l\
FiS^
U.S. Department
of Commerce
Volume 114
Number 3
July 2016
Fishery
Bulletin
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National Marine
Fisheries Service
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for Fisheries
' V
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Richard Brodeur National Marine Fisheries Service, Newport, Oregon
John Carison National Marine Fisheries Service, Panama City, Florida
Kevin Craig National Marine Fisheries Service, Beaufort, North Carolina
John Graves Virginia Institute of Marine Science, Gloucester Point, Virginia
Rich McBride National Marine Fisheries Service, Woods Hole, Massachusetts
Rick Methot National Marine Fisheries Service, Seattle, Washington
Bruce Mundy National Marine Fisheries Service, Honolulu, Hawaii
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Dave Somerton National Marine Fisheries Service, Seattle, Washington
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U.S. Department
of Commerce
Seattle, Washington
Volyme 114
Number 3
July 201fi
Fishery
Bulletin
Contents
Articles
261 -273 Walker, Justin H. , Arthur C. Trembanis, and Douglas C. Miller
Assessing the use of a camera system within an autonomous underwater
vehicle for monitoring the distribution and density of sea scallops
IPlacopecten mageHanicus) in the Mid-Atiantic Bight
274-287 Van Noord, Joel E., Robert J. Olson, Jessica V. Redfern, Leanne M. Duffy,
and Ronald S. Kaufmann
Oceanographic influences on the diet of 3 surface-migrating mytophids in
the eastern tropical Pacific Ocean
288-301 Caldarone, Elaine M., Sharon A. Maclean, and Brian R. Beckman
Evaluation of nucleic adds and plasma IGF1 levels for estimating short-term
responses of postsmolt Atlantic salmon (Salmo salar) to food availability
The National Marine Fisheries
Service (NMFS) does not approve,
recommend, or endorse any proprie-
tary product or proprietary material
mentioned in this publication. No
reference shall be made to NMFS,
or to this publication furnished by
NMFS, in any advertising or sales
promotion which would indicate or
imply that NMFS approves, rec-
ommends, or endorses any propri-
etary product or proprietary mate-
rial mentioned herein, or which has
as its purpose an intent to cause
directly or indirectly the advertised
product to be used or purchased be-
cause of this NMFS publication.
302-316 LeClair, Larry L, Ocean Eveningsong, and Jesse M. Schultz
Seasonal changes in abundance and compelling evidence of migration
for 2 rockfish species ISebastes aurkulatus and S. caurinus) inhabiting a
nearshore, temperate-water artificial reef
317-329 Goldman, Sarah F., Dawn M. Glasgow, and Michelle M. Falk
Feeding habits of 2 reef-associated fishes, red porgy (Pagrus pagrus) and
gray triggerfish (Balistes capriscus), off the southeastern United States
330-342 Syah, Achmad F., Sei-lchi Saitoh, Irene D. Alabia, and Toru Hirawake
The NMFS Scientific Publications
Office is not responsible for the con-
tents of the articles.
Predicting potential fishing zones for Pacific saury (Cololabis saira) with
maximum entropy models and remotely sensed data
Fishery Bulletin 114(2)
343-359 Stevens, Bradley G., and Vincent Guida
Depth and temperature distribution, morphometries, and sex ratios of red deepsea crab iChaceon quinquedens) at 4
sampling sites in the Mid-Atlantic Bight
360-369 Weinberg, Kenneth L , Cynthia Yeung, David A. Somerton, Grant G. Thompson, and Patrick H. Ressler
is the survey selectivity curve for Pacific cod iGodus microcephalus) dome-shaped? Direct evidence from trawl studies
Short communication
370-372 Willey, Angel L, Linda S. Barker, and Mark Sampson
A comparison of circle hook and J hook performance in the recreational shark fishery off Maryland
373-376 Guidelines for authors
261
NOAA
National Marine
Fisheries Service
Fishery Bulletin
<%• established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Assessing the use of a camera system within an
autonomous underwater wehicle for monitoring the
distribution and density of sea sollops IPIacopecten
mageHanicm} in the Mid-Atlantic Bight
Abstract~The sea scallop (Placo-
pecten magellanicus) fishery in the
Atlantic is assessed during annual
surveys by using both dredging
and surface-deployed imaging tech-
niques. In this pilot study in the
Mid-Atlantic Bight, we used an au-
tonomous underv/ater vehicle (AUV)
to photograph the seafloor and to
evaluate its use for determining
scallop density and size. During 22
surveys in 2011, 257 km of seafloor
were photographed, resulting in over
203,000 color images. Using trained
annotators and photogrammetric
software, we determined scallop
density and shell heights for 15,252
scallops. The inshore scallop grounds
near Long Island (at depths <40 m)
had a density of 0.077 scallops per
m^, whereas the inshore grounds
of the New York Bight had a den-
sity of 0.012 scallops per m^. Shell
heights derived from images were
found to agree well with measure-
ments from scallops collected with
a commercial dredge. We show that
images obtained with an AUV can be
used to reliably estimate both den-
sity and shell height consistent with
direct sampling from the same area.
Moreover, side-scan sonar images
obtained v/ith an AUV can be used
to detect dredge scars and, there-
fore, can provide a simultaneous,
relative estimate of fishing effort in
that area. AUVs provide a highly ac-
curate suite of data for each survey
site and therefore allow the design
of experimental studies of fishing
practices.
Manuscript submitted 9 April 2015.
Manuscript accepted 22 March 2016.
Fish. Bull. 114:261-273 (2016).
Online publication date: 26 April 2016.
doi: 10.7755/FB.114.3.1
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Justin H= Walker’
Arthur C. Trembanis (contact author)’'*
Douglas C, Miller*
Email address for contact author: art@udel.edu
’ Department of Geological Sciences
University of Delaware
109 Penny Hail
Newark, Delaware 19716
2 School of Marine Science and Policy
University of Delaware
Lewes, Delaware 19958
The sea scallop iPlacopecten magel-
lanicus, Gmelin 1791) of the Mid-
Atlantic Bight Atlantic fishery has
been commercially active for over 100
years, and in recent years has con-
sistently ranked in the top five most
valuable domestic U.S. fisheries at
around a half billion dollars (NMFS,
2009-2013). To promote the sustain-
ability of the sea scallop fishery, the
National Marine Fisheries Service
(NMFS) monitors the fishery annually
through a combination of survey ap-
proaches (Stokesbury et al., 2004; Kel-
lyi; DuPaul and Rudders^; NEFSC^;
’ Kelly, K. H. 2007. Results from the
2006 Maine sea scallop survey, 34 p.
Maine Dep. Mar. Res., W. Boothbay Har-
bor, ME. [Available at website.)
2 DuPaul, W. D., and D. B. Rudders.
2008. An assessment of sea scallop
abundance and distribution in selected
closed areas: Georges Bank area I and
II, Nantucket Lightship and Elephant
Trunk. VIMS Mar. Res. Rep. 2008-3, 47
p. Virginia Institute of Marine Science,
College of William and Mary, Gloucester
Point, VA. [Available at website.]
® NEFSC (Northeast Fisheries Science
Center). 2010. 50th northeast re-
gional stock assessment workshop (50th
Rudders and DuPauF). The results of
these monitoring efforts are used to
determine annual catch limits that
balance overfishing and sustainabil-
ity against potentially unnecessary
economic loss (Rosenberg, 2003; Nai-
du and Robert, 2006).
The sea scallop fishery stock is
monitored by means of both dredge
surveys (DuPaul and Rudders^;
NEFSC^), and drop-camera surveys
(Jacobson et al., 2010; Carey and
Stokesbury 2011; Stokesbury, 2012;
Hart et al., 2013). Dredging is per-
formed by towing either a commer-
cial or scientific survey dredge across
the seafloor and has a direct impact
on scallops, bycatch organisms, and
SAW) assessment report. Northeast
Fish. Sci. Cent. Ref. Doc. 10-17, 844 p.
[Available at website.)
^ Rudders, D. B., and W. D. DuPaul.
2012. An assessment of sea scallop
abundance and distribution in open
access areas: New York Bight and the
southern New England area. VIMS
Mar. Res. Rep. 2012-8, 48 p. Virginia
Institute of Marine Science, College of
William and Mary, Gloucester Point,
VA. [Available at website.)
262
Fishery Bulletin 114(3)
the seafloor itself. Imagery-based surveys have fewer
direct impacts on the seafloor and its inhabitants and
have the advantage of covering large areas efficiently.
Early studies were performed with cameras mounted
on a rigid stationary pyramid-shaped platform that
was lowered from a vessel to the seafloor (Stokesbury,
2002). More recently the HabCam system has been de-
veloped, which is a towed camera sled tethered to a
ship, and it can photograph long stretches of the sea-
floor (Rosenkranz et ah, 2008). In 2010, the National
Marine Fisheries Service (NMFS) formally expressed
the need to develop and apply new approaches to stock
assessment of sea scallop in the Mid-Atlantic Bight
(NMFS, 2010). A recent NOAA-sponsored workshop
(NOAA®) gathered numerous researchers engaged in
seabed imaging to highlight the development of a va-
riety of imaging platforms, and among their findings,
the potential value of autonomous imaging platforms
was recognized for future survey efforts. The present
study is a an application of those recommendations by
extending previous smaller scale camera studies with
the use of autonomous underwater vehicles (AUVs) in
Iceland (Singh et ah, 2013 and 2014) to a larger spatial
scale study through surveys conducted within the Mid-
Atlantic Bight.
AUVs have been shown to be an effective platform
for mapping benthic habitat (Tolimieri et ah, 2008;
Forrest et ah, 2012; Raineault et ah, 2012; Seiler et
ah, 2012; Raineault et ah, 2013) by coupling images
obtained by underwater camera with highly accurate
preprogrammed navigation. In this study, we used an
AUV to assess sea scallop shell height and abundance,
as well to estimate biomass in the shallow (< 40 m)
open scallop fishing grounds within the Mid-Atlantic
Bight. Because shallow grounds are not typically with-
in the scope of the annual NMFS survey, this study
offers unique findings of the sea scallop populations in
such areas. Moreover, our results show that an AUV is
a suitable platform for collecting images as part of the
sea scallop stock assessment process. Our goal in this
pilot study was to test and show the feasibility of the
AUV platform by using synchronous commercial dredg-
ing samples to illustrate the efficacy of the underwater
camera system for what could be scaled up to be a use-
ful tool for a full stock assessment process.
Materials and methods
Field sampling
The Mid-Atlantic Bight is the shallow portion of the
continental shelf that extends from Cape Hatteras,
NC, to Cape Cod, MA. Our study area was selected to
fulfill the needs of the Mid-Atlantic Fishery Manage-
® NOAA. 2014. Undersea Imaging Workshop: workshop re-
port; Red Bank, N.J., 14-15 January, 34 p. New Jersey Sea
Grant Consortium, NOAA, Fort Hancock, NJ. [Available at
website.]
ment Council’s Research Set-Aside (RSA) program to
survey heavily fished inshore scallop grounds (<40 m
depth) that are not regularly monitored. All of the AUV
surveys reported here were conducted in the New York
Bight (NYB) and Long Island (LI) regions during July
2011 (Fig. 1).
As part of their survey sampling design, the Na-
tional Marine Fisheries Service uses a 30x30 minute
latitude/longitude grid system. Our AUV surveys were
executed at randomly selected sites within each block
area of an 8-block grid. They involved photographically
surveying at least 37,500 m^ of seafloor at two or more
sites within each grid. Sites were either chosen from
recent NMFS survey sites for scallop stocks or were
randomly chosen from within each grid to meet the
predetermined total area. All of the surveys were con-
ducted within 70 km of the coast of Delaware, New Jer-
sey, or New York, and the water depths sampled ranged
from 20 to 50 m (Table 1), which is within the normal
habitable zone for the sea scallop (Merrill®; Hart and
Chute, 2004). Extensive details of the sampling design
were compiled in the master’s thesis for the pilot study
(Walker, 2013) and were reviewed and approved by both
an internal and external panel of scientists selected by
NMFS as part of the final project review process.
Survey design
At each site, we deployed the AUV on a preplanned
path that ranged from 3 to 16 kilometers of contigu-
ous survey trackline. Surveys lasted up to 3 hours, an
operational limit imposed by the life of a single battery
pack. The AUV was programmed in a terrain-following
mode with a commanded altitude of 2.2 m. Postprocess-
ing analysis of the survey logs showed that the AUV
remained within a 16 cm standard deviation of the 2.2
m commanded altitude, a deviation that is consistent
with previous studies in which the same vehicle sys-
tem has been used (e.g., Forrest et ah, 2012; Raineault
et ah, 2012). Precise navigation of the vehicle is ac-
complished by using a DVL-aided (Doppler Velocity
Log) INS (Inertial Navigation System), which has been
shown in the literature to provide a positional drift
rate of 0.5 m/h (Patterson et al., 2008) or 0.1% of dis-
tance traveled (Rankey and Doolittle, 2012). Compari-
son of known targets (such as stationary man-made ob-
jects on the seafloor) in side-scan sonar imagery from
repeated passes showed positional precision of within 2
m from one survey to the next — a level that is consis-
tent with results from other published benthic habitat
mapping studies conducted with this same vehicle sys-
tem (e.g., Forrest et al., 2012; Raineault et al., 2013).
Because this was a pilot study, several trackline
designs were tested to determine the most effective
geometric design for image and acoustic sampling. The
survey design that we used most often comprised a se-
ries of parallel boustrophedon lines, commonly known
® Merrill, A. S. 1971. The sea scallop. In Annual report for
1970, p. 24-27. Am. Malacol. Union Inc.
Walker et al.: Use of an underwater camera to monitor distribution and density of Piacopecten magellanicus
263
Figure 1
A map of the Mid-Atlantic Bight showing the sites where photographs of the sea bottom
and sea scallops {Piacopecten magellanicus) were taken with an underwater camera from
an autonomous underwater vehicle (AUV) at 22 survey sites in 2011.
as a “lawn mower” pattern. Multiple equidistant tran-
sects were run parallel to each other at a commanded
even spacing that ranged between 2 to 40 m laterally.
This method had the advantage of allowing 100% im-
aging and side-scan sonar coverage depending on tran-
sect spacing. Less frequently, our survey design con-
sisted of equidistant oblique transects that propagated
along only one of the transect axes in a slalom path.
This design would be most useful for sampling an elon-
gated bed of scallops. The third most used survey de-
sign consisted of equidistant orthogonal transects that
propagated along both transect axes (in the profile of
a staircase). This design provided the largest extent of
geographic coverage from a single battery charge.
Equipment
Our surface vessel was the FV Christian and Alexa,
a 30-m eastern rig, commercial fishing ship with port
and starboard New Bedford style 15-ft (4.57-m) scallop
dredges. For comparison of the AUV imagery data, each
survey site was dredged immediately after the AUV
survey with the starboard scallop dredge by towing for
15 minutes at 4.5 to 5.0 knots at every site along the
initial AUV transect line. The dredges were fitted with
4-inch (10.2-cm) interlocking rings to coincide with
commercial fishing requirements, along with an 11-
inch (27.9-cm) twine mesh top and turtle chains. Shell-
height-frequency data were collected on the deck from
the dredged contents by using standard survey meth-
ods for sizing a randomly selected bushel of scallops.
The photographic imaging platform used was a Tele-
dyne Gavia AUV that has an operational depth limit
of 500 m. The AUV was run in an imaging and sonar
mapping configuration consisting (from front to back)
of a nose cone camera, lithium ion battery module,
GeoSwath phase measuring bathymetric sonar (500
kHz) module, Kearfott T-24 inertial navigation sys-
tem (INS) and Doppler velocity log (DVL), command
module (900/1800 kHz Marine Sonic side-scan sonar),
and a propulsion module. During a survey, the AUV
can simultaneously optically image the seafloor, map
the seafloor with side-scan sonar and phase measuring
bathymetric sonar, log depth and altitude of the vehi-
cle, and measure water temperature, dissolved oxygen
saturation, turbidity, and salinity.
The nose cone camera was a Point Grey Scorpion
20SO research camera, equipped with a Sony ICX274
Type 1/1.8” (8.923 mm diagonal) CCD camera, with a
resolution of 800x600 pixels. This camera was config-
ured to acquire images at a rate of 3.75 images per
second. Illumination was provided by LED strobe array,
positioned obliquely aft of the camera. The camera has
a Fujinon DF6HA-1B 6-mm focal length lens and a hor-
izontal viewing angle of 44.65° in salt water based on
a salinity of 35 (PSU). Calibration results determined
264
Fishery Bulletin 114(3)
Table 1
Summary of environmental data and measurements of sea scallops (Placopecten magellanicus) derived from photographs
taken with an underwater camera within an autonomous underwater vehicle (AUV) during surveys within the Long Island
(LI) and New York Bight (NYB) areas.
AUV
survey
site
Latitude
(°)
Longitude
n
Bottom
Water water Survey
depth temperature distance
(m) (“O (m)
Survey
area
(m^)
Number
of bottom
images
Number
of
scallops
Scallop
density
scallops/m^)
Mean
shell
height
(mm)
Mean
meat
weight
(g/scallop)
Long Island
LIl
40.5529
-72.5899
41.9
8.8
15,904
26,834
14,742
2,172
0.081
121.1
37.0
area
LI2
40.5503
-72.5872
43.5
8.8
3,015
5,280
2,387
894
0.169
119.6
35.2
LI3
40.4712
-72.5294
45.4
8.5
10,337
18,135
8,065
3,706
0.204
103.7
23.7
LI4
40.3449
-72.8817
45.8
8.6
12,280
21,689
9,992
1,365
0.063
101.4
21.8
LI5
40.3111
-73.0825
42.1
8.9
10,773
19,085
8,338
1,850
0.097
102.8
23.6
LI6
40.3961
-73.3818
31.7
11.9
14,211
23,473
11,329
422
0.018
100.0
25.3
LI7
40.3551
-73.3483
33.7
10.8
12,271
20,384
10,163
227
0.011
112.6
33.5
LIS
40.3213
-73.2749
35.3
9.8
12,154
21,328
9,780
1,403
0.066
104.2
26.5
Mean
Mean
Total
Total
Total
Total
Mean
Mean
Mean
Summary
39.3
9.6
90,945
156,208
74,796
12,039
0.077
107.7
27.3
New York
Bight area
NYBl
40.2368
-73.7828
35.5
11.0
10,398
17,684
9,141
82
0.005
106.4
28.4
NYB2
40.0279
-73.8078
27.7
11.5
12,511
21,000
9,523
16
0.001
112.5
37.0
NYB3
39.5942
-73.5386
41.5
8.4
11,691
19,079
9,544
508
0.027
116.4
35.5
NYB4
39.8873
-73.6105
32.8
9.1
12,181
19,069
9,479
212
0.011
130.2
51.4
NYB5
39.9019
-73.5318
36.9
9.2
11,752
20,440
9,425
801
0.039
117.2
36.7
NYB6
39.9793
-73.6383
37.9
9.4
12,133
20,036
9,281
331
0.017
119.7
37.7
NYB7
39.2332
-73.6423
46.6
8.0
12,196
18,228
12,068
506
0.028
121.0
35.9
NYB8
39.3621
-73.5099
50.7
8.2
12,149
20,006
9,572
140
0.007
120.6
37.2
NYB9
39.3266
-73.7925
40.0
9.5
13,086
21,704
10,950
523
0.024
128.9
45.8
NYBIO
39.1000
-74.4470
21.9
11.6
11,791
19,740
9,170
3
<0.001
92.2
23.3
NYBll
39.1431
-74.0397
38.7
10.0
13,499
23,559
7,050
1
<0.001
86.8
14.0
NYB12
39.1431
-74.0397
28.2
11.6
12,207
20,700
7,345
0
0
-
-
NYB13
39.4200
-74.0267
20.1
12.7
8,292
13,494
6,285
0
0
-
-
NYB14
39.0950
-73.984
42.0
9.2
12,331
21,334
9,437
90
0.004
126.7
43.6
Mean
Mean
Total
Total
Total
Total
Mean
Mean
Mean
Summary
36.2
9.9
166,218
276,073
128,270
3,213
0.012
120.8
38.9
from a set of images taken within a test tank described
below show that scale distortions in relation to the im-
age center were less than 2 pixels over 65% of the full
frame (Fig. 2). Each image had a metadata header that
contained navigation (i.e. latitude, longitude, altitude,
depth, etc.) and near seafloor environmental conditions
corresponding to the capture time of the photo from the
sensors of the AUV.
Calibration of the camera system was conducted
with photos gathered with the AUV camera system in
a saltwater tank. The calibration process entailed a se-
quence of images of a standard planar checkerboard
pattern viewed from multiple angles and processed by
using the Camera Calibration Toolbox for Matlab de-
veloped by Bouguet (2011) and based on the models
of Zhang (2000) and Heikkila and Silven (1997). The
analysis (Fig. 2) provided a direct quantitative measure
of the camera field of view (FOV) and showed that min-
imal radial and tangential lens distortion affected the
camera. These results agreed closely with previously
published results from the same AUV and camera sys-
tems (Gudmundsson, 2012; Singh et al. 2013; Singh et
ah, 2014 ) and were further confirmed by independent
analysis of the images (Rzhanov'^).
The camera calibration (Fig. 2) showed the spatial
pattern as that of the AUV camera, namely the impact
of spherical and tangential lens distortion at each pix-
el point within the full image frame. Most of the area
within each image (65%) exhibits distortion of less than
2 pixels (~5 mm in ground distance), except for the up-
per and lower left corners, which have 7 or more pixels
of displacement (~16 mm in on the ground distance),
representing a maximum error of <1% of total pixel
width. These distortions will have generally less than
1% impact on the estimation of scallop shell height be-
cause the average distortion of 1-2 pixels translates to
^ Rzhanov, Y. 2015. Personal commun. Center for Coastal
and Ocean Mapping, Univ. New Hampshire, Durham, NH
03824.
Walker et al.: Use of an underwater camera to monitor distribution and density of Placopecten magellanicus
265
Distortion contours (measured from 1 to 7 pixels) in rela-
tion to the center of an image for the AUVs underwater
camera used in a study of the distribution and abundance
of the sea scallop {Placopecten magellanicus) during 2011.
and used to correct the calculation, although in other
studies (Gudmundsson, 2012; Singh et ah, 2013, 2014)
both pitch and roll were found to be negligible factors.
Not accounting for pitch would have resulted in a po-
tential 3% (mean) overestimation of image height for
all of the photos. For Equation 1, the AUV is assumed
to image a flat seafloor over the area of the full frame,
and the equation also does not account for roll of the
vehicle. The roll-induced error associated with image
width is less than 1.0% (at 2 m altitude) if vehicle roll
is less than 10° from horizontal, and log data showed
that the AUV operated with roll characteristics of
x=4.01°C and cf=1.11° for all survey sites. Singh et al.
(2013 and 2014) reported a similar ground distance er-
ror (<2%) due to both AUV pitch and roll for the same
Scorpion 20SO camera when surveying at an altitude
of 2 m. Similarly, Gudmundsson (2012) performed as
detailed a calibration of the same AUV camera system
as that used in our study and reported negligible ef-
fects of camera distortion, pitch, and roll.
Scallop counts and sizing
between 0.23 and 0.46 cm in distance on the ground.
This distortion uncertainty is approximately within
<5% of the average shell height directly measured in
the dredge tow samples, with which the image-based
measurements were favorably compared. It is impor-
tant to note, however, that camera distortions have no
impact on the enumeration of scallops and the result-
ing analysis of scallop counts. In previously published
studies of sea scallop shell height and abundance, this
same combination of AUV camera was used and cali-
brated camera distortions along with both pitch and
roll of the AUV were found to be negligible (GuSmunds-
son, 2012; Singh et al. 2013; Singh et al., 2014). Our
study, therefore, is consistent with the findings of the
previous research cited above, suggesting that the in-
fluence of roll bias (< 1%), camera distortions (< 1%),
and manual digitization (< 1%) overall contributes less
than 5% uncertainty for estimates of shell height. The
width (W) of a single image was determined by using
the image metadata collected by the AUV navigational
system and sensors.
W = 2tan
[z-1.3siii(-0 )],
(Eq. 1)
where W =
a,, =
2 =
0p =
seafloor image width in meters;
horizontal viewing angle (degrees) of the
camera in water;
height above the seafloor in meters; and
pitch of the AUV in degrees.
Knowing the horizontal viewing angle of the cam-
era in water (a;,=44,65°), and the height above the sea-
floor iz), we were able to calculate real world dimen-
sions on the seafloor in each image. The pitch of the
AUV (Op) and the arm length (1.3 m) from the camera
to the AUV navigational reference point were known
The 22 AUV surveys resulted in 203,066 images of
the seafloor; see Figure 3 for a selection of represen-
tative images. In order to process all of the images,
we engaged a team of graduate students and interns
to count and size scallops using software written in-
house for this project. Each scallop annotator received
training on identifying sea scallops in benthic images,
and was required to successfully identify at least 95%
of the scallops from a standardized image data set be-
fore being allowed to annotate the rest of the images.
Repeated digital measurement of the same scallop by
the same annotator (N=53, where N is the number of
sea scallops) yielded a standard deviation of 5.0 mm
in shell height measurement. This value of annotation
repeatability for size determination is in agreement
with the 5 mm annotator measurement error reported
by Singh et al. (2014). Furthermore, it is worth noting
that in comparison with manually sized scallops from
dredge samples, manually sizing was itself segmented
into 5-mm bin intervals and thus the discretization of
image-based sizes was on par with the discretization
from physical samples. The protocol used for image se-
lection and sizing was the following:
1 All images that were taken at a height between 1.5
m and 2.5 m above the seafloor were counted (re-
moving the starting descent and ending ascent por-
tions of each survey).
2 Each sea scallop in an image was counted individu-
ally, unless it had already been counted from the
previous image that overlapped the same section of
seafloor. Annotators examined photos sequentially
and were trained to recognize overlapped images, so
that scallops were not counted more than once.
3 Each scallop shell height was sized on the basis of
the distance from the shell umbo to the ventral mar-
gin by using a pixel-measuring tool. The projected
266
Fishery Bulletin 1 14(3)
i
* . • ^ 't
' *■ * , • *
Figure 3
Representative examples of images from the database of photographs from the 2011 survey
of sea scallops (Placopecten magellanicus) in the Long Island and New York Bight areas.
The sea bottom was photographed with an underwater camera mounted inside the nose cone
of an autonomous underwater vehicle. Images A, C, D, and E show sea scallops resting on
the seafloor. Images B and F show other species incidentally photographed during the AUV
surveys including crabs, fish, and skates.
on-the-ground length represented by the pixels was
then calculated from the metadata of each image
(e.g., altitude, pitch, and camera FOV) with Equa-
tion 1.
4 Shell height was not recorded if more than half
of the entire scallop was not contained within the
frame.
5 Scallops identified as disarticulated shells were nei-
ther counted nor sized.
6 The final count for a survey was the number of scal-
lops that could be sized.
Scallop densities were calculated for each survey
site. The number of scallops that were identified and
sized for each survey were summed and divided by the
area of the seafloor that had been photographed. In or-
der to limit the effect of image overlap (as much as 5%
in the current surveys), the AUV transect length was
calculated from the global positioning system (GPS)
start and end point of each survey line. The transect
length was then multiplied by the mean image width
for that transect, and the vehicle control kept the AUV
to v/ithin 16 cm standard deviation of the 2.2 m alti-
Walker et al.: Use of an underwater camera to monitor distribution and density of Placopecten magellanicus
267
tilde set point along the trackline. As part of the image
analysis and review process, annotators classified the
quality of each image on the basis of whether the im-
age was out of focus, too dark, or the water was too tur-
bid for scallops to be recognized. More than 95% of all
the images v/ere of sufficient quality for the annotators
to recognize, count, and size the scallops. It is worth
noting that many towed camera systems have only a
fractional portion of the images annotated, whereas we
were able to annotate all of our images. Additionally,
the stability of the AUV platform ensured that fewer
images (<5%) were removed with altitude or image
quality filtering.
Biomass
Because our project methods were based on seabed im-
ages, we used an empirical relationship from the litera-
ture to estimate the meat weight of scallops for com-
parative purposes. This parameter has been shown to
vary on the basis of a number of geographical and en-
vironmental factors and decreases with depth (Hennen
and Hart, 2012). The equation chosen from Rothschild
et al. (2009) is based on meat-weight measurements
of sea scallops dredged from within the Mid-Atlantic
Bight (the study area) and therefore was not further
corrected for latitude and longitude. The meat-weight
biomass was calculated for each scallop by using the
photogrammetrically measured shell height of each
scallop and the depth recorded for each image with the
following equation:
W (Eq. 2)
where = meat-weight biomass of the sea scallop in
grams;
1^5= shell height of the sea scallop in
millimeters;
d - depth of the sea scallop in meters.
Fishing effort
Commercial fishing dredges create distinctive pat-
terns of sediment disturbance on the seafloor, and
these dredge scars are visible with side scan sonar
(Dickson et al., 1978; NRC, 2002; Lucchetti and Sala,
2012; Krumholz and Brennan, 2015). For each survey,
the dredge marks were determined from the side-scan
data collected by the AUV at the same time that the
photos were gathered. SonarV/iz 5 (Chesapeake Tech-
nology Inc., Mountain View, CA) was used to process
the acoustic data collected by the 900 kHz side-scan
sonar and gridded at a 0.25x0.25 m horizontal resolu-
tion for inspection. Each dredge scar was then manu-
ally traced in each side-scan mosaic by using the So-
narWiz digitizing tool. The track length was then mul-
tiplied by the measured width of the dredge scar (4.57
m) to determine the total area of the dredge scar. The
area dredged was compared with the area acoustically
surveyed (survey track length multiplied by a 20-m
swath width) to give a ratio that represented a mea-
sure of recent fishing effort. For one site, we ran the
AUV both before and after the dredge and verified
that our dredge track was visible in the side-scan im-
agery. In most of the sonar mosaic images there were
many dredge marks visible such that our sampling
mark was only a small fraction of the total estimated
dredge area.
Results
Over the 10-day cruise in July 2011, we completed 22
surveys with the AUV and covered 257 km of track
line for a combined surveyed area of 490,000 m^. In
all, 203,000 images of the seafloor were produced, from
which annotators identified and digitally sized 15,252
sea scallops.
Scallop density
The New York Bight (NYB) region was surveyed over
14 discrete sites and sea scallops were identified from
images collected from 12 of those sites (i.e., 2 survey
sites had no scallops). Overall, 276,000 of seafloor
were surveyed (optically and acoustically) in the NYB,
and densities for each survey ranged from 0 to 0.039
scallops per (Table 1). The area-weighted mean
scallop density for the region was 0.012 scallops per
m^. The 6 sites that had scallop densities «0.01 scal-
lops per were the shallowest surveys (20.1-35.5 m)
and also coincided with the warmest near bottom tem-
peratures (10.0-12.7°C). We also observed that these
sites typically had dense sand dollar populations.
The histogram in Figure 4A shows the shell-height
frequency for all of the photogrammetrically sized sea
scallops within the NYB. Taken together, 1.5% (48) of
the 3,213 sized scallops fell into the recruit size class
(<70 mm), and 13.8% were of a size larger than that of
recruits but smaller than the 4" dredge rings (>70 mm
and <101.6 mm). The harvestable size class accounted
for the remaining 84.7%, which results in an exploit-
able (harvestable) scallop density of 0.010 scallops per
for NYB. The mean shell height for the NYB region
was found to be 121 mm. These results indicate that
the NYB had a size population dominated by large har-
vestable scallops.
The Long Island (LI) region was surveyed at 8
distinct sites, and an area of over 156,000 of sea-
floor was photographed in the region. The sea scal-
lop density was 0.077 scallops per m^, and there was
a large variability in densities ranging from 0.01 to
0.20 scallops per (Table 1). As found in the NYB
region, the denser scallop populations were found at
near bed temperatures of 8-9°C, whereas the warmer
(>10°C), shallower survey sites had the lowest popula-
tion densities.
The distribution of shell heights in the LI region is
shov/n in Figure 4B. Of the 12,039 scallops that were
sized, 61.2% (7,368) were classified as harvestable and
268
Fishery Bulletin 114(3)
CO
Q.
o
"cc
o
CO
I I Recruit (1 .5%)
ES£]Sublegal(13.8%)
Harvestable (84.7%)
Shell height (mm)
"O
CD
o
CD
3
S'
CQ
CD
Shell height (mm)
Figure 4
Frequency histograms of digitally sized shell heights (in
millimeters) of sea scallops {Placopecten magellanicus)
within (A) New York Bight (3213 sea scallops) and (B)
Long Island areas (12,039 sea scallops).
37.9% (4,563) were classified as larger than the size of
recruits but smaller than the 4" rings. This distribu-
tion yields an exploitable scallop density (of harvest-
able size scallops) of 0.047 scallops per m^. The re-
maining 0.9% (108) scallops were classified as recruits.
The mean shell height for the region was 108 mm. As
with the NYB sites, the scallop population was found
to be dominated by scallops with a large shell height
and only a small number of recruit-size scallops were
observed (Fig. 5).
Comparisons of results from dredge tows with those
from camera imagery were performed for a subset
of the surveys from the NYB region (NYB4-8). The
dredged scallops were manually sized into 5-mm bins.
The dredged scallop sizes were compared with shell-
height sizes obtained with the AUV from the same
surveys by using size-class distribution plots (Fig. 6).
The means of the manually measured scallop shell
heights obtained with dredging (range of mean values
122-135 mm, N=54-22,) were found to be within 6%
of the co-located AUV image-sized shell height means
(range of mean values 117-130 mm, N=140-801, Fig.
6). The lower means of the AUV image-sized scallops
are expected because recruit-size scallops are included
within the distribution. By design, dredges do not ac-
curately sample scallops under 101.6 mm (4" diameter
ring), thereby skewing the shell height distribution to-
ward larger sizes (Yochum and DuPaul, 2008).
Biomass
Using a published equation (Eq. 2) we calculated the
meat weight of each individual scallop from the shell
height measurements derived from AUV images and
the results are plotted in Figure 7. The majority of
sea scallop biomass off LI is due to a high frequency
of smaller meat weights (10-30 g each). The highest
density sites in the LI region were typically coincident
with smaller shell heights. The bulk of sea scallop bio-
mass in the NYB region is due to a higher frequency of
meat weights ranging from 30-50 g each.
Fishing effort
Digitized dredge scars in the side-scan mosaics re-
vealed that over 174,000 m^ or 35.5% of the total
surveyed seafloor area showed signs of dredging. We
found that higher dredging effort (>7% of the bottom
area dredged) coincided with the highest scallop den-
sities, whereas a low scallop density area typically
showed little or no dredging. It was not uncommon for
a site to have a single dredge scar from a commercial
vessel — perhaps the mark of a test dredge tow that
did not yield a large enough catch for continued fish-
ing effort.
There was a noticeable difference between fishing
efforts in LI and NYB. We found that the NYB had
significantly less dredging (5% overall) than that
found in the LI region. The scallop densities at all
NYB sites were considerably less than those at LI
counterparts. NYB8 had the most concentrated dredg-
ing in the region with 11.9% of the area dredged. In
addition, the shell height distributions for the heavily
fished sites were positively skewed because of the size
selectivity of the commercial scallop dredge (Fig. 5).
The LI sites had an overall density 7 times that of
the NYB region. As a result, the LI region had sig-
nificant commercial dredging >18% of the total area
dredged for 5 out of the 8 survey sites. Operationally,
digitizing dredge scars did not add significant process-
ing time of the data. After side-scan sonar mosaics
had been produced for each site, it took a total of 8
man-hours to manually digitize and calculate the area
dredged for all 22 survey sites.
Walker et aL: Use of an underwater camera to monitor distribution and density of Placopecten magellanicus
269
Figure 5
Boxplots of shell heights of sea scallops {Placopecten magellanicus) obtained from photo-
graphs taken with an underwater camera of an autonomous underwater vehicle with the
Long Island (LI) and New York Bight (NYB) areas. Surveys where <16 sea scallops were
collected were not plotted.
Discussion
Automated underwater vehide as an image-produdng
survey platform
The AUV is an efficient platform that allows surveys
from images (optical and acoustical simultaneously)
over 15 km of seafloor on a single battery charge, and
allows the noninvasive study of benthic organisms over
any bed type, including rocky or uneven terrain that
would be difficult or impossible for dredges. For sea
scallops, we found that an altitude of 2.2 m allov/ed for
the largest image area, while still maintaining visibil-
ity and resolution to size scallops. Particulate matter
in the water column drastically decreased visibility of
the seafloor for altitudes over 4 m. Continual logging
of geographic and environmental conditions allowed
accurate sizing and enumeration of scallops after pro-
cessing. The highly accurate navigation — typically a
1-m drift over 1 km of trackline of the AUV — allowed
precise repeatability of survey lines. Targets visible in
overlapping side-scan sonar imagery exhibited horizon-
tal offsets of less than 2 m — a finding that is consis-
tent with numerous other AUV benthic and geomorphic
survey studies (e.g. Patterson et ah, 2008; Forrest et
aL, 2012; Rankey and Doolittle, 2012; Raineault et aL,
2013). This navigational precision allowed for the re-
occupation of survej’’ lines.
A variety of survey designs were evaluated in our
study. Although we believe designs that propagate in
a continuous linear direction (e.g., in a stair-case pat-
tern) have a use for surveying an extremely elongated
bed of scallops, we did not find those designs suited
this type of study or fully incorporated the strengths
of the AUV. The boustrophedon survey design, or a
more regular and approximately rectangular pattern
design, was found to be most useful in simultaneously
photographing the seafloor and acoustically mapping it.
Surveys were designed to allow complete coverage of a
rectangular survey site (-1.75 kmxO.3 km) with side-
scan sonar. The use of the geo-referenced data of each
image also made it possible to plot the precise location
of each scallop and to evaluate the distribution of indi-
viduals within the population (Trembanis et aL, 2012;
Walker, 2013).
Logistically, the AUV offers an effective and produc-
tive platform for the collection of sea scallop images as
part of a larger stock assessment effort. The ability to
quickly deploy and retrieve the AUV from a support
vessel allows the rapid acquisition of photographic and
acoustic data that can be analyzed at sea during tran-
sit time or after the completion of the cruise. Imaging
the seafloor is a noninvasive way to survey the scallop
population and gather data about the small-scale spa-
tial structuring of the population, seafloor texture and
morphological features, and water quality. Photogram-
metric sizing of the scallops was rapid, requiring only
a few seconds once a scallop had been located in an
image. We found that the digital sizes agreed favorably
with the measurements of dredged specimens from the
survey sites.
One of the major advantages of the AUV is the high
volume of data that can be collected in a few hours, but
this high volume also results in a significant challenge
for data processing. However, we showed that with the
aid of sizing software, a team of trained scallop annota-
270
Fishery Bulletin 114(3)
NYB4
NYB5
NYB8
Digitally sized scallops (AUV survey)
Manually sized scallops (dredge survey)
NYB6
NYB9
Shell height (mm)
NYB7
NYB10
Figure 6
Histographs of shell height distrihution for digitally sized sea scallops (Placopecten magellanicus)
photographed with an underwater camera of an autonomous underwater vehicle (AUV) and for sea
scallops collected with a commercial dredge in fishing operations undertaken at the same time and
at the same locations in the New York Bight area.
tors could complete the observation of 203,000 images in
98 man-hours (a rate of 2,000 images per hour). Walker
(2013) showed that the hours required to complete an-
notation of a set of images were directly related to the
number of scallops and associated fauna.
Over 200,000 bottom photographs were obtained in
this study, and all were examined by annotators trained
to count scallops and measure their shell height. We
found this manual step to require many hours of effort
and some expense. We investigated statistical approaches
by repeated random sampling simulations and text book
formulae (Zar 1999, p. 109) that can be used to gauge the
loss in precision by examining only a random subset of
images. Overall, we found the mean density to be 0.075
scallops/image, with a standard deviation of 0.35. These
values were sufficient to compute the standard error of
the mean density from a smaller random subset of im-
ages with the formula for the standard error, SE = s/Vn,
where s is the standard deviation and n is the number of
photos. For example, a random subset of 40,000 images
would have a standard error of 0.35/^40,000=0.00175,
giving a 95% confidence interval (i.e., twice the standard
error) of ±0.0035. This bound is at ±5% of the mean value
(i.e., the relative error) obtained from all photographs
and can be the expected precision when examining a ran-
dom sample of only 20% of the images that we collected.
Sampling half that number (20,000) increases the rela-
tive error to 6.6%, while doubling it to 80,000 decreases
the relative error to 3.3%. Because imagery-based as-
sessments typically generate large numbers of images.
Walker et al.: Use of an underwater camera to monitor distribution and density of Placopecten magellanicus
271
Meat weight (g)
Meat weight (g)
Figure 7
Histograms of calculated biomass based on meat weight
(g) of sea scallops (Placopecten magellanicus) collected
in 2011 from (A) the New York Bight (NYB) and (B)
Long Island (LI) areas.
the examination of a much smaller random subset may
yield sufficiently precise density values and substantial
savings in time and effort.
Sea scallop stock assessment
The results of the inshore surveys showed that the LI
region had an overall density of 0.077 scallops per m^,
which agrees with the density of 0.061 scallops per m^
reported by Rudders and DuPaul'^ for dredge-based
survey of the LI region in 2011. The NYB inshore sites
were only slightly less populated (0.013 scallops per
m^) in comparison both with the density of 0.015 scal-
lops per m^ reported by Rudders and DupauP for the
deeper NYB waters and with the population density in
the LI region in general. The higher population level
of the LI region has been hypothesized by Law (2007)
to be due to seeding from the Georges Bank area. Con-
versely, the lower NYB region densities could be ex-
plained by the interruption of scallop larvae transport
from the LI region caused by the influx of freshwater
from the Hudson River (Law, 2007). Additionally, the
Hudson Shelf Valley forms a natural bathymetric di-
vide between the two regions. The two scallop popula-
tions were also different in their shell height distribu-
tions. The LI population was skewed toward smaller
shell heights in contrast with the more symmetrical
distribution of the NYB population. Both regions had
very few recruit-size class scallops (<1.5%) and were
found overall to possess large-size scallop populations.
We also noted that the largest scallop populations oc-
curred around the 9°C ocean water isotherm, which
corresponds well with the optimal scallop growth tem-
perature of 10°C reported by Posgay (1953).
Dredging effort and sea scallop density
The combined optical and acoustic AUV method used
in this study was found to be an efficient way to fur-
ther use commonly collected side-scan data to quantify
dredging effort. This method could be used to assess
the effects of dredging effort on other benthic organ-
isms, particularly on common bycatch species in the
scallop fishery. As would be expected, a direct compari-
son of dredging effort with scallop density revealed
that fishermen concentrated dredging in only the most
populated sites, and that size-selective dredges had a
noticeable impact on the shell height distribution of
the remaining scallop population (see Fig. 5).
The effects of dredging on the substrate of the sea-
floor have been investigated in multiple studies (Har-
getts and Bridger®; Caddy, 1973; Krost, 1990; Hall-
Spencer and Moore, 2000; Jenkins et al. 2001; NRC,
2002; Lucchetti and Sala, 2012; Krumholz and Bren-
nan, 2015). These studies have found that substrate
texture and fishing effort are the leading variables in
the preservation of trawl marks. Finer grained sedi-
ment (muddy sediment versus sandy bottom) allows
the gear to penetrate further into the substrate due
to lower mechanical resistance between the substrate
and the gear (Krost, 1990). Researchers have reported
dredge marks remaining for up to 1.5 years on con-
tinually fished substrate (Hall-Spencer and Moore,
2000). In the absence of dredging, disturbed bed con-
touring effects last for significantly longer periods of
time; Hall-Spencer and Moore (2000) reported dredge
scars can remain for up to 2.5 years without further
fishing efforts and Bernhard (reported by Krost, 1990)
reported a single trawl scar remaining for up to 5 years
® Margetts, A. R., and J. P. Bridger. 1971. The effect of a
beam trawl on the sea bed. ICES Council Meeting (C.M.)
Documents 1971/B:8, 9 p. [Available at website.]
272
Fishery Bulletin 114(3)
in a bay setting devoid of fishing and strong near-bed
tidal currents.
The fine-sand seabed of the study site allows for the
formation of relatively shallow dredge scars. The lim-
ited seasonal time scale for discernibility of the dredge
scars is due to ongoing fishing efforts that rework the
surface sediment and the reworking of sediment from
wave driven near-bed currents. As such, side-scan sur-
veys at our study sites can be a useful tool for quanti-
fying fishing effort but only for a current season.
Acknowledgments
This project was funded by the NOAA Research Set-
Aside Program (award number: NA11NMF4540011).
The authors are grateful to the crew of the FV Chris-
tian and Alexa: Co-Captain A. Ochse, Co-Captain K.
Ochse, M. Newman, D. Crosson, and R. Adams; the late
W. Phoel; D. Hart at NMFS; V. Schmidt; C. DuVal, A.
Norton, AUV Team: J. Gutsche and B. Keller; and the
Digital Image Scallop Annotator Team: V. Amrutia, B.
Reed, M. Christie, T. Santangelo, and D. Wessell.
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274
NOAA
National Marine
Fisheries Service
Abstract — We examined the stom-
ach contents of 3 vertically migrat-
ing myctophid fish species from the
eastern tropical Pacific (ETP) Ocean
and used a classification tree to ex-
amine the influence of spatial, bio-
logical, and oceanographic predictor
variables on diet. Myctophum nitid-
ulum (n=299), Symbolophorus rever-
sus (n=199), and Gonichthys tenui-
culus, (n=82) were collected with dip
nets from surface waters, and prey
taxa were quantified from bongo net
tows from August through November
2006. A classification tree produced
splits with longitude and sea surface
salinity (SSS), thereby separating 3
geographically and oceanographi-
cally distinct regions of the ETP
(offshore, nearshore, and intermedi-
ate), where diet was similar among
the 3 species. Myctophids consumed,
primarily, ostracods offshore (76.4%
mean percentage by number [MAi,;]),
euphausiids nearshore (45.0%), and
copepods (66.6%) in the intermediate
region. The offshore region was char-
acterized by a greater abundance of
ostracods in the zooplankton commu-
nity (17.5% by number) and within
a deep mixed-layer depth (MLD)
(mean 52.6 m, max 93.0 m). SSS was
low in the nearshore region (<32.9
psu) and the MLD was shallow. The
intermediate region represented a
transition zone between the oceano-
graphic condition of the offshore and
nearshore regions. Our results indi-
cate that these 3 myctophid species
share a similar regional diet that is
strongly influenced by longitude, os-
tracod availability, SSS, and MLD.
Manuscript submitted 13 May 2015.
Manuscript accepted 6 April 2016.
Fish. Bull. 114:274-287 (2016).
Online publication date: 28 April 2016.
doi: 10.7755/FB.114.3.2
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Fishery Builetin
<%■ established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Oceanographic influences on the diet of 3
surface^migrating myctophids in the eastern
tropical Pacific Ocean
Joel E. Van Noord (contact author)’''*
Robert J. Olson^
Jessica V. Redfern^
Leanne M. Duffy^
Ronald S. Kaufmann’
Email address for contact author: ioel.vannoord@noaa.gov
Present address: California Wetfish Producers Association
P.O. Box 1951
Buellton, California 93427
' Marine Science and Environmental Studies Department
University of San Diego
5998 Alcala Park
San Diego, California 92110
^ Inter-American Tropical Tuna Commission
8901 La Jolla Shores Drive
La Jolla, California 92037
3 Southwest Fisheries Science Center
National Marine Fisheries Service, NOAA
8901 La Jolla Shores Drive
La Jolla, California 92037
The Myctophidae (lanternfishes)
comprise a family of fishes whose
members are both extremely abun-
dant and distributed throughout the
world’s oceans (Gjosaeter and Kawa-
guchi, 1980; Irigoien et al., 2014).
Species making up this family of fish
serve roles as both important preda-
tors (Pakhomov et al., 1996) and prey
(Naito et al., 2013); furthermore myc-
tophids transfer energy from lower
to higher trophic levels in food webs
(Brodeur et al., 1999). Myctophids
are also influential in the transfer of
carbon to the deep sea because they
feed in surface waters and return to
the mesopelagic zone (Davison et al.,
2013). The family is speciose, with
as many as 250 species in 33 gen-
era (Catul et ah, 2011). In some in-
stances, as many as 50 species can be
found in close proximity, simultane-
ously feeding on similar prey (Hop-
kins and Gartner, 1992).
Resource partitioning, broadly de-
fined as differences in resource use
among co-occurring species (Schoen-
er, 1974), has been used to explain
how diverse myctophid assemblages
can co-occur without competitively
excluding one another (Hopkins and
Gartner, 1992). Myctophids have
been shown to partition resources by
size (myctophid size) (Shreeve et al.,
2009; Saunders et al., 2015), migra-
tion depth, and prey type (Hopkins
and Gartner, 1992; Pepin, 2013).
Co-occurring myctophid species of
similar size that are found in the
same habitat either partition di-
etary resources or feed opportunisti-
cally on prey in the proportions that
are available. For example, dietary
resource partitioning has been de-
Van Noord et al.: Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
275
scribed in myctophids in the Gulf of Mexico (Hopkins
and Gartner, 1992; Hopkins and Sutton, 1998), Cen-
tral Pacific (Clarke, 1980), western tropical Pacific (Van
Noord 2013), Kuroshio Current (Watanabe et al., 2002),
California Current (Suntsov and Brodeur, 2008), South-
ern Ocean (Cherel et al., 2010; Shreeve et al., 2009),
and North Atlantic (Pusch et al., 2004). Conversely,
generalist behavior has been described by Kinzer and
Schulz (1985), who found that 7 myctophid species in
the equatorial Atlantic fed opportunistically on similar
calanoid copepods. Pakhomov et al. (1996) also found
that 4 myctophid species in the Southern Ocean fed op-
portunistically on the same mesozooplankton, whereas
Tyler and Pearcy (1975) found that myctophids in the
California Current fed on a diverse and overlapping
diet. These previous studies, although valuable, were
primarily descriptive in nature, did not provide mea-
surements of prey availability, were restricted to geo-
graphically small areas, and therefore do not provide a
broad picture of myctophid feeding and the variables
that govern their diet. Understanding the factors that
influence the diet of myctophid fishes will provide in-
sight into food-web dynamics and the structure of re-
lated communities. If myctophids are opportunistic
feeders, for example, bottom-up forcing or environmen-
tal changes in the system would have a dynamic effect
on their feeding patterns, which, in turn, would rever-
berate throughout the food web (Fiedler et al., 2013).
Little is known about the ecology or biology of myc-
tophids from the eastern tropical Pacific (ETP) but in
surveys of larval fish in the ETP, high densities, as well
as a diversity, of myctophid species have been encoun-
tered (Ahlstrom, 1972, 1971). Studies investigating the
ecological role of myctophids in this region have lumped
species together as a forage base for top predators (e.g.,
Pitman et al.^; Maas et al. 2014) and myctophids have
been documented as prey for cetaceans (Perrin et al.,
1973; Scott et al., 2012), tunas, swordfish, and other
large pelagic fish (Moteki et al., 2001), squids (Shchet-
innikov, 1992), and seabirds (Spear et al., 2007) in the
ETP. Given their importance as prey, their feeding be-
havior can have ramifications on how energy is trans-
ferred from lower to higher trophic levels.
The eastern tropical Pacific Ocean encompasses ar-
eas of upwelling and oligotrophy (Fiedler and Talley,
2006), and this oceanographic variability produces di-
verse zooplankton prey assemblages (Fernandez-Alamo
and Farber-Lorda, 2006). There are also diverse and
abundant communities of myctophids (Ahlstrom, 1972,
1971). With the abundance of myctophids and their
zooplankton prey in this region, the ETP presents an
opportunity to assess feeding strategies for these fish.
Using samples collected across a productivity gra-
dient along the North Equatorial Countercurrent
^ Pitman, R. L., L. T. Bailance, and P. C. Fiedler. 2002. Tem-
poral patterns in distribution and habitat associations of prey
fishes and squids. NOAA, Natl. Mar. Fish. Serv., Southwest
Fish. Sci. Cent. Admin. Rep. LJ-02-19, 52 p. [Available at
website.]
(NECC), we quantified the diets of 3 common surface-
migrating myctophids, and assessed the availability
of prey for these species from zooplankton net hauls.
Then, using a bagged (i.e., bootstrap aggregating, where
classifications of randomly generated training sets are
combined to improve overall model performance) clas-
sification tree (Kuhnert et al., 2012), we investigated
the influence of spatial, oceanographic, and biologic
(prey and predator) variables on myctophid diets. We
postulate that, if dietary resources were partitioned,
the diets of each species would be unique, whereas if
feeding was opportunistic, myctophid diets would be
related to broad-scale patterns of prey availability and
oceanography.
Materials and methods
Study area and data coliection
The study area is located in the ETP between the sub-
tropical gyres of the North and South Pacific (Fiedler
and Talley, 2006). The ETP contains 3 major surface
currents: the North Equatorial Current (NEC), North
Equatorial Countercurrent (NECC), and the South
Equatorial Current (SEC [Fig. 1]). The NECC is a
warm, eastward flowing current in which upwelling
causes shoaling of the thermocline along an east-to-
west gradient near 5°N (Fiedler and Talley, 2006). Two
eastern boundary currents at the northern (California
Current) and southern (Peru Current) extent of the
ETP bring cold, nutrient-rich water into the system
(Fiedler and Talley, 2006). Nearshore waters associated
with the Gulf of Panama have characteristically low
sea-surface-salinity (SSS) values owing to high local
rainfall (Amador et al., 2006).
Myctophids (n=580) were collected aboard National
Oceanic and Atmospheric Administration (NOAA) re-
search vessels RV MacArthur II and RV David Starr
Jordan during surveys conducted in the ETP by NO-
AA’s Southwest Fisheries Science Center (SWFSC)
from August to November 2006. Myctophids were sys-
tematically collected every night in dip nets at prede-
termined stations (Fig. 2) located on line transects (Fig.
3). A randomized subsample of myctophids captured at
32 stations was available for this study. Dipnet sam-
pling began one hour after local sunset and lasted for 1
hour. Long-handled (~6-m) dip nets with 1-m wide bas-
kets and 0.5-cm mesh size were used to catch mycto-
phids under deck lights that illuminated approximately
10 m2 of the water surface (Goad, 1998). Researchers
at the SWFSC have collected specimens using this
standardized method for decades (Fiedler et al., 2013;
Pitman et al.^). The dipnet method is unique in com-
parison with that of traditional net tows because fish
are collected from the ocean environment individually
and not retained in a net, thus excluding the possibility
of postcapture feeding. Net avoidance associated with
the bow-wave of large towed equipment is also negated
with handheld dip nets. Myctophids exhibit size-related
276
Fishery Bulletin 114(3)
160°W 150°W 140°W ISO^W 120'’W IIO'W lOO'W 90°W 80°W
Major currents and oceanographic features in the eastern tropical Pacific Ocean. Ar-
rows indicate direction of the currents. Dashed ovals signify distinct oceanographic
features.
depth stratification throughout the water column, and
certain, often larger, individuals remain deeper in the
column (Collins et ah, 2008; Saunders et ah, 2015).
Additionally, not all members of a surface-migrating
population migrate each night, and surface-migration
is likely spurred by feeding. Therefore, our samples
are not representative of all size classes within this
population; instead, we focused entirely on the surface-
migrating myctophids that were found in surface wa-
ters during the time of capture. Specimens were frozen
whole at sea.
Zooplankton were sampled with a bongo net (0.6-
m mouth diameter, 333-pm mesh) towed obliquely to
a depth of 200 m at an average ship speed of 1.75 kn.
A flow meter was attached to the net to determine the
amount of filtered seawater. We analyzed only net tows
at the 32 stations where myctophids were collected
(Fig. 2). The sampling depth of the bongo tows does not
cover the entire depth range for myctophids because
our study focused exclusively on the surface-migrating
members of the population and we were interested in
the prey that might be available to this subset of the
fish community. Zooplankton also conduct diel vertical
migrations from deep-water to near-surface waters and
it is likely that some zooplankton had migrated from
deeper than 200 m (Longhurst and Harrison, 1988).
Depth-integrated zooplankton samples were used be-
cause myctophids feed during migration (Watanabe et
ah, 1999). Net tows commenced 30 min after the con-
clusion of dipnet sampling and the zooplankton sam-
ples were preserved at sea in 3.7% buffered formalin.
Systematic oceanographic sampling was conducted
during the surveys (for details, see Fiedler and Phil-
brick^). Sea surface temperature (SST) and SSS values
were recorded with a thermosalinograph at 2-min in-
tervals along transects (Fig 3). Surface chlorophyll-a
(SCHL) concentrations were measured at approximate-
ly 55-km intervals along transects by using a fluorom-
eter. Mixed layer depth (MLD), i.e. the depth at the top
of the thermocline, was estimated as the depth (m) at
which the temperature is 0.5°C less than the surface
temperature. MLDs were derived from data obtained
from expendable bathythermograph (XBT) and conduc-
tivity, temperature, and depth (CTD) casts. XBT casts
were made at approximately 55-km intervals along
transects to a depth of 760 m. CTD casts were under-
taken at sunrise and sunset each day to a depth of
1000 m. Using these data, Barlow et al. (2009) created
smoothed (using the Kriging method) maps of SST, SSS,
MLD, and SCHL data (Fig. 3) and are presented here
with permission. In the classification tree model we
considered, only variables coinciding with the 32 dipnet
stations at which myctophids were collected.
In the laboratory, myctophids were thawed individu-
ally, identified (by using keys devised by Wisner, 1974
and Gago and Ricord, 2005), blotted, weighed to the
nearest mg, and measured to the nearest mm (standard
length, SL). Stomachs were dissected whole from each
2 Fiedler, P. C., and V. A. Philbrick. 2002. Environmental
change in the eastern tropical Pacific Ocean: observations
in 1986-1990 and 1998-2000. NOAA, Natl. Mar. Fish.
Serv., Southwest Fish. Sci. Cent. Admin. Rep. LJ-02-15, 16
p. [Available at website.]
Van Noord et al.: Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
277
140°W lao^w 120°W 110“W 100°W 90°W 80°W
Species distribution of the 580 myctophid individuals of 3 myctophid species collected
from the eastern tropical Pacific Ocean by dip net during 2006.
fish, weighed, fixed in 3.7% formalin, and stored in 70%
ethyl alcohol. The amount of time specimens were left
either unfrozen or unpreserved was minimized to avoid
degradation of stomach contents.
Displacement volumes of small zooplankton from
oblique net tows were measured in the laboratory. This
measurement excluded all fishes, large cephalopods,
pelagic crabs, and large plankters (>5 mm), including
Thaliacea and medusae (Ohman and Smith, 1995). Net
samples were split to a one-eighth volume by using a
Folsom plankton splitter, and individuals were identi-
fied under a dissecting microscope to the taxonomic
level of order. Identifications were made to order level
for comparison with the taxonomic resolution of most
gut-content identifications. This taxonomic resolution
restricted our diet analysis because we could not ex-
clude the possibility that resource partitioning occurs
at a lower taxonomic level. Zooplankton densities were
standardized as numbers of individuals per m^ of wa-
ter filtered at each station by using methods of Smith
and Richardson (1977) and were converted to numeric
percentages for comparison with gut contents.
We calculated mean percentage by number (MW,) by
using the following equation:
N::
N-
xlOO,
(1)
where Wy = the count of prey type i in fish j;
Q = the number of prey types in the stomach of
fish j; and
P = the number of fish with food in their stom-
achs in any particular sampling stratum
(Chipps and Garvey, 2007).
We calculated mean percentage by weight {MWi) simi-
larly, substituting prey weights (W) for counts (W). Per-
cent occurrence (O,) was calculated as the number of
fish containing a specific prey item i, divided by the
total number of fish sampled, including those mycto-
phids with empty stomachs, and multiplied by 100. We
focused our analysis on the numeric predation data for
comparison with the numeric zooplankton prey data.
Ciassification tree analysis
Diet composition
We identified stomach contents to the lowest possible
taxon and enumerated and weighed contents by taxo-
nomic group. Pieces of plastic found in stomachs were
not included in the analysis of the natural diet. Stom-
achs void of all material, including unidentifiable sub-
stance, were classified as empty.
We applied Classification and Regression Tree (CART)
analysis to the myctophid diet data, using the modi-
fied approach of Kuhnert et al. (2012 [see also Olson
et al., 2014]). CART is a nonparametric modeling ap-
proach described by Breiman et al. (1984). Diet data
are partitioned by forming successive splits on predic-
tor variables in order to minimize an error criterion,
in this case the Gini index, which represents a mea-
278
Fishery Bulletin 114(3)
Figure 3
Oceanographic maps smoothed (with the Kriging method) and created hy Barlow et al. (2009) and used with permission,
displaying (clockwise from top left) surface temperature, surface salinity, surface chlorophyll, and mixed layer depth
values in the eastern tropical Pacific (shaded region). Ship track-lines are shown with solid or dashed lines. Solid lines
indicate sampling was continuous. Dashed lined indicated sampling was conducted at 55-km intervals. Numbers along
isopleths indicate values for the variable represented in each map. Only variables coinciding with the 32 dipnet stations
were used in the classification and regression tree (CART) analysis.
sure of diet diversity ranging from 0 (no diet diver-
sity) to 1 (high diet diversity) among predicted prey
categories. A large tree is produced and 10-fold cross-
validation is used to prune the tree to within one
standard error of the tree yielding the minimum er-
ror (i.e., the “1 SE” rule [Breiman et al., 1984; Kuh-
nert et al., 2012]). Predictions are made by partition-
ing a new observation down the tree until it resides
in a terminal node. The prey group with the greatest
numeric proportion among a suite of prey in the diet
is displayed at each terminal node. The vector of prey
proportions, in numbers of prey eaten by an individual
predator is represented as a univariate categorical re-
sponse variable of prey type (class), with observation
(case) weights equal to the proportion of the prey type
eaten by the predator. Fish with empty stomachs were
omitted from this analysis because we were interested
in how predictor variables influenced prey type. Rank-
ings of variable importance are computed to identify
which predictor variables are most important in the
model. In addition, Kuhnert et al. (2012) implemented
a spatial bootstrapping technique to account for spa-
tial dependence in the data and to assess uncertainty
in the predicted diet composition at each node in the
classification tree. The classification was implemented
in R software, vers. 3.1.1 (R Core Team, 2014) with
the ‘rpart’ package (Therneau et al., 2013); further de-
tails can be found in Kuhnert et al. (2012).
We used CART analysis to explore the relationship
among 12 dependent spatial, oceanographic, and bio-
logical predictor variables (Table 1) and the response
variable, diet composition. Spatial predictors included
latitude and longitude, oceanographic predictors con-
sisted of MLD, SSS, SST, and SCHL concentration, and
biological predictors contained information on the zoo-
plankton prey community by using data from the net
samples and the myctophid predators. Data represent-
ing the zooplankton community (potential prey) includ-
ed ostracod, copepod, and euphausiid numeric composi-
tion and zooplankton displacement volume in the net
samples (Table 2). Standard fish length was used to
assess the effects of ontogenetic diet. We used species
as a predictor variable to assess resource-partitioning
among species.
Van Noord et al.: Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
279
Table 1
Geographic, oceanographic, and biologic predictor variables used in the analysis to determine the diet of 3
myctophids in the eastern tropical Pacific Ocean. Fish were collected from August through November 2006.
Predictor variable
Type of variable
Mean (Min. -Max)
Longitude
Spatial
140.7°W to 80.4°W
Latitude
Spatial
11.0°S to 10.8°N
Myctophid species
Biological
Myctophum nitidulum, Symbolophorus
reversus, Gonichthys tenuiculus
Myctophid standard length
Biological
50.4 mm (25-80)
Ostracod zooplankton (ZP) composition
Biological
10.9% (1.2-37.0)
Copepod ZP composition
Biological
72.2% (45.0-87.3)
Euphausiid ZP composition
Biological
4.4% (1.8-20.7)
Zooplankton volume
Biological
97.5 mL (l,000)/m3 (44-241)
Mixed layer depth (MLD)
Oceanographic
38.1 m (6-93)
Sea surface salinity (SSS)
Oceanographic
33.25 psu (31.21-35.58)
Sea surface temperature (SST)
Oceanographic
21.2'’C (21.9-29.2)
Surface chlorophyll (SCHL)
Oceanographic
0.184 mg/m3 (0.002-0.382)
We categorized the myctophid diet into 17 prey
groups in the CART analysis (14 are shown in Table
3). These groups ranged in taxonomic level from fam-
ily (e.g., Euchaetidae) to phylum (e.g., Mollusca) be-
cause the taxonomic resolution of prey identifications
varied and because some rare prey were combined
into broader taxa along with unidentifiable specimens.
For the CART analysis, all mollusks were grouped to-
gether, as were all euphausiids, and all cyclopoid co-
pepods. Rare calanoid copepods, defined as types con-
tributing less than 1% MNi to all 3 myctophid species
were grouped as “other copepods.” Rare amphipods,
defined as types contributing less than 0.3% in MNi
were grouped as “other amphipods.” The “other” co-
pepod and amphipod groups contained a majority of
unidentifiable specimens. Decapods (0.5% combined
mean MNi), fish eggs (0.3%), and the one cephalopod
(<0.1%) were not included in the analysis because of
their scarcity.
Results
Oceanographic variables
The MLD, SSS, SST, and SCHL concentrations each
showed distinct geographic patterns within the study
area. MLD deepened from east to west along the NECC,
between the equator and 10°N (Fig. 3). At its shallow-
est, MLD (mean 38.1 ±20.5 m standard deviation [SD],
averaged over the 32 dipnet stations) was 6 m deep
nearshore (8°N, 91°W) and reached 93 m at the station
farthest offshore (6°N, 140°W). SSS (mean 33.3 ±1.20
practical salinity units [psu]) was lowest (31.21 psu)
near the coast of Central America, and became more
saline farther offshore and south of the equator (max.
of 35.5 psu). SST (mean 21.2 ±1.90° C) showed little
variation along the NECC, where the majority of sta-
tions occurred. Surface chlorophyll-a values (mean 0.20
±0.08 mg/m^) were greatest along the coast of southern
Mexico and Ecuador and decreased offshore (Fig. 3).
Myctophid size-composition
The individuals collected at the surface nightly by dip
net differed morphologically (Fig. 4). Symbolophorus re-
versus (71=199; 172 with identifiable prey remains) was
the largest of the 3 species in length (mean=55.9 ±8.8
mm SD) and weight (2.66 ±1.27 g SD). Myctophum niti-
dulum (?7=299; 275 with identifiable prey remains) was
intermediate in length (47.9 ±6.6 mm) and weight (1.82
±0.80 g). Gonichthys tenuiculus (7i=82; 26 with identifi-
able prey remains), was the smallest species in length
(37.8 ±4.3 mm) and weight (0.54 ±0.21 g [Fig. 4]).
Diet composition
Prey composition data for each of the 3 species are
summarized by the 3 diet indices, MNi, MWi, and Oj in
Table 2. We focused our data analysis on the numeric
diet index for consistency with the numeric data on
prey availability. We included the weight and occur-
rence indices in Table 2, however, so that our data are
comparable with other published data.
Zooplankton community
Seventeen unique taxonomic groups of zooplankton
were identified and enumerated (?i=178,090 individu-
als) in the net tows. Copepods were by far the most
abundant group, representing as much as 87.3% of
the community sampled and never less than 45.0% at
any station (Table 3, Fig. 5). Ostracods were the sec-
ond most abundant group overall (8.65 ±10.1%). Eu-
phausiids and amphipods each contributed <5% of the
sampled community.
280
Fishery Bulletin 114(3)
Table 2
Percentages of the prey composition for 3 myctophids collected at 32 stations in the eastern tropical Pacific
Ocean. Samples of zooplankton prey were taken with an oblique haul of a bongo net. Offshore, intermedi-
ate, and nearshore regions were identified by a classification tree analysis (Fig. 7). Standard deviations
are shown in parentheses.
Latitude
Longitude
Amphipods
(%)
Copepods
(%)
Euphausiids Euphausiids
(%) (%)
Other
prey
(%)
Nonprey
items
(%)
6.30°N
140.72°W
0.55
72.9
2.37
12.1
3.29
8.78
0.23°N
119.92°W
1.52
76.6
3.07
3.09
2.79
13.0
11.03°N
119.28°W
1.43
82.8
2.92
1.80
4.06
7.00
5.02°N
113.58°W
1.62
61.0
2.58
22.3
2.38
10.1
8.25°N
113.17°W
1.38
45.0
5.98
33.6
2.66
11.3
3.37°N
110.85°W
2.17
67.5
2.35
9.74
4.00
14.3
6.07°N
110.70°W
2.05
45.2
4.61
37.0
5.17
6.04
1.62°S
110.65°W
1.07
69.8
4.94
5.16
1.38
17.6
5.65°N
108.00°W
1.45
61.1
5.54
19.7
6.29
5.84
1.90°S
107.58°W
1.73
76.7
4.36
2.78
0.36
14.1
6.48°N
104.38°W
1.02
49.3
3.12
32.9
2.00
11.6
6.33'’N
101.73°W
1.15
70.5
3.89
15.4
1.78
7.30
7.25''N
101.37°W
1.35
65.0
5.13
17.6
2.19
8.68
2.78'’S
96.37°W
1.24
78.4
3.87
3.11
1.67
11.7
7.07'’N
95.32°W
0.82
82.5
2.35
1.53
3.55
9.20
2.68°N
93.65°W
0.82
81.8
2.50
5.18
4.36
5.29
10.8°S
93.62°W
0.76
61.7
20.7
1.48
1.58
13.8
9.02°N
93.05°W
2.56
82.1
3.63
2.00
7.57
2.14
6.15°N
92.20°W
1.91
79.9
4.37
3.21
3.01
7.64
8.37°N
91.68°W
1.76
79.8
4.01
1.66
2.60
10.2
6.23°N
90.90°W
2.15
76.2
3.07
3.73
2.86
12.0
5.30°N
89.20°W
1.57
75.8
4.20
3.06
1.14
14.3
7.35°N
86.93°W
1.15
72.7
5.51
5.49
1.09
14.1
1.73°S
85.45°W
1.72
80.7
3.29
1.21
4.98
8.04
7.47°N
85.00°W
1.15
81.2
3.74
1.21
1.77
10.9
4.77°N
84.15°W
1.22
77.4
4.41
3.54
0.83
12.6
1.17°S
82.45°W
0.48
87.3
1.78
1.45
3.22
5.73
3.72°N
81.82°W
1.08
77.0
3.73
4.58
1.72
11.9
4.57°N
81.52°W
1.07
76.7
4.07
2.76
5.76
9.64
4.73°N
80.88°W
1.34
69.6
5.29
6.40
2.60
14.8
6.83°N
80.83°W
1.23
75.5
4.21
5.23
1.14
12.7
5.18°N
80.43°W
0.61
70.5
5.44
6.62
3.83
12.9
Region
Offshore
1.40
63.9
3.90
17.5
3.20
10.1
Intermediate
1.50
80.5
3.30
2.60
3.50
8.60
Nearshore
1.11
75.1
4.55
4.48
2.34
12.5
Mean
1.35
72.2
4.41
8.65
2.93
10.5
(±0.49)
(±10.7)
(±3.16)
(±10.1)
(±1.69)
(±3.46)
Classification tree analysis
The classification tree analysis produced a tree with
2 splits and 3 terminal nodes (Fig. 6A) and yielded
a cross-validated error rate of 0.73 (standard er-
ror [SE]=0.04, coefficient of multiple determination
(i?2]=~27%). The rankings of variable importance (Fig.
6B) indicated that longitude was the most important
variable (i.e., rank=1.00) for predicting the diet com-
position of these myctophids. The ostracod numeric
composition of the zooplankton (rank=0.74), the cope-
pod composition of the zooplankton (rank=0.61), MLD
(rank=0.61), and SSS (rank=0.60) were the next most
important. Myctophid species (rank=0.08) was a less
important predictor variable in the classification tree
given our collection of surface-migrating fishes and at
the taxonomic level possible in this study. Latitude,
myctophid length, SST, SCHL, zooplankton volume,
and euphausiid composition in the zooplankton net
samples yielded an importance rank of zero.
The initial split in the tree provided the greatest
reduction in deviance over the entire data set and par-
Van Noord et al.; Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
281
Table 3
Summary of stomach contents (including pieces of plastic) of 3 myctophid species collected in the eastern tropical Pa-
cific Ocean during 2006. Diet indices include mean percentages by number (MNi), weight {MWi), and percent occurrence
(0,). Fourteen of the 17 prey groups used in the classification tree analysis are designated with an “X.” Unidentifiable
and rare individuals (generally contributing <1% MNi to the diet) within the broader taxonomic group are not displayed.
CART=classification and regression tree analysis. Bold font represents total values for a subclass and order of prey.
Used (X)
in CART
Myctophum
nitidulum
Symbolophorus
reuersus
Gonichthys
tenuiculus
MNi
MWi
Oi
MNi
MW,
o,
MN,
MW,
O,
Copepoda
42.7
39.1
69.6
32.S
28.3
50.3
18.6
17.6
7.3
Calanoida
36.4
37.5
62.5
27.1
23.3
45.2
18.6
17.6
7.3
Calanidae
X
1.01
1.44
10.7
0.29
0.15
1.51
3.85
4
1.22
Candaciidae — Candacia spp.
X
1.47
1.84
14.4
5.53
5.04
16.1
0
0
0
Eucalanidae
X
1.79
2.51
14.4
0.12
0.27
1
0
0
0
Euchaetidae
X
7.33
10.2
32.1
6.94
15
15.1
3.85
4
1.22
Pontellidae
X
0.5
0.64
6.69
0
0
0
3.01
2.44
2.44
Cyclopoida
6.26
2.89
35.5
5.33
4.99
14.1
0.55
0
1.22
Corycaeidae — Corycaeus spp.
X
1.43
0.56
12.7
0.37
0
1.51
0
0
0
Oncaeidae — Onceaea spp.
X
4.8
2.33
27.4
4.73
1.81
13.6
0
0
0
Ostracoda
41.5
39.1
45.5
24.4
18.1
26.1
34.6
36
11
Cypridinidae — Cypridina americana
X
41.3
38.8
45.1
24.4
18.1
26.1
34.6
36
11
Euphausiacea
X
3.29
3.42
13
29.6
34.5
47.2
19.4
16.4
7.32
Euphausia diomedeae
0
0
2.86
6.53
0
0
E. mutica
0.08
0.67
4.15
10.1
0
0
E. tenera
0.16
2.01
2.34
8.04
0
0
Euphausia spp.
2.18
10
19.6
7
19.4
7.32
Amphipoda
8.38
12.1
35.8
7.58
9.61
20.1
27.3
30
9.76
Hyperiidae
X
3.86
5.42
20.1
4.6
5.32
15.1
9.34
11.5
3.66
Pronoidae
X
1.23
2.54
8.36
0.24
0.37
3.02
4.81
6
2.44
Platyscellidae
X
0.32
1.11
3.34
0.3
1.09
3.02
0
0
0
Mollusca
X
2.98
4.35
14.7
2.48
3.59
8.54
0
0
0
Atlantidae
0.12
0.32
2.01
0.39
0.75
2.51
0
0
0
Janthinidae
1.44
1.99
8.01
1.42
1.8
2.51
0
0
0
Limacinidae — Limacina spp.
0.4
0.48
1
0
0
0
0
0
0
Cavoliniidae — Diacria schmidti
0.03
0.16
0.67
0.03
0.16
0.5
0
0
0
Unidentified Mollusk
0.98
1.35
5.69
0.64
0.88
3.02
0
0
0
Larval fish
X
0.12
0.19
0.33
2.09
3.63
7.04
0
0
0
Decapoda
0.33
0.47
3.01
1.09
1.86
3.02
0
0
0
Fish egg
0.78
0.16
3.34
0.08
1.21
0.5
0
0
0
Cephalopoda
0
0
0
0.19
0.3
0.5
0
0
0
Plastic
2.01
0
1.22
Total stomachs
299
199
82
titioned the diet composition for 271 myctophids sam-
pled east of 100°W, on the left side of the tree (node 2),
from the diet composition of 196 myctophids sampled
west of 100°W, on the right side of the tree (i.e., ter-
minal node 3) (Figs. 6 and 7). Ostracod composition
in the zooplankton was a strong competitor-split vari-
able, i.e, ostracod composition in the zooplankton pre-
formed only 2% worse than longitude at this partition
(node 2). The diet composition of the myctophids east
of 100°W was variable, and the tree further separated
169 samples caught in waters of relatively high salin-
ity, SSS >32.86, east of 100°W (terminal node 4) from
102 samples caught in waters of relatively low salinity,
SSS <32.86, east of 100°W and near the Panama Bight
(terminal node 5 [Figs. 6 and 7]).
Terminal node 3 All myctophids in the offshore re-
gion (Fig. 7) consumed large proportions of the os-
tracod Cypridina americana (mean MAC,: 76.4%) and
small numbers of several other prey (Fig. 7). The diet
diversity (0.22) of the myctophids in this region (ter-
minal node 3) was lowest among all terminal nodes.
Ostracods were the most numerically abundant and
the MLD was the deepest at the 13 stations within the
offshore region.
Terminal node 4 The 169 myctophids residing in ter-
minal node 4 consumed large proportions of copepods
(mean MNf. 66.6%) that were identifiable as euchae-
tids. These myctophids were captured at 9 stations at
intermediate distances from the coast, between 100°W
282
Fishery Bulletin 114(3)
Figure 4
Length-frequency plot for the 3 myctophid species captured from sur-
face waters in the eastern tropical Pacific during 2006. Sizes reflect
our unique specimen collection and are not representative of the en-
tire population because only surface-migrants were targeted.
and 89°W, and nearshore off Ecuador (Fig. 7). Net
samples revealed copepods were the most numerically
abundant zooplankton (80.5%, compared with 63.9 and
75.1% in the offshore and nearshore regions) in this
region (Table 3). This intermediate region was charac-
terized by moderate values of MLD, SSS, and SCHL
(Fig. 3), and it appears to represent a transition zone
between the offshore and nearshore regions.
Terminal node 5 The myctophids sampled at 8 near-
shore stations near the Panama Bight, east of 87°W
and north of 3°N, (Fig. 7) consumed primarily euphau-
siids (mean MNi. 45.0%). SSS in this region was low
(<32.86 [Fig. 3]), the MLD was shallow (mean MLD:
22.9 m), and SCHL concentrations (0.22 mg/m^) were
greater than those at stations identified within the
other regions.
Interspecific patterns
Collectively, the predominant prey of these myctophids
came from 4 groups, copepods (MiV'j=37.7%), ostracods
(34.9%), euphausiids (13.7%), and amphipods (9.1%),
which accounted for more than 95% of the diet, by
number. The remaining 5% comprised mollusks (ptero-
pods and heteropods, 2.6%), larval fishes, decapods, fish
eggs, one squid paralarva, and one terres-
trial insect (Table 2).
Interspecific dietary differences were
apparent and might have been more de-
finitive if the prey were identified at a
lower taxonomic level. Previous research
has, for example, indicated that these
species are selective feeders (Van Noord
et al., 2013b). We further assessed these
previous findings by including a broad
suite of predictor variables and found
that “myctophid species” ranked relatively
low in explaining diet patterns across the
ETR Myctophum nitidulum fed on cope-
pods (42.7%) and ostracods (41.5% [Table
2]). Symbolophorus reversus fed primarily
on copepods (32.5%), euphausiids (29.6%),
and ostracods (24.4%). Gonichthys tenui-
culus took prey from only 4 groups, pri-
marily ostracods (34.6%) and amphipods
(27.3% [Table 2]).
Distribution patterns differed some-
what among the 3 myctophids. Figure
2 displays spatial trends in abundance;
greater numbers of S. reversus and G.
tenuiculus occurred in the nearshore and
intermediate areas, respectively. The indi-
viduals in this study, however, represent
subsamples of the captured myctophids,
and no quantitative distribution analysis
was possible. However, representatives
of each species were captured across the
entire sampling region, resulting in ad-
equate distributional overlap, but the tree
analysis did not indicate that myctophid species are
an important variable in characterizing the diet of the
fishes in this study.
Discussion
We used a classification tree to examine the influence
of spatial, biological, and oceanographic predictors on
diet and found that feeding by the collection of surface-
migrating myctophids in this study was controlled by
prey distribution and resource-driven processes, such
as mixed-layer depth, productivity, and sea surface sa-
linity, whereas the influence of dietary resource par-
titioning was a minor controlling factor. These myc-
topMds shared a similar diet, consisting primarily
of copepods, ostracods, euphausiids, and amphipods.
Diet of all 3 species changed geographically, and with
oceanographic conditions and zooplankton prey compo-
sition. Myctophids consumed ostracods offshore where
the mixed layer depth was deep and ostracods were
more abundant in the prey community, euphausiids
nearshore where the MLD was shallow, and copepods
at intermediate stations between those stations where
they were most abundant. Understanding myctophid
feeding behavior can provide insight into how these
Van Noord et al.: Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
283
140°W 130°W 120°W 110°W 100°W 90°W 80°W
Distribution of the prey community sampled with an oblique bongo net in the eastern tropical
Pacific Ocean. Each color represents a zooplankton prey species, other prey species, or non-prey
species. Circle size reflects zooplankton displacement volume. The numbers 44, 110, and 241
indicate zooplankton displacement volume (mL/lOOOm^).
communities are structured and how energy is trans-
ferred through the food web.
Longitude had the greatest variable importance
ranking among all predictors, and this is likely be-
cause water masses and prey composition co-varied
geographically along the NECC. The NECC is charac-
terized by a shoaling thermocline and by increased pro-
ductivity from west to east (Fiedler and Talley, 2006),
and the classification tree allowed us to identify dis-
tinct regions along the NECC where myctophid diet
was different. The zooplankton samples collected from
the stations in each of the 3 geographic regions had
different percentages of prey groups that contributed
to myctophid diet patterns.
The offshore region was defined by a high abundance
of pelagic ostracods in myctophid diets. This region was
oceanographically distinct because of its mixed layer
depth, low productivity, and high abundance of ostra-
cods in contrast to the other regions. A deep MLD cor-
responds to reduced mixing, lower nutrient availability
in surface waters, and oligotrophic conditions (Fiedler
and Talley, 2006). Pelagic ostracods are typically most
abundant in such oligotrophic conditions because of
their greater ability to exploit environments low in
food availability (Le Borgne and Rodier, 1997; Angel
et ah, 2007).
The nearshore region was defined by a high abun-
dance of euphausiids in myctophid diets. This region
was oceanographically distinct because of its shallow
MLD and low saline waters. It typically displays el-
evated primary productivity and low oxygen levels
(Fiedler and Talley, 2006). Extreme local rainfall and
westward transport of water vapor across the Isthmus
of Panama contribute to the low-salinity water mass in
this location (Amador et ah, 2006). Euphausiid abun-
dance is typically greatest in productive, nearshore
waters (Brinton, 1979; Simard et ah, 1986), and that
is the case here. Upwelling and biological production
are greatest near the coast in the ETP, particularly the
Gulf of Panama and the Costa Rica Dome than in other
regions in the ETP (Lavin et ah, 2006). Additionally, an
oxygen minimum zone exists in the ETP; low oxygen
values extend south into the Gulf of Panama (Fiedler
and Talley, 2006). Some euphausiids, such as Euphau-
sia diomedeae and E. mutica that were consumed by
the myctophids in this study, are tolerant of low oxygen
(Brinton, 1979).
Myctophids in the intermediate region had high
numbers of copepods in their diets. This region, a tran-
sition zone between the nearshore and offshore, showed
moderate mixed layer depths, salinities, and surface
chlorophyll values in comparison with the higher and
lower values of the other regions, respectively. Cope-
pods were abundant throughout the study area but
284
Fishery Bulletin 1 14(3)
East
<0.11
More
saline
1) Longitude: 100°W
Competitor; ZcomO
2)SSS: 32.86
West
>0.12
m
Ostracod — Cypridina
Less americana
saline
m El
Copepod— Euphausiid
other
B
Figure 6
(A) The classification tree (at a 1 SE resolution) used to predict myctophid (Myctophum niti-
dulum, Symbolophorus reversus, Gonichthys tenuiculus) diet composition from geographic,
oceanographic, and biologic predictor variables (see Materials and methods section for further
explanation). The prey group identified at each terminal node is that with the highest propor-
tional numeric composition among all the prey in the myctophid samples that were mapped to
each terminal node. (B) A variable importance plot showing rankings of each nonzero predic-
tor variable used in the classification tree model. Lon^longitude; ZcomO=ostracod composition
in the zooplankton net samples; ZcomC=copepod composition in the zooplankton net samples;
mld=mixed layer depth; SSS=sea surface salinity; Spp=myctophid species
made up more than 80% of the community in the in-
termediate region, perhaps reflecting a competitive
advantage that various copepods have in moderately
oceanographic conditions (McGowan and Walker, 1985;
Turner, 2004). In contrast, ostracods were limited in
their range to oligotrophic conditions, and euphausiids
were more dominant in productive nearshore environ-
ments (Brinton, 1979).
Previous research has indicated that M. nitidulum
selects amphipods and ostracods and that S. reversus
prey on euphausiids and amphipods (Van Noord et al.
2013b), and in fact dietary resource partitioning among
myctophids has commonly been reported (e.g., Hopkins
and Gartner 1992: Hopkins and Sutton 1998: Cherel
et al., 2010), but the influence of oceanography on diet
is less often considered. The selective feeding behavior
observed by Van Noord et al, (2013b) is indicative of
resource partitioning, but the current study expands
on these initial findings and presents a more complete
ecosystem-based analysis by including spatial, biologi-
cal, and oceanographic variables in addition to dietary
information. The current study indicates a very low
level of resource partitioning among these species, as
evidenced by the low importance of myctophid species
in the ranking of variables. Indeed, when considering
a fuller compliment of oceanographic, spatial, and prey
composition data, we found that resource partition-
ing between species is not the most important aspect
controlling diet. Therefore, dietary resource partition-
ing and competition among these species played minor
roles in regulating feeding behavior, and spatial and
oceanographic predictor variables outweighed resource
partitioning. The importance of considering spatial,
biological, and oceanographic variables when evaluat-
ing feeding behavior is clear, and the findings obtained
from these variables have implications for interpreting
previous results.
A diverse fish community structured through di-
etary resource partitioning can be affected by distur-
bance events and bottom-up forcing. For example, flying
fish in the ETP consume many of the same prey that
are consumed by myctophids, which could introduce
a level of food competition (Van Noord et al., 2013a).
During the course of our investigations, (August-No-
vember 2007), a tropical storm bisected the sampling
area (15-17 October), resulting in enhanced upwelling,
productivity, and zooplankton biomass in the wake of
the storm. The flying fish community reflected these
changes. Feeding success increased and diet composi-
tion changed in accordance with storm-induced chang-
Van Noord et aL: Oceanographic influences on the diet of myctophids in the eastern Pacific Ocean
285
<» 5
Figure ?
Map of terminal node groups 3, 4, and 5 in the classification tree of myctophid prey composition and showing the boot-
strapped diet proportions for the myctophids grouped at each terminal node. Map displays symbols, which indicate the sam-
pling stations where myctophids were feeding similarly according to the classification tree analysis. All stations occurred
in waters >3000 m and bathymetric contours (in m) are displayed to show the depth ranges of our sampling. Diet diversity
(D) values ranging from 0 (no diet diversity) to 1 (high diet diversity), are shown above each graph. Color gradients are pro-
vided for ease of viewing. Abbreviations are as follows: A=amphipod; C=copepod; E=euphausiid; A.Hyp=hyperiid amphipods;
A.Otr=unidentifiable and rare ampliipod types; A.Pla=platyscellid amphipods; A.Pro=pronoid amphipods; C.Cal=calanid
copepods; G.Can=candaciid copepods; C.Cyc=;cyclopoid copepods; C.Euc=euchaetid coepods; C.Eucl=eucalanid copepods;“C.
Otr=unidentifiable and rare copepod types; C.Pon=pontellid copepods; C.Tem=temorid copepods; E.Eup=euphausiids,;
LF=:larvaI fishes; M=mollasks, O.Ca=Cypridina americana (ostracod); O.Hal=HaIocyprida ostracods.
es in the prey community (Fiedler et al., 2013). These
studies document the dynamic nature of the feeding
habits of fish, and show/ that feeding patterns are not
necessarily static; fish clearly respond to oceanographic
conditions, in addition to displaying intrinsic behaviors
that result in a more typical pattern of resource parti-
tioning. This dynamic feeding behavior highlights the
necessity of obtaining samples that adequately cover
both temporal and spatial scales.
We sampled only surface migrating myctophids and
therefore the interpretation of our data and implica-
tions for the broader myctophid community are limited.
We did not include deeper dwelling individuals, and
this limitation could alter both the feeding patterns
observed and the size class of myctophids encountered.
Sampling a broader spectrum of the myctophid popu-
lation by using a suite of sampling gear that would
cover the entire depth range for these fish could help
to elucidate distributional patterns in the ETP and bet-
ter address the role of resource partitioning in this fish
community. As with all studies of fish feeding habits,
taxonomic resolution of stomach contents impacts in-
terpretation of the results. A finer taxonomic resolution
may reveal a more subtle species-level diet partition-
ing among the myctophids. Prey size is also a function
of the resolution of stomach samples and because we
were unable to consistently quantify prey size in this
study, it is possible that some species of myctophids
partition diets on the basis of prey size rather than
species, or some combination of size and species. As
with most studies, a greater temporal sampling reso-
lution would be beneficial for addressing longer term
nuances in feeding ecology, and future work would
benefit from seasonal and yearly sampling. Both these
improvements are reinforced by the fact that our cur-
rent analysis has shown the importance of physical
variables in fish diet studies and highlights the need
to include spatial, oceanographic and biological factors
when evaluating feeding patterns of myctophids and of
fish in general.
Acknowledgments
This research was partially funded by the University
of San Diego and a Stephen Sullivan Memorial Schol-
arship. We thank the many scientists at the South-
west Fisheries Science Center, NOAA, who made these
samples available, including: L. Ballance, P. Fiedler, V.
Andreassi, C. Hall, M. Kelley, R. Pitman, and G. Wat-
286
Fishery Bulletin 114(3)
ters. We thank W. Watson for laboratory space and
W. Walker for identifying the myctophid samples. We
thank J. Barlow and P. Fiedler for use of smoothed
oceanographic maps and 3 anonymous reviewers for
their comments and editorial suggestions to improve
this article at the manuscript stage.
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288
NOAA
National Marine
Fisheries Service
Fishery Bulletin
established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Evaluation of nucleic acids and plasma l€F1
levels for estimating short-term responses
of postsmolt Atlantic salmon iSatmo salary
to food availability
Email address for contact author: brian.beckman@noaa.gov
Abstract — We evaluated 4 potential
indices obtained by nonlethal sam-
pling for use in determining nutri-
tional state and short-term growth
rate in postsmolt Atlantic salmon
{Salmo salar): the ratio of RNA to
DNA, both RNA and DNA normal-
ized to protein, and plasma levels of
insulin-like growth factor 1 (IGFl).
Fish reared in the laboratory for
27 days were fed, fasted, or refed.
Short-term growth rates (7 to 23 day
intervals) were calculated on a wet-
weight basis. RNA/DNA values were
highly correlated to growth rates,
responded rapidly to changes in food
availability and were the best able
to consistently distinguish between
the fasted and fed treatments. RNA/
protein values were also well cor-
related with growth rate; however,
within any one sampling day, feed-
ing groups could not be differentiat-
ed with this index. DNA/protein in-
creased during fasting but was nei-
ther strongly correlated with growth
rate nor an accurate discriminator of
nutritional state. IGFl values were
positively correlated with growth
rates and responded rapidly with
refeeding but changed little during
the 3 weeks of fasting — a result that
may have been influenced by sam-
pling serially. We propose that RNA/
DNA is a useful nonlethal technique
for estimating recent growth rates
and for identifying the nutritional
condition of individual postsmolt At-
lantic salmon exposed to short-term
changes in food availability.
Manuscript submitted 15 May 2015.
Manuscript accepted 31 March 2016.
Fish. Bull. 114:288-301 (2106).
Online publication date: 3 May 2016.
doi: 10.7755/FB.114.3.3
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Elaine M. Caldarone'
Sharon A. MacLean'
Brian R. Beckman (contact author)^
' Narragansett Laboratory
Northeast Fisheries Science Center
National Marine Fisheries Service, NOAA
28 Tarzwell Drive
Narragansett, Rhode Island 02882
^ Environmental and Fisheries Sciences Division
Northwest Fisheries Science Center
National Marine Fisheries Service, NOAA
2725 Montlake Boulevard East
Seattle, Washington 98112
The ability to measure the growth
rate of a fish can be a powerful tool
for evaluating the survival potential
of an individual. The ability to assess
the nutritional state of a fish, wheth-
er the animal is feeding or fasting
and for how long the fish has been in
that state (hours to days to weeks)
is also highly desirable information
because variation in nutritive state
leads to variation in growth rate.
Currently, there are a limited num-
ber of nonlethal techniques avail-
able for estimating growth rates or
nutritional state (or both) in field-
caught juvenile fish. Longitudinal
cohort analysis is a direct approach
to assessing changes in size (growth);
however obtaining multiple samples
of the same cohort in the field can
be challenging. Biochemical indices
that indirectly yield estimates of
growth rate or nutritional state have
the advantage of providing estimates
within a single sampling. This point
estimate allows an investigation of
the connectivity between nutritional
state and environmental parameters
on relevant temporal and spatial
scales.
In this study we evaluated 4 poten-
tial biochemical indices of short-term
growth-rate or nutritional state in
postsmolt Atlantic salmon (Salmo sa-
lar): the ratio of RNA to DNA (RNA/
DNA), both RNA and DNA on a pro-
tein basis (RNA/pro and DNA/pro,
respectively) and circulating plasma
insulin-like growth factor 1 (IGFl).
Considerable effort has been directed
toward hatchery-based restoration of
Atlantic salmon to 8 rivers in Maine,
where the population has been listed
as endangered since 2009 under the
United States Endangered Species
Act (Federal Register, 2009). Restora-
tion managers require tools to both
assess whether hatchery-reared fish
are thriving in the natural environ-
ment and to assess the condition of
native postsmolts. Identifying a mini-
mally invasive, nonlethal method to
provide an index of growth rate or
nutritional state in postsmolt Atlan-
Caldarone et al.: Biological indices of growth rate and nutritional state of Salmo solar
289
tic salmon would allow restoration managers to evalu-
ate the condition of field-captured fish.
Since their first application in the 1970s, RNA-hased
indices have been used to determine the nutritional
state and growth rates of larval and juvenile fish in
both the laboratory and field (Bulow, 1970; Buckley,
1979; Buckley et ah, 1999; Gwak and Tanaka, 2001;
Vasconcelos et al., 2009; Ciotti et al., 2010; among many
other studies). Juvenile fish grow rapidly through ac-
cretion of protein, and the amount of RNA in a cell is a
measure of the capacity of a cell to synthesize protein
(Millward et al., 1973). MacLean et al. (2008) evaluated
4 tissues in Atlantic salmon postsmolts and determined
that RNA/DNA values from muscle tissue were those
that were the most highly correlated with growth rate,
and that muscle tissue samples could be obtained by
nonlethal means with a biopsy punch. DNA/protein has
been shown to increase during fasting (Bulow, 1970;
Mathers et al., 1993; Fukuda et al., 2001) and thus
could provide useful information about the nutritional
state of a fish. Circulating plasma insulin-like growth
factor 1 (IGFl) is a polypeptide that is involved in a
number of regulatory processes, including differentia-
tion and proliferation of cells. The preponderance of ev-
idence indicates a significant relation between growth
rates and the plasma level of IGFl in fish within some
constraints (see review by Beckman, 2011). Pierce et
al. (2001) have shown that blood can be drawn by non-
lethal means to obtain samples for this index. In most
studies of juvenile fish, sampling has been too infre-
quent to establish the response time of nucleic-acid-
based indices or of IGFl to food variability. Because
our field recaptures of hatchery-reared postsmolts oc-
cur 2 to 3 weeks after their release, we designed our
experiment to focus on nutritive responses to short-
term changes in food availability rather than to lon-
ger term changes. Results presented here are part of
a larger laboratory study designed to evaluate a va-
riety of nonlethal techniques for detecting short-term
changes in the nutritional status of postsmolt Atlantic
salmon. Results regarding proximate body composition,
Fulton’s K, and bioelectrical impedance analysis (BIA)
of the same individuals reported in the present study
can be found in Caldarone et al. (2012).
Materials and methods
Smolts used in this study were progeny of field-caught
Atlantic salmon from the Penobscot River, Maine. They
had been spawned at Craig Brook National Fish Hatch-
ery, East Orland, Maine, and reared at the Green Lake
National Fish Hatchery, Ellsworth, Maine, for 13-15
months. In 2008, 80 randomly selected smolts (52-113
g, 16-21 cm) were anesthetized in buffered tricaine
methane sulfonate (MS-222, 150 mg/L) and were im-
planted intramuscularly with a passive integrated
transponder tag (PIT tag, Biomark, Boise, ID^) to per-
' Mention of trade names or commercial companies is for iden-
mit identification of individuals. The smolts were then
returned to the hatchery tank to allow time for full re-
covery, resumption of feeding, and removal of any tag-
ging-related mortalities (5 fish). Twenty-five days later
the fish were transported to the University of Rhode
Island’s Blount Aquarium facility in Narragansett,
Rhode Island, where they were randomly placed in two
aerated, flow-through tanks (360-L capacity) initially
filled with freshwater trucked from the hatchery. Over
a period of 5 to 6 hours, freshwater was gradually re-
placed with sand-filtered seawater (10°C, 30 ppt). Dur-
ing the next 3 weeks, while the fish were recovering
from the transfer and acclimating to seawater, the wa-
ter temperature was gradually raised to 12°C. During
this period fish were fed to satiation twice per day with
a commercial feed (Corey Optimum Hatchery Feed for
Salmonids, Corey Nutrition Co., Fredericton, NB, Can-
ada), supplemented with freeze-dried krill (Euphau-
sia pacifica, Aquatic Eco-Systems, Inc., Apopka, FL).
Twenty-five days after the initial transfer to seawater,
when the now postsmolts appeared to be acclimated
and feeding well, the experiment commenced (day 0).
Throughout the experiment, water temperature in
each flow-through tank was recorded hourly with an
HOBO® data logger (Onset Computer Corp., Bourne,
MA), and ammonia levels and salinity were tested
weekly. Water temperatures averaged 12.0°C, standard
deviation (SD)=0.2; salinity averaged 31 ppt, SD=1;
and the photoperiod was 15 hours of light to 9 hours
of dark. Part (two-thirds) of each tank surface was
covered with black plastic to provide a low-light ref-
uge, and the remaining third was exposed to overhead
fluorescent lighting that was covered with red plastic
to better mimic natural light.
Feeding treatments and sampling schedule
Five fish were randomly selected on day 0 from the
acclimation tanks, sacrificed, and sampled to provide
baseline biochemical data. The remaining 70 postsmolts
were subdivided into 3 feeding treatments (tanks): fed,
fasted, and fasted then refed. The purpose of the differ-
ent feeding regimens was to produce fish growing at a
range of rates, not to test the effect of ration on growth
rate. By measuring and sampling tagged fish we were
able to assess the relation of the biochemical indices to
growth rate on an individual basis.
The fed treatment (n=24) was fed ad libitum, the
fasted treatment (n-24) received no food, and the refed
treatment in=22) received no food for 11 days followed
by feeding for 16 days. Before being placed in 360-L
flow-through treatment tanks on day 0, all individu-
als were anesthetized with buffered MS-222 (150 mg/L)
in chilled (12°C) seawater, blotted dry, measured for
initial weight (wet weight, WWi„n, nearest 0.1 g) and
for fork length (FL, nearest 0.1 cm), examined for any
gross external abnormalities, and their PIT tag number
tification purposes only and does not imply endorsement by
the National Marine Fisheries Service, NOAA.
290
Fishery Bulletin 114(3)
Table 1
Sampling schedule for postsmolt Atlantic salmon (Salmo salar) reared in the laboratory at 12“C under 3 feeding regimens
(fed; fasted; fasted then refed) in order to determine the response time to varyhing food availability. Condition indices ob-
tained by nonlethal sampling techniques (RNA/DNA; RNA/protein; DNA/protein; IGFl) and wet-weight-based growth rate
were determined for each fish. The refed group was fasted for 11 days and then fed for 16 days. Numbers listed are number
of fish sampled.
Sampling day and feeding regimen
Day 0
Day 3
Day 7
Day 11
Baseline
Fed
Fasted
Refed
Fed
Fasted
Refed
Fed
Fasted
Refed
Fed
Fasted
Refed
Length, weight
5
24
24
22
4
4
0
4
4
0
4
4
22
Muscle plugs
for nucleic acid
and protein
5
0
24
0
4
4
0
4
4
0
4
4
22
Blood sample for
IGFl measurement
5
0
24
0
4
4
0
4
4
0
4
4
22
Day 15
Day 19
Day 23
Day 27
Fed
Fasted
Refed
Fed
Fasted
Refed
Fed
Fasted
Refed
Fed
Fasted
Refed
Length, weight
4
4
5
4
4
5
4
4
5
0
0
7
Muscle plugs for
nucleic acid
and protein
4
4
5
4
4
5
4
4
5
0
0
7
Blood sample for
IGFl measurement
4
4
5
4
4
5
4
4
5
0
0
7
was recorded. Additionally, 2 muscle plugs and a blood
sample were obtained from fish assigned to the fasting
treatment in order to track individual response times
to fasting. Fish in the group of refed postsmolts were
again weighed and measured and then sampled on day
11 to obtain individual baseline fasting values before
fish were refed. Total time needed for the biochemical
sampling was less than 1 minute per fish. From day 3
onward, 5 fish from the fasted and fed treatments were
sampled and sacrificed every 4 days for 20 days. From
day 15 onward, 5 fish from the refed treatment were
sampled and sacrificed every 4 days until day 27 when
7 fish were sacrificed (Table 1). Final wet weight, FL,
2 muscle plugs for biochemical analysis, and a blood
sample for IGFl determination were obtained from all
sacrificed fish. All fish were also sampled for bioelec-
trical impedance analysis (BIA) indices and proximate
body composition (see Caldarone et al., 2012). All as-
pects of this experiment were conducted in accordance
with guidelines established by the Institutional Animal
Care and Use Committee (lACUC) at the University of
Rhode Island
Sampling protocol and biochemical analyses
IGFl Blood samples (0.3 mL) for IGFl analysis were
obtained from the caudal vein using a sterile heparin-
ized syringe (23-gax25-mm needle). Samples were im-
mediately transferred to a microfuge vial, stored on
wet ice for < 0.5 hour, and centrifuged at 5000xg for
5 minutes. Plasma was removed by pipet, transferred
to a 1.5 mL microfuge vial and stored at -SO^C until
further analysis. Samples were analyzed at the Na-
tional Marine Fisheries Service, Northwest Fisheries
Science Center by using an immunoassay to measure
the concentration of IGFl. Briefly, IGFl was isolated
from plasma by acid-ethanol extraction, and measured
by TRF immunoassay by using a modification of the
methods described by Small and Peterson (2005). Each
sample was analyzed in duplicate, and samples with
low (<30%) or high (> 85%) binding, as well as those
with a coefficient of variation exceeding 10%, were re-
analyzed or excluded. IGFl values are reported as ng/
mL plasma.
Nucleic acids and protein A 2-mm diameter biopsy
punch (MacLean et al., 2008) was used to remove 2
muscle samples for analysis of nucleic acids and pro-
tein. Samples were taken from the epaxial muscle be-
tween the lateral line and dorsal fin. Each muscle plug
was immediately placed in a microfuge vial, stored on
wet ice for <0.5 hour and then transferred to -80°C
until analysis. Nucleic acid levels were measured by
using a 2-enzyme (RNase, DNase) ethidium bromide
fluorometric microplate method. On the day of analy-
sis, each muscle plug was transferred to a cold glass
slide and any fat layer, skin, or blood was removed.
The top 2 mm of the muscle plug was transferred to
Caldarone et al.: Biological indices of growth rate and nutritional state of Salmo salar
291
a microfuge vial containing 150 jiL 1% N-lauroylsar-
cosine. The vial was placed in an ice slurry and the
sample was sonicated for three 5-second pulses fol-
lowed by 45 minutes of vortexing at room temperature.
From that point onward, we followed the protocol of
Caldarone et al.^ for nucleic acid analysis. Results from
duplicate plugs were averaged. The ratio of the slope
of the DNA standards to the slope of the RNA stan-
dards was mean=2.5, SD=0.05 {n-7 microplates). This
value can be used to convert the reported RNA/DNA
data for direct comparison with other published stud-
ies (Caldarone et al., 2006). The remaining extract was
stored frozen and later analyzed for protein content by
using a bicinchoninic-acid-based assay adapted for a
microplate format (Caldarone, 2005). Nucleic acids (pg)
are expressed as a RNA to DNA ratio (RNA/DNA; pg/
pg), RNA to protein ratio (RNA/pro; pg/mg) and DNA
to protein ratio (DNA/pro; pg/mg).
Calculations of growth rates Individual instantaneous
weight-based growth rates (per d) were calculated with
the following formula:
growth rate (G) = (In WWt2 - lnWWti)/(/2 - /i)
(Ricker, 1979), (1)
where WW = the wet weight of an individual at time
t (day).
For comparison with previously published data, growth
rates were converted to specific growth rates (% per d)
with the following formula:
SGR=100(eG - 1). (2)
Growth rates for fish in the fed and fasted treatments
were calculated from day 0 until the day the fish were
sacrificed. Growth rates were calculated from day 0
until day 11 for the fasted portion of the refed treat-
ment fish; for the fed portion of the refed treatment
fish, growth rates were calculated from the first day
of refeeding (day 11) until the day the fish were sacri-
ficed. Because there is inherent variability in measur-
ing the wet weight of fish, coupled with small changes
in weight over short time intervals, growth rates from
time intervals <4 days were not included in any of the
statistical analyses.
Data analysis To examine the effect of the feeding
treatment and sampling day on growth rate, RNA/
DNA, RNA/pro, DNA/pro and IGFl, a 2-way multivari-
ate analysis of covariance (MANCOVA) for unbalanced
design was used with WWjnit as the covariate. When
interactions were significant, feeding treatment was
nested in day, and follow-up comparisons were exam-
ined by using Tukey’s HSD multiple range test. Lin-
ear growth rate models with all combinations of the
^ Caldarone, E. M., M. Wagner. J. St. Onge-Burns, and L. J.
Buckley. 2001. Protocol and guide for estimating nucleic
acids in larval fish using a fluorescence microplate read-
er. Northeast Fish. Sci. Cent. Ref. Doc. 01-11, 22 p. [Avail-
able at website]
4 biochemical variables plus WWi^jt were constructed.
Akaike’s information criterion for small sample sizes
(AICc; Wagenmakers and Farrell, 2004) was used to se-
lect the best candidate model from the 31 models test-
ed. Because of high collinearity of RNA/DNA with the
other 3 biochemical indices, all combinations of models
without the RNA/DNA term were also investigated. To
examine the response of the 4 biochemical indices and
growth rate in individual fish to food withdrawal or in-
troduction, paired initial and final data from individual
fish from both the starved and refed fish were analyzed
by using a repeated measure ^-test.
Within each feeding group, a Dunnett 2-tailed ^-test
with WWinit as a covariate was used to detect changes in
growth rate and the 4 biochemical variables compared
with those in a control. Day 0 values were specified as
the control for the biochemical variables for both fasted
and fed treatments. The average growth rate of all fish
from the time they were tagged until day 0 (50 days)
was used as the control growth-rate value with the un-
derstanding that growth rates during this time would
have been less than optimal. For the refed treatment,
values for day 11 (day they were refed) were used as
the control for all variables. An ANCOVA was used to
test whether the slope of the relation of growth rate
to the measured biochemical indices was significantly
different between the fed and refed groups. All statisti-
cal analyses were carried out with SAS software, vers.
9.3 (Statistical Analysis Software Inst., Inc., Cary, NC)
with a significance level set at P<0.05.
Results
At the start of the experiment (day 0) -78% of the
fish exhibited frayed and -12% exhibited eroded dor-
sal and pectoral fins. The frequency and severity of
these conditions did not change throughout the experi-
ment and there were no mortalities during the study.
All fish appeared to be immature and sex was not a
significant factor in any of the statistical analyses. On
day 0, WWjnit ranged from 43 to 132 g and FL from
18 to 23 cm. Initial size distributions (WWjnit) between
feeding treatments were not significantly different (fed
mean=76 g, SD=12; fasted mean=75 g, SD=13; fasted
then refed mean=80 g, SD=4).
Weight-based growth rates of the fish responded
quickly to changes in food availability. Fasted fish lost
weight beginning on day 7 and by day 11 their growth
rates were statistically significantly less than the con-
tinually fed fish (Fig. lA). Negative growth rates of
the fasted fish remained constant throughout the ex-
periment (Dunnett, P=0.747), whereas fed fish growth
rates increased in relation to day 0 rates (Dunnett,
P<0.0001). On day 19, fed fish had faster growth rates
than refed fish, whereas the relation was reversed on
day 23. Refed fish grew significantly faster than fasted
fish beginning 4 days after refeeding (day 15). During
the experiment we noted that the feeding intensity
of the salmon visibly decreased when the total num-
292
Fishery Bulletin 1 14(3)
A
B
Figure 1
(A) Specific growth rates (% wet weight per d); and (B)
RNA/DNA values of postsmolt Atlantic salmon (Salmo sa-
lar) reared in the laboratory at 12°C. Fish were either fed ad
libitum, fasted, or refed (fed after 11 days of fasting). Values
are mean values (±standard deviation [SD]) for each sampling
day. Growth rates for fish in the fed and fasted treatments were
calculated from day 0 until the day they were sacrificed. Growth
rates for the refed treatment were calculated from the first
day of refeeding (day 11) until the day fish were sacrificed.
Within a sampling day, food treatments showing a common
superscript, or without superscripts, do not differ significantly
(Tukey’s HSD multiple range tests). Where error bars would
overlap, data are offset to facilitate viewing. The arrow indi-
cates the day when food was introduced to the refed group. For
fed and fasted fish, n-4 for each sampling day. For refed fish,
n=22 for day 11, n=5 for days 15, 19, and 23, and re=7 for day
27.
ber of fish in the tanks fell below 8 individu-
als because of sampling. This observation was
confirmed by the decrease in average growth
rates for fish sampled on the last day of both
the fed (day 23) and refed (day 27) treatments
(Fig. lA).
After 11 days, RNA/DNA values were sig-
nificantly greater in fed fish than in the fasted
portion of the refed fish (Fig. IB), and from
day 15 onward, significantly greater than val-
ues for fish in the fasted group. Twelve days
after refeeding, RNA/DNA values of the refed
group were greater than the fasted fish and
equal to the continually fed fish (day 23, Fig.
IB). Mean RNA/DNA values in fed and refed
fish increased in relation to their mean start
values (Dunnett, F=0.011, P<0.0001 respec-
tively), whereas mean RNA/DNA values for
fasted fish decreased beginning 15 days after
food was withheld (Dunnett, F=0.003). Re-
peated measurements from individuals in the
fasted group exhibited an overall significant
decrease in RNA/DNA from their start values
(Student’s paired t test F<0.0001, Fig. 2A).
Repeated measurements of refed fish exhib-
ited an overall significant increase from their
individual start values (Student’s paired Ntest
F<0.0001, Fig. 2B). RNA/DNA values were
highly positively correlated with growth rates
in the fed group, refed group, and the all-data-
combined group, but not in the fasted group
(Table 2).
Beginning on day 11, RN A/pro values were
generally greater in the fed fish than in the
fish in the fasted treatment (Fig. 3A). In fed
fish, mean RNA/pro values did not change from
mean initial values (Dunnett F=0.391), where-
as fasted fish showed modest decreases with a
significant Dunnett value (F=0.009), primarily
driven by 1 fish on day 19 (Fig. 3A). Beginning
8 days after refeeding (day 19), mean RNA/pro
values of refed fish increased from the mean
start value (Dunnett F<0.0001). The same pat-
tern was seen in paired data from individuals;
repeated measurements from fasted fish exhib-
ited an overall significant decrease from their
start values (Student’s paired /-test F=0.002),
whereas values of refed fish increased (Stu-
dent’s paired /-test F<0.0001) (plots not shown).
RNA/pro values were positively correlated with
growth rates in the fed group, refed group, and
the all-data-combined group, but not in the
fasted group (Table 2).
The DNA/pro ratio of fasted and refed fish
was higher (smaller cells) than in fed fish, and
the main effect of feeding treatment on DNA/
pro was statistically significant (Fig. 3B); but,
because of high daily variability, coupled with a
small sample size, most Tukey- Kramer post-hoc
comparisons of feeding treatment within a sam-
Caldarone et al.: Biological indices of growth rate and nutritional state of Salmo solar
293
r
Q
2 -
I
W
w
ill
¥
TA
▼ ;
▼i
7 11 15
Days fasted
19
23
B
<
z 4
Q ^
Z
a: 3
nil
48 12 16
Days after refeeding
Figure 2
Each arrow represents changes in RNA/DNA
values of individual laboratory-reared postsmolt
Atlantic salmon (Salmo salar) that were either
(A) fasted or (B) refed (fed after 11 days of fast-
ing). Direction of the triangle is the direction of
change in the values from (A) day 0 start val-
ues (when fish were fed) through the number of
days (23 d) that fish were fasted; and (B) day 11
values (start of fasting) through number of days
(16 days) that fish were refed after fasting. The
open and closed triangles differentiate between
the two different directions of change.
pie day were not statistically significant. Within each
food treatment; DNA/pro did not change from mean ini-
tial values (Dunnett P=0.295, 0.090, 0.071 fasted, fed,
refed, respectively). However, repeated measurements
of individuals indicated that DNA/pro in individual fish
increased during fasting (Student’s repeated measure
/-test P=0.033) (plot not shown). DNA/pro values were
not correlated with growth rates in the 3 individual
food treatment groups but had a significant, although
Table 2
Pearson product-moment correlations (r) between the
instantaneous weight-based growth rate (per d) of
postsmolt Atlantic salmon (Salmo salar) and the ratio of
RNA:DNA (RNA/DNA, pg/pg), RNA and DNA on a pro-
tein basis (SNA/pro, DNA/pro, respectively, pg/mg), and
circulating plasma insulin-like growth factor 1 (IGFl,
ng/mL). Fish were either fed or fasted for 23 days, or
refed (fed for 16 days after 11 days of fasting). For each
feeding treatment, boldface type highlights the high-
est significant correlation with growth rate. *F<0.05,
**P<0.005, ***P<0.0001. «,=number of fish sampled.
Variable
Fed
Fasted
Refed
All data
n
19
19
17
55
RNA/DNA
0.882***
-0.295
0.853***
0.832***
RNA/pro
0.765***
-0.190
0.666**
0.727***
DNA/pro
-0.354
0.090
-0.238
-0.507***
IGFl
0.502*
-0.403
0.543*
0.661***
low, negative correlation when all three groups were
combined (Table 2).
Within a sample day, IGFl values between feed-
ing treatments were not statistically significantly dif-
ferent (Fig. 3C). As with DNA/protein measurements,
high variance (SD), coupled with a small sample size,
yielded very low statistical power to detect differences
between treatments. Beginning on day 15 and con-
tinuing until the conclusion of the experiment, mean
IGFl values in fed fish were significantly greater than
day-0 mean values (Dunnett P<0.0001). Fasted fish
showed no change in IGFl with time, either on a dai-
ly mean (Dunnett F=0.722) or on an individual basis
(Student’s repeated measure /-test P=0.065, Fig. 4A).
Mean IGFl values of refed fish increased 12 days af-
ter food was introduced (day 23, Dunnett F<0.0001),
and repeated measurements of individuals indicated
that final IGFl values in refed fish were greater than
their start values (Student’s repeated measure /-test
F=0.0001, Fig. 4B). IGFl values were positively and
significantly correlated with growth rates in the fed
group, refed group, and the all-data-combined group
(Fig. 5, Table 2).
A plot of growth rate vs. RNA/DNA by food treat-
ment revealed a difference in the relation of RNA/DNA
to growth rate between the fed and refed groups (Fig.
6). ANCOVA results confirmed that the slopes of the
regression lines of the two feeding treatments were the
same but the intercept of the refed data was signifi-
cantly greater. Slopes and intercepts of the regressions
between the other 3 biochemical measures and growth
rate did not differ between the fed and refed groups.
Linear growth models containing all combinations of
WWjnit, RNA/pro, DNA/pro, RNA/DNA, and IGFl were
examined (31 models). On the basis of AICc values, the
best candidate model for predicting growth rate in-
294
Fishery Bulletin 114(3)
05 "
E
3: 22
C
'a)
2 18
Q.
a:
Fed
— Fasted
-- Refed
i
a
^ I
\
Cl
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c5)
c
LL
33
o
19
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5
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3
6
9 12 15 18 21
Day
Figure 3
(A) RNA/protein (pg/mg); (B) DNA/protein (pg/mg) and
(C) IGFl (ng/mL plasma) values of postsmolt Atlantic
salmon {Sal/no salar) reared in the laboratory at 12°C.
Values are mean values (±standard deviation [SD]) for
each sampling day. Fish were either fed ad libitum,
fasted, or refed (fed after 11 days of fasting). Within a
sampling day, food treatments showing a common su-
perscript, or without superscripts, do not differ signifi-
cantly (Tukey’s HSD multiple range tests). Where error
bars would overlap, data are offset to facilitate viewing.
The arrow indicates the day when food was introduced
to the refed group. For fed and fasted fish, n=4 for each
sampling day. For refed fish, n=22 for day 11, n=5 for
days 15, 19, and 23 and n=7 for day 27.
eluded RNA/DNA and IGFl (Table 3). Because RNA/
DNA was highly correlated with the other biochemical
terms, we also tested all combinations of the remain-
ing 4 terms after eliminating RNA/DNA (15 models).
The best candidate for a growth rate model from this
grouping included RNA/pro, DNA/pro, and IGFl, and
was essentially identical in predictive capability and
mathematically equivalent to the model containing
RNA/DNA and IGFl (Table 3).
Summary
RNA/DNA ratios and recent growth rates of fed fish
increased throughout the study and were highly cor-
related. Fed and fasted feeding treatments could be
differentiated by RNA/DNA values after 11 days of
fasting, and on an individual basis, significant decreas-
es in RNA/DNA values were observed after 7 days of
fasting. Growth rates and RNA/DNA values of previ-
ously fasted fish increased rapidly beginning 4 days
after refeeding. The intercept from regressing growth
rate on RNA/DNA was greater in refed fish than in
continually fed fish, whereas the slopes were parallel.
In the fasted group, the rate of weight loss remained
fairly constant throughout the experiment and RNA/
DNA values decreased.
In all 3 feeding treatments, RNA/pro values showed
similar trends to those of RNA/DNA values; however,
there was less statistical differentiation between the
feeding treatments on most sampling days. Overall,
fasted fish had significantly greater DNA/pro values
(smaller cells) than fed fish, yet feeding treatments
within a day could not be distinguished on this basis.
Mean IGFl values increased in fed fish but remained
constant in fasted fish owing to inconsistent individual
responses to fasting. Based on repeated measurements
of individuals, IGFl values responded rapidly (4 days)
to refeeding. Owing to high daily variability, feeding
treatments within a sampling day could not be distin-
guished with this index. A positive and significant rela-
tion was found between IGFl and growth rate.
Of the 31 models tested, the best-fit growth rate
model included RNA/DNA and IGFl with a coefficient
of determination (r^) =0.73.
Discussion
The goal of our research and its companion study
(Caldarone et ah, 2012) was to identify physiological
indices that could be obtained by nonlethal means
and that would respond rapidly to short-term changes
(4-23 days) in the nutritional state (feeding and fast-
ing) of individual postsmolt salmon. The response time
of an index allows investigators to match the index to
environmental parameters on relevant temporal and
spatial scales. Of the four indices we measured in this
study, RNA/DNA was the most highly correlated with
short-term growth rate. In sexually immature fish, an
index that reflects protein production should be appro-
Caldarone et al.; Biological indices of growth rate and nutritional state of Salmo salar
295
80
65
CD
E
m
M
a
1
c
^ 35
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<-
i_
A
▼
LL
g
20
i
V-
1
A ^
e
V
%
f
A
1 1
'A
A
7 11 15
Days fasted
19
23
cd
E
m
a
Q.
D)
C
O
80
65
50
35
20
B
48 12 16
Days after refeeding
Figure 4
Each arrow represents changes in IGFl values (ng/mL
plasma) of individual laboratory-reared postsmolt Atlantic
salmon {Salmo salar) that were either (A) fasted or (B)
refed (fed after 11 days of fasting). Direction of the triangle
is the direction of change in the values from (A) day 0 start
values (when fish were fed) through the number of days (23
d) that fish were fasted; and (B) day 11 values (start of fast-
ing) through number of days (16 days) that fish were refed
after fasting. The open and closed triangles differentiate
between the two different directions of change.
priate for estimating growth. At this stage, juvenile fish
are directing their energy toward increasing their size
to enable them to better escape predators and search
for and capture prey (Shulman and Love, 1999). RNA
based indices have consistently been shown to be well
correlated with both weight-based and protein-based
recent growth rates in multiple species of juvenile fish
(Arndt et al., 1994; Peck et al., 2003; Stierhoff et al.,
2009; Ciotti et al., 2010). RNA/DNA values of our fish
responded quickly to changes in food availability. On
the basis of repeated measurements of individuals,
one-half of the refed fish sampled exhibited increases
in RNA/DNA 4 days after food re-introduction, and
RNA/DNA values in all refed fish increased by the
gth Other researchers have reported statistically
significant increases in RNA/DNA and RNA con-
centration in fish within 1-4 days after being refed
(Malloy and Targett, 1994; Stierhoff et al., 2009;
Ciotti et ah, 2010). The differing response times to
refeeding is most likely linked to varying lengths of
time fasted before food was re-introduced, to sizes
of the fish, and to developmental stage or species.
Our fish lost weight after 7 days of fasting and re-
peated measurements of individuals indicated that
RNA/DNA values also decreased within this time
frame. Decreases in RNA/DNA and RNA concentra-
tion have been observed after 1-14 days in a variety
of juvenile fish (Loughna and Goldspink, 1984; Low-
ery and Somero, 1990; Arndt et al., 1996; Stierhoff
et al., 2009; Ciotti et al., 2010). A differing response
time of RNA/DNA to fasting is most likely due to
temperature, species, developmental stage, and
amount of fat stored (i.e., resistance to fasting). For
example, Arndt et al.’s (1996) Atlantic salmon fry
were much smaller than our postsmolts, averaged a
weight loss rate lOx faster (-4.3% vs. -0.36%), and
their RNA/DNA values decreased in approximately
1/2 the time compared with that of our postsmolts.
But in all instances, response time of RNA/DNA to
fasting has been observed over a time period of days
to two weeks. This relatively rapid response of RNA/
DNA values to short-term changes in food availabil-
ity would allow researchers to investigate linkages
between environmental variables and nutritional
status of postsmolt Atlantic salmon on ecologically
relevant scales.
The rate of protein accumulation is the differ-
ence between the rate of degradation and the rate
of protein synthesis, and the rate of protein synthe-
sis is dependent not only on RNA concentration but
also its activity (rate of translation) and efficiency,
among other factors (see review by Fraser and Rog-
ers, 2007). Our fasted fish lost weight at a fairly
constant rate throughout the experiment; however,
a wide range of RNA/DNA values (4 to 2.5, Fig. 6)
were associated with this negative growth rate and
there was a noticeable trend toward lesser values
as fasting days increased. These results indicate
that, at least initially, the observed weight loss was
either due to protein degradation rates increasing
or translation rates decreasing (or both) before RNA
concentrations decreased. An initial decrease in trans-
lation rates preceding a decrease in ribosomal num-
ber has been observed in fasting fish (Loughna and
Goldspink, 1984; Lowery and Somero, 1990). During a
previous study of Atlantic salmon postsmolt (MacLean
et al., 2008), we observed a similar range of RNA/DNA
values (4 to 2) associated with negative growth rates
(Fig. 7). Because both studies were conducted at com-
parable temperatures and nucleic acids were analyzed
with identical methodologies, RNA/DNA values from
the two studies can be combined. On the basis of the
data from both studies, we propose an RNA/DNA value
of 3.0 as a conservative cutoff for distinguishing be-
tween positive and negative growth rates in juvenile
296
Fishery Bulletin 114(3)
Figure 5
Growth rate (% wet weight per d) versus IGFl for postsmolt At-
lantic salmon {Salmo salar) reared in the laboratory at 12°C and
sampled throughout a 27-day period. Fish were fed ad libitum,
fasted, or refed (fed after 11 days of fasting). Regression lines rep-
resent fed (— ) and refed (- -) fish.
RNA/DNA
Figure 6
Specific growth rate (% wet weight per d) versus RNA/DNA for
postsmolt Atlantic salmon {Salmo salar) reared in the laboratory
at 12°C and sampled throughout a 27-day period. Fish were fed ad
libitum, fasted, or refed (fed after 11 days of fasting). Regression
lines represent fed (• — ) and refed (- -) fish.
Atlantic salmon residing at temperatures
near 12°C.
Changes in RNA translation rates also
may have influenced the relation of RNA/
DNA to growth rate in the refed fish. Refed
fish accumulated more protein per unit of
RNA than their continually fed counterparts
as evidenced by the significantly greater re-
gression intercept (Fig. 6). This increase in
protein accumulation could be due to an in-
crease in translation rate or to a decrease
in protein degradation rate (or to both). Re-
searchers who have observed an increase in
protein accumulation per unit of RNA have
attributed it to a translation increase (Mc-
Millan and Houlihan, 1988, 1989; Miglavs
and Jobling, 1989) although direct published
evidence for choosing between the two path-
ways is scarce. Because traditional estimates
of nucleic-acid-based growth-rates do not in-
clude a translation rate estimate, field esti-
mates of RNA/DNA-based growth rates will
not be exact. Nonetheless, by combining our
refed with the fed and fasted data sets we ob-
tained a significant regression between RNA/
DNA and growth rate (r2=0.692, P<0.0001)
that can be used to coarsely estimate field
growth rates at temperatures near 12°C. Be-
cause temperature affects protein degrada-
tion and translation rates (Buckley et ah,
1999; McCarthy et al., 1999; Ciotti et ah,
2010), a model incorporating an interaction
term of temperature with RNA/DNA would
need to be constructed before growth rates
at different temperatures could be estimated.
RNA/pro In our study, RNA/pro values were
less correlated with growth rate than the
RNA/DNA values, although the relation of
both indices to growth rate was similar, i.e.,
there was a high correlation with positive
growth rates but a range of values associ-
ated with a constant negative growth rate.
Unlike RNA/DNA, RNA/pro from both the
fed and refed groups had the same relation
to positive growth rates which could be ad-
vantageous for estimating field growth rates
where the past feeding history of the animal
is unknown. Repeated measurements of in-
dividuals indicated that RNA/pro responded
quickly to food withdrawal (7 days) and re-
introduction (4 days), but within any one-day
values were variable, resulting in sampling
days where the feeding groups could not be
differentiated with this index. The positive
and negative response of growth rate, RNA/
DNA, and RNA/pro in individual fish to the
positive and negative changes in food avail-
ability, respectively, and the high correlation
Caldarone et al.: Biological indices of growth rate and nutritional state of Salmo salar
297
Table 3
Coefficients and Akaike’s second-order information criterion for small sample sizes (AICc) for the top candidate regression
models for growth rate of postsmolt Atlantic salmon (Salmo salar) reared at 12°C under 3 feeding regimens in order to gener-
ate a range of nutritional condition and growth rates. RNA/DNA (pg/pg); IGFl=:circulating plasma insulin-like growth factor
1 (ng/mL); RNA/pro=RNA/protein (pg/mg); DNA/pro=DNA/protein (pg/mg); AAICc=difference in AICc values with respect to
the best candidate model. For all models P<0.0001. r^=coefficient of determination.
Dependent variable
n
Model
AICc
AAICc
All variables tested
Growth rate (per d)
53
-0.0181-^0.0040(RNA/DNA)-l-0.0001(IGFl)
0.733
-547.81
0
Growth rate (per d)
53
-0.0173+0.0048(RNA/DNA)
0.686
-542.39
5.42
RNA/DNA not included
Growth rate (per d)
53
-0.0045-i-0.0011(RNA/pro)-0.0036(DNA/pro)+0.0001(IGFl)
0.738
-546.53
1.28
Growth rate (per d)
53
0.0001-!-0.0013(RNA/pro)-0.0045(DNA/pro)
0.712
-543.82
3.99
1.5
CD
Q.
^ 1.0
This study
Maclean et at, 2008
0.5
cP A
* B
"i * '
» ^ cP □
^ □
O
o
□ □ a 5 P
°a Dj
□ „_na dp ^
0.0
-0.5
2 3 4 5 6 7 8
RNA/DNA
Figure 7
Specific growth rate (% wet weight per d) versus RNA/
DNA for postsmolt Atlantic salmon (Salmo salar) reared
in the laboratory. ♦ denotes data from fed and fasted fish
held at 12° C and sampled throughout a 27-day period
(present study). □ denotes data from the study of MacLean
et al. (2008) in which postsmolts were sampled at the end
of 30 days at a final water temperature of 12.8°C. In both
experiments nucleic acid values were determined by the
same method.
of RNA/DNA and RNA/pro to fed and refed growth
rates are evidence that the relations between RNA
indices and growth rate were not altered by repeated
sampling of individual fish.
How best to standardize RNA values (RNA/DNA vs.
RNA/pro) is not clear and may depend upon the devel-
opmental stage of the fish. Fish muscle is unique in
that it increases in size throughout the life of a fish
owing to both hyperplasia (increase in cell number)
and hypertrophy (increase in cell size) (Weatherly et
al., 1988; Higgins and Thorpe, 1990; Koumans et al.,
1993; Mommsen, 2001). Hyperplastic muscle growth
is accomplished by fusion of myosatellite cells, re-
sulting in a brief initial increase in DNA per cell
followed by a nearly constant amount of DNA per
cell. In contrast, muscle growth through hypertrophy
produces multiple nuclei per cell and often multiple
copies of DNA per nucleus (polyploidy) resulting in a
variable amount of DNA per cell (Jimenez and Kin-
sey, 2012). Higgins and Thorpe (1990) investigated
muscle growth in Atlantic salmon and concluded that
juvenile Atlantic salmon (<15 cm) increased muscle
mass by hyperplasia, whereas hypertrophy was more
important in autumn and winter when growth of the
salmon was slow. Weatherly et al. (1988) concluded
that in fish smaller than approximately 44% of their
maximum size, most fish muscle growth was due to
hyperplasia. Our fish were recent postsmolts, approx-
imately 23% of their maximum size, and most likely
increasing their muscle size predominantly through
hyperplasia. In our study, RNA/DNA performed bet-
ter than RNA/pro for indicating short-term growth.
In general, RNA/DNA may be the better indicator of
growth rate during larval and juvenile stages when
a fish is growing rapidly by increasing cell numbers.
Until the relation of RNA to DNA in polyploidy cells
is better known, RNA/pro may be the preferred in-
dicator of growth rate in older fish where growth
by hypertrophy predominates. In adults, however,
RNA-based indices may not be an appropriate index
of condition or growth rate. In the adult stage, pro-
tein synthesis is directed more toward protein turnover
rather than protein accretion. Additionally, fat reten-
tion or gonad development may be the driving force
behind weight-specific growth. This increase in nonpro-
tein mass would cause an uncoupling of the relation of
RNA-mass to growth rate. Because the turnover rate
of RNAs (mRNA, tRNA, rRNA) ranges from minutes to
a few days (see Fraser and Rogers, 2007), RNA-based
indices would be most useful for estimating recent
growth rates and current nutritional state and would
298
Fishery Bulletin 1 14(3)
not be an appropriate index to measure growth rates
over long periods of time (months).
DNA/pro Some studies have reported an increase in
DNA/pro (or its equivalent DNA/dry weight) during
starvation, presumably due to muscle protein being
used as an energy source while DNA content remained
stable (Fukuda et ah, 2001; Mathers et al., 1993; Mal-
zahn et al., 2003). Our results are consistent with this
observation with our fasted fish having significantly
more DNA per unit of protein than both the fed and
refed groups. However, DNA/pro was not strongly cor-
related with growth rate and feeding treatments with-
in a day could not be distinguished on the basis of this
index. Given the complex relation between DNA con-
centration and hyperplasia and hypertrophy, DNA/pro
would not be a good potential physiological index of
short-term changes in growth rate or nutritional state
in juvenile salmon.
IGF1 IGFl is an essential component in the endocrine
system that regulates growth. Because of this attribute,
experiments have been conducted to investigate the en-
docrine response of the coupled growth hormone and
IGFl systems (GH-IGFl) to nutritional state to help un-
derstand how that system regulates growth. Numerous
studies have reported decreases in IGFl in fish fasted
for 4 or more weeks (Moriyama et al., 1994; Larsen et
al., 2001; Picha et al., 2008) but few studies have inves-
tigated its use to assess the nutritional condition of fish
over short time periods. Shimizu et al. (2009) reported
a decline in IGFl levels in coho salmon (Oncorhynchus
kisutch ) after 1 week of fasting and a statistically sig-
nificant decrease after 3 weeks, whereas IGFl levels
in young Chinook salmon {Oncorhynchus tshawytscha)
decreased significantly 6 days after fasting (Pierce et
al., 2005). Based on repeated measurements of indi-
viduals in our study, IGFl values in our fasting fish
changed little throughout the 3 weeks. Different resis-
tances to fasting may explain the different results. Of
the aforementioned studies, Chinook salmon had low
fat levels (3-5% by weight) and had the greatest rate
of weight loss. Fat content of our Atlantic salmon was
7-8%; their body composition remained relatively stable
throughout the experiment and there was only a small
loss of fat in the fasted treatment (Caldarone et al.,
2012). Based on repeated measurements of individuals,
IGFl levels in our fish responded rapidly to refeeding;
values increased 4 days after the fish were refed. Im-
mature rainbow trout {Oncorhynchus mykiss) that had
been fasted for 4 weeks also exhibited increases in IGFl
levels 4 days after they were refed (Gabillard et al.,
2006), whereas Atlantic salmon smolts after 15 days
of fasting showed no change 7 days after being refed
(Wilkinson et al., 2006). Further research is needed to
determine factors affecting the response time of IGFl
to changes in food availability.
High variability in both the fasted and fed groups,
coupled with a small sample size, hampered detection
of statistically significant differences in IGFl between
our food treatments. Researchers have suggested that
large differences in growth rate or a large sample size
may be needed to use IGFl levels to separate fish by
nutritional condition (Beckman et al., 2004a, 2004b)
(also see below with regard to serial sampling, acute
stress, and IGFl levels).
A significant linear relation has been observed be-
tween circulating plasma IGFl levels and growth rate
in a variety of salmonids (Pierce et al., 2001; Beckman
et al., 2004a; Dyer et al., 2004). Beckman (2011) stated
a number of caveats for the use of IGFl as a growth
index; in particular, do not compare fish in differing
stages of maturation, be aware of issues which may
be introduced by rapid changes in temperature, and be
aware of potential difficulties which may be introduced
by acute stress. Indeed in some studies, nonsignificant
relations between IGFl and growth have been reported
(Silverstein et ak, 1998; Andrews et al., 2011, in large
but not small juvenile lingcod; Beckman et al., 2004b,
in juvenile coho salmon soon after transfer to cool wa-
ter, but not fish maintained in warm water nor fish
acclimated to cool water). In our study the relation be-
tween IGFl levels and growth rate was positive and
significant but not highly correlative. It is possible that
the IGFl values were affected by our serial sampling
protocol (multiple nonlethal blood draws). Pierce et al.
(2001) compared IGFl and growth relations between
terminally and serially sampled juvenile coho salmon
and found a large decrease in the correlation coefficient
(r=0.78 vs r=0.51) between the two protocols. The cor-
relation between IGFl and growth in the present work
(r=0.66) was more in line with Pierce’s serially sampled
values than with the more highly correlated responses
found in studies with terminally sampled values (see
Beckman, 2011).
The best candidate model for estimating growth rate
did contain both IGFl and RNA/DNA terms. These two
indices reflect differing aspects of the physiology of
growth. As part of the GH-IGFl endocrine system, IGFl
levels reflect a specific stimulus for cellular growth,
whereas RNA/DNA is a measure of a cell’s capacity for
growth. Thus the two measures together would reflect
both upstream regulation of cellular growth and down-
stream response to that regulation.
Circulating levels of plasma IGFl in fish are regu-
lated by a suite of at least 6 different IGF binding pro-
teins (Duan, 2002). These binding proteins themselves
are differentially regulated by nutritional state as well
as other factors, perhaps including stress (Kelley et
ah, 2001). The circulating level of IGFl in the blood
generally is determined by the most abundant binding
protein (IGFBP2b), which itself is regulated by nutri-
tional states (Shimizu et al., 2009; Kawaguchi et al.,
2013). The establishment of methods to measure IGF
binding proteins in fish blood is still on-going (Shimizu
et al., 2011a, 2011b) and our understanding of the fac-
tors that regulate the abundance of different binding
proteins and how they affect IGFl levels is quite in-
complete. We do not have the technical capacity to de-
termine whether or not the current results (IGFl and
Caldarone et al.: Biological indices of growth rate and nutritional state of Salmo solar
299
fasting, IGFl and growth, IGFl and refeeding) were
due to the induction of different suites of binding pro-
teins and how these proteins may have affected circu-
lating IGFl levels differently from those of other stud-
ies. Shimizu et al. (2009) demonstrated a significant
increase in 41kDa IGFBP of fasting fish in response
to refeeding; perhaps the IGFl increase we observed
in our individual refed fish was modulated by changes
in circulating IGFBP levels. The fact that IGFl levels
of fasted fish did increase in response to refeeding and
that the overall relation of IGFl to growth was positive
and significant gives us confidence that IGFl responds
to changes in nutrition and growth. The use of IGFl
measures has been demonstrated in several ecological
studies of juvenile salmonids where differences in IGFl
levels have been observed in fish reared in different ar-
eas (Bond et al., 2014; Daly et ah, 2014; Ferriss et al.,
2014). However, we suggest that the specific response
of IGFl and IGFBPs to fasting, feeding, and growth,
in combination with acute or chronic stress, should be
investigated.
Of the indices reported here (RNA/DNA, RNA/pro,
DNA/pro, IGFl) and in Caldarone et al. (2012) (Ful-
ton’s K, BIA), RNA/DNA was the most suited for es-
timating recent growth rates and identifying the nu-
tritional condition of our individual postsmolt Atlantic
salmon exposed to short-term changes in food avail-
ability. Removing muscle samples with a biopsy punch
for RNA/DNA analysis did not result in any mortalities
and did not appear to inhibit growth of the fish, as evi-
denced by the rapid increase in growth rates of refed
fish soon after a muscle sample was taken. The short
response time of RNA/DNA (4-8 days) in individual
fish to both positive and negative changes in food avail-
ability would allow researchers to investigate linkages
between environmental variables and nutritional state
on ecologically relevant scales. With the addition of a
temperature calibration, estimates of growth rates in
the field at a variety of temperatures could be calcu-
lated with RNA/DNA values
Acknowledgments
The authors would like to thank E. Baker, and K.
Fredrick for assistance in aquarium setup and tem-
perature control, M. Prezioso and J. St. Onge-Burns
for help in rearing the salmon, K. Cooper for running
the IGFl analyses, and the University of Rhode Island
Graduate School of Oceanography for the use of Blount
Aquarium.
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302
NOAA
National Marine
Fisheries Service
Fishery Bulletin
<%• established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Seasonal changes in abundance and compelling
evidence of migration for 2 rockfish species
ISebmtes auriculatm and S. caurinm} inhabiting
a nearshore^ temperate-miater artificial reef
Abstract— We used scuba over fixed-
width strip transects to monitor sea-
sonal abundances of brown rockfish
{Sebastes auriculatus) and copper
rockfish (S. caurinus) on a nearshore
artificial reef in Puget Sound, Wash-
ington, over a 7-year period. Spring
and fall abundances were intermedi-
ate and marked transitional phases
between seasons of highest (sum-
mer) and lowest (winter) abundance
for both species. Analyses of length
classes indicated that the numbers
of seasonal juvenile recruits were
not sufficient to account for the
marked differences in abundance
between summer and winter. For
both species, the proportion of large
fish (>20 cm in total length) to the
total number observed in summer
and winter was significantly greater
during the winter. Late-stage gravid
brown rockfish occurred in greatest
abundance during the spring and
late-stage gravid copper rockfish
were observed only in the summer.
We examined auxiliary data from
a genetics study of brown rockfish
that was conducted concurrently at
the reef and interpreted the results,
along with our survey findings, as
providing compelling evidence of
seasonal migrations on and off the
reef.
Manuscript submitted 20 October 2015.
Manuscript accepted 19 April 2016.
Fish. Bull. 114:302-316 (2016).
Online publication date: 6 May 2016.
doi: 10.7755/FB.114.3.4
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Larry L. LeOair Ccantact author)
Ocean Eveningsong
Jesse M. Schulte
Email for contact author: larry.ledair@dfw.wa.gov
Washington Department of Fish and Wildlife
600 Capitol Way North
Olympia, Washington 98501
Understanding fish movement is par-
amount to the design and implemen-
tation of effective resource conser-
vation and management strategies.
Movement influences the dynamics,
demographics, and genetics of popu-
lations; the structure and function
of ecosystems; species interactions;
modes of energy transfer; and bio-
diversity (Rothschild, 1986; Frank,
1992; Merz and Moyle, 2006; Clark et
al., 2009; Condal et ah, 2012). Known
patterns of movement are often key
considerations in the development
of harvest management plans es-
tablished to protect fish populations
from overexploitation. For example,
in the northeast Pacific Ocean, ling-
cod {Ophiodon elongatus) are widely
believed to participate in seasonal
nearshore-offshore spawning mi-
grations (Jagielo, 1990, 1995), and
in some regions (e.g., Puget Sound),
recreational fisheries that target
lingcod are managed to protect near-
shore spawning fish (Palsson et al.^).
Pacific halibut {Hippoglossus stenol-
1 Palsson, W. A., T. J. Northup, and M. W.
Barker. 1998. Puget Sound Ground-
fish Management Plan, 48 p. Washington
Dep. Fish Wildl., Olympia. [Available
at website.]
epis) also undergo seasonal migra-
tions (St-Pierre^), and establishment
of the commercial fishery season by
the International Pacific Halibut
Commission is designed in large part
to protect offshore spawning popula-
tions (Loher, 2011).
Fish movement also has crucial
implications for the design of scien-
tific sampling strategies and stock
assessments, and movement poses
both operational and conceptual chal-
lenges for the selection of appropriate
temporal and spatial scales in ecolog-
ical studies. Inferences about the eco-
logical processes under investigation
may be constrained or confounded
when, as is often the case, scales of
operational convenience, rather than
ecological relevance, are incorporated
into study designs. Failure to identi-
fy and integrate fish movement into
study designs can lead to the selec-
tion of temporal or spatial scales of
observation that are ill-fitted to the
study objectives, particularly when
movement occurs over multiple habi-
tat types. Sampling strategies that
2 St-Pierre, G. 1984. Spawning loca-
tions and season for Pacific halibut. Int.
Pac. Halibut Comm., Sci. Rep. 70, 46
p. [Available at website.]
LeClair et al.: Seasonal changes in abundance and migration of Sebastes auriculatus and 5. caurinus
303
focus on single habitat types are also subject to bias
when based on untested assumptions about habitat
use, extent of home range, and site fidelity, as reviewed
by Pittman and McAlpine (2003). These authors assert
that if information on movement is not available, the
assumption of single habitat use should be considered
carefully or rejected entirely. They advocate for an as-
sumption of the use of multiple habitats because it al-
lows for the consideration of broader-scale movement
and potential linkages among habitat types. Movement
patterns, whether over short (e.g., diel) or long (e.g.,
seasonal, annual) temporal scales, rank as one of the
most important behavioral sources of bias in fish stock
assessments (Gayanilo and Pauly, 1997; Sparre and
Venema, 1998). Statistical methods for incorporating
patterns of fish movement into stock assessments are
advancing (Hilborn and Walters, 1992; Methot, 2011),
and the integration of known fish behavior parameters,
such as diel and seasonal movements, will likely lead
to substantial improvements in the accuracy of stock
assessment models (Freon et al., 1993).
Although the potential conservation benefits of indi-
vidual marine protected areas (MPAs) have been dis-
cussed for decades, there is currently a growing world-
wide interest in establishing coordinated networks of
MPAs that are ecologically joined over broad geographic
regions, and this approach has been advocated for rock-
fishes in the northeast Pacific Ocean (Yoklavich, 1998;
Parker et al., 2000). Further, understanding migrations
and other movement patterns of adult rockfishes has
been identified as critical for formulating effective re-
covery plans that may include MPAs for rockfishes in
Puget Sound (Wyllie-Echeverria and Sato, 2005). The
trend toward MPAs, however, is not without controver-
sy— much of it centering on how to choose and config-
ure MPA sites into mosaics that are adequately sized
and placed to achieve prescribed conservation goals.
The related and equally critical issue of how best to
assess the performance of such networks once estab-
lished is also a topic of considerable debate. The size
and placement controversy owes much of its genesis to
attempts at applying theories of island biogeography
to the design of nature reserves (Diamond, 1975) and
continues under what is widely known as the SLOSS
(single large or several small) debate (Simberloff and
Abele, 1982). Fundamental to the debate is the con-
cept of source-sink dynamics (Pulliam, 1988) whereby,
under optimal MPA performance conditions, increased
regulatory protection is expected to result in a net ex-
port of individuals to unprotected habitat or to mar-
ginally suitable habitat within an MPA through larval
advection, density-dependent displacements of later
life history stages (spillover), or both. Many criteria for
MPA design and site selection lack robust scientific jus-
tification and most established temperate-water MPAs
are not subjected to systematic, or even periodic, per-
formance evaluations relative to fishery enhancement,
species recovery, biodiversity preservation, or other
desired outcomes. Although the number of theoretical
MPA performance models is proliferating (Willis et al.,
2003), and presumably improving, these models rarely
incorporate fish movement (but see Attwood and Ben-
nett, 1995; Roberts and Sargant, 2002; Berezansky et
al., 2011). Understanding the frequency, periodicity, and
scale of fish movement will aid modelers and resource
managers in choosing and scaling MPA sites, and in
constructing MPA networks that adequately serve the
ecological needs of species targeted for conservation.
In this study, we seasonally monitored the abun-
dance of 2 demersal rockfish species, brown rockfish
(Sebastes auriculatus) and copper rockfish (S. cauri-
nus) over a 7-year period on an artificial reef in Puget
Sound, Washington. Counts for each of the 2 species
were obtained by using scuba-based underwater visual
censuses (UVCs) conducted over fixed-width strip tran-
sects. Brown and copper rockfish belong to the subge-
nus Pteropodus and occur sympatrically in many re-
gions of the northeast Pacific Ocean, including much of
Puget Sound. They share similar life history attributes,
habitat affinities, behavioral characteristics, and food
preferences (Washington et al.^; Lea et al., 1999; Stout
et al., 2001; Love et al., 2002) and, in Puget Sound
there is evidence of hybridization between the species
(Seeb, 1998; Schwenke, 2012). In Washington State,
they are managed as “bottomfish” and brown rockfish
stock status throughout Puget Sound is classified as
“precautionary,” whereas copper rockfish are classified
as either precautionary (north Puget Sound) or “vul-
nerable” (south Puget Sound), as defined by Palsson et
ah'*
Although tagging studies involving brown or copper
rockfish have occurred throughout much of the range
of these species and have encompassed a variety of in-
vestigative objectives (Miller et al., 1967; Miller and
Geibel, 1973; Dewees and Gotshall, 1974; Hallacher,
1977; Walton^; Laufle®; Gowan, 1983; Mathews and
Barker, 1983; Hueckel et al.^; Matthews, 1985; Mat-
thews et al., 1987; Hartmann, 1987; Matthews, 1990a;
Matthews, 1990b; Lea et al., 1999; Eisenhardt, 2004;
Lowe et al., 2009; Tolimieri et al., 2009; Reynolds et
al., 2010; Longabach, 2010; Starr et al.®; Hannah and
^ Washington, P. M., R. Gowan, and D. H. Ito. 1978. A bio-
logical report on eight species of rockfish (Sebastes spp.) from
Puget Sound, Washington, 50 p. Northwest Alaska Fish.
Cent. Proc. Rep. Northwest Alaska Fish. Cent., Natl. Mar.
Fish. Serv., NOAA, Seattle. [Available at website.]
Palsson, W. A., T.-S. Tsou, G. G. Bargmann, R. M. Buck-
ley, J. E. West, M. L. Mills, Y. W. Cheng, and R. E. Pa-
cunski. 2009. The biology and assessment of rockfishes
in Puget Sound. Wash. Dep. Fish Wildl. FPT-09-04, 208
p. [Available at website.]
® Walton, J. M. 1979. Puget Sound artificial reef study. Wash.
Dep. Fish., Tech. Rep. 50, 130 p.
® Laufle, J. C. 1982. Biological development and materials
comparisons on a Puget Sound artificial reef Wash. Dep.
Fish. Tech. Rep. 72, 183 p.
Hueckel, G. J., R. M. Buckley, and B. L. Benson. 1983. The
biological and fishery development on concrete habitat en-
hancement structures off Gedney Island in Puget Sound,
Washington. Wash. Dept. Fish. Tech. Rep. 78, 67 p.
® Starr, R. M., D. Wendt, K. T. Schmidt, R. Romero, J. Dur-
yea, E. Loury, N. Yochum, R. Nakamura, L. Longabach, E.
304
Fishery Bulletin 114(3)
Figure 1
Location of Point Heyer Artificial Reef in central Puget Sound, Washington,
where 2 rockfish species (brown rockfish [Sebastes auriculatus] and copper
rockfish [S. caurinus]) were monitored over a 7-year period to determine sea-
sonal changes in abundance and to find evidence of seasonal migrations.
Rankin, 2011; Hanan and Curry, 2012; Rankin et.al.,
2013), long-term trends in seasonal abundance have
not been specifically addressed, and drawing informed
conclusions from these studies about potential seasonal
changes in abundance or movement patterns is ham-
pered by the temporal or spatial scales over which they
were conducted, numbers of fish tagged, or insufficient
information (e.g., mark and recapture dates). Collective-
ly, the studies indicate that most adults of both species
maintain high site fidelity, although some exceptions
have been observed; that habitat type (e.g., high-relief,
low-relief, natural, artificial) may influence site fidelity
and movement behavior; and that some level of homing
ability from beyond their putative home range is likely.
Estimates of home range for brown and copper rockfish
vary widely, from <10 m^ over high relief habitat to
4656 m^ over low relief habitat (Matthews 1990b; Tol-
imieri et ah, 2009; Rankin et ah, 2013).
The goal of our study was to determine whether
there were patterned seasonal changes in abundance
on the reef for either species, and if so, whether the
observed patterns differed between species. In order
to gain further insight into our monitoring results, we
examined auxiliary data from a genetic study of brown
Nakada, D. Rasmussen, N. Hall, K. Green, and S. McMil-
lan. 2010. Baseline surveys of nearshore fishes in and near
central California marine protected areas 2007-2009. Final
project report submitted to the Ocean Protection Council,
124 p. California Sea Grant College Program, La Jolla,
CA. [Available at website.]
rockfish that was conducted concurrently at our study
site. These data, along with our findings, are discussed
in the context of providing compelling evidence of rock-
fish migratory behavior. Migrations are well known for
many temperate-water marine fishes (e.g., cods, her-
rings, and sharks) and are often associated with chang-
es in seasonally variable resources, such as food sup-
ply or shelter, or with spawning or mating behaviors
(Harden Jones, 1968; McCleave et al., 1984; McKeown,
1984; Smith, 1985).
Materials and methods
Point Heyer Artificial Reef (PHAR) is a high-relief, in-
sular reef located along the eastern shore of Vashon
Island in the hydrographically defined “main basin”
(Ebbesmeyer et al. 1984) of central Puget Sound (Fig.
1). Puget Sound is a glacially formed saltwater estu-
ary Qord characterized by mixed semidiurnal tides.
It is connected to the Pacific Ocean through one, ap-
proximately east-west running strait (Strait of Juan de
Fuca) that is bounded to the north by Canada’s Van-
couver Island, and by a north-south running inland
waterway between Vancouver Island and the Canadian
mainland. It consists of 5 sub-basins that are sepa-
rated by shallow-water sills. The bathymetry of Puget
Sound extends to depths of nearly 300 m (all depths
reported herein are corrected to mean lower low water
depths).
LeClair et al.: Seasonal changes in abundance and migration of Sebastes auhculatus and 5. cauhnus
305
The reef was constructed in 1983 by the Washington
Department of Fisheries (now the Washington Depart-
ment of Fish and Wildlife) for the purpose of increasing
the number of productive recreational fishing sites in
the region (Buckley 1982). It covers an area of approxi-
mately 5400 m^ and is constructed of various-size quar-
ried boulders and cobble interspersed with long hori-
zontally placed concrete beams. The near- and offshore
margins of the reef lie at a depth of about 4 and 36 m,
respectively. The surrounding seafloor consists primar-
ily of unconsolidated sand, shell hash, and gravel, as
well as widely dispersed small glacially deposited boul-
ders. The reef is situated on a steeply sloping bottom
that descends to depths of nearly 240 m over a distance
of about 3 km to the approximate center of the passage
that separates Vashon Island from the mainland (East
Passage, Fig. 1). Large year-round patches of eelgrass
{Zostera spp.) occur in the shallow water shoreward of
the reef and dense growths of perennial nonfloating
macroalgae (e.g., laminarians, ulvas, palmarials) form
over the shallower portions of the reef during the sum-
mer and fall. Bull kelp {Nereocystis leutkeana), the pre-
dominant canopy-forming floating kelp in Puget Sound,
does not grow on or near the reef. Twenty-two years
had elapsed between the construction of the reef and
the commencement of our study and we presume that
sufficient time had passed for ecological succession to
have occurred.
In 2005, 3 permanent straight-line 60-m transects
(T-1, T-2, and T-3), each running due east-west (as per
standard compass) and separated by a distance of at
least 10 m, were established on the reef. The tran-
sects ran perpendicular to shore and were strategi-
cally placed in order to capture the dominant micro-
and macrohabitat features of the reef (e.g., boulder,
cobble, beams, sandy bottom, high and low relief, reef
margins, crevice and overhang space). The nearshore
ends were positioned in 4.5, 4.0, and 6.0 m and the
offshore ends in 21.5, 21.0, and 20.5 m for T-1, T-2, and
T-3, respectively. The offshore ends of each transect
were semipermanently marked with a buoyed line of
about 1 m in length fastened to a hollow-core cinder
block of approximately 40x20x20 cm affixed to the
seafloor with 2 steel bars. Coordinates (based on the
North American Datum of 1983) for the offshore mark-
ers were as follows: T-1, 47.420040°N, 122.427145°W;
T-2, 47.420082‘>N, 122.427182'>W; T-3, 47.420579°N,
122.426947°W. Real-time coordinate-corrected positions
were obtained by connecting a line between the tran-
sect marker to a surface buoy and registering the posi-
tion with a GeoExplorer 6000 Centimeter Edition® GPS
receiver (Trimble Navigation Ltd., Sunnyvale, CA).
The transects were divided into twelve, 5-m seg-
ments each and were surveyed by scuba divers swim-
ming in tandem along the bottom from deep to shallow
9 Mention of trade names or commercial companies is for iden-
tification purposes only and does not imply endorsement by
the Washington Department of Fish and Wildlife or the Na-
tional Marine Fisheries Service, NOAA.
and pausing briefly at each segment marker. During
surveys, divers counted fish in each segment on their
respective sides of the transect centerline to a width
of 2 m (total bottom coverage per transect=240 m^)
and as high into the water column as visibility per-
mitted. Hand-held lights were used to search beneath
overhangs, in crevices, and in other poorly lit areas. In
order to ensure consistent effort among surveys, the
slowest practical swimming speed was maintained over
each transect as governed by the maximum allowable
safe bottom-time using conventional scuba.
All species of fish that were conspicuous to the div-
ers were recorded and enumerated. Highly cryptic spe-
cies or species that remain very small into adulthood,
though occasionally noted, were not targeted in the
search effort. Careful written and hand-signal com-
munication between divers reduced the risk of count-
ing fish twice when they were swimming across tran-
sect from one survey lane to the other. Individual fish
from the 3 most visually dominant taxonomic families
(Sebastidae, Embitocidae, and Hexagrammidae) were
recorded to species and their length (all fish lengths
herein are reported as total length [TL] in centimeters)
was estimated into length classes, which varied among
species. The occurrence of apparent late-stage gravid
brown and copper rockfish, evidenced by their promi-
nently distended abdomens, was also noted. Cooper
(2003) showed that bulging abdomens can be a reliable
means for identifying late-stage gravid copper rockfish
when they are viewed underwater.
In 2005, surveys were conducted on all 3 transects
during the summer, but only on T-2 in the fall, and no
surveys were conducted during the spring of 2005 or
the winter of 2005-2006. Beginning in the spring of
2006, each transect was surveyed at least once dur-
ing each season through summer of 2012. In most in-
stances, multiple transects were not surveyed on the
same day. The order in which transects were surveyed
during any given season was randomly determined.
No attempt was made to synchronize the surveys to
the cycle of the tides; therefore the surveys occurred
over a broad range of tidal conditions. Strong tidal cur-
rents are not generally encountered over the reef and
current velocities rarely exceed 1.5 knots. The mean
range of the tide at PHAR is approximately 2.4 m.
Temperature data loggers (HOBO® Pro v2, Onset Com-
puter Corporation, Bourne, MA) were deployed at the
near- and offshore margins of the reef (4.5 m and 28
m, respectively) and they recorded water temperature
every 4 hours for a period of one year beginning 8 De-
cember 2006.
In order to mitigate the potential effects of observer
variation, only 5 divers were used throughout the en-
tire course of the study and all surveys on the south
side of the transect center-lines were conducted by the
same diver. Four different divers conducted surveys on
the north side of the transect center-lines; but nearly
all (-96%) of those surveys were conducted by just 2
divers. All scuba divers had extensive experience in
surveying rockfish on Puget Sound rocky reefs prior to
306
Fishery Bulletin 114(3)
Table 1
Number of surveys, by season and tide cycle, conducted over a 7-year period (from
summer 2005 through summer 2012) at Point Heyer Artificial Reef, Puget Sound,
Washington.
Transect
Flood tide
Slack water
before
Ebb tide flood tide
Slack water
before
ebb tide
Total surveys
by transect
Spring
T-1
4
4
1
3
12
T-2
2
5
0
1
8
T-3
3
4
1
0
8
Summer
T-1
0
6
1
0
7
T-2
2
6
0
0
8
T-3
3
7
0
0
10
Fall
T-1
3
3
1
0
7
T-2
7
0
0
1
8
T-3
6
1
0
0
7
Winter
T-1
2
3
0
1
6
T-2
2
4
0
0
6
T-3
1
5
0
0
6
Grand totals
35
48
4
6
93
participating in this study, and they periodically used
hand-held graduated staffs to calibrate their visual es-
timates of fish length.
The genetic data were compiled from a study in
which molecular markers had been used to estimate
genotyping error rates from brown rockfish cap-
tured at PHAR (Hess et al. 2012). In that study, 718
brown rockfish ranging in length from 10 to 37 cm (M
[mean]=22; SD [standard deviation]=7.1) were sampled
and returned alive to their point of capture during all
seasons between spring of 2004 and summer of 2009.
The genetic data were used to identify individuals that
were recaptured in multiple years.
Results
A total of 93 survey dives were conducted between 30
June 2005 and 18 September 2012. All surveys com-
menced between 1.5 and 7 hr after sunrise (M=4 hr,
SD=1.2), and the mean survey time per transect was
28 minutes (SD=7.8). In no case was diver-estimated
visibility less than twice the width of a survey lane.
The numbers of surveys by tide cycle are presented in
Table 1. The total numbers of brown and copper rock-
fish observed by length class summed over all 3 tran-
sects are presented in Figure 2. A list of all species
recorded on transect over the course of the study (a
subjective appraisal of how often the species were ob-
served) and length classes for species from the 3 visu-
ally dominant taxonomic families are presented in the
Supplementary Table [Online].
We fitted a generalized linear mixed model
(GLMM) to the data by maximum likelihood by using
the Laplace approximation and a Poisson link with
the lme4 package, vers. 1.1-8 (Bates et al., 2015) and
statistical software R, vers. 3.1.1 (R Core Team, 2014).
For each of the 2 species, we ran a random effects
only (null) model with count as the response variable,
and year and transect as random effects. We then
added season as the explanatory variable to produce
a full model. We used AN OVA to compare the null and
full models and for both species the results were sig-
nificant (x^=386.64 and 214.09 [3 dfj for brown and
copper rockfish, respectively, P<0.001). The full model
was selected over the null model by both Akaike in-
formation criteria (Akaike, 1974) and Bayesian infor-
mation criteria (Schwarz 1978). The log-likelihood in-
creased, and the deviance, which in linear models is
equal to the residual sum of squares, decreased with
the full model, further indicating that the full model
provided a better fit to the data (Table 2). The GLMM
back-transformed seasonal mean counts with 95% con-
fidence intervals (confidence intervals were computed
before back-transformation) are presented in Figure 3.
We conducted a multiple means comparison of counts
between seasons with Bonferroni corrected alpha
(0.0042 from 0.05) to test the null hypothesis of no
difference in mean counts between seasons. For both
species, spring was not significantly different from
LeCiair et al.: Seasonal changes in abundance and migration of Sebastes auriculatus and 5. caurinus
307
Length class
Figure 2
Total numbers (summed over 3 transects) by length class (total lengths in
centimeters) of brown and copper rockfish (Sebastes auriculatus and S. cari-
nus, respectively) observed during seasonal surveys at Point Heyer Artificial
Reef, Puget Sound, Washington, from summer 2005 through summer 2012.
summer, fall, or winter; summer was significantly dif-
ferent from fall and winter; and fall was significantly
different from winter.
For each species and for any given year, the sum-
mer fish density summed over all length classes was
more than twice that for winter, and the densities did
not vary greatly over time. To evaluate the potential
impact of seasonal juvenile recruitment on overall sea-
sonal abundances, we combined the 2 smallest length
classes (<5 and 5<10 cm) and examined the relative
proportion of these fish to the overall counts, by season,
and summed over all surveys for both brown and cop-
per rockfish. The number of juveniles encountered was
greatest during the summer for both species, as was
the relative proportion of juvenile copper rockfish to
the total number of copper rockfish encountered (14%).
Brown rockfish juveniles, however, represented the
greatest proportion during the winter (9%) (Fig. 4). We
used a two-tailed z-test for comparison of 2 proportions
to determine whether juvenile rockfishes composed a
significantly greater proportion of the total number
of fish observed during either summer or winter. The
proportion of juvenile brown rockfish was significantly
greater in the winter (^=2.2, P<0.05), but the propor-
tions did not differ significantly between summer and
winter for copper rockfish (2=1.6, P>0.05) (satisfactory
n*Pi >5 and /z[l-pj>5 sample-size tests where n=sample
size and p=proportion).
To determine whether there were qualitative differ-
ences between brown and copper rockfish that occupied
the reef in the summer and winter we divided them
into 2 length classes, small (<20 cm) and large (>20
cm). Summed over all surveys, the densities of both
small and large fish were greatest during the summer,
and large fish were more abundant than small fish year
round (Fig. 5). For both species, the proportion of large
fish to the total numbers observed was significantly
greater in the winter (2=2.5 [brown rockfish] and 4.2
Table 2
Summary of analysis of variance (ANOVA) comparisons between generalized linear mixed model (GLMM) null models (fish
count as the response variable, and year and transect as random effects) and full models (season added as explanatory
variable) for seasonal counts of brown and copper rockfish at Point Heyer Artificial Reef, Puget Sound, WA.; AIC=Akaike
information criteria; BIC=Bayesian information criteria; df =degrees of freedom.
Model
df
AIC
BIC
Log-likelihood
Deviance
y} df P (>y})
Brown rockfish Null model
Brown full
3
1032.33
1039.93
-513.17
1026.33
Full model
6
651.69
666.89
-319.85
639.69
386.64
3 <0.001
Copper rockfish Null model
Copper rockfish
3
1003.44
1011.04
-498.72
997.44
Full model
6
795.36
810.55
-391.68
783.36
214.09
3 <0.001
308
Fishery Bulletin 114(3)
35
30
25
20
15 -
10 -
0
35 1
■D
ffl
E
o
'm 30 -
c
CQ
25 -
20 -
o
ro
m 15 .
10
5 ^
0
Brown rockfish
Copper rockfish
spnng
fall
uinler
Figure 3
Backtransformed mean counts (summed over 3 transects and all years)
and 95% confidence intervals for brown and copper rockfish {Sebastes
auriculatus and S. carinus, respectively) observed at Point Heyer Artifi-
cial Reef , Puget Sound, WA, from summer 2005 through summer 2012.
1
]
(95% '
;
!' 97%
90%
Brown rockfish >10
Brown rockfish < 1 0
Copper rockfish >10
Copper rockfish < 1 0
86%
87%
91%
91%
Spring
Summer
Fall
Winter
Figure 4
Counts and percent proportions (summed over 3 transects and all years)
of brown and copper rockfish {Sebastes auriculatus and S. carinus, re-
spectively) <10 and >10 centimeters (total length) observed at Point
Heyer Artificial Reef, Puget Sound, WA, from summer 2005 through
summer 2012.
[copper rockfish], P<0.05; two-tailed z-test for compari-
son of 2 proportions; satisfactory n*Pi>5 and re[l-pi]>5
sample size tests) (Fig. 6).
Summed over all surveys, a total of 70 late-stage
gravid brown and copper rockfish were observed, all
of these in the spring and summer. Of the total num-
ber of brown rockfish >10 cm observed in the spring
(A(=377) and summer (N=998), 9% and 2%, respective-
ly, were noted as late-stage gravid (we assume that no
female rockfish reach maturity at <10
cm [Washington et al.^; Gowan, 1983]).
Late-stage gravid copper rockfish were
only observed during the summer, and
of the total number of copper rockfish
>10 cm observed (493), 3% were noted
as late-stage gravid (Fig. 7). If we as-
sume a population sex ratio of 1:1, the
percentages double with respect to the
total number of potential female spawn-
ers. In order to determine whether there
were differences in time of spawning by
length, we grouped the late-stage grav-
id brown rockfish into 2 length classes
(10<30 and >30 cm) on the basis of 50%
maturity at approximately 30 cm TL
(Love et al., 2002). The proportion of
late-stage gravid brown rockfish >30 cm
to the total numbers of late-stage gravid
fish observed in the spring and summer
was significantly greater in the spring
(2=2.4, P<0.05; 2-test for comparison of
2 proportions; satisfactory n*pi>5 and
re[l-pj]>5 sample-size tests).
Fifty-one (7%) of the 718 brown
rockfish >10 cm sampled by Hess et
al. (2012) were fish that had been re-
captured (2 of these were recaptured
twice) according to genotype matching.
The number of days at liberty between
first and final capture ranged from 1
to 1518 (M=615; SD=448.8). Thirty-one
fish (4%) ranging in length from 17 to
35 cm (M=27; SD=4.1), including the 2
fish that were recaptured twice, were
at liberty for more than one year be-
tween first and final capture. A total of
136 (19%) of the 718 samples were from
late-stage gravid fish and 12 of those
were captured twice in late-stage gravid
condition in different years. The num-
ber of days at liberty between captures
for these fish ranged from 328 to 1469
(M=635; SD=447.2). Overall, the lengths
of the late-stage gravid brown rockfish
sampled ranged from 21-35 cm (M=27;
SD=3.28; includes only the length at
time of first capture for fish that were
captured twice).
Miniumum and maximum recorded
temperatures during 2006-2007 at the
near- and offshore margin of the reef ranged from 7.5°
to 14.6°C and from 8.1° to 13.4°C, respectively. Mean
daily temperature changes were at least twice as great
in the spring and summer as they were in the fall and
winter at both locations, and daily temperature flucua-
tions tended to be slightly greater at the nearshore
margin year-round (Table 3, Fig. 8). The mean monthly
air temperatures during the 12-month water tempera-
ture recording period were all within 2% of the aver-
LeClair et al.: Seasonal changes in abundance and migration of Sebastes auriculatus and 5. caurinus
309
Spring Summer Fall Winter
Figure §
Mean densities and standard errors (summed over 3 transects and all
years) for small (< 20 cm in total length [TL]) and large (> 20 cm TL)
brown and copper rockfish (Sebastes auriculatus and S. carinus, respec-
tively) observed at Point Heyer Artificial Reef , Puget Sound, WA, from
summer 2005 through summer 2012.
age monthly air temperatures summed over a 12-year
period beginning in 2000 and recorded at a weather ob-
servation station located less than 10 km from PHAR.
Our water temperature data were therefore deemed to
be an acceptable proxy for trends in seasonal tempera-
ture at PHAR during the study.
is usually distinguished from emigra-
tion (a form of dispersal), whereby re-
turn to an area does not occur (Lidicker
and Stenseth, 1992), or occurs only by
chance. Adding confusion (or clarity, de-
pending on one’s perspective) to charac-
terizing fish movement is the concept
of home range (Burt 1943). According
to McLoughlin and Ferguson (2000),
home range is established once the cu-
mulative area that is used ceases to in-
crease over time (i.e., an asymptote is
reached). However, and consistent with
Burt (1943), it is generally accepted
that home ranges comprise only those
areas within which routine activities oc-
cur over finer temporal scales, and that
they do not include infrequent spatially
broad-scaled movements, migration cor-
ridors, or the movements of planktonic
life history phases for which the total
area used may not reach an asymptote
over time.
We have shown that both brown and
copper rockfish exhibited pronounced
changes in abundance between summer
and winter at PHAR, that the changes
occurred with regularity over a broad
time span, and that the observed pat-
terns were similar for both species.
Whether the seasonal changes in abundance reflect
migratory behavior hinge on whether the same fishes
return to repopulate the reef during the summer. If,
for instance, fish populations disperse over broad geo-
graphic areas while overwintering in deeper water and
return to shallower water without predilection toward
Discussion
The different sensory inputs that
motivate animals to move and the
variety of spatiotemporal scales
over which movements may occur
has led to some blurring among
specialists over what constitutes
migration (Dingle and Alistair
Drake, 2007). The most broadly ac-
cepted definitions of fish migration
include some element of to-and-fro
movement during the life cycle of a
fish, and some predictability of oc-
currence. Heape (1931) described
migration as, “...that class of move-
ment which impels migrants to
return to the region from which
they have migrated.” Harden Jones
(1984) defines fish migration as
“...a coming and going with the sea-
sons on a regular basis...” Migration
Summer Winter Summer Winter
W=1045 N=563 N=156
Figure 6
Relative proportions of large (>20 cm in total length [TL]) and small (<20
cm TL) brown and copper rockfish (Sebastes auriculatus and S. carinus, re-
spectively) to the total number (N) of fish observed for each species at Point
Heyer Artificial Reef, Puget Sound, WA, during summer and winter from
2005 through 2012. Whiskers denote the 95% confidence intervals for the 2-
test comparisons of the 2 proportions.
310
Fishery Bulletin 114(3)
30 1
25 :
20 -
o
10
s
• Brown rockfish, summer
I Brown rockfish, spring
Copper rockfish, summer
10 <20
20 <30 30 <40
Length Class
>40
Figure 7
Total numbers (summed over 3 transects) of visually apparent late-stage
gravid brown and copper rockfish (Sebastes auriculatus and S. carinus,
respectively) by length class (total lengths in centimeters) observed
during seasonal surveys at Point Heyer Artificial Reef, Puget Sound,
WA, from summer 2005 through summer 2012. Note: Late-stage gravid
copper rockfish were observed only during the summer, and late-stage
gravid brown rockfish were observed only in the spring and summer.
15
14
13
12
6 II
10
9
Nearshore
□
□
1
♦
►
rrp
Offshore
I
□
Spring Summer Fall Winter Spring Summer
Fall
Winter
Figure 8
Temperatures at the near- and offshore reef margin, by season, at Point
Heyer Artificial Reef, Puget Sound, WA, during 2006-2007. Whiskers
indicate the minimum and maximum temperatures recorded, boxes cap-
ture the first and third quartiles, and the mean is denoted by a diamond
shape.
their nearshore point of departure, then the behavior
may be characterized as emigrative (Heape, 1931).
Moreover, if emigrant populations lose their cohesive-
ness once they leave the reef, the seasonal return of
itinerant individuals to the nearshore environment
would result in an annual shuffling of members among
geographically proximate, or possibly even distant,
populations. Whether emigrants wander as groups or
individuals, their return to the nearshore environ-
ment could serve to replenish local populations with
harvest-size Ashes, and may provide a buffer against
localized overfishing provided they ar-
rive from populations that are capable
of sustaining a net export of individu-
als (i.e., source populations sensu stric-
to Pulliam, 1988). Conversely, local
populations made up predominantly of
seasonal migrants may be more vulner-
able to depletion because replenishment
would be less dependent on harvest-
sized immigrants and more dependent
on reproductive success and juvenile re-
cruitment, both of which are known to
be highly variable for rockflshes (Lea-
man and Beamish 1984; Ralston and
Howard 1995; Ralston et ah, 2013). We
note here that the aforesaid statement
lies in contrast to Mathews and Bark-
er’s (1983) view that local populations
of “migratory” rockflshes would be less
vulnerable to depletion; however, their
opinion appears to have been formed
around an implied working definition
of migration that includes any type of
movement beyond a narrowly defined
geographic area, and without regard
to whether the same fish are coming
and going. This contrast in conclusions
serves to underscore the importance of
adequately defining the terms used to
characterize fish movements.
We could not determine whether the
brown rockfish recaptures identified by
Hess et al. (2012) that were at liberty
for more than one year remained on the
reef year-round or left the reef in the
winter and returned during the summer
(i.e., migrated), although only one of the
fish was recaptured in the winter. The
recapture data indicate some degree of
reef fidelity for some brown rockfish at
PHAR. The relatively low abundance of
brown rockfish on the reef during the
winter, the year-round sampling ef-
fort, and the high rate of recapture in
relation to effort lend substantial cre-
dence to the notion of seasonal move-
ments by individuals on and off the reef
over spatial scales that exceed reported
maximum home ranges. Further, the 12
genetically identified brown rockfish that were encoun-
tered as late-stage gravid individuals in multiple years
indicate that more than one spawning by the same fish
occurred at the same location (assuming the fish car-
ried their larvae through to parturition).
Diver effects on fish behavior can be a significant
source of bias when producing estimates of standing
stock or community structure by using noninstanta-
neous UVCs (i.e., strip transects) (see Bozec et al., 2011
and references therein). In this study, we assumed that
bias due to diver effects remained constant over time
LeClair et al.: Seasonal changes in abundance and migration of Sebastes auriculatus and 5. caurinus
311
Table 3
Maximum and mean daily temperature (t) (°C) changes (At) by season recorded at the near- and offshore reef margins of
Point Heyer Artificial Reef, Puget Sound, WA, during 2006-2007. SD=standard deviation.
Spring Summer Fall Winter
24 hr max. Mean daily 24 hr max. Mean daily 24 hr max. Mean daily 24 hr max. Mean daily
Reef margin
At
At (SD)
At
At (SD)
At
At (SD)
At
At (SD)
Nearshore
2.2
0.7 (0.44)
2.1
0.8 (0.44)
1.1
0.3 (0.21)
1.1
0.2 (0.22)
Offshore
1.6
0.4 (0.31)
1.7
0.6 (0.32)
0.6
0.2 (0.14)
0.8
0.2 (0.19)
and thus was not a factor in assessing relative changes
in abundance. Tides were also not judged to be a factor
because the numbers of summer and winter surveys
by tide cycle were not substantially different. Although
rockfish are popular among Puget Sound anglers, rec-
reational harvest was considered an unlikely source of
bias, and commercial rockfish harvest is prohibited in
central Puget Sound. From spring of 2005 through fall
of 2006 the reef was closed to all rockfish retention.
From fall of 2006 through spring of 2010, the rockfish
season and retention rules were highly restrictive in
Puget Sound, and PHAR attracted very few anglers.
The minimal harvest that did occur took place dur-
ing the summer, when rockfish abundance was high-
est. Since May of 2010, recreational rockfish retention
throughout nearly all of Puget Sound, including PHAR
and adjacent waters, has been prohibited. Effects from
potential diel movements were also dismissed as a
source of bias in estimating rockfish densities because
all surveys were conducted approximately halfway be-
tween sunrise and mid-day.
Moulton (1977) observed a winter decrease in copper
rockfish densities over the course of scuba surveys of
nearshore rocky reefs in north Puget Sound. On the ba-
sis of seasonal density differences, over multiple depth
strata, he concluded that over-wintering in deeper wa-
ter beyond the survey range of his study was the most
likely explanation. Richards (1987), observing a simi-
lar trend over rocky habitats, offered an alternative
explanation. She postulated that reduced activity and
more cryptic behavior by copper rockfish during winter
months can lead to lower abundance estimates from
scuba surveys over rocky habitat. This hypothesis is
consistent with Patten’s (1973) observation that copper
rockfish on a small low-relief rocky reef in Puget Sound
were more thigmotactic in the winter and spring. Simi-
lar behavior has been noted for dusky (S. ciliates) and
yellowtail (S. flavidus) rockfish surveyed by scuba div-
ers in southeast Alaska (Carlson and Barr, 1977). In
reference to Richards’ (1987) observation, Matthews
(1990c) noted that winter decreases in brown and
copper rockfish abundance had been observed in the
nearshore environment of Puget Sound over sparsely
vegetated low-relief reefs and sandy-bottom habitat,
where hiding space is limited or nonexistent. The same
author, however, also reported that brown and copper
rockfish were more reclusive on high-relief reefs during
the winter (Matthews, 1990a).
To ensure that our observed winter decreases in
abundance were not due to fish moving into the inter-
stices of the reef and beyond our vision, divers equipped
with digging and prying tools searched for fish by ex-
cavating several off-transect boulder and cobble sites
during the winter months. The excavations occasion-
ally revealed rockfish that could have gone unnoticed
with the use of our standard survey method, but the
encounters were rare and we do not believe that they
occurred with enough frequency to explain the marked
decreases in abundance we observed during the win-
ter. Also, several surveys, with roving divers covering
distances of up to 2.5 km of the nearshore waters ad-
jacent to and on either side of PHAR, were conducted
during the winter in order to ascertain whether winter
decreases in abundance might have been due to fish
moving off the reef but remaining nearby within the
same depth strata. No rockfish were encountered dur-
ing any of these off-reef surveys. It was also possible
that fish may have been crowding the deepest parts of
the reef (beyond our maximum survey depth) during
the winter. We conducted several winter dives along
the deep offshore margin of the reef and found no evi-
dence to indicate that fish remained, though at greater
depths than those surveyed, on or near the reef during
the winter.
For some fish species, seasonal changes in abun-
dance may be attributed to an infiux of juveniles that
leads to higher counts during certain times of the year
(Allen and Horn, 1975; Relini et al., 1994, Allen et al.,
2002, Barreiros et al., 2004). In our study, although the
proportion of juvenile brown rockfish was significantly
greater in the summer, juveniles of both species (length
<10 cm) accounted for a very small proportion of the
overall counts by season. Young-of-the-year fish made
up an even smaller proportion because the <10 cm
length class would have included some fish that were
greater than 1 year in age. We conclude that the sea-
sonal changes in abundance that we observed were not
due to juvenile recruitment. The higher overall num-
ber of copper than brown rockfish juveniles observed
during the spring, summer, and fall is likely due to
312
Fishery Bulletin 1 14(3)
the highly successful recruitment of juvenile copper
rockfish observed in Puget Sound in 2006 (LeClair et
ah, 2007; Palsson et ah, 2012). Although the numbers
of juveniles did not influence the overall pattern of
change in seasonal abundance for either species, juve-
nile recruits during one or more years may have been
plentiful enough to account for the overall statistically
significant greater proportion of small fish (< 20 cm)
observed in the summer. Other potential explanations
for the disproportion include seasonal mortality, preda-
tion, and movement.
Washington et al.^ and Gowan (1983) reported fe-
male first-spawning lengths for both brown and cop-
per rockfish in Puget Sound to be in excess of 20 cm
(age 3-4 years) and our observations at PHAR are
in general agreement, although a single late-stage
gravid brown rockfish less than 20 cm was encoun-
tered in our study and we have observed late-stage
gravid brown rockfish elsewhere in Puget Sound as
small as 18 cm (determined by cannulation). All of the
late-stage gravid brown rockfish sampled by Hess at
al. (2012) were in excess of 20 cm. In our study, the
percentages of late-stage gravid rockfish in relation
to the number of potential female spawners are con-
servative because some fish >10 cm would not have
reached maturity. The higher numbers of late-stage
gravid brown rockfish encountered by Hess et al.
(2012) than the numbers we observed reflect an inten-
tional sampling bias toward gravid rockfish in their
study.
We observed more late-stage gravid brown rockfish
in the spring {N=35) than in the summer (N=22). The
larger length classes comprised a statistically signifi-
cant greater proportion of the spring observations,
and this is consistent with Bobko and Berkeley (2004)
and Love et al. (1990), who found that parturition oc-
curs earlier for older black iS. melanops) and yellow-
tail rockfish. Cooper (2004) also found the same to be
true for copper rockfish in Puget Sound. Because of
sampling bias, we did not examine length-by-season
for the late-stage gravid brown rockfish sampled by
Hess et al. (2012). Nevertheless, the mean length of
the late-stage gravid fish sampled in that study falls
near the center of the length class that accounted for
most of our observations of late-stage gravid brown
rockfish. In Puget Sound, peak parturition is known
to occur earlier in the year for copper rockfish than
for brown rockfish (DeLacy et al.^°; Washington et
al.^). Curiously, we did not observe any late-stage
gravid copper rockfish in the spring at PHAR. Of the
13 late-stage gravid copper rockfish observed, 10 were
encountered during the final 2 years of the study and
only 2 of those were in the largest length class. On
the basis of length-frequency changes over time and a
substantial increase in copper rockfish abundance over
*°DeLacy, A. C., C. R. Hitz, and R. L. Dryfoos. 1964. Mat-
uration, gestation, and birth of rockfish (Sebastodes) from
Washington and adjacent waters. Wash. Dep. Fish. Fish.
Res. Pap. 2:51-67.
the study period after 2006, we surmise that most
of the observed late-stage gravid copper rockfish be-
longed to the strong 2006 year class noted above. If
so, they were just reaching maturity during the final
years of the study and may have been spawning later
in the season, as has been noted for black, yellowtail,
and copper rockfish (see above).
Consistent with many habitat selection models, the
results of Matthews (1990a, 1990b) indicated that the
apparent homing ability of some rockfish species may
enable them to embark on periodic exploratory excur-
sions in response to unfavorable changes in habitat,
allowing them to assess other environments but re-
turn to their point of departure if more suitable sur-
roundings are not encountered. Matthews (1990c) fur-
ther noted that the winter disappearance of canopy-
forming bull kelp, with the structure and associated
prey it provided, may have explained the seasonal
exodus of brown and copper rockfish she observed on
naturally formed low-relief reefs. Although bull kelp
does not occur at PHAR, the seasonal presence of non-
floating seaweeds may provide similar levels of refuge
and prey. The study areas of Matthews (1990c) includ-
ed a high-relief artificial reef (Boeing Creek Artificial
Reef) also located in the main basin of Puget Sound.
The reef is comparable in age, size, depth, and con-
struction to PHAR; is subject to similar wave energy,
current, and temperature regimes; and supports a
similar ichthyofauna and flora that is devoid of cano-
py-forming kelp. However, the highest densities of >20
cm brown and copper rockfish recorded by Matthews
at that site occurred during the fall and winter, not
during the summer as observed in our study.
Resiliency to temperature fluctuations is not known
for copper rockfish. However, Wilson et al. (1974) stud-
ied metabolic compensation in response to temperature
in brown rockfish, and vermilion rockfish {S. miniatus).
This latter species resides below the thermocline and
is therefore not exposed to the same seasonal tempera-
ture fluctuations experienced by brown rockfish resid-
ing above the thermocline. Wilson et al. concluded that
there are metabolic differences between the 2 species
that correlate with differences in depth distribution,
and that brown rockfish have a higher capacity to accli-
mate over a wider range of temperatures. Both brown
and copper rockfish have a similar biological range, oc-
curring from the subtropics to the subarctic (Horn et
al., 2006) and are found in warmer inland seas, as well
as colder oceanic waters (Love et al., 2002). The mean
daily recorded temperature changes at PHAR were
highest during the spring when both species began
appearing on the reef, and during the summer when
they appeared on the reef in their greatest abundance.
Although we do not have temperature data beyond
the offshore perimeter of the reef, water column data
(available at website) in East Passage conducted by the
Washington State Department of Ecology indicate that
diurnal and seasonal temperature regimes become less
labile with increasing depth. If, as noted by Neill and
Gallaway 1989, fish move in response to the totality of
LeClair et al.: Seasonal changes in abundance and migration of Sebastes auriculatus and S. caurinus
313
their environment and not to any single environmen-
tal factor in isolation (e.g., temperature), we consider
it unlikely that either species moved on and off the
reef in direct response to temperature alone, especially
given that they would be leaving the relatively stable
thermal environment of deeper water for the more
broadly fluctuating temperatures encountered over the
reef during the spring and summer.
We hypothesize on the basis of our survey flndings
and the evidence gleaned from Hess et al. (2012) that
the observed changes in abundance of brown and cop-
per rockflsh at PHAR are the result of seasonal reloca-
tions of these species to different migratory destina-
tions beyond their home ranges; most likely in response
to reduced refuge space and prey density (e.g., due to
reduced macroalgal cover and associated prey) during
the winter months. Behaviors associated with spawning
and mating may also play a crucial role in determin-
ing the seasonal movements and spatial distributions
for these 2 rockflsh species. The statistically signiflcant
greater proportion of large brown and copper rockflsh
present on the reef during the winter could be attrib-
uted to an overall suboptimal year-round habitat that
is interspersed with enclaves of microhabitats suitable
for year-round occupancy and that are held more suc-
cessfully by larger territorial fishes.
The applicability of our hypothesis to brown and
copper rockflsh populations elsewhere in Puget Sound
is unclear. If habitat quality is correlated with rockflsh
movement, behavioral variability among local popula-
tions is likely to be high and our observed seasonal
changes in abundance would not be conserved across
sites. If, as proposed by Matthews et al. (1987), there
is a relationship between habitat quality and rockflsh
movement on and off reefs, determining the timing and
magnitude of seasonal variability in rockflsh abundance
at different sites could prove to be a useful means for
ranking the relative importance of those sites for rock-
fish conservation efforts. This research could be critical
for establishing MPAs and for determining the spatial
scales over which protection should be afforded.
Exploitation of aggregating behavior by fisheries,
such as often occurs with cods, forage fish, and other
species, may be detrimental to the recovery of declin-
ing rockflsh stocks if the aggregations are composed
of migrant adults. Fishery managers may wish to con-
sider the potential for, and management implications
of, local rockflsh migratory behavior. Concentrating
fisheries in the nearshore environment during times of
year when migratory rockflsh are present could result
in the depletion of local populations, particularly if ag-
gregations are linked to spawning, courtship, or mating
behavior.
Generalized linear mixed-effects models, parameter-
ized with spatially and temporally explicit habitat, prey
availability, and movement data could aid researchers
in identifying the key habitat attributes and environ-
mental indicators that characterize essential habitat
for these and other fish species.
Acknowledgments
We thank R. Buckley and T. Parra for assisting with
data collection during the transect survey dives. Diver
surface support was provided by P. Campbell, W. Dezan,
R. Heikkila, L. Hiller, J. Hoback, W. Morris, B. Power,
S. Reszczynski, J. Rohr, M. Ulrich, and T. Wilson. We
are grateful to M. Hess for generously providing the
genetic recapture data. Expert assistance with the sta-
tistical analyses and interpretation was provided by K.
Fenske. We thank L. Hillier, D. Lowry, R. Pacunski, and
3 anonymous reviewers for providing helpful comments
on an earlier draft.
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NOAA
National Marine
Fisheries Service
Fishery Bulletin
established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Feeding habits of 2 reef-associated fishes,
red porgy iPagrm pagrus} and gray triggerfish
iBatistes capriscmX off the southeastern
United States
Email address for contact author: sarahfgoldman@gmaii.com
Abstract — -The feeding habits of red
porgy {Pagrus pagrus) and gray trig-
gerfish (Balistes capriscus) were in-
vestigated by examining the gut con-
tents of specimens collected during
2009-2011 from live bottom habitats
off the southeastern United States.
Red porgy had a diverse diet of 188
different taxa. Decapods, barnacles,
and bivalves were their main prey.
Canonical correlation analysis indi-
cated that depth, season, and fish
length were statistically significant
factors determining the degree of
variability in the diet of red porgy.
Gray triggerfish also had a diverse
diet, composed of 131 different prey
taxa. Barnacles, gastropods, and
decapods were their main prey. Of
the 4 explanatory variables, latitude
was highly significant, and season,
depth, and length were statistically
significant. Red porgy and gray trig-
gerfish were observed to have a gen-
eralized feeding strategy of feeding
opportunistically on a wide range of
prey. This study contains fundamen-
tal trophic data on 2 important fish-
ery species in the southeastern Unit-
ed States. Most importantly, it pro-
vides fisheries managers with some
of the data necessary for the imple-
mentation of an ecosystem-based ap-
proach to fisheries management.
Manuscript submitted 23 April 2015.
Manuscript accepted 6 May 2016.
Fish. Bull. 114:317-329 (2016).
Online publication date: 26 May 2016.
doi: 10.7755/FB.114.3.5
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Sarah F. Goldman (contact author)
Dawn M. Glasgow
Michelle M. Falk
South Carolina Department of Natural Resources
P.O. Box 12559
Charleston, South Carolina 29422-2559
There have been numerous calls and
mandates to adopt an ecosystem-
based approach to fisheries manage-
ment (Link, 2002; Latour et ah, 2003;
NMFS, 2009). An ecosystem-based
approach to fisheries management
requires extensive knowledge of the
dynamics of the ecosystem in ques-
tion, the trophic ecology of individual
species, and the food web as a whole
(Byron and Link, 2010), as well as
information on environmental and
biological and economic factors. As
fisheries managers move toward an
ecosystem-based approach to man-
agement, the data inputs for ecosys-
tem models, including diet informa-
tion, must be acquired (Link et ah,
2008; NMFS, 2009; SAFMCi). These
models require long-term monitoring
of the food web and information on
species interactions — data that are
lacking for most species in the south-
eastern United States (SAFMC^).
Red porgy {Pagrus pagrus) and
gray triggerfish {Balistes capriscus)
support commercial and recreational
' SAFMC (South Atlantic Fishery Man-
agement Council). 2009. Fishery eco-
system plan of the South Atlantic region.
Volume V: South Atlantic research pro-
grams and data needs, 177 p. SAFMC,
North Charleston, SC. [Available at
website.]
fisheries along the entire southeast-
ern U.S. Atlantic continental shelf,
often referred to as the South Atlan-
tic Bight (SAB) (Bearden and McK-
enzie^; Manooch, 1977; Antoni et ah,
2011), and both species are in the
snapper grouper complex managed
by the South Atlantic Fisheries Man-
agement Council. Much of the fishery-
independent data used by managers
for the snapper grouper complex are
provided by the Marine Resources
Monitoring, Assessment, and Predic-
tion program, which is a coopera-
tive, long-term, fishery-independent
monitoring survey. A recent report
on analysis of data from this survey
program revealed that red porgy and
gray triggerfish were the third and
fifth most commonly caught species
in chevron traps used in this survey,
respectively (MARMAP^).
2 Bearden, C. M., and M. D. McKenzie.
1969. An investigation of the offshore
demersal fish resources of South Caroli-
na. South Carolina Wildl. Resour. Dep.,
Tech. Rep. 2, 19 p. [Available at web-
site.]
3 MARMAP (Marine Resources Moni-
toring, Assessment, and Prediction).
2014. Semi-annual progress report.
[Project report for the period 1 May-31
October 2014. Available from MAR-
MAP, South Carolina Dep. Nat. Resour.,
217 Fort Johnson Rd, (Charleston, SC
29412.]
318
Fishery Bulletin 114(3)
Previous studies regarding the trophic habits of red
porgy and gray triggerfish in the SAB were limited in
scope or are dated and, therefore, may not reflect possi-
ble recent dietary shifts that result from natural or an-
thropogenic disturbances. There has been, for example,
only one published study on the feeding habits of red
porgy in the southeast (Manooch, 1977). Although that
study was very comprehensive and had a large sample
size (72=779), it was completed more than 40 years ago.
Additionally, we found a report from 1984 (SCWMRD"^)
on feeding of red porgy in the SAB in which diet by
size class and calculated diet overlap were examined
in relation with other common reef fishes. Information
on the food habits of gray triggerfish is also limited,
and the few studies that have been undertaken have
focused on their feeding behavior on artificial reefs
(Blitch, 2000; Kauppert, 2002) and on their interactions
with sand dollars (Frazer et ah, 1991; Kurz, 1995).
Ecological dynamics and processes can be influenced
by changing environmental conditions and anthropo-
genic disturbances (Byron and Link, 2010), such as
fishing. It is likely that intense fishing pressure has an
impact on predator-prey relationships, and when these
relationships are altered the food web can become un-
stable (Holling, 1973). Therefore, it is reasonable to
postulate that intense fishing pressure over the last
several decades not only has affected predatory fish
species, such as red porgy and gray triggerfish, directly
but has also altered other ecological interactions. An
additional change in the trophic dynamics of fish spe-
cies of the U.S. southeastern waters has been the ac-
cidental introduction of piscivorous lionfishes {Pterois
spp.) (Whitfield et ah, 2002; Meister et ah, 2005) The
scale of the ecological impact of lionfishes is uncertain
as its range expands, but studies have indicated that
lionfish predation has caused a reduction in prey com-
munities and, therefore, a decrease of prey for native
predators (Albins and Hixon, 2008; Morris and Akins,
2009).
This article provides descriptions of the current
feeding habits of red porgy and gray triggerfish col-
lected from natural, live bottom habitats in the SAB.
This study is the first one on feeding habits of gray
triggerfish on natural reefs off the Carolinas and
Georgia. The primary objectives of this study were 1)
to qualitatively and quantitatively describe the diet
of red porgy and gray triggerfish; 2) to determine
whether prey consumption differs significantly among
seasons, depth zones, and latitudes; 3) to describe on-
togenetic shifts in diet; 4) to determine the feeding
strategy of each species; and 5) to provide data on diet
to managers that use ecosystem-based models for fish-
eries management.
^ SCWMRD (South Carolina Wildlife and Marine Resources
Department). 1984. Final report: South Atlantic OCS
Area Living Marine Resources Study, Phase III, vol. 1, 223
p. Prepared for Minerals Management Service, Washing-
ton, D.C., under contract 14-12-0001-29185. [Available from
Mar. Resour. Library, South Carolina Dep. Nat. Resour., 217
Fort Johnson Rd., Charleston, SC 29412.]
Materials and methods
Collections
Red porgy and gray triggerfish were collected during
seasonal cruises (May-October) from 2009 through
2011 in the SAB (Fig. 1) with hook-and-line fishing.
The hooks were baited with cut squid (lllex sp.) and cut
round scad (Decapterus sp.). Sampling was conducted
during the day and night while the research vessel was
anchored or drifted over hard-bottom reef habitat. Ten
specimens of each species were targeted in each of 16
sampling zones. Each sampling zone consisted of 1 of 2
depth zones (20-50 m or >50 m) and 1 of 8 latitudinal
zones (1° from 27°N through 34°N).
All specimens were weighed to the nearest gram,
and total length (TL) was measured in millimeters. The
digestive tract (gut) was excised from the esophagus
to the anus and individually labeled. Intestines were
included because both species consume prey with some
anatomical features that are particularly resistant to
digestion, and gray triggerfish lack a distinct stomach.
Guts were fixed in 10% formalin for at least 14 days
and then rinsed with freshwater. After rinsing, gut con-
tents were scraped into individual jars containing 70%
ethanol and stored for identification.
Identification of gut contents
Gut contents were sorted by taxa, enumerated, and
weighed (wet weight to the nearest 0.001 g) with a
Sartorius® balance, model BP211D (Sartorius AG, Goet-
tingen, Germany). Prey items were identified to the
lowest possible taxon. Multiple fragments of individual
organisms were counted as single individuals, unless
the number could be estimated by counting structures,
such as eyes, claws. Colonial organisms (i.e., bryozoans
and tunicates) were counted as one individual. Fishes
were identified according to the identification guide
of Carpenter (2002a, 2000b), decapods were identi-
fied by using Williams (1984), bivalves and gastropods
were identified by using Abbott (1968), zooplankters
were identified by using Johnson and Allen (2005) and
Boltovsky (1999), echinoderms were identified by us-
ing Hendler et al. (1995), and isopods were identified
by using Schultz (1969). Voucher specimens from the
Southeastern Regional Taxonomic Laboratory of the
South Carolina Department of Natural Resources were
used to confirm some identifications.
Diet analyses
Description of general diet To quantify feeding habits,
the relative contribution of food items to the total diet
was determined by using 3 traditional indices: percent
frequency of occurrence (%F), percent composition by
number (%N), and percent composition by weight (%W).
® Mention of trade names or commercial companies is for iden-
tification purposes only and does not imply endorsement by
the National Marine Fisheries Service, NOAA.
Goldman et al.: Feeding habits of Pagrus pagrus and Batistes capriscus
319
Figure 1
Map of catch locations off the southeastern United States, where speci-
mens of red porgy {Pagrus pagrus) and gray triggerfish {Batistes ca-
priscus) were collected for analysis of gut content in 2009-2011. Gray
lines represent bathymetry (in meters).
Ontogenetic, temporal, and spatial changes in diet Prey
were pooled on the basis of taxonomy (e.g., decapods
and gastropods). Percent composition by weight was
calculated for guts grouped by intervals of TL, season,
depth (in meters), and latitude, and this metric was
used for all analyses. For analytic purposes, prey types
that contributed less than 1% by weight to the diet
were excluded.
Canonical correspondence analysis (CCA; ter Braak,
1986), a multivariate direct gradient analysis tech-
nique, was used to determine the degree of variability
in the diets of red porgy and gray triggerfish, explained
by the canonical axes. The canonical axes are linear
combinations of the 4 explanatory variables correlated
to weighted averages of the prey within the cells of
the response matrix (ter Braak, 1986; Garrison and
Link, 2000). The CCA was performed with the com-
munity ecology package vegan, vers. 2.0-10
(Oksanen et al., 2013), an extension to the
statistical software R, vers. 3.1.2 (R Core
Team, 2014).
Each element in the response matrix
was the mean percent weight of each prey
taxon in a given length category, season,
depth, and latitude combination. Prey data
(%W) were log-transformed (ln[x-(-l]) to
normalize the data. The explanatory vari-
ables were coded as ordinal variables with
the exception of season, which was coded
as a categorical variable. The variance
inflation factor was used to detect nearly
collinear constraints (environmental vari-
ables), although it must be noted that these
constraints are not a problem with the al-
gorithm that is used in the CCA function
of the vegan package to fit a constrained
ordination (Oksanen et al., 2013). Any use-
less constraints would have been removed
from the estimation, and no biplot scores or
centroids would have been calculated (Ok-
sanen et al., 2013). Permutation tests were
used to determine the significant explana-
tory variables (ter Braak, 1986). A biplot of
prey species and explanatory factors was
constructed to examine the correlations be-
tween the explanatory variables (factors)
and the canonical axes and to observe any
dietary patterns associated with these fac-
tors. A descriptive analysis was generated
for each of the significant factors identified
by the CCA.
Hydrographic conditions were used to
derive seasonal categories: spring: April
through June; summer: July through Sep-
tember, and autumn: October through
December. Latitudes were grouped into
3 categories: southern (27-29°N), middle
(31-32°N), and northern (33-34°N). To
examine the effect of fish length on the
diets of red porgy and gray triggerfish,
specimens were grouped into 50-mm-TL categories so
that all members of a category displayed a reasonably
consistent diet composition, and %W was calculated
for each group. Groups with low sample sizes (fz<3)
were trimmed to minimize outliers. Cluster analyses
(Euclidean distance, average linkage method) were
used to group these length classes into broader cat-
egories that represented relationships among the diet
compositions.
Feeding strategies The feeding strategies of each spe-
cies were analyzed according to the graphical method
of Costello (1990), modified by Amundsen et al. (1996).
Through the use of this method, prey-specific abun-
dance was plotted against %F, making it possible to
explore feeding strategies as well as shifts in niche use.
Prey-specific abundance was defined as
320
Fishery Bulletin 114(3)
Percent composition or frequency
Figure 2
Percent frequency of occurrence (%F), percent composition by
number (%N), and percent composition by weight (%W) of prey
types present in the diet of 140 red porgy {Pagrus pagrus) cap-
tured in the South Atlantic Bight from 2009 through 2011. Prey
items consumed by fewer than 5% of predators are not included.
Miscellaneous=fish scales, foraminifera, eggs, macroalgae, and
sediment.
Pi = (XSi/5:St)*ioo, (1)
where Sj = the sum of prey i; and
St = the sum of all prey items found in only
those predator guts that contained prey i. Percent com-
position by weight was the summed variable. On the
graph that results from this method (Amundsen et ah,
1996, fig. 3), the percent abundance, which increases
along the diagonal from the lower left to the upper
right corner, provides a measure of prey importance,
with dominant prey on the top and rare or unimport-
ant prey on the bottom. The vertical axis represents
feeding strategy: specialization versus generalization.
Prey points on the upper part of the graph represent
prey on which predators have specialized, and prey
positioned on the bottom half of the graph have been
eaten occasionally or infrequently.
Results
Unidentified prey items were often encountered be-
cause both species bite or grind their food instead of
consuming it whole. Fortunately, the majority of prey
have parts that are resistant to digestion, making
them easily identifiable on the basis of characteristic
parts. For example, crab claws and legs, pieces of echi-
noderm test and spines, and pieces of barnacles were
often seen in stomach contents. A full listing
of prey items for both species is available in
Suppl. Tables 1 and 2 [Online].
Red porgy
From 2009 through 2011, gut contents from
140 red porgy were collected. Lengths of red
porgy ranged from 274 to 508 mm TL. Sample
sizes were low at the extremes of our sampling
range (i.e., 34°N and 27°N).
General diet description Red porgy had a di-
verse diet, composed of 188 different taxa
that belong to 18 taxonomic groupings: deca-
pods, bivalves, polychaetes, gastropods, bryo-
zoans, unidentified crustaceans, echinoderms,
bony fishes, barnacles, miscellaneous (e.g., fish
scales and foraminifera), tunicates, amphipods,
squid, cnidarians, stomatopods, isopods, ostra-
cods, and protochordates. Decapods, barnacles,
and bivalves were the main prey of red porgy,
accounting for 44%, 20%, and 11% of the diet
by weight, respectively (Fig. 2). The most fre-
quently consumed decapods were parthenopid
crabs (29%), portunid crabs (28%), calappid
crabs (28%), and shrimps (28%). The most fre-
quently consumed bivalve was the painted egg-
cockle {Laevicardium pictum) (7%). Although
polychaetes were consumed by 50% of red por-
gy, this taxon accounted for only 6% by weight
and 8% by number. Other groups that were
frequently consumed included gastropods (46%), bryo-
zoans (45%), echinoderms (33%), and bony fishes (32%);
however, these species contributed little by weight.
Ontogenetic, temporal and spatial changes in diet We
determined that 6% of the total variability in the diet
data was explained by the CCA. The first and second
canonical axes accounted for 51% and 22%, respective-
ly, of the constrained variation. Of the 4 environmental
variables, depth and season were the most important
(P<0.001), followed by length (P<0.05) (Fig. 3).
Although decapods were consumed in all seasons,
fewer were consumed in the summer (29%) when bar-
nacles were the primary food source (43%) (Fig. 4A). In
the spring, red porgy consumed mostly decapods (50%)
and bivalves (11%). In the autumn, decapods (53%) and
polychaetes (20%) were the primary prey types.
Red porgy captured on the inner shelf (depths: 20.1-
50.0 m) consumed a higher percentage of barnacles and
bivalves than did their counterparts on the outer shelf,
but decapods dominated diets of red porgy regardless
of depth. Outer shelf red porgy also consumed bony
fishes and polychaetes (Fig. 4B).
Decapods were the dominant prey at all latitudes,
but fewer of them were consumed in the middle lati-
tudes (31-32°N) (Fig. 4C). Red porgy captured at the
middle latitudes (31-32°N) consumed barnacles (27%)
and bivalves (11%) in addition to decapods. Barnacles
Goldman et al.; Feeding habits of Pagrus pagrus and Batistes capriscus
321
CCA1
Figure 3
Biplot determined with canonical correspondence analysis (CCA) for the diet
of red porgy (Pagrus pagrus) captured in the South Atlantic Bight from 2009
through 2011. Arrows represent significant explanatory factors, and dots rep-
resent prey types. The canonical axes represent linear combinations of the 4
explanatory variables (i.e., fish length, latitude of capture, season, and depth).
made up less than 1% of prey consumed at the north-
ern latitudes (33-34°N).
The quantity of decapods in the diet of red porgy
increased with increasing length (Fig. 4D), whereas
smaller fish (<420 mm TL) consumed more barnacles
and bivalves than their larger counterparts.
Feeding strategy According to the Amundsen graphical
method, the feeding strategy of the red porgy popula-
tion is generalized (points cluster lower on the y-axis
of the graph) (Fig. 5), and therefore most prey types
are eaten on occasion. Xanthid crabs were consumed
by individual red porgy that were concentrating on this
prey type as indicated by the point on the top left of
the graph. The predator population had a broad niche
width because most of the points are located along or
below the diagonal from the upper left to the bottom
right of the graph. A few prey items were eaten oc-
casionally by most individuals, and these items are
represented by the points on the bottom right of the
graph (Fig. 5).
Gray triggerfish
Description of general diet Gut contents were collected
from 82 gray triggerfish that ranged in size from 304
to 595 mm TL. Gray triggerfish had a diverse diet, com-
posed of 131 different prey taxa that were combined
into 19 broader taxonomic groups: gastropods, amphi-
pods, decapods, unidentified crustaceans, polychaetes,
bivalves, bryozoans, barnacles, bony fishes, echinoderms,
tunicates, miscellaneous items (e.g., fish scales, fora-
minifera, and Sargassum spp.), stomatopods, isopods,
cnidarians, ostracods, cephalopods, copepods, and un-
identified mollusks. Barnacles, gastropods, and decapods
were the main prey of gray triggerfish, accounting for
29%, 11%, and 11% of the diet by weight, respectively
(Fig. 6). Although most gastropods were unidentified,
13 species were pelagic pteropods (group Thecosomata);
cavolinid pteropods (40%) were the most frequently con-
sumed pelagic pteropods. Unidentified shrimps were the
most frequently consumed decapod (30%). Although am-
phipods were consumed by 63% of predators, this taxon
accounted for only 0.5% of the diet by weight and 10%
by number. Other species consumed frequently included
unidentified crustaceans (59%), polychaetes (46%), bi-
valves (46%), and bryozoans (43%); however, these spe-
cies contributed little by weight.
Ontogenetic, temporal, and spatial changes in diet We
determined that 15% of the total variability in the
diet data could be explained by the CCA. The first and
second canonical axes accounted for 41% and 36% of
the constrained variation, respectively. Latitude and
season were the most important explanatory variables
(P<0.001), followed by depth and length (P<0.05) (Fig. 7).
322
Fishery Bulletin 114(3)
Crustaceans, unid.
Cnidarians
Bryozoans
Gastropods
Squid
Barnacles
Tunicates
Protochordates
Bony fishes
Polychaetes
Echinoderms
Bivalves
Decapods
Autumn
W=14
■ Summer
A/=39
■ Spring
N=86
10
20
30
40
50
Percent weight
Percent weight
60
Tunicates
Squid
Polychaetes
Q.
g Gastropods
^ Echinoderms
Decapods
Crustaceans, unid.
Bony fishes
Bivalves
Barnacles
D
■ Cluster 2 (large)
N=39
■ Cluster 1 (small)
A/=99
10
20
30
40
50
60
70
Percent weight
Figure 4
Diet composition by weight of red porgy (Pagrus pagrus) collected in the South Atlantic Bight from 2009 through 2011
presented by (A) season, (B) depth, (C) latitude, and (D) length. The number (AO of specimens collected in each season, at
each depth zone, latitude range, or within each length cluster (small=321-420 mm in total length; large=421-520 mm TL)
is given in the legends, unid^unidentified.
100
c
re
n
0 0.2 0.4 0.6 0.8
Frequency of occurrence (%)
Figure 5
Graph of the feeding strategy of red porgy {Pagrus
pagrus), captured during 2009-2011 in the South At-
lantic Bight. The graph was developed in this study by
using the Amundsen graphical method. Each dot repre-
sents a different prey species.
Barnacles (35%) and decapods (17%) were the pri-
mary prey for gray triggerfish captured in the spring
(Fig. 8A). In the summer, the principal prey of gray
triggerfish were barnacles (24%) and bivalves (23%),
and, in the autumn, gray triggerfish consumed primar-
ily gastropods (40%) and bony fishes (32%).
Gray triggerfish caught on the inner shelf consumed
more barnacles, decapods, and polychaetes than did
their outershelf counterparts, whereas, on the outer-
shelf, they consumed more gastropods and bivalves
(Fig. 8B).
Latitudinal differences in diet were substantial (Fig.
8C). Fish captured at the southern latitudes (27-29°N)
preyed upon decapods (59%), and fish captured at the
northern latitudes (33-34°N) consumed mostly barna-
cles (57%). Gray triggerfish caught in the central re-
gion (31-32°N) had a more diverse diet consisting of
decapods, gastropods, barnacles, and bony fishes.
Small fish (<400 mm TL) consumed decapods and
Goldman et al.: Feeding habits of Pagrus pagrus and Batistes capriscus
323
Cnidarians
Isopods
Stomatopods
Miscellaneous
Tunicates
Echinoderms
% Bony fishes
o
o) Barnacles
>>
2^ Bryozoans
Q.
Bivalves
Polychaetes
Crustaceans, undet.
Decapods
Amphipods
Gastropods
BSS2SES
EHS2SSS
Co
issss
I
%w
%N
%F
0 20 40 60 80
Percent composition or frequency
Figure 6
Percent frequency of occurrence (%F), percent composition by number
(%N), and percent composition by weight (%W) of prey types present
in the diet of 82 gray triggerfish (Balistes capriscus) captured in the
South Atlantic Bight from 2009 through 2011. Prey items consumed
by fewer than 5% of predators are not included.
relatively few bivalves. In contrast, large fish had a
diet dominated by barnacles and bivalves. (Fig. 8D).
Feeding strategy On the basis of Amundsen graphi-
cal method, the feeding strategy of the gray trigger-
fish population is generalized (cluster of points lower
on the y-axis of the graph) (Fig. 9); several prey items
are eaten occasionally by most individuals. As with red
porgy, the predator population has a broad niche width
(points are all located below the diagonal from the up-
per left to the bottom right of the graph) (Fig. 9).
Discussion
Red porgy
Across the broad sampling range of this study, red por-
gy had a very diverse diet. Much of this diversity is
likely a reflection of localized prey assemblages rather
than a preference for specific prey items (Bearden and
Mckenzie^; Manooch, 1977). Manooch (1977) and SC-
WMED"* reported findings similar to those of our study
in that they found the red porgy to be a generalized
predator. However, Manooch (1977) and SCWMRD^
identified only 69 and 80 prey taxa, respectively, com-
pared with the 188 taxa found in our study. In the case
of the Manooch (1977) study, the difference in number
of prey taxa may be attributed to the limited geograph-
ic range of his investigation; samples in that study
came from only North and South Carolina, whereas
samples from our study came from an area spanning
from North Carolina to Florida.
It is also possible that the abundance of certain
prey has shifted and, therefore, that red porgy have
had to diversify their food resources. SCWMRD'* found
the preferred prey were decapods and fishes and that
fishes made up the greatest volume of prey. We found
fishes to be far less important prey (6%W). In contrast
to Manooch (1977) and our study, SCWMRD^ identified
more nektonic and fewer benthic prey. In addition, SC-
WMRD® found very few mollusks in comparison with
our study. The scientists at SCWMRD suggested that,
because Manooch (1977) used stomach and intestine of
red porgy and shelled organisms are slow to be digest-
ed, bivalves and gastropods would appear to be present
more frequently than taxa such as small crustaceans
and polychaetes. This suggestion could be one explana-
® SCWMRD (South Carolina Wildlife and Marine Resources
Department). 1981. South Atlantic OCS Area Living Ma-
rine Resources Study, vol. 1, 297 p. Prepared for Bureau of
Land Management, Washington, D.C, under contract AA551-
CT9-27. [Available from Mar. Resour. Library, South Caro-
lina Dep. Nat. Resour., 217 Fort Johnson Rd., (Charleston, SC
29412.]
324
Fishery Bulletin 114(3)
Figure 7
Biplot determined with canonical correspondence analysis (CCA) for
the diet of gray triggerfish (Balistes capriscus) captured in the South
Atlantic Bight from 2009 through 2011. Arrows represent significant
explanatory factors, and dots represent different prey types. The ca-
nonical axes represent linear combinations of the 4 explanatory vari-
ables (i.e., fish length, latitude of capture, season, and depth [shown
in bold type]).
tion for the frequently observed bivalves and gastro-
pods in the diet of red porgy in our study.
Season was the second most significant explanatory
factor in the CCA in our study, but Manooch (1977)
found only slight seasonal variation in several groups
of invertebrates. In our study, barnacles were the main
food source in the summer, whereas, in the autumn and
spring, red porgy depended more heavily on decapod
prey. This seasonal shift in diet could have been the
result of lower decapod availability during the summer
and that in turn would have led to red porgy consum-
ing more barnacles. In fact, Manooch (1977) found that
several groups of invertebrates varied seasonally both
in volume and frequency. Red porgy are not dependent
on one type of food source; therefore this species has
the advantage of being able to switch prey as necessary
with fluctuating seasonal prey populations.
There were significant differences in prey among
length classes. Small fish (<420 mm TL) generally con-
sumed small prey (barnacles and bivalves), and large
fish consumed larger prey (decapods). The SCWMED"^
study found that red porgy consumed more fishes and
fewer decapods as they grew — a finding that also con-
trasts with our results. However, that study included
smaller fish (51-350 mm in standard length) than
those collected in our study (274-508 mm TL), and that
size difference is likely to be the main reason for the
reported differences in prey types by fish length.
A generalized feeding strategy (Fig. 5) is not unex-
pected for a species that consumes such a great diver-
sity of prey items. Manooch (1977) suggested that the
tremendously diverse diet of red porgy probably re-
flects localized forage assemblages rather than a pref-
erence for a specific food and supports the idea of clas-
sifying red porgy as trophic generalists. He also noted
that they have certain behavioral and morphological
characteristics that make it easy to feed on a diversity
of prey: swimming speed and strong molariform teeth
that enable these fish to crush armored prey, such as
sea urchins, crabs, and gastropods. This feeding strat-
egy has a selective advantage because red porgy are
not dependent on a small number of food types, and,
therefore, are less likely to face competition.
Gray triggerfish
Gray triggerfish were found to have a very diverse diet
of 131 prey taxa across a broad sampling range. Unlike
the prey that we found, previous researchers found the
most important prey of gray triggerfish to be bivalves,
barnacles, and echinoderms (Vose, 1990; Vose and Nel-
son, 1994; Kauppert, 2002). However, fish living around
Goldman et al.: Feeding habits of Pagrus pagrus and Balistes capriscus
325
Cnidarians
A
Autumn
Stomatopods
F
W=18
Bryozoans
r
■ Summer
Amphipods
■
A/=14
Q.
D
Bivalves
tJ
■ Spring
o
Tunicates
N=48
D)
Poiychaetes
0
Echinoderms
qI
Bony fishes
(jastropods i
Crustaceans, undet.
mm .
Decapods
Barnacles
0 10 20 30 40
Percent weight
Q.
D
O
Tunicates
Polychaetes
Bony fishes
Crustacean, undet.
Gastropods
Bivalves
Echinoderms
Decapods
Barnacles
f- B
frz,
■ Outer shelf
N=33
m Inner shelf
N=49
0 10 20 30 40
Percent weight
Echinoderms
Cnidarians
Bony fishes
a.
3
Bivalves
g
D)
Polychaetes
>.
Barnacles
0
iX
Amphipods
Tunicates
Gastropods
Crustaceans, undet.
Decapods
20 40
Percent weight
33-34°
/V=15
1 31-32°
N=67
, 27-29°
N=16
60
Tunicates
CL
Q Polychaetes
O’ Gastropods
>-
o Echinoderms
Q.
Decapods
Crustaceans, undet
Bony fishes
Bivalves
Barnacles
Figures 8
Diet composition by weight of gray triggerfish (Balistes capriscus) collected in the South Atlantic Bight from 2009
through 2011 presented by (A) season, (B) depth, (C) latitude, and (D) length. The number (N) of specimens in each
season, depth group, latitude range, or length cluster (small=350-400 mm in total length; large=401-600 mm TL) is
given in the legends.
artificial structures (as opposed to the natural reefs ex-
amined in our study) were examined in those previous
studies, and other research focused on gray triggerfish
interaction with sand dollars (Frazer et ah, 1991; Kurz,
1995). Vose (1990) wrote that gray triggerfish are high-
ly dependent on reef-associated prey and found diets of
gray triggerfish to be quite different for natural and ar-
tificial reefs. On natural reefs, bivalves were a common
food, whereas artificial reefs that were examined were
dominated by fouling organisms such as barnacles. Of
the previously published work, only one study on gray
triggerfish collected from artificial reefs in the Gulf
of Mexico had findings similar to those in our study:
Blitch (2000) found pelagic mollusks and crustaceans
to be the most important prey.
In our study, echinoderms were found in 28% of guts,
but this finding may be an underrepresentation of their
importance in the diet of gray triggerfish because the
soft tissue of echinoderms may have been digested be-
fore a gray triggerfish was caught. Frazer et al. (1991)
cautions that because gray triggerfish eat only soft tis-
sue and not the hard test, echinoderms may be under-
represented in studies of stomach contents because of
different digestion rates. We were able to identify sand
dollars in guts only when gray triggerfish had eaten an
entire organism with its test.
The diet of gray triggerfish was dominated by gas-
tropods (primarily pelagic pteropods) in the autumn,
a result that confirms Kauppert’s (2002) observations
that feeding habits of gray triggerfish in the autumn
shifted to 60% nektonic and planktonic feeding, espe-
cially when compared with substrate feeding in the
spring and summer. Some species of pteropods are re-
ported to reproduce in the spring and summer (Ram-
pal, 1975; Dadon and de Cidre, 1992) and could re-
sult in increases in pteropod numbers in the autumn
months and consequently the seasonal shift in preda-
tion. Furthermore, seasonal migrations occur in some
species of pteropods (Sardou et ah, 1996). Results
from Sardou et al. (1996) and Franqueville (1971)
indicate that the pyramid clio (Clio pyramidata), a
pteropod species commonly consumed by gray trig-
gerfish in our study, becomes abundant at shallower
depths in autumn. This occurrence offers a plausible
explanation for the increased pteropod predation in
the autumn.
326
Fishery Bulletin 114(3)
Frequency of occurrence (%)
Figure 9
Graph of the feeding strategy for gray triggerfish {Bati-
stes capriscus), captured from 2009 through 2011 in the
South Atlantic Bight. The graph was developed by us-
ing the Amundsen graphical method. Each dot repre-
sents a different prey species.
Another reason for seasonal variation in diet could
be the reproductive behavior of gray triggerfish. They
spawn from April through September and peak spawn-
ing occurs from May through August (Kelly, 2014). Dur-
ing this time, they are found at deeper depths, and it
is possible that their feeding behavior could change be-
cause they are nest guarders. Gray triggerfish caught
on the outer shelf consumed more gastropods (primar-
ily pteropods) than the gray triggerfish captured on
the inner shelf Pteropod distribution patterns remain
poorly described (Bednarsek et ah, 2012), but it has
been reported that their distribution and migration
vary seasonally (Dadon and de Cidre, 1992; Parra-
Flores and Gasca, 2009).
Latitude was a highly significant explanatory factor
in defining the diet for gray triggerfish, and there were
changes in diet with fish length that might also have
influenced our results. Small fish consumed more poly-
chaetes and decapods, and large fish consumed more
barnacles and bivalves (the opposite was true with
red porgy). Decapod prey consumed by gray triggerfish
were often smaller crab species or crustaceans in lar-
val stages (i.e., crabs, shrimps, and lobsters). Gastropod
consumption increased with predator size.
The percentages of explained variation found in this
study are comparable to those in similar studies of diet
composition (Jaworski and Ragnarsson, 2006; Latour et
ah, 2008). Although a relatively small proportion of the
total variation is explained by the CCA, a small propor-
tion is expected because the percentage-explained iner-
tia (variance) for ecological data is typically low (<10%)
(ter Braak and Verdonschot, 1995).
Some prey of gray triggerfish and red porgy have
diel vertical migrations (at least 32 taxa) (Boltovskoy,
1973; Alldredge and King, 1980; Hopkins et ah, 1994;
Angel and Pugh, 2000). Pteropods, for example, exhibit
diurnal vertical migrations along the depth range of
0-100 m. During the day, pteropods move to deeper
waters but migrate to the surface at night (Angel and
Pugh, 2000). They tend to concentrate in the upper lay-
ers during the night to feed and avoid predators (Hays,
2003). Gray triggerfish are rarely caught at night dur-
ing cruises of the Marine Resources Monitoring, As-
sessment, and Prediction program (senior author, per-
sonal observ.), and they have been previously described
as diurnal predators (Randall, 1968). It is possible that
these fish are not caught on the bottom at night be-
cause this species migrates into the water column, fol-
lowing pelagic prey. Many fish species migrate in a diel
pattern, both vertically (Narver, 1970; Blaxter, 1973;
Begg, 1976) and horizontally (Baumann and Kitchell,
1974; Hobson, 1974; Bohl, 1979; Krumme, 2009), fol-
lowing prey migrations (Ahlbeck et ah, 2012). Although
gray triggerfish are highly reef associated, they also
rely on migrating pelagic species as food sources. Other
studies of reef fishes have reported trophic connections
that are primarily dependent on these vertically mi-
grating food webs (Weaver and Sedberry, 2001; Gold-
man and Sedberry, 2010).
Although competition between species was not a
focus of our research, other studies have had results
worth discussing in the context of our work. Johnson
(1977) suggested that when %F exceeds 25% between
2 or more predators, competition is likely. In contrast,
Pianka (1976) stated that competition for identical re-
sources is only likely if resources are in short supply.
Red porgy and gray triggerfish do share many of the
same prey (e.g., decapods, gastropods, bivalves, bryozo-
ans, echinoderms, polychaetes, and bony fishes), and, if
food resources become scarce, then such scarcity could
lead to competition. Possible causes for a short supply
could be prey consumption by invasive lionfishes, ocean
acidification, or other anthropogenic effects (e.g., fish-
ing). In this study, we did not examine food availability,
nor did we observe anything that indicated evidence of
food scarcity.
Ocean acidification is of particular concern for gray
triggerfish because a large part of its diet is composed
of pelagic pteropods. Ocean acidification causes shell
dissolution in pteropods and some benthic inverte-
brates that are CaCOs-secreting organisms (Doney et
ah, 2009). Calcified structures provide protection from
predators; therefore, pteropods would be adversely af-
fected by the rising atmospheric CO2 levels caused by
human fossil fuel combustion and deforestation (Doney
et ah, 2009), and adverse effects on pteropods would, in
turn, have serious effects on populations of gray trig-
gerfish. This study is far more comprehensive than pre-
vious studies have been and covers a large geographic
area, providing a baseline study that can be used to
monitor potential dietary shifts that result from cli-
mate change.
The temporal and geographic differences in prey for
red porgy and gray triggerfish highlight the need to
incorporate information on fish food habits into ecosys-
tem models. Many of the prey species consumed by fish
Goldman et al.: Feeding habits of Pagrus pagrus and Balistes capriscus
327
in our study are not well studied in the southeast, and
their population statuses are not well known. Changes
in their status could have unanticipated consequences
for commercial fish species like red porgy and gray
triggerfish. The most significant predator-prey inter-
actions are those between red porgy and decapods and
bivalves and those between gray triggerfish and gas-
tropods. The information reported here complements
the findings of previous studies and provides a critical
link between the biology of red porgy and gray trigger-
fish and their role as predators in marine ecosystems.
Although both species rely primarily on hard-bottom
habitats for feeding, opportunistic prey switching al-
lows both red porgy and gray triggerfish to adapt to
ecological changes. This research and that of similar
studies contribute to our understanding of the role of
predators in changing ecosystems and provide fisheries
managers with some of the data necessary for the im-
plementation of an ecosystem-based approach to fish-
eries management in the southeastern United States.
Acknowledgments
For their help with identification of prey items, we
thank D. Burgess, J. Cowan, D. Knott, C. Willis, and D.
Wyanski. Thanks are extended to the staffs of the Ma-
rine Resources Monitoring Assessment and Prediction
program and of the Southeast Fishery-independent
Survey, NOAA Southeast Fisheries Science Center, and
to the crews of the RV Palmetto and RV Savannah.
G. Sedberry, W. Anderson, C. Barans, K. Spanik, and
W. Bubley provided helpful comments on early drafts
at the manuscript stage. This work was supported
through funds provided by the Southeast Area Moni-
toring and Assessment Program — South Atlantic. This
paper is contribution number 734 from the South Caro-
lina Marine Resources Division.
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330
NOAA
Spencer F. Baird
National Marine
Fisheries Service
Fishery Bulletin
fy’ established 1881 •.
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
&
Predicting potential fishing zones for Pacific
saury iCoiolabis saira} with maicinium entropy
models and remotely sensed data
Email address for contact author: fachrudinsyah@gmail.com
' Laboratory of Marine Environment and Resource Sensing
Faculty of Fisheries Sciences
Hokkaido University
3-1-1 Minato-cho
Hakodate 041-8611, Japan
^ Department of Marine Science
University of Trunojoyo Madura
Jalan Raya Telang
P.O. Box 2 Kamal
Bangkalan-Madura, Indonesia
3 Arctic Research Center
Hokkaido University
N21-W11 Kita-ku
Sapporo 001-002, Japan
Abstract — Fishing locations for Pa-
cific saury (Cololabis saira) obtained
from images of the Operational
Linescan System (OLS) of the U.S.
Defense Meteorological Satellite
Program, together with maximum
entropy models and satellite-based
oceanographic data of chlorophyll-
a concentration (chl-a), sea-surface
temperature (SST), eddy kinetic en-
ergy (EKE), and sea-surface height
anomaly (SSHA), were used to evalu-
ate the effects of oceanographic con-
ditions on the formation of potential
fishing zones (PFZ) for Pacific saury
and to explore the spatial variabil-
ity of these features in the western
North Pacific. Actual fishing regions
were identified as the bright areas
created by a 2-level slicing method
for OLS images collected August-De-
cember during 2005-2013. The re-
sults from a Maxent model revealed
its potential for predicting the spa-
tial distribution of Pacific saury and
highlight the use of multispectral
satellite images for describing PFZs.
In all monthly models, the spatial
PFZ patterns were explained pre-
dominantly by SST (14-16°C) and
indicated that SST is the most influ-
ential factor in the geographic distri-
bution of Pacific saury. Also related
to PFZ formation were EKE and
SSHA, possibly through their effects
on the feeding grounds conditions.
Concentration of chl-a had the least
effect among other environmental
factors in defining PFZs, especially
during the end of the fishing season.
Manuscript submitted 20 July 2015.
Manuscript accepted 12 May 2016.
Fish. Bull.:330-342 (2016).
Online publication date: 2 June 2016.
doi: 10.7755/FB.114.3.6
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Achmad F. Syah (contact author)
Sei-lchi Saitoh’'^
Irene O. Alabia^
Toru Hirawake'
The Pacific saury {Cololabis saira)
is widely distributed in the west-
ern North Pacific from subarctic to
subtropical waters and is one of the
commercially important pelagic spe-
cies in Japan, Russia, Korea, and
Taiwan. The total landings of this
species in these countries increased
from 171,692 metric tons (t) in 1998
to 449,738 t in 2011. Over the last
half century, annual catches of Pacif-
ic saury in Japan, for example, have
averaged around 257,800 t (Tian et
al., 2003) and have fluctuated greatly
from 52,207 t in 1969 to 207,770 t in
2011 (Fisheries Agency and Fisheries
Research Agency of Japan, 2012).
The number, size, and location of
fishing grounds for Pacific saury are
largely affected by oceanographic
conditions (Yasuda and Watanabe,
1994; Kosaka, 2000; Tian et al.,
2002), and the significant effect of
environmental factors on abundance
of Pacific saury was evident in the
unexpected drop in both the catch
and catch per unit of effort in 1998,
following a period of high abundance
(Tian et al., 2003). The distribution
and migratory patterns of Pacific
saury have been associated with
chlorophyll-a (chl-a) concentration
and sea-surface temperature (SST)
(Watanabe et al., 2006; Mukai et
al., 2007; Tseng et al., 2013). More-
over, sea-surface height indicates
water mass movements and, by ex-
tension, the flow of heat and nutri-
ents, which will subsequently influ-
ence productivity (Ayers and Lozier,
2010). Sea-surface height can also be
used to infer physical oceanographic
features, such as eddies, fronts, and
convergences (Polovina and Howell,
2005). Therefore, understanding the
relationship between oceanographic
Syah et al.: Predicting potential fishing zones for Cololabis saira
331
factors and the migration and distribution of species is
essential for fisheries management.
Most studies of Pacific saury have concentrated on
distribution and migration and have used in situ or
logbook data (Huang et al., 2007; Tseng et al., 2013),
and models have been developed to investigate growth
and abundance (Tian et al., 2004; Ito et al, 2004, 2007;
Mukaietal., 2007). In contrast, Watanabe et al. (2006)
proposed a spatial and temporal migration model for
stock size that was dependent on SST. However, inte-
grated high-resolution nighttime satellite images, such
as those available in the time-series data from the Op-
erational Linescan System (OLS) of the Defense Me-
teorological Satellite Program, U.S. Department of De-
fense, together with habitat and environmental model-
ing, have not been used to predict the potential fishing
zones for Pacific saury.
In Japan, fishing vessels operate at night and use
stick-held dip nets, locally known as bouke ami, which
are equipped with lights to attract fishes (Fukushima,
1979). These fishing vessels, equipped with lights, as
are vessels that fish for Pacific saury, can be identified
by the OLS sensor, which also enables the detection
of moonlight-illuminated clouds and lights from cit-
ies, towns, industrial sites, gas flares, and ephemeral
events, such as fires and lightning-illuminated clouds
(Elvidge et al., 1997). In addition, OLS nighttime im-
ages can be used to estimate fishing vessel numbers
and fishing areas for squid (Kiyofuji and Saitoh, 2004;
Kiyofuji et al., 2004). The relationship between the
number of lit pixels in OLS nighttime images and the
number of fishing vessels also has been analyzed for
the fishery of Illex argentinus (Waluda et al., 2002).
The brightly lit areas seen in nighttime images of the
western North Pacific are the result of vessels fishing
for Pacific saury or squid (Semedi et al., 2002; Saitoh
et al., 2010; Mugo et al., 2014).
Predictive habitat modeling has become an increas-
ingly useful tool for marine ecologists and conservation
scientists in order to estimate the patterns of species
distribution and to subsequently develop conservation
strategies (Johnson and Gillingham, 2005; Tsoar et
al., 2007; Ready et al., 2010). The maximum entropy
method (Phillips et al., 2006) involves one of the most
widely used machine-learning algorithms for inferring
species distributions. In recent studies, the method of
maximum entropy has been applied to both terrestrial
(Peterson et al., 2007) and marine ecosystems (Ready
et ah, 2010; Edren et ah, 2010; Alabia et ah, 2015). In
this study, we used a maximum entropy approach with
multi sensor satellite datasets and OLS-derived spe-
cies occurrences to create an accurate prediction model
and investigate the potential fishing zones for Pacific
saury in the western North Pacific. The objectives of
this study were to evaluate the effects of oceanographic
factors on the formation of potential fishing zones for
Pacific saury and to examine the variability in spatial
patterns of potential fishing zones in relation to the
prevailing oceanographic conditions in the western
North Pacific.
Materials and methods
Study area
This study was conducted in the western North Pacific,
extending from 140° to 155°E and from 34° to 46°N
(Fig. 1). In this study area, located between the sub-
arctic and subtropical domains of the North Pacific,
the confluence of the warm Kuroshio Current and the
cold Oyashio Current forms the Kuroshio-Oyashio
transition zone (Roden, 1991), also called the subarc-
tic-subtropical transition zone. The Kuroshio Current
is characterized by warm, low-density, nutrient-poor,
and high-salinity surface waters (Yatsu et al., 2013),
whereas the Oyashio Current is characterized by low-
salinity, low-temperature, and nutrient-rich waters
(Sakurai, 2007). The Kuroshio-Oyashio transition
zone is characterized by the mixing of various water
masses and complex physical oceanographic structures
(Roden, 1991). Moreover, 3 major oceanic fronts exist
in this region: the Polar Front, Subarctic Front, and
Kuroshio Extension Front (Science Council of Japan^).
The characteristic patterns of these oceanic fronts also
have been well documented in earlier studies (Kitano,
1972; Roden et al., 1982; Belkin and Mikhailichenko,
1986; Miyake, 1989; Belkin et ah, 1992, 2002; Yoshida,
1993; Onishi, 2001; Murase et ah, 2014; Shotwell et
al., 2014).
Satellite nighttime images
Daily cloud-free OLS nighttime images were download-
ed from the Satellite Image Database System of the
Agriculture, Forestry and Fisheries Research Informa-
tion Center of the Japan Ministry of Agriculture, For-
estry and Fisheries [the system is no longer operating].
The images were then used to determine the location
of the vessels that fish for Pacific saury in the western
North Pacific. A TeraScan^ system, vers. 4.0 (Seaspace
Corp., Poway, CA) was used to analyze the images and
to process the nighttime lights into digital numbers
(DNs), in a range of 0-63, that represent the visible
pixels in relative values. We selected 1264 single pass
images collected from August through December dur-
ing 2005-2013 (9 years) by 6 Defense Meteorological
Satellite Program satellites (F13, F14, F15, F16, F17,
and F18) (Table 1). The period from August through
December was chosen for analysis because it corre-
sponds with the fishing season of Pacific saury. To con-
struct the habitat suitability model, the daily images
were reprocessed with a 1-km resolution and then com-
piled in a monthly database. The location of the vessels
was assumed to represent the location of Pacific saury.
1 Science Council of Japan. 1960. The results of the Japa-
nese oceanographic project for the International Geophysical
Year 1957/8, 145 p. National Committee for the Interna-
tional Geophysical Year, Science Council of Japan, Tokyo.
^ Mention of trades names or commercial companies is for
identification purposes only and does not imply endorsement
by the National Marine Fisheries Service, NOAA.
332
Fishery Bulletin 1 14(3)
Hokkaid6
Sanriku
Joban
byashi(?.te§io|2.
Kui;oshio/egion^ ^
140'’E 142°E 144°E 146°E US^E ISO^E 152'’E 154‘’E
46“N
44°N
42‘’N
40°N -
38°N -
SG'N -
34''N
"v- - > ’ ^ '• '"*^^***‘ -
's^ A'. ’ ^ ‘ '
i s.' vv V s ^ > ' »
V* ■ It*' ' %
H;- tiV' y V '
, ' SuU^dlic-^ptrppicar 3/-
Trgnsitipnzone'
\ V- - ■ '
.. V -c
V--* , ‘ 1 V
I Depth (m)
-8000
-6000
-4000
-2000
0
Figure 1
Map of the study area in the western North Pacific with the hydro-
graphic and topographic features of the ocean basin. The line with
dashes and dots represents the boundary of the EEZ of Japan. The
lines with dashes correspond to the 3 major oceanic fronts — the Po-
lar Front (PF), Subartic Front (SAF), and Kuroshio Extension Front
(KEF). The subarctic-subtropical transition zone is also shown. Re-
drawn after Murase et al. (2014).
Detection of fishing vessel
We examined the histograms of DNs in our analyses
of OLS images for each month in order to identify the
fishing areas. Several peaks in DNs were recorded
over the examined 5-month periods (Fig. 2). To extract
the areas with fishing-vessel lights, DN thresholds for
identifying Pacific saury fishing vessels were calculated
for each month because of the monthly differences in
DN frequency distribution. A 2-level slicing method
was used to extract the bright areas thought to be
caused by the fishing fleet. This method is used to find
a statistical optimum threshold from the DN frequency
distribution (Takagi and Shimoda, 1991).
The thresholds, k, were determined through the
use of the following method proposed by Kiyofuji and
Saitoh (2004), and the variance, cf(k), was calculated
with the equations proposed by Takagi and Shimoda
(1991);
where
N
P.
(Oq
Ao
(7Hk)=o)o(iJ,-I^Ty^ + ct>i (1)
the number of pixels at i levels;
the total number of pixels;
nJN;
Y!l=xPi and cOi =
T,Li^P^ and /i-i = T,Lk+i^P^
liT= T!i=iiPi-
With these methods, 5 thresholds were identified (Table
2). Class 1, 2, 3, and 4 thresholds indicate ocean water
or cloud coverage, and the class 5 threshold indicates
bright areas resulting from fishing vessel lights. There-
fore, class 5 threshold values were applied to extract
the bright areas that represented fishing vessel lights.
Lights from vessels that fish for Pacific saury and
those that fish for squid are contained in OLS images.
These lights are difficult to distinguish from each other;
therefore, it is necessary to generate OLS images with
less contamination from the lights of vessels fishing for
Syah et al.: Predicting potential fishing zones for Cololabis saira
333
Table 1
Number of images from the Operational Linescan System of the U.S. Defense Meteorological Satel-
lite Program for the period 2005-2013, by month and year, that were used in this study to predict
fishing locations of Pacific saury (Cololabis saira) in the western North Pacific.
Month
2005
2006
2007
2008
2009
2010
2011
2012
2013
August
37
24
14
0
0
15
15
12
4
September
44
43
9
2
7
27
17
29
17
October
67
70
55
3
11
47
36
33
31
November
72
53
69
16
16
43
34
27
36
December
51
31
21
1
10
30
43
22
20
squid. In this study, we used SST to
distinguish between the lights of the
vessels that fish for Pacific saury and
those of other fishing vessels because
Pacific saury prefers colder areas for
their migration routes (Saitoh et al.,
1986) and this approach was used
earlier by Mugo et al. (2014).
Because Pacific saury are dis-
tributed below the upper SST limit
(Table 3), we split the nighttime light
images into 2 categories. All lights
that occurred above the upper SST
limit were categorized as lights re-
lated to squid fishing, and all lights
that occurred below this limit were
assumed to be from vessels fishing
for Pacific saury. Consequently, only
the locations of lights that indicated
fishing for Pacific saury were used
for our habitat modeling procedures.
Environmental data
We used satellite-derived data — chl-
a, SST, eddy kinetic energy (EKE),
and sea-surface height anomaly
(SSHA) — from 2005 through 2013 as
environmental factors in the maxi-
mum entropy models. Daily chl-a
and SST values were derived from
satellite images from the Moder-
ate Resolution Imaging Spectroradi-
ometer (MODIS)-Aqua mission and
were downloaded from NASA God-
dard Space Flight Center [website].
These data were processed with the
SeaDAS package, vers. 6.4 (NASA
Goddard Space Flight Center, Green-
belt, MD) and reprocessed to create
maps with a 1-km resolution.
Daily SSHA and geostrophic ve-
locities (u, v) from the Topex/Posei-
don and ERS-1/2 altimeters were
20
18
16
14
12
lllllillll
20 B
18
16
18
16
14
12
10
8
6
4
2 I
0 ■
llllllllu...
10 20
10 20 30 40 50 60
Digital number value
Figure 2
Histograms of the relative frequency of visible pixels derived from monthly
composite images obtained from the western North Pacific from the Opera-
tional Linescan System of the U.S. Defense Meteorological Satellite Pro-
gram for (A) August, (B) September, (C) October, (D) November, and (E)
December for the period 2005-2013
334
Fishery Bulletin 114(3)
Table 2
Thresholds for digital numbers (in pixels) for satellite
images from the Operational Linescan System of the
U.S. Defense Meteorological Satellite Program for the
period 2005-2013. Thresholds were calculated from the
histogram in Figure 2. Pixels within the class 5 range
represent fishing vessel lights. Classes 1-4 represent
reflected light from ocean water or light from cloud
cover.
Month
Class 1
Class 2
Class 3
Class 4
Class
August
10
17
23
30
40
September
9
16
22
28
38
October
8
14
19
27
38
November
8
13
19
28
38
December
7
12
18
27
38
Table 3
Mean monthly sea-surface temperature (SST) values
(°C) and standard deviations (SD), used to distinguish
the light of vessels fishing for Pacific saury (Cololabis
saira) from the lights of fishing fleets fishing for other
fish. All lights occurring below the upper SST limit
were categorized as locations of vessels targeting Pa-
cific saury.
Month
Mean
SD
Upper SST limit
August
20.79
2.69
23.48
September
18.89
2.47
21.36
October
15.90
2.58
18.48
November
14.56
2.88
17.44
December
13.60
2.89
16.49
produced and distributed by Archiving Validation and
Interpretation of Satellite Oceanographic Data (AVISO;
website) at a spatial resolution of 0.33°x0.33°. The sur-
face geostrophic velocities were used to compute for EKE
by using the following equation (Steele et al., 2010):
EKE = 1/2 (u’2 + n’2), (2)
where w’ and v’ = the zonal and meridional components
of geostrophic currents, respectively.
With the grid function of the software package Ge-
neric Mapping Tools, vers. GMT 4.5.7 (website),we
were able to calculate the monthly averages for each
environmental variable from daily data sets, resampled
to 1-km resolution and converted to Esri ASCII grid
format(Esri, Redlands, CA) or to comma-separated val-
ues (CSV) format, as required by the software program
Maxent (website).
Construction of a maximum entropy model
To develop a model with a maximum entropy approach,
we used the software program Maxent, vers. 3.3.3k.
Phillips et al. (2006) provided detailed information on
the mode of operating this software. We constructed
models using default values for regulation parameter
(1), maximum iteration (500), and automatic feature
class selection. We used a cross-validation procedure
to evaluate the performance of the models. For back-
ground points, we generated pseudo-absences (10:1
ratio of pseudo-absence to presence) following Barbet-
Massin et al., (2012) on the basis of random spatial
sampling within the study area (excluding points of
presence of Pacific saury). We used the density.tools.
Randoms ample command line in Maxent to generate
the random pseudo-absences. For each monthly model,
the data were randomly split into 2 categories: one
category for training data (70%) and one for test data
(30%). The test points were then used to calculate the
area under the curve (AUG) of the receiver operating
characteristic (ROC) (Phillips et al., 2006).
Evaluation and validation of the model
We used the AUG metric of the ROC curve to evaluate
model fit (Elith et al., 2006; Phillips et al., 2006). The
relative contribution of individual environmental vari-
ables within the maximum entropy model was exam-
ined by using the heuristic estimates of variable impor-
tance based on the increase in the model gain, which is
associated with each environmental factor and its cor-
responding model feature. Response curves generated
for each factor were examined to derive the favorable
environmental ranges for potential fishing zones.
Independent sets of monthly OLS data from 2011
through 2013 were used to validate the models. The
base models were used to create habitat suitability
indices (HSIs) that assimilated similar environmental
layers for the corresponding period from 2011 through
2013. Spatial HSI maps were generated and over-
lain with information on OLS data from the period
2011-2013.
Results
Spatiotemporal distribution of fishing locations, and envi-
ronmental data
Figure 3 shows the variation in the distribution of
fishing vessel lights from August through December
during 2005-2013. Vessels started to appear off the Ku-
ril Islands and east of Hokkaido in August (Fig. 3A). At
the same time, fishing also occurred around the Sanriku
coast of Japan and an offshore area between 150°E and
41°N that extended northeast tol55°E and 43°N.
During September (Fig. 3B), fishing vessels were
distributed mostly north of 42°N, especially off east-
Syah et al.; Predicting potential fishing zones for Cololabis saira
335
14rE 144°E 147“E 150°E 153°E 14rE 144°E 147°E ISO'E 153°E 14rE 144°E 147°E 150°E 153°E
Figure 3
Spatial distribution of fishing locations for Pacific saury (Cololabis saira) in the western
North Pacific pooled during (A) August, (B) September, (C) October, (D) November, and (E)
December for the period 2005—2013.
ern Hokkaido, whereas the number of vessels off the
Sanriku coast decreased. In October (Fig. 3C), fishing
vessels were widely distributed in Hokkaido and San-
riku waters. The distribution of fishing vessels moved
slightly to the south and approached the shores of
southeastern Hokkaido and Sanriku (38-41°N). During
this same month, the offshore fishing locations (148°E
and 48°N) also increased and extended northeast to
154°E and 43°N.
During November (Fig. 3D), fishing vessels moved
southward. The number of fishing vessels in eastern
Hokkaido waters decreased, but the number of fishing
vessels around the Sanriku coast increased (38-41°N)
and moved northeast to 155°E and 43°N. A small num-
ber of fishing vessels also appeared off the Joban coast.
In December (Fig. 3E), fishing vessels appeared mostly
along the Sanriku coast and were distributed in near-
shore waters between 38°N and 40°N; however, a small
number of fishing vessels still remained offshore and
along the Joban coast.
The monthly averaged time series of environmental
data for the period 2005-2013 are shown in Figure 4.
Mean SST values indicated a decreasing trend of tem-
perature on the fishing locations from August through
December (Fig. 4A). Mean chl-a concentrations (Fig.
4B) increased in September but declined in December.
The mean chl-a concentration was highest in Septem-
ber (0.93 mg/m^), when most vessels were concentrated
off the eastern coast of Hokkaido and near the south-
ern Kuril Islands. Mean EKE and SSHA values (Fig. 4,
C-D) increased in trends that corresponded with the
southward shift of fishing vessels, especially from Sep-
tember until November.
Model performance and potential fish habitat
All monthly maximum entropy models significantly
fitted better than they were fitted by chance as sup-
ported by the modest values of the performance metric
(AUC>0.5; Table 4). This outcome indicates the high
predictive success of these models (Elith et al., 2006;
Phillips et al., 2006). The relative contribution of each
environmental variable to model prediction is shown
in Table 5. Model results indicate that the 2 most im-
portant factors in August and October were SST and
EKE, and in September the most important factors
were SST and chl-a. In November and December, the
2 highest contributions to model gain were SST and
SSHA.
Figure 5 provides the model-derived preferred rang-
es for each environmental variable. The plots in this
figure show the performance and contribution of the
various environmental data to model fit. High prob-
abilities of occurrence of Pacific saury were observed
in varied ranges for each month. In general, occurrence
of Pacific saury had the highest probabilities in cool
(14-16“C) waters with chl-a concentrations of 0. 5-2.0
mg/m^. In addition, there were high probabilities of oc-
currence of Pacific saury at low to moderate EKE and
positive SSHA values.
336
Fishery Bulletin 114(3)
AUG SEP OCT NOV DEC
Month
AUG SEP OCT NOV DEC
Month
AUG SEP OCT NOV DEC
Month
Figure 4
Monthly mean time series of (A) sea-surface temperature (SST), (B)
chlorophyll-o (chl-a), (C) sea-surface height anomaly (SSHA), and (D)
eddy kinetic energy (EKE) in the western North Pacific from August
through December for the period 2005-2013.
Table 4
Summary statistics derived from the monthly models
for the period 2005-2010. The base models were cali-
brated with 70% of Pacific saury occurrence data, and
values for the area under the curve (AUC) were calcu-
lated from the remaining 30% of the occurrence data.
The total number of fishing locations (N) is given for
each month. All the models fitted significantly better
than if they were fitted by chance (AUC>0.5).
Month
AUC
N
August
0.907
8074
September
0.910
7411
October
0.912
10,062
November
0.886
5162
December
0.949
429
Table 5
Heuristic estimates of the relative percent contribu-
tion of environmental variables to models derived by
using a maximum entropy approach. The 2 most impor-
tant variables for each monthly model are presented in
bold. SST=sea surface temperature; chl-a=chlorophyll-
a; EKE=eddy kinetic energy; SSHA=sea-surface height
anomaly.
Environmental predictors
Model
SST
Chl-a
EKE
SSHA
August
55.6
7.1
28.1
9.2
September
56.8
21.6
14.4
7.2
October
72.2
5.9
13.6
8.3
November
73.2
2.9
9.4
14.5
December
57.6
0.8
6.2
35.4
Prediction and validation of occurrence
Maps of predicted HSI for August-December (2011-
2013) are shown in Figure 6. In August, the predict-
ed probability of occurrence of Pacific saury covered
the entire Oyashio region, but it did so with a small
value of HSI (Fig. 6, A-C). In September, high prob-
ability areas (HIS >0.6) increased, especially east of
Hokkaido and the Kuril Islands. The presence of fish-
ing locations derived from OLS images also increased
east of Hokkaido during this period (Fig. 6, D-F). In
October, the known peak of the fishing season, a high
Syah et al.: Predicting potential fishing zones for Cololabis saira
337
probability of occurrence of Pacific saury remained for
east and southeast of Hokkaido and south of the Ku-
ril Islands. During the same month, the results from
the predicted HSI indicated the Kuroshio-Oyashio
transition zone at 40°N, and a correspondingly high
probability of occurrence of Pacific saury (Fig. 6, G-I).
In November, the high predicted HSI in the transi-
tion zone (38-42°N and 142-156°E) increased, espe-
cially off the Sanriku (39-41°N) and Joban (38-39°N)
coasts (Fig. 6, J-L). At the end of the fishing season
in December, the predicted probability of occurrence
dramatically decreased in the offshore areas but re-
mained high off the Sanriku and Joban coasts (Fig.
6, M-0). In general, the distribution of Pacific saury
based on the HSI showed moderate spatial correlation
with actual fishing locations derived from OLS imag-
es, although it did so with relatively low HSI values,
particularly in August.
Discussion
We used fishing locations for Pacific saury and oceano-
graphic variables with maximum entropy models to pre-
dict the potential fishing zones for Pacific saury in west-
ern North Pacific waters. Analyses of OLS nighttime
images allowed us to locate fishing vessel lights across
space and time, and we assumed that Pacific saury were
caught in areas where fishing vessels were identified.
On the basis of the derived fishing vessel locations, we
were able to estimate the spatial and temporal distribu-
tion of potential fishing zones for Pacific saury.
338
Fishery Bulletin 114(3)
140°E 144°E 148°E 152°E UQ-E 144°E US'E 152°E 140°E 144°E 148°E 152°E
40'’N
36°N
44°N
40°N
36°N
44°N
40“IM
36'’N
44°N
40‘’N
36°N
44°N
40°N
36°N
I- I I I
0.0 0.2 0.4 0.6 0.8 1.0
Figure 6
The spatial distribution of fishing locations (red dots) for Pacific saury (Cololabis saira) in the western North Pacific derived from
analyses of images from the Operational Linescan System of the U.S. Defense Meteorological Satellite Program for the period
August-December during 2011-2013, overlain on maps of habitat suitability predicted with base models. The suitability is de-
picted as an Habitat Suitability Index (HSI) score ranging from 0 to 1, representing “poor” to “good” habitat quality, respectively.
Syah et al.: Predicting potential fishing zones for Cololabis saira
339
At the beginning of the fishing season, fishing loca-
tions derived from OLS images showed that most of
the vessels that fished for Pacific saury appeared east
of Hokkaido and south of the Kuril Islands (Fig. 3, A
and B). In the middle of the fishing season (October
to November) (Fig. 3, C and D), vessels that fish for
Pacific saury moved slightly to the south and appeared
mostly around the eastern coasts of Hokkaido and
Sanriku — a finding that potentially resulted from the
southward extension of Oyashio fronts (Watanabe et
al., 2006; Tseng et al., 2011). At the end of the fishing
season, vessels that fish for Pacific saury were concen-
trated along the Sanriku coast (Fig. 3E).
Images from the OLS also showed that some of the
fishing vessels appeared outside the FEZ, possibly be-
cause Pacific saury is an oceanic spawner, unlike oth-
er small pelagic fishes, such as the Japanese sardine
iSardinops melanostictus) and the Japanese anchovy
[Engraulis japonicus), that generally spawn in the
coastal and near shore waters of Japan (Zenitani et
al., 1995). The low capture of fish west of 150°E from
June through July before the fishing season indicates
that Pacific saury caught by Japanese fishing vessels
were located far from the northeastern coasts of Japan
(Tohoku National Fisheries Research Institute^).
The predicted distribution of Pacific saury in the
western North Pacific revealed areas of high probabil-
ity of occurrence off Hokkaido and the Kuril Islands
(Fig. 6, A-F), areas that gradually moved south toward
the Sanriku and Joban coasts by the end of the fish-
ing season (Fig. 6, M-0). These patterns coincided with
the north-south migration of Pacific saury that marks
the start and end of the fishing season. Results from
a maximum entropy approach further indicate that
the highest probability of presence occurred along the
Kuroshio-Oyashio transition zone in November (Fig. 6,
J-L).
The occurrence of large-size Pacific saury (>29.0 cm
in knob length) off the southern Kuril Islands dur-
ing their spawning migration indicates that a high
proportion of large-size Pacific saury moved from the
high seas to coastal waters at the beginning of their
migration toward the southwest — movement that was
then followed by a similar migration of medium-size
Pacific saury (24.0-29.0 cm in knob length). Therefore,
abundance of Pacific saury off the coastal waters in our
study is higher than the abundance observed in regions
in the high seas (Huang, 2010). In addition, the high
density of Pacific saury off Hokkaido and the Kuril Is-
lands was probably related to the southward movement
of the Oyashio Current (Tseng et al., 2011). The high
presence of Pacific saury at the coasts also could be
a result of a westward current intensification, which
can result in the formation of oceanic fronts (Huang,
2010). These frontal features have been known as the
^ Tohoku National Fisheries Research Institute. 2010. The
58*** Annual Report of the Research Meeting on Saury Re-
sources, 250 p. Tohoku Natl. Fisheries Res. Inst., Hachi-
nohe, Japan. [In Japanese.]
preferred migratory routes of Pacific saury and other
marine species (Saitoh et al., 1986; Zainuddin et al.,
2008).
Although oceanographic conditions are likely to af-
fect species distribution, other factors, such as prey
density, are equally important. In the Kuroshio-Oyas-
hio transition zone, Oyashio intrusions transport or-
ganic matter, thereby supporting the production of
copepods, which are the primary prey of Pacific saury
(Odate, 1994; Shimizu et al., 2009). This salient physi-
cal process could potentially explain the existence of
habitat areas of Pacific saury in the transition zone, ar-
eas that were identified with maximum entropy models
and that consequently highlight the importance of this
region as migratory and feeding corridors for Pacific
saury.
The variability of the performance of the maximum
entropy model was very low across the monthly base
models, where AUCs higher than 0.9 indicate that
models had excellent agreement with the test data
(Table 4). As pointed out earlier, productivity and fish
distribution are influenced by changes in the environ-
ment evident from the variations in temperature, cur-
rents, salinity, and wind fields (Southward et al., 1988;
Alheit and Hagen, 1997). In our study, SST (among the
set of oceanographic variables examined) showed the
highest contribution to all monthly base models (Table
5), indicating the sensitivity of Pacific saury to tem-
perature changes. For instance, increasing SST will
directly reduce juvenile growth and prevent, or delay,
the southern migration of Pacific saury in winter (Ito
et al., 2013). Moreover, changes in winter SSTs in the
Kuroshio-Oyashio transition zone and in the Kuroshio
and Oyashio regions also affected the abundance of the
large-size (winter cohort) and medium-size (spring co-
hort) groups of Pacific saury (Tian et al., 2003).
To our knowledge, this study was the first attempt to
use both EKE and SSHA to describe potential fishing
habitat of Pacific saury in relation to mesoscale ocean-
ography variability. Our results indicate that fishing
activities occurred in areas with low to moderate EKE
(Fig. 5), reflecting the likely association of this species
with eddies. Meandering eddies likely trap prey of Pa-
cific saury, creating good feeding opportunities through
local enhancement of chl-a and zooplankton abundance
and through the aggregation of prey organisms (Owen,
1981; Zhang et al., 2001). The importance of forage
availability for Pacific saury is further reflected in the
higher contribution of chl-a concentration to the base
model in September (Table 5). Together with SST, chl-a
has been found to influence Pacific saury growth, re-
cruitment, distribution, and migratory patterns (Ito et
al., 2004; Oozeki et al., 2004; Yasuda and Watanabe,
2007). However, from November through December,
the distribution of Pacific saury likely is not limited
by food availability because of a general increase in
ocean mixing and a decrease in water column stratifi-
cation during this period. These oceanographic condi-
tions consequently enhance the chl-a concentration in
the mixed-water region (Mugo et al., 2014).
340
Fishery Bulletin 114(3)
Finally, OLS nighttime images were found to be use-
ful for investigating the distribution of the lights of
fishing vessels — an outcome that supports the results
of earlier studies (Semedi et ah, 2002; Saitoh et al.,
2010). However, cloud contamination significantly lim-
ited the use of OLS images and reduced the density
of proxy fishing locations; therefore, logbook data are
needed to confirm the validity of fish occurrences in
the future. The integration of these empirical data with
multi sensor remote sensing information within a mod-
eling platform could offer a powerful and innovative
way to identify the potential fishing zones for Pacific
saury and could be used to support fisheries manage-
ment decisions.
Acknowledgments
This work was supported by the Directorate General
of Higher Education of the Republic of Indonesia. We
thank the 3 anonymous reviewers for their valuable
comments. We also recognize the use of OLS images
downloaded from the Satellite Image Database System
of the Ministry of Agriculture, Forestry and Fisheries,
SST and chl-a data from NASA’s Goddard Space Flight
Center, and SSHA and geostrophic velocity data from
the AVISO website.
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343
NOAA
National Marine
Fisheries Service
Fishery Bulletin
established 1881 -.
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Depth and temperatyre distribution,
morphometries, and sex ratios of red deepsea
crab iChaceon quinquedens^ at 4 sampling sites
in the Mid-Atlantic Bight
Email address for contact author: bgstevens@umes.edu
Abstract— The red deepsea crab
{Chaceon quinquedens) supports a
small fishery of <2000 metric tons
annually along the U.S. East Coast,
but little is known about the life
history of this crab. We sampled
red deepsea crab from 4 sites and 3
depth strata (250-450 m, 450-700
m, and 700-850 m) in the Mid-At-
lantic Bight in January 2011 and
2012 and in July 2013. Crab size
decreased with depth, whereas shell
age indices increased with depth.
Crab occurred at temperatures from
4.6°C to 10.6°C (mean: 6.37°C) and
there was little difference between
sexes. Size at 50% maturity (SM50)
could not be determined with chela
or abdomen allometry, but SM50
was estimated at 61.6 mm in cara-
pace length for females on the ba-
sis of gonopore condition. Sex ratios
(M:F) involving female crab above
the SM50 were <0.5, indicating that
large males are depleted in com-
parison with female abundance. The
proportion of ovigerous females was
33% in January 2012 and <6% in
July 2013, proportions that support
the hypothesis of a biennial (or lon-
ger) reproductive cycle. Red deepsea
crab probably recruit to deep water
(>1000 m), move upslope during ado-
lescence, and become mature in the
shallowest strata, before undergoing
an ontogenetic migration back to in-
termediate depths.
Manuscript submitted 29 May 2015.
Manuscript accepted 2 May 2016.
Fish. Bull. 114:343-359 (2016).
Online publication date: 2 June 2016.
doi: 10.7755/FB.114.3.7
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Bradley G. Stevens (contact author)^
Vincent Guida^
' Department of Natural Sciences
University of Maryland Eastern Shore
Carver Hall
Princess Anne, Maryland 21853
2 Northeast Fisheries Science Center
National Marine Fisheries Service, NOAA
James J. Howard Marine Sciences Laboratory
74 Magruder Road, Sandy Hook
Highlands, New Jersey 07732
The red deepsea crab {Chaceon
quinquedens) ranges from the Gulf
of Maine to the Gulf of Mexico, at
depths from 200 to 1800 m, and
temperatures of 5-8°C (Haefner and
Musick, 1974; Wigley et ah, 1975;
Serchuk^; Steimle et ah, 2001; Wahle
et ah, 2008; NEFSC^). Stocks along
the Atlantic coast are considered a
single population and distinct from
the stock in the Gulf of Mexico. Red
deepsea crab support a small but
valuable fishery in federally man-
aged waters along the continental
slope of southern New England and
the Mid-Atlantic, a fishery that has
^ Serchuk, F. M. 1977. Assessment of
red crab (Geryon quinquedens) popula-
tions in the northwest Atlantic. Natl.
Mar. Fish. Serv., Northeast Fish. Sci.
Cent. Lab. Ref. 15 p. [Available
at website.]
2 NEFSC (Northeast Fisheries Science
Center). 2009. The Northeast Data
Poor Stocks Working Group report, De-
cember 8-12, 2008 meeting. Part A.
Skate species complex, deep sea red
crab, Atlantic wolffish, scup, and black
sea bass. NOAA, Natl. Mar. Fish. Serv.,
Northeast Fish. Sci. Cent. Ref Doc. 09-
02, 496 p. [Available at website.]
been managed since 2002 by the New
England Fishery Management Coun-
cil (Wigley et ah, 1975; Wahle et ah,
2008). In recent years, 4 vessels have
fished for red deepsea crab and have
averaged annual landings of 1360
metric tons (t) over the time period
2002-2013, but landings have de-
clined from 1600 to 930 t during that
period (Chute^). Red deepsea crab
are a data-poor fishery stock. Very
little is known about their biology,
abundance, growth, age, or reproduc-
tion, and, as a result, management
consists primarily of controls on total
allowable catch, currently set at 2688
t. Because of inadequate information
on biomass, the New England Fish-
ery Management Council Scientific
and Statistical Committee has not
set a fishing-induced mortality rate
or determined whether the stock is
in a status of overfished or overfish-
ing (Chute et ah'*).
® Chute, A. 2014. Personal commun.
Northeast Fish. Sci. Cent., Natl. Mar.
Fish. Serv., NOAA, Woods Hole, MA
02543.
^ Chute, A., L. Jacobson, P. Rago, and A.
344
Fishery Bulletin 114(3)
Because of their extended depth range, few red
deepsea crab are captured during semiannual assess-
ment surveys conducted by the National Marine Fish-
eries Service. Red deepsea crab have been studied
during several previous surveys. McRae (1961) found
significant concentrations of crab southeast of Ocean
City, Maryland, but concluded that they were too
sparse to support a commercial fishery. In two surveys,
abundance of populations of red deepsea crab was es-
timated by using towed camera systems. The first sur-
vey (Wigley et al., 1975) was conducted in 1974 before
the onset of commercial fishing. The second, conducted
during 2003-2005 (Wahle et al., 2008), showed a 250%
increase in overall biomass (mostly due to juveniles),
after a decade of targeted harvesting of males, but a
42% decline in the biomass of large males at depths
of 350-500 m where fishing occurs, as well as a de-
cline in body condition indices (carapace length [CL]:
weight ratios) (Weinberg and Keith, 2003). In addition,
the size of landed crabs has declined from 114 mm in
carapace width (CW) in 1974 to <90 mm CW by 2008
(Chute et al.'^).
There is scant information on biological parameters
of red deepsea crab, such as size at maturity, fecun-
dity, or timing of reproduction. Fecundity increases
with body size (Hines, 1988). Size at maturity for fe-
male red deepsea crab has been estimated by Haefner
(1977, 1978) to be between 65-75 mm CL, but a large
portion of his samples were barren, indicative of bi-
ennial spawning. Size at 50% maturity has been es-
timated with ratios of chela width (ChW) to CW for
the congener C. affinis from the Canary Islands (males:
129 mm CW; females: 99 mm CW) (Fernandez-Vergaz
et al., 2000), by gonad condition for C. affinis in the
northeast Atlantic (males: 94 mm CW; females: 109
mm CW) (Robinson, 2008), and for male C. maritae
in South Africa (93 mm CW) by using growth incre-
ment analysis (Melville-Smith, 1989). Spawning of C.
affinis in the Canary Islands occurs from October to
May, but ovigerous females were found only in March
and April (Lopez Abelian et al., 2002) and from Octo-
ber to March in the Azores (Pinho et al., 2001). In the
Gulf of Mexico, male golden deepsea crab (C. fenneri)
produce sperm in late winter and mate with females
during March-April, but females do not extrude eggs
until the following fall (Hinsch, 1988a, 1988b). Life his-
tory characteristics of other geryonid crab species were
reviewed and compared by Hastie (Hastie, 1995).
Maturity of female crabs can be inferred from the
presence of eggs, gonopore condition, or ovary develop-
ment, but maturity of male crabs is difficult to deter-
mine. Male crabs may carry spermatophores, indicative
of physiological maturity, at sizes well below that at
MacCall. 2009. Deep sea red crab. In Northeast Data
Poor Stocks Working Group report, December 8-12, 2008
meeting. Part A. Skate species complex, deep sea red crab,
Atlantic wolffish, scup, and black sea bass. NOAA, Natl.
Mar. Fish. Serv., Northeast Fish. Sci. Cent. Ref. Doc. 09-02,
p. 181-214. [Available at website.]
which they can mate. Many genera (e.g., Chionoecetes,
Lithodes, Cancer) exhibit allometric growth of the che-
lae at the pubertal molt, after which they are classified
as morphometrically mature and are distinguishable
by an increase in the slope and intercept of the ratio of
chela height (ChH) to CW (ChH:CW) (Somerton, 1980;
Somerton and Macintosh, 1983; Comeau and Conan,
1992; Stevens, et al., 1993; Corgos and Freire, 2006).
Lack of biological, survey, and fishery information
for the red deepsea crab causes major uncertainties
about the status of its stock and possible management
approaches. Up to 85% of the catch of this species con-
sists of females and undersize crab that are discarded
and that result in a possible mortality of about 5%
(Tallack, 2007). At present, it is not possible to calcu-
late biological reference points (e.g., biomass or fish-
ing-induced mortality at maximum sustainable yield
[Bmsy, Fmsy; respectively]) because of a lack of informa-
tion on growth, longevity, and mortality (NEFSC®). For
the same reasons, it is not possible to predict future
stock status, biomass, or response to changes in climate
or fishing mortality. Although landings of red deepsea
crab have stabilized at intermediate levels in recent
years, the landed size has declined from 114 mm CW
in 1974 to 105 mm CW in 2005, and there is concern
about sperm limitation because of reductions in bio-
mass of large males.
At a minimum, effective management requires in-
formation on growth, mortality, and size at maturity.
In particular, it is necessary to know the frequency of
molt and reproduction in females, the presence or ab-
sence of terminal molt and multiple fertilizations, and
the status of sperm storage and fecundity. The NOAA
Red Crab Working Group has made a variety of high-
priority research recommendations for understanding
the life history of red deepsea crab, including a bet-
ter understanding of the reproductive cycle, maturity
schedule, and fecundity of female red deepsea crab;
of the potential reproductive consequences of remov-
ing large males from the population; and of the growth
rate and molt cycle of red deepsea crab (Miller et al.®).
We began studies of the red deepsea crab in 2011
to provide data on reproduction and life history for
this species. Data were collected aboard NOAA re-
search vessels during 3 cruises jointly sponsored by
the NOAA Northeast Fishery Science Center and the
Living Marine Resources Cooperative Science Center
at the University of Maryland Eastern Shore. The ob-
jectives for these cruises were to sample the continen-
tal shelf fauna during winter (in 2011 and 2012) and
® NEFSC (Northeast Fisheries Science Center). 2006. 43rd
Northeast Regional Stock Assessment Workshop (43''® SAW);
43''® SAW assessment summary report. NOAA, Natl. Mar.
Fish. Serv., Northeast Fish. Sci. Cent. Ref. Doc.. 06-14, 54
p. [Available at website.]
® Miller, T., R. Muller, B. O’Boyle, and A. Rosenberg. 2009. Re-
port by the Peer Review Panel for the Northeast Data Poor
Stocks Working Group, 38 p. NOAA, Natl. Mar. Fish. Serv.,
Northeast Fish.s Sci. Cent., Woods Hole, MA. [Available at
website.]
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
345
76'0‘0'’W 75»0’0"W 74°0’0"W 73'0'0"W 72”0'0"W 71'’0'0"W
Figure. 1
Locations of sampling sites for red deepsea crab {Chaceon quinque-
dens) during cruises aboard the NOAA Ship Delaware II in the Mid-
Atlantic Bight in 2011 and 2012 and aboard the NOAA Ship Gordon
Gunter in 2013. The sites were Block Island Canyon (BIC), Hudson
Canyon (Hud), Baltimore and Washington Canyons (BWC), and Nor-
folk Canyon (Nor).
to collect samples of red deepsea crab. Specific goals
for research of red deepsea crab were to determine 1)
the distribution of crab by sex, size, shell condition,
depth, and temperature, 2) to obtain morphometric
data for determination of sexual maturity, and 3) to
collect specimens for studies of reproductive biology.
This article presents information on distribution and
morphometry of red deepsea crab collected during the
3 NOAA cruises.
Materials and methods
Sampling locations
Two research cruises were conducted aboard the NOAA
Ship Delaware II (10-21 January 2011 and 21-30 Jan-
uary 2012) and one cruise was completed aboard the
NOAA Ship Gordon Gunter (5-8 July 2013). Red deep-
sea crab were sampled in 4 general areas within the
Mid-Atlantic Bight (defined as coastal waters along the
U.S. Atlantic coast from Cape Cod to Cape Hatteras),
and stations were selected to cover a range of lati-
tudes and depths: near Block Island Canyon (BIC), at
the mouth of Hudson Canyon (Hud), on the continen-
tal slope between Baltimore and Washington Canyons
(BWC), and on the slope near Norfolk Canyon (Nor;
Fig. 1). Actual locations within each site where trawl
nets were hauled were chosen for their relatively flat
contours within specified depth ranges (see below) af-
ter reconnaissance with multibeam sonar. Goals of the
cruise in 2011 were primarily focused on sampling fish;
red deepsea crab were caught incidentally in the deep-
er (>300 m) tows, and sampling of crab was mostly op-
portunistic. In 2012 and 2013, stations were specifical-
ly defined to capture red deepsea crab, and tows were
made in 3 depth strata defined as shallow (250-450 m),
middle slope (450-700 m), and deep (700-850 m) (Table
1). One attempt to tow a trawl net at a depth of 1000 m
failed when the net was snagged and both trawl warps
were broken, resulting in loss of a trawl net. Because of
inclement weather and technical delays, site BIC was
sampled only in 2012, and site BWC was not sampled
in 2011.
Water temperature and depth profiles were recorded
with a conductivity, temperature, and depth profiler be-
fore each trawl tow at each site and depth stratum. In
2011, a Yankee 36 otter trawl with an 18.3-m headrope,
346
Fishery Bulletin 1 14(3)
Table 1
Data collected from trawl tows and expanded catch data from surveys of red deepsea crab (Chaecon quinquedens) conducted
in the mid-Atlantic Bight during 3 cruises (2011-2013): depth stratum of trawl (Strat; l=shallow [250-450 m], 2=middle
slope [450-700 m], and 3=deep [700-850 m]); bottom temperature (Btemp, °C); swept area (Area, m^); number of male crab
caught (Males), number of female crab caught (Females); total number of crab caught (Total); density of male crab (Mdens,
individuals/ha); density of female crab (Fdens, individuals/ha), total density of crab (Tdens, individuals/ha); expansion fac-
tor for subsampled tows (ExpFac); mean weight of male crab (Mwt, kg); and mean weight of female crab (Fwt, kg). Stations
were located at 4 sites: Block Island Canyon (BIG), Hudson Canyon (Hud), Baltimore and Washington Canyons (BWC), and
Norfolk Canyon (Nor).
Depth
Station
Year
Date
Strat
(m)
Btemp
Area
Males
Females
Total
Mdens
Fdens
Tdens
ExpFac
Mwt
Fwt
Hud-1
2011
1/15/2011
1
403.7
7.8
30,512
170
307
477
55.7
100.7
156.3
3.613
0.236
0.265
Hud-2
2011
1/15/2011
2
499.4
6.4
33,057
480
655
1134
145.1
198.0
343.1
5.643
0.357
0.206
Hud-2
2011
1/15/2011
2
558.5
7.3
31,866
1017
1645
2662
319.2
516.1
835.3
10.820
0.213
0.156
Hud-3
2011
1/14/2011
2
631.7
5.5
31,413
725
1755
2480
230.7
558.8
789.5
10.206
0.289
0.130
Nor-l
2011
1/18/2011
1
363.4
9.0
29,312
20
177
197
6.8
60.2
67.0
2.487
0.360
0.350
Nor-3
2011
1/17/2011
2
580.8
5.1
26,645
388
509
897
145.7
190.9
336.6
6.693
0.263
0.284
BIC-1
2012
1/19/2012
1
246.9
10.2
47,921
0
0
0
0.0
0.0
0.0
0
BIC-2
2012
1/19/2012
2
483.6
6.1
41,463
103
211
315
25.0
51.0
75.9
4.312
BIC-3
2012
1/19/2012
3
731.5
4.6
30,482
214
62
276
70.1
20.3
90.4
3.444
Hud-1
2012
1/21/2012
1
294.0
11.5
42,011
0
0
0
0.0
0.0
0.0
0
Hud-2
2012
1/26/2012
1
298.3
8.8
32,071
277
92
369
86.3
28.8
115.1
5.127
Hud-3
2012
1/26/2012
2
644.2
6.9
34,345
125
200
326
36.5
58.3
94.8
2.022
0.278
0.20
BWC-1
2012
1/25/2012
1
134.8
14.2
30,847
0
5
5
0.0
1.6
1.6
1
BWC-2
2012
1/25/2012
2
571.4
5.6
25,973
520
2092
2612
200.2
805.3
1005.5
11.556
0.386
0.190
BWC-3
2012
1/25/2012
3
760.5
5.1
27,007
100
51
151
37.0
18.9
55.9
1
Nor-l
2012
1/23/2012
1
321.4
9.2
37,555
0
0
0
0.0
0.0
0.0
0
Nor-2
2012
1/23/2012
2
521.9
6.8
42,703
377
882
1259
88.3
206.5
294.7
6.389
Nor-3
2012
1/22/2012
3
773.7
4.8
25,800
90
64
154
34.8
24.8
59.6
1.830
Hud-1
2013
7/7/2013
1
263.6
8.1
34,124
0
0
0
0.0
0.0
0.0
0
Hud-2
2013
7/7/2013
2
569.2
5.7
42,385
0
0
0
0.0
0.0
0.0
0
Hud-3
2013
7/7/2013
3
792.5
4.8
32,560
113
26
139
34.7
8.0
42.7
1
0.27
0.326
BWC-1
2013
7/8/2013
1
288.7
11.2
34,070
1
10
11
0.3
2.9
3.2
1
0.306
0.221
BWC-2
2013
7/8/2013
2
500.8
6.5
33,171
387
1391
1778
116.7
419.4
536.1
5.610
0.306
0.221
Nor-l
2013
7/5/2013
1
236.5
12.2
37,488
0
0
0
0.0
0.0
0.0
0
Nor-2
2013
7/5/2013
1
414.4
8.1
31,094
151
416
567
40.4
110.8
151.2
3.883
0.401
0.332
Nor-3
2013
7/5/2013
3
750.0«
7.1
33,694
336
78
414
99.8
23.1
122.9
2.101
0.211
0.185
“ Conductivity, temperature, and depth sensor failed; depth estimated from chart.
a codend that had a 1-cm mesh liner, and deepwater
headrope floats (“rock hoppers”) was deployed from the
stern trawl A-frame by using both trawl winches and
2.5-cm trawl wires. In 2012 and 2013, a similarly size
4-seam otter trawl net (with 6.0-cm body mesh and 2.5-
cm codend liner) was used. In all years, a 30-min tow
was made at -1.5 m/s (3 kt) along a specified depth
contour at each site and stratum. Distance towed was
determined from GPS coordinates, and area towed was
estimated as the distance multiplied by average net
width (13.0 m). Tows were made during all hours of
day or night. Time constraints prevented measuring
all crab in tows with larger catches (catch for 6 of the
tows exceeded 1000 crab); as a result, a goal of 150-200
crab per catch was set. All catches that consisted of
up to 3 baskets or a total of 60 kg of red deepsea crab
(approximately 150 crabs) were sampled completely.
whereas, for larger catches, a subsample of 2-3 baskets
that composed from 10% to 50% of the catch was taken.
The subsample was sorted by sex, after which males
and females were weighed separately to determine the
proportion of their biomass in the whole catch. A sam-
pling factor for each tow was recorded along with each
crab for later data expansion.
For each crab in a subsampled tow, the sex and
shell condition were recorded. Shell condition includes
coloration and abrasions of the carapace, sternum,
and dactyls, and therefore provides a crude but inte-
grated index of time since molt. Shells were classified
into 4 standard categories, defined by the National
Marine Fisheries Service for brachyuran crabs (see
Jadamec et ah, 1999), that represented relative time
since molting, determined by radiometric aging (Nev-
issi et ah, 1996). We have adapted the following cat-
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
347
egories for red deepsea crab: 1) new-shell crab were
relatively soft, clean, and brightly colored, had sharp
dactyls, and indicated that the crab had molted (prob-
ably) within the last 1-2 months; 2) hard-shell crab
had harder shells with some discoloration and scratch-
es but were still glossy and may have molted within
the last 6-12 months; 3) old-shell crab had lost their
glossy, reflective sheen, had numerous dark patch-
es, scratches, and dull dactyls, and probably had not
molted for 2 or more years; 4) very-old-shell crab were
much darker and discolored, indicating these crab had
not molted for 4-6 years.
Electronic calipers were used to measure different
dimensions of the crab. We used CL instead of CW as
our standard dimension of size, measured from the rear
margin of the right eyesocket to the rear midline of
the carapace. Carapace length is a more accurate mea-
surement because spines are usually included in CW,
and spines can wear down over time. In addition, we
redefined the width measurement between spine tips
as spine width (SW), as opposed to CW, which is often
measured across the carapace in front of the spines.
For comparative purposes, we also recorded SW for
48% and CW for 12% of the measured crab to allow
for conversions between them. Time constraints pre-
vented taking all measurements on all crabs, but ad-
ditional measurements were taken for a subset of the
sampled crabs that were systematically selected to fill
out size categories for reproductive studies. Additional
measurements included chela propodus length (ChL),
ChH (males only), abdomen width (AW) at the wid-
est point (females only), and presence and condition of
eggs (females).
Haefner (1977) reported that abrasion and discol-
oration (blackening) around the gonopores (which he
termed “vulvae”) of female red deepsea crab were indi-
cations of previous mating, and he demonstrated that
87% of 67 female red deepsea crab with open, discol-
ored gonopores contained sperm, whereas none of the
38 crabs with immature (closed) gonopores contained
sperm. Therefore, in 2012 and 2013, in our surveys
maturity of females was estimated on the basis of
gonopore condition; females with closed and unabraded
gonopores were classified as immature, whereas those
with open or discolored gonopores (or external eggs)
were considered mature.
Data analysis
For subsampled tows, the average weight of crab was
calculated separately for males and females, and the
proportion of each sex by weight was determined. Total
catch for each sex (Cggx) was calculated by multiplying
the total catch weight (Wt) by the weight proportion
(Pgex) dividing the result by mean weight (MWsex)
of each sex in the subsample:
Csex = Wt • Pg,x • MWgex-l •
Density of crab was calculated as the catch (total
number) of each sex divided by the area towed and
expressed as the mean number of crab-per hectare,
for comparison with results reported by Wahle et al.
(2008).
Because replicate tows were not made at each sta-
tion, density of each sex was compared separately be-
tween years, sites, and depth strata by using single-fac-
tor analysis of variance (ANOVA), and P-values <0.05
were considered significant. If factor effects were signif-
icant, pairwise comparisons were made with the Bon-
ferroni correction. Likewise, differences in mean size
(CL) were compared between sexes, sites, and depth
strata with a weighted ANOVA, where the sampling
factors were used as weights to account for unequal
subsampling. Weighting had little impact on post-hoc
pairwise comparisons; therefore, post-hoc comparisons
were unweighted. Proportions of male and female crab
within 0.5°C categories were also compared by using
ANOVA and a Kruskal- Wallis test.
Sex ratios were calculated after summing the catch
of crab in bins of 5 mm CL. Comparisons were made
between sites (with depths as replicates) because sites
were geographically separated. Red deepsea crab may
make seasonal vertical migrations for reproduction,
and crab at different depths would comingle; there-
fore, they were considered to represent a single local
mating pool. In most brachyuran species, males are
larger than females, and assortative mating is com-
mon: females pair with males up to 40% larger, as re-
ported for snow crab {Chionoecetes opilio; Sainte-Marie
et al., 1999) and southern Tanner crab (C. bairdi; Ste-
vens et al., 1993). Male red deepsea crabs in 10 mat-
ing pairs observed by Wahle et al. (2008) were 50%
larger than their female partners, and males in 3 mat-
ing pairs observed in another study were 28% larger
than their female counterparts (Elner et al., 1987).
Therefore, in our study, sex ratios were calculated be-
tween numbers of crab in offset size categories. Given
that the mean size of females was about 75 mm CL,
the number of females in each 5-mm bin was com-
pared with the number of males in bins that were 20
mm larger (e.g., number of females in the bin of 50-55
mm CL was compared with that of males in the bin of
70-75 mm CL).
Relationships between morphometric characters,
such as CL, ChL, ChH, and AW were determined for
selected crabs by using analysis of covariance, with sex
as a categorical factor. Data were linear and therefore
were not transformed, but the slopes of the log-trans-
formed relationships were calculated to determine the
allometry coefficient. The size at 50% maturity (SM50)
for females was calculated by using logistic regression
with maturity (0, 1; determined on the basis of gono-
pore condition) as the dependent variable, and CL as
the independent variable. Standard error (SE) of SM50
was calculated with a bootstrap analysis with 1000 rep-
etitions. Shell conditions and proportion of mature crab
with eggs were determined and plotted. All data analy-
sis was conducted with R, vers. 3.0.2 (R Core Team,
2013). Most mean values are presented with standard
deviations (SDs), and a few are noted with SEs.
348
Fishery Bulletin 1 14(3)
Table 2
Mean temperatures (°C), with standard deviations (SD) and results of analysis
of variance between years, from surveys of red deepsea crab {Chaecon quinque-
dens) conducted in the Mid-Atlantic Bight in 2011, 2012, and 2013. Results are
averaged across all trawl tows made at each site (Temps), weighted by numbers
of crabs caught (Tempe), and for females with eggs (Tempg). Also shown are
results of analysis of variance between years, including i^-value {F), probability
(P), and degrees of freedom (df).
Year and
results of
variance
Tows
Temps
Tempc
Tempe
Jan 2011
6
6.9 (SD 1.5)
6.41 (SD 0.96)
6.05 (SD 0.76)
Jan 2012
12
7.8 (SD 3.0)
6.07 (SD 1.10)
6.27 (SD 0.62)
Jul 2013
8
8.0 (SD 2.6)
6.71 (SD 1.11)
7.68 (SD 0.72)
Total
26
7.8 (SD 2.5)
6.37 (SD 1.09)
6.25 (SD 0.82)
E
0.361
44.48
26.08
P
0.701
<0.001
<0.001
df
2,23
2,2813
2,330
Results
Catch and density
During cruises of NOAA research vessels in 2011,
2012, and 2013, 26 deepwater tows were completed
for research of red deepsea crab (Table 1). One site
(BIG) was sampled only in 2012, whereas others were
omitted in some years (e.g., BWC in 2011), and not all
depths were sampled each year because of time con-
straints. Mean bottom temperatures at all sampled
stations did not differ significantly between years de-
spite sampling in January of 2011 and 2012 and in
July of 2013 (Table 2). Temperatures weighted by
number of crab captured differed significantly among
years, but the greatest differ-
ence was <0.7°C. Temperatures
at which ovigerous females oc-
curred also differed significantly
among years and temperatures
were warmer in July 2013 than
in January of either 2011 or 2012.
Although differences between sta-
tions were minimal, crab concen-
trated at specific depths in each
season, and, as a result, crab-
weighted temperatures showed
greater differences because of
changes in crab distribution.
During the 3 cruises combined,
5594 male and 10,627 female
crab were captured for a total of
16,221 crab, of which 2815 crab
(17.4%) were measured, including
1191 males (21.3% of males) and
1624 females (15.3% of females).
Highest mean densities occurred
in the middle slope depth stra-
tum (450-700 m; Table 3) for both males (131 indi-
viduals/ha) and females (300 individuals/ha), but dif-
ferences between sites were not significant (Table 3).
However, mean densities of male crab were signifi-
cantly greater in 2011 than in 2012 or 2013; a simi-
lar but nonsignificant decline occurred for females.
This difference remained even after removal of site
BIG (only sampled in 2012) and was mostly due to
samples at sites Hud and Nor. Estimates of biomass
density were calculated with mean weights from 13
subsampled tows and ranged from 0 to 241 kg/ha,
with a mean of 49.7 kg/ha (SD 69.6). Biomass aver-
aged across years was lowest at site BIG (14.7 kg/ha
[SD 13.1]) and highest at site BWG (77.4 kg/ha [SD
106.4]) (Table 4).
Table 3
Mean density (individuals/ha), with standard deviations (SDs), of red deepsea crab {Chaecon quinquedens) averaged across
depth strata, years, and sites sampled in the Mid-Atlantic Bight during 2011-2013. Analysis of variance results include
E-value (E), probability (E), and degrees of freedom (df). Superscript letters indicate similar groups (within columns) where
E<0.05. Sampling occurred at 3 depth strata, shallow (250-450 m), middle slope (450-700 m), and deep (700-850 m), at 4
sites. Block Island Canyon (BIC), Hudson Canyon (Hud), Baltimore and Washington Canyons (BWC), and Norfolk Canyon
(Nor).
Stratum
Male
Female
Year
Male
Female
Site
Male
Female
Shallow
18* (SD 30.7)
30* (SD 47.7)
2011
151“ (SD 114)
271 (SD 214)
BIC
32 (SD 35.6)
24 (SD 25.6)
Middle
131“ (SD 100)
300“ (SD 263)
2012
48* (SD 57.9)
101 (SD 229)
BWC
71 (SD 86.6)
250 (SD 358)
Deep
55* (SD 29.0)
19* (SD 6.6)
2013
37* (SD 47.6)
73 (SD 147)
Hud
81 (SD 98.2)
125 (SD 193)
Nor
55 (SD 61.4)
96 (SD 95.9)
Analysis of
variance
E
2.559
0.47
7.263
2.97
0.319
0.817
P
0.123
0.5
0.013
0.09
0.811
0.498
df
2, 23
2, 23
1, 24
1,24
3, 22
3, 22
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
349
Table 4
Total biomass density (kg/ha) of red deepsea crab (Chae-
con quinquedens) at each site and depth stratum sam-
pled in the Mid-Atlantic Bight during 2011-2013, and
summaries across sites and depth strata are provided.
Sampling occurred at 3 depth strata, shallow (250—450
m), middle slope (450-700 m), and deep (700-850 m),
at 4 sites. Block Island Canyon (BIC), Hudson Canyon
(Hud), Baltimore and Washington Canyons (BWC), and
Norfolk Canyon (Nor).
Depth stratum
Year
Site
Shallow
Middle
Deep
Mean
2011
Hud
39.8
126.8
105.1
2011
Nor
0
92.5
92.5
2012
BIC
0
18.9
25.2
14.7
2012
Hud
16.0
21.6
17.9
2012
BWC
0.0
241.4
17.9
86.4
2012
Nor
0.0
72.8
15.9
29.5
2013
Hud
0.0
0.0
9.7
3.2
2013
BWC
1.0
128.4
64.2
2013
Nor
32.0
25.3
29.8
Mean
13.6
95.6
18.8
47.4
Size of crab
Carapace length was measured on all sampled crabs
except for 133 crab from site BIC in 2012; for those
crab, CL was calculated from the regression of CL on
SW and used in all further analyses. The mean size
of male crab captured (79.4 mm CL [SD 14.7], range:
31.6-126.5 mm CL) was significantly greater (^=11. 62,
df=1974, F<0.0001) than that of female crab (73.7 mm
CL [SD 10.1], range: 26.5-103.6 mm CL). Mean size
of males differed between years (weighted F, Table 5)
and was lower in July 2013 (73.9 mm CL [SD 17.5])
than in January 2011 (80.5 mm CL [SD 10.6]) or 2012
(83.2 mm CL [SD 13.6]). Mean size of females also dif-
fered between years (weighted F, Table 5), but pairwise
comparisons among years were not significant. Lack of
sampling at some sites and depths prevented making
annual comparisons among all samples; therefore, fur-
ther comparisons were made by combining data across
years. Mean weights determined from 13 subsampled
tows (for which sexes were weighed in aggregate) were
294 g (SD 68) for males and 227 g (SD 71) for females.
Length-frequency distribution of males showed a
mode in the range of 80-90 mm CL, and a distinct drop
in abundance at sizes >90 mm CL (Fig. 2). Hard-shell
crab predominated below 70 mm CL, old-shell crabs
were more abundant from 75 to 100 mm CL, and most
crabs >100 mm CL were classified as very-old-shell.
Female crab exhibited a mode at 70-75 mm CL. Hard-
shell females predominated below 60 mm CL, and old-
shell females were more abundant in all size groups
above 60 mm CL.
Morphometries
Sex did not affect the relationship between CL and
SW; therefore, a combined regression equation was
derived for both sexes (Tables 5 and 6; Fig. 3A). The
inverse relationship was also determined and used to
predict CL for 133 crab that were missing CL measure-
ments. The relationship between ChL and CL differed
between sexes with a significant interaction (Table 5);
males had longer chelae at sizes >50 mm CL, but fe-
males had longer chelae below 50 mm CL (Fig. 3B).
Males had an allometry coefficient (the log-transformed
slope) of 1.09, indicating isometric growth, whereas fe-
males had an allometry coefficient of 0.862, implying
slight negative allometry. Among male crab, the rela-
tionship between ChH and CL had an allometry co-
efficient of 1.16, indicating slightly positive allometry
(Table 6, Fig. 3C), and the relationship between ChH
and ChL had an allometry coefficient of 1.06 (Fig. 3D).
Neither the relationship between ChL and CL nor the
relationship between ChH and ChL revealed any ap-
parent inflections in the growth pattern that could be
used to determine maturity. The relationship between
female AW and CL was significant but did not differ
with maturity status (Table 5). Nonetheless, there was
a significant interaction effect; therefore, combined and
separate equations for immature and mature females
are presented in Table 6.
Distribution by depth, temperature, crab size, and shell
condition
Females were more abundant than males at depths
from 400 to 650 m, but males predominated at great-
er depths (Fig. 4). Weighted ANOVA showed that size
varied with both depth and sex, and a significant in-
teraction occurred (Table 5). Mean CL of male crab de-
creased with depth: 83.1 mm CL (SD 13.7), 79.7 mm
CL (SD 11.6), and 78.2 mm CL (SD 17.9) in the shal-
low, middle slope, and deep strata, respectively (Fig.
5A). Mean CL for males differed significantly between
the shallow and deep strata (pairwise t-test, P<0.05
with Bonferroni correction), but the values for neither
strata differed from the middle slope stratum. Mean
CL of females also decreased with depth to a greater
degree than it did for males (Table 5, Fig. 5B): 80.6 mm
CL (SD 10.1), 73.8 mm CL (SD 9.1), and 67.0 mm CL
(SD 12.8) in the shallow, middle slope, and deep stra-
ta, respectively, and all differed significantly (P<0.05).
Mean CL of male crab did not differ between sites (Ta-
ble 5, Fig. 6C), whereas mean CL of female crab was
significantly greater at site Nor than at all other sites
(P<0.05; Fig. 6D).
Mean shell condition for males was significantly less
in stratum 1 (2.2) than in stratum 2 (2.6) or stratum 3
(2.5), but the latter 2 strata did not differ significantly
(Fig. 6A). Mean shell condition for females was signifi-
cantly greater in stratum 2 (2.8) than in either stra-
tum 1 or 3 (both 2.4), but strata 1 and 3 did not differ
significantly (Fig. 6B). New-shell male crab were most
350
Fishery Bulletin 114(3)
Table S
Analysis of variance results for comparisons among carapace length (CL), year, sex, shell width (SW),
chela propodus length (ChL), site, depth or stratum, shell condition, bottom temperature (Btemp),
abdomen width (AW), and maturity (females only) of red deepsea crab {Chaecon quinquedens) cap-
tured from the Mid-Atlantic Bight during 2011-2013. Other abbreviations: df=degrees of freedom,
SS=Sum of squares, MS=Mean square, F=F-value, P=P-value.
Response
Predictor
df
SS
MS
F
P
CL (males)
Year
1
5233
5233
6.67
0.01
Residual
1189
932,745
784
CL (females)
Year
1
19,286
19,286
33.88
<0.001
Residual
1622
923,249
569
SW
CL
1
427,647
427,647
52,382
<0.001
Sex
1
0
0
0.020
0.887
Residual
1313
10,719
ChL
CL
1
76,716
76,716
13,008
<0.001
Sex
1
3505
3505
594
<0.001
CL X sex
1
1555
1555
263
<0.001
Residual
321
1893
6
AW (females)
CL
1
19,761
19,761
5310
<0.001
Maturity
1
8.1
8.1
2.17
0.143
CL X maturity
1
20.2
20.2
5.43
0.021
Residual
179
666.2
3.7
CL
Depth
1
90,540
90,540
144
<0.0001
Sex
1
140,428
140,428
224
<0.0001
Sex X depth
1
24,764
24,764
39.4
<0.0001
Residual
2811
1,765,210
628
CL (male)
Depth
1
7915
7915
10.1
0.002
Residual
1189
930,063
782
CL (female)
Depth
2
35,721
17,861
31.9
<0.001
Residual
1621
906,814
559
CL (male)
Site
3
3644
1215
1.54
0.202
Residual
1187
934,334
787
CL (female)
Site
3
57,588
19,196
35.14
<0.001
Residual
1620
884,947
546
Shell (male)
Stratum
2
82.2
41.1
25.5
<0.001
Residual
1188
1911
1.61
Shell (female)
Stratum
2
103
51.6
33.2
<0.001
Residual
1621
2518
1.55
Btemp
Sex
1
31.4
31.4
6.02
0.014
Residual
2813
14,683
5.22
Btemp (female)
Eggs
1
362
362
75.4
<0.001
Residual
1406
6759
4.81
abundant in the shallow stratum (<450 m), whereas
new-shell females were most abundant in the deep
stratum (>700 m). Hard-shell male crab predominated
in the shallow and deep strata, whereas old-shell crab
predominated in the middle slope stratum. Hard-shell
female crab predominated in the shallow strata, where-
as old-shell females predominated in the middle slope
and deep strata.
Bottom temperatures at which crabs were captured
ranged from 4.6°C to 10.6°C, but mean temperatures dif-
fered by sex (Table 5). The mean temperatures at which
crab were captured were 6.27°C (SD 1.18) for males
(n=1191) and 6.45°C (SD 1.01) for females (n=1624).
Because these data were not normally distributed, a
Kruskal-Wallis analysis was conducted and also indi-
cated significant differences (x^=20.12, P<0.0001). Ovig-
erous females occurred at slightly colder temperatures
(6.25°C [SD 0.82]) than those temperatures at which fe-
males without eggs were found (6.59°C [SD 1.05]; Krus-
kal-Wallis test (%2=26.69, P<0.0001). Only 11 crabs were
caught at temperatures above 9.0°C; these crab were
captured in one sample at a temperature of 11.2°C and
Stevens and Guida: Biological paranneters of Chaceon quinquedens in the Mid-Atlantic Bight
351
depth of 288 m. There was no relationship between tem-
perature and size (CL) of male crab (F=0.833, coefficient
of determination [r2]= -0.0001, P=0.362, df=1189), but
size of female crab increased with temperature (F=31.3,
r2=0.018, P<0.001, df=1622).
Sex ratios (M:F) varied greatly both among sizes
and between sampling sites. For pairs in the smallest
size group for their sex (females: 55-60 mm CL; males:
75-80 mm CL) and in which females carried eggs, sex
ratios ranged from 2.1 to 3.6; however, for the interval
in which female sexual maturity occurs (60-65 mm CL),
ratios exceeded 1.0 only at sites BIC and Nor (Fig. 7).
For females between 70 and 80 mm CL, only site BIC
had a sex ratio >0.5, and ratios at all other sites were
<0.4. For females >80 mm CL, there were no sites or size
categories where sex ratios exceeded 0.1. At female sizes
above 60 mm CL, crab at sites BIC and Nor generally
had higher sex ratios than crab at sites Hud or BWC.
Female maturity and ovigerity
The smallest female with external eggs was 58.5 mm
CL. Logistic regression of maturity, based on gono-
pore condition, showed that the SM50 was 61.6 mm
CL (SE 0.1), equivalent to 78.2 mm SW (Fig. 8). In
January 2012, 33.3% of mature female crab
were ovigerous, and the maximum propor-
tion exceeded 50% only in the size group
of 95-100 mm CL (Fig. 9). In contrast, in
July 2013, only 5.9% of mature female crab
were ovigerous, and the maximum propor-
tion was 17.9% in the size group of 80-85
mm CL. Analysis of egg samples taken in
July 2013 indicated that 80% of eggs were
at stage 6 (prehatching or hatching stage),
whereas 20% of eggs were at stage 1 (early
cell division).
Discussion
Our results add significantly to previous
studies of red deepsea crab. Wigley et al.
(1975) sampled extensively off the southern
New England shelf but included only 2 sta-
tions off the Maryland coast, and all sites
sampled by Wahle et al. (2008) were north
of Delaware Bay (at approximately 38°40'N).
We sampled 2 sites (BWC and Nor) that were
farther south and that represent locations
that are targeted heavily by the current
commercial fishery. In addition, we captured
about 10 times more crabs than Wigley et
al. (1975) and twice as many as Wahle et
al. (2008), and we sampled twice as many
females as Haefner (1977). Our report is the
first to conduct detailed analysis of morpho-
metries of the red deepsea crab and the first
to provide detailed information on distribu-
tion by temperature and shell condition.
Catch and density
Tows made during our cruises were not optimized for
estimating abundance of red deepsea crab because the
net was not outfitted with mensuration gear to mea-
sure the net width or bottom contact. As a result, area
towed was estimated on the basis of the operator’s
(subjective) estimate of contact time, distance towed,
and average net width. Furthermore, differences in
vessel characteristics, operational protocols, and net
efficiency make any direct comparisons with previous
surveys questionable. The trawl nets we used had a
belly mesh of 6 cm and smaller mesh codend liners
than those in nets with 3.8-cm mesh used by Wigley
et al (1975) and Wahle et al (2008), but all trawl nets
caught a similar size range of crab and few crab <50
mm SW. Nonetheless, because there are no other esti-
mates of density of red deepsea crab, our data can be
compared with previous estimates in a relative context.
Two of our sites (Hud and BWC) overlap with the
area defined as “geographic zone A” by Wigley et al.
(1975) (referred to as “sectors” by Wahle et al [2008]).
Therefore, we estimated biomass density of red deepsea
crab separately within each depth stratum over those 2
352
Fishery Bulletin 114(3)
Figure 3
Morphometric relationships for a subsample of 185 male and 138 fe-
male red deepsea crab (Chaceon quinquedens) captured in the Mid-
Atlantic Bight during 2011-2013: (A) carapace width with spines
(spine width) versus carapace length, (B) chela length versus carapace
length, (C) male chela height versus carapace length, and (D) male
chela height versus chela propodus length.
sites (12.6, 107.5, and 13.8 kg/ha, respec-
tively), and we multiplied those values by
area estimates for similar depth strata
within the same geographic sector from
Wahle et al. (2008) to provide a depth-
stratified estimated biomass of 9143 t
for sector A. This value was lower than
the approximately 30,000 t estimated by
Wahle (2008) during 2003-2005, but it is
almost identical to the 9000 t estimated
by Wigley et al. (1975) 20 years earlier.
We could not separate biomass by sex or
size because crab were usually weighed
in aggregate. During the survey by Wahle
et al. (2008), the highest biomass densi-
ties occurred in sectors C and D along the
edge of the southern New England shelf,
whereas most of our tows were made in
sectors A and B, which had the lowest
biomass in both the 1974 and 2003-2005
surveys. Mean biomass density over all
our stations (42.8 kg/ha) was in the same
range (7-80 kg/ha) as levels observed for
C. maritae off Namibia (Hastie, 1995),
but it was much greater than the 1.9 kg/
ha calculated for the golden deepsea crab
off the coast of South Carolina (Wenner
and Barans, 1990) that were surveyed
with an occupied submersible.
Size of crabs
Selectivity of commercial crab traps
ranges from 0% at 80 mm CW to 100%
at 120 mm CW (Wahle et al., 2008),
Table 6
Morphometric relationships for male and female red deepsea crab (Chaecon quinquedens)
captured from the mid-Atlantic Bight during 2011-2013. Response and predictor variables
are, abdomen width (AW), chela propodus length (ChL), carapace length (CL), spine width
(SW). Fem(i or m) refers to immature or mature females. Other abbreviations: intercept (Int),
coefficient of determination (r^), degrees of freedom (df), and allometry coefficient (AC; slope
of log-transformed relationship).
Sex
Response
Predictor
Int
Slope
r2
df
AC
Both
SW
CL
5.45
1.180
0.976
1313
0.94
Both
CL
SW
-2.65
0.826
0.976
1313
1.03
Male
ChL
CL
-5.78
0.962
0.977
184
1.09
Fern
ChL
CL
7.55
0.671
0.952
137
0.86
Fem(i)
AW
CL
-13.0
0.735
0.967
105
1.40
Fem(m)
AW
CL
-8.38
0.677
0.937
74
1.19
Fem(all)
AW
CL
-12.26
0.725
0.966
182
Male
ChH
CL
-3.52
0.362
0.954
184
1.16
Male
ChH
ChL
-1.44
0.378
0.983
184
1.06
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
353
equivalent to a range of 63.4-96.5 mm CL,
and the median size of crab captured by traps
was 92.5 mm CW, or 73.8 mm CL. Therefore,
abundance of males declines abruptly above 90
mm CL, which approximately corresponds with
the minimum size captured by the fishing in-
dustry. Width frequencies of crab captured by
Wahle et ai. (2008) during 2003-2005 showed
a mode in the range of 65-75 mm CW (equiva-
lent to 51-59 mm CL) for males and in the
range of 95-105 mm CW (76-84 mm CL) for
females. In contrast, male red deepsea crab
captured during our study were larger, with a
mode in the range of 80-90 mm CL, whereas
females were slightly smaller, with a mode at
70-75 mm CL.
Differences in mean size of male and fe-
male red deepsea crab (79.4 and 73.7 mm
CL, respectively, equivalent to 99.1 and 92.4
Depth (m)
Figure 4
Depth distribution of male and female red deepsea crab (Cha-
ceon quinquedens) captured during 2011-2013 in the Mid-Atlan-
tic Bight, expressed as density or number of crab per hectare
(ha). Minimum depths are shown for each 50-m depth bin.
C)
c
_Q)
(D
O
ra
D.
CO
CD
o
B
8
la
lb
1 1 1
250-450m 450-700m 700-850m
Depth (m)
Mean size of red deepsea crab (Chaceon quinquedens) sampled during 2011-2013
at 3 depth strata (years and sites combined) for (A) males and (B) females and at
4 sites (years and depth strata combined) for (C) males and (D) females. Letters
indicate similar groups within frames. The 4 sites in the Mid-Atlantic Bight were
Block Island Canyon (BIC), Hudson Canyon (Hud), Baltimore and Washington Can-
yons (BWC), and Norfolk Canyon (Nor)
354
Fishery Bulletin 114(3)
A B
o o
250-450m 450-700m 700-850m 250-450m 450-700m 700-850m
Depth strata
Figure 6
Proportion of (A) male and (B) female red deepsea crab (Cha-
ceon quinquedens) in each of 4 categories of shell condition at
3 depth strata sampled in the Mid- Atlantic Bight during 2011—
2013 (years and sites combined). Shell conditions are new (light
gray), hard (medium gray), old (dark gray), and very old (black).
mm SW) have been previously noted (McRae, 1961;
Haefner, 1978; Weinberg and Keith, 2003). According
to McRae (1961), mean weights for a “random sam-
ple” of crabs were 794 g for males, and
312 g for non-ovigerous females, equiva-
lent to sizes of 116.4 mm CL and 88.4
mm CL, respectively, or 144.2 and 110.2
mm SW (converted with the equation
for CW from Weinberg and Keith, 2003).
The source of this sample was not de-
scribed, but presumably it was near
our sampling area. Therefore, either
mean size of red deepsea crab has de-
clined significantly since McRae’s study
in 1960, or his random sample was bi-
ased toward large crab. The mean size
of male crab reported by McRae (1961)
was 31% larger than the mean size of
females. This difference is similar to the
mean size differential of 27.9% report-
ed by Elner et al. (1987) for 3 pairs of
crab (involving 2 males and 2 females)
observed mating in captivity, but it is
smaller than the differential of 50%
between 10 mating pairs observed by
Wahle et al. (2008) during tows with
video cameras. Although sample sizes
for the latter 2 studies were small, they
indicate that the relative size of male
and female crabs observed by McRae
(1961) offered adequate opportunities
for mating.
Sex ratios are commonly used to deter-
mine whether fishing has affected a crab
population, but they are usually calculated
over large geographic areas. However, function-
al maturity (i.e., the ability of male crabs to
mate in competitive, natural environments) is
dependent on both size (Paul, 1984) and shell
condition (Stevens, et al., 1993) because harder
shells are necessary to grasp females and de-
fend them from other males. As a result, the
effective sex ratio of mating-capable partners
may vary greatly over small geographic areas.
For this reason we calculated effective sex ra-
tio only within sampling sites, where the sam-
ples were geographically close, and these ratios
were calculated between abundance of females
in 5-mm-CL bins and abundance of males that
were 20 mm CL larger. We also ignored shell
condition and depth because both could change
between the time sampled and mating season,
and we did not include year effects in order to
preserve adequate sample sizes.
Sex ratios were generally biased toward
males in the smaller size intervals, but for
intervals larger than the SM50 for female red
deepsea crab, all ratios were <0.7, and many
ratios were much lower. These data indicate
that male mating partners for females be-
come exceedingly scarce as females grow. Mating of
male crab with multiple females has been observed
for red deepsea crab (Elner, et al., 1987), southern
(M
X
0)
CO
75.55 80.60 85.65 90.70 95.75 100.80 105.85 110.90 115.95 120.100
Minimum size (mm CL) of pairs (M,F)
Figure 7
Sex ratio (M:F) of red deepsea crab (Chaceon quinquedens) at each
of 4 sites sampled in the Mid-Atlantic Bight during 2011-2013, com-
pared by offset 5-mm categories, for pairs in which the minimum size
of males is 20 mm in carapace length (CL) greater than the minimum
size of females. Missing bars indicate either a lack of males or females
in one category. The 4 sites were Block Island Canyon (BIC), Hudson
Canyon (Hud), Baltimore and Washington Canyons (BWC), and Nor-
folk Canyon (Nor)
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
355
Figure 8
Proportion of female red deepsea crab (Chaceon
quinquedens) that were mature (as defined by presence
of eggs or condition of the gonopores) in each size group
classified in intervals of 5 mm in carapace length [CL]
(circles) and predicted maturity from logistic regression
(line). The estimated size at 50% maturity (SM50) was
61.57 mm CL
Tanner crab (Paul, 1984), and snow crab (Rondeau
and Sainte-Marie, 2001). Male southern Tanner crab
may mate with as many as 10 partners, but usu-
ally with less than 5 (Paul, 1984). Guarding time
and the amount of sperm transferred by male snow
crabs declines with sex ratio because males try to
conserve sperm and, therefore, may leave
females with inadequate supplies to fertil-
ize a clutch of eggs (Rondeau and Sainte-
Marie, 2001). Blue crab (Callinectes sapi-
dus) show a marked decline in the rate
of courtship initiation at sex ratios below
2 (Jivoff and Hines, 1998). The minimum
sex ratio for successful fertilization of all
females in a crab population is unknown,
but may lie between 0.1 and 0.5; a con-
servative estimate would be 0.25, indicat-
ing that most females above the mean size
in our study do not have access to an ad-
equate number of males.
The crab in our study were considerably
smaller than C. affinis from the Canary
Islands (mean sizes of males and females
were 130 and 120 mm CW) (Fernandez-Ver-
gaz et al., 2000) or the Azores (107 and 91
mm CL) (Pinho et al., 2001); however, crab
in the Canaries and Azores were captured
by traps, which are highly size selective;
only 3 crab <80 mm CW were caught by
Fernandez-Vergaz et al. (2000).
Morphometries
Sexual maturity in our sample of red deepsea crab can-
not be inferred from morphometric characteristics. A
variety of methods have been proposed for determin-
ing the maturity of crabs. Somerton (1980) described
a computer technique that determined SM50 for male
crabs by fitting morphometric data with a logistic re-
gression. He defined 4 patterns of allometric growth,
based on the relationship between chela and carapace
measurements, and applied those relationships to de-
termine size at sexual maturity for male snow crab
in the Bering Sea (Somerton, 1981) and later for blue
king crab (Paralithodes platypus', Somerton and Ma-
cintosh, 1983). Allometric patterns in species of Chi-
onoecetes are curvilinear, and variation increases with
size, but patterns become linear when log-transformed.
The slope of the log-transformed relationship is defined
as the allometry coefficient.
The relationship between ChL and CL for our male
red deepsea crab was linear, did not show increased
variance with size, and did not require transformation.
It has an allometry coefficient of 1.09, indicating iso-
metric growth and has no inflection point that could
be used to define the onset of sexual maturity. The
relationship between ChL and CL for female crabs,
however, indicated clear sexual dimorphism and was
negatively allometric. The relationship between male
ChH and CL was also isometric, with an allometry co-
efficient of 1.06. Similar to that of males, the relation-
ship between female AW and CL was linear, had no
apparent inflexion point corresponding to maturity, and
did not differ between maturity types.
Similar results were obtained for C. affinis in the
Azores; no inflections were found in the relationships
between CL and CW, ChW (height), or female AW, and
CO
30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105
Carapace length (mm)
Figure 9
Proportion of mature female red deepsea crab (Chaceon quinque-
dens) with external eggs and captured in the Mid-Atlantic Bight in
January 2012 and July 2011. Each size group is classified by inter-
vals of 5 mm in carapace length (CL). Maturity was not recorded
in 2011.
356
Fishery Bulletin 114(3)
male:female dimorphism was present in the chelae but
not in CW (Pinho et ah, 2001). In contrast, allometric
relationships for ChL and ChW in C. affinis from the
Canary Islands were strongly positive (approximately
1.3-1. 5) and were used in hierarchical cluster analysis
to distinguish immature from mature individuals of
both sexes (Fernandez-Vergaz et ah, 2000). Logistic re-
gression of these crab indicated SM50 values of 129 mm
CW for male C. affinis — a size that would be equivalent
to 103 mm CL for red deepsea crab if converted with
the regression of CL on SW for the latter (Fernandez-
Vergaz et ah, 2000).
Determination of sexual maturity on the basis of
morphometries works well for crabs of the families Or-
egonidae {Chionoecetes spp.) and Majidae. The spider
crab (Maja hrachydactyla) shows a typical curvilinear
relationship between CL and ChH that becomes linear
upon log-transformation, and Corgos and Freire (2006)
used discriminant analysis to separate immature and
mature male clusters. Their data were fitted even bet-
ter by a 3-stage growth model, which included an in-
flection point between juveniles and adolescent males.
Therefore, excluding one study on C. affinis, morpho-
metric relationships have not proved useful for deter-
mining sexual maturity in the genus Chaceon.
Distribution by depth and temperature
At our sampling sites, highest abundance of red deep-
sea crab occurred at depths between 500 and 650 m,
and few crab were captured at depths <400 m. Female
red deepsea crab dominated catches taken at depths
shallower than 600 m, and males were more prevalent
at greater depths. Haefner et al. (1974) reported that
the highest abundance occurred at depths between 265
and 512 m, and they observed that females dominated
trawl catches above 400 m in and near Norfolk Canyon
but that males became dominant below 400 m.
Our data show a slight but significant decline in size
of crab with increasing depth — a drop that was much
more apparent for females. This decline in size is con-
sistent with other reports that indicate that juvenile
red deepsea crab are more common at greater depths
(Wahle et al., 2008). We also found that the proportion
of males increased with depth. Off the Namibian coast,
C. maritae (misidentified as C. quinquedens) show simi-
lar depth ranges; females predominate above 400 m at
temperatures of ~8°C and males are more abundant
down to 900 m and 4°C (Beyers and Wilke, 1980; as
cited by Melville-Smith, 1989). In contrast, Kilgour
and Shirley (2008) caught red deepsea crab by traps
at depths of 533 to 1950 m in the Gulf of Mexico but
found no significant relationships between depth and
crab size or sex. Pinho et al. (2001) caught C. affinis
with traps around the Azores Islands and found that
the highest abundance occurred at depths between 700
and 900 m. In that study, size of both sexes decreased
slightly with increasing depth, but the proportion of
males declined with increasing depth, in contrast to
our results.
Despite differences in depth distribution observed
for red deepsea crab in our surveys, the differences in
temperature distribution by sex were minor, and much
overlap occurred between males and females. Simi-
larly, differences in bottom temperature between years
were minor despite sampling in either January or July,
and differences weighted by crab catch were even less.
These data indicate that temperatures at the depths
sampled do not show great annual variation, and red
deepsea crab tend to stay within a narrow range of pre-
ferred temperature. This information indicates that red
deepsea crab recruit as juveniles to waters deeper than
those sampled, move upslope during development, and
become mature in the shallowest zones, after which
they undergo an ontogenetic migration back to inter-
mediate depths.
Female maturity and ovigerity
Our estimate of SM50 for female red deepsea crab (61.6
mm CL) was calculated by nonlinear logistic regression;
therefore, a point estimate was possible. Haefner (1977)
estimated female maturity on the basis of the relation-
ship of AW to CL for females classified as mature or im-
mature by gonopore condition, and he determined that
maturity occurred over a size range of 65-75 mm CL.
Haefner (1977) calculated 2 separate regression equa-
tions for females with mature or immature gonopores
(total 71=251) for the relationship between AW and CL
that had similar slopes but different intercepts. How-
ever, the equation for immature females was influenced
by 3 extremely small crab. Likewise, AW of C. affinis
has been reported to change in intercept at maturity,
between 95 and 105 mm CW (equivalent to 76-84 mm
CL) (Fernandez-Vergaz et al., 2000).
In contrast, covariance analysis of our data did not
support the hypothesis that the 2 relationships were
different, and there were no extreme outliers (total
number of females analyzed=182). Abdomen morphom-
etry indicated that C. affinis females become function-
ally mature (i.e., capable of bearing eggs) before reach-
ing physiological maturity (which is assessed on the
basis of apparent ovarian stage) (Fernandez-Vergaz et
al., 2000). Logistic regression indicated SM50 values of
108 mm CW (equivalent to 86.6 mm CL) for abdominal
maturity and 113.4 mm CW (91 mm CL) for gonopore
maturity of crab in the Canary Islands (Fernandez-
Vergaz et al., 2000), whereas the SM50 for female red
deepsea crab in the Azores determined by gonopore
condition was 83.1 mm CL (Pinho et al., 2001).
The presence of eggs on <50% of female crabs is a
strong indicator that reproduction occurs at biennial
(or longer) intervals. Haefner (1977) examined female
red deepsea crab from the Norfolk Canyon, and report-
ed that only 25.5% of females >71 mm CL were oviger-
ous in January 1976. He also reported that abraded
gonopores were present in 93.5% of female red deepsea
crab >71 mm CL but not in any crab <70 mm CL. In
the Azores, ovigerous C. affinis were found only in the
fourth and first quarters of the year, with a maximum
Stevens and Guida: Biological parameters of Chaceon quinquedens in the Mid-Atlantic Bight
357
of 33% ovigerous crab. Lack of annual mating for red
deepsea crab was previously hypothesized by other au-
thors (Weinberg and Keith, 2003). Female C. maritae in
South Africa were also reported to have asynchronous
molting and aseasonal reproductive cycles (Melville-
Smith, 1989).
Reproductive cycles >1 year may occur among crabs
living at extremely low temperatures. Blue king crab
in the Bering Sea living at temperatures ranging from
-1°C to 4°C reproduce biennially (Somerton and Ma-
cintosh, 1985; Jensen and Armstrong, 1989; Stevens
et al., 2008), and approximately 50% of females bear
fertilized embryos each spring. Female snow crab re-
produce biennially in the Gulf of St. Lawrence at tem-
peratures <1.0°C and have only 2 broods over their
reproductive lifespan (Moriyasu and Lanteigne, 1998;
Comeau et al., 1999), whereas snow crab living at high-
er temperatures (and greater depths) reproduce annu-
ally, potentially producing 4 lifetime broods (Kuhn and
Choi, 2011).
Switching from biennial to annual reproduction can
potentially halve or double lifetime reproductive output,
depending on direction of change (Webb et al., 2007). A
change of only 1°C can advance or delay hatching of
red king crab (Paralithodes camtschaticus) by about 2
weeks, possibly contributing to year class failure from
a mismatch between larval hatching and food sources
(Stevens et al., 2008). Other crabs with reproductive
cycles longer than 1 year include the golden king crab
{Lithodes aequispinus) and others that live at depths
>500 m and produce lecithotrophic larvae (Shirley and
Zhou, 1997; Paul and Paul, 2001). Biennial spawning
has been reported only for crab species living at tem-
peratures <4°C, and for those with lecithotrophic lar-
vae, but has not been reported for crabs with plankto-
trophic larvae living at temperatures >6°C. Therefore,
crabs of the genus Chaceon are unusual in this respect.
The extremely low proportion of egg-bearing females
and the advance stage of egg development observed in
July 2013 indicate that hatching was nearly completed
at that time, and some crab bore newly fertilized eggs
in very early developmental stages. These observations
indicate that hatching and ovulation events are sepa-
rated by a time interval, possibly up to a year in red
deepsea crab (Brachyura). This separation of events is
in contrast with the reproductive strategy of red king
crab (Anomura), which molt, mate, and extrude a new
clutch of eggs within hours after releasing larvae (Ste-
vens and Swiney, 2007). All species of king crab lack
the ability to store sperm, however, and, as a result,
comparisons to brachyurans are more appropriate.
Snow crab (Brachyura) can store sperm, and multipa-
rous crab may use stored sperm to produce additional
clutches of eggs; however, those crab that re-mate must
do so within 4-7 days after releasing larvae in order
to produce viable clutches (Paul and Adams, 1984).
Therefore, it appears that red deepsea crab differ from
species of Chionoecetes in their ability to separate the
process of larval release (and presumably mating) from
that of ovulation and fertilization.
The current fishery for red deepsea crab is expand-
ing into the southern portion of the Mid-Atlantic Bight,
including the Norfolk and Washington Canyon areas.
This expansion is a result of changing abundance, as
well as of changes in the availability of processing fa-
cilities close to fishing grounds (Williams'^). Therefore,
the population targeted by the fishery is different from
that fished 20 years or even 10 years previously. The
results of this study lay a foundation for other syn-
optic studies on red deepsea crab in the Mid-Atlantic
Bight. As we went to press (May 2016), we were con-
tinuing our work with red deepsea crab, analyzing tis-
sue samples from crab collected during the cruises in
2011-2013, as well as from samples collected aboard
commercial fishing vessels in 2014 and 2015. The re-
sults of this further analysis should reveal more details
about the biology of the red deepsea crab, including
size at maturity, reproductive cycles, fecundity, and em-
bryonic and larval development.
Acknowledgments
This research was conducted with partial funding
from the NOAA Living Marine Resources Cooperative
Science Center, NOAA grant NA11SEC4810002. We
gratefully acknowledge the assistance of the officers
and crews of the NOAA Ships Delaware II and Gordon
Gunter. We also appreciate the efforts of student par-
ticipants on all 3 cruises, who were too numerous to
name individually; still, major assistance to this proj-
ect was provided by B.-J. Peemoeller, A. Stoneman, and
I. Suyuheda. We thank R. Langton for his service as co-
chief scientist in 2013 and to S. Smith and S. Van Sant
for their participation as watch supervisors during the
2012 and 2013 cruises, respectively. Comments from L.
Stehlik and anonymous reviewers helped improve the
manuscript.
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360
NOAA
National Marine
Fisheries Service
Fishery Bulletin
fb- established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
Is the sunrey selectivity curve for Pacific cod
iGadus macrocephalus} dome-shaped?
Direct evidence from trawl studies
Email address for contact author: cynthia.yeung@noaa.gov
’ Resource Assessment and Conservation Engineering Division
Alaska Fisheries Science Center
National Marine Fisheries Service, NOAA
7600 Sand Point Way NE
Seattle, Washington 98115
2 Resource Ecology and Fisheries Management Division
Alaska Fisheries Science Center
National Marine Fisheries Service, NOAA
7600 Sand Point Way NE
Seattle, Washington 98115
Abstract — Survey selectivity can be
viewed as a function of the availabil-
ity of the stock to the sampling gear
and the sampling efficiency of the
gear. A dome-shaped survey selectiv-
ity function is one in which survey
selectivity decreases with larger and
older fish. Such a function is esti-
mated for eastern Bering Sea (EBS)
Pacific cod (Gadus macrocephalus) in
the NOAA National Marine Fisher-
ies Service stock assessment model,
which would be appropriate if large
(>55 cm in fork length) Pacific cod
avoid capture by the EBS survey
bottom trawl. To test this assump-
tion, a field study was conducted to
determine whether large Pacific cod
escape capture by either outswim-
ming the survey trawl or by swim-
ming above the trawl. Our results
show that large Pacific cod do not
outswim the trawl because catches
did not increase when we increased
towing speed. Additionally, large Pa-
cific cod do not routinely swim above
the trawl because analysis of acous-
tic backscatter collected concurrent-
ly with trawl hauls indicated that
only 4% of the acoustic backscatter
attributed to Pacific cod occurred
at heights above the headrope. We
found no evidence that survey-gear
efficiency decreased with increasing
fish length either because large fish
outswam the trawl or because they
tend to occur further from the bot-
tom. Therefore the results of our
experiment do not support the use
of a dome-shaped survey selectivity
function in the EBS Pacific cod as-
sessment model.
Manuscript submitted 16 June 2015.
Manuscript accepted 20 May 2016.
Fish. Bull. 114:360-369 (2016).
Online publication date: 14 June 2016.
doi: 10.7755/FB.114.3.8.
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Kenneth L. Weinberg’
Cynthia Yeung (contact author)’
David A. Somerton’
Grant G. Thompson^
Patrick H. Ressler’
Fisheries stock assessment surveys
are intended to produce an index of
relative stock abundance that varies
over time in constant proportion to
the true stock abundance. In stock
assessment models, the scaler that
relates modeled abundance to a sur-
vey index is often considered a prod-
uct of a constant catchability and of
a fish age- or length-dependent sur-
vey selectivity function (which, here-
after, for reasons of simplicity, we re-
fer to as length-dependent functions,
but the same concept applies to age-
dependent functions). Both catch-
ability and selectivity are typically
estimated when a stock assessment
model is fitted to data (Maunder and
Finer, 2015), although, in some cases,
the catchability coefficient is fixed a
priori (Thompson’’^’^). The selectiv-
’ Thompson, G. G. 2013. Assessment of
the Pacific cod stock in the eastern Ber-
ing Sea. In Stock assessment and fish-
ery evaluation report for the groundfish
ity of a survey can be viewed as a
function of the availability of the
various biological components of the
fish stock to the sampling gear and
of the sampling efficiency of the gear
(i.e., the proportion of encountered
animals that are captured; Maunder
et ah, 2014). However, the relative
resources of the Bering Sea/Aleutian
Islands regions, p. 239-380. North Pa-
cific Fishery Management Council, An-
chorage, AK. [Available at website.]
2 Thompson, G. G. 2014. Assessment of
the Pacific cod stock in the eastern Ber-
ing Sea. In Stock assessment and fish-
ery evaluation report for the groundfish
resources of the Bering Sea/Aleutian
Islands regions, p. 255-436. North Pa-
cific Fishery Management Council, An-
chorage, AK. [Available at website.)
^ Thompson, G. G. 2015. Assessment of
the Pacific cod stock in the eastern Ber-
ing Sea. In Stock assessment and fish-
ery evaluation report for the groundfish
resources of the Bering Sea/Aleutian
Islands regions, p. 251-470. North Pa-
cific Fishery Management Council, An-
chorage, AK. [Available at website.)
Weinberg et al.: Survey selectivity for Gadus macroceph
361
0 -I ' 1 ' 1 ' 1 ' 1 ' 1 ' 1
0 20 40 60 80 100 120
Length (cm)
Figure 1
Length-based survey selectivity curve derived from the
stock assessment of Pacific cod (Gadus macrocephalus)
for the Bering Sea region in 2013. Lengths are given
in fork lengths.
importance of availability (e.g., Do small fish occur at
depths shallower than those of surveys?) and sampling
efficiency (e.g., Do small fish pass through trawl mesh?)
in determining the shape of a selectivity function is
difficult to determine without additional information.
The shape of the survey selectivity function is at
issue for the model used for stock assessment of Pa-
cific cod (Gadus macrocephalus] Thompson^’^’^) in the
eastern Bering Sea (EBS). The assessment model, con-
ducted with the Stock Synthesis package, vers. 3.24q
(Methot and Wetzel, 2013), is fitted to commercial
catch data dating back to 1977, as well as to fisheries-
independent data from the National Marine Fisheries
Service annual bottom trawl survey of demersal fishes
in the EBS (hereafter referred to as the survey). The
survey provides estimates of relative abundance and
length compositions dating back to 1982 and age com-
positions from 1994 onward (Lauth and Nichol, 2013).
The current assessment model accepted by the
NOAA National Marine Fisheries Service for fishery
management, in addition to several historical model
configurations, includes a flexible survey selectivity
function that, after being fitted to the data, decreases
at larger (>55 cm in fork length [FL]) fish sizes (Thomp-
goni-2,3; pjg This dome-shaped functional form has
rising and descending limbs to either side of the top.
The descending limb on the right side suggests that
larger fishes are less vulnerable to the survey in some
way, perhaps because they are better able to escape the
trawl or are separated spatially from smaller fishes.
In contrast, the more traditional asymptotic, survey
selectivity function implies that the survey is sampling
a greater proportion of the large fishes in the popula-
tion. If an assessment model is not well informed hy
the data, there will be uncertainty about whether the
shape of the estimated function accurately reflects the
survey sampling processes or whether it reflects pa-
rameter confounding in the model (Maunder and Punt,
2013). The difference between interpretations of the
shape of the estimated function with regard to these
2 types of uncertainty may have a pronounced effect
on the determination of stock size and recommended
harvest rates.
Field studies designed to describe survey-gear effi-
ciency and stock availability provide a source of “di-
rect” evidence and can be useful in the fitting of the
selectivity function (Cadrin et al., 1999; Weinberg et
al., 2004; Clark and Kaimmer, 2006; Nichol et al., 2007;
Somerton et ah, 2007; Somerton et al., 2013). We pres-
ent the results from a new study and review results
from previous works to determine whether direct evi-
dence from field studies corroborates the dome-shaped
survey selectivity function estimated by the current as-
sessment model used for Pacific cod. Although we focus
on Pacific cod, the concept that field experiments can
better inform assessment models is applicable world-
wide for multiple species.
If it is assumed that the survey covers the entire
geographic range of Pacific cod in the EBS, a dome-
shaped selectivity function could result from a progres-
sive decrease in trawl sampling efficiency for larger fish
sizes. Sampling efficiency is dictated by 3 processes:
vertical herding, horizontal herding, and escapement,
all of which are dependent on trawl design, fishing pro-
cedures, fish behavior, and swimming endurance. To-
gether, these processes play an important role in esti-
mates of abundance and size composition of groundfish
resources (Godp and Walsh, 1992).
Although studies on the behavior of Pacific cod are
scarce, evidence has been collected from various field
and laboratory experiments on other cold-water gadids
and various demersal species, clearly showing that fish
swimming stamina and reactions to trawling are spe-
cies specific (He and Wardle, 1988; Winger et al., 1999),
size dependent (Main and Sangster, 1981; He and War-
dle, 1988; Winger et al., 1999), temperature affected
(He, 1991; Winger et al., 1999), light responsive (Glass
and Wardle, 1989; Walsh, 1991), and often density de-
pendent (God0 et al., 1999; Kotwicki et al., 2014). Not
all studies have come to the same conclusions for all
species, or even within the same species in all cases,
but the most universal observation is the inverse re-
lationship between swimming speed and endurance.
The faster a fish swims, the more energy required and
the less time it is capable of sustaining such speed. If,
however, a fish is able to swim fast enough and long
enough to outpace a survey trawl, sampling efficiency
will be reduced. Likewise, if large Pacific cod, more so
than smaller Pacific cod, have the strength and stami-
na to outswim the survey trawl, survey selectivity will
be reduced for the larger animals.
In addition to the possibility that larger Pacific cod
avoid capture by outswimming the trawl, it is also pos-
sible that larger Pacific cod occur higher in the water
column and are more likely to swim over the headrope
of the survey trawl. The presence of fish in the wa-
ter column can be documented by using acoustic data
collected at the time of trawling. Analysis of acoustic
362
Fishery Bulletin 114(3)
data to estimate abundance has not been attempted for
Pacific cod because of concerns stemming from the con-
founding of backscatter signals close to the seabed (i.e.,
separating the weaker fish signal from the stronger
seabed signal), in the area known as the acoustic dead-
zone (Ona and Mitson, 1996), and from the difficulty of
separating species-specific backscatter when multiple
species with swim bladders, such as Pacific cod and
walleye pollock (Gadus chalcogrammus), co-occur.
Our objective was to report the results of an ex-
periment aimed at examining whether survey trawl
efficiency decreases for large-size Pacific cod because
they outswim the trawl or because they pass over its
headrope. If such size-specific trawl efficiency can be
demonstrated, it would support the application of a
dome-shaped function in the stock assessment model
for Pacific cod.
Materials and methods
Experimental design
Our experiment was designed to test the hypothesis
that a substantial proportion of large Pacific cod avoid
capture by outswimming the survey trawl under stan-
dard survey protocols (Stauffer, 2004). Secondarily, we
were also able to provide a test of the hypothesis that a
substantial proportion of Pacific cod are unavailable to
the trawl because they are in the water column above
the headrope of the survey trawl. A Pacific cod was con-
sidered large if its FL was >55 cm, a definition based
on lengths at the right tail of the selectivity schedule
estimated in the 2013 stock assessment of EBS Pacific
cod (Thompson^), for which estimated survey selectivity
was less than 100.0 percent (Table 1, Fig. 1).
The experiment took the form of paired parallel
tows: one vessel trawled at the survey standard speed
of 1.5 m/s (3 kn, slow), while the other vessel towed at
a faster speed of 2.1 m/s (4.0 kn, fast). Various Bering
Sea fishermen of Pacific cod have reported tow speeds
that range from 1.25 to 2.25 m/s (2. 5-4. 5 kn), depend-
ing on vessel power, mesh size, and other trawl design
features (senior author, personal commun.). We felt the
upper limit for towing the survey trawl should be no
more than 2.1 m/s in order to maintain proper fishing
configuration (Weinberg, 2003). At such a speed, we
were 0.15 m/s short of the fastest speeds for commer-
cial trawling. If the number of large Pacific cod cap-
tured in the standard slow tows is no different from
the number caught in the faster tows, we would con-
clude that Pacific cod did not outswim the survey trawl.
Field operations
The experiment was conducted during 3-5 August im-
mediately following the 2013 NOAA EBS bottom trawl
survey aboard the 2 trawlers used for the survey. An
83-112 eastern trawl (standard for the EBS survey)
was used in this experiment. The 83-112 eastern trawl
Table 1
Survey selectivity (rounded to one decimal place) by
length group based on the length-based schedule of
the 2013 assessment model used for Pacific cod (Gadus
macrocephalus) in the eastern Bering Sea. Ranges for
length groups are provided in fork lengths (FLs).
Survey selectivity Length group (cm FL)
1.0
34-54
0.9
55-60
0.8
61-65
0.7
66-69
0.6
70-74
0.5
75-79
0.4
80-88
0.3
89-105
is a 2-seam flatfish trawl with a 25.3 m (83 ft) long
headrope and a 34.1 m (112 ft) long footrope (more de-
tails are provided in Weinberg, 2003; Lauth and Nichol,
2013). The simple 5.2 cm diameter footrope is weight-
ed with 75 kg of chain hung in equal loops along its
length from which the nylon netting is attached. Mesh
size varies from a maximum of 10.2 cm in the wings
and throat to a minimum of 3.2 cm for the liner in
the codend. Each side of the net is attached to a steel
V-door (1.8x2. 7 m) that weighs approximately 816 kg
by a pair of 54.9-m-long, 1.6-cm-diameter bare wire
bridles. Because faster trawling has been shown to ex-
acerbate inconsistencies in seabed contact of this trawl
(Weinberg, 2003), an additional 34 kg of weight was
secured to the footrope, then monitored with a bottom
contact sensor for all tows in this experiment.
The major difference between tows of our experiment
and standard survey tows was towing speed. All other
trawling procedures followed those used during the
survey (e.g., straight-line towing, locked winches with
equal lengths of warp, standard warp length to depth
ratios, and setting and retrieval methods designed to
lower the net down on the seabed in fishing configura-
tion quickly at the start of a tow and to raise it off the
seabed quickly at the end of a tow). Our balanced-pair
design called for repetitive parallel towing and vessels
safely separated by no more than 463 m (0.25 nmi). On
odd-numbered pairs, one vessel was randomly selected
to tow at the standard survey speed of 1.5 m/s, while
the other vessel towed at the faster speed of 2.1 m/s.
On even-numbered pairs, the vessels switched towing
speeds. To reduce potential bias from sea conditions,
the faster boat was randomly appointed to fish either
the port or starboard side of the slower boat.
When fishing with 2 boats at different speeds, we
had a choice of enforcing either consistent tow duration
(time) or consistent tow length (distance). Because it
has been shown that variation in tow durations (15.0
Weinberg et al.: Survey selectivity for Gadus macroceph
363
and 30.0 min) did not affect the size distribution of
catches for some Atlantic species, including Atlantic
cod {Gadus morhua; God0 et ah, 1990; Walsh'*), we
elected to reduce the duration of the faster tows so that
the distance fished and swept area of tows were similar
between the 2 speeds (Wileman et ah, 1996). Hence,
the duration of the slow (1.5 m/s) and fast (2.1 m/s)
tows were set at 30.0 and 22.5 min, respectively, mea-
sured from the time the nets were on bottom and the
winches were locked to the time when trawl retrieval
was initiated.
Towing occurred at 2 independent sites, one at a
depth of 136 m and the other at a depth of 86 m. Ten
successful pairs of fast and slow tows were made at
the deep site, and 14 pairs were completed success-
fully at the shallow site. All captured Pacific cod (sex
not determined) were measured to the nearest centi-
meter (FL).
Data analysis
Swept area Swept area for each haul was estimated as
the average net width from data collected with a Mar-
port^ acoustic net mensuration system (Marport Stout
Inc., Snohomish, WA), multiplied by the length of the
tow path, derived from GPS data of vessel locations at
first and last contact of the footrope with the seabed;
seabed contact was determined with a bottom contact
sensor (Somerton and Weinberg, 2001). Outlier mea-
surements of net width were removed by using a se-
quential outlier rejection algorithm, and the remaining
data were fitted with a smoothed spline from which the
average net width was calculated for each tow (Kot-
wicki et ah, 2011).
Measuring the swept area of each tow was compli-
cated by instrument failure during some tows. There-
fore, only a subset of all tows produced valid net width
data. Paired /-tests were used to test for a difference
in the swept area between the fast and the slow tows
of each pair where net widths were available for both
tows. If the difference was found not to be significant
(P>0.05) in this subset of tows after the data from our
bottom contact sensors were examined thoroughly for
anomalies that would indicate the likelihood of high
variability in net width during a tow, we assumed the
swept area was not different for any paired tows and
used the raw catch (counts) from all tows as the depen-
dent variable in subsequent analyses.
Effect of towing speed on catch The null hypothesis
that the catch of large Pacific cod at a fast towing
speed (Cf) was no different than the catch of large Pa-
cific cod at a slow towing speed (Cg) was tested by using
paired-sample tests, against the one-sided alternative
^ Walsh, S. J. 1991. Effect of tow duration on gear selectiv-
ity. NAFO SCR Doc. 91/84, 9 p. [Available at website.]
® Mention of trade names or commercial companies is for iden-
tification purposes only and does not imply endorsement by
the National Marine Fisheries Service, NOAA.
that Cf was greater than Cg. First, the probability of ei-
ther towing speed being equally likely to obtain great-
er catch was calculated with a sign test: the binomial
probability that Cf was greater than Cg in x pairs (suc-
cesses) out of the total y pairs of tows (trials) observed
if the null hypothesis of no effect of speed on catch
was true. A paired /-test was then conducted to fur-
ther confirm the result of the less-sensitive, but more
robust, sign test. The null hypothesis of the /-test was
that there was no mean difference id) between In(Cf)
and InlCg) of the paired tows (Hq: d=0, i.e. the mean
ratio Cf/Cg = 1), assuming that the differences between
pairs were normally distributed. The power (1-P) of
the /-test was calculated for a 1-sided (H^: d>0) alter-
native hypothesis on the basis of the /-distribution, ob-
served standard deviation (SD) of In(Cf) - InlCg), sample
size in) of 24 pairs of tows, and significance level (a) of
0.05. The power was calculated for a range of d for
from 0.1 to 1.0, where e'^=Cf/Cs.
Finally, we estimated d on the basis of the length-de-
rived, double normal, survey selectivity schedule from
the stock assessment model for Pacific cod in the EBS
(see appendix A in Methot and Wetzel, 2013; Thomp-
son*). For our study, we assumed that at the fast tow-
ing speed, no large Pacific cod can escape the net and
all available fish are caught and that at the slow tow-
ing speed, the large Pacific cod available can escape the
net in the proportion indicated by the survey selectiv-
ity function. To increase our sample size, we pooled the
numbers of fish caught in this experiment into length
groups with the same survey selectivity, rounded to the
first decimal place (Table 1). The total expected catch in
a tow based on the curve (Cg) was calculated as the sum
of the catch in each length group in the slow tow (Cs_i)
divided by the survey selectivity for that length group
55
cm FL) and included in further analyses. The bottom
temperatures during the experiment ranged between
2.6°C and 2.7°C.
Swept area
Of the 24 paired tows, 16 pairs had reliable net men-
suration data with which we could test differences in
swept area by pair. The mean difference in swept area
between paired tows (fast and slow) was -0.072 ha,
a variance that was not significant (^=-0.492, df=15,
P=0.63). The fast tows swept a greater area than that
swept by the slow tows during half of the pairs (8 of 16
tows). Conversely, the slow tows swept a greater area
than that swept by the fast tows during the other half
of pairs. Bottom contact sensors provided reliable data
Weinberg et al.; Survey selectivity for Gadus macroceph
365
Table 2
Catch of large (>55 cm in fork length) Pacific cod (Gadus macrocephalus) at fast (Cf)
and slow (Cg) towing speeds for each pair of tows conducted for this study in the
eastern Bering Sea in August 2013. Pairs 1-10 were deep tows. Pairs 11-24 were
shallow tows. The expected catch (Ce) was calculated on the basis of the length-based
selectivity curve from the 2013 National Marine Fisheries Service stock assessment
as described in the Materials and methods section.
Tow pair
Cf
Cg
Cf/Cg
^e/^s
1
17
22
0.8
33
1.5
2
16
6
2.7
8
1.4
3
14
10
1.4
19
1.9
4
11
15
0.7
26
1.8
5
5
12
0.4
18
1.5
6
7
26
0.3
42
1.6
7
5
5
1.0
8
1.5
8
7
9
0.8
15
1.7
9
9
9
1.0
15
1.6
10
15
13
1.2
19
1.5
11
14
14
1.0
20
1.4
12
19
42
0.5
57
1.4
13
22
10
2.2
14
1.4
14
17
15
1.1
19
1.3
15
17
16
1.1
22
1.4
16
22
36
0.6
50
1.4
17
11
27
0.4
38
1.4
18
22
19
1.2
31
1.6
19
16
23
0.7
32
1.4
20
16
15
1.1
20
1.4
21
15
8
1.9
13
1.6
22
7
7
1.0
10
1.5
23
6
7
0.9
9
1.3
24
16
9
1.8
13
1.4
on all tows, indicating that trawl footropes were firmly
in contact with the substrate and providing evidence
for our decision to use all 24 pairs of data in subse-
quent analyses.
Effect of towing speed on catches
Fast tows had larger catches of large Pacific cod in only
10 of 24 paired tows. In those 10 pairs, the catches
from fast tows were 1.1 to 2.7 times (mean: 1.6 times)
greater than the catches from slow tows (Table 2). A
sign test indicated that larger catches were not sig-
nificantly more frequent in fast tows (successes=10, tri-
als=24, P=0.924); larger catches in at least 18 of the 24
pairs would be required for significance (P<0.05).
The mean difference d between In(cf) and In(cs) of
-0.08 (SD 0.55) was approximately normally distrib-
uted according to a goodness-of-fit test (xV2-i=l-226,
P=0.54; Fig. 3). The mean of Cf/Cg was 1.1 (SD 0.58)
(range: 0.3-2. 7; Table 2). A paired ^-test indicated that
the difference in Inicatch) between fast and slow tows
was not statistically significant (^23=-0.69, P=0.50). The
expected mean ratio of the catch of large Pacific cod in
fast tows over slow tows (Cf/Cg) was 1.5 (range: 1.3-1. 9).
If the expected ratio of 1.5 were true, then the power
of a 1-sided ^-test (Hg;. d>0) would be 97% in rejecting
Ho (Table 3).
Vertical distribution
Demersal fish backscatter was fairly low, as would be
expected given the low numbers of Pacific cod captured.
The strongest demersal fish backscatter (S^ — 45 dB)
appeared very close to the acoustically detected sea-
bed; fish backscatter farther off the seabed was gener-
ally weaker in comparison (Sy — 65 dB). The demersal
fish backscatter observed below the average headrope
height of 2.0 m during this study was a very large frac-
tion of fish backscatter integrated over all depth lay-
ers examined (median proportion: 0.96; Fig. 4). In an
absolute sense, the highest demersal fish backscatter
values were found within the depth layer of 0.25-2.0 m
(Fig. 5); the median fish in this layer was more than
14 times that in any other depth layer.
Discussion
We failed to detect a difference between slow (1.5 m/s)
and fast (2.1 m/s) towing speeds in the rates at which
366
Fishery Bulletin 114(3)
-1.5 -1.0 -0.5 0.0 0.5 1.0
ln{Cf)-ln(Cs)
Figure 3
Normal distribution curve fitted to a histogram of the differences in \n{catch) of
large Pacific cod (Gadus macrocephalus) between fast and slow towing speeds
(goodness-of-fit: x25.2.i=1.226, P=0.54) from this study conducted in 2013 in the
eastern Bering Sea. ln(cf)=catch at the fast towing speed of 2.1 m/s; ln(cs)=catch
at the slow towing speed of 1.5 m/s.
Table 3
Power of /-test (probability of rejecting Hq when
it is false) for the mean difference d between
In(cf) (cr=catch of fast tows) and InCcg) (Cs=catch
of slow tows), where Hq: d=0, against one-sided
H^: d>0 alternative hypothesis. The /-distribution
was used with a degree of freedom of 23 and a
significance level (a) of 0.05.
d
e^=Cf/Cs
Power
0.1
1.1
0.21
0.2
1.2
0.53
0.3
1.3
0.83
0.4
1.5
0.97
0.5
1.6
0.99
1.0
2.7
1.00
large Pacific cod (>55 cm FL) were caught with
the 83-112 eastern trawl. Therefore, we surmise
that if the dome-shaped selectivity estimated in
recent stock assessments (Thompson^’^.^) is due to
a decrease in trawl efficiency for large Pacific cod,
that decrease is not attributable to fish outswim-
ming the net. We are unaware of other direct
studies on the swimming behavior of Pacific cod
in relation to trawling activity. Consequently, to
make inferences, we must draw upon the conclu-
sions from research conducted on other, similar
species.
Of the many species studied for their swim-
ming capabilities, the Atlantic cod is most close-
1
0.9
0.8
0 7
0.6
0 5
04
0 3
Both vessels
Figure 4
Boxplot indicating the proportion of demersal fish backscat-
ter, in all depth layers examined (0.25-16.0 m above the
sounder-detected bottom echo), found below the average hea-
drope height but above the 0.25-m dead zone (0.25-2.0 m;
n=20 tows), for this study conducted in August 2013 in the
eastern Bering Sea. The line within the shaded box indicates
the median value, the shaded box indicates the first and third
quartiles, the horizontal lines outside the shaded box indicate
a distance of 1.5 times the interquartile range above the third
quartile and below the first quartile, and the plus marks in-
dicate outliers outside these lines.
j- 0)
Is
(D^
I J
C 0
CO
I-
d:«
ly related to Pacific cod. Winger et al. (2000) performed a
comprehensive tank study on the swimming stamina of At-
Weinberg et al.: Survey selectivity for Gadus macroceph
367
0.25-2.0 2.0-2. 5 2.5-3.0 3.0-7. 0
Depth layer (m)
7.0-16.0
Figure 5
Boxplots of demersal fish backscatter per unit of area (sa)
at 5 depth layers within 16 m of the sounder-detected bot-
tom (n-20 tows), determined from acoustic data collected at
a frequency of 38 kHz in August 2013 in the eastern Bering
Sea. The horizontal line across the shaded box indicates the
median value, the shaded box indicates the first and third
quartiles, the lines outside the shaded box indicate a distance
of 1.5 times the interquartile range above the third quartile
and below the first quartile, and the plus marks indicate out-
liers outside these lines.
lantic cod and deduced that changes in towing
speed would affect the catching efficiency of this
species. In their study, Atlantic cod were sub-
jected to water velocities that were slower than
our towing speeds, but water temperatures were
close to those in our study (2.6°C). At the towing
speeds used by fishermen in the northeast Atlan-
tic (1.0 m/s), Atlantic cod were able to maintain
sustained swimming speeds for 10 min, but at a
speed of 1.5 m/s (the slow towing speed in our
study), they could maintain swimming speed for
only 1 min. If Pacific cod swimming abilities are
indeed similar to those of Atlantic cod, then, giv-
en the towing speeds of 1.5 m/s or greater used in
our experiment, we expect that Pacific cod maxi-
mum sustained swimming speeds would not be
enough to elude capture even during a haul last-
ing 22.5 min, the shorter tow duration used in
our experiment.
Large Pacific cod do not escape capture by out-
swimming the survey trawl, as indicated by our
study results: catches when towing at the fast
speed were no different than catches when tow-
ing at the slow speed. This result indicates that,
once Pacific cod reach the trawl mouth, they lack
the means to swim fast enough or long enough
to escape forward around the wing ends. In situ
video evidence shows that this species tends to
hold station in front of the footrope for only brief
periods before slipping back into the net (Rose®).
Large Pacific cod are unlikely to swim over the
net because acoustic backscatter indicates that
most Pacific cod, when in the presence of a trawler, oc-
cur very close to the bottom within the vertical fish-
ing dimensions of the trawl. In addition, findings from
previous studies on gadid behavior indicate that trawl
gear elicits a diving response in fish, not a rising re-
sponse. The remaining avenues for escapement that
could explain lowered trawl efficiency are 1) large Pa-
cific cod could swim through the small mesh of the sur-
vey net, an option that is physically impossible and 2)
they could escape beneath the footrope, the frequency
of which has been previously shown to be negligible
(Weinberg et ah, 2002).
If large Pacific cod are not outswimming the trawl,
perhaps they are swimming over the headrope — a no-
tion that would also explain a drop in selectivity for
large fish related to both trawl sampling efficiency and
availability. Here, we used fish backscatter to within
0.25 m of the seabed to assess the vertical distribu-
tion of Pacific cod near the seafloor during our experi-
ment. This process discards potential backscatter from
fish in the acoustic dead zone (Ona and Mitson, 1996),
which is located very close to the seabed and could be
an area of concern for an absolute estimate of all fish
Sa- However, the distribution of fishes within the dead
zone is less important for our main interest of detect-
® Rose, C. R. 2010. Unpubl. data. Resour. Assess. Conserv.
Eng. Div., Alaska Fish. Sci. Cent., NOAA, Seattle, WA 98115.
ing Pacific cod occurrence in relation to the headrope
height of the trawl; indeed, if most Pacific cod are in
the acoustic dead zone, they clearly are not above the
headrope height during vessel passage.
Analysis of acoustic backscatter collected during
towing indicated that only 4% of the total backscat-
ter attributed to Pacific cod occurred above the height
of the survey headrope, although the backscatter was
measured at the vessel rather than at the net itself,
meaning that any upward movement of fish after ves-
sel passage would be undetected. Again, there are no
previous studies on the vertical swimming behavior
of Pacific cod in relation to trawls from which we can
draw inferences. Studies of walleye pollock (Kotwicki
et ah, 2013) and Atlantic cod show that these 2 com-
mercially important gadids were stimulated to dive,
rather than rise; their response to trawl warps may be
both acoustically, as well as visually, driven according
to Handegard and Tjpstheim (2005). This behavior is
also acknowledged by commercial fishermen who tend
to drag their nets below semipelagic schools. There is,
therefore, little reason to believe that Pacific cod swam
over the headrope during this experiment.
Nichol et al. (2007) did, however, on the basis of 11
archival tags, provide evidence of an off-bottom portion
of the Pacific cod vertical distribution during daylight
hours (the time during which the EBS survey is con-
ducted) when the fish were in an undisturbed state
368
Fishery Bulletin 1 14(3)
(i.e., tags were deployed in the absence of vessel noise
or oncoming trawl gear). They postulated that large Pa-
cific cod swim above the survey-wide average height of
the headrope (2.5 m) approximately 53% of the time
and within 10 m of the seabed 95% of the time. Al-
though their study was based on an interpretation
of estimated tidal activity, their work has had a pro-
nounced impact on the current stock assessment model,
such that the catchability coefficient was fixed so that
the average product of catchability and selectivity size
range (60-81 cm FL) equaled 47% (Thompson^’^’^).
We agree with Nichol et al. (2007), in that it seems
unlikely for the survey trawl to catch 100% of the Pa-
cific cod in its path 100% of the time; however, we cast
doubt on the conclusion that more than 50% of large
fish swim above the trawl in the presence of trawling
activity. Nichol et al.’s study was based on a very small
sample, and one could argue that our study similarly
lacked broad geographical range, over areas with vary-
ing habitat complexity, light intensity, and tempera-
tures that (although never shown) may all have an
effect on Pacific cod vertical distributions or perhaps
even swimming speeds (Ferno et al., 2011). Additional
experiments focusing on these factors would shed ad-
ditional light on the matter.
Survey selectivity functions in stock assessment
models are designed to be a parsimonious representa-
tion of the relative size dependency of the survey sam-
pling process. However, stock assessment models can
be quite complex, often including hundreds of param-
eters that must be estimated when the models are fit-
ted to data (Maunder and Punt, 2013; Methot and Wet-
zel, 2013), and such complexity can lead to parameter
correlation and confounding during model fitting. One
example of this confounding is the correlation between
survey selectivity parameters and the natural mortal-
ity rate (Thompson, 1994), a relationship that can lead
to ambiguity in ascribing unexpectedly low catches at
a particular fish length to either reduced survey selec-
tivity or to an underestimated natural mortality rate.
We are, therefore, unable to corroborate the dome
shape for the selectivity function of the survey of Pa-
cific cod in the EBS by using direct evidence from this
and other field studies in which trawl sampling effi-
ciency has been examined. If the estimated survey se-
lectivity function determined from the model is indeed
correct, then the mechanisms that explain the steep de-
scent of the right-hand tail must consist of something
other than sampling efficiency. Four possible explana-
tions for this steep descent of the right-hand tail are
that 1) large fish migrate out of the survey grid, hence
becoming unavailable to the survey; 2) sampling effort
in preferred habitat of large fish embedded within the
EBS survey area is not sufficient; 3) large fish prefer
the small areas of rough, untrawlable bottom embedded
within the EBS survey area; and 4) the relationships
between availability and efficiency, on the one hand,
and between catchability and selectivity, on the other,
are complicated enough that studies of availability or
efficiency alone are insufficient to explain catchability
or selectivity (see Suppl. Text [Online]). If something
is misspecified in the assessment model (e.g., perhaps
the natural mortality rate is too low or varies with fish
size), the selectivity of the survey for large Pacific cod
would be closer to unity and could lead to a change
in the harvest quotas. Therefore, further research on
these subjects is needed to clarify the mechanisms re-
sponsible for the selectivity of the survey.
Acknowledgments
Funding for this project was provided by the National
Marine Fisheries Service, National Cooperative Re-
search Program with Industry. We are grateful for the
advice provided by A. De Robertis on echo-integration
techniques and for the helpful comments from our
reviewers D. Nichol and S. Kotwicki. In addition, we
thank our anonymous reviewers who sacrificed their
valuable time to contribute to the advancement of fish-
eries science.
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370
NOAA
National Marine
Fisheries Service
Fishery Bulletin
ftx- established 1881
Spencer F. Baird
First U.S. Commissioner
of Fisheries and founder
of Fishery Bulletin
A comparison of circle hook and J hook
performance in the recreational shark
fishery off Maryland
Email address for contact author: angel.willey@maryland.gov
Abstract — The purpose of this study,
conducted from 2012 through 2014,
was to gather data on the differ-
ent effects of circle and J hooks on
hooking outcome, frequency of deep
hooking, and catch rate in the recre-
ational shark fishery off Maryland.
Circle hooks clearly outperformed J
hooks. Interactions of sharks with
circle hooks resulted in a 91% hook-
ing rate (of which 3% were deep
hookings), an 88% capture rate, and
a catch rate of 0.9 sharks/hook inter-
action. The hooking rate for J hooks
was 75% (of which 6% were deep
hookings), a capture rate of 68%,
and a catch rate of 0.7 sharks/hook
interaction. These results indicate
that circle hooks can improve fishing
success and serve as a conservation
measure by maximizing the prob-
ability of survival for sharks during
recreational shark fishing.
Manuscript submitted 31 August 2015.
Manuscript accepted 6 June 2016.
Fish. Bull. 114:370-372 (2016).
Online publication date: 21 June 2016.
doi: 10.7755/FB.114.3.9
The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National
Marine Fisheries Service, NOAA.
Angel L. Willey (contact author)
Linda S. Barker
Mark Sampson
Fisheries Service
Maryland Department of Natural Resources
580 Taylor Avenue
Annapolis, Maryland 21401
Numerous studies of the recreational
use of circle hooks in teleost fisheries
and the commercial pelagic longline
fishery indicate that fewer fish are
“deep hooked” on circle hooks and
that catch efficiency with circle hooks
is equal to, or better than, that with
J hooks (Cooke and Suski, 2004; Se-
rafy et ah, 2012). These studies have
helped circle hooks gain acceptance
and have provided the data used to
set forth regulatory requirements
for some fisheries and tournaments
(Cooke and Suski, 2004). In the rec-
reational shark fishery, some anglers
have been reluctant to switch to cir-
cle hooks because of concerns about
catch efficiency and doubts about the
applicability of the results of teleost
studies to the catchability of sharks
(Prince et ah, 2002; Lucifora et ah,
2009; Serafy et ah, 2012). Therefore,
scientific evidence that supports the
benefits of circle hooks is needed to
convince recreational shark anglers
to voluntarily switch hook types and
support regulatory measures that re-
quire circle hook use in their fishery.
We undertook this study from 2012
through 2014 to gather data on the
effects of circle and J hooks on hook-
ing outcome, frequency of deep hook-
ing, and catch rate in the recreation-
al shark fishery off Maryland.
Materials and methods
Field methods
All data were collected by a charter
captain that specialized in shark
fishing off the Atlantic coast of Mary-
land. He fished as he normally did
but dedicated 2 surface lines to our
study, set with a circle hook and a
comparable-size J hook. Circle hooks
were limited to Mustad^ 39960D
hooks in sizes 16/0 when fishing oc-
curred offshore and 13/0 when fish-
ing occurred nearshore (O. Mustad &
Son A.S., Gjovik, Norway). Bait type
was identical in size and species for
both lines and was refreshed at the
same time.
The outcome of each shark inter-
action with the line (called a strike)
was recorded as a bite, as lost, or
as captured) — terminology similar
to that of Skomal et al. (2002). A
bite was defined as a strike that re-
sulted in the shark taking the bait
but not being hooked. An event was
not recorded if the captain or mate
1 Mention of trade names or commercial
companies is for identification purposes
only and does not imply endorsement by
the Maryland Department of Natural
Resources.
Willey et al.; A comparison of circle hook and J hook performance
371
Foul Jaw Throat Gut
Hook location
Figure 1
Hook locations (n=622) observed, 2012-2014, during a study of
interactions of sharks with circle and J hooks in the recreational
shark fishery off Maryland. Data for 2 landed sharks were not
included in this figure because either a hook location was not
recorded or the shark had become entangled in the line and a
hooking event did not occur. A location at throat or gut was con-
sidered a deep hooking.
Bite Lost Captured
Hooking outcome
Figure 2
Outcomes of hooking events (n=781) observed during 2012-2014
as part of a study of interactions of sharks with circle and J
hooks in the recreational shark fishery off Maryland, classified
into 3 categories: 1) bite, when a shark took the bait but was not
hooked; 2) lost, when a hooked shark became unhooked before
the mate could grab the leader; and 3) captured, when a shark
was fully played to the boat and the mate grabbed the leader.
could not confirm that it was a shark bite. A lost clas-
sification was defined as the outcome where a hooked
shark became unhooked before the mate could grab the
leader. A captured classification was the outcome when
a shark was fully played to the boat and the mate
grabbed the leader. Hook location was recorded as jaw,
throat, gut, or foul (external). Entangled fish were docu-
mented but excluded from the analysis because they
were not actually hooked. Deep hooking was
defined as hooking in the throat or gut.
Statistical methods
Trips were identified as nearshore or offshore
because of differences in species composition
and tackle requirements. Nearshore trips oc-
curred in waters within 32.2 km (20 mi) of
land, and offshore trips took place in waters
32.2 or more kilometers from land. Most of the
nearshore fishing occurred within 1.6-9. 7 km
(1-6 mi) of the beach, and the majority of off-
shore fishing took place between 32.2 and 48.3
km (20 and 30 mi) from the beach.
Data were pooled across years, and the fol-
lowing tests were performed. Chi-square analy-
sis was used to determine whether nearshore
and offshore trip data could be pooled. Hypoth-
esis tests of proportions were conducted to com-
pare hooking outcomes and to compare rates of
deep hooking between hook types. Catch rate
was defined as the number of sharks captured
per interaction and calculated as the mean of
trip values. Student’s Atest was used to com-
pare catch rates between hook types.
Results
Data were collected during 24 offshore and
180 nearshore trips, and the results of chi-
square analysis indicated that nearshore and
offshore data could be pooled for all analyses
(all P>0.10). During this study, 624 sharks
representing 10 shark species were captured,
primarily dusky shark (Carcharhinus obscu-
rus; n=235), spinner shark {Carcharhinus bre-
vipinna; n=180), sandbar shark {Carcharhinus
plumbeus; n=89), and Atlantic sharpnose shark
{Rhizoprionodon terraenovae; n=70). The other
species caught were the blue shark {Prionace
glauca; n=15), blacktip shark {Carcharhinus
limbatus; ?z=13), tiger shark {Galeocerdo cu-
vier; n=7), shortfin mako {Isurus oxyrinchus;
n=7), scalloped hammerhead {Sphyrna lewi-
ni] n=5), and smooth hammerhead {Sphyrna
zygaena; n=3).
There were 438 shark interactions with cir-
cle hooks and 343 interactions with J hooks.
Interactions with circle hooks resulted in a
91% hooking rate of which 95% of sharks were
hooked in the jaw and only 3% were deep hookings
(Fig. 1). Circle hooks had an 88% capture rate (Fig.
2) and a catch rate of 0.9 sharks/hook interaction. For
J hooks, the hooking rate was 75% of which 82% of
sharks were hooked in the jaw and 6% deep hookings.
The capture rate was 68% and the catch rate was 0.7
sharks/hook interaction. All differences were significant
with P<0.01.
372
Fishery Bulletin 1 14(3)
Discussion
The data clearly indicate that circle hooks outper-
form J hooks. Circle hooks had both a higher hooking
rate and capture rate than J hooks. Circle hooks had
a lower deep-hooking rate and a higher proportion of
sharks hooked in the jaw — results that are consistent
with those of many teleost studies (Prince et ah, 2002;
Skomal et al., 2002). Both the higher catch rate and
the lower deep-hooking rate indicate that circle hooks
can improve fishing success and serve as a conserva-
tion measure for recreational shark fishing. In addi-
tion, the results of this study indicate that the use of
circle hooks could increase adherence to the federal
regulations regarding prohibited shark species — reg-
ulations that are outlined in a compliance guide for
highly migratory species (NMFS^). These regulations
require that shark species for which retention is pro-
hibited be released in a manner that maximizes the
probability of their survival.
^ NMFS (National Marine Fisheries Service). 2015. HMS
recreational compliance guide: guide for complying with the
Atlantic billfishes, swordfish, sharks, and tunas regulations,
p. 30. Off. Sustainable Fish., Highly Migratory Species
Manage. Div., Natl. Mar. Fish. Serv., NOAA, Silver Spring,
MD. [Available at website, accessed June 2016.]
Acknowledgments
We would like to thank the 3 anonymous reviewers for
their constructive comments at the manuscript stage.
Literature cited
Cooke S. J., and C. D. Suski.
2004. Are circle hooks an effective tool for conserving ma-
rine and freshwater recreational catch-and-release fish-
eries? Aquat. Conserv. 14:299-326.
Lucifora, L. O., V. B. Garcia, and A. H. Escalante.
2009. How can the feeding habits of the sand tiger shark
influence the success of conservation programs? Anim.
Conserv. 12:291-301.
Prince, E. D., M. Ortiz, and A. Venizelos.
2002. A comparison of circle hook and “J” hook perfor-
mance in recreational catch-and-release fisheries for
billfish. Am. Fish. Soc. Symp. 30:66-79.
Serafy, J. E., S. J. Cooke, G. A. Diaz, J. E. Graves, M. Hall, M.
Shivji, and Y. Swimmer.
2012. Circle hooks in commercial, recreational, and arti-
sanal fisheries: research status and needs for improved
conservation and management. Bull. Mar. Sci. 88:371-
391.
Skomal, G. B., B. C. Chase, and E. D. Prince.
2002. A comparison of circle hook and straight hook per-
formance in recreational fisheries for juvenile Atlantic
bluefin tuna. Am. Fish. Soc. Symp. 30:57-65.
373
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Fishery Bulletin 1 14(3)
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