C O N T R I B U T E D P A P E R
Loggerhead marine turtles (Caretta caretta) nesting at
smaller sizes than expected in the Gulf of Mexico:
Implications for turtle behavior, population dynamics,
and conservation
Allison M. Benscoter1
| Brian J. Smith2
| Kristen M. Hart1
1Wetland and Aquatic Research Center,
U.S. Geological Survey, Fort Lauderdale,
Florida, USA
2Department of Wildland Resources and
Ecology Center, Utah State University,
Logan, Utah, USA
Correspondence
Allison M. Benscoter, Wetland and
Aquatic Research Center, U.S. Geological
Survey, 3321 College Avenue, Fort
Lauderdale, FL 33314, USA.
Email: abenscoter@usgs.gov
Funding information
Deepwater Horizon Oil Spill Natural
Resource Damage Assessment; USGS
Ecosystems Mission Area; USGS Priority
Ecosystem Science Program
Abstract
Estimates of parameters that affect population dynamics, including the size at
which individuals reproduce, are crucial for efforts aimed at understanding
how imperiled species may recover from the numerous threats they face. In
this study, we observed loggerhead marine turtles (Caretta caretta) nesting at
three sites in the Gulf of Mexico at sizes assumed nonreproductive in this
region (≤87 cm curved carapace length-notch [CCL-n]). These smaller individ-
uals ranged from 74.0 to 86.9 cm CCL-n, and the proportion of smaller nesting
loggerheads was 0.13 across three study sites: Gulf Shores, AL; Dry Tortugas
National Park, Florida (FL); and Everglades National Park (ENP), FL. The
greatest proportion of smaller nesters was observed at ENP at 0.24. Tracking
data indicated that the smaller nesters migrated shorter distances and swam in
shallower waters compared to the larger nesting loggerheads (>87 cm CCL-n)
in our dataset. These results provide valuable information on two of the
smallest subpopulations of NW Atlantic loggerheads and understudied ENP
turtles. Our results have potential applications in the classification and inter-
pretation of stranding limits and bycatch estimates, population modeling
(e.g., stage durations and fecundity), and understanding threats and subpopu-
lation recovery efforts for multiple subpopulations of this imperiled species.
KEYWOR D S
Bayesian hierarchical behavior-switching state-space model, Caretta caretta, curved
carapace length, Gulf of Mexico, foraging, loggerhead, marine sea turtles, migration, size
at reproduction
1
|
INTRODUCTION
Understanding the demography of imperiled species is cru-
cial to countering the threats they face and supporting their
recovery. Population (or subpopulation) models rely on
accurate estimates of demographic parameters that affect
population persistence (Heppell, 1998; Heppell, Crowder,
Crouse, Epperly, & Frazer, 2003; Piacenza, Balazs,
Received: 7 May 2021
Revised: 19 October 2021
Accepted: 23 October 2021
DOI: 10.1111/csp2.581
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2021 The Authors. Conservation Science and Practice published by Wiley Periodicals LLC on behalf of Society for Conservation Biology. This article has been contributed
to by US Government employees and their work is in the public domain in the USA.
Conservation Science and Practice. 2021;e581.
wileyonlinelibrary.com/journal/csp2
1 of 14
Hargrove, Richards, & Heppell, 2016), including age at
maturity, duration of life stages, and reproductive output
(Caswell, 2006; Crouse, Crowder, & Caswell, 1987). How-
ever, demographic parameters for small subpopulations
may differ from estimates from larger subpopulations
(Hatch, Haas, Richards, & Rose,
2019; Richards
et al., 2011), and substantial variation in reproductive traits
can exist among subpopulations of the same species (van
Buskirk & Crowder, 1994). Furthermore, animals can
exhibit plasticity in both size at maturity and fecundity
(Gotthard & Nylin, 1995; Kuparinen & Merila, 2007),
which can affect demographic rates and the ability of a spe-
cies to recover from declines (Piacenza et al., 2016). Elastic-
ity analysis, which evaluates the relative input of each vital
rate (age-specific survival and fecundity) to the annual pop-
ulation (or subpopulation) growth rate, also indicates that
subpopulations of the same species can have varying elas-
ticity patterns (Heppell, 1998). For marine sea turtles, the
focus of our study, evidence exists for variation in elasticity
patterns (Heppell, 1998) and reproductive traits (van
Buskirk & Crowder, 1994) within a single species. This
calls for the need to understand subpopulation-specific
demography to assess the growth, recovery, and success of
imperiled (and often small) subpopulations of marine tur-
tles, which also face numerous threats.
Loggerhead marine turtles (Caretta caretta) in the North-
west Atlantic Ocean are part of a distinct population seg-
ment (DPS) listed as federally threatened under the
U.S. Endangered Species Act (ESA, 1973, as amended). In
total, there are nine DPSs that all together represent logger-
head marine turtles globally; they are differentiated based
on ecology, distributions, genetics, and movements and
allow for the unique assessment of risks, endangered status,
and recovery objectives and criteria for each DPS (Conant
et al., 2009). The Northwest Atlantic Ocean DPS is com-
prised of five recovery units (or subpopulations) outlined in
the Recovery Plan that vary in size: the Northern, Peninsu-
lar Florida (FL), Dry Tortugas (DRTO), Northern Gulf of
Mexico, and Greater Caribbean Recovery Units (RU).
Nesting trends for Northwest Atlantic loggerhead, which
affect overall species persistence, indicate either a declining
trend, no trend, or unknown trend (NMFS-USFWS, 2008;
TEWG, 2009; Witherington, Kubilis, Brost, & Meylan, 2009).
For example, data show declining loggerhead nesting trends
in the Northern Gulf of Mexico (1995–2007; NMFS-
USFWS, 2008),
Peninsular FL
(1989–2008; NMFS-
USFWS,
2008),
and DRTO
(2001–2009;
Richards
et al., 2011). And, more recent data through 2018 indicate a
lack of significant nesting trend for the Northern Gulf of
Mexico and Peninsular FL, with insufficient data for DRTO
(Bolten et al., 2019). The presence of either a negative trend
or no trend in nesting numbers indicates that these RUs are
not meeting Recovery Objectives and Demographic
Recovery Criteria in the Northwest Atlantic Ocean logger-
head Recovery Plan (Bolten et al., 2019). Globally, the log-
gerhead sea turtle is classified as vulnerable, is decreasing in
numbers,
and populations are
severely
fragmented
(Casale & Tucker, 2017), and recommendations exist for
regional assessments of extinction risk for marine turtle spe-
cies (Seminoff & Shanker, 2008; Wallace et al., 2010), includ-
ing for that of the loggerhead marine turtle.
Loggerhead marine turtles in the Northwest Atlantic
Ocean face numerous threats. In-water threats include
anthropogenic activities such as fisheries bycatch (Bolten
et al., 2019; Hart et al., 2018a; Hays, Broderick, Godley,
Luschi, & Nichols, 2003; Iverson, Benscoter, Fujisaki,
Lamont, & Hart, 2020), ship strikes (Casale et al., 2010),
energy development (e.g., oil spills; Henkel, Suryan, &
Lagerquist, 2014; Vander Zanden et al., 2016; Bolten
et al., 2019), and plastics (Bolten et al., 2019). Other threats
are harmful algal blooms (HABs; Hart et al., 2018a; Bolten
et al., 2019) and climate change (Bolten et al., 2019),
including sea level rise (Conant et al., 2009). There are also
numerous threats to nesting habitat, such as anthropogenic
development, beach traffic (pedestrian and vehicular),
lighting on beaches, erosion control structures that inhibit
nesting movements, beach erosion, beach pollution, and
sand extraction (Conant et al., 2009; NMFS-USFWS, 2008).
Threats to the loggerhead marine turtles can vary based on
life
stage
and
in
their
impact
on population
(or subpopulation) growth rates (Bolten et al., 2011).
Evaluating proposed management actions to respond
to these threats requires accurate estimation of vital rates,
including size at sexual maturity. Understanding the size at
which females achieve sexual maturity can affect stage
durations in population models (Heppell, 1998; Piacenza
et al., 2016), bycatch estimates (Gulf Coast Ecosystem Res-
toration Council, 2013), and incidental stranding limits
(ISLs; Hart, Mooreside, & Crowder, 2006). Comprehending
the size at sexual maturity may also affect how Recovery
Objectives, Demographic Recovery Criteria, and Recovery
Actions defined in the Recovery Plan for the Northwest
Atlantic Ocean DPS of loggerhead marine turtles are
achieved (NMFS-USFWS, 2008).
In this study, we observed nesting loggerhead marine
turtles that were below the standard size that is considered
as reproductive in this region (curved carapace length-
notch [CCL-n] ≤87 cm). The size classification for repro-
ductively mature females is reported as >87 cm CCL-n in
various studies and in the Recovery Plan for the Northwest
Atlantic Ocean DPS of loggerhead marine turtles (adults
defined as >87 cm CCL-n in Witherington, 1986; Bjorndal,
Bolten, & Martins, 2000; Bjorndal et al., 2001; NMFS, 2001;
NMFS-USFWS, 2008). Because this size threshold of 87 cm
CCL-n is used in various research and management appli-
cations, we quantified the proportion of nesting loggerhead
2 of 14
BENSCOTER ET AL.
females that were ≤87 cm CCL-n at three sites in the Gulf
of Mexico from 2011 to 2019. Because the smaller size of
these nesting females may also have implications for sub-
population demography (e.g., fecundity), space-use behav-
ior, and potential exposure to threats (e.g.,
fisheries
bycatch, boat strikes), we also compared inter-nesting,
migration, and foraging characteristics between these
smaller reproductive females and those that are >87 cm
CCL-n, using satellite tracking. Our goals were to (1) quan-
tify the frequency at which these smaller reproductive tur-
tles nest (ratio of smaller nesters to total nesters) across
multiple recovery units of the Northwest Atlantic Ocean
loggerhead marine turtle DPS, and (2) to assess potential
differences in space-use behavior between the smaller
female reproductive loggerheads and their larger counter-
parts, given size differences in the two groups.
2
| METHODS
2.1
| Study sites and data collection
In the Gulf of Mexico, we sampled, tagged, took size mea-
surements, and satellite-tracked nesting
loggerhead
females from 2011 to 2019 at three sites that represent
different segments of Northwest Atlantic loggerhead
marine turtle population (Caretta caretta): Gulf Shores,
Alabama (AL; 30.228
N, 87.852
W), Dry Tortugas
National Park (DRTO; 24.629
N, 82.873
W), and Ever-
glades National Park (ENP; 25.142
N, 81.109
W) follow-
ing established protocols (Hart, Guzy, & Smith, 2021;
Hart, Lamont, Sartain, & Fujisaki, 2014; Hart, Lamont,
Sartain, Fujisaki, & Stephens, 2013; NMFS-SEFSC, 2008).
These nesting subpopulations each comprise an individ-
ual Recovery Unit (RU, as mentioned earlier) for the
Northwest Atlantic loggerhead marine turtle population
(3 of 5 total recovery units). The DRTO RU is the smallest
(330 females, includes Cay Sal Bank, Bahamas), the AL
subpopulation is a part of the second smallest RU, the
Northern Gulf of Mexico RU (430 females), and the
ENP subpopulation is purported to be a part of the Penin-
sular FL RU (NMFS-USFWS, 2008; Richards et al., 2011).
Sampling was conducted during the nesting season each
year at different times and durations depending on the
site: AL was sampled once per year for a duration of
18 days per sampling occasion, DRTO was sampled three
times per year for a duration of 1 week per sampling
occasion, and ENP was sampled once per year for a dura-
tion of 1 week per occasion. Across all years in the study
period, from 2011 to 2019, AL was sampled from 2011 to
2017, DRTO was sampled from 2011 to 2019, and ENP
was sampled from 2014 to 2019.
We categorized nesting females as smaller if CCL-n
was ≤87 cm, as measured from the midline anterior point
(nuchal scute) to the midline posterior notch. The 87 cm
division between subadults and adults represents a conser-
vative division applied in numerous other studies (Bjorndal
et al., 2000, 2001; NMFS, 2001; Witherington, 1986). The
use of CCL-n is recommended for assessing CCL, because
there is greater variability in CCL-tip because of deviation
of the measuring tape from the midline (Bjorndal &
Bolten, 1989; Bolten, 1999) and turtle carapace injuries
from factors such as ship strikes.
2.2
| Proportion of smaller-sized nesters
We determined the proportion of these smaller nesting
loggerheads at each study site, and the mean CCL-n of
reproductive female
loggerheads that were ≤87 cm
CCL-n and >87 cm CCL-n, across all sites (n = 352 total
turtles). To quantify if the proportion of smaller logger-
head nesters varied by site and year, we fit generalized
linear models (GLMs) with a binomial distribution, and
applied model selection using AICc in the MuMIn
package (Barton, 2020) and determined R2 in the perfor-
mance package (Lüdecke, Makowski, Waggoner, & Patil,
2020)
in
the program R (version 4.0.3; R Core
Team, 2020). We fit a null model, a model with year as
covariate, a model with site as a covariate, and a model
with both year and site as covariates. Lastly, we also
determined the size threshold defining female reproduc-
tive loggerheads at which 10, 5, 2.5, and 1% of our
observed nesters would be classified as smaller-sized.
2.3
| Satellite tracking and switching
state-space modeling
We fitted platform terminal transmitters (PTTs; SPOT5,
SPOT6, or SPLASH10; Wildlife Computers, Redmond, WA)
to loggerhead females after they nested (n = 110 turtles),
according to established protocols (NMFS-SEFSC, 2008)
and methods outlined in Hart et al. (2014, 2018b, 2021);
methods were approved by Institutional Animal Care and
Use Committee Protocol (see Acknowledgments for more
details). All tagged turtles were released within 2 hr at their
capture location. Satellite location data were downloaded
via Satellite Tracking and Analysis Tool (STAT; Coyne &
Godley, 2005; accessible via SEATURTLE.ORG Inc. [www.
seaturtle.org] prior to July 2014, and via the Wildlife Com-
puters Portal
[www.wildlifecomputers.com] after July
2014). The satellite-based Argos system was used to collect
the satellite location data, and location data were assigned
BENSCOTER ET AL.
3 of 14
accuracy estimates (CLS, 2015) using Kalman filtering
(CLS, 2015; Kalman, 1960). Satellite
locations were
excluded if they were classified into location class (LC) Z,
indicating no location error estimate was available. We
summarized the data until the transmitters stopped deliver-
ing information or until
the time of data analyses:
September 17, 2020.
We estimated the location and behavioral mode for
each turtle by fitting a Bayesian hierarchical behavior-
switching state-space model (hDCRWS model; hierarchical
first difference correlated random walk switching model)
to the marine turtle satellite data using the R package bsam
(Jonsen, 2016; Jonsen, Bestley, Wotherspoon, Sumner, &
Flemming, 2017; Jonsen, Mills Flemming, & Myers, 2005)
using a time step of 24 hr (1 point per day). This type of
switching state-space model (SSM) estimates movement
parameters jointly across all individuals to improve behav-
ioral state estimation, and accounts for location error.
Behavioral modes based on SSM output were defined as
either “area-restricted searching” or “transiting” (Jonsen
et al., 2013; Jonsen, Myers, & James, 2007), the former rep-
resented by locations with comparatively shorter step
lengths and greater turning angles (tortuous tracks) and
the latter represented by comparatively longer step lengths
and smaller turning angles (less turning, straighter move-
ment). The models were fit by the R package bsam by call-
ing JAGS (R package rjags; Plummer, 2019) to run the
Markov chain Monte Carlo (MCMC) algorithm. We ran
two independent parallel chains of MCMC, used adap-
tive sampling for the first 3500 iterations, and discarded
3500 additional samples as the burn-in. We then drew
10,000 samples from the posterior distribution, and
thinned by 5 to reduce within-chain autocorrelation,
resulting in 2,000 posterior samples for inference. To
avoid fitting the SSM to satellite tracks with temporal
gaps, where long temporal gaps lead to less informed
SSM trajectories, we defined a threshold gap size of
20 days for each turtle, above which the gap period was
removed and trajectory was split and re-estimated. Multi-
ple trajectories (separated by a temporal gap in satellite
data) for the same turtle were re-combined after SSM
(see previous application of this method in Hart, Lam-
ont, Iverson, & Smith, 2020). The minimum number of
locations in a split trajectory was set to 50, and split tra-
jectories with fewer than 50 locations were omitted. In
addition to running the SSM with a 24 hr time step, we
also ran the SSM using both a time step of 12 and 8 hr
and spatially compared the outputs. We opted for the
timestep of 24 hr to reduce autocorrelation in the
modeled locations (in one case we supplemented an SSM
migration point from the 8 hr time step output because
we observed a clear migration path that was short in
duration).
2.4
| Behavioral characteristics
After we delineated each SSM turtle track into area-
restricted searching or transiting modes, we characterized
the SSM locations representing migration path (trans-
iting)
and
the
foraging
locations
(area-restricted
searching) for each turtle. Because all turtles in this
dataset were tagged after nesting, we used date of last
beach encounter, a plot of cumulative distance traveled
versus deployment duration (e.g., Hart et al., 2021;
Tucker, MacDonald, & Seminoff, 2014), and mode
assigned by SSM to delimit migration and foraging
behavioral modes. We also visually inspected each SSM
track and compared it to the corresponding satellite track
for quality assurance. We identified the first migration
date, last migration date, first foraging date, and last for-
aging date of each turtle, where the foraging period is
represented by the locations after the last migration date.
Location filters to the SSM data were applied to account
deviations in the location data that may not have represen-
ted in-water turtle movements during each behavioral
mode. We filtered out SSM locations that fell on land, loca-
tions that represented movement speeds >5 kph during
foraging, or locations that fell in waters deeper than
200 m (neritic zone delineation) during foraging. Logger-
heads are typically located in water within the continental
shelf, shallower than 200 m deep (Hawkes et al., 2011).
Additionally, if the turtle exhibited a stopover during
migration (two or more consecutive days of area-restricted
searching locations during migration) or a foray during for-
aging (two or more consecutive days of transiting locations
during foraging), we excluded these points.
We determined the nesting interval between nesting
events in a given season for turtles with available data;
identification of nesting events followed protocol outlined
in Hart, Zawada, Fujisaki, and Lidz (2010). First, we com-
piled all nesting encounters observed on the ground. Next,
we filtered satellite data before the start of migration to
include only the highest quality locations (LC 1–3;
CLS, 2015) that occurred close to or on land (within the
error estimate for each LC class), that were clustered dur-
ing a short-time span, and occurred during night-time
hours; in some rare cases lower quality locations (LC A–B)
were used to infer nesting if they were clustered in time,
space, and occurred at night (Tucker, 2010; Vincent,
McConnell, Ridoux, & Fedak, 2002). These filtered satellite
locations were used to infer nesting events only if they met
location, clustering, and time-based criteria outlined above.
We combined these inferred nesting events with known
nesting events observed on the beach, and determined
nesting interval as the days between nesting events.
To assess whether migration and foraging traits differed
between smaller nesting loggerheads that were ≤87 cm
4 of 14
BENSCOTER ET AL.
CCL-n and those that were >87 cm CCL-n, we calculated
the following behavioral characteristics from the SSM
tracks: the length of the migration path (km), the mean
depth along the migration path (m), the depth at the forag-
ing centroid (m), and the distance to shore from the forag-
ing centroid (km). We determined migration path distance
by converting the migration SSM points to a line, and cal-
culating the length of the line. We determined foraging
centroids for each turtle using the geometric center (arith-
metic mean position) of the foraging SSM points. All depth
calculations were conducted using the ETOPO1 Bedrock
cell-registered bathymetry (Amante & Eakins, 2009) and
the shoreline layer used was the Global Self-consistent,
Hierarchical,
High-resolution
Geography
Database
(GSHHG; Wessel & Smith, 1996). All depth and distance
calculations were made in ArcGIS 10.7.1 (ESRI, 2019; Data
Management, Analysis, Tracking Analysis, and Spatial
Analyst toolboxes) and all summary statistics were calcu-
lated in R using the package dplyr (Wickham, François,
Henry, & Müller, 2020).
To evaluate whether migration and foraging charac-
teristics varied based on turtle size category (≤87 cm or
>87 cm CCL-n), we ran two sets of linear regression
models: one for migration traits (n = 99 turtles) and one
for foraging traits (n = 110 turtles). For the migration
traits, we assessed whether the migration path distance
and the depth along the migration path varied according
to size and site. For the foraging traits, we assessed
whether the distance to shore from the foraging centroid
and the depth at the foraging centroid and varied
according to size and site. All migration and foraging
response variables were ln-transformed (natural loga-
rithm) because their distributions were positively skewed
(mean > median); we used absolute values of depth vari-
ables in the models. We also generated kernel density
estimate plots (equivalent to a smoothed histogram) for
each migration or foraging response variable to visually
compare the distribution of values (the area under the
curve is equal to 1) for each behavioral trait (Venables &
Ripley, 2002) in the R package ggplot2 (Wickham, 2016).
3
| RESULTS
3.1
| Proportion of smaller-sized nesters
The total number of individually sampled turtles was
352 (AL: n = 157, DRTO: n = 161, ENP: n = 34). The
CCL-n of the smaller-sized nesting loggerhead females
ranged
from 74.0
to 86.9 cm (n = 44, mean
size = 84.4 cm, median size = 85.5 cm, SD = 2.9). For
comparison, the CCL-n of larger nesters ranged from 87.3
to 108.9 cm (n = 308, mean size = 94.9 cm, median
size = 94.5 cm, SD = 4.9; Figure 1; see Benscoter &
Hart, 2021). The mean proportion of smaller nesters was
0.13 across all sites. Model selection, determined via AICc
and model weight (ω), indicated that the top two models
were the site model and the null model. Although, there
was not a high level of differentiation between the site
and null model in terms of AICc (ΔAICc <1 between the
site model and the null model), the site model had
greater model weight and slightly higher R2 compared to
the null model (Lüdecke, Makowski, Waggoner, & Patil,
2020), therefore we present the site model as the top
model (AICc = 266.75, df = 3, ω = 0.56; see Tables S1a
and S1b, Supporting Information). The site model indi-
cated that the proportion of smaller-sized nesters varied
according to site, where the proportion of nesting females
≤87 cm CCL-n was higher at ENP compared to AL (the
intercept, z = 2.20, p = 0.02). The greatest proportion of
smaller-sized reproductive loggerheads was observed at
ENP (0.24; n = 8 out of 34 turtles), then DRTO (0.13;
n = 21 out of 161 turtles), followed AL (0.10; n = 15 out
of 157 turtles; Figure 2).
We also determined the threshold size defining
female reproductive loggerheads at which 10, 5, 2.5, and
1% of our observed nesters would be classified as smaller-
sized. This exercised revealed that the size thresholds at
which 10, 5, 2.5, and 1% of the turtles in our data set
would be classified as smaller-sized nesters were 86.5,
85.3, 82.4, and 79.3 cm CCL-n, respectively.
FIGURE 1 Histogram showing the sizes of female
reproductive loggerhead turtles (Caretta caretta; curved carapace
length-notch, CCL-n) nesting at three sites in the Gulf of Mexico:
Gulf Shores, Alabama, Dry Tortugas National Park, Florida (FL),
Everglades National Park, FL; the black line represents the
threshold between the smaller (≤87 cm CCL-n, n = 44) nesting
females and the larger (>87 cm CCL-n, n = 308) size class, where
the standard size considered as reproductive for loggerhead females
in this region is >87 cm CCL-n (as defined in Witherington, 1986;
Bjorndal et al., 2000, 2001; NMFS, 2001; NMFS-USFWS, 2008)
BENSCOTER ET AL.
5 of 14
3.2
| Behavioral characteristics
Of all the reproductive female loggerheads tagged at the
three sites, 110 turtles were also satellite-tracked and had
data to calculate inter-nesting (n = 95), migration (n = 99),
and foraging characteristics (n = 110) (see Benscoter &
Hart, 2021). The inter-nesting interval for smaller-sized
nesters was 12.1 days (±2.1 SD for n = 13 turtles) and
13.0 days for the nesters >87 cm CCL-n (±2.0 SD for
n = 81 turtles). There were differences between the smaller
reproductive females and their larger (>87 cm CCL-n)
counterparts in behavioral traits, particularly for migration
(Figure 3,4). The mean migration path distance was shorter
for the smaller (mean = 142.9 m, 95% CI: 81.5–250.3 m)
versus the larger (mean = 362.1 m, 95% CI: 291.2–450.4 m)
nesters (R2 = 0.09; t = 3.09, p < 0.01). The mean depth
along the migration path was shallower (less negative)
for smaller (mean = 21.7 m, 95% CI: 9.7 to 48.3 m)
versus the larger (mean = 69.4 m, 95% CI: 50.8 to
94.7 m) nesters (t = 2.65, p < 0.01; R2 = 0.06;
Figure 3a,b). We also observed the general patterns that
smaller reproductive loggerheads foraged at more shallow
depths and foraged closer to shore compared to larger
nesters, but the 95% confidence intervals between the two
size classes of turtles overlapped for the estimates of these
response variables (p > 0.05; Figure 3c,d). Although we
accounted for site in our models, we did not observe a con-
sistent significant effect of site for the behavioral models;
therefore, we present the pooled estimate of the migration
and foraging behavioral traits in Figure 3 based on the size
effect alone.
4
| DISCUSSION
In this study, we observed that 13% of the loggerheads
nesting on beaches at three sites in the Gulf of Mexico
were smaller than the standard size considered as a
reproductive female for this species in this region
(≤87 cm CCL-n; sites: Gulf Shores [AL], DRTO [FL], and
ENP [FL]). For loggerheads nesting at ENP, the propor-
tion of smaller-sized nesters was 24%. We also deter-
mined that the size thresholds potentially defining
reproductive loggerhead females at which 10, 5, 2.5, and
1% of the turtles in our data set would be classified as
smaller-sized were 86.5, 85.3, 82.4, and 79.3 cm CCL-n,
FIGURE 2 The proportion of smaller (≤87 cm curved carapace
length-notch, CCL-n) reproductive loggerhead (Caretta caretta)
females varied by site. AL: Gulf Shores, Alabama; DRTO: Dry
Tortugas National Park, Florida (FL); ENP: Everglades National
Park, FL. Black circles represent the predicted values of the
proportion of small-sized reproductive females at each site, the
black lines represent the estimated 95% confidence intervals around
the predicted value (total n = 352 turtles). The proportion of
nesting females ≤87 cm CCL-n was higher at ENP compared to the
intercept, AL (z = 2.20, p = 0.02)
FIGURE 3
(a) Mean migration distance (path length, km),
(b) mean depth along the migration path (m), (c) the distance to
shore from the foraging centroid (km) and (d) mean depth at the
foraging centroid (m), for each size class of female reproductive
loggerheads (Caretta caretta; smaller-sized: ≤87 cm curved
carapace length-notch [CCL-n], and: >87 cm CCL-n). Black circles
represent means and black lines represent the estimated 95%
confidence intervals around the model predictions
6 of 14
BENSCOTER ET AL.
respectively. This exercise provided a preliminary evalua-
tion of how the proportion of smaller-sized reproductive
loggerhead females could change if the size threshold
classifying adult reproductive female loggerheads shifted.
We caution however, that our data set is from three of
the five RUs for Northwest Atlantic Ocean DPS of logger-
head marine turtles, and we sampled during only a por-
tion of the nesting season. Longer duration studies that
continue to evaluate the proportion of loggerheads
nesting at smaller sizes that what is typically considered
reproductive may lend to increased understanding of
the size female loggerheads begin reproducing in this
region. For example, Phillips, Stahelin, Chabot, and
Mansfield (2021) recently determined that the mini-
mum size interval (the range of values from the
smallest individual up to two standard deviations below
the mean) of mature loggerhead females nesting at
Archie Carr National Wildlife Refuge from 1982 to 2019
was 70.6–83.2 CCL-n (n = 9855 turtles; size conversion
equations obtained from NOAA-NMFS, 2009). Coordi-
nation with
studies
such as Phillips,
Stahelin,
et al. (2021) to include a broader spatial and temporal
coverage of the Northwest Atlantic Ocean DPS of log-
gerhead marine turtles is necessary to fully evaluate the
appropriate size threshold defining reproductive female
loggerheads in this region.
The smaller reproductive females in our data set
behaved differently than their larger counterparts, specif-
ically they exhibited shorter migration distances and
migrated along shallower depths compared to the larger
(>87 cm CCL-n) reproductive females. In general, the
probability of migrating is associated with body size
(mass) for swimming and walking species (birds and
mammals; Soriano-Redondo, Gutiérrez, Hodgson, &
Bearhop, 2020). Here, we observed a similar pattern
within species, where longer migration distances were
FIGURE 4 Location of the foraging centroids for (a) smaller-sized reproductive loggerheads (Caretta caretta, ≤87 cm curved carapace
length-notch [CCL-n], triangles, n = 15) and (b) and reproductive loggerheads that are >87 cm CCL-n, circles, n = 95). Turtles were
satellite-tracked after nesting on beaches in Gulf Shores, AL (orange star), Dry Tortugas National Park, Florida, (FL; DRTO, yellow star), or
Everglades National Park, FL (ENP, purple star). Density plots for (c) migration distance (path length, km), (d) depth along the migration
path (m), (e) distance to shore from the foraging centroid (km), and (f) depth at the foraging centroid (m) for each size class of female
reproductive loggerheads (light gray = smaller-sized nesters, dark gray = nesters >87 cm CCL-n)
BENSCOTER ET AL.
7 of 14
associated with larger-individuals, and short migration
distances were associated with smaller individuals. Varia-
tion in movement behavior of individuals in a given pop-
ulation or
subpopulation may potentially
expose
individuals to different threats (e.g., exposure to fisheries,
boat strikes, algal blooms), and understanding behavioral
differences between different sizes of nesting loggerhead
females is valuable for recognizing how current regula-
tions offer protection for reproductive female loggerhead
turtles.
Our results have potential implications for the classi-
fication of reproductive adults in bycatch estimates and
incidental stranding limits (ISLs). Understanding the
number of strandings in the mature (i.e., adult) age class
is an important component of species management for
imperiled marine reptiles that are susceptible to human
and environmental threats. Whether an individual is cat-
egorized as an adult in a stranding occurrence effects
ISLs and the application of ISLs into fisheries manage-
ment to reduce bycatch (Hart et al., 2006). Currently, the
RESTORE Act aims to reduce bycatch (Gulf Coast Eco-
system Restoration Council, 2013) and the classification
of reproductive individuals
in bycatch estimates
is
applied based on our understanding of what size defines
a reproductive adult. The size classification in bycatch
estimates also may affect whether recovery criteria in the
Recovery Plan for the Northwest Atlantic Ocean DPS of
loggerhead marine turtles (NMFS-USFWS, 2008) are
being met.
The smaller size at reproduction can also affect popu-
lation demography. Although development of population
models for loggerheads is limited by knowledge gaps in
species biology (Heppell, 1998), in particular for the early
oceanic life stage (National Research Council, 1990), the
size at maturity affects reproductive attributes and repro-
ductive success in marine turtles. The size at reproduc-
tion can affect clutch size (smaller clutch size for smaller
marine turtles; Broderick, Glen, Godley, & Hays, 2003)
and the number of clutches produced in a reproductive
season (more clutches produced in larger animals; Brost
et al., 2015). Similarly, body size is positively correlated
with traits such as egg size and overall reproductive effort
in marine turtles (van Buskirk & Crowder, 1994). The
small size of nesting loggerhead females in this study is
notable because of their imperiled statuses and the low
population sizes (i.e., hundreds not thousands) of the
DRTO and Northern Gulf of Mexico (Gulf Shores, AL)
RUs, where small turtle size may limit the ability to
recover from population declines or environmental per-
turbations (e.g., oil spills). We also provide valuable infor-
mation on loggerheads nesting at ENP, which are
understudied
component
of
the
Peninsular
FL
RU. Variation in the size at reproduction within each
distinct subpopulation can affect life stage durations and
fecundity estimates, is important for accurately modeling
subpopulation and population dynamics, and may also
affect movement behavior.
The trends observed here may apply to other hard-
shelled marine turtles in other locations. For example,
for female green turtles (Chelonia mydas) tagged and
satellite-tracked after nesting in the Galapagos Archipel-
ago (Ecuador), the largest turtles exhibited different
migration and foraging behavioral patterns compared to
the smallest turtles, whereby the largest turtles performed
oceanic migrations to neritic foraging areas and the
smallest turtles remained in the Galapagos (Seminoff
et al., 2008). Similarly, for loggerhead turtles satellite-
tagged after nesting at Keewaydin Island, FL, larger tur-
tles migrated to the northern Gulf of Mexico and the
Bahamas and foraged in those locations, and smaller tur-
tles remained near the nesting beach in south Florida
and
foraged
locally
(Phillips, Addison, Sasso, &
Mansfield, 2021). The differences in movement behavior
between turtles of different sizes have implications for
managing the diverse threats that occur in shallow
coastal areas versus deeper oceanic zones. For example,
the management of nearshore marine areas for recrea-
tional and commercial use may not currently protect
areas that smaller reproductive loggerheads use, if des-
ignated based on larger turtle movement information.
Furthermore, there exists a greater impact of anthropo-
genic drivers in ocean areas that are shallow and near
the shore (Halpern et al., 2008), including areas that
loggerheads use.
There is evidence for variation in marine turtle size
for female Northwest Atlantic loggerhead marine turtles.
The size of nesting loggerheads in this study ranged from
74.0 to 108.9 cm CCL-n (n = 352), which suggests our
turtles are smaller than other Northwest Atlantic logger-
heads. For example, nesting loggerhead females from
Archie Carr NWR (Peninsular FL RU) ranged from 82.3
to 114.5 CCL-n (n = 46; Evans, Carthy, & Ceriani, 2019);
size
conversion equations obtained
from NOAA-
NMFS (2009). However, a recent study by Phillips,
Stahelin, Chabot, and Mansfield (2021) documents
mature loggerheads as small as 70.6 CCL-n nesting at
Archie Carr National Wildlife Refuge (n = 9855 turtles
from 1982 to 2019; size conversion equations obtained
from NOAA-NMFS, 2009). Nesting female loggerheads
from the Northern RU for Northwest Atlantic logger-
heads ranged from 80.2 to 111.4 CCL-n (n = 64; Griffin
et al., 2013). Moreover, the CCL-n size range of the
nesting population at Blackbeard Island National Wild-
life Refuge in Georgia (Northern RU) ranged 84.6–
111.1 cm (from 2001 to 2008; Cason, 2009). Another pop-
ulation in coastal Georgia ranged from 94.6 to 114.9 cm
8 of 14
BENSCOTER ET AL.
(Kraemer, 1979). All of these studies report a larger mini-
mum and maximum size of nesting female loggerheads
compared to the turtles we observed, except for Phillips,
Stahelin, et al. (2021). However, many of them also have
observations of female loggerheads nesting at sizes less
than 87 cm CCL-n.
Size data across various sites in the Gulf of Mexico
(from NOAA-NMFS, 2009) show a similar pattern of a
broad range of sizes representing the size of first-time
(neophyte) nesters for loggerheads, indicating high varia-
tion in marine turtle size. Putative first-time loggerhead
nesters in the Peninsular FL Subpopulation were smaller
(mean size = 95.4 CCL-n, n = 300) compared to putative
first-time nesters in the Northern (mean = 98.0 CCL-n,
n = 158) and Greater Caribbean (mean = 97.2 CCL-n,
n = 368) RU. Data on loggerheads on the SE U.S. coast
show a wide range of sizes in neophyte nesters, ranging
from 80.4 to 115.0 CCL (n = 826; Scott, Marsh, &
Hays, 2012; TEWG, 2009). The minimum size of sexual
maturation estimated (via skeletochronological analysis)
for
loggerheads along
the Atlantic
coast of
the
United States was 78.5 cm CCL (mean = 96.3,
max = 108.6, n = 32; Avens et al., 2015; size conversion
equations obtained from NOAA-NMFS, 2009; Avens
et al., 2013). It is notable that other studies also report
loggerheads nesting at sizes less than the 87 cm CCL
threshold for which loggerhead females in this region are
considered sexually mature. However, the smallest size of
sexually mature females in many of these other studies
are still larger than those we report (smallest size in this
study = 74.0 cm CCL).
Our results provide an interesting parallel to research
in the Mediterranean, where observed sizes of reproduc-
tive loggerheads are very small. The minimum, mean,
and maximum size at sexual maturity for nesting female
loggerheads in the Mediterranean was reported as 66.4,
69.0, and 84.7 cm CCL, respectively (summarized in
Avens et al., 2015; Casale, Mazaris, Freggi, Vallini, &
Argano,
2009; Casale, Conte,
Freggi, Cioni, &
Argano, 2011; Casale, Mazaris, & Freggi, 2011; Piovano
et al., 2011). Tiwari and Bjorndal (2000) reported smaller
body sizes in Mediterranean loggerheads, compared to
other loggerheads in Brazil and FL (east coast of FL). The
smaller body size of Mediterranean turtles may be
explained in part by latitude, where a negative correla-
tion was observed between body size and latitude
(Tiwari & Bjorndal, 2000), and could be related to factors
such as growth rate.
The smaller sizes of nesting loggerhead females in the
three RUs in the Northwest Atlantic may be indicative of
slower growth rates and/or maturation at younger ages,
which may represent a shorter juvenile stage for these
turtles. Interestingly, Bjorndal et al. (2013) report a
decline in growth rates in Northwest Atlantic logger-
heads from 1997 to 2007. Both slower growth rates and
maturation at younger ages have potential implications
for the timing of ontogenetic shifts, the age structure of
the population, reproductive success, and ultimately pop-
ulation dynamics. Numerous other marine ectotherms
show maturation at younger ages and sizes from stressors
such as fisheries (Hutchings & Reynolds, 2004; Morita &
Fukuwaka, 2007; Piacenza et al., 2016) and warming
(Audzijonyte et al., 2016; Daufresne, Lengfellner, &
Sommer, 2009; Jonsson, Jonsson, & Finstad, 2013;
Ohlberger, 2013); fisheries bycatch is identified as the
greatest marine threat to the Northwest Atlantic Ocean
loggerhead marine turtle DPS (Bolten et al., 2019).
The size and number of females that are reproducing
in the population is vital to understanding how Recovery
Objectives, Demographic Recovery Criteria, and Recov-
ery Actions defined in the Recovery Plan for the North-
west Atlantic Ocean DPS of loggerhead marine turtles
are being met (NMFS-USFWS, 2008). Recovery Objec-
tives in the Recovery Plan include increasing the number
of nests per recovery unit, associated increases in nesting
females with nest number increases, minimizing fisheries
bycatch, and minimizing trophic changes from fisheries
harvest and habitat alteration (NMFS-USFWS, 2008).
There are also Demographic Recovery Criteria related to
nest numbers and rates of increase, and ensuring that
neritic strandings do not increase at a greater rate than
in-water abundance trends for similar age classes
(NMFS-USFWS, 2008). Recovery Actions include moni-
toring nesting and in-water trends, and implementing
measures to minimize bycatch. If these Recovery Objec-
tives, Criteria, and Actions are evaluated based on the
threshold size greater than 87 cm CCL-n representing
mature females, these evaluations may not accurately
represent what is occurring in the population. The life
history of the loggerhead marine turtle is complex, and
different threats are shown to interact with different life
stages for this species (Bolten et al., 2011). Therefore, dif-
ferences in maturation size and behavior (and conse-
quently other potential factors such as reproductive
output, stage durations, space use over time) can interact
with different threats, and the relative importance each
threat poses to the population growth rate (Bolten
et al., 2011). Understanding the risk of each threat to
population recovery has been identified as crucial to the
success of recovery actions and reaching recovery objec-
tives for imperiled species (Bolten et al., 2011). Wide-
ranging marine species show inter-population variation
in life history traits and population dynamics that merit
management specific to individual populations (Wallace
et al., 2010). This is especially important for species such
as sea turtles because their intrinsic traits of longevity,
BENSCOTER ET AL.
9 of 14
large body size, late maturity, low fecundity, rarity, and
high market value make them particularly vulnerable to
and prone to extinction (He et al., 2017).
When we compared the proportion of smaller-sized
reproductive females between sites in our study, the
site model indicated that ENP had a greater proportion
of smaller-sized reproductive females compared to AL.
Although the site model represented the lowest AICc,
highest ω, highest R2, and had a significant effect of site
(p = 0.02), we note that there was not a high degree of
differentiation between the site model and the null model
in terms of the AICc (ΔAICc <1 between the site model
and the null model), and the R2 value was low for the site
model (R2 = 0.04). However, the mean proportion of
smaller-sized reproductive females was 0.13 across all
sites, and ranged from 0.10 at AL to 0.24 at ENP, which
we think alone is a crucial finding. The primary aim of
this study is to document the presence and frequency of
female loggerhead turtles that are nesting at sizes smaller
than what is typically considered reproductive for this
species in this region, which is evident across all three
study sites. The sampling frequency and duration in this
data set only covers a portion of the nesting season,
therefore future efforts to increase sample sizes and sam-
ple locations could allow researchers to better understand
the frequency of smaller-sized reproductive females both
spatially and temporally in the Northwest Atlantic Ocean
loggerhead DPS.
Our behavioral models had low R2 values (range:
0.06–0.09). We find this unsurprising, as the response
variables we used are affected by a number of complex
ecological and evolutionary factors in addition to turtle
size, and it was not our goal to capture those other fac-
tors. Turtle size was a better predictor of migration traits
than of foraging traits: the two migration trait response
variables had a mean R2 = 0.08, while the two foraging
trait response variables had a mean R2 = 0.02 and were
not significant (although the foraging depth trait had a
p-value of .06). While size clearly does not predict turtle
migration traits extremely well, our finding that size
alone can explain nearly 8% of the variation in migration
in our data set is important. Notably, we did not observe
any small-sized reproductive loggerheads migrating long
distances or migrating in the deeper water; all of the
smaller-sized reproductive turtles migrated shorter dis-
tances in shallow water across the entire study period
(2011–2019). We did not observe any smaller reproduc-
tive females migrating across the FL Straits to the
Bahamas or Cuba, or across the Gulf of Mexico to the
Yucatan Peninsula, as observed in the larger (>87 cm
CCL-n) reproductive loggerheads. Similarly, the smaller-
sized reproductive turtles did not forage at the deeper
end of foraging depths observed in our data set. The
smaller reproductive female turtles also foraged close to
shore, with the exception of 1 individual, which we
believe contributed to the high confidence interval
around the foraging distance to shore variable. The min-
imum values for migration distance, migration depth,
foraging depth, and foraging distance to shore all
pertained to the smaller-sized loggerheads. Variation in
migration patterns based on turtle size can affect the
degree and duration these turtles interact with threats
such as fisheries and boat strikes, their overlap in space
use with marine protected areas, and use of habitat areas
(Shimada, Limpus, Jones, & Hamann, 2017). It would be
valuable for other studies on the Northwest Atlantic
Ocean loggerhead marine turtle DPS and for this RMU
to examine the proportion of smaller-sized nesters and
their migration and foraging behavioral characteristics
to increase our understanding of how trends in propor-
tion of smaller nesters and their behavior may vary
across space and time, and how they interact with
threats, habitat use patterns, and marine protected area
delineations.
The observation that female loggerheads are nesting at
smaller sizes than typically considered reproductive for this
species in this region is important and has numerous con-
servation and management implications, especially given
that loggerhead marine turtles face many threats to recov-
ery, ranging from in-water threats (e.g., fisheries bycatch,
climate change, oil spills, ingestion of plastics) to nesting
habitat threats (e.g., anthropogenic development, beach
erosion, sea-level rise). We also provide analyses that aim
to decipher patterns related to the proportion of these small
females nesting over space and time, as well as behavioral
patterns that may differ for these smaller-bodied reproduc-
tive females. However, most importantly, the observation
of smaller-sized loggerhead females nesting at three sites in
the Gulf of Mexico has crucial conservation and manage-
ment
implications,
including classification of
turtle
strandings, bycatch estimates, developing population
models (e.g., stage durations, fecundity), understanding
population trends, and the ability to monitor and meet
recovery objectives for this species. Future studies investi-
gating the degree to which these smaller females are rep-
roducing could provide critical information to resource
managers. The sampling we conducted at each study site
in our data set occurs during a portion of the nesting sea-
son (1–3 weeks per year depending on the site in our
study). Greater sampling frequency, duration, and extent
(e.g., different spatial areas) could help differentiate possi-
ble patterns in the ratio of smaller reproductive females
and their behavior across space and time. The application
of more in-depth studies across all of the RU's within this
Northwest Atlantic Ocean DPS on the proportion and
behavior of smaller reproductive females may have serious
10 of 14
BENSCOTER ET AL.
implications for long-term population recovery of the
imperiled loggerhead marine turtle.
ACKNOWLEDGMENTS
Work was conducted under authority of research permits
from: Florida Fish & Wildlife Conservation Commission
Marine Turtle Permit #176 (issued to K. Hart), Bon
Secour National Wildlife Refuge Special Use Permit
#12-006S (issued to K. Hart), Federal U.S. Fish & Wildlife
Permits #TE206903-1
(issued
to
J. Phillips)
and
#TE98424-1 (issued to K. Hart), Dry Tortugas Scientific
Research Permits DRTO – 2010-SCI-0009, 2012-SCI-0008,
2014-SCI-0004, 2016-SCI-0008, 2018-SCI-0007 (issued to
K. Hart), Everglades Scientific Research Permits EVER –
2010-SCI-0041, 2012-SCI-0025, 2014-SCI-0031, 2016-SCI-
0032, 2018-SCI-0023 (issued to K. Hart), and the
U.S. Geological Survey Animal Care (USGS) and Use Per-
mit #SESC-2011-05 (issued to K. Hart). Funding partially
provided by USGS Priority Ecosystem Science Program,
Deepwater Horizon Oil Spill Natural Resource Damage
Assessment, and USGS Ecosystems Mission Area.
CONFLICT OF INTEREST
The authors declare no potential conflict of interest.
AUTHOR CONTRIBUTIONS
Allison M. Benscoter led the analyses and writing and
contributed to design. Brian J. Smith contributed to data
acquisition, design, analyses,
and writing. Kristen
M. Hart led the conception and design, secured funding
and permits, led the data acquisition, and contributed to
analyses and writing. All authors contributed to the revi-
sion and preparation of the final version.
DATA AVAILABILITY STATEMENT
Data are accessible via ScienceBase repository, via the fol-
lowing DOI link: https://doi.org/10.5066/P96S4B8P
ETHICS STATEMENT
All methods were approved by Institutional Animal Care
and Use Committee Protocol (USGS-Southeast Ecological
Science Center: USGS-WARC-GNV #2011-05
and
#2019-14 and the United States National Park Service
SER-BISC-BUIS-DRTO-EVER-Hart-Sea
Turtles-Terra-
pins-2018-A2). All appropriate permits were obtained
(see Acknowledgments section).
ORCID
Allison M. Benscoter https://orcid.org/0000-0003-4205-
3808
Brian J. Smith https://orcid.org/0000-0002-0531-0492
Kristen M. Hart https://orcid.org/0000-0002-5257-7974
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SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of the article at the publisher's website.
How to cite this article: Benscoter, A. M., Smith,
B. J., & Hart, K. M. (2021). Loggerhead marine
turtles (Caretta caretta) nesting at smaller sizes
than expected in the Gulf of Mexico: Implications
for turtle behavior, population dynamics, and
conservation. Conservation Science and Practice,
e581. https://doi.org/10.1111/csp2.581
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