Conservation Genetics 6: 133–139, 2005.
DOI 10.1007/s10592-004-7737-6
Ó Springer 2005
Estimated contribution of Atlantic Coastal loggerhead turtle nesting
populations to offshore feeding aggregations Mark A. Roberts1, Christopher J. Anderson1, Bruce Stender2, Al Segars3, J. David
Whittaker2, James M. Grady4 & Joseph M. Quattro1,*
1
Department of Biological Sciences, Marine Science Program, University of South Carolina, Columbia, SC,
USA; 2South Carolina Department of Natural Resources, Marine Resources Division, Charleston, SC, USA;
3
South Carolina Department of Natural Resources, Beaufort, SC, USA; 4Department of Biological Sciences,
University of New Orleans, New Orleans, LA, USA (*Corresponding author: phone: 803-777-3240; e-mail:
[email protected]) Sequences reported in this manuscript have been deposited in GenBank (accession
numbers AY680687–AY680691).
Received 1 July 2004; accepted 1 November 2004
Key words: loggerhead turtles, aquatic conservation, endangered species, mitochondrial DNA, mixed stock
analyses
Abstract
Seasonal feeding grounds for loggerhead sea turtles present relatively unchecked anthropogenic hazards.
Commercial fisheries, recreational boating and environmental contamination indirectly threaten subadult
feeding areas. The potential effects of these types of threats are difficult to establish without an understanding of the relationship between the feeding areas and individual nesting areas. We perform a mixed
stock analysis on seasonal subadult feeding grounds from North Carolina to northern Florida. A total of
216 individuals were captured using either commercial shrimping vessels or vessels with standardized sea
turtle trawls. A fragment of the mitochondrial control region was sequenced from each of the individuals
and compared with haplotypes at nesting beaches identified previously. Twelve haplotypes were resolved
among individuals captured. Mixed stock analysis indicates that the nearby NEFL-NC nesting populations
disproportionately contribute to the feeding aggregate and thus perturbations to this feeding ground would
weigh most heavily on this nesting area.
Introduction
Effective conservation strategies for critically
endangered species should consider all life history
stages and threats specific to each. For example,
nesting beach habitat is a critical resource for sea
turtles that has declined in quantity and quality
(Eckert 1995; Nishiguchi et al. 1997; Venizelos &
Smith 1997; Rumbold et al. 2001). However, a
concerted effort to protect nesting habitat has
ameliorated the threat and, in some regions, contributed to increased nesting density (Hughes
1969, 1974; Richardson et al. 1978; Mortimer
1985; Owens et al. 1994; Limpus 1995; Hillis-Starr
& Phillips 2000). With improving quality of nesting habitat, conservation efforts might then focus
on other critical life history stages; e.g. protecting
subadult loggerhead turtles is an effective conservation management strategy (Crouse et al. 1987;
Crowder et al. 1994; Heppell et al. 1996).
Logically, a heightened potential for subadult
maturation provides for increased likelihoods of
long-term reproduction and, potentially, species
persistence. However, anthropogenic activities
such as commercial fisheries, recreational boating
and environmental contamination indirectly target
134
subadult feeding habitats, threaten feeding
assemblages and the future reproductive generations they represent. For example, the overwhelming majority of sea turtles captured in
commercial shrimp trawls in South Carolina and
Georgia are subadults (Hillestead et al. 1995;
Laurent et al. 1996). Subadult loggerhead sea
turtles here, as in the rest of the western Atlantic
Ocean, typically have moved from their juvenile
pelagic oceanic habitats to a variety of near shore
demersal habitats once they reach approximately
50 cm curved carapace length (Carr 1986), placing
them in greater proximity to anthropogenic influences.
Since female sea turtles are strongly philopatric, the composition of subadult aggregations is an
important consideration for conservation management (Meylan et al. 1990; Bowen et al. 1992,
1993, 1994). For example, if subadult feeding
aggregations comprise individuals ‘‘related’’ via
natal origin, then activities that undermine
‘‘segregated’’ feeding aggregations threaten the
long-term viability of specific nesting beaches,
more so than if feeding assemblages comprise
individuals from several beaches. If feeding
aggregations are in fact ‘‘segregated’’, then nesting
beaches supporting relatively small nesting
populations, such as those in South Carolina
(Hopkins-Murphy & Murphy 1994), are affected
disproportionately. Interestingly, loggerhead nests
in South Carolina have declined steadily from an
average of 5412 nests per season in the early 1980s
to 2876 nests in the early 2000s, approximately 3%
per year (Hopkins-Murphy SR, South Carolina
Department of Natural Resources, Wildlife and
Freshwater Fisheries Division, personal communication 2004Þ. Thus, in this instance, determining
the contribution of individual nesting beaches to
offshore feeding assemblages helps define the risk
to future reproductive communities and refine
conservation strategies.
Here we use mtDNA haplotype data to evaluate
the composition of loggerhead feeding aggregations and the management implications this genetic
makeup has for nesting populations; particularly
low-density nesting rookeries such as those found
in South Carolina. Since female sea turtles are
strongly philopatric, maternally-inherited mtDNA
haplotypes are similarly partitioned among nesting
beaches, in some instances on a site-specific basis
(Meylan et al. 1990; Bowen et al. 1992, 1993, 1994).
The ability to differentiate individuals originating
from genetically distinct nesting areas provides the
basis for statistical estimates of an individual
nesting area’s contribution to offshore feeding
aggregations using Mixed Stock Analyses (Grant
et al. 1980). Fortunately, Encalada et al. (1998)
surveyed mtDNA variation of 249 individuals
representing the major Atlantic and Mediterranean
Ocean loggerhead nesting populations, recovering
six areas with significantly different haplotype
frequencies: Northeast Florida to North Carolina,
USA (NEFL-NC), southern Florida, USA (SFL),
Northwest Florida, USA (NWFL), Quintana Roo,
Mexico (MEX), Bahia, Brazil (BRA) and Kiparissia Bay, Greece (GRE). We use these baseline
genetic data to estimate the relative contribution of
each area to subadult feeding aggregations in
coastal areas from North Carolina to northern
Florida.
Materials and methods
Blood samples were obtained from loggerhead
turtles taken during a South Carolina Department
of Natural Resources and University of Georgia
Marine Extension Service survey of 851 offshore
stations between Winyah Bay, South Carolina and
St Augustine, FL, USA. The sampled foraging
grounds included bottom types ranging from sand
to hard-bottom with moderate relief (gear prevents
sampling in higher relief areas) within the shallow
nearshore areas. Three vessels were double-rigged
with standardized sea turtle trawls (18.3 m headrope with 20.3 cm stretch mesh) developed by the
Corps of Engineers and National Marine Fisheries
Service. Trawls were conducted at randomly
selected stations and at 4.6–12.2 m depth with
sampling locations of the vessels divided into
northern, central and southern zones. Two commercial shrimping vessels were used to take additional samples, one operating in the Brunswick,
GA, area and a second in the Charleston, SC area.
Under permit from the National Marine Fisheries
Service, each commercial vessel conducted normal
shrimping operations for 14 consecutive days,
except nets were not equipped with Turtle
Excluder Devices (TED). For the commercial
vessels, sampling was from normal shrimping
routes, not at pre-determined stations. Loggerhead
turtles taken during trawling were tagged with
135
Inconel tags placed in the proximal posteroaxial
margin of both anterior flippers and one internal
passive integrated transponder (PIT). Straight-line
carapace length and width, head width, curved
shell carapace length and width, and body weight
were recorded for each individual. No tagged
turtles were recaptured during the study.
Whole blood (approximately 500 ll) was
drawn from each individual, added to 9 ml of lysis
buffer (100 mM Tris-HCL, 100 mM EDTA,
10 mM Nacl, 1.0% SDS; pH 8.0), and placed on
ice. Total DNA was prepared from blood tissue
samples using GeneReleaser following the manufacturer’s (Bioventures) protocol. The mitochondrial DNA (mtDNA) control region was amplified
via the Polymerase Chain Reaction (PCR) using
primers CR-1 and CR-2 and amplification conditions described in Norman et al. (1994). Amplifications were performed in 50 ll reactions [10 mM
Tris-HCl (pH 8.3), 50 mM KCl, 2.5 mM MgCl2;
0.1% Tween 20; 5% DMSO; 200 mM each dNTP,
10 pmol each primer and one unit of Taq DNA
polymerase] in an MJ Thermal Cycler 6400 (MJ
Research, Inc.). Amplification products were
purified by PEG precipitation and washed with
80% cold ethanol. A 1 ll aliquot of purified
amplification product was used as template in a
Big Dye terminator cycle sequencing reaction
(Applied Biosystems). All samples were sequenced
in the forward direction using CR-1; some
samples were also sequenced in the reverse direction with CR-2 to confirm haplotype designations.
Sequencing reaction products were separated on
an ABI 377 automated sequencer for 7 hrs at 28W
constant power.
Sequences were compiled in Sequencher
3.1.1 (Gene Code Corp.) and then exported into
BioEdit (Hall 1999) and aligned manually.
Aligned sequences were filtered with MacClade
(Maddison & Maddison 1992) to remove redundancies and identify unique haplotypes. Individual haplotypes were compared to loggerhead
turtle sequences in the GenBank database to
assign identity consistent with data in Encalada et
al. (1998). Haplotypes were then used in mixed
stock analyses to estimate the contribution of the
six genetically distinct nesting areas described by
Encalada et al. (1998) to the feeding aggregation
using the conjugate gradient (CG) algorithm of
the computer program SPAM (Alaska Department of Fish and Game 2003a). Bootstrap
resampling (N = 5000) was used to estimate errors associated with each estimated contribution.
The program SPAM estimates the contribution of
each potential donor or baseline population (six
genetically distinct nesting areas for loggerhead
turtles) to a mixed stock of individuals (offshore
feeding aggregations). Underestimation of baseline contributions occurs when mixed stocks include unique haplotypes, i.e. haplotypes not
recorded in baseline populations. SPAM addresses this problem by estimating haplotype
frequencies for alleles not found in baseline populations by a variation of the Smouse et al. (1990)
expectation-maximization algorithm (Alaska
Deparment of Fish and Game 2003b).
To test that all boats were sampling turtles
within the same general life history stage, size class
variation among turtles sampled was assessed
using a one-way ANOVA on straight-line carapace length by boat.
Results
Partial [376 base pairs (bp)] mitochondrial control
region sequences were obtained from 216 loggerhead turtles. Twelve haplotypes were recovered
(Table 1), seven of which correspond to previously
published sequences (haplotypes A, B, C, G,
H, I and J in Encalada et al. 1998). We retain
the published haplotype designations for these
seven. Five previously unreported haplotypes were
recovered and given designations on the basis of
homology to published sequences followed by a
unique number determined by order of observation; haplotypes A2 and A3 were most similar to
the published A haplotype, while B2, B3 and B4
were most similar to haplotype B (see Table 1).
Two of 12 haplotypes (A, B) were present at a
combined frequency of 88%, identical to that observed among the six genetically distinct nesting
areas described by Encalada et al. (1998). Haplotype C, found previously in six nesting individuals
(two each in NWFL, SFL and MEX) was recovered from seven individuals. Haplotypes G, H, I
and J, found in a combined total of eight individuals, were also found in very low frequency in
the nesting areas. Conversely, three haplotypes
recorded in the nesting beach survey, two of which
136
Table 1. Mitochondrial DNA control region haplotypes observed in this study and from nesting beaches described in Encalada et al.
(1998). Dots indicate identity to the reference sequence (haplotype A; GenBank accession number AJ001074) and dashes indicate
insertion/deletion events
Haplo-
Nesting beach
Position
In-water
aggregation
type
NEFL-NC
SFL
NWFL
34
22
14
MEX
BRA
GRE
111122222233333333333333
223445789155802335800011124445555
580466197245133792757804807890126
A
TGTTTAGAAACGGCCGCA-AATAACC------A
A2
......A....A...A..-.......------.
117
A3
......A..G.A...A..-.......------.
B
CACC-G..G.TA.TTATGG.GCG..TTGCAAG.
B2
CACC-GA.G.TA.TTATGG.GCG..TTGCAAG.
1
B3
.ACC-G..G.TA.TTATGG.GCG..TTGCAAG.
1
B4
CACC-G..G.TA.TTATGG.GCG.ATTGCAAG.
C
CACC-G..G.TAATTATGG.GCG..TTGCAAG.
D
...........A...A..-.......------.
E
CACC-G..G.TA.TTATGG.GCG..TTGCAAG-
F
CACC-G..G.TA.TTATGG.GCG-.TTGCAAG.
G
CACC-G..G.TA.TTATGGGGCG..TTGCAAG.
H
CACC-G..G..A.TTATGG.GCG..TTGCAAG.
1
1
I
CAC.-G.GG.TA.TTATGG.GCG..TTGCAAG.
1
2
J
CACC-G..G.TA.TTATGG.GCG..TTGCAGG.
7
1
4
24
1
11
19
74
1
2
2
2
7
11
1
2
2
1
4
1
5
Contribution
0.19
0.47
0.18
0.05
0.00
0.06
SE
0.15
0.20
0.17
0.04
0.00
0.09
For clarity, only variable sites are shown; numbered positions are relative to haplotype A. Contributions for each nesting beach to the offshore
aggregation were estimated from a mixed stock analysis using SPAM (Alaska Department of Fish and Game 2003). See Materials and Methods
for site abbreviations.
were rare (E, F) and one fixed in Brazil (D), were
not recovered in this study.
Florida populations (NWFL and SFL) had a
disproportionate estimated contribution to the
feeding aggregation (65.2%); estimated contribution of the nesting area north of St Augustine,
FL (NEFL-NC) was 19.1% (Table 1). All other
source populations were estimated to be infrequent
contributors. These estimates were robust to the
exclusion of haplotypes not present in the potential source populations.
Turtle straight-line carapace lengths were not
significantly different among individuals and
across samples (p < 0.01; overall mean = 64.8).
Sizes ranged from 49.2 to 97.6 cm; however, only
18 individuals were larger than 80 cm, suggesting
that individuals from different vessels were within
the same general size class.
Discussion
Conservation efforts for critically endangered
species, including sea turtles, should be based on
comprehensive life history information. Reducing
threats to one life-history stage, e.g. reproduction,
can have little effect on species conservation if
subsequent phases are unprotected. Despite being
familiar symbols of the current biodiversity crisis,
much of sea turtle life history is poorly understood, including the relationship between natal
origin and offshore distribution during the maturation phase. Previous molecular genetic studies
on loggerhead turtle populations indicate a minimum of three genetically distinct nesting areas
along the Atlantic coast of the USA (Encalada et
al. 1998), but, unfortunately, the offshore distribution of individuals from these subpopulations
137
Figure 1. Map of collection sites for both this study and the
previous nesting beach survey (Encalada et al. 1998). Closed
circles indicate approximate locations of nesting beach samples
included here as ‘‘SFL’’, open circles represent samples included
in the ‘‘NEFL-NC’’ area and stippled circles represent the
‘‘NWFL’’ nesting beaches. The darkened coastline from St
Augustine, FL to Winyah Bay, SC indicates the area of sampling for the in-water aggregate.
has not been examined extensively. However,
restriction fragment analyses of mtDNA indicated
that juveniles foraging in both Chesapeake Bay
and Charleston Harbor were preferentially derived
from the Georgia and Carolina nesting assemblages (Sears et al. 1995; Norrgard & Graves
1996). Also, mtDNA control region sequences
indicate that western Atlantic nesting areas contribute substantially to juveniles inhabiting the
Mediterranean Sea; however, the larger subadults
in this region were derived only from Mediterranean nesting areas (Laurent et al. 1998).
Available data point to segregation by genetically distinct nesting areas among feeding aggregations in the Atlantic. Epifaunal characteristics
and heavy metal accumulations in subadult and
adult loggerhead turtles suggest some segregation
among offshore aggregations according to natal
origin, specifically between the NEFL-NC and
NWFL/SFL nesting areas (Stoneburner et al.
1980; Caine 1986). Similarly, Meylan et al. (1983)
indicated that loggerheads from Florida nesting
beaches feed preferentially in the Caribbean or
Gulf of Mexico, while loggerheads from the
NEFL-NC nesting beaches have foraging areas
from mid-Florida to New Jersey (HopkinsMurphy SR, South Carolina Department of
Natural Resources, Wildlife and Freshwater
Fisheries Division, pers. comm. 2004). Therefore,
subadult turtles in the NEFL-NC foraging area
should disproportionately represent nearby nesting beaches, a hypothesis that has important
implications for the management of loggerhead
turtles. Impacts on the NEFL-NC offshore
aggregation would negatively threaten future
reproductive output of NEFL-NC beaches and
thus the persistence of this genetically distinct
nesting area.
The majority of offshore turtles in the NEFLNC feeding area were derived from the Florida
nesting assemblage (65.2%). However, a significant proportion of offshore individuals (19.1%)
were from the geographically proximate NEFLNC nesting area. This NEFL-NC contribution is
significant for several reasons. The NEFL-NC
nesting area contains only 9% of the loggerhead
nesting activity along the Atlantic Coast (NMFS/
USFWS 1991), but mixed stock analysis assigned
greater than 19% of the feeding aggregation to this
area. This observation is consistent with mixing of
individuals from various nesting assemblages in
offshore areas and concentration of subadults
from NEFL-NC beaches in offshore feeding areas
– the NEFL-NC nesting area is contributing disproportionately to nearby offshore feeding aggregations. Therefore, mortality to subadults in the
NEFL-NC feeding grounds will have a disproportionate effect on reproductive viability of the
NEFL-NC nesting area. Although the estimated
frequency of NEFL-NC individuals in the offshore
aggregation was low (19%), this proportion might
represent the majority of the reproductive output
of the NEFL-NC nesting area.
The offshore distribution of loggerhead turtle
haplotypes in the NEFL-NC area has profound
conservation implications. Subadult turtles hatched from this area appear to annually return to
nearby offshore feeding areas during the warm
weather seasons. Thus, subadult mortality in
the offshore assemblage could significantly compromise the reproductive viability of the NEFLNC populations. Furthermore, turtle mortalities
occurring on these feeding areas could compromise other populations as well. The majority
(65%) of the turtles represented Florida nesting
populations and small percentages (5% each)
138
represented infrequent, but potentially important,
contributions from Mexico and the Mediterranean. Also, 5% of the turtles possess haplotypes
not encountered in any of the nesting populations.
These haplotypes might represent another
unidentified, but genetically identifiable, nesting
population for which this is a critical feeding area.
The robustness of a MSA is improved by
comprehensive surveys of genetically distinct
source populations (Xu et al. 1994). While the six
regions surveyed by Encalada et al. (1998) represent the overwhelming majority of nesting in the
Atlantic and Mediterranean, and thus are the most
appropriate source populations in a MSA, characterization of smaller populations along the
western coast of Africa and elsewhere in the
Mediterranean is needed (see Encalada et al. 1998
for a discussion of the nature of their sampling).
However, a MSA is most powerful when potential
source populations can be uniquely differentiated,
a variable that we cannot control, and does not
apply to the source populations used here. Fortunately, Xu et al. (1994) showed that increased
sampling of potential source populations is more
informative than increased sampling of mixed
populations. Therefore, increasing the baseline
sample sizes is a means to describe more precisely
the mixed populations. Similarly, temporal variation in both the source and the mixed populations
warrants investigation, since, on average, loggerhead sea turtles nest every other year (Richardson
and Richardson 1982).
While large standard errors associated with the
present study necessitate cautious interpretation of
the data, it is clear that subadult sea turtles, such
as sampled for this study, represent what should
now be a primary focus of conservation efforts. No
amount of protection afforded to nesting beaches
can be successful without an adequate supply of
sexually mature individuals to continually supply
nests. Protection of subadult loggerheads while on
these warm-season feeding grounds is important to
the recovery of the small and declining nesting
populations in NEFL-NC as well as other areas.
Acknowledgements
We thank Sally Murphy, Brian W. Bowen,
William B. Driggers, Patricia Kearney, Kenneth M.
Oswald, Lisa M. Wickliffe, Peter Smouse and one
anonymous reviewer for valuable information and
suggestions that improved earlier drafts of the
manuscript. We thank the crews of the Lady Lisa,
Miss Hilda, Miss Tina and the University of
Georgia Marine Extension Service/Georgia Bulldog. Funding for this project was provided in part
by grants from the Cooperative Institute for Fisheries Molecular Biology [FISHTEC; NOAA/
NMFS (RT/F-1)] and SC SeaGrant (R/MT-5) to
JMQ.
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