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RESEARCH ARTICLE
S. G. Wilson ÆM. E. Lutcavage ÆR. W. Brill
M. P. Genovese ÆA. B. Cooper ÆA. W. Everly
Movements of bluefin tuna (
Thunnus thynnus
) in the northwestern
Atlantic Ocean recorded by pop-up satellite archival tags
Received: 16 April 2004 / Accepted: 25 June 2004 / Published online: 2 September 2004
Springer-Verlag 2004
Abstract Pop-up satellite archival tags were implanted
into 68 Atlantic bluefin tuna (Thunnus thynnus
Linnaeus), ranging in size from 91 to 295 kg, in the
southern Gulf of Maine (n=67) and off the coast of
North Carolina (n=1) between July 2002 and January
2003. Individuals tagged in the Gulf of Maine left that
area in late fall and overwintered in northern shelf
waters, off the coasts of Virginia and North Carolina,
or in offshore waters of the northwestern Atlantic
Ocean. In spring, the fish moved either northwards
towards the Gulf of Maine or offshore. None of the
fish crossed the 45W management line (separating
eastern and western management units) and none
traveled towards the Gulf of Mexico or the Straits of
Florida (known western Atlantic spawning grounds).
The greatest depth recorded was 672 m and the fish
experienced temperatures ranging from 3.4 to 28.7C.
Swimming depth was significantly correlated with
location, season, size class, time of day, and moon
phase. There was also evidence of synchronous vertical
behavior and changes in depth distribution in relation
to oceanographic features.
Introduction
Atlantic bluefin tuna (Thunnus thynnus) are widely dis-
tributed throughout the northern Atlantic Ocean,
ranging from Norway to Africa in the east and from
Newfoundland to Brazil in the west. The species is
considered to be overexploited (NRC 1994) and is cur-
rently managed by the International Commission for the
Conservation of Atlantic Tunas (ICCAT) as two distinct
populations, an eastern stock and a western stock sep-
arated by 45W longitude. The two groups are believed
to have markedly different reproductive patterns, with
eastern fish spawning at a smaller size (15–45 kg vs
135+ kg) and younger age (3–5 years vs 6–10 years)
than those in the western Atlantic Ocean (Rodriguez-
Roda 1967; Baglin 1982; NRC 1994; Nemerson et al.
2000). The eastern stock reproduces between June and
August in the Mediterranean Sea while the western stock
spawns between April and June in two known areas, the
Gulf of Mexico and the Straits of Florida (Roule 1924;
Rivas 1954; Richards 1976).
For decades, stock assessments have indicated that
the putative western population is more depleted than
the eastern population (Sissenwine et al. 1998). Conse-
quently, catch quotas and size limits in the two man-
agement areas have been different (NRC 1994).
However, there is some evidence that Atlantic bluefin
tuna could comprise a single stock. These include con-
ventional tag returns, similarity in growth rates, syn-
chronous long-term catch trends in the east and west,
and a seamless trans-Atlantic distribution of longline
catches (ICCAT 2001). Reviews of conventional tag re-
turns provide mixing rate estimates ranging from 1–10%
(e.g. NRC 1994; Mather et al. 1995). Recent findings
from electronic tagging studies (Lutcavage et al. 1999;
Block et al. 2001a), however, suggest that transfer rates
Communicated by J.P. Grassle, New Brunswick
S. G. Wilson (&)ÆM. E. Lutcavage ÆA. W. Everly
Edgerton Research Laboratory,
New England Aquarium, Boston,
MA 02110, USA
E-mail: steven.wilson@unh.edu
Fax: +1-603-8622717
R. W. Brill
Virginia Institute of Marine Science,
Gloucester Point, VA 23062, USA
M. P. Genovese
F.V. ‘‘White Dove Too’’, Cape May,
NJ 08210, USA
A. B. Cooper
Department of Natural Resources,
University of New Hampshire, Durham,
NH 03824, USA
Present address: S. G. Wilson ÆM. E. Lutcavage
Department of Zoology, University of New Hampshire,
Durham, NH 03824, USA
Marine Biology (2005) 146: 409–423
DOI 10.1007/s00227-004-1445-0
may be significantly higher in some years and possibly
warrant management of Atlantic bluefin tuna as a single
stock.
An improved understanding of bluefin tuna migra-
tion patterns, spawning locations and stock structure is
clearly necessary for fishery management regulations to
be equitable and for rebuilding efforts to have maximal
effect. Additionally, knowledge of the depth distribution
of bluefin tuna and the physiological limitations and
environmental conditions controlling vertical behavior
are crucial to the development of habitat-based stock
assessments (e.g. Hinton and Nakano 1996; Bigelow
et al. 2002; Graves et al. 2003). Until recently,
researchers interested in addressing such issues had few
options available to them: (1) analysis of catch statistics;
(2) conventional tag-recapture studies; or (3) acoustic
tracking studies (Boustany et al. 2001). Unfortunately,
these techniques are either biased by spatial and tem-
poral patterns in fishing effort or limited to short time
scales. Recent technological advances, however, provide
us with new, fishery-independent telemetry techniques
that can track the movements of fish for periods ranging
from months to several years (Block et al. 1998). In the
present study, we used pop-up satellite archival tags
(PSATs) to examine the horizontal and vertical move-
ments of the Atlantic bluefin tuna seasonally inhabiting
the Gulf of Maine.
Materials and methods
Tagging
PSATs (model PTT-100, Microwave Telemetry,
Columbia, MD, USA) were deployed on 68 Atlantic
bluefin tuna (Thunnus thynnus Linnaeus): 67 in the
southern Gulf of Maine and one off North Carolina. In
addition to recording ambient light levels (used to pro-
vide geolocation estimates), these tags recorded depth
(into 5.38-m bins) and temperature (resolution
±0.17C) data at 1-h intervals. Monofilament tethers
were used to attach the PSATs to flat metal darts, con-
structed of either stainless-steel or titanium (Wildlife
Computers, Redmond, WA, USA). The metal darts
were implanted in the dorsal musculature of the fish
using a modified harpoon tagging pole (Chaprales et al.
1998). PSATs were programmed to detach from the fish
and transmit their archived light-level, depth, and tem-
perature data through the Argos data collection and
location service (DCLS) on 1 June 2003. A fail-safe
mechanism in each tag initiates release and data trans-
mission if the tag approaches its depth limit (approx.
1,200 m) or remains at a constant depth for 4 days (e.g.,
if the fish is dead on the bottom or the tag has prema-
turely detached and is floating at the surface).
In the southern Gulf of Maine, bluefin tuna schools
were captured by the purse seiner ‘‘White Dove Too’’
between mid-July and late September 2002. Some
members of each school were allowed to escape and were
tagged as they left the net (n=65 fish). Temperature
profiles of the water column were recorded using
expendable bathythermographs (XBTs) (Sippican,
Marion, MA, USA) after all purse seine tag deploy-
ments. Two tags were also deployed on fish caught in the
southern Gulf of Maine on rod and reel from the sport-
fishing vessel ‘‘Cookie Too’’ in early October 2002 using
methods previously described (Lutcavage et al. 1999).
The North Carolina fish was caught on rod and reel
from the sport-fishing vessel ‘‘Striker’’ on 14 January
2003.
Horizontal movements
Geolocation estimates were computed from recovered
light-level data using a proprietary algorithm (Micro-
wave Telemetry) derived from US Naval Observatory
data. These estimates are based on daily records of the
time of sunrise and sunset, taking into account prevail-
ing conditions measured by the light, pressure, and
temperature sensors, and data from the preceding days.
A state-space Kalman filter model (Sibert and Fournier
2001; Sibert et al. 2003) was then applied to estimate
movement parameters and provide a ‘‘most probable’’
trackline for each fish. Residency periods in two sea-
sonal habitats, the Gulf of Maine and coastal waters off
Virginia and North Carolina, were calculated by deter-
mining the mean dates of arrival and departure for all
fish that entered these areas. For this analysis, the Gulf
of Maine was defined as waters north of 40N latitude
and west of 65W longitude (these boundaries include
Georges Bank in the Gulf of Maine habitat area). Vir-
ginia and North Carolina waters were bounded to the
north by 38N latitude and to the east by 73W longi-
tude. Only permanent movements into or away from
these areas were considered (i.e. brief excursions inside
or beyond these boundaries were ignored).
Fixed kernel utilization distribution contours (Wor-
ton 1989) representing 50% (core areas of distribution)
and 95% (overall range of distribution) of the pooled
daily geolocation estimates were created for seasonal
subsets of the data to examine temporal patterns in
horizontal distributions. These were derived using the
animal movement analysis extension (Hooge and Ei-
chenlaub 1997) and the ArcView Geographic Informa-
tion System (version 3.2, Environmental Systems
Research Institute, Redlands, CA, USA). Contour
smoothing parameters were calculated using least-
squares cross-validation (Silverman 1986).
Vertical movements
We used generalized estimating equations (GEEs) (Li-
ang and Zeger 1986) to examine the effects of the fol-
lowing variables: location (inshore, offshore,
indeterminate), season (July–October, November–Feb-
ruary, March–May), size class ( £136 kg, >136 kg),
410
time of day (dawn, day, dusk, night), and moon phase
(full moon, new moon, intermediate moon) on vertical
distribution, as repeated observations of depth are cor-
related. If autocorrelation is ignored, multiple mea-
surements of a single sampling unit are treated as single
measurements from multiple sampling units. Such
pseudoreplication erroneously increases the sample size
and inflates the power of the statistical analysis, leading
to the description of phenomena that the data may not
actually support.
Locations were determined by examining the filtered
tracklines and depth records of each fish. Indeterminate
locations were those where it was not possible to assign
an inshore or offshore locality with any certainty. The
smaller size class presumably contained immature (i.e.
non-spawning) fish, if western bluefin tuna are fully
mature at a weight of approximately 136 kg (Baglin
1982; NRC 1994). The larger size class was presumed to
represent entirely adult fish. Dawn, day, dusk, and night
were defined as 0500–0600 hours, 0700–1600 hours,
1700–1800 hours, and 1900–0400 hours, respectively
(Eastern Standard Time). No adjustments were made to
account for the effects of longitudinal movements or
seasonal change on the time of sunrise and sunset. Full
and new moons refer to the day of each full or new
moon and the two days preceding and following it.
We assumed that observations were distributed as
gamma random variables and that correlation between
depth observations could be modeled as an autoregres-
sive process with lag one. This allowed us to account for
the fact that all data were bounded at zero (depths of
zero or greater were set to 0.1 m) and assume that
correlation between observations decreased exponen-
tially as the time between observations increased. A
powerful advantage of GEEs over more traditional
mixed effect models is that GEEs treat the correlation
coefficients as nuisance parameters, and therefore the
statistical tests are robust to mis-specification of the
correlation structure (Diggle et al. 1994).
The analysis was implemented in SAS (version 8.02,
SAS Institute, Cary, NC, USA) using the PROC
GENMOD procedure. Significance tests are based on
type III Wald statistics, which are chi-square distributed,
with an alpha level of 0.05 for main effects and 0.10 for
interaction effects (Sokal and Rohlf 1981). Type III test
statistics are ‘‘marginal statistics’’ in that they report the
significance of a given variable after taking into account
the other variables in the model. If a main effect is in-
volved in a significant interaction, the main effect is re-
tained in the model regardless of its significance
(McCullagh and Nelder 1989). Differences between lev-
els of the categorical variables were analyzed using Wald
chi-square tests based on population marginal means
(Searle et al. 1980), and adjusted for multiple compari-
sons using Bonferroni adjustments (adjusted
P-value=estimated P-value multiplied by the number of
comparisons). Marginal population means are the pre-
dicted means of the dependent variable (depth) associ-
ated with each level of an independent variable (e.g.
location) when all other variables in the model are set to
their estimated mean values.
Results
Data were received from 60 of the 68 tags, three of which
remained attached until the programmed pop-up date.
One fish died immediately after release, leaving 59 tags
for inclusion in the dataset. A summary of the dates and
locations of the start and end of each tag deployment,
fish weights, days at liberty, and distance traveled is
provided in Table 1.
Horizontal movements
Sufficient geolocation data were available to estimate the
horizontal movements of 50 bluefin tuna. The maximum
distance traveled was 5820 km in 304 d, with average
daily movements ranging from 1.6–71.6 km day
-1
(mean±SE 16.18±1.95 km day
-1
) (Table 1). Of the 50
fish, 23 remained in northern coastal waters between
Maryland and Nova Scotia (many of these tags detached
after only short periods at liberty). The fish tagged off
North Carolina (03–01) stayed in that area for the
duration of tag attachment. Of the remaining 26 fish, 13
traveled southwest to coastal waters off Virginia and
North Carolina after leaving the Gulf of Maine
(Fig. 1A). Nine moved offshore (i.e. beyond the shelf
break) into the northwestern Atlantic Ocean (Fig. 1B).
Four fish traveled to more than one defined locality: two
fish (02–13 and 02–17) first moved offshore and then
into coastal waters off Nova Scotia; one individual (02–
25) spent time off the Virginia coast before moving off-
shore into the Atlantic Ocean; and another (02–34)
traveled to Nova Scotia waters, then to areas off Vir-
ginia and then back to Nova Scotia waters before
returning to the Gulf of Maine.
Fish tagged in the Gulf of Maine left that area in late
October (mean±SE 25 Oct 2002 ±16.26 days) (n=34
fish). Of those that entered coastal waters off Virginia
and North Carolina, the mean dates of arrival and
departure were 24 Nov 2002 ±11.90 days (n=16 fish)
and 4 Feb 2003 ±10.84 days (n=3 fish), respectively. As
a result of tag shedding and the 1 June 2003 pro-
grammed pop-up date, only three records of fish
returning to the Gulf of Maine were obtained. The mean
date of arrival was 5 May 2003 ±12.47 days, but this is
likely biased towards early returning fish.
Temporal patterns in the distribution of bluefin tuna
are shown in the seasonal distribution contours pre-
sented in Fig. 2A–C. In summer/fall (July-October), the
50% and 95% probability contours are centered around
the tagging location in the southern Gulf of Maine
(Fig. 2A). Over the winter months (November–Febru-
ary), the core area of distribution (50% probability
contour) shifted southwards to coastal waters off Vir-
ginia and North Carolina (Fig. 2B). The overall range
411
Table 1 Dates and locations of the start and end of each tag
deployment on bluefin tuna (Thunnus thynnus). Reporting date/
location refers to the point at which the tag transmitted its data to
the satellite. Locations are provided in decimal degrees. Fish
weights were initially estimated to the nearest 50 lb and then con-
verted to kg. Days at liberty is the period for which the tag re-
mained attached to the fish. Distance traveled is along the ‘‘most
probable’’ trackline
Fish ID Weight
(kg)
Tagging
date
Tagging location Reporting
date
Reporting location Days at
liberty
Distance
traveled
(km)
Distance
traveled
(km) d
-1
Latitude Longitude Latitude Longitude
2–1 136 17 Jul 02 41.97N 69.39W 4 Aug 02 41.65N 69.06W 18 535 29.7
2–2 181 17 Jul 02 41.97N 69.39W 27 Jul 02 41.81N 69.46W 10 19 1.9
2–3 204 17 Jul 02 41.97N 69.39W 18 Sep 02 39.99N 69.36W 63 354 5.6
2–4 136 17 Jul 02 41.97N 69.39W 22 Jan 03 36.31N 73.74W 189 - -
2–5 204 17 Jul 02 41.97N 69.39W 18 Sep 02 44.79N 60.87W 63 1912 30.3
2–6 181 17 Jul 02 41.97N 69.39W 29 Jul 02 41.88N 69.43W 12 19 1.6
2–7 136 17 Jul 02 41.97N 69.39W 18 Mar 03 36.83N 73.45W 244 1476 6.0
2–8 136 17 Jul 02 41.99N 69.40W 20 Feb 03 35.82N 60.45W 218 2995 13.7
2–9 159 17 Jul 02 41.99N 69.40W 16 Sep 02 42.10N 67.76W 61 391 6.4
2–10 113 17 Jul 02 41.99N 69.40W 17 Mar 03 38.93N 65.53W 243 4535 18.7
2–11 136 1 Aug 02 42.02N 69.02W 9 Dec 02 34.16N 77.12W 130 1445 11.1
2–12 136 1 Aug 02 42.02N 69.02W 25 Jan 03 36.22N 63.05W 177 2216 12.5
2–13 159 1 Aug 02 42.02N 69.02W 1 Jun 03 41.15N 66.90W 304 2050 6.7
2–14 181 1 Aug 02 42.02N 69.02W 7 Apr 03 39.12N 71.65W 249 2870 11.5
2–15 159 1 Aug 02 42.02N 69.02W 7 Mar 03 40.10N 55.43W 218 2486 11.4
2–16 204 1 Aug 02 42.02N 69.02W 22 Jan 03 39.55N 63.22W 174 1458 8.4
2–17 181 1 Aug 02 42.02N 69.02W 7 Feb 03 42.89N 62.21W 190 3512 18.5
2–18 136 1 Aug 02 42.02N 69.02W 7 May 03 40.42N 68.71W 279 2302 8.3
2–19 136 1 Aug 02 42.02N 69.02W 5 Oct 02 40.47N 68.56W65 - -
2–20 181 1 Aug 02 42.02N 69.02W 29 Dec 02 38.31N 72.72W 150 2217 14.8
2–21 136 1 Aug 02 42.02N 69.02W 20 Feb 03 43.24N 60.49W 203 2245 11.1
2–22 181 1 Aug 02 42.02N 69.02W 14 Dec 02 34.46N 75.15W 135 1462 10.8
2–23 136 1 Aug 02 42.02N 69.02W 30 Jan 03 33.99N 76.36W 182 1578 8.7
2–24 181 1 Aug 02 42.02N 69.02W 13 Dec 02 39.06N 68.45W 134 1525 11.4
2–25 181 1 Aug 02 42.02N 69.02W 1 Jun 03 40.66N 52.55W 304 5820 19.1
2–26 136 1 Aug 02 42.11N 69.07W 15 Sep 02 42.08N 67.50W 45 240 5.3
2–27 113 1 Aug 02 42.11N 69.07W 19 Oct 02 42.95N 68.57W 79 555 7.0
2–28 113 1 Aug 02 42.11N 69.07W 29 Oct 02 37.17N 74.96W 89 1274 14.3
2–29 91 1 Aug 02 42.11N 69.07W 6 Nov 02 40.69N 69.10W 97 1869 19.3
2–30 136 1 Aug 02 42.11N 69.07W 27 Nov 02 37.12N 74.44W 118 1303 11.0
2–31 91 1 Aug 02 42.11N 69.07W 2 Jan 03 38.62N 72.77W 154 858 5.6
2–32 136 8 Aug 02 41.88N 68.84W 16 Feb 03 36.75N 75.17W 192 1947 10.1
2–33 136 8 Aug 02 41.88N 68.84W 22 Feb 03 43.38N 61.96W 198 1623 8.2
2–34 113 8 Aug 02 41.88N 68.84W 1 Jun 03 40.26N 68.14W 297 5764 19.4
2–35 136 8 Aug 02 41.88N 68.84W 11 Dec 02 41.05N 64.82W 125 1743 13.9
2–36 159 8 Aug 02 41.88N 68.84W 18 Aug 02 41.76N 67.98W 10 221 22.1
2–37 91 8 Aug 02 41.88N 68.84W 21 Aug 02 39.93N 72.74W 13 931 71.6
2–38 136 8 Aug 02 41.88N 68.84W 19 Sep 02 41.74N 66.41W 42 775 18.5
2–39 159 8 Aug 02 41.88N 68.84W 24 Sep 02 40.63N 71.54W 47 655 13.9
2–40 159 8 Aug 02 41.88N 68.84W 15 Dec 02 33.59N 77.32W 129 1565 12.1
2–41 136 8 Aug 02 41.88N 68.84W 31 Aug 02 41.83N 69.34W 23 622 27.0
2–42 159 8 Aug 02 41.88N 68.84W 26 Oct 02 41.94N 66.72W 79 396 5.0
2–43 136 8 Aug 02 41.88N 68.84W 18 Aug 02 41.90N 67.72W 10 186 18.6
2–44 91 8 Aug 02 41.88N 68.84W 7 Mar 03 41.19N 61.28W 211 3263 15.5
2–45 136 8 Aug 02 41.88N 68.84W 4 Nov 02 42.50N 66.93W 88 1154 13.1
2–46 147 8 Aug 02 41.88N 68.84W 19 Dec 02 41.88N 62.89W 133 1173 8.8
2–47 113 17 Aug 02 41.88N 68.72W 1 Mar 03 37.85N 50.77W 196 4147 21.2
2–48 204 6 Sep 02 41.30N 69.17W 25 Sep 02 39.41N 72.12W19 - -
2–49 204 30 Sep 02 41.43N 68.98W 24 Oct 02 39.88N 70.75W24 - -
2–50 227 30 Sep 02 41.43N 68.98W 1 Feb 03 36.00N 73.18W 124 948 7.6
2–51 204 30 Sep 02 41.43N 68.98W 1 Nov 02 33.87N 75.17W 32 1461 45.7
2–52 295 30 Sep 02 41.43N 68.98W 12 Oct 02 41.76N 68.78W12 - -
2–53 272 30 Sep 02 41.43N 68.98W 16 Oct 02 33.61N 71.22W 16 995 62.2
2–54 249 30 Sep 02 41.43N 68.98W 6 Oct 02 39.79N 69.72W6 - -
2–55 227 30 Sep 02 41.43N 68.98W 6 Oct 02 41.84N 68.06W6 - -
2–56 181 30 Sep 02 41.43N 68.98W 8 Oct 02 41.59N 69.02W8 - -
2–57 181 10 Oct 02 41.35N 69.20W 16 Oct 02 40.36N 71.38W6 - -
2–58 272 10 Oct 02 41.35N 69.20W 9 Nov 02 33.89N 76.63W 30 1298 43.3
3–1 125 14 Jan 03 34.38N 76.52W 11 May 03 38.24N 72.91W 117 1229 10.5
412
(95% probability contour) extended northwards to
Nova Scotia waters and offshore as far as 60W longi-
tude. In the spring months (March–May), the core area
of distribution remained in coastal waters off Virginia
and North Carolina while the overall range extended
offshore as far as 50W longitude (Fig. 2C).
Vertical movements
Depth and temperature data, recorded at one-hour
intervals, were recovered from all 59 tags in the dataset.
Figure 3A shows the percentage time-at-depth (10-m
intervals) in darkness and during the day. The fish spent
>25% of their time in the top 10 m of the water column
(night=27.5%, day=29.8%) and >50% of their time
at depths of £20 m (night=57.0%, day=51.0%). The
maximum depth recorded by any fish was 672 m. Most
deep descents (to depths of >200 m) were made during
the day. Figure 3B shows the percentage time-at-tem-
perature (2C intervals) for night and day combined.
The fish spent >50% of their time in water of 15–23C
and encountered ambient temperatures of 3.4–28.7C.
Temperature changes of up to 19C were experienced in
a single day, with most fish encountering differentials of
15–17C (Fig. 4). A weak correlation was found between
Fig. 1 Exemplary Kalman
filtered tracks of bluefin tuna
(Thunnus thynnus): Afish 02–07
and Bfish 02–15. The 200-m
isobath (black line) indicates
approximate position of the
shelf break. NS Nova Scotia,
MD Maryland, VA Virginia,
NC North Carolina
413
Fig. 2A–C Distribution
contours comprising 50% and
95% of the pooled geolocation
data. AJuly–October (n=50
fish), BNovember–February
(n=33 fish), and CMarch–May
(n=11 fish). The 200-m isobath
(black line) indicates
approximate position of the
shelf break. NS Nova Scotia,
MD Maryland, VA Virginia,
NC North Carolina
414
fish size and maximum daily temperature change (linear
regression: r
2
=0.218, P<0.05), with larger fish experi-
encing larger daily temperature changes than smaller
fish.
GEE analysis indicated that swimming depth was
significantly correlated with location, season, size class,
time of day, and moon phase (Tables 2, 3). The effect of
season differed by location and the effect of size class
differed by season. Time of day and moon phase effects
differed by both location and season. Swimming depths
at inshore locations were shallower than those at off-
shore and indeterminate locations (C
12
=51.47, adjusted
P<0.001; C
12
=75.98, adjusted P<0.001), but depths at
offshore and indeterminate locations did not differ
(C
12
=2.48, adjusted P=0.35).
Swimming depths during the winter months
(November-February) were deeper than those during the
summer/fall (July-October) and spring (March-May)
Fig. 3 Histograms showing percentage Atime-at-depth
(night=2000–0500 hours, day=0600–1900 hours) and Btime-at-
temperature. Data from all fish in dataset pooled (n=59 fish)
Fig. 4 Scatterplot of estimated fish size versus maximum daily
temperature change (n=38). Fish with depth records of <30 days
were excluded from this analysis. Linear regression line and 95%
confidence intervals are included
Table 2 Wald statistics for type III analyses
Variable df Chi-square P-value
Location 2 76.25 <0.001
Season 2 53.89 <0.001
Season ·location 4 54.12 <0.001
Size class 1 3.25 0.072
Size class ·season 2 7.16 0.028
Time of day 3 70.47 <0.001
Time of day ·location 6 77.89 <0.001
Time of day ·season 6 79.77 <0.001
Time of day ·location ·season 12 462.04 <0.001
Moon phase 2 16.07 <0.001
Moon phase ·location 4 4.43 0.350
Moon phase ·season 4 20.03 <0.001
Moon phase ·location ·season 8 53.01 <0.001
Table 3 Mean depths (m) of variable categories
Variable Category Mean depth (m)
Location Inshore 22.17*
Offshore 45.45
Indeterminate 53.19
Season July–October 29.15
November–February 54.95*
March–May 29.85
Size class £136 kg 32.36
>136 kg 38.02
Time of day Dawn 33.78
Day 40.82*
Dusk 34.25
Night 32.05
Moon phase Full moon 36.90*
New moon 33.56
Intermediate moon 34.48
* significantly different from other categories of the same variable
415
(C
12
=36.46, adjusted P<0.001; C
12
=45.36, adjusted
P<0.001), but were similar during summer/fall and
spring (C
12
=0.12, adjusted P=2.19). However, there
were exceptions: depths during the winter were similar to
those during the spring at indeterminate locations; and
depths during the summer/fall were shallower than those
during the spring at indeterminate locations.
The main effect of size class was not significant
(C
12
=3.25, P=0.072) (i.e. the swimming depths of the
two size classes, overall, were similar). There was,
however, a significant interaction between size class and
season (C
12
=7.16, P=0.028), with smaller fish swim-
ming at shallower depths than larger fish during the
summer/fall (C
12
=6.36, adjusted P=0.035). In contrast,
the two size classes had similar swimming depths during
the winter and spring months (C
12
=0, adjusted P=1.0;
C
12
=0.1, adjusted P=1.0).
Daytime swimming depths were deeper than those at
dusk, night, and dawn (C
12
=38.87, adjusted P<0.001;
C
12
=25.62, adjusted P<0.001; and C
12
=25.17, ad-
justed P<0.001), while depths at dusk, night, and dawn
were all similar. However, there were exceptions: depths
during the day were not different from those at night at
inshore locations; depths during the day were not dif-
ferent from those at dusk at indeterminate locations;
depths during the day were not different from those at
dusk, night, and dawn at offshore locations; depths at
dusk were different from those at dawn at inshore lo-
cations; depths at dusk were different from those at
night at indeterminate locations; day and dawn depths
were similar during the summer/fall; and depths during
the day were similar to those at dusk, night, and dawn
during the winter.
During full moons, the fish were deeper than during
intermediate or new moons (C
12
=13.58, adjusted
P<0.001; C
12
=9,60, adjusted P=0.006) and depths
during intermediate and new moons were similar
(C
12
=0.95, adjusted P=0.99). However, there were
exceptions: depths during full moons were similar to
those during intermediate and new moons at offshore
and indeterminate locations; depths during full moons
were similar to those during new and intermediate
moons in the summer/fall; depths during full moons
were similar to those during new moons in the winter;
depths during full moons were similar to those during
intermediate moons in the spring; and depths during
intermediate moons were deeper than those during new
moons in the spring.
Figure 5A,B shows simultaneously recorded depth
and temperature data from four fish located in the Gulf
of Maine (16–22 August 2002). These individuals were
tagged at three different locations over a 7-day period,
suggesting that similarities in their profiles indicate
synchronous behavior patterns rather than evidence that
they regrouped into a single school. Evident in these
profiles are deep descents made at times of light transi-
tion (i.e. at dusk and dawn), with the dusk descent
usually to greater depths than the dawn descent. These
vertical movements at the beginning and end of each day
were sporadic, and usually absent when fish were in
waters off the Virginia and North Carolina coasts and
beyond the edge of the continental shelf (Fig. 6A–C).
Hourly depth records are plotted over contoured
hourly temperature data in Fig. 7A,B. Fish 02–12 ap-
pears to have spent its first three weeks at liberty in
coastal waters, descending to a maximum depth of 75 m
during that period (Fig. 7A). The warm temperature
signature of the Gulf Stream (or associated eddies and
filaments) is evident in weeks 3–7, with only shallow
descents (to a maximum depth of 129 m) made while
swimming in this water mass. A change in the vertical
behavior of this individual occurred after emerging from
the Gulf Stream, with deeper (to a maximum depth of
237 m) and more frequent descents being made. Fish 02–
35 entered the Gulf Stream twice between weeks 3–6 and
8–10, with its depth patterns becoming shallower each
time (Fig. 7B). Periods spent in cooler waters were again
characterized by deeper (to a maximum depth of 344 m)
and more frequent dives. Similar patterns were observed
in other fish spending extended periods offshore.
Discussion and conclusions
Of the 68 tags deployed in this study, only three re-
mained attached until the programmed pop-up date.
Possible causes of premature tag release include: (1) dart
shedding/ tissue rejection (resulting from dart design,
suboptimal placement, etc.); and (2) failure of the tether
or the tag’s nosecone pin (resulting from material wear/
fatigue, corrosion, predation events, rubbing against the
seafloor, etc.). Estimated average daily displacements
(1.6–71.6 km day
-1
) were consistent with results from a
previous acoustic tracking study in the Gulf of Maine
(Lutcavage et al. 2000). All the fish remained west of the
45W management line for the period that the tags re-
mained attached. In contrast, 29% of the single-point
PSATs deployed in 1997 by Lutcavage et al. (1999) in
the Gulf of Maine reported from locations east of the
45W management line. However, the fish tagged in the
present study were significantly smaller than those in the
previous study (mean estimated fork length 201 cm vs
224 cm) and bluefin tuna dispersal patterns are known
to vary with size and environmental conditions (Mather
et al. 1995). Block et al. (2001a) found that 31% of
recovered implantable archival tags and 3% of reporting
PSATs deployed primarily during the winter in North
Carolina waters were east of the 45W management line.
Most of the fish tagged in the southern Gulf of Maine
in late summer/early fall remained in that area until late
October, consistent with previous studies (Mather et al.
1995; Lutcavage et al. 1999). Of the 33 fish with PSATs
remaining attached over the winter months, 14 remained
in northern shelf waters (between Maryland and Nova
Scotia), 14 moved south to waters off the coasts of
Virginia and North Carolina, and 5 were in offshore
waters of the northwestern Atlantic Ocean. In spring, 6
of the 11 fish with tags remaining either stayed in
416
northern waters or moved to that area from Virginia and
North Carolina waters and the other five fish moved
offshore into the mid-Atlantic Ocean. Similar seasonal
movement patterns were displayed by individuals tagged
in coastal waters off North Carolina (Block et al. 2001a,
2001b; Gunn and Block 2001). During the winter
months, these fish remained either on the Carolina shelf
or in offshore waters of the northwestern Atlantic Ocean
and moved offshore along the path of the Gulf Stream in
spring. By summer, many were in northern shelf waters.
Fig. 5 Hourly Adepth and
Btemperature data from two
fish (02–11 and 02–30) tagged on
1 August 2002 and two fish
(02–39 and 02–42) tagged on 8
August 2002 for a 7-day period
(16–22 August 2002). Shaded
areas indicate nighttime
417
The residency periods calculated for the Gulf of Maine
and coastal waters off Virginia and North Carolina
temporally coincide with commercial and recreational
fisheries targeting bluefin tuna in these habitats.
None of the 11 fish (6 of which were of mature size
i.e. ‡136 kg) at liberty between March and May moved
towards a known western Atlantic spawning ground.
There are, however, conventional tag records of fish
tagged in the Gulf of Maine being recaptured in the Gulf
of Mexico during the spawning season (Mather et al.
1995). Individuals tagged off North Carolina have also
traveled to the Gulf of Mexico and were presumed to
have spawned there (Block et al. 2001a; Gunn and Block
2001). Atlantic bluefin tuna are believed to spawn in sea
surface temperatures of 24C and higher (Richards 1976;
NRC 1994; Mather et al. 1995; Schaefer 2001), yet none
of our temperature records of 24C and higher were
collected during the spring spawning period. Our data,
therefore, imply either that: (1) mature fish do not spawn
each year (Lutcavage et al. 1999); or (2) they spawn at
other locations in waters cooler than 24C, such as off
the Carolinas, along the edge of the Gulf Stream, in the
Caribbean Sea, or in the central Atlantic Ocean. These
areas have been proposed as possible spawning grounds
(Mather 1974; Baglin 1976; Suzuki and Ishizuka 1990;
Lutcavage et al. 1999; Block et al. 2001a; Secor et al.
2002). Bluefin tuna larvae have been collected along the
shelf break off North Carolina, but these were thought
to have been advected northwards in the Gulf Stream
from known spawning grounds (McGowan and
Richards 1989). As a number of individuals moved into
the mid-Atlantic Ocean in the spring, we cannot dis-
count the possibility that some fish may have moved to
the Mediterranean or other spawning areas after either
tag detachment or the programmed 1 June 2003 pop-up
date. Records obtained from implanted archival tags
have shown such movements (Block et al. 2001a; Gunn
and Block 2001). Recently, we verified that data recep-
tion from current PSATs by Argos DCLS receivers is
poor to nonexistent in the central and western Medi-
terranean (Lutcavage et al., unpublished data). Bluefin
of mature size have historically been captured through-
out the central Atlantic Ocean and in the Caribbean Sea
(Bullis and Captiva 1955; Wilson and Bartlett 1967),
where they are still encountered by pelagic longliners.
These areas do not include known feeding or spawning
grounds and the reproductive status of these fish is not
known (Richards 1976; Mather et al. 1995; Lutcavage
and Luckhurst 2002).
Archival tags utilize light-level data to estimate lati-
tude (from day length) and longitude (from time of local
noon). Several factors can influence the accuracy of
these estimates, including equinoxes, light attenuation,
water clarity, resolution of the light sensor, and vertical
behavior of the fish (Arnold and Dewar 2001; Musyl
et al. 2001). A detailed analysis of the accuracy of the
geolocation estimates presented here will be provided in
a subsequent paper (Sibert et al., in preparation).
Our data show that Atlantic bluefin tuna spend the
majority of their time in the top 20 m of the water
Fig. 6 Hourly depth data from
fish 02–25 for three 7-day
periods when located in Athe
Gulf of Maine, Bcoastal waters
off Virginia and North Carolina,
and Coffshore waters. Note that
days are not necessarily
consecutive due to incomplete
data transmission. Shaded areas
indicate nighttime
418
column, descending occasionally to depths in excess of
500 m. The wide range of environmental temperatures
experienced (3.4–28.7C) by the fish was similar to that
previously reported for this species in the northwestern
Atlantic Ocean (Carey and Lawson 1973; Lutcavage
et al. 2000; Block et al. 2001a, 2001b; Brill et al. 2002).
Daily temperature changes of up to 19C were recorded
and a weak relationship was noted between fish size and
maximum daily temperature change. Brill and Lutca-
vage (2001) suggested that bluefin tuna tolerate maxi-
mum changes of 14C and that this is independent of fish
size, as in other tuna species (e.g. yellowfin tuna, Thun-
nus albacares, Brill et al. 1999).
The vertical behavior of bluefin tuna differed among
locations, with shallower swimming depths occurring
when fish were in inshore waters. It seems unlikely that
this reflects bathymetric constraints, as mean swimming
depths at offshore and indeterminate locations were
shallower than the seafloor in inshore habitats. Rather,
these distributions may reflect shallower prey depths in
coastal waters. Alternatively, these visual predators may
be distributed closer to the surface due to reduced light
penetration in turbid inshore waters. Atlantic bluefin
tuna inhabiting the Gulf of Maine during the summer
months are known to have a predominantly piscivorous
diet, with sandlance (Ammodytes americanus), Atlantic
herring (Clupea harengus), Atlantic mackerel (Scomber
scombrus), and unidentified squid species the most
common prey items (Crane 1936; Lutcavage et al. 2000;
Chase 2002; Estrada et al., submitted). In contrast,
stomach contents of individuals captured in the winter
fishery off North Carolina contain mostly Atlantic
menhaden (Brevoortia tyrannus) and unidentified port-
unid crabs (J.A. Buckel, North Carolina State Univer-
sity, personal communication). In offshore waters,
bluefin tuna sampled during pelagic longline cruises had
mostly mesopelagic fishes and squid in their stomachs
(Matthews et al. 1977), indicating very different feeding
regimes. Fish arriving in the Gulf of Maine in early
summer are often quite emaciated, and stable isotope
analysis of their tissues suggests that they feed on prey
items from lower trophic levels in the months preceding
their arrival (Estrada et al., submitted). Similarly,
Young et al. (1997) found that juvenile southern bluefin
tuna (Thunnus maccoyii) have a diet composed mainly of
fish when on the continental shelf and squid and
planktonic crustaceans when in offshore waters.
We found that swimming depths varied among sea-
sons, with fish distributed significantly deeper during the
winter months, despite many fish being located in shal-
low coastal waters off the coasts of Virginia and North
Carolina at that time of year. Kitagawa et al. (2000) also
Fig. 7 Hourly depth data from
Afish 02–12 and Bfish 02–35
plotted over contoured hourly
temperature data
419
noted seasonal differences in the vertical distributions of
small Pacific bluefin tuna (Thunnus orientalis), with
deeper distributions occurring during the winter months
in association with a mixed water column. During the
summer, they found that fish were limited to mostly
surface waters by strong thermal gradients. Similarly,
strong thermoclines develop in the Gulf of Maine during
the summer and fall months, evident in the XBT profile
presented in Fig. 8. It is not surprising, therefore, that
most of the maximum daily temperature changes pre-
sented in Fig. 4 were recorded during this period. In
contrast, shelf waters off North Carolina are known to
be only weakly stratified during the winter months due
to storm mixing and cooling (Werner et al. 1999). Fur-
thermore, temperature data recorded by our tags during
the winter often revealed a relatively homogenous water
column.
We have also found that Atlantic bluefin tuna tagged
in the Mediterranean Sea (DeMetrio et al., unpublished
data), where warm isotherms extend to depths of hun-
dreds of meters in certain locations, have deeper distri-
butions and are more vertically active than those in the
present study. This suggests that strong thermal gradi-
ents limit the vertical movements of Atlantic bluefin
tuna. This is illustrated in the vertical profiles of fish 02–
25 over the different seasons (Fig. 6A–C). The location
of prey in the different habitats occupied by the fish at
different times of the year may also contribute to sea-
sonal changes in vertical behavior (Nakamura 1965;
Mather et al. 1995; Marcinek et al. 2001).
Overall, no significant difference was found between
the depths of the two size classes. The relatively large
size (91–136 kg) of the smaller size class in this study
may account for this (i.e. fish in the smaller size class
may have exhibited adult depth patterns). Previous
studies have noted that the depth distributions of juve-
nile Atlantic bluefin tuna (Roffer 1987; Brill et al. 2002)
and Pacific bluefin tuna (Marcinek et al. 2001; Itoh et al
2003) are restricted to the mixed surface layer, with only
brief excursions made to significant depths. As body
mass is known to affect the rate of change in muscle
temperature following a change in ambient temperature
(Neill and Stevens 1974; Neill et al. 1976; Brill et al.
1994), small fish may need to spend most of their time in
surface waters in order to maintain optimal body tem-
peratures. Similarly, Brill and Lutcavage (2001) report
that small bigeye tuna (Thunnus obesus) have shallower
daytime depths than larger individuals. Holland et al.
(1992) and Dagorn et al. (2000) suggested that small
bigeye tuna make frequent daytime excursions into
surface waters in order to increase their body tempera-
tures and repay oxygen debt. We did find, however, that
the depths of smaller fish were shallower than those of
larger fish during the summer/fall. Although there was
no difference between the temperature changes routinely
experienced by acoustically tracked juvenile and adult
Atlantic bluefin tuna (Brill and Lutcavage 2001), our
data imply that the strong summer thermoclines that
develop in the Gulf of Maine may constrain the vertical
movements of smaller fish to a greater extent than those
of larger individuals. This is corroborated by the weak
correlation identified between fish size and maximum
daily temperature change.
Daytime depths were significantly deeper than those
at dusk, night, and dawn. Clear day-night differences
have been identified in the vertical distributions of many
large pelagic fishes, including tunas (e.g. Yuen 1970;
Holland et al. 1992; Josse et al. 1998; Dagorn et al. 2000;
Kitagawa et al. 2000; Schaefer and Fuller 2002; Itoh
et al. 2003; Musyl et al. 2003), billfishes (e.g. Carey and
Robison 1981; Carey 1990; Holland et al. 1990), and
sharks (e.g. Carey and Scharold 1990; Nelson et al. 1997;
West and Stevens 2001). In each of these studies, day-
time distributions were deeper than those occurring
during the night. Such depth patterns might be expected
if the fish were following certain isolumes/light levels
(Blaxter and Parrish 1965; Boden and Kampa 1967;
Carey and Robison 1981) or diurnal vertical migrations
of the deep scattering layer (DSL) and associated prey
(e.g. Carey 1990; Josse et al. 1998; Dagorn et al. 2000;
Marcinek et al. 2001).
The majority of deep descents (to depths of >200 m)
occurred during daytime. They likely represent foraging
excursions (Holland et al. 1992; Kitagawa et al. 2000;
Schaefer and Fuller 2002). In other studies, such des-
cents appear to be associated with an increase in the
frequency of vertical excursions, but this is difficult to
ascertain with our data given the hourly depth-sampling
interval. Hypotheses proposed to account for such reg-
ular up-and-down movements in the water column in-
clude: (1) fish swim up and glide down to conserve
energy (Weihs 1973); (2) it is a form of behavioral
thermoregulation (Carey and Scharold 1990); (3) the
movements represent a search pattern used to detect
odors in different strata of the water column and thus
guide foraging or migratory movements (Westerberg
1984; Carey and Scharold 1990; Gunn et al. 1999); and
Fig. 8 Vertical profile of water temperature recorded with an XBT
in the southern Gulf of Maine on 17 August 2002. Note the strong
summer thermocline
420
(4) the descents are made to detect magnetic fields in the
seafloor and thus aid in navigation (Klimley et al. 2002).
We also noted dramatic depth changes at dawn and
dusk, a recurring feature in the vertical behavior of large
pelagic fishes, including bluefin tuna (Lutcavage et al.
2000; Marcinek et al. 2001), other tunas (e.g. Block et al.
1997), billfishes (Carey and Robison 1981), and sharks
(Nelson et al. 1997). While certainly related to changing
light levels, their function remains unknown. A number
of hypotheses have been suggested, however, including:
(1) the descents represent the day’s first and last
opportunities to visually locate the DSL and associated
prey (Davis and Stanley 2001); (2) fish are avoiding
certain light levels at which predators would have a vi-
sual advantage (Itoh et al. 2003); and (3) the descents
represent a shift between behavioral modes (Newlands
et al. 2004). In the present study, consistent dawn and
dusk descents occurred only when fish were located in
the Gulf of Maine, but similar patterns have been de-
tected in fish tagged in North Carolina (Gunn and Block
2001). Lutcavage et al. (2000) suggested that bluefin
tuna dive at times of light transition in the Gulf of
Maine to prey upon sandlance rising up off the bottom.
In other locations, it may be that this behavior is not
always beneficial and, therefore, not always exhibited.
Swimming depths were found to be significantly
deeper around full moons. A number of other studies
have found relationships between the vertical distribu-
tion of large pelagic fishes and moon phase, with deeper
nighttime distributions found in bigeye tuna (Schaefer
and Fuller 2002; Musyl et al. 2003), school sharks
(Galeorhinus galeus) (West and Stevens 2001), and
swordfish (Xiphias gladius) (Carey and Robison 1981)
during full moons. It seems likely that these vertical
changes reflect shifts in the depth distribution of prey in
response to increased lunar illumination.
Depth records from fish tagged on different days and
in different areas of the Gulf of Maine were remarkably
similar. Such synchronized behavior is well known
among fishermen targeting bluefin tuna in these waters,
with large numbers appearing almost simultaneously at
the surface over large areas on so-called ‘‘show days’’
(Lutcavage and Kraus 1995). Upon entering the Gulf
Stream, the swimming depth of fish noticeably shoaled
and extensive vertical movements ceased (Fig. 7A,B).
This behavioral change may again be related to the
strong thermal gradients associated with the warm water
mass and the cooler waters it flows over. After emerging
from the Gulf Stream into cooler and relatively
homogenous waters along the edge of the current, reg-
ular descents to significant depths resumed. This finding
contrasts with a report of bluefin tuna diving to depths
of 1,000 m in the Gulf Stream (Gunn and Block 2001).
While the present study has revealed new insights into
the horizontal and vertical movements of Atlantic
bluefin tuna, many important questions still remain.
Although many of the fish exhibited similar movement
patterns, they were different from those detected for
larger fish in previous years (Lutcavage et al. 1999) and
from individuals tagged in North Carolina waters (Block
et al. 2001a, 2001b; Gunn and Block 2001). The area
occupied by fish in our study represents only a small
portion of the northwestern Atlantic Ocean known to be
occupied by adult bluefin tuna at the same time of year
(e.g. Tiews 1963; Nakamura 1965; Wilson and Bartlett
1967; Mather et al. 1995). Although PSATs are fishery-
independent, as opposed to implanted archival tags that
must be recovered (Arnold and Dewar 2001), current
models do not provide data records of sufficient dura-
tion to identify possible spawning and alternative for-
aging areas, and data reception problems remain. This
highlights the need for improved tag technologies, ex-
panded deployments throughout the bluefin tuna’s
range, and incorporation of movement patterns into
operational models to support stock assessment and
biomass estimation.
Acknowledgements We are grateful to Anthony Genovese, Mark
Genovese and the crew of the F.V. ‘‘White Dove Too’’,Captain
Edward Murray Jr. and Anthony Mendillo of the F.V. ‘‘Cookie
Too’’, and Captain Paul Evans and the crew of the F.V. ‘‘Striker’’
for their assistance in this project. We also thank Al Barker, Frank
Cyganowski, Michael Dormier, Jim Hannon and Sippican, George
Harms, Paul Howey, Jon Lucy, Anders Nielsen, John Sibert,
Donald Stott Jr., and Dave Thompson for their valuable contri-
butions. This work was supported by a grant from the National
Marine Fisheries Service (grant no. NA16FM2840) to Molly Lut-
cavage. This paper is dedicated to the memory of Pete Wilson (not
related).
References
Arnold G, Dewar H (2001) Electronic tags in marine fisheries re-
search: a 30-year perspective. In: Sibert JR, Nielsen JL (eds)
Electronic tagging and tracking in marine fisheries. Kluwer,
Dordrecht, pp 7–64
Baglin RE Jr (1976) A preliminary study of the gonadal develop-
ment and fecundity of the western Atlantic bluefin tuna. IC-
CAT Coll Vol Sci Pap 5:279–289
Baglin RE Jr (1982) Reproductive biology of western Atlantic
bluefin tuna. Fish Bull 80:121–134
Bigelow K, Hampton J, Miyabe N (2002) Application of a habitat-
based model to estimate effective longline fishing effort and
relative abundance of Pacific bigeye tuna (Thunnus obesus). Fish
Oceanogr 11:143–155
Blaxter JHS, Parrish BB (1965) The importance of light in shoaling,
avoidance of nets and vertical migration by herring. J Cons Int
Explor Mer 30:40–57
Block BA, Keen JE, Castillo B, Dewar H, Freund EV, Marcinek
DJ, Brill RW, Farwell C (1997) Environmental preferences of
yellowfin tuna (Thunnus albacares) at the northern extent of its
range. Mar Biol 130:119–132
Block BA, Dewar H, Farwell C, Prince ED (1998) A new satellite
technology for tracking the movements of Atlantic bluefin tuna.
Proc Natl Acad Sci USA 95:9384–9389
Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED,
Farwell CJ, Boustany A, Teo SL, Seitz A, Walli A, Fudge D
(2001a) Migratory movements, depth preferences, and thermal
biology of Atlantic bluefin tuna. Science 293:1310–1314
Block BA, Dewar H, Blackwell SB, Williams T, Prince E, Boustany
AM, Farwell C, Dau DJ, Seitz A (2001b) Archival and pop-up
satellite tagging of Atlantic bluefin tuna. In: Sibert JR, Nielsen
JL (eds) Electronic tagging and tracking in marine fisheries.
Kluwer, Dordrecht, pp 65–88
421
Boden BP, Kampa EM (1967) The influence of natural light on the
vertical migrations of an animal community in the sea. Symp
Zool Soc Lond 19:15–26
Boustany AM, Marcinek DJ, Keen J, Dewar H, Block BA (2001)
Movements and temperature preferences of Atlantic bluefin
tuna (Thunnus thynnus) off North Carolina: a comparison of
acoustic, archival and pop-up satellite tags. In: Sibert JR,
Nielsen JL (eds) Electronic tagging and tracking in marine
fisheries. Kluwer, Dordrecht, pp 65–88
Brill RW, Lutcavage ME (2001) Understanding environmental
influences on movements and depth distributions of tunas and
billfishes can significantly improve population assessments. In:
Sedberry GR (ed) Proceedings of the Charleston Bump Collo-
quium, Am Fish Soc Symp 25:179–198
Brill RW, Dewar H, Graham JB (1994) Basic concepts relevant to
heat transfer in fishes, and their use in measuring the physio-
logical thermoregulatory abilities of tunas. Environ Biol Fish
40:109–124
Brill RW, Block BA, Boggs CH, Bigelow KA, Freund EV, Mar-
cinek DJ (1999) Horizontal movements and depth distribution
of large adult yellowfin tuna (Thunnus albacares) near the
Hawaiian Islands, recorded using ultrasonic telemetry: impli-
cations for the physiological ecology of pelagic fishes. Mar Biol
133:395–408
Brill R, Lutcavage M, Metzger G, Bushnell P, Arendt M, Lucy J,
Watson C, Foley D (2002) Horizontal and vertical movements
of juvenile bluefin tuna (Thunnus thynnus) in relation to
oceanographic conditions of the western North Atlantic,
determined with ultrasonic telemetry. Fish Bull 100:155–167
Bullis HR Jr, Captiva FJ (1955) Preliminary report on exploratory
long-line fishing for tuna in the Gulf of Mexico and Caribbean
Sea. Comm Fish Rev 17:1–20
Carey FG (1990) Further acoustic telemetry observations of
swordfish. In: Stroud R (ed) Proceedings of the second inter-
national billfish symposium. Planning the future of billfishes:
research and management in the 90’s and beyond. National
Coalition for Marine Conservation, Savannah, pp 103–122
Carey FG, Lawson KD (1973) Temperature regulation in free-
swimming bluefin tuna. Comp Biochem Physiol 44A:375-
Carey FG, Robison BH (1981) Daily patterns in the activities of
swordfish, Xiphias gladius, observed by acoustic telemetry. Fish
Bull 79:277–292
Carey FG, Scharold JV (1990) Movements of blue sharks (Prionace
glauca) in depth and course. Mar Biol 106:329–342
Chaprales W, Lutcavage M, Brill R, Chase B, Skomal G (1998)
Harpoon method for attaching ultrasonic and ‘‘popup’’ satellite
tags to giant bluefin tuna and large pelagic fishes. Mar Technol
Soc J 32:104–105
Chase BC (2002) Differences in diet of Atlantic bluefin tuna
(Thunnus thynnus) at five seasonal feeding grounds on the New
England continental shelf. Fish Bull 100:168–180
Crane J (1936) Notes on the biology and ecology of giant tuna
Thunnus thynnus, L., observed at Portland, Maine. Zoologica
212:207–212
Dagorn L, Bach P, Josse E (2000) Movement patterns of large
bigeye tuna (Thunnus obesus) in the open ocean, determined
using ultrasonic telemetry. Mar Biol 136:361–371
Davis TLO, Stanley CA (2002) Vertical and horizontal movements
of southern bluefin tuna (Thunnus maccoyii) in the Great Aus-
tralian Bight observed with ultrasonic telemetry. Fish Bull
100:448–465
Diggle PJ, Liang K-Y, Zeger SL (1994) Analysis of longitudinal
data. Oxford University Press, Oxford.
Graves JE, Kerstetter DW, Luckhurst BW, Prince ED (2003)
Habitat preferences of billfishes in the western North Atlan-
tic: applicability of archival tag data to habitat-based stock
assessment methodologies. ICCAT Coll Vol Sci Pap 55:594–
602
Gunn J, Block B (2001) Advances in acoustic, archival and satellite
tagging of tunas. In: Block BA, Stevens ED (eds) Tuna: phys-
iology, ecology and evolution. Academic Press, San Diego, pp
167–224
Gunn JS, Stevens JD, Davis TLO, Norman BM (1999) Observa-
tions on the short-term movements and behaviour of whale
sharks (Rhincodon typus) at Ningaloo Reef, Western Australia.
Mar Biol 135:553–559
Hinton MG, Nakano H (1996) Standardizing catch and effort
statistics using physiological, ecological, or behavioral con-
straints and environmental data, with an application to blue
marlin (Makaira nigricans) catch and effort data from Japanese
longline fisheries in the Pacific. Bull Inter-Am Trop Tuna
Comm 21:171–200
Holland KN, Brill RW, Chang RKC (1990) Horizontal and ver-
tical movements of Pacific blue marlin captured and released
using sportfishing gear. Fish Bull 88:397–402
Holland KN, Brill RW, Sibert JR, Fournier DA (1992) Physio-
logical and behavioral thermoregulation in bigeye tuna Thunnus
obesus. Nature 358:410–412
Hooge PN, Eichenlaub B (1997) Animal movement extension to
ArcView, version 2.04. Alaska Biological Science Center, US
Geological Survey, Anchorage, AK
ICCAT (2001) Report of the ICCAT workshop on bluefin mixing
(Madrid, 3–7 September, 2001). ICCAT working document
SCRS/01/20
Itoh T, Tsuji S, Nitta A (2003) Swimming depth, ambient water
temperature preference, and feeding frequency of young Pacific
bluefin tuna (Thunnus orientalis) determined with archival tags.
Fish Bull 101:535–544
Josse E, Bach P, Dagorn L (1998) Simultaneous sonic observations
of tuna movements and their prey by sonic tracking and
acoustic surveys. Hydrobiologia 372:61–69
Kitagawa T, Nakata H, Kimura S, Itoh T, Tsuji S, Nitta A (2000)
Effect of ambient temperature on the vertical distribution and
movement of Pacific bluefin tuna Thunnus thynnus orientalis.
Mar Ecol Prog Ser 206:251–260
Klimley AP, Beavers SC, Curtis TH, Jorgensen SJ (2002) Move-
ments and swimming behavior of three species of sharks in La
Jolla Canyon, California. Environ Biol Fish 63:117–135
Liang K-Y, Zeger SL (1986) Longitudinal data analysis using
generalized linear models. Biometrika 73:13–22
Lutcavage M, Kraus S (1995) The feasibility of direct photographic
assessment of giant bluefin tuna, Thunnus thynnus, in New
England waters. Fish Bull 93:495–503
Lutcavage M, Luckhurst B (2002) Consensus document: workshop
on the biology of bluefin tuna in the mid-Atlantic 5–7 May
2000, Hamilton, Bermuda. ICCAT Coll Vol Sci Pap 52:803–808
Lutcavage ME, Brill RW, Skomal GB, Chase BC, Howey PW
(1999) Results of pop-up satellite tagging of spawning size class
fish in the Gulf of Maine: do North Atlantic bluefin tuna spawn
in the mid-Atlantic? Can J Fish Aquat Sci 56:173–177
Lutcavage ME, Brill RW, Skomal GB, Chase BC, Goldstein JL,
Tutein J (2000) Tracking adult North Atlantic bluefin tuna
(Thunnus thynnus) in the northwestern Atlantic using ultrasonic
telemetry. Mar Biol 137:347–358
Marcinek DJ, Blackwell SB, Dewar H, Freund EV, Farwell C, Dau
D, Seitz AC, Block BA (2001) Depth and muscle temperature of
Pacific bluefin tuna examined with acoustic and pop-up satellite
archival tags. Mar Biol 138:869–885
Mather FJ (1974) The bluefin tuna situation. Proc 16th Annu Int
Game Fish Res Conf 17:93–106
Mather FJ, Mason JM Jr, Jones AC (1995) Historical document:
life history and fisheries of Atlantic bluefin tuna. NOAA
Technical Memorandum NMFS-SEFSC-370
Matthews FD, Damkaer DM, Knapp LW, Collette BB (1977)
Food of western North Atlantic tunas (Thunnus) and lancetfish
(Alepisaurus). NOAA Technical Report NMFS SSRF-706
McCullagh P, Nelder JA (1989) Generalized linear models. Chap-
man and Hall, London
McGowan MF, Richards WJ (1989) Bluefin tuna, Thunnus thynnus,
larvae in the Gulf Stream off the southeastern United States:
satellite and shipboard observations of their environment. Fish
Bull 87:615–631
Musyl MK, Brill RW, Curran DS, Gunn JS, Hartog JR, Hill RD,
Welch DW, Eveson JP, Boggs CH, Brainard RE (2001) Ability
422
of archival tags to provide estimates of geographical position
based on light intensity. In: Sibert JR, Nielsen JL (eds) Elec-
tronic tagging and tracking in marine fisheries. Kluwer,
Dordrecht, pp 343–367
Musyl MK, Brill RW, Boggs CH, Curran DS, Kazama TK, Seki
MP (2003) Vertical movements of bigeye tuna (Thunnus obesus)
associated with islands, buoys, and seamounts near the main
Hawaiian Islands from archival tagging data. Fish Oceanogr
12:152–169
Nakamura H (1965) Tuna distribution and migration. Fishing
News, London
NRC (National Research Council) (1994) An assessment of
Atlantic bluefin tuna. National Research Council. National
Academy Press, Washington, D.C.
Neill WH, Stevens ED (1974) Thermal inertia versus thermoregu-
lation in ‘warm’ turtles and tunas. Science 184:1008–1010
Neill WH, Chang RKC, Dizon AE (1976) Magnitude and eco-
logical implications of thermal inertia in skipjack tuna, Ka-
tsuwonus pelamis (Linnaeus). Environ Biol Fish 1:61–80
Nelson DR, McKibben JN, Strong WR Jr, Lowe CG, Sisneros JA,
Schroeder DM, Lavenberg RJ (1997) An acoustic tracking of a
megamouth shark, Megachasma pelagios: a crepuscular vertical
migrator. Environ Biol Fish 49:389–399
Nemerson D, Berkeley S, Safina C (2000) Spawning site fidelity in
Atlantic bluefin tuna, Thunnus thynnus: the use of size-fre-
quency analysis to test for the presence of migrant east Atlantic
bluefin tuna in the Gulf of Mexico spawning grounds. Fish Bull
98:118–126
Newlands NK, Lutcavage ME, Pitcher TJ (2004) Analysis of for-
aging movements of Atlantic bluefin tuna (Thunnus thynnus):
individuals switch between two modes of search behaviour.
Popul Ecol (in press)
Richards WJ (1976) Spawning of bluefin tuna (Thunnus thynnus)in
the Atlantic Ocean and adjacent seas. ICCAT Coll Vol Sci Pap
5(2):267–278
Rivas LR (1954) A preliminary report on the spawning of the
western north Atlantic bluefin tuna (Thunnus thynnus) in the
Straits of Florida. Bull Mar Sci Gulf Carib 4:302–322
Rodriguez-Roda J (1967) El atun, Thunnus thynnus (L.) del sur de
Espana, en la campana almadrabera del ano 1966. Invest Pesq
31:349–359
Roffer MA (1987) Influence of the environment on the distribution
and relative apparent abundance of juvenile Atlantic bluefin
tuna along the United States east coast. PhD thesis, University
of Miami
Roule L (1924) E
ˆtude sur les de
´placements et la peˆ che du thon
(Orcynus thynnus L.) en Tunisie et dans la Me
´diterrane
´e occi-
dentale. Bull Sta Oceanogr Salammbo 2:1–39
Schaefer KM (2001) Reproductive biology of tunas. In: Block BA,
Stevens ED (eds) Tuna: physiology, ecology and evolution.
Academic Press, San Diego, pp 225–270
Schaefer KM, Fuller DW (2002) Movements, behavior, and habitat
selection of bigeye tuna (Thunnus obesus) in the eastern equa-
torial Pacific, ascertained through archival tags. Fish Bull
100:765–788
Searle SR, Speed FM, Milliken GA (1980) Population marginal
means in the linear model: an alternative to least square means.
Am Stat 34:216–221
Secor DH, Campana SE, Zdanowicz VS, Lam JWH, Yang L,
Rooker JR (2002) Inter-laboratory comparison of Atlantic and
Mediterranean bluefin tuna otolith microconstituents. ICES J
Mar Sci 59:1294–1304
Sibert J, Fournier D (2001) Possible models for combining tracking
data with conventional tracking data. In: Sibert JR, Nielsen JL
(eds) Electronic tagging and tracking in marine fisheries. Klu-
wer, Dordrecht, pp 443–456
Sibert J, Musyl MK, Brill RW (2003) Horizontal movements of
bigeye tuna (Thunnus obesus) near Hawaii determined by Kal-
man filter analysis of archival tagging data. Fish Oceanogr
12:141–152
Silverman BW (1986) Density estimation for statistics and data
analysis. Chapman and Hall, London
Sissenwine MP, Mace PM, Powers JE, Scott GP (1998) A com-
mentary on western Atlantic bluefin tuna assessments. Trans
Am Fish Soc 127:838–855
Sokal RR, Rohlf FJ (1981) Biometry. Freeman, San Francisco
Suzuki Z, Ishizuka Y (1990) Comparison of population charac-
teristics of world bluefin stocks, with special reference to the
west Atlantic bluefin stock. ICCAT Coll Vol Sci Pap 35:240–
243
Tiews K (1963) Synopsis of biological data on bluefin tuna Thunnus
thynnus (Linnaeus) 1758 (Atlantic and Mediterranean). FAO
Fish Rep 6:422–481
Weihs D (1973) Mechanically efficient swimming techniques for
fish with negative buoyancy. J Mar Res 31:194–209
Werner FE, Blanton BO, Quinlan JA, Luettich RA Jr (1999)
Physical oceanography of the North Carolina continental shelf
during the fall and winter seasons: implications for the trans-
port of larval menhaden. Fish Oceanogr 8 [Suppl 2]:7–21
West GJ, Stevens JD (2001) Archival tagging of school shark,
Galeorhinus galeus, in Australia: initial results. Environ Biol
Fish 60:283–298
Westerberg H (1984) The orientation of fish and the vertical
stratification at fine- and micro-structure scales. In: McCleave
JD, Arnold GP Dodson JJ, Neill WH (eds) Mechanisms of
migration in fishes. Plenum Press, New York, pp 179–203
Wilson PC, Bartlett MR (1967) Inventory of U.S. exploratory
longline fishing effort and catch rates for tunas and swordfish in
the northwestern Atlantic 1957–1965. U.S. Fish Wildl Serv Spec
Sci Rep Fish 543:1–52
Worton BJ (1989) Kernel methods for estimating the utilization
distribution in home-range studies. Ecology 70:164–168
Young JW, Lamb TD, Le D, Bradford RW, Whitelaw AW (1997)
Feeding ecology and interannual variations in diet of southern
bluefin tuna, Thunnus maccoyii, in relation to coastal and oce-
anic waters off eastern Tasmania, Australia. Environ Biol Fish
50:275–291
Yuen HSH (1970) Behavior of skipjack tuna, Katsuwonus pelamis,
as determined by tracking with ultrasonic telemetry. J Fish Res
Board Can 27:2071–2079
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