Assessing Risks from Harbor Dredging to the Northernmost Population
of Diamondback Terrapins Using Acoustic Telemetry
T. Castro-Santos1,2
& M. Bolus2 & A. J. Danylchuk2
Received: 2 August 2017 /Revised: 28 September 2018 /Accepted: 1 November 2018
# This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright
protection 2018
Abstract
The northern diamondback terrapin (Malaclemys terrapin terrapin) is a saltmarsh-dependent turtle that occupies coastal habitats
throughout much of the Atlantic coast of North America. We used a novel application of acoustic telemetry to quantify both
mobility and occupancy of terrapins within a dredged harbor and surrounding habitats, and used these metrics to quantify relative
risk to individuals posed by harbor dredging. Terrapins showed strong fidelity to brumating areas within subdrainages, but
extensive movements between these zones during the active period. Activity was greatest in late spring and early summer,
declining to near zero by December. Occupancy of the dredge zone was also greatest during spring and summer and declined
throughout the autumn months to an annual minimum during winter. Taken together, these data indicate that risks from harbor
dredging are minimized during the autumn and early winter months.
Keywords Terrapin . Telemetry . Dredging . Brumation . Hibernation .Movement . Modeling . Risk . Assessment
Introduction
Coastal and estuarine environments accommodate a range of
human activities, including fisheries, aquaculture, recreation,
and transportation. These activities are supported by infrastruc-
ture, the maintenance of which can affect sensitive species that
inhabit these zones (Culloch et al. 2016;MoserandRoss 1995).
One such activity is harbor dredging. Harbors are typically
located in sheltered waterways, often with additional armoring
to protect anchorages and ports. This sheltered quality creates
an opportunity for sediments to accumulate, and harbors must
be dredged periodically to maintain navigability. Dredging
requires heavy equipment and the removal of large volumes
of sediment. It is highly disruptive to the environment and
esthetically unpleasant, interfering with economically and cul-
turally important activities such as boating, aquaculture, and
tourism. To minimize these effects, dredging is often undertak-
en during winter months, when human activities are reduced.
Dredging also poses several potential threats to wildlife,
including suspension of sediments (which may contain toxic
chemicals) and direct mechanical contact with the dredge
equipment (O’Donnell et al. 2007; Wilkens et al. 2015). One
species that is vulnerable to harbor dredging is the northern
diamondback terrapin (Malaclemys terrapin terrapin, hereaf-
ter referred to as Bterrapin^), a saltmarsh-adapted species that
occupies nearshore habitats along the East Coast of North
America (Brennessel 2006). Historic overharvest, combined
with fishery bycatch and habitat destruction, has caused many
populations to be extirpated, and the species is listed for pro-
tection in many states throughout its range (Butler et al. 2006;
Hart and Lee 2006). During winter months, terrapins enter a
period of dormancy known as brumation, during which they
aggregate and remain essentially immobile, buried in the ben-
thos (Brennessel 2006; Haramis et al. 2011; Yearicks et al.
1981). Given that coastal dredging also often occurs during
this period, there is the potential for considerable mortality of
terrapins that brumate within the dredge zone, prompting
management agencies to restrict dredging to summer months,
Communicated by Nathan Waltham
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s12237-018-0481-9) contains supplementary
material, which is available to authorized users.
* T. Castro-Santos
tcastrosantos@usgs.gov
1 USGS, Leetown Science Center–S.O. Conte Anadromous Fish
Research Center, One Migratory Way, Turners Falls, MA 01376,
USA
2 Department of Environmental Conservation, University of
Massachusetts Amherst, Amherst, MA 01003, USA
Estuaries and Coasts
https://doi.org/10.1007/s12237-018-0481-9
when the high level of activity presumably confers ability to
volitionally avoid dredging equipment.
The most northerly terrapin population resides in Wellfleet
Harbor, Massachusetts (USA), where the species is listed as
threatened under the Massachusetts Endangered Species Act
(MESA, MGL c131A). The harbor is a federal waterway and
municipal anchorage, both subject to periodic dredging, and
terrapins are regularly observed throughout the dredge zone.
Large breeding aggregations occur each spring in a cove ad-
jacent to the harbor, indicating that this is vital habitat for this
population, and raising concerns that brumation may be oc-
curring within the dredge zone.
While any mortality holds the potential to affect the popu-
lation, the magnitude of the threat posed by dredging depends
in part on which portion of the population is at risk. If dredg-
ing is performed during brumation, and if the dredge zone
comprises preferred brumation habitat, then dredging will
likely pose serious risks, both to individuals and to the local
population. The objective of this study was to use acoustic
telemetry to assess seasonality of risk from dredging by quan-
tifying rates of movement and occupancy of terrapins within
the dredge zone of Wellfleet Harbor. Our observations can
inform decisions on timing of dredging activity to minimize
risk to this threatened coastal species.
Methods
Study Area
Wellfleet Harbor is a protected harbor in Cape Cod Bay locat-
ed in the Town ofWellfleet, MA, USA (41° 55′ 48″N, 70° 01′
30″ W; Fig. 1). It is a Spartina spp. grass-dominated marsh
system, comprising several subdrainages with a mix of inlets,
rivers, and creeks. It has an extensive intertidal zone, with
regular tidal fluctuations of 3–4 m. The area of primary con-
cern was the harbor proper, which consists of the federal and
town anchorages (hereafter called the anchorage) and the main
navigation channel, all of which are dredged (Fig. 1). In addi-
tion to the anchorage, the study area also included each of the
primary subdrainages within the Wellfleet Harbor watershed.
Capture and Handling
Mature terrapins were collected during three distinct time pe-
riods to ensure that we characterized movement behaviors of a
representative sample of the population. We focused on mature
individuals, both to ensure that they were of sufficient size to
bear the mass of the tag, and also because impacts on mature
individuals are more likely to affect the population (Heppell
et al. 2000). The first and third collections were performed
during the mating aggregation in Chipman’s Cove (Duck
Creek, adjacent to the dredge zone) shortly after terrapins
emerged from brumation (April–May, 2011 and 2012). These
individuals were intended to provide information on whether
and to what extent terrapins brumated nearby, and to maximize
the likelihood of identifying individuals at risk if the dredge
zone proved to include important brumation habitat.
The second collection was performed during July, 2011,
and was intended to be representative of the entire population.
To that end, terrapins were captured in the tributaries (South of
Lt. Island (hereafter termed BWBWS^ or Bsanctuary^),
Blackfish Creek, Herring River, and Duck Creek). The July
collection occurred after their reproductive period, when ter-
rapins were dispersed throughout the watershed. The purpose
of this group was to help us to identify other brumation sites,
in the event that dispersal rates were low.
Transmitters and Tag Lots
Terrapins were tagged with acoustic transmitters (V9 coded
tags, 69 kHz; VEMCO Division, AMIRIX Systems Inc.,
Halifax, Nova Scotia, Canada). Tags were purchased in two
separate groups (Btag lots^). Each group had a distinct pro-
gramming scheme, intended to ensure maximum longevity,
and in particular to allow for documentation of onset of
brumation in each of 2 years for each tag. To achieve this, they
were programmed to transmit every 50–180 s (randomly dis-
tributed), and to have a dormant period during the first winter
following tagging. These were originally intended to be applied
during 2010 and 2011. However, owing to permitting restric-
tions, all tags were deployed during 2011 and 2012. This meant
that the first tag lot became dormant and re-activated later than
the initial study design intended, and only one brumation onset
event was observed for this tag lot (Tables 2 and 3).
Collection Methods and Transmitter Attachment
Terrapins were collected manually using dip nets.
Transmitters were attached to the first and second marginal
scutes to the left of the supracaudal scute (Fig. S1). Two small
holes were drilled through the scutes and the supporting der-
mal plate, through which were inserted small cable ties. Each
transmitter was secured with the cable ties and embedded in
epoxy (ACE Quick Set epoxy, Henkel AG & Co. KGaA,
40191 Düsseldorf, Germany). The epoxy was thickened with
colloidal silica (West Systems 406 Colloidal Silica Adhesive
Filler, West Systems, Bay City, MI, USA) and mixed with
black pigment (Evercoat Coloring Agent, Evercoat,
Cincinnati, OH, USA). This produced a smooth finished prod-
uct with no sharp edges to snag on vegetation and fishing gear,
and cryptic coloration which we hoped would reduce risk of
predation. To avoid biofouling on the transmitters and poten-
tial adverse effects on the animals, we coated the entire trans-
mitter package with anti-fouling paint (Interlux Micron CSC,
International Paint LLC, Union, NJ, USA). The tagging
Estuaries and Coasts
procedure was approved by the University of Massachusetts
Amherst IACUC (protocol 2011-0009). All captured terrapins
were sexed (Brennessel 2006), measured, weighed, and re-
leased at their point of capture.
Fixed-Receiver Array
We used an array of fixed-station receivers to monitor broad-
scale movements and distribution of terrapins. We deployed 20
submersible receivers (VR2W, VEMCO Division, AMIRIX
Systems Inc., Halifax, Nova Scotia Canada) throughout
Wellfleet Harbor during 2011, and 21 during 2012 and 2013
(Fig. 1; Tables 1 and 2). Receivers were placed to optimize our
ability to test key hypotheses regarding movement of terrapins
inWellfleet Harbor, and placement was consistent across years.
Themost important metrics concerned rates of occupancywith-
in the anchorage throughout the year, seasonal changes in mo-
bility (including onset of brumation), and fidelity to brumation
sites among years. The array was deployed in March and re-
trieved in January, which ensured complete coverage during the
active phase of the transmitters (Table 2).
Each receiver was attached to a 40-kg concrete mooring
using a buoy system that optimized its ability to detect passing
terrapins at any phase of the tidal cycle (Fig. S2). Receivers were
deployed in a series of Bgates^ (channel constrictions where a
swimming terrapin would have to pass through the detection
zone in order to pass the receiver) and Bnodes^ (distributed sites
within an area of interest) so that movement among detection
zones aswell as residency at key locations (e.g., brumation sites)
was documented. Maximum receiver detection ranges were
measured by deploying a range testing transmitter (V9, coded
tag range testing transmitter emitting at a 69 kHz signal, battery
life = 14 days, VEMCO Division, AMIRIX Systems Inc.,
Halifax, Nova Scotia, Canada) concentrically in all four cardinal
directions in 50-m increments (max = 600m) from each receiver
location (Selby et al. 2016). The maximum range at which a tag
was detected was assumed to represent the maximum detection
range for that receiver. Receivers were downloaded biweekly,
and on each download, clocks were synchronized with official
US Naval time, and any clock drift was corrected assuming a
linear rate of drift between downloads.
Temperature loggers (HOBO Pendant Temperature/Light
Data Logger 64 bit—UA-002-64, Onset, Pocasset, MA,
USA) were also deployed on four receivers (one each at the
mouths of Blackfish Creek (receiver 14), Herring River (re-
ceiver 3), and Duck Creek (receiver 9) as well as in the Main
Channel (receiver 11; Fig. 1). Loggers were configured to
record water temperature every 15 min.
Manual Tracking
We performed manual tracking from a variety of vessel types
to verify fixed-station observations and to identify exact loca-
tions of brumation sites of those terrapins we were able to
detect. Terrapins that remained stationary during multiple
scanning events were assumed to be brumating. Surveys
Fig. 1 Receiver deployment
locations in Wellfleet Harbor,
Wellfleet, MA (white area
indicates water). The map shows
the proposed dredging project
(stippled and striped area near the
breakwater), subdrainages
(labeled according to either the
legend or body of Table 1), and
receiver locations (numerals).
Receiver numbers are sized to
approximate the typical detection
range at each site
Estuaries and Coasts
began in October and were performed weekly as weather and
tides permitted. We used two receiver types for this: a Vemco
VR-100 (VEMCO Division, AMIRIX Systems Inc., Halifax,
Nova Scotia, Canada) and a Sonotronics USR-08
(Sonotronics, Tucson, AZ, USA). Both receiver types were
outfitted with directional and omni-directional hydrophones
and were able to decode all tags.
We established density of scanning transects based on de-
tection ranges of known brumating terrapins. Wind and tide
made it impossible to follow planned transects exactly, but this
detection range was used to establish a grid that was covered
throughout the dredge zone during each manual tracking ses-
sion. Thus, the individual transects scanned varied by session,
but were always designed to ensure a strong likelihood of
detecting tags that were present anywhere within the surveyed
zone. Similar methods were used outside the dredge zone, but
because of the importance of identifying any brumating terra-
pins within that zone, we concentrated our efforts there.
Data Management and Analysis
All data for this study were compiled in a relational Microsoft
Access database and analyzed using R statistical software (R
3.2.3; R Core Team 2014).
Occupancy and Movement
Vulnerability of terrapins was assessed by measuring both
occupancy of the dredge zone and mobility. Occupancy ad-
dresses when animals were present within the dredge zone,
Table 1 Locations of the 21
acoustic telemetry receivers
(latitude and longitude in decimal
degrees). Map ID refers to
numbers shown on Fig. 1; station
names are referred to throughout
the text. Subdrainages refer to the
four primary drainage areas in the
system (Herring River (HR),
Duck Creek (DC), Blackfish
Creek (BFC), Wellfleet Bay
Wildlife Sanctuary (WBWS)) or
various locations outside of these
drainages within Wellfleet Harbor
(WH). Receivers marked with an
asterisk (*) were affixed with a
temperature logger
Map ID
Station name
Subdrainage
Intertidal
Latitude
Longitude
1
Herring River 3
HR
Yes
41.931394
− 70.063555
2
Herring River 2
HR
Yes
41.930683
− 70.066383
3*
Herring River 1
HR
Yes
41.92375
− 70.056983
4
Great Island
WH
No
41.912694
− 70.060944
5
Jeremy Point
WH
No
41.89137
− 70.06682
6
Mooring Basin
DC
No
41.9284
− 70.033016
7
Anchorage
DC
No
41.926194
− 70.028194
8
The Cove
DC
Yes
41.922138
− 70.027277
9*
Duck Creek
DC
Yes
41.930133
− 70.024166
10
Railroad Bridge
DC
Yes
41.933861
− 70.027194
11
Channel 1
WH
No
41.922166
− 70.036388
12
Indian Neck 1
WH
No
41.91295
− 70.030616
13
Indian Neck 2
WH
No
41.912950
− 70.037236
14*
Blackfish 1
BFC
Yes
41.9029
− 70.012916
15
Fox Island
BFC
Yes
41.910277
− 70.014416
16
Pleasant Point
BFC
Yes
41.910116
− 69.995183
17
Loagy Bay
BFC
Yes
41.900111
− 70.005527
18
Lt. Island
WH
No
41.894333
− 70.02780
19
Sanctuary 2
WBWS
Yes
41.890055
− 70.00850
20
Sanctuary
WBWS
Yes
41.8876
− 69.99936
21
Eastham
WH
No
41.877983
− 70.020041
Table 2 Period of coverage for fixed receivers (Rx coverage) and tags.
Date on and Date off indicate expected on-off cycles, based on manufac-
turer’s programming. First detection and Last detection indicate actual
observations, and are presented as median (range). Note that some tags
were detected before their programmed activation date—evidently arising
from a manufacturing defect in programmed on/off times
Tag lot
Date on
Date off
First detection
Last detection
Rx coverage
1
02 Jun 2011
3 Jan 2012
25 May 2011 (24 May–15 Jun)
18 Oct 2011 (13 Jul–25 Dec)
18 Mar 2011–10 Jan 2012
2
04 Jul 2011
18 Dec 2012
19 Jul 2011 (5 July–14 Aug)
05 Oct 2011 (12 Sep–15 Nov)
1
01 Jun 2012
06 Aug 2012 (expired)
23 May 2012 (16 Apr–24 May)
05 Aug 2012 (15 Jun–27 Aug)
20 Mar 2012–07 Jan 2013
2
18 Apr 2012
18 Dec 2012
25 Apr 2012 (18 Apr–13 May)
09 Oct 2012 (01 Jun–18 Dec)
2
19 Apr 2013
13 Jul 2013 (expired)
29 Apr 2013 (9 Apr–25 Jul)
01 Jul 2013 (28 Apr–02 Aug)
19 Mar 2013–02 Aug 2013
Estuaries and Coasts
and so vulnerable to equipment; mobility addresses the ability
of terrapins to actively avoid the dredge, given that they be
present during operations.
Occupancy of the anchorage and dredge zone was mea-
sured as the proportion of available active tags detected within
the Duck Creek subarray. This included all receivers deployed
from the mouth of Duck Creek (receiver 10) out to the break-
water, including the entire dredge zone (Fig. 1) on each day of
the study.
Movement was considered an indicator of each animal’s
Bmobility^ (and by association its ability to avoid dredge
equipment), and was measured by identifying transitions in
detections between receivers within the Duck Creek system.
Transitions were determined based on occupancy events with-
in the detection zone of each receiver. We applied time-to-
event techniques, whereby the log density function of interval
durations between detections at each receiver were used to
identify times when terrapins entered and left each detection
zone (Castro-Santos and Perry 2012).
The density of receivers within the Duck Creek subarray
meant that it was possible to discern movements throughout
the subdrainage. Data from all receivers were combined, and
any detections occurring within 20 s of each other on two or
more receivers were identified, retaining only the first of
these detections and assigning the location to that receiver.
These simultaneous detections were very rare, comprising <
0.1% of the total detections. More commonly, there was a
gap between detections as terrapins moved around the har-
bor, passing among the detection zones of the array; > 95%
of all new detections were separated by > 1 transmission
interval. Taken together, the low incidence of simultaneous
detections combined with successive receivers typically be-
ing separated by more than one transmission interval sug-
gests that any error associated with animals occupying over-
lapping zones must be trivial, and that successive detections
at distinct receivers represented actual movements of ani-
mals among the receivers in the array. Distance between
receivers was known, and at each transition, an individual
animal was assigned this distance minus 300 m (the average
radius of one receiver’s detection range). This provided a
conservative estimate of movement distance, balancing con-
siderations of detection range, detection probability, trans-
mission rate, and rate of movement of the turtles, and as-
suming a straight-line path between receivers. In reality,
movement paths are rarely truly straight, and so, actual
movement was probably greater that what we estimate using
this method. The transition distances were then summed for
each detected terrapin on each day, and median daily values
were then calculated based on all detected animals. Note that
by using only receivers within the Duck Creek drainage, this
also provides a conservative measure of mobility. Since
most movements occurred within drainages, however, and
because we used the median value, influence of extreme
values was minimized, providing a conservative but realistic
index of movement.
Loess smooth functions were fitted to both the occupancy
and movement data, providing a continuous estimate of aver-
age occupancy and movement by terrapins throughout the
year. Means and 95% confidence intervals were calculated
for both metrics.
Combined Risk
The exposure risk was assumed to be directly proportional to
the probability of being present within the dredge zone on a
given date. We therefore used the untransformed occupancy
metric described above as a direct index of risk (Ro):
Ro ¼ P Occupancy
ð
Þ
ð1Þ
where P (Occupancy) ∈[0, 1] is the proportion of the popula-
tion present in the dredge zone on a given day of the year as
estimated by the loess smooth.
Next, we produced an index of relative mobility risk (Rm):
Rm ¼ 1− Md
Mmax
ð2Þ
whereMd is the median observedmovement on a given day
and Mmax is the annual maximum of these values. Values for
Rm range from 0 to 1, with 0 being associated with the day of
greatest mobility and 1 associated with the day of least mobil-
ity within a given year. Thus, brumating terrapins experience
the greatest mobility-related risk, and this risk is minimized on
the day of greatest activity.
Values used for calculating both Ro and Rm were taken from
the among-years loess smooth. Combined risk exposure (RT)was
then calculated as the product of occupancy and mobility risks:
RT ¼ Ro  Rm
ð3Þ
Results
Capture and Handling
Seventy-five terrapins (56 females and 19 males) were tagged
during the 2011 field season (Table 3). Of these, 30 females
and 19 males comprised the spring collection from the pro-
posed dredging area (Table 2; Fig. 1). Twenty-six terrapins
were also tagged, distributed throughoutWellfleet Harbor dur-
ing July (Table 3). During this second period, no males were
captured that were large enough to tag. Instead, all transmitters
were attached to mature females.
An additional 25 terrapins (13 females and 12 males) were
tagged during the 2012 mating aggregation (Table 3). Thus,
74 of 100 terrapins were captured within the anchorage area.
Estuaries and Coasts
By concentrating our collections near the dredge zone, we
expected the observed proportion of brumating terrapins with-
in this zone to overestimate their representation in the larger
population. In this way, we ensured that assessments of occu-
pancy risk were conservative, i.e., biased in favor of detecting
occupancy when it occurred.
Females were larger and more variable in size than males.
Mean and standard deviations of straight carapace length and
in-air mass of females were 18.4 ± 1.3 cm and 1071 ± 224 g;
of males, they were 12.3 ± 0.4 cm and 280 ± 27 g. There was
no difference in size or mass between years within sexes (p-
> t > 0.3 in all cases). All terrapins were held overnight and
released within 18–30 h of capture. They all swam away once
released; no abnormal or disoriented behavior was observed.
The total transmitter package weighed 9 g in air, or
0.84% ± 18% of the average body mass of females and
3.21% ± 0.31% of the average body mass of males; on no
individual did it exceed 3.7% of the body mass. Most tags
activated and deactivated within a day of their programmed
dates. Some drift in these settings did occur, however with at
least one tag activating at least 10 days before its programmed
date (Table 2; Fig. S3).
Receiver Array
Receivers performed well throughout the deployment period
(Table 2). Tested detection ranges ranged from 117 to 602 m
(mean = 421 m), and varied with tide and bathymetry. Range
testing was typically performed within 2 h of high tide, and so,
these represent maximum values. At low tide and shallow
conditions, these ranges were reduced, with periods (< 2 h)
of zero efficiency for receivers in the intertidal zone
(Table 1). Thus, the 300-m detection ranges used for calculat-
ing relative movement over the course of the study were ap-
propriate, given the available information.
Mobility
Terrapins were active during the entire period of telemetry
coverage (April–December: Fig. 2). Total movement had little
relationship to water temperature (Figs. 2 and S4; Kendall’s
tau = 0.056). Instead, activity was greatest in mid-May, with
median movement values of about 2 km/day. This
corresponded with the breeding period of this population.
Table 3 Numbers and location of terrapin captures. Capture locations
are abbreviated as CC (Chipman’s Cove), BFC (Blackfish Creek), DC
(Duck Creek), WBWS (Wellfleet Bay Wildlife Sanctuary—actually in-
cludes marshes and beaches south of Lt. Island), and HR (Herring River).
Anchorage refers to the federal and town dredge zones, adjacent to
Chipman’s Cove
Date
Tag lot
Capture location
Females Males
Total
May 2011
1
CC, anchorage
30
19
49
July 2011
2
WBWS
8
0
8
2
HR
8
0
8
2
BFC
8
0
8
2
CC, anchorage
2
0
2
May 2012
2
CC, anchorage
13
12
25
Total
69
31
100
0
2000
4000
6000
8000
Apr
Jul
Oct
Jan
Date
Median Distance (m)Year
2011
2012
2013
Fig. 2 Median known distance traveled per day by detected terrapins. Points represent median for a given day on a given year. The loess smooth averages
across years
Estuaries and Coasts
There was a slight decrease in movement in mid-summer,
which corresponded with the female nesting season, followed
by another broad peak from August to October, where the
median movement was about 1.8 km/day. Movement then
began to decrease until reaching a minimum in December,
shortly before the tags shut down for the winter. By
December 1, it became common for entire days to pass with-
out any observed movement between receivers (Fig. 2).
Occupancy and Brumation
Because the tags became active in late April or later (Table 2),
it is not possible to estimate actual dates of emergence and
onset of activity. The fixed array, however, provides some
insights into this. In both 2012 and 2013, many terrapins were
already active on the date that the tags turned on (Fig. S3).
Dates of last detection in the fall do not correspond with re-
duced activity. Median dates of last detection were 30
September (2011) and 3 October (2012), with no difference
between sexes (Kruskal-Wallis, p > 0.57 in both years).
Although it is tempting to infer from this that brumation had
begun, those terrapins that were detected after these dates
continued to be highly active, and it is likely that the absence
of detections instead indicates that the terrapins had moved
elsewhere in the system, away from the anchorage and the rest
of the fixed-receiver array.
This Bdeparture hypothesis^ is supported by the occupancy
data (Fig. 3; Table 4). Occupancy in the anchorage was greatest
during the May breeding aggregation (58% of tagged terrapins
being present on any given day (%/day)), with another strong
plateau inmidsummer, with about 45%/day. Occupancy declined
rapidly from late August– to September. By October 1, only
about 20% of the population occupied the dredge zone, and this
proportion continued to decline until most movement ceased in
December. It is possible that as movement declined, some terra-
pins might have been present but undetected because they occu-
pied zones outside the detection radius of the receivers. Any
associated error in the occupancy estimate appears to be negligi-
ble, however: in each year, eight individuals were detected in the
anchorage using manual tracking, corresponding to 11% of
tagged terrapins in 2011 and 8% in 2012. This is consistent with
the smoothed occupancy estimate (Fig. 3).
Data from the larger receiver array supports the interpreta-
tion that most terrapins left the anchorage for the winter. Of
128 last fixed-receiver detections in 2011 and 2012, 97%were
within creeks, with only four at open water receivers (Table 4,
Fig. S5; see also Table 1 and Fig. 1). The distribution of the
last date of detection was broadly distributed among the four
major drainages within the Wellfleet Harbor estuary (mean ±
SD number of individuals per drainage were 18 ± 3 in 2011
and 12 ± 2 in 2012), suggesting a pattern of dispersal, rather
than aggregation.
0.0
0.3
0.6
0.9
Apr
Jul
Oct
Jan
Date
ProportionYear
2011
2012
2013
Fig. 3 Mean proportion of tagged terrapins detected within the dredge
zone. Data from each year are indicated by dots. The loess smooth
represents the mean across years. The shaded area is the 95%
confidence interval for this mean. Note the consistent aggregation that
occurs in May of each year. This appears to correspond with the known
mating aggregation that occurs at that time. This is followed in each year
by a departure (perhaps reflecting nesting activity) but then by a
subsequent return to the dredge zone in late June, which persists until
mid-August. From mid-August through September, there is a dramatic
exodus, with about half of the terrapins leaving the Duck Creek
subdrainage. The remaining terrapins stay within the subdrainage until
early November, when they also begin to leave. By December, nearly all
of the terrapins have left the subdrainage, with only about 5% detected on
any given day
Estuaries and Coasts
We also observed evidence of interannual, creek-specific
fidelity in selection of fall and winter habitat. Of the 26 terra-
pins that carried active tags through December of both 2011
and 2012 (Table 2), 23 individuals (88%) were last detected
by fixed receivers after September 1 in both years.Of these, all
but one were last detected in the same subdrainage in both
years, most of them being detected on the same receiver as
on the previous year (Fig. 4). We observed a similar pattern
with emergence. During the spring emergence events of 2012
and 2013, terrapins were typically detected in the same drain-
age as their last detection (Fig. S6). Notably, however, there
were several first detections outside of the drainages where
they had been last detected the previous fall, and nearly all
of these occurred within the zone between the breakwater and
Duck Creek. Because tags from tag lot 1 were dormant from
January to May, and from December to April for tag lot 2
(Tables 2 and 3), it was not possible to determine with certain-
ty when this movement occurred. By comparing the distribu-
tions of last vs. first detections, however, it is possible to infer
that activity had already begun by mid-April, making it more
likely that those movements that were observed occurred in
the early spring, before tag re-activation (Fig. S3).
Most terrapins occupied habitat outside the anchorage dur-
ing the fall and winter periods. Combined risk from occupan-
cy and mobility restrictions was calculated by multiplying
occupancy (Fig. 3; Eq. 1) by the transformed mobility risk
(Fig. 2, Eqs. 2 and 3). The results indicate that a tradeoff exists
between the two risk metrics: Occupancy is greatest at the
same time that mobility is near its peak, resulting in a mini-
mum combined risk occurring both during the spring period
and again during the fall (Fig. 5). The low risk in spring is
Table 4 Relationship between capture and brumation sites in 2011 and
2012. Data are presented as n (proportion of population captured within
that subdrainage). Subdrainage labels are defined in Table 1. Note that a
substantial proportion of terrapins captured within the Duck Creek
watershed distribute throughout the harbor, while those caught outside
of Duck Creek tend to brumate within the subdrainage where they were
captured
Subdrainage
Year
Capture
Brumation
2011
2012
BFC
BFC
5
(0.63)
4
(0.67)
DC
0
(0.00)
0
(0.00)
HR
0
(0.00)
1
(0.17)
WBWS
3
(0.38)
1
(0.17)
WH
0
(0.00)
0
(0.00)
DC
BFC
11
(0.22)
6
(0.23)
DC
23
(0.45)
14
(0.54)
HR
8
(0.16)
2
(0.08)
WBWS
6
(0.12)
1
(0.04)
WH
3
(0.06)
3
(0.12)
HR
BFC
0
(0.00)
0
(0.00)
DC
0
(0.00)
0
(0.00)
HR
8
(1.00)
7
(1.00)
WBWS
0
(0.00)
0
(0.00)
WH
0
(0.00)
0
(0.00)
WBWS
BFC
1
(0.13)
1
(0.13)
DC
0
(0.00)
0
(0.00)
HR
0
(0.00)
0
(0.00)
WBWS
7
(0.88)
7
(0.88)
WH
0
(0.00)
0
(0.00)
2011
H
e
rrin
g
R
ive
r 3
H
e
rrin
g
R
ive
r 2
H
e
rrin
g
R
ive
r 1
Gre
a
t
Isla
nd
Je
re
m
y Po
in
t
M
o
o
rin
g
Ba
sin
An
ch
o
ra
g
e
Th
e
C
o
ve
D
u
ck C
re
e
kR
a
ilro
a
d
Brid
ge
C
h
a
n
n
e
l
1
In
d
ia
n
N
e
ck 1
In
d
ia
n
N
e
ck 2
Bla
ckfish
1
Fo
x I
sla
n
d
Ple
a
sa
n
t
Po
in
t
L
o
a
g
y BayL
t.
I
sla
nd
Sa
n
ctu
a
ry 2
Sa
n
ctu
a
ryE
a
sth
a
m
2012Herring River 3
Herring River 2
Herring River 1
Great Island
Jeremy Point
Mooring Basin
Anchorage
The Cove
Duck Creek
Railroad Bridge
Channel 1
Indian Neck 1
Indian Neck 2
Blackfish 1
Fox Island
Pleasant Point
Loagy Bay
Lt. Island
Sanctuary 2
Sanctuary
Eastham
# Observations
1
2
3
4
Fig. 4 Correlation between years
of last receiver detection
locations. Dashed rectangles
delineate the four primary
subdrainages (Fig. 1)
Estuaries and Coasts
driven by mobility, and in the fall by reduced occupancy. Any
terrapins that remain in the anchorage after late November are
assumed to be at high mortality risk, owing to their limited
mobility. Although a small proportion of the population did
remain near the anchorage at this time in both years, their
locations fell primarily outside of the dredge zone (Fig. S7).
Nevertheless, across the 2 years, three individuals were last
detected within the dredge zone. The combined data thus in-
dicate that a prolonged period of reduced risk exists from
September to December, and probably through much of the
winter. Nevertheless, there is a small but significant risk to
individuals during the winter months.
Discussion
Data from this study provide a useful gauge to infer risk from
harbor dredging, but the implications go beyond this. Risks
from other activities can also be inferred, along with associat-
ed seasonality, etc. The study has also shown some interesting
patterns that shed light more generally on the movement ecol-
ogy of this species. The tagged terrapins were highly mobile,
in some cases traveling several kilometers in a single day.
They actively moved between creeks, although this move-
ment appeared to be primarily restricted to spring and summer
months, and they exhibited strong fidelity to wintering habitat.
This fidelity puts them at some risk from catastrophic events
(e.g., severe weather, chemical spills, etc.)—a brumating pop-
ulation that is locally extirpated may take considerable time to
recover (Tucker et al. 2001). The evidence suggests, however,
that the Wellfleet population is widely distributed throughout
the available habitat, and there does not appear to be a single
site that would render the population vulnerable to such an
event. These observations differ from previous studies in that
although other authors have described strong within-creek site
fidelity, movements among creeks have been thought to be
rare (Muehlbauer 1987; Gibbons et al. 2001; Tucker et al.
2001; Harden et al. 2007). Some of this difference, however,
may be an artifact of the techniques used. By continuously
monitoring movement with a fixed-receiver array, we were
able to identify movements that can be missed using other
mark-recapture techniques, and our observations may just be
the result of improved resolution offered by acoustic teleme-
try. Regardless, we did observe strong between-year fidelity to
0.00
0.25
0.50
0.75
1.00
Apr
Jul
Oct
Jan
Date
Relative Daily RiskFig. 5 Three risk components, showing total risk scale. Occupancy
risk (Ro. Eq. 1; dashed curve) is the proportion of known terrapins in
the dredge zone and is on the same scale as in Fig. 3. Mobility
risk (Rm Eq. 2; dash-dot) was calculated from the loess smooths for
each year of data shown in Fig. 2 (Mmax = 2416m/day; Eq. 2). Combined
risk (RT Eq. 3) is the product of occupancy andmobility components, and is
shown by a solid black curve
Estuaries and Coasts
creeks during the fall months, which is consistent with other
studies.
In other ways, however, our observations were similar to
previous studies. For example, we were unable to find and
capture males during the summer months. Roosenburg et al.
(1999) described within-creek habitat partitioning by sex and
size, with larger mature females using more open, deep water
habitats in contrast to the males and juvenile females using
upper marsh habitats. Such sex-based partitioning might ex-
plain our inability to capture males in summer. The fixed-
station data did not show clear evidence of this, however; in
our study, both sexes occupied open water areas, moving to
the upper intertidal zones in late summer and early fall. Other
authors have described age-dependent variability in location
of brumacula (brumation sites), with adults remaining in the
intertidal zone, either on top of the substrate, under scarred-out
banks, or buried in mud, frequently in aggregations of several
individuals (Haramis et al. 2011; Yearicks et al. 1981).
Hatchlings, juveniles, and subadult terrapins often overwinter
terrestrially, buried under the soil or dense vegetation above
mean high water line (Lawler andMusick 1972; Muldoon and
Burke 2012; Pitler 1985). We did not observe these patterns;
however, we specifically targeted adult individuals in this
study. If demographic segregation is occurring, it is likely to
be happening primarily within the upper intertidal zone or
above, in locations where we were unable to monitor.
High levels of gene flow are common among terrapin pop-
ulations. Published data suggest that there is a tendency towards
male-biased dispersal, with limited genetic separation by dis-
tance (Hauswaldt and Glenn 2005; Sheridan et al. 2010). Our
collection data suggest that some sex-based habitat partitioning
did occur. More work is needed to determine the extent of this
partitioning, and whether this is typical of the species or if it
reflects a unique characteristic of this population.
It is unclear why the terrapins congregate in the harbor
during summer months. Interestingly, this is the period of
greatest human activity within the harbor. Also during this
period, ground tackle (moorings, floats, etc.) is deployed
throughout the anchorage. This gear creates a reef effect, with
abundant invertebrate communities that may serve as forage
for terrapins (Tucker et al. 1995). This equipment is removed
in the winter to prevent ice damage—if terrapins are attracted
to this structure in summer, its absence in winter might help to
explain the timing of the fall exodus. Comparable studies per-
formed at lower latitudes where ground tackle remains in
place throughout the year might yield different results. In
any event, it is evident that activity within the harbor does
not repel terrapins, which calls into question the assumption
that they would actively avoid a dredge should that activity
occur during summer (Brennessel 2006; Cecala et al. 2009).
Further, the summer occupancy of this zone suggests that any
activity that did repel them might constitute harm to the pop-
ulation through deprivation of access to vital resources.
Adequacy of the Approach
We applied a movement-theoretic approach to quantifying
movement and occupancy. By analyzing the log-linear rela-
tionship between the density function of the intervals between
detections, we were able to differentiate between departures
from receivers and the missed detections associated with im-
perfect detection efficiency and movements near the periphery
of receiver detection zones (Castro-Santos and Perry 2012).
This approach recognizes the mixed distribution nature of
movement data (Langton et al. 1995), and is an improvement
over techniques that apply arbitrary thresholds to these inter-
vals (e.g., Andrews and Quinn 2012; Chamberlin et al. 2011;
Rohde et al. 2013). This approach, combined with a dense
array of receivers, provided near-continuous monitoring of
movements within the system of interest.
By combining occupancy and mobility, we were able to
produce a reasoned estimate of how these two factors combine
to produce total risk. The occupancy component of the model
is robust, biased only by the deliberately disproportionate
number of terrapins collected within the zone of interest.
The interannual fidelity raises concerns that portions of the
population that are impacted might be slow to re-colonize
(Tucker et al. 2001). These data were for last observations
on fixed receivers, however, which we have shown did not
correspond with cessation of movement or actual locations of
brumation. Instead, brumation appears to occur further up the
intertidal zone within the creeks. Furthermore, the anchorage
had the lowest level of interannual fidelity, suggesting that any
disturbance in this area would represent low risk to the popu-
lation. A less biased study would have selected terrapins from
throughout the harbor. However, given that the aggregation
appears to draw from the entire population, the actual bias
may be small, and the results are conservative.
The other source of bias in our risk assessment comes from
the assumption that there is zero risk when terrapins are max-
imally mobile and 100% risk when they are dormant. While it
is likely true that a dormant terrapin would not be able to avoid
a dredge, the dredge would have to be at the same site, and if
the brumation location does not co-occur with the dredge, then
the risk to the dormant animal is overestimated using our
approach. Conversely, the risk may be underestimated to the
extent that terrapins are unable to avoid the dredge when max-
imally active. Furthermore, we assume that the greatest dis-
tance traveled corresponds with greatest ability to avoid the
dredge. At the time of greatest movement in late May, the
water temperature ranged from 15 to 20 °C. Mean daily tem-
peratures reached as high as 25 °C in the summer, however.
Terrapins are ectotherms, and performance tends to increase
with temperature. This relationship is not linear though, and
for many species, the greatest scope for activity occurs at
temperatures below the maximum environmental temperature
that they are likely to encounter (Brett and Glass 1973;
Estuaries and Coasts
Peterson et al. 1990). More work is needed to better under-
stand the relationship between temperature and avoidance per-
formance of terrapins. Still, it is important to recognize that the
increased metabolic costs associated with activity during ele-
vated temperatures often induce a state of reduced activity,
meaning that it is possible for terrapins to be at greater risk
from both exposure and mobility during the summer months.
Given the data, it is possible to gauge the effect of any
error that might exist in our approach. First, if some vul-
nerability exists even during maximum activity, then the
combined outcome would increase the expected risk dur-
ing spring and summer. The fall/winter predictions would
be relatively unaffected, indicating that the same period
would still constitute the optimum period for risk minimi-
zation. This same logic applies to any reduction in protec-
tion from avoidance performance: If we are willing to as-
sume that a dormant terrapin has zero avoidance ability, the
general shape of the relationship will remain unchanged,
with increased benefits accruing to performing dredging
during fall and winter.
In conclusion, the data compiled in this study provide
strong evidence that risk to the Wellfleet Harbor population
of diamondback terrapins is minimized during late fall
through early winter. The approach described here could read-
ily be applied to other species and environments, and holds
promise as a conservation tool for sensitive populations.
Acknowledgements Many people and organizations made important
contributions to this project. Special thanks to Bob Prescott and the staff
of the Massachusetts Audubon’s Wellfleet Bay Wildlife Sanctuary; Dr.
Barbara Brennessel of Wheaton College; and Michael Flanagan and the
staff of the Town of Wellfleet Harbormaster’s Office. These individuals
and groups provided key resources and guidance, without which the
project would have been impossible. We also thank agency staff for pro-
viding guidance and insights into the management context for the study,
including Eve Schluter, KevinMooney, and the staff of theMassachusetts
Department of Conservation and Recreation and the Natural Heritage and
Endangered Species Program, as well as Todd Randall and Craig Martin
(US Army Corps of Engineers). This project was funded by a grant from
the Massachusetts Department of Conservation and Recreation
Waterways Grant (Project # P11-2660-G01 (3803-G)), the University of
Massachusetts Amherst, Department of Environmental Conservation, the
Diamondback Terrapin Working Group, and Zoar Outdoor (Charlemont,
MA). A.J. Danylchuk is supported by the National Institute of Food &
Agriculture, U.S. Department of Agriculture, the Massachusetts
Agricultural Experiment Station and Department of Environmental
Conservation. Any use of trade, product, or firm names is for descriptive
purposes only and does not imply endorsement by the U.S. Government.
References
Andrews, K.S., and T.P. Quinn. 2012. Combining fishing and acoustic
monitoring data to evaluate the distribution and movements of spot-
ted ratfish Hydrolagus colliei. Marine Biology 159 (4): 769–782.
Brennessel, B. 2006. Diamonds in the marsh: A natural history of the
diamondback terrapin. Hanover: University Press of New England.
Brett, J.R., and N.R. Glass. 1973. Metabolic rates and critical swimming
speeds of sockeye salmon (Oncorhynchus nerka) in relation to size
and temperature. Journal of the Fisheries Research Board of
Canada 30 (3): 379–387.
Butler, J.A., G.L. Heinrich, and R.A. Seigel. 2006. Third workshop on the
ecology, status and conservation of diamondback terrapins
(Malaclemys terrapin): results and recommendations. Chelonian
Conservation and Biology 5 (2): 331–334.
Castro-Santos, T., and R.W. Perry. 2012. Time-to-event analysis as a
framework for quantifying fish passage performance. In Telemetry
Techniques, ed. N.S. Adams, J.W. Beeman, and J. Eiler, 427–452.
Bethesda: American Fisheries Society.
Cecala, K.K., J.W. Gibbons, andM.E. Dorcas. 2009. Ecological effects of
major injuries in diamondback terrapins: implications for conserva-
tion and management. Aquatic Conservation-Marine and
Freshwater Ecosystems 19 (4): 421–427.
Chamberlin, J.W., A.N. Kagley, K.L. Fresh, and T.P. Quinn. 2011.
Movements of yearling Chinook salmon during the first summer
in marine waters of Hood Canal, Washington. Transactions of the
American Fisheries Society 140 (2): 429–439.
Culloch, R.M., P. Anderwald, A. Brandecker, D. Haberlin, B.McGovern,
R. Pinfield, F. Visser, M. Jessopp, and M. Cronin. 2016. Effect of
construction-related activities and vessel traffic on marine mam-
mals. Marine Ecology Progress Series 549: 231–242.
Gibbons, J.W., J.E. Lovich, A.D. Tucker, N.N. Fizsimmons, and J.L.
Greene. 2001. Demographic and ecological factors affecting conser-
vation and management of diamondback terrapins (Malaclemys
terrapin) in South Carolina. Chelonian Conservation and Biology
4: 66–74.
Haramis, G.M., P.P.F. Henry, and D.D. Day. 2011. Using scrape fishing to
document terrapins in hibernacula in Chesapeake Bay.
Herpetological Review 42: 170.
Harden, L.A., N.A. Diluzuzio, J.W. Gibbons, and M.E. Dorcas. 2007.
Spatial and thermal ecology of the diamondback terrapin
(Malacelmys terrapin) in a South Carolina salt marsh. Journal of
the North Carolina Academy of Sciences. 123: 154–162.
Hart, K.M., and D.S. Lee. 2006. The diamondback terrapin: the biology,
ecology, cultural history, and conservation status of an obligate es-
tuarine turtle. Studies in Avian Biology 32: 206–213.
Hauswaldt, J.S., and T.C. Glenn. 2005. Population genetics of the dia-
mondback terrapin (Malaclemys terrapin). Molecular Ecology 14
(3): 723–732.
Heppell, S.S., H. Caswell, and L.B. Crowder. 2000. Life histories and
elasticity patterns: perturbation analysis for species with minimal
demographic data. Ecology 81 (3): 654–665.
Langton, S.D., D. Collett, and R.M. Sibly. 1995. Splitting behavior into
bouts—a maximum-likelihood approach. Behaviour 132 (9): 781–
799.
Lawler, A.R., and J.A. Musick. 1972. Sand beach hibernation by a north-
ern diamondback terrapin, Malaclemys terrapin terrapin (Schoepff).
Copeia 1972 (2): 389–390.
Moser, M.L., and S.W. Ross. 1995. Habitat use and movements of
shortnose and Atlantic sturgeons in the Lower Cape-Fear River,
North-Carolina. Trans. Am.Fish.Soc. 124 (2): 225–234.
Muehlbauer, E. (1987). Field and laboratory studies of tidal activity in the
turtle Malaclemys terrapin terrapin. Thesis New York University.
New York, New York. USA. PhD thesis, New York University.
Muldoon, K.A., and R.L. Burke. 2012. Movements, overwintering, and
mortality of hatchling diamond-backed terrapins (Malaclemys terra-
pin) at Jamaica Bay, New York. Canadian Journal of Zoology-
Revue Canadienne de Zoologie 90 (5): 651–662.
O’Donnell, K.P., R.A. Wahle, M. Bell, and M. Dunnington. 2007.
Spatially referenced trap arrays detect sediment disposal impacts
on lobsters and crabs in a New England estuary. Marine Ecology
Progress Series 348: 249–260.
Estuaries and Coasts
Peterson, C.C., K.A. Nagy, and J. Diamond. 1990. Sustained metabolic
scope. Proceedings of the National Academy of Sciences of the
United States of America 87 (6): 2324–2328.
Pitler, R. 1985. Malaclemys terrapin terrapin (northern diamondback ter-
rapin) behavior. Herpetological Review 16: 82.
R Core Team. 2014. R: A language and environment for stattistical com-
puting. (3.1.1). Vienna: R Foundation for Statistical Computing.
Rohde, J., A.N. Kagley, K.L. Fresh, F.A. Goetz, and T.P. Quinn. 2013.
Partial migration and diel movement patterns in Puget Sound Coho
Salmon. Transactions of the American Fisheries Society 142 (6):
1615–1628.
Roosenburg, W.M., K.L. Haley, and S. McGuire. 1999. Habitat selection
and movements of diamondback terrapins, Malaclemys terrapin, in
a Maryland estuary. Chelonian Conservation and Biology 3: 425–
429.
Selby, T.H., K.M. Hart, I. Fujisaki, B.J. Smith, C.J. Pollock, Z. Hillis-
Starr, I. Lundgren, and M.K. Oli. 2016. Can you hear me now?
Range-testing a submerged passive acoustic receiver array in a
Caribbean coral reef habitat. Ecology and Evolution 6 (14): 4823–
4835.
Sheridan, C.M., J.R. Spotila, W.F. Bien, and H.W. Avery. 2010. Sex-
biased dispersal and natal philopatry in the diamondback terrapin,
Malaclemys terrapin. Molecular Ecology 19 (24): 5497–5510.
Tucker, A.D., N.N. Fitzsimmons, and J.W. Gibbons. 1995. Resource
partitioning by the estuarine turtle Malaclemys terrapin—trophic,
spatial, and temporal foraging constraints. Herpetologica 51: 167–
181.
Tucker, A.D., J.W. Gibbons, and J.L. Greene. 2001. Estimates of adult
survival and migration for diamondback terrapins: conservation in-
sight from local extirpation within a metapopulation. Canadian
Journal of Zoology 79 (12): 2199–2209.
Wilkens, J.L., A.W. Katzenmeyer, N.M. Hahn, J.J. Hoover, and B.C.
Suedel. 2015. Laboratory test of suspended sediment effects on
short-term survival and swimming performance of juvenile
Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus, Mitchill,
1815). Journal of Applied Ichthyology 31 (6): 984–990.
Yearicks, E., R.Wood, andW. Johnson. 1981. Hibernation of the northern
diamondback terrapin, Malaclemys terrapin terrapin. Estuaries 4
(1): 78–80.
Estuaries and Coasts