Crowe et al. Movement Ecology(2020) 8:32
https://doi.org/10.1186/s40462-020-00218-6

RESEARCH

Open Access

Riders on the storm: loggerhead sea turtles
detect and respond to a major hurricane in
the Northwest Atlantic Ocean
Leah M. Crowe1*, Joshua M. Hatch2, Samir H. Patel3, Ronald J. Smolowitz3 and Heather L. Haas2

Abstract
Background: Extreme weather events, including hurricanes, have considerable biological, ecological, andanthropogenic impacts. Hurricane Irene caused substantial economic damage when it hit the Mid-Atlantic Bight(MAB) off of the eastern United States in August of 2011. The MAB is highly stratified during the summer when astrong thermocline separates warm, surface water from deep, cold water, and this oceanographic phenomenon
makes modeling hurricane strength difficult. Loggerhead sea turtles (Caretta caretta) forage in the MAB primarily
during the stratified season and their dive behavior to the bottom allows them to experience the oceanographic
conditions of the entire water column.
Methods: In this study, we analyzed the movements and dive behavior of juvenile and adult-sized loggerhead sea
turtles (n = 18) that were foraging in the MAB as Hurricane Irene moved through the region. The satellite tags
deployed on these turtles transmitted location data and dive behavior as well as sea surface temperature (SST) andtemperature-depth profiles during this time.
Results: Behavioral and environmental shifts were observed during and after the hurricane compared to conditions
before the storm. During the hurricane, most of the turtles (n = 15) moved north of their pre-storm foraging
grounds. Following the storm, some turtles left their established foraging sites (n = 8) moving south by 7.3–135.0
km, and for the others that remained (n = 10), 12% of the observed dives were longer (0.54–1.11 h) than divesobserved before the storm. The in situ data collected by the turtle-borne tags captured the cooling of the SST(Mean difference = 4.47°C) and the deepening of the thermocline relative to the pre-storm conditions.
Conclusions: Some of the loggerhead behavior observed relative to a passing hurricane differed from the regularpattern of seasonal movement expected for turtles that forage in the MAB. These data documented the shifts in
sea turtle behavior and distribution during an ecosystem-level perturbation and the recorded in situ data
demonstrated that loggerheads observe environmental changes to the entire water column, including during
extreme weather events.
Keywords: Satellite telemetry, Temperature, Behavioral response, Dive behavior, Cold pool, Mid-Atlantic bight,
Extreme weather event* Correspondence: leah.crowe@noaa.gov
1
Integrated Statistics under contract to the Northeast Fisheries Science
Center, National Marine Fisheries Service, National Oceanic and Atmospheric
Administration, 166 Water Street, Woods Hole, MA 02543, USA
Full list of author information is available at the end of the article© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
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Crowe et al. Movement Ecology(2020) 8:32

Background
Extreme weather events, including hurricanes, have considerable biological, ecological, and anthropogenic impacts [1, 2], and the risk of loss increases as more people
and resources interact with these disasters [2]. Hurricanes occur seasonally within each ocean basin, andhave become more intense overtime, with this trend
expected to continue [3]. Hurricane Irene hit the MidAtlantic Bight (MAB) of the United States’ eastern seaboard in August 2011, causing 49 human deaths andcost an estimated $15.8 billion (USD) in damages,
mostly because of widespread flooding [4].
During the Atlantic hurricane season, the oceanography in the MAB is dynamic [5] and difficult to model[6] because a Cold Pool forms beneath a warm, surface
layer [7–9]. Hurricane Irene was preempted by a 6°–
11°C decrease in sea surface temperature (SST; i.e.
ahead-of-eye cooling) and a deepening of the thermocline by more than 15 m [10], primarily due to hurricane
forced vertical mixing which was not accurately
accounted for in hurricane modeling [10, 11]. The forecast for Hurricane Irene anticipated higher wind speedsthat would have kept it along its projected path, but instead, the cooled surface waters decreased the strengthof the storm before it made landfall, causing the storm
to stall in areas that were unprepared [11]. Although theforecast models for Irene did not account for ahead-ofeye cooling, this phenomenon has occurred for all tropical cyclones that have interacted with the stratified
conditions in the MAB since 1985 [10].
In addition to the impacts on the oceanography andhuman population, tropical storms and hurricanes cancause changes in the behavior of marine species. American lobsters (Homarus americanus) moved out of estuarine waters and into coastal waters during the passingof Hurricane Bob [12]. Sea snakes (Laticauda spp.) andjuvenile blacktip sharks (Carcharhinus limbatus) moved
into deeper waters as hurricanes and tropical storms
caused barometric pressure to drop [13, 14]. Several
shark species were temporarily displaced from study
areas during the landfall of tropical storms [15], and increased emigration and daily movement rates of graytriggerfish (Balistes capriscus) were highly correlatedwith wave orbital velocity during the passing of two hurricanes [16]. Spotted seatrout (Cynoscion nebulosus)
spawning was potentially delayed because of decreased
water temperature due to a hurricane [17]. Finally, Eastern brown pelicans (Pelecanus occidentalis carolinensis)
were observed sheltering in coastal regions during hurricanes to possibly allow for protection and rest [18].
There are few examples of sea turtle interactions withlarge storm events. Both a tagged loggerhead (Caretta
caretta) and hawksbill (Eretmochelys imbricata) nestingfemale became more active when overlapping with

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extreme storms [19, 20]. Early tagging efforts of loggerhead sea turtles revealed some interaction between
storms and two nesting females, but the data transmissions were thought to have been negatively impacted by
the weather [21]. Adult loggerheads may have left theirbreeding areas in response to decreasing barometricpressure, a possible signal of worsening conditions [22].
Juvenile hawksbill turtles moved to deeper waters during
two consecutive intense hurricane events in the Caribbean [23]. Modeling studies show that hurricanes candisrupt the migratory routes of younger sea turtles, potentially pushing them into unsuitable habitats [24, 25].
Foraging juvenile and adult loggerheads occur along
the shelf in the MAB between May and September [26],overlapping substantially with the Atlantic hurricane
season (June – November) [27] and the period when theCold Pool is present (approximately May – October) [7].
The oceanography of the MAB is likely to play an important role in hurricane behavior and disaster preparation in the future, and this has encouraged the use of
gliders to collect in situ data as storms work their way
up the Northwest Atlantic Ocean [9]. Loggerhead sea
turtle morphology and foraging behavior make themgood observers of oceanographic variables throughout
the entire water column where they forage [8, 28], andthe data derived from turtle-borne data loggers are currently an under-utilized resource that has the potential
to improve forecasting models [29].
In this study, we analyzed loggerhead sea turtle behavior in the MAB and the environmental conditions observed from turtle-borne satellite tags in relation to
Hurricane Irene. We determined that as the storm
passed, the tagged turtles altered their dive behavior andmovement patterns. These observed changes in behavior
can provide insight into turtle reactions to other perturbations. The turtle-borne tags also recorded the environmental changes to the water column as the hurricane
passed through the MAB, highlighting these data as avalid resource for weather forecasting models alongsideother in situ data sources.

Methods
Loggerhead sea turtles were captured in early June andlate July 2011 in the MAB with a large dip net. Netted
turtles were transferred to a chartered commercial fishing vessel for sampling and tag attachment. Turtles were
measured and weighed in compliance with the UnitedStates Endangered Species Act permitting requirements.
Satellite relay data loggers from the Sea Mammal Research Unit at the University of St. Andrews were attached to the carapace with a two-part epoxy. Tag
parameterization was designed to allow for a lifespanachieving approximately 13 months [8]. For full details
on handling and capture protocols as well as theCrowe et al. Movement Ecology(2020) 8:32

parameterization of the tags used in this study, see Patelet al. [8]. A random sample of temperature-depth anddive data were transmitted [30], and recorded divesbegan when the tag was at or below 1.5 m depth for atleast 20 s until it was dry or above 1.5 m depth. Tags
were programmed to include both Fastloc-GPS and
Argos locations for approximately the first three monthsof deployment, and Argos throughout the lifespan of thetag.
Location data from Argos and Fastloc-GPS data were
filtered and combined into a single dataset. Only location quality classes 1–3 were retained for Argos positions, and Fastloc-GPS data were filtered for locations
that were obtained using five or more satellites [31]where the residuals were greater than 0 and less than 25.
These location data were combined and a speed filter
with a maximum rate of 10 km h− 1 was applied to all location data [32]. Locations were mapped to ensure thelower resolution Argos locations fell within the path of
the higher resolution Fastloc-GPS positions, and any
visually erroneous points were excluded [33]. Data werecompiled and analyzed using R 3.5.1 [34] and the dplyr[35], geosphere [36], lubridate [37], and plyr [38] R
packages.
Hurricane Irene first formed on 21 August 2011 andwas absorbed on 30 August 2011 [4]. Using the best
track from the National Hurricane Center [39], thestorm’s position at each location of a tagged turtle wasdetermined using linear interpolation according to thefollowing:~x; ~y ¼ ð1 − αÞðx1 ; y1 Þ þ αðx2 ; y2 Þ
where (x̃ , ỹ) is the interpolated storm location, (x1, y1) isthe beginning location of the storm, (x2, y2) is the ending
location of the storm, and α is the proportion of regularinterval time between the timestamp of (x1, y1) and thetimestamp associated with the tagged turtle’s location.
The shortest distance along an ellipsoid between thetagged turtle and the interpolated track of Hurricane
Irene was then calculated.
Data derived from turtle-borne tags that were within
100 km of Hurricane Irene’s path at their closest point(T0) were included in this analysis. This distance ensured
the inclusion of shelf-foraging turtles that were within
the scope of the hurricane (approximately 180 km wide)
as it passed through the MAB [4, 39]. Location data,
temperature-depth profiles, and dive data two weeks before and after T0 were compiled to obtain pre- and poststorm conditions and behaviors. These data were divided
into five phases: Before, Approach, During, Departure,
and After where the Approach and Departure phases
provided 1.5 day buffers around the one day During
period to distinguish clear 12 day Before and After phases

Page 3 of 13(Fig. 1a). Because each turtle had a unique T0 and eachtag transmitted at different times, the hurricane phases
covered slightly different time periods for each turtle(Fig. 1b).
Behavioral data

The pre-storm foraging range for each turtle was calculated as the latitudinal range between the 5th and 95th
percentile of the latitudinal extent for the turtle’s movements three to six weeks prior to T0. There was lessfocus on longitudinal movements as loggerhead sea turtles within the region typically remain resident during
the foraging season and take seasonal long-distance latitudinal migrations when arriving and leaving the MAB[26]. Box plots of turtle latitude were calculated for the
Before, During, and After phases to assess the extent oflatitudinal movement. Turtle movements were characterized by analyzing the interquartile range (the middle
50% of the distribution) of latitudinal movements within
the hurricane phases relative to the foraging range—ifthese overlapped, a turtle was considered to haveremained in its foraging range.
Dive behaviors were assessed by analyzing daytime(0600–2000 EDT) dive duration and maximum divedepth for individuals that remained in their foraging
ranges in order to investigate dive behavior relative to
local changes in the habitat. Daytime diving was specifically chosen because changes to dive behavior could substantially impact the availability of turtles at the surface
during line-transect surveys, and subsequent abundance
estimates [40]. Dive duration relative to maximum divedepth was analyzed to better understand the composition of the type of dive behavior exhibited in eachphase. To compare dive behavior relative to the hurricane, dive duration and maximum dive depth data werepooled and summarized for these turtles in the Before
and After phases.
Environmental data

Turtles that remained in their foraging ranges along asimilar latitudinal range were considered the best observers of the hurricane, and, therefore, SST data andtemperature-depth profiles collected from the turtleborne tags of these individuals were analyzed. Data
collected nearshore (< 5 km) were excluded to ensure
the comparison of temperatures was only across shelfwaters and not from shallow, warmer regions. SST
values were collected at 2.0 m depth and data collected from all turtle-borne tags were compiled together to gain a perspective on the conditions theturtles were experiencing throughout the passage of
Hurricane Irene. SST data were pooled and summarized for these turtles in the Before and After phases
to further compare these changes. Full water column

Crowe et al. Movement Ecology(2020) 8:32

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Fig. 1 a The five hurricane phases were divided relative to the time when the turtle and the hurricane were closest to each other (T0) as follows:
Before (14–2 days before T0), Approach (2–0.5 days before T0), During (0.5 days before–0.5 days after T0), Departure (0.5–2 days after T0), and After (2–14 days after T0). The Approach and Departure phases provided 1.5 day buffers around the During phase to determine clear Before and Afterphases. The length (days) of each phase is displayed within each colored section of the bar. b The range of the dates within each phase for eachturtle are characterized by the colored sections of the horizontal bars. Each turtle had a different T0, and each turtle-borne tag transmitted at
different times, therefore, the hurricane phases covered slightly different time periods per turtle. T0, which occurred at some time on 28 August
2011 for all turtles, is indicated by the white circle within the red, During section

profiles were analyzed relative to each phase for eachturtle to understand how the local water column may
have been affected by the hurricane. Temperaturedepth profiles reaching within 15% of ETOPO1 Ice
Surface Global Relief Model [41] bathymetry wereconsidered full water column profiles as described inPatel et al. [8]. Bathymetry was analyzed using theraster [42] and rgdal [43] R packages.
Turtle-borne tag locations and the hurricane’s path
were plotted using ArcGIS 10 [44] (Fig. 2a, b). The
National Oceanic and Atmospheric Administration’s
National Data Buoy Center Station 44009 is positioned at 38.457°N, 074.702°W [45], halfway north tosouth between the turtles’ extent. Due to its location
and availability of data, this buoy was identified as
the best source of traditional in situ weather data(barometric pressure, SST, wave height, and windspeed) for this region during Hurricane Irene (Fig.
2c).
Figures 1, 2c, 3, 4 and 5 were created using the ggplot2[46] and ggpubr [47] R packages.

Results
Eighteen turtles were within 9.4–80.1 km of the eye of
Irene at their closest points (Fig. 2a). Their straight carapace length (SCL), measured from nuchal notch to posterior marginal tip, ranged from 58.1 to 87.0 cm (n = 17,
Mean = 73.0 cm; Table 1). Six turtles (e, g, h, m, p, and r)
measured a SCL greater than 75 cm, which was consistent with adult size according to Avens et al. [48]. Additionally, the curved carapace lengths measured fromnuchal notch to posterior marginal tip (n = 18, Mean =78.9 cm) were used to identify the life stage corresponding to potential reproductive output according to
Murray [49]. Six classifications are within this scheme
ranging from Stage I to Stage V (adult)—Stage IV is divided into two categories, IVa and IVb, where Stage IVb
has a wide range of reproductive potential [49]. Turtles
in this study represented middle and later juvenile Stages
III (n = 7), IVa (n = 7), and IVb (n = 4) (Table 1).
The turtles were closest to Hurricane Irene’s path (T0)on 28 August 2011 for all individuals when the severityof the storm ranged between a hurricane and a tropicalCrowe et al. Movement Ecology

Fig. 2 (See legend on next page.)(2020) 8:32

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Crowe et al. Movement Ecology(2020) 8:32

Page 6 of 13(See figure on previous page.)
Fig. 2 All locations transmitted from tagged turtles between 14 August and 11 September 2011 (green circles), the track of Hurricane Irene (pinksymbols and lines, UTC) [39], and the environmental conditions two weeks before and after the hurricane recorded by buoy 44009 (yellow
diamond) [45]. a The position where the hurricane and each turtle were closest to each other (T0) occurred on 28 August 2011 for all turtles andare indicated by the red circles. Buoy 44009 was close to the hurricane path and approximately in the middle of the turtle positions within thistime period. b The inset map, denoted by the blue square, illustrates the wind speeds associated with Hurricane Irene. The dark grey indicates
Category 1 hurricane strength (119–153 km h-1), and the light grey indicates tropical storm strength (63–119 km h-1). c Barometric pressure, sea
surface temperature, wave height, and wind speed data gathered by buoy 44009. The red vertical line denotes T0, the grey shaded area borderedby the grey vertical lines denotes the 0.5 day period on either side of T0 spanning the time frame of the During phaseFig. 3 a The latitudinal movements of tagged turtles in the Before, During, and After phases relative to the passing of Hurricane Irene. For each ofthese phases, the colored box represents the interquartile range (25th to 75th percentile), the horizontal black line within the colored box
represents the median value, the upper and lower whiskers represent values that fall within 1.5x the interquartile range, and the black dots
represent the outlying points [46]. The grey shaded area for each turtle represents its foraging range which spanned between the 5th and 95th
percentile of the latitudinal extent for the time period three to six weeks prior to T0. Turtles a – j (light green) remained in their foraging range as
the interquartile range within the After phase overlapped with their foraging range, while turtles k – r (darker green) left their foraging grounds
after the hurricane passed. The light red line connects the medians between each phase to highlight the overall movement pattern. b Example
turtle movements in all phases: c) This animal was one of the turtles that revisited their foraging grounds after moving north in the During and
Departure phases; i) This animal did not leave its pre-storm foraging area in the During phase, but did move a bit south in the After phase; k) This
animal did not return to its foraging ground, and instead was the only animal in this study that moved inshore; r) One of the animals that did
not return to its foraging ground, and instead went south by almost 2° of latitude in the After phaseCrowe et al. Movement Ecology(2020) 8:32

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Fig. 4 Dive duration (hours) relative to the maximum dive depth (m) throughout all phases for turtles that remained in their foraging grounds
after Hurricane Irene passed (a – j)storm. Within the five phases defined here (Before, Approach, During, Departure, and After), 5573 positions
were transmitted from all turtle-borne tags between 14
August 2011 and 11 September 2011. Fastloc-GPS transmissions were received throughout the study period, andsimilar numbers of positions came from each source in
the Before and After phases (ARGOS: Before = 720,
After = 698; Fastloc-GPS: Before = 1782, After = 1617;
Supplementary Fig. 1A, Additional file 1). Of the 108
turtle-phase combinations (Supplementary Fig. 1B, Additional file 1), there were only six instances where more
locations came from Argos than Fastloc-GPS (k and r in
the Before, a and k in the Approach, and d and k in the
During phases), and there were six cases where there
was only Fastloc-GPS data. An additional interactive
map can be used to further investigate the tracks, including the location source, for the turtles throughout
this study period [see Additional file 2].

Behavioral data

Turtle pre-storm foraging areas occurred between
36.80°N and 40.47°N and were calculated from 6708 positions. This period occurred between 17 July 2011 and
14 August 2011 for all turtles except turtle l where theincluded data began the day after it was tagged, 27 July
2011. The latitudinal extent of each area varied amongst
individuals and ranged between 9.7 and 82.7 km(Fig. 3a).
Turtle residency Before the hurricane was primarily
consistent with each turtle’s pre-storm foraging area, but
movement out of the foraging area was observed within
the During and After phases of the hurricane. In the
During phase, all but three of the turtles (m, o, and q)
moved north, and about two thirds of the turtles (a, c, d,e, f, g, h, j, l, and q) had interquartile ranges north oftheir foraging areas—one turtle (m) had an interquartile
range south of its foraging area. Turtles moved 0.3

Crowe et al. Movement Ecology(2020) 8:32

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Fig. 5 In situ water temperature data collected from turtle-borne tags b – i. These turtles remained in their foraging areas in the After phase andwere along a similar latitudinal range (between 37.68°N and 39.30°N). a Sea surface temperature values collected at 2 m depth and b full watercolumn (within 15% of the bottom) temperature-depth profiles throughout all phases

Table 1 Deployment details, straight carapace length (SCL), measured from the nuchal notch to posterior marginal tip, and sizeclass for each tagged turtle used in this analysis. Life stages III and IV are mid and later stage juveniles, respectively [49]Crowe et al. Movement Ecology(2020) 8:32

(turtle q)—62.1 km (turtle c) between the median latitudes of the Before and During phases.
Despite some temporary northward movement During
the hurricane, the interquartile range in the After phase
was at least partially within the pre-storm foraging areafor 10 turtles (a – j; Fig. 3a, light green), and completely
outside of it for eight turtles (k – r; Fig. 3a, darker
green), which had mostly moved south. A comparison ofmedian latitudes of the 10 turtles that remained in theirforaging areas showed that all of them went north in the
During phase and then came south in the After phase(Fig. 3a, e.g. Fig. 3b, turtle c). Two of the turtles thatremained did not leave their foraging area in the Duringphase (e.g. Fig. 3b, turtle i). Of the eight turtles that wentout of their foraging grounds after the hurricane, one ofthem went inshore (Fig. 3b, turtle k), and the rest went
south, traveling 7.3–135.0 km between the southern limitof their pre-storm foraging site and the median latitudeof the After phase (e.g. Fig. 3b, turtle r).
Dive duration and maximum dive depth changed as
the hurricane passed the animals remaining in their foraging areas (n = 1185 total dives, Fig. 4). Longer dive durations were observed in the During phase andcontinued into the Departure phase when the longest
dive was observed (1.70 h). While dive duration shortened moving from the Departure to the After phase, they
were still longer than dives in the Before and Approach phases. Before the passage of the hurricane, all
but one dive was less than 0.54 h. After the hurricane,approximately 12% of the dives, taken by nine of the 10
turtles, exceeded 0.54 h, including a few that exceeded
one hour (Max = 1.11 h, Fig. 4). The Before and Afterphases had similar numbers of dives (Before: n = 381;
After: n = 366), and the dive duration was longer (hours;
Before: Mean = 0.19, SD = 0.13; After: Mean = 0.23, SD =0.24) and maximum dive depth was shallower (m; Before:
Mean = 26.33, SD = 20.57; After: Mean = 20.60, SD =19.91) in the After phase. However, shallow and deep dives were observed throughout all phases of the hurricane(Fig. 4).
Environmental data

Turtles b – i were considered good hurricane observers
as these animals remained in their foraging grounds andwere also within a similar latitudinal range (between
37.68°N and 39.30°N). Data collected in this region (n =354) showed SST dropping at T0 followed by a warming
throughout the After phase (Fig. 5a). The number of
SST data points collected in the Before and After phases
were similar (Before: n = 249; After: n = 251), and the
SST was cooler in the After phase (°C; Before: Mean =25.14, SD = 1.20; After: Mean = 20.67, SD = 1.36).
Additionally, temperature-depth profiles (n = 225) werecompiled for these turtles relative to all five phases (Fig.

Page 9 of 135b). These profiles revealed changes in the thermocline
relative to the passing of the hurricane, and for all turtles, deeper and cooler thermoclines were observed in
the After phase.
T0 for the weather buoy was also identified as 28
1August 2011. A decrease in barometric pressure and
SST and an increase in wave height and wind speed after
T0 was recorded during this period (Fig. 2c) consistent
with the passing of a Category 1 hurricane [4, 10].
The location, dive, and temperature-depth data generated and analyzed in this study are available in Additional
file 3.

Discussion
Hurricane Irene tracked along a large portion of the UnitedStates eastern seaboard that is valued for recreation, shipping, fishing, seismic exploration, and wind farm development. It is also an important habitat for many protected
species [50], and supports densely populated coastal communities [51]. Due to this confluence of potentially conflicting interactions between humans and protected
species, this region is highly managed in order to reduce
harmful anthropogenic impacts. As the region experiences
a rising intensity in ecosystem perturbations, including
hurricanes [3], effective management becomes harder asanimals may become displaced in space and time.
Ecosystem-level perturbations can cause turtles to alter
their routine behavior by direct effects or through habitat
modifications. Here we show that sea turtle distribution
and dive behavior change with an extreme weather event.
Elsewhere, storm degraded habitats have possibly resulted
in shifts in loggerhead foraging areas [52]. During a marine heatwave, loggerheads moved into shallower regions
where the destruction of seagrass beds may have revealed
short-term access to new benthic forage [53]. Anthropogenic perturbations can also illicit direct or indirectchanges to sea turtle behavior. Multiple low-sample-sizestudies suggest the possibility that sound may trigger a response in turtles [54, 55]. Dredge operations were associated with changes in flatback sea turtle (Natator
depressus) distribution and dive behavior, possibly due tonoise impacts and changes to the benthos [56]. Seismic
activity, windfarm development, and marine recreation
may impact sea turtle distribution and dive behavior directly or through habitat alterations [54, 57–59]. The longterm, cumulative impacts of climate and anthropogenic
impacts on sea turtle behavior and distribution in the
MAB warrant consideration [57, 60] and may have legacy
effects [53] for sea turtle research and management.
Behavior

Loggerhead sea turtles overlap spatiotemporally with extreme weather events, and turtle dive behavior did not
return to pre-storm behavior within at least two weeks

Crowe et al. Movement Ecology(2020) 8:32

following a storm. The latitudinal displacement andchanges in loggerhead dive behavior are the consequences of either an acute perturbation, an alteration oflarger scale oceanographic conditions, or both. The behavioral changes observed in this study are an opportunistic look at neritic turtle behavior relative to ahurricane, and it is currently unclear what aspect of theenvironment (i.e. sound from increased wind, shifts inbarometric pressure, altered currents, lower SSTs, deepened thermocline, or disrupted prey fields) led to the observed behavior.
The turtles that left their foraging ranges moved south
earlier than would be expected from normal patterns of
seasonal movement, and earlier than the seasonal watercolumn cooling [7, 8, 26]. Hurricane Irene passed throughthe MAB at the end of August 2011 when there was still
more than a month of the foraging season remaining [26](Supplementary Fig. 2 Additional file 1), and more than amonth before the Cold Pool normally dissipates due tothe autumn turnover [7, 8]. Despite this, nearly half of theturtles in this study vacated their pre-storm foraging areas
and moved south by as far as 135 km after the hurricane—a distance that is nearly 25% of a typical southward migration to the coastal waters of North Carolina [26]. While in
the MAB, loggerheads usually exhibit seasonal homerange fidelity and occupy a SST thermal range between
18.2°–29.2°C [28]. Although the water temperatures
quickly cooled due to the storm, the turtles that remainedin their pre-storm foraging ranges did not experience
SSTs outside of typically occupied temperatures (Fig. 5).
Turtles that stayed in their foraging ranges took longer
dives after the hurricane. The difference in mean dive duration before and after the hurricane may not be biologically significant, but the increased range suggests that thestorm, and its impacts on the water column, may have
had an effect. The changes in dive duration observed withthe passing of the hurricane are similar to behavior
changes observed with seasonal decreases in SST [61].
Loggerhead behavior is likely sensitive to these changes inthermal conditions, as research has identified that a 2°C
difference in SST can alter dive behavior [62, 63]. Thesechanges in dive behavior could have been triggered by thetransformation of the entire water column, including thedecrease in SST [64], disruption of the thermocline, andthe weakening of the overall stratification [65].
The northward movements for most of the turtles during the hurricane aligned with the direction of the dominant along-shelf surface current associated with thestorm’s passing [10]. In the 12 h after the eye of Irene
passed the MAB, the current velocity at up to 20 m
depth was 0.4–0.8 m s-1 moving northward [10]. The
horizontal movement of loggerhead sea turtles in all life
stages are influenced by surface currents, either by physical mechanisms [66, 67] or by learned experiences [68].

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Smaller turtles that swim slower than currents are able
to influence their overall trajectory and survival successby purposeful alignment and short periods of active
swimming [67, 69–71]. Juvenile loggerheads are capableof escaping current patterns [69, 72], but powerful currents can alter the course of even a strong, adult turtle[73]. The movement north of most of the turtles in thisstudy during the hurricane could possibly be a tactic toconserve energy by purposeful alignment [69, 72, 74].
A shift in sea turtle distribution and diving behavior can
influence the calculations used in creating abundance estimates from aerial surveys, and abundance estimates thatassume constant sea turtle behavior through time may appear more accurate than they are [38, 75]. As other studies
have reported, neglecting the variability of environmentally influenced dive behavior can have substantial effects
on density estimates [75]. Analysis of visual survey datacollected after extreme weather events or other perturbations should consider that turtles may be triggered toleave an area and/or alter their dive patterns.
Animal-borne & weather buoy in-situ environmental
observations

Tagged turtles that remained in their foraging regions
during Hurricane Irene effectively recorded the SST drop
as well as the vertical mixing of the stratified MAB. The
water temperature data from the turtle tags were consistent with weather buoy and glider observations during thisperiod, but more spatially extensive than other oceanographic data sources [10]. Stratified environments arechallenging to model, and more data from in situ sources
are needed and being sought to improve hurricane forecasting in these types of regions [9, 11]. The ahead-of-eye
cooling is a characteristic of Atlantic hurricanes that comethrough the MAB during the stratified summer period[10], and this aspect has proven to be a major limiting factor to accurately model storms as well as prepare regions
for hurricane damage. We show in this study that turtleborne tags collect additional in situ data on the MAB during a time of year that is the perfect storm of turtle foraging season, stratification and formation of the Cold
Pool, as well as the Atlantic hurricane season.

Conclusions
Consistent with Patel et al. [11], turtle-borne data canprovide in situ oceanography data in the seasonallystratified MAB as loggerhead sea turtles observe the entire water column profile, including during extreme weather events. This study gave one example of how
loggerhead behavior and distribution changed during an
ecosystem perturbation, suggesting that we cannot assume consistency through time. Future analysis of turtle
behavior should consider the dynamic environments inwhich they live.

Crowe et al. Movement Ecology(2020) 8:32

Supplementary information

Page 11 of 13

Received: 3 April 2020 Accepted: 3 July 2020

Supplementary information accompanies this paper at https://doi.org/10.
1186/s40462-020-00218-6.
Additional file 1. Location source for tagged turtles and previously
observed proportions of tagged turtles in the Mid-Atlantic Bight by month.
Additional file 2. Interactive map of turtle tracks before, during, andafter Hurricane Irene.
Additional file 3. Location source for tagged turtles and previously
observed proportions of tagged turtles in the Mid-Atlantic Bight by month.

Abbreviations
cm: Centimeter; EDT: Eastern Daylight Time; Fig.: Figure; GPS: Global
positioning system; h: Hour; km: Kilometers; m: Meters; MAB: Mid-Atlantic
Bight; °N: Degrees North; n: Sample size; SCL: Straight carapace length;
SD: Standard deviation; SST: Sea Surface Temperature; T0: Time when theturtle is at its closest point to Hurricane Irene; USD: United States Dollars;°W: Degrees West; degrees C: Degrees; Celsius: Seconds
Acknowledgements
Thank you to the captains and crew at Viking Village Fisheries, and to thescientists on the cruises, particularly Eric Matzen. Thank you to Sean Hayes,
Mike Simpkins, and anonymous reviewers for their helpful comments that
improved the manuscript.
Authors’ contributions
HLH and RJS collected the data. SHP conceived of the original idea. JMH,
LMC, and SHP performed the data analysis. HLH, LMC, and SHP created thefigures. LMC wrote the initial draft of the manuscript in consultation with
HLH. All authors contributed to the design of the study, the interpretation of
the data, the final version of the manuscript, and approved the final
manuscript.
Funding
Turtle satellite tagging was made possible by funding from the Sea Scallop
Research Set Aside program (NA11NMF4540024) and by a US Department ofInterior, Bureau of Ocean Energy Management Inter-Agency Agreement(M10PG00075).
Availability of data and materials
Data generated and analyzed during this study are included in thispublished article [Additional file 3].
Ethics approval and consent to participate
This study meets the legal requirements of capturing, handling, andattaching satellite tags to loggerhead sea turtles in the United States under
Endangered Species Act Permits #1551 issued to the Southeast Fisheries
Science Center, #1576 issued to the Northeast Fisheries Science Center, and#14249 issued to the Coonamessett Farm Foundation.
Consent for publication
Not applicable.
Competing interests
The author(s) declare(s) that they have no competing interests.
Author details
1
Integrated Statistics under contract to the Northeast Fisheries Science
Center, National Marine Fisheries Service, National Oceanic and Atmospheric
Administration, 166 Water Street, Woods Hole, MA 02543, USA. 2Northeast
Fisheries Science Center, National Marine Fisheries Service, National Oceanicand Atmospheric Administration, 166 Water Street, Woods Hole, MA 02543,
USA. 3Coonamessett Farm Foundation, 277 Hatchville Road, East Falmouth,
MA 02536, USA.

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