Capture

Date

Capture

Time

Capture

Location

Salinity

(ppt)

Tw

(ºC)

Tb

(ºC)

SCL

(cm)

SCW

(cm)

Carapace

Area

(cm2)

Entanglement

Time (min)

Physical

Grade

Lk 1 6/6/2007 13:15 33.9505N

77.9457W 32 27.3 27.6 29.9 32.0 751.5 45 A

Lk 2 6/30/2007 08:29 33.9017N

77.0347W 33 28.5 30.5 37.6 34.5 1021.8 107 B

Lk 3 7/3/2007 09:24 33.9116N

77.9980W 34 26.2 22.4 19.9 350.1 30 A

Lk 4 8/31/2007 09:20 33.9238N

77.9589W 38 28.7 29.3 38.1 36.6 1095.2 30 B

X 29.1 32.0 30.8 804.7 53

SD 1.5 7.4 7.5 337.2 36.7

Cm 1 6/7/2007 09:00 33.9315N

77.9723W 33 26.9 27.5 32.2 25.0 632.2 63 C

Cm 2 6/8/2007 10:57 33.9361N

77.9664W 32 28.2 28.3 29.3 22.7 526.5 218 D

Cm 3 6/14/2007 10:30 33.9493N

77.9574W 34 27.0 26.3 28.6 22.7 512.1 132 C

Cm 4 7/4/2007 12:19 33.9422N

77.9483W 33 27.0 27.0 32.2 24.9 632.2 49 C

Cm 5 8/20/2007 13:11 33.9267N

77.9539W 35 32.3 33.0 27.6 23.0 498.6 143 D

Cm 6

9/2/2007 12:58

33.9177N

77.9707W 38 27.0 26.2 19.7 405.4 30 B

Cm 7 9/2/2007 16:13 33.9177N 38 27.0 28.3 35.7 27.4 768.3 30 C

31

77.9707W

Cm 8 9/8/2007 13:11 33.9181N

77.9709W 37 27.8 31.8 28.8 23.2 524.8 30 B

Cm 9 9/12/2007 13:34 33.9212N

77.9682W 37 28.7 26.9 20.0 522.5 70 C

Cm 10 9/19/2007 15:35 33.8942N

77.9591W 38 23.3 26.3 30.6 23.8 572.0 30 B

Cm 11 9/26/2007 14:42 33.9215N

77.9678W 35 28.3 30.2 29.6 23.0 529.3 20 A

Cm 12 10/19/200

7 13:11

33.8900N

77.9632W 39 27.4 27.8 27.0 21.6 458.0 212 B

Cm 13 10/19/200

7 14:57

33.8900N

77.9632W 39 27.4 28.0 32.2 25.7 652.5 88 C

Cm

14

10/19/200

7 18:13

33.8900N

77.9632W 39 27.4 25.0 20.3 400.6 240 C

X 28.6 29.4 23.1 544.6 96.8

SD 2.2 2.9 2.2 100.2 78.4

32

Table 2: INITIAL blood parameters of green and Kemp’s ridley sea turtles captured in the lower Cape Fear River, North Carolina,

May - October 2007.

Green Turtles Kemp’s Ridley Turtles

Mean Normal Blood Values Initial (N=12) Initial (N=4)

Blood Parameter

Range

SD

Range

SD

Green

Turtles

Kemp’s Ridley

Turtles

LDH (U·L-1

) 187 - 6420 897.8 1795.6 1-2045 1164.3 913.0 135a, 109.4

b 1298.7

g

CPK (U·L-1

) 1629 - 31000 7148.3 9007.2 80 - 4734 2412.3 2235.4 425c

AST (U·L-1

) 227 - 702 311.6 129.6 59 - 183 108.8 54.9 178a, 141.0

b 144.7

g

Na+ (mEq·L

-1) 159 - 173 165.1 5.3 158 - 332 202 86.7 172

a, 152.2

b 140.5

e, 153.3

g

K+ (mEq·L

-1) 4.8 - 8.5 6.4 1.2 5.2 - 8.8 6.3 1.7 5.3

a, 5.0

b 6.3

e, 3.6

g

Cl- (mEq·L

-1) 103.0 - 131.0 116.5 7.0 118 - 380 187 128.7 113

a, 109.0

b 112.2

e, 115.2

g

P (mg·dL-1

) 5.3 - 14.5 9.7 2.6 3.8 - 13.2 7.5 4.0 6.7a, 7.9

b 6.8

g

Ca2+

(mg·dL-1

) 8.2 - 15.7 11.2 2.1 8.5 - 28.0 13.5 9.7 9.1a, 8.4

b 7.4

g

Total Protein (g·dL-1

) 2.4 - 5.0 3.8 0.7 1.5 - 3.6 2.6 0.9 5.1a, 4.3

b 3.1

g

Albumin (g·dL-1

) 0.8 - 1.7 1.5 0.3 0.5 - 1.1 0.9 0.3 1.5a, 0.9

b 1.3

g

Globulin (g·dL-1

) 1.6 - 3.3 2.3 0.5 1.0 - 2.5 1.7 0.6 3.6a, 3.0

b 1.8

g

Uric Acid (mg·dL-1

) 0.6 - 4.3 2.2 1.3 0.2 - 2.9 1.3 1.2 1.5a, 0.8

b

Urea Nitrogen (mg·dL-1

) 2 - 28 9.8 9.1 39 - 86 68.3 20.7 7a, 1.0

b 73.7

g

Glucose (mg·dL-1

) 89 - 192 136.3 34.9 60 - 178 112.3 48.8 114a, 86.6

b 115.2

g

Lactate (mmol·L-1

) 13.1 - 50.2 30.6 10.2 16.0 - 19.4 17.5 1.4 0.5c, 1.1

d 0.7

e

CORT (ng·ml-1

) 0.29 - 51.8 20.8 16.5 3.5 - 19.3 7.8 7.7 0.7b 3.1

f

X X

33

a Bolten and Bjorndal 1992,

b Aguirre et al. 1995,

c Butler et al. 1984,

d Berkson 1966,

e Stabenau et al. 1991,

f Gregory and Schmid

2001, g

Carminati et al. 1994

34

Table 3: Results of paired t-test analysis for INITIAL and PRE-RELEASE blood parameters of

green sea turtles captured in the lower Cape Fear River, North Carolina, May - October 2007 (N

= 6 for all parameters except for lactate and CORT, where N = 7). Time between INITIAL and

PRE-RELEASE samples ranged from 45 - 79 minutes.

Blood Parameter Initial Pre-Release df t P

X SD X SD

LDH (U∙L-1

) 534.0 623.2 652.2 783.2 5 -1.53 0.188

CPK (U∙L-1

) 6790.5 6601.7 8306.5 8213.6 5 -1.97 0.105

AST (U∙L-1

) 327.7 185.2 324.3 147.8 5 0.18 0.864

Na+ (mEq∙L

-1) 162.0 2.3 158.8 10.5 5 0.72 0.502

K+ (mEq∙L

-1) 6.3 1.5 5.9 1.4 5 1.02 0.356

Cl- (mEq∙L

-1) 112.8 5.3 110.5 5.0 5 0.73 0.497

P (mg∙dL-1

) 9.1 2.3 8.2 2.4 5 1.68 0.153

Ca2+

(mg∙dL-1

) 11.0 2.7 10.9 3.9 5 0.24 0.819

Total Protein (g∙dL-1

) 3.8 1.0 3.7 0.9 5 0.86 0.428

Albumin (g∙dL-1

) 1.4 0.4 1.4 0.3 5 0.25 0.809

Globulin (g∙dL-1

) 2.4 0.6 2.3 0.6 5 1.07 0.332

Uric Acid (mg∙dL-1

) 2.5 1.6 3.3 2.1 5 -2.68 0.044

Urea Nitrogen (mg∙dL-1

) 8.2 6.6 7.8 5.6 5 0.60 0.576

Glucose (mg∙dL-1

) 134.0 32.1 142.7 36.6 5 -1.93 0.112

Lactate (mmol∙L-1

) 30.8 12.9 32.4 11.6 6 -0.85 0.430

CORT (ng∙ml-1

) 19.9 16.0 24.0 12.5 6 -1.82 0.119

35

a)

Entanglement Time (min)

0 50 100 150 200 250

[Lacta

te] m

mol/L

0

10

20

30

40

50

60

b)


0 50 100 150 200 250

[LD

H]

U/L

0

500

1000

1500

20006250

6500

c)


0 50 100 150 200 250

[CP

K] U

/L

0

5000

10000

15000

2000030000

31000

32000

33000

36

d)


0 50 100 150 200 250

[P]

mg

/dL

0

2

4

6

8

10

12

14

16

e)


0 50 100 150 200 250

[Glu

co

se] m

g/d

L

0

50

100

150

200

250

f)


0 50 100 150 200 250

[CO

RT

] ng

/mL

0

10

20

30

40

50

60

37

Figure 1: a) Blood lactate, b) LDH, c) CPK, d) phosphorus, e) glucose, and f)

corticosterone of juvenile green sea turtles (N = 12) entangled in shallow-set gillnets for

20 to 240 minutes. Physical grade for each individual turtle is indicated by symbols:

physical grade A (●), physical grade B (○), physical grade C (▼), physical grade D (Δ).

CHAPTER 2. MOVEMENTS AND POST-RELEASE MORTALITY OF JUVENILE

SEA TURTLES RELEASED FROM GILLNETS IN THE LOWER CAPE FEAR

RIVER, NORTH CAROLINA

Submitted to Endangered Species Research (3/26/09)

ABSTRACT

The coastal waters of North Carolina, USA serve as an important seasonal

foraging habitat for several species of endangered sea turtles, including the green sea

turtle (Chelonia mydas) and Kemp’s ridley sea turtle (Lepidochelys kempii). Sea turtle

habitat utilization in the Cape Fear River region has not been well-documented compared

with other coastal regions, but increased numbers of sea turtle interactions with fishing

gear in this region suggest that sea turtles may be present in high abundance during the

summer months. An understanding of sea turtle movement patterns is important for

assessing the potential for seasonal overlap with fishing operations and developing

appropriate mitigations strategies for reducing interactions. I used satellite telemetry to

1) monitor movements of juvenile green and Kemp’s ridley sea turtles released from

gillnets in the lower Cape Fear River and 2) assess the potential for using satellite

telemetry to document post-release mortality of sea turtle released from gillnets in an

inshore environment. Tracking durations for the fourteen sea turtles on which I

deployed satellite transmitters ranged from 6 – 45 days. Twelve out of fourteen turtles

released from gillnets stayed in the lower Cape Fear River throughout the tracking

duration, and 50% of locations received via satellite fell within a 33 km2

area that

included the capture site. The region most utilized by turtles consisted of high salinity

waters (35 – 39 ppt) of 1 – 5 meters depth. I observed an abundance of algae, fish and

39

invertebrates that could be food items for greens and Kemp’s ridleys in the high-use

region. I documented one confirmed post-release mortality and three suspected post-

release mortalities during the course of this study.

INTRODUCTION

Sea turtles face many threats to their survival, including loss of nesting and

foraging habitat, egg and hatchling predation, pollution, and other anthropogenic factors

such as boat strikes and encounters with recreational and commercial fishing gear

(Lutcavage et al., 1997). Efforts to protect sea turtles on nesting beaches are well-

established, but in-water threats remain a topic of great concern for sea turtle

conservationists and policy-makers. Bycatch of sea turtles in commercial fishing gear

has been identified as a significant source of mortality contributing to population declines

(Magnuson et al., 1990; Lewison et al., 2004). Knowledge of sea turtle habitat and the

potential for overlap with fisheries, as well as an understanding of the impacts of

incidental entanglement on the behavior and survivability of sea turtles, are high

priorities for management. Mitigation of fisheries interactions with juvenile sea turtles is

of particular importance, as protection of this age class is thought to be critical to

recovery efforts (Crouse et al., 1987; Read et al., 2004).

North Carolina coastal waters serve as an important foraging ground for juvenile

sea turtles in the summer months (Epperly et al., 1995a; Epperly et al., 1995b). The most

common species found in North Carolina are loggerheads (Caretta caretta), greens

(Chelonia mydas) and Kemp’s ridleys (Lepidochelys kempii) (Epperly et al., 1995a).

40

While resident in coastal foraging habitats, sea turtle movements are typically limited to a

home range of approximately 5 km2, which is determined by availability of food sources

and nightly resting sites (Brill et al., 1995; Seminoff et al., 2002; Makowski et al., 2005).

Sea turtles display strong homing behaviors for particular areas and pinpoint specific

daytime foraging and nighttime sleeping sites, which they return to within the same

season and even between years (Lohmann et al., 1997; Avens et al., 2003). Sea turtles

also display predictable diel movement patterns during summer months. Mendonça

(1983) showed that juvenile green turtles at Mosquito Lagoon, Florida routinely shuttle

between shallow foraging grounds during the morning and evening and deeper channels

in mid-afternoon when surface Tw increases. Several studies have shown that green

turtles return to the same resting sites night after night (Mendonça, 1983; Brill et al.,

1995; Seminoff et al., 2002; Southwood et al., 2003).

Entanglement of sea turtles in the gillnet fisheries of coastal North Carolina has

become a critical concern for fisheries managers, as there have been mass stranding

events that coincide with the peak season for this fishery (Federal Register, 2004;

Gearhart, 2001; NCDMF, 2005; Price, 2005). The deep-water gillnet fishery in Pamlico

Sound, NC was shut down in 2002 due to interactions with sea turtles (Federal Register,

2002) and fishing effort is now restricted to shallow waters (< 3 m) in this region, as this

reduces the likelihood that captured turtles will drown in nets. Although the majority of

sea turtles entangled in shallow-set gillnets are released alive (Gearhart, 2001), the

ultimate fate of these turtles is unknown. Severe physiological disruptions and injuries

incurred while entangled in gillnets could result in undocumented post-release mortality

(Lutcavage and Lutz, 1991; Stabenau and Vietti, 2003; Harms et al., 2003).

41

Juvenile green and Kemp’s ridley turtles are also captured in gillnets set in the

lower Cape Fear River, NC (Thorpe and Beresoff, 2005). Due to an increasing number

of sea turtle interactions with gillnet fisheries, North Carolina Division of Marine

Fisheries (NC DMF) has placed restrictions on gillnetting in the lower Cape Fear River.

The NC DMF requires full-time net attendance during the summer fishing season so that

fishermen may immediately remove any turtles that become entangled (Pate, DMF,

2006). This restriction effectively closes the summer gillnet fishery in this region

because fisherman are unwilling to stay with their nets throughout the 12 hours of a

typical set. The implementation of strict fisheries regulations by the NC DMF reflects

the concern that there are significant numbers of sea turtles in the lower Cape Fear River

region during the summer. However, very little is known of the movement patterns of

sea turtles in this area, with most of the available data coming from Marine Patrol

observations, anecdotal reports from fishermen and a previous study by Thorpe and

Beresoff (2005). Information on sea turtle movements and habitat utilization is vital for

developing appropriate bycatch management strategies for the lower Cape Fear River.

I used satellite telemetry to monitor the movements of juvenile green and Kemp’s

ridley sea turtles released from gillnets set in the lower Cape Fear River. My primary

goals were to 1) document sea turtle movements and habitat utilization in this shallow,

inshore environment, and 2) to investigate the potential for using satellite telemetry to

document post-release mortality of sea turtles captured in a coastal gillnet fishery. The

use of satellite telemetry to refine post-release mortality estimates for sea turtles released

from pelagic longline fishing gear has been met with varying degrees of success

(Chaloupka et al., 2004; Swimmer et al., 2006; Sasso and Epperly, 2007). Determining

42

the post-release fate (survival or mortality) of sea turtles using satellite telemetry is

complicated by the fact that cessation of a satellite signal may be attributable to factors

other than mortality, such as tag failure or tag loss due to shedding (Chaloupka et al.,

2004; Hays et al., 2004). I reasoned that use of satellite telemetry to determine post-

release mortality of sea turtles would be more feasible in an inshore environment, as

opposed to open ocean, because I would have the opportunity to locate and retrieve

carcasses that stranded on land to confirm mortalities. To optimize my chances of

locating stranded turtles, I deployed VHF radio beacons along with satellite transmitters.

This study was conducted as part of a larger research initiative to assess the physiological

and behavioral impacts for sea turtles entangled in shallow-set gillnets (Snoddy et al., in

press; Southwood et al., 2008).

METHODS

Field Procedures

Sea turtles were captured in mesh gillnets set at depths of 1-2 m in the lower Cape

Fear River, North Carolina during daylight hours (06:00 – 16:00) from May through

October of 2007 (Fig. 3). Gillnets remained in water for a maximum of 6 hours and were

attended at all times, as per NC DMF regulations (Proclamation M-13-2007), so that I

could document time of capture. A total of 18 sea turtles (14 green turtles and 4 Kemp’s

ridley turtles) were captured during the course of this study. Captured turtles remained in

the net for up to 240 min, and were closely monitored for signs of distress while in the

net. If a turtle remained submerged for greater than 20 minutes or appeared to be in

43

danger of drowning due to airway or swimming restriction, it was immediately removed

from the net. Turtles that were tracked post-release (N = 14) were entangled for 20 – 218

minutes ( X ± SD = 85.5 ± 67.7 minutes). Environmental variables (water temperature

(TW), air temperature (TA), salinity) were recorded at the capture site, and GPS locations

for capture sites were documented. I also identified algae and invertebrates found in the

capture area that could be potential food sources for juvenile greens and Kemp's ridleys.

Upon removal from nets, turtles were brought on board our boat and restrained in

a 16 cm × 43 cm padded plastic bin. Turtles were shaded from direct sunlight and

periodically sprayed with seawater. I used calipers to measure the straight carapace

length notch to notch (SCLnn) and straight carapace width (SCW), and marked turtles for

future identification by inserting passive induced transponder (PIT) tags above the left

front flipper. I used a two-part fast-setting marine epoxy (PowerFast, Powers Fasteners,

Inc., New Rochelle, NY) to attach satellite transmitters (SPOT 5, Wildlife Computers,

Redmond, WA, USA) (7.9 cm length x 4.9 cm width x 1.8 cm height, 90 g) and VHF

radio beacons (SI-2F, Holohil Systems, Inc., Carp, Ontario, Canada) (3.5 cm length x 1.0

cm dia, 11 g) to 14 of the 18 turtles I captured (Fig. 2). The other four turtles were too

small for transmitter deployment based on my size criteria. I did not deploy transmitters

on turtles for which the total mass of transmitter and epoxy was greater than 5% of the

turtle’s mass in air, as calculated from a length-weight power regression (NOAA

Beaufort Laboratory, unpublished data). Estimated masses of turtles captured ranged

from 1-10 kg (6.3 ± 2.4 kg). Prior to transmitter attachment, the vertebral scutes of the

carapace were cleared of barnacles, cleaned with acetone to remove biofouling, lightly

sanded with sand paper, and given a final acetone rinse. Epoxy was used to secure the

44

VHF radio beacon to the third or fourth vertebral scute with the antenna facing toward

the head of the turtle and laying flat on the carapace surface. The satellite transmitter was

secured with epoxy to the first and second vertebral scutes of the carapace. The epoxy

base for the transmitter was molded such that drag effects would be reduced. While

epoxy was setting, I examined turtles for net-inflicted external injuries, tested reflex

responses, and took a blood sample to assess the physiological impacts of entanglement

(Snoddy et al., in press). Turtles were on board the boat for an average of 58 minutes

(range 10 min-110 min) and were then released within 10 meters of the capture site. All

procedures used for this study were approved by University of North Carolina

Institutional Animal Care and Use Committee (protocol #2006-12) and The NOAA

Fisheries Office of Protected Resources (permit # 1572).

Analysis of Location Data

The satellite transmitters were programmed for a 24 hour duty cycle and

transmitted location data to Service Argos network satellites when turtles surfaced to

breathe. Transmitter positions were assigned to one of six location classes (LC 3, 2, 1, 0,

A and B) by Service Argos based on the number of transmissions received, the number of

satellites receiving transmissions, and the angle and speed of satellites relative to the

transmitter at the time of transmissions. For location classes 3, 2, 1, and 0, the location

accuracies are less than 150 m, 350 m, 1000 m, and greater than 1000 m, respectively.

For location classes A and B, no location accuracy is assigned. The percentage of

transmissions of each location class for all turtles combined was calculated (Fig. 4).

45

Location data were downloaded and analyzed using the Satellite Tracking and

Analysis Tool (STAT) program available at www.seaturtle.org (Coyne and Godley,

2005). Ideally, only high quality location class data (LC 3, 2, and 1) would be used in the

tracking analysis, however the majority of positions I received were of low quality

location class (LC A and B). I included all location data in our initial analysis and

applied a multi-step filtering procedure to exclude implausible locations. Based on

diagnostic data provided by Service Argos, I excluded any location that had a satellite

pass time of less than 240 seconds. The remaining locations were then plotted

sequentially on a map, and filtered based on speed and distance thresholds established in

previous studies of sea turtle movement patterns in coastal environments (Read et al.,

2004). Locations that were separated by distances that could not be covered at a swim

speed of less than 5 km/hour were excluded from analysis, as were locations that would

have required turtles to pass implausibly over land barriers. Because transmissions from

land may indicate a stranding event, particularly high quality location class transmissions

along the shoreline, all land-based transmissions were carefully analyzed. If low quality

land-based transmissions were interspersed over time with transmissions from water,

these points were excluded from analysis. Filtered data were mapped in ArcGIS (version

9.2) and Hawth's Tools extension was used to create 25 and 50% volume contours of

filtered location data for all turtles combined.

Assessment of Mortality

Satellite transmissions received during the 30 days following release from gillnet

were analyzed for patterns indicative of mortality based on 1) documented behavioral

http://www.seaturtle.org/

46

patterns of green and Kemp’s ridley turtles in nearshore environments, 2) behaviors

associated with compromised health, and 3) knowledge of the process of decay and

onshore stranding of sea turtle carcasses. I predicted that a mortality event would be

reflected by satellite transmission patterns that deviated from previously documented

patterns and were consistent with the process of decay and putrefaction (criteria described

below). The 30 day monitoring period was chosen because turtles are exposed to

numerous threats in their marine environment, and the more time that passes the more

difficult it becomes to attribute mortality to the gillnet interaction. I reasoned that

physiological and behavioral consequences of gillnet entanglement and vulnerability to

other threats would be greatest in the first few weeks following entanglement.

Previous satellite telemetry studies of sea turtles in coastal environments have

demonstrated that short surfacing intervals (< 1 min) and low profile surfacing patterns

typically result in receipt of low quality location class data (LC A or B) (Godley et al.,

2003; Read et al., 2008). Sea turtles that are injured, fatigued, or have experienced large

disruptions in blood biochemistry due to enforced submergence may require extensive

amounts of time at the surface to recover (Lutz and Bentley, 1985; Stabenau and Vietti,

2003), which would be reflected by receipt of high quality locations (LC 3, 2, 1). I

interpreted prolonged periods of numerous, high quality location class transmissions that

occurred in the hours to days immediately following release as representative of a surface

recovery period. I compared the percentage of high quality location class transmissions

(LC 3, 2, 1) received during the first 24 hours following release to the percentage of high

quality location transmissions received in the subsequent 72 hours for each turtle using an

ANOVA and Tukey’s test. Significance was set at P < 0.05.

47

I predicted that mortality events would be reflected by alterations in the quality

and quantity of location data transmitted via satellite. Specifically, I predicted that

satellite transmissions would cease for several days following a mortality event as the

carcass sank below the surface, but that frequent, high quality location class

transmissions (LC 3, 2, 1) would resume for a brief period when putrefaction and build-

up of gases caused the carcass to temporarily float back to the surface (Epperly et al.,

1996; Committee on Sea Turtle Conservation, National Research Council, 1990).

Increases in the quality and frequency of satellite transmissions along the shoreline were

interpreted as a possible shore stranding event. In such cases, a VHF radio receiver (TR-

5, Telonics, 932 E. Impala Avenue Mesa, AZ, 85204 USA) and directional H antenna

(RA-2AK, Telonics, 932 E. Impala Avenue Mesa, AZ, 85204) were used to search for

the VHF radio beacon signal so that I could locate the carcass and verify mortality.

Turtles that did not display transmission patterns indicative of a mortality event

within 30 days of release were considered survivors. Turtles that displayed satellite

transmission patterns indicative of mortality but for which I did not locate a carcass were

categorized as suspected mortalities. Turtles that displayed satellite transmission patterns

indicative of mortality and for which I located a carcass were categorized as confirmed

mortalities. Carcasses that were located were examined for indications of boat strike,

predation, and gut impaction. I compared the percentage of high quality locations (LC 3,

2, 1) for the entire track duration of suspected mortalities and confirmed mortalities (N =

4) to those of survivors (N = 10) using a student’s t-test.

48

RESULTS

Movements and Habitat Utilization

Sea turtles were tracked for 17.0 ± 8.9 ( X ± SD) days following release from

gillnets (range 6 - 42 days). Filtered location data indicate that the majority of sea turtles

remained in the lower Cape Fear River for the tracking duration. A small percentage (16

%) of low quality locations that passed the filter criteria placed turtles in the ocean

around the river mouth or off the eastern shore of the barrier island complex of

southeastern North Carolina. Approximately 95% of filtered high quality location data

(LC 3, 2, 1) for all but two turtles (Cm 3 and Cm 13) were limited to within

approximately 2 - 3 km radius of the turtle’s capture site. Fifty percent of all filtered

locations were encompassed by a 33 km2 area and 25% of all locations were

encompassed by a 12 km2 area, which included 10 of the 14 capture sites (Fig. 3). The

50% volume contour was bordered on the north by 33.966 N, -77.947 W, on the south by

33.888 N, -77.978 W, on the east by 33.939 N, -77.934 W, and on the west by 33.922 N,

-77.999 W.

Two turtles, Cm 3 and Cm 13, migrated out of the Cape Fear River following

release from gillnets. Turtle Cm 3, captured on 06/14/07, remained in the lower Cape

Fear River for three days following release and then exited the river and moved north

along the North Carolina coastline for 10 days. The last transmission from turtle Cm 3

was received on 06/27/07 from the lower White Oak River near Swansboro, North

Carolina (Fig. 5). Turtle Cm 13, captured on 10/19/07, exited the Cape Fear region 20

days after release and traveled south along the coasts of North Carolina and South

49

Carolina for 22 days before transmissions ceased (Fig. 6). The last transmission was

received from east of the mouth of St. Helena Sound, South Carolina on 11/24/07.

Post-Release Mortality

Juvenile green and Kemp’s ridley turtles released from gillnets were classified as

confirmed mortalities, suspected mortalities, or survivors based on patterns observed in

satellite transmissions (Fig. 19a – 19n, and Table 4). The one turtle for which I directly

documented mortality by recovering the carcass (Kemp’s ridley Lk 2, captured 06/30/07)

displayed a pattern of satellite transmissions that met my criteria for mortality. Between

06/30/07 and 07/04/07 I received 14 transmissions from this turtle. Following a LC B

transmission on 07/04/07, there was a period of several days during which no signals

were received. Transmissions resumed at 23:09 on 07/06/07, and all further

transmissions were of high location class quality (Fig. 7, Fig. 19a). The rising tide likely

stranded the carcass in the marsh, with high tide at 01:18 on 07/07/07. The carcass was

located within 1 km of gillnet capture site on 07/07/07 by a wildlife enforcement officer

during a mid-morning patrol of Oak Island. When the carcass was discovered, the tide

was low but rising. The officer transported the satellite tag approximately 2 km to

Southport, NC and contacted me that afternoon. I was receiving transmissions

throughout this transport period and had initiated my search for the carcass. Investigation

of the carcass yielded no evidence of boat strike, predation, or gut impaction, and this

turtle was classified as a confirmed mortality.

Three other turtles, one Kemp’s ridley (Lk 4) and two green turtles (Cm 2 and Cm

3), displayed transmission patterns indicative of a mortality event. Carcasses were not

50

located for these turtles, so they were classified as suspected mortalities. Turtle Lk 4 was

released after a 30 minute gillnet entanglement on 08/31/07. Several high quality

location class data points were received from this turtle in the initial 2 days post-release, a

pattern suggestive of a lengthy surface recovery period (Fig. 19b). Signals received over

the course of the next several days revealed that the turtle moved 24 km up river from the

capture site (Fig. 8). Turtle Lk 4 was the only turtle that ventured this far north into the

river. High quality location signals were reported on the low to rising tide in the river

north of Snow’s Cut on 09/06/07, with more high quality signals received the following

day (09/07/07). I checked repeatedly for the VHF radio beacon for this turtle over the

course of these two days, but did not detect any signals. Satellite transmissions for this

turtle ceased on 09/09/07, with the last location reported on the river side of Snow’s Cut.

I did not locate this turtle’s carcass, but the up-river movements and increase in high

quality transmissions towards the end of the tracking period led me to believe that a

mortality may have occurred.

Turtle Cm 2 was released after a 218 minute gillnet entanglement on 06/08/07.

Prior to release, this turtle had demonstrated weakened reflex responses and low activity

levels on-board the boat. Upon release from the boat, the turtle sank slowly beneath the

water surface with no active flipper strokes. High winds and choppy seas prevented me

from visually relocating and recapturing this turtle, however I picked up her VHF radio

beacon within minutes of release. I received numerous high quality location class data

points from this turtle during the 8 hours following release, which indicates that she was

at the surface for an extended period of time. I continued to receive daily low quality

transmissions from this turtle until 06/19/07. After this date, I received high quality

51

location class data intermittently for the next several months. Transmissions received on

06/30/07 (LC 3), 08/09/07 (LC 2), 08/18/07 (LC 3), and 10/26/07 (LC 1) were clustered

along a partially submerged rock wall within 500 m distance of the site where I had

captured the turtle. Although this area was checked frequently, I was unable to detect the

VHF radio signal for this turtle or locate a carcass or shed transmitter. Intermittent

transmissions likely reflect the exposure of the transmitter, either detached or still

attached to a carcass, at low tide. The poor condition of this turtle, behavior of turtle at

release, and pattern of satellite transmissions led me to categorize this turtle as a

suspected mortality.

Transmission patterns for turtle Cm 3 also led me to believe that this turtle had

died post-release. Transmissions from this turtle ceased after a period of approximately 9

days (06/14/07 – 06/22/07) spent traveling northwards along the coast of North Carolina

from her capture site in the lower Cape Fear to just off the coast of Emerald Isle close to

Bogue Inlet. Transmissions resumed 4 days later on 06/26/07, and several high quality

location class transmissions were received from within the lower White Oak River

adjacent to Swansboro, NC. The pattern of signal disappearance and reappearance close

to the shoreline several days later suggests that this turtle died and stranded temporarily

along the shoreline due to tidal flow (Fig. 19d). I received the strongest signals on the

rising tide, which may indicate that the carcass was washed ashore temporarily. I was

unable to recover a carcass before transmissions permanently ceased.

The remaining ten turtles on which I deployed satellite and VHF radio

transmitters did not display transmission patterns indicative of a mortality event as

defined by my criteria, and were thus classified as “survivors” (Fig. 19e-n). Satellite

52

transmissions received from survivors were predominantly of low quality location class,

sometimes with intermittent high quality signals received throughout the monitoring

period (Figs. 6a, 6b, 10 – 18). There was a significantly larger percentage of high quality

transmissions for the entire tracking period for the confirmed and suspected mortalities

(N = 4) compared to the survivors (N = 10) (P = 0.017). For several turtles classified as

survivors (Cm 1, Cm 4, Cm 7, Cm 8), the 24 hour period immediately following release

was characterized by receipt of several high quality location class transmissions. This

pattern suggests that turtles were spending extended periods of time at the surface,

potentially recovering from physiological disturbances incurred while entangled in

gillnets (Snoddy et al., in press). The results from the ANOVA for all tagged turtles (N =

14) indicate that there was a significantly higher percentage of high quality transmissions

(LC 1, 2, 3) within the first 24 hours following release compared with the subsequent 72

hours (P = 0.014).

DISCUSSION

One goal of this study was to investigate the potential for using satellite telemetry

to document post-release mortality of sea turtles released from gillnets. Previous studies

have attempted to use satellite telemetry to determine post-release mortality of sea turtles

released from longline pelagic fishing gear. Swimmer et al. (2006) were only able to

document one clear example of post-release mortality for 15 longline-captured turtles

based on dive data. Sasso and Epperly (2007) inferred 3 mortalities out of 39 longline-

captured turtles based on dive data, with several turtles of unknown fate due to problems

53

of tag retention, which I discuss later. For pelagic studies, confirmation of mortality is

hindered by the difficulties of recovering a carcass in the open ocean. In this study, I was

able to recover the carcass of the one confirmed mortality, Lk 2, which permitted me to

verify the satellite transmission patterns indicative of mortality in a nearshore

environment. The pattern observed for Lk 2 in the 5 days following release (Fig. 19a)

reflects the sinking of the animal upon death (cessation of signals), subsequent re-

surfacing as gases accumulate in the animal due to putrefaction (reappearance of signals)

and, in this case, an onshore stranding event with the rising tide. The carcass of Lk 2 was

recovered with the satellite transmitter still attached to the carapace within 8-10 hours of

stranding.

Turtles that were suspected mortalities were classified as such because their

satellite transmission patterns were similar to those of the confirmed mortality, with gaps

in transmissions and/or intermittent, repetitive, high quality transmissions from shoreline

locations. Tides play an important role in the ability to recover a carcass, and movement

of carcasses on and off of the shoreline with the rising and falling tides may have

impeded my ability to locate suspected mortalities. I cannot entirely discount the

possibility that transmitters for the three suspected mortalities were shed early and

washed ashore, given that I did not recover carcasses of these animals. There were,

however, distinct differences in transmission patterns for suspected mortalities and

survivors with short duration tracks, namely that transmissions from survivors were of

consistently low quality location class and ceased abruptly.

I documented one confirmed mortality and classified three turtles as suspected

mortalities in this study. Based on these data, I estimate that that post-release mortality

54

of sea turtles released from shallow-set gillnets lies somewhere between 7.1 and 28.6%.

It is important to acknowledge that these figures are for soak times of 4 hours or less, and

nets are typically left to soak overnight in the coastal North Carolina gillnet fishery.

Blood samples taken from green sea turtles entangled in gillnets show significant positive

relationships between entanglement time and blood biochemical parameters indicative of

restraint stress and hypoxia (i.e., lactate and glucose) (Snoddy et al., in press). Given the

impact of entanglement time on physiological status of green sea turtles, longer

entanglement times would be expected to result in an increase in recovery time and,

potentially, post-release mortality rates.

My assessment of mortality for turtles released from gillnets was hampered by

short track durations. I had planned to monitor satellite transmissions for signs of

mortality for 30 days following release from gillnets, but the maximum track duration

was 42 days and 12 track durations were 23 days or less. For turtles classified as

survivors, the satellite transmissions up until the time when transmissions ceased did not

show a pattern indicative of mortality as defined by my criteria. Therefore, I concluded

that the short track durations were due to premature shedding of the transmitters rather

than mortality.

Previous satellite telemetry studies conducted with juvenile green turtles in

inshore waters of North Carolina have documented difficulties with transmitter retention

(Read et al., 2008). Signals received from transmitters deployed on juvenile green turtles

in Core and Pamlico Sounds, NC during the summer were typically of low quality

location class (LC A and LC B) and track durations ranged from 17 – 154 days, with an

average track duration of 67.7 days (Read et al., 2008). Rapid growth rates of juvenile

55

green turtles that utilize coastal waters of North Carolina as a seasonal foraging habitat

during the warm summer months may contribute to short transmitter retention times

(Shaver, 1994). The epoxy bond with the carapacial scutes may become weakened as the

scutes increase in diameter. Average transmitter retention time in my study was only

17.1 days, even shorter than retention times documented for juvenile green turtles in Core

and Pamlico Sounds. This may be due to differences in habitat. Green turtles typically

utilize seagrass habitats with minimal rough substrate in Core and Pamlico Sounds,

whereas 10 of the turtles in my study were captured along a partially submerged rock

wall where they may have been foraging on algae or invertebrates. Abrasion against the

rocky substrate at this foraging site may have contributed to pre-mature shedding of

transmitters. Transmitters deployed on green turtles in Core and Pamlico Sounds (Read

et al., 2008) and in the lower Cape Fear River were retained for a longer duration when

deployed late in the season (October – November), just prior to fall migration. In my

study, turtles Cm 12 and Cm 13 were tagged in mid-October and their track durations (25

and 42 days, respectively) were approximately 2 times longer than the average track

duration for all turtles.

The majority of location data obtained from sea turtles behaving normally in

inshore areas are typically of low quality, due to surfacing behavior in this habitat

(Godley et al., 2003; McClellan, pers. comm.). Turtles that are physiologically stressed

from enforced submergence or intense struggling may spend more time recovering at the

surface (Lutz and Bentley, 1985; Stabenau and Vietti, 2003), which would result in more

frequent and high quality satellite transmissions. I documented a significantly higher

percentage of high quality transmissions in the first 24 hours post-release compared with

56

the subsequent 72 hours, which supports the idea that turtles released from gillnets

require extended surface recovery periods immediately following release. This behavior

may render turtles more susceptible to shark predation or boat strike.

Through the course of this study I gained insight into habitat utilization of

juvenile sea turtles in the lower Cape Fear River. This area is dominated by marshes,

small coves and bays, sand islands, and tidal creeks. The dominate marsh grasses are

Spartina sp., Juncus roemerianus, and Salicornia sp., and the bottom substrate is a mud

and sand mix. During the period when my study was conducted (May and October 2007)

there was low rainfall and I recorded high salinities (32 - 39 ppt), consistently clear

water, and Tw of 23.3 °C to 32.3 °C. As previously mentioned, 10 of 18 turtles were

captured along a partially submerged, human engineered rock wall that divides two

northern bays from the river to the west (Fig. 3). I identified various types of algae

growing on the rock wall and in the bays that could serve as potential food sources for

green turtles, including Enteromorpha, Gracilaria, Halymenia, Codium, Ulva and

Sargassum species. Several types of algae present in the lower Cape Fear River have

been observed in stomach contents of green turtles (Bjorndal, 1997). I also observed

many different invertebrates living along the rock wall which could serve as a food

source for juvenile Kemp’s ridley turtles, including blue mussels (Mytilus edulis), mud

snails (Ilyassoma obsoleta), blue crabs (Callinectes sp.), stone crabs (Menippe

mercenaria), spider crabs (Libinia sp.) and lady crabs (Ovalipes ocellatus). Stomach

contents of Kemp's ridley turtles stranded in Texas consisted of 93.6% crabs, 3.2%

shrimp, 2.2% molluscs, 0.4% fish, and 0.3% vegetation (Shaver, 1991). Analysis of fecal

content of Kemp's ridley turtles in the coastal waters of New York revealed that this

57

species preyed upon spider crabs (Libinia emarginatus), rock crabs (Cancer irroratus),

lady crabs (Ovalipes ocellatus), blue mussels (Mytilus edulis), and various algae (Fucus

sp., S. natans, Ulva, Z. marina) (Burke et al., 1993; Burke et al., 1994).

Home ranges for sea turtles in nearshore habitats include both foraging sites and

shelter sites where turtles rest during nocturnal hours. Their movements are typically

limited to a 5 km2 area (Brill et al., 1995; Seminoff et al., 2002; Makowski et al., 2005).

In areas where food resources are patchily distributed, home ranges for green turtles tend

to be larger than in areas where food resources are concentrated and abundant (Seminoff

et al., 2002; Makowski et al., 2006). Home range for juvenile Kemp’s ridley turtles (5 –

30 km2) tends to be slightly larger than that observed for green turtles (Schmid et al.,

2003). Previous studies to assess home range of sea turtles in nearshore habitats used

radio and sonic telemeters with transmission ranges of 1 - 3 km. Satellite transmitters

provide a less accurate estimate of location, but permit remote monitoring of sea turtle

movements over a larger area. Godley et al. (2003) documented nearshore resident

movements of green turtles on the coast of Brazil in July, and their data showed that

resident movements were within a few square kilometers, despite low quality location

data. Location data from the turtles that remained in the lower Cape Fear River after

release from gillnets were of low quality location class, which likely resulted in an

overestimation of range. Ninety-five percent of high quality locations that I received

placed turtles within a 12- 28 km2 area of their capture sites, which is within reason when

compared to previous estimates of inshore sea turtle movements. The "hot spots" that

were described by 25 - 50% of all location data encompassed areas of 12 - 33 km2,

respectively, which included the capture sites of 11 of the turtles in this study (Fig. 3).

58

The data I obtained support the growing body of evidence that the Cape Fear

River is an important seasonal foraging ground for juvenile green and Kemp's ridley

turtles. My results also provide evidence that gillnet entanglement results in a prolonged

surface recovery for sea turtles, and entanglement times of 4 hours or less result in post-

release mortality rates of 7.1 – 28.6%. Currently, seasonal gillnet attendance regulations

in the lower Cape Fear River greatly restrict fishing activities during the summer months

when sea turtles are present in large numbers (Pate, NCDMF, 2006). Results from my

study suggest that these management decisions are justified and should continue to be

enforced.

59

Table 4: Track duration and percentage of high quality locations (LC 3, LC 2, LC 1) for

entire track duration for all turtles captured.

Turtle ID

Track

Duration

(days)

% High

Quality

Locations

Confirmed mortality

Lk 2 8 44.4

Suspected mortality

Lk 4 10 30.5

Cm 2 23 57.1

Cm 3 16 34.0

Survivor

Lk 1 13 0

Cm 1 17 36.1

Cm 4 15 22.2

Cm 5 15 0

Cm 7 12 28.0

Cm 8 20 43.9

Cm 10 6 7.0

Cm 11 16 14.3

Cm 12 25 10.2

Cm 13 42 14.9

X ± SD 17.0 ± 8.9

60

Figure 2: Satellite and VHF radio tags deployed on turtle Lk 1 prior to release in lower

Cape Fear River.

61

Figure 3: Squares are capture locations of all turtles captured (N = 18). Circles are

filtered location data for all turtles that remained in Cape Fear River for track duration.

Inner two circles represent 25% contours and outer circle represents 50% contour for all

turtles that remained in the Cape Fear River for the track duration.

62

Location Class

LC3 LC2 LC1 LC0 LCA LCB LCZ

Pe

rce

nt

of

To

tal T

ran

sm

issio

ns

0

10

20

30

40

50

60

Figure 4: Proportions of location classes of the total transmissions received for all turtles

(N = 14) tagged in the lower Cape Fear River, North Carolina.

63

Figure 5: Filtered location data for turtle Cm 3, suspected mortality. Stars are LC 3

locations, triangles are LC 2 locations, squares are LC 1 locations and circles are LC A

and LC B locations.

64

a)

65

b)

Figure 6: a) All filtered location data for turtle Cm 13, b) expanded view of the lower

Cape Fear region filtered location data for turtle Cm 13. Triangles are LC 2 locations,

squares are LC 1 locations and circles are LC A and LC B locations.

66

Figure 7: Filtered location data for turtle Lk 2, confirmed mortality. Stars are LC 3


and LC B locations.

67

Figure 8: Filtered location data for turtle Lk 4, suspected mortality. Stars are LC 3


and LC B locations.

68

Figure 9: Filtered location data for turtle Cm 2, suspected mortality. Stars are LC 3


and LC B locations.

69

Figure 10: Filtered location data for turtle Cm 1, survivor. Stars are LC 3 locations,

triangles are LC 2 locations, squares are LC 1 locations and circles are LC A and LC B

locations.

70



locations.

71



locations.

72



locations.

73



locations.

74



locations.

75



locations.

76



locations.

77

Figure 18: Filtered location data for turtle Lk 1, survivor. Stars are LC 3 locations,


locations.

78

a)

Hours

0-2

4

24-4

8

48-7

2

72-9

6

96-1

20

120-1

44

144-1

68

168-1

92

Num

ber

of T

ransm

issio

ns

0

2

4

6

8

10

LC 3

LC 2

LC 1

LC A

LC B

Turtle Lk 2, confirmed mortality

b)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

16

18LC 3

LC 2

LC 1

LC A

LC B

Turtle Lk 4, suspected mortality

79

c)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

40

8-4

32

43

2-4

56

45

6-4

80

48

0-5

04

50

4-5

28

52

8-5

52

Nu

mb

er

of

Tra

nsm

issio

ns

0

1

2

3

4

5

6

LC 3

LC 2

LC 1

LC A

LC B

Turtle Cm 2, suspected mortality

d)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

16

18

LC 3

LC 2

LC 1

LC A

LC B

Turtle Cm 3, suspected mortality

80

e)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

Nu

mb

er

of

Tra

nsm

issio

ns

0

1

2

3

4

5

6

7

LC 3

LC 2

LC 1

LC A

LC B

Turtle Cm 5, survivor

f)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

16

LC 3

LC 2

LC 1

LC A

LC B


81

g)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

Nu

mb

er

of

Tra

nsm

issio

ns

0

1

2

3

4

5

6

LC 3

LC 2

LC 1

LC A

LC B


h)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8 LC 3

LC 2

LC 1

LC A

LC B


82

i)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

40

8-4

32

43

2-4

56

45

6-4

80

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

16

LC 3

LC 2

LC 1

LC A

LC B


j)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10LC 3

LC 2

LC 1

LC A

LC B


83

k)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

Nu

mb

er

of

Tra

nsm

issio

ns

0

1

2

3

4

5

6

7

LC 3

LC 2

LC 1

LC A

LC B


l)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

40

8-4

32

43

2-4

56

45

6-4

80

48

0-5

04

50

4-5

28

52

8-5

52

55

2-5

76

57

6-6

00

Nu

mb

er

of

Tra

nsm

issio

ns

0

1

2

3

4

5

6

7

LC 3

LC 2

LC 1

LC A

LC B


84

m)

Hours

0-2

42

4-4

84

8-7

27

2-9

69

6-1

20

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

31

2-3

36

33

6-3

60

36

0-3

84

38

4-4

08

40

8-4

32

43

2-4

56

45

6-4

80

48

0-5

04

50

4-5

28

52

8-5

52

55

2-5

76

57

6-6

00

60

0-6

24

62

4-6

48

64

8-6

72

67

2-6

96

69

6-7

20

72

0-7

44

74

4-7

68

76

8-7

92

79

2-8

16

81

6-8

40

84

0-8

64

86

4-8

88

88

8-9

12

91

2-9

36

93

6-9

60

96

0-9

84

98

4-1

00

8

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

LC 3

LC 2

LC 1

LC A

LC B


n)

Hours

0-2

4

24

-48

48

-72

72

-96

96

-12

0

12

0-1

44

14

4-1

68

16

8-1

92

19

2-2

16

21

6-2

40

24

0-2

64

26

4-2

88

28

8-3

12

Nu

mb

er

of

Tra

nsm

issio

ns

0

2

4

6

8

10

12

14

LC 3

LC 2

LC 1

LC A

LC B

Turtle Lk 1, survivor

85

Figure 19: Number of transmissions received for each 24 hour period tracked post-

release for a) turtle Lk 2, b) turtle Lk4, c) turtle Cm 2, d) turtle Cm 3, e) turtle Cm 5, f)

turtle Cm 1, g) turtle Cm 4, h) turtle Cm 7, i) turtle Cm 8, j) turtle Cm 10, k) turtle Cm

11, l) turtle Cm 12, m) turtle Cm 13, and n) turtle Lk 1.

CONCLUSIONS

Results from this study contribute to the growing body of evidence that suggests

the lower Cape Fear River, NC is an important seasonal foraging habitat for juvenile

green and Kemp’s ridley sea turtles. Proper management of gillnet fisheries in this area

will be essential for reducing incidental bycatch and mortalities of sea turtles in the

future. As observed in other studies of nearshore habitat utilization by sea turtles,

juvenile sea turtles resident in the lower Cape Fear during the summer use a relatively

small area for foraging and resting. Ninety-five percent of the high quality locations I

received (locations with smaller error estimates) were within a 2-3 km radius of where

they were captured. The large number of low quality location classes (no error estimates)

received likely resulted in an overestimation of the area utilized by turtles, however my

estimates of sea turtle movements were within reason when compared with previous

studies. I identified “hot spots”, especially along the rock wall, where turtles were found

and captured reliably, although I did not recapture any turtles in this study. If turtles

restrict themselves to a relatively small area, the potential exists for recapturing the same

turtle multiple times in fishing gear. Multiple entanglements may compound the degree

of physiological disruption experienced by a turtle and therefore increase a turtle’s

susceptibility to disease, infection, predation or boat strike.

I found that physiological disruptions, often quite severe, occur in turtles that

were forcibly submerged in gillnets for 20 – 240 minutes. There was a trend towards

increased physiological disruption (lactate, glucose, LDH, CPK, phosphorus) with

increased entanglement time, however many other factors may influence the degree of

87

disruption, such as the way in which turtles are entangled and the depth at which they are

entangled. I observed high variability in the behavioral responses to entanglement,

particularly the degree to which turtles struggled and, consequently, the degree of

entanglement severity and ability of the turtle to reach the surface to breathe. I developed

a grading system based on a simple physical examination of reflex responses, activity

level and injuries that could be performed by fisherman in the field to assess whether the

turtle is suitable for release or whether it should be taken to the Sea Turtle Hospital.

Physical grades were good indicators of degree of physiological disruption in blood

biochemistry.

I estimate that post-release mortality of sea turtles released from gillnets lies

between 7.1 and 28.6%. Though I was only able to recover one carcass to confirm

mortality, satellite transmission patterns of three other turtles were similar to the satellite

transmission pattern for the confirmed mortality. Surprisingly, turtles that were classified

as confirmed and suspected mortalities did not necessarily have the largest disruptions in

blood biochemistry, and there were no significant differences in lactate (t4.17 = -0.56, P =

0.519), corticosterone (t4.1 = -0.51, P = 0.636), glucose (t4.22 = 0.26, P = 0.808), LDH (t9.6

= 0.57, P = 0.582) and CPK (t6.39 = 0.25, P = 0.808) between turtles that survived and

those that I suspect died. Additionally, there was no correlation between biochemical

indicators of hypoxia (lactate [r = 0.3, P = 0.372]) or a systemic stress response

(corticosterone [r = 0.3, P = 0.433] and glucose [r = 0.4, P = 0.232]) and satellite track

duration. This observation lends support to the assertion that in most cases the short track

durations were caused by premature tag shedding rather than mortality. All four turtles

classified as confirmed or suspected mortalities had net wrapped tightly around the head

88

and/or neck while entangled in the net. Based on my data, there is reason to believe that

entanglement around the head, and particularly the soft tissues of the neck, may cause

internal injuries to respiratory pathways which could impede recovery and cause delayed

mortality.

There was a high degree of variability in both physiological and behavioral

responses of sea turtles to gillnet entanglement. At the onset of this study, I had hoped to

determine a “safe” soak time for gillnets that would help prevent or avoid in-net and post-

release mortality of sea turtles. Unfortunately, many factors in addition to the time spent

in net influence the condition of the turtle upon removal and confound attempts to avoid

mortality by simply limiting soak time. In this study, turtles that were in the net for as

little as 30 minutes could become so deeply or severely entangled in the net that they had

to be removed early in the soak duration due to the risk of drowning. The longest

entanglement time that I observed in this study was 4 hours, which is conservative

considering most gillnets are soaked for 12 – 15 hours. Given the severe physiological

disruptions I observed in turtles entangled for 4 hours or less, it is very likely that turtles

entangled in nets for 12 – 15 hours would experience more severe physiological

disruptions and higher levels of in-net and post-release mortality. For these reasons, the

current summer closure of the lower Cape Fear River gillnet fishery should continue to be

enforced.

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