ICES mar. Sei. Sym p., 196: 211-215. 1993
Management implications of changes in by-catch rates of Pacific
halibut and crab species caused by diel behaviour of groundfish
in the Bering Sea
Sara A . Adlerstein and Robert J. Trumble
Adlerstein, S. A ., and Trumble, R. J. 1993. Management implications o f changes in
by-catch rates o f Pacific halibut and crab species caused by diel behaviour o f
groundfish in the Bering Sea. - ICES mar. Sei. Symp., 196: 211-215.
This study compares day and night by-catch rates o f prohibited species (ratio of
prohibited species to groundfish catch) in U S domestic bottom-trawl fisheries for
Pacific cod (G adu s m acrocephalus) and walleye pollock ( Theragra chalcogram m a) in
the Bering Sea to identify m anagement options to reduce by-catch. Bottom trawl
fisheries in the Bering Sea cause significant by-catch mortality o f Pacific halibut
(H ippoglossus stenolepis) and other prohibited species such as king crab (Paralithodes
camtschatica) and Tanner crabs ( Chionoecetes spp.) By-catch rates are higher during
night hours than during the day. W e propose that by-catch differences are caused by
diel vertical migration and other behavioural characteristics o f the species that result in
fluctuations o f their relative abundance near the seabed between the two time periods.
Avoiding night bottom fishing in the Pacific cod and walleye pollock fisheries may
permit by-catch rate reduction. Fishing exclusively during day hours could produce
total savings from 13 to 16% o f the observed by-catch o f halibut, king crab, and T anner
crabs.
Sara A . Adlerstein and R ob ert J. Trumble: International Pacific H alibut Com m ission,
P O B ox 95009 Seattle WA 98145-2009, USA.
Introduction
By-catch o f prohibited sp ecies such as Pacific halibut
( H ip p o g lo ss u s sten o lep is), king crab (P aralith odes
c a m tsch atica ), and T ann er crabs (C h ion o ec ete s sp p .) in
the B ering Sea causes trem en d ou s lo sses, both in
groundfish and in prohibited sp ecies fisheries. M a n a g e ­
m ent regulations for by-catch in the region set q u otas for
prohibited sp ecies (to n n es o f halibut and nu m b er o f
crabs) in the various groundfish fisheries and require
prom pt discard o f the by-catch to the ocea n . By-catch
quotas are often reached b efore the groundfish quotas
are tak en , and th ese fisheries are clo sed b efore their
allow a nces are harvested. A m o n g the bo tto m trawl
fisheries in the region, catches with high proportion o f
Pacific cod (G a d u s m a cro ce p h a lu s) ex p erien ce high hali­
but by-catch rates. Fisherm en have reported that higher
by-catch rates occur during night hours than during the
day. Variation in these rates is m ost probably related to
the diel vertical m igration o f Pacific cod. C o d sp ecies,
usually foun d in close association with the se a b e d during
day hours, have b e e n reported to migrate to the surface
during the night (B e a m is h . 1966; Turuk, 1973). T h e goal
o f this study is to investigate the reported day and night
d ifferences in by-catch rates and to understand the
behavioural processes o f the various sp ec ies inv olv ed in
the fishery to use this inform ation for m an agem en t
purposes. O ur approach was statistically to com pare
fishery data, and to co m p lem e n t the results with b io lo g i­
cal inform ation on the s p e c ie s’ behaviour.
Material and methods
Pacific halibut and crab sp ec ies by-catch rates vary with
the co m p o sitio n o f the groundfish sp ec ies in the catch
(i.e . w a lley e p o llo ck (T heragra c h a lc o g r a m m a ) , Pacific
co d , yellow fin sole (L im a n d a a sp e ra ), rock so le (L e p ido p se tta bilineata) and o ther flatfish) (B e rg e r et a l.,
1989; Clark, 1990; A d lerstein , 1991). T his analysis in­
vestigates w h eth er by-catch rates in the Pacific co d and
w alleye p ollock fisheries vary from day to night after
accou nting for system atic cha ng es in sp ecies c o m p o ­
sition in the catch. T h e study uses data from individual
211
b o tto m trawl hauls from the 1990 d om estic op era tion s in
the w estern region o f A r e a 511 in the Eastern B e rin g Sea
(Fig. 1). Pacific c o d is part o f several bottom -traw l
m ultispecies fisheries and is an im portant c o m p o n e n t o f
the total catch o f Pacific c o d and w alley e p ollock fish­
eries. Fishing o p e r a ted in the area from January to May.
Pacific co d is also caught by trawls in A r e a s 513, 517,
5 19, 521, and 522, bu t w e se lec ted A r e a 511 be c a u se o f
data availability. D a ta w ere p rovided by the N ational
M arine F isheries Service ( N M F S ) , S e a ttle, and are from
a haul by haul datab ase co lle cte d by observers in the
N orth Pacific and B erin g Sea ( N O R P A C ) ge n e rate d by
(A d le r stein , 1991). Y ellow fin s o le , anoth er im portant
c o m p o n e n t o f the overall catch, w as not included as
c ovariate b ecau se it w as no t part o f the d o m e stic fish­
eries in 1990. M on th w as u sed as a fixed factor because
by-catch o f halibut and crab sp ecies e x p e r ie n c e s te m ­
poral variations (A d le r stein , 1991).
D a ta were subjected to the m od e l Y ij = /u + a t + ßj +
a ß jj + b ljjX l + b2jjX2 w h ere Y is the natural logarithm
o f the prohibited sp ecies by-catch rate + 1 (in kilogram s
o f halibut or nu m ber o f crabs per to n n e o f groundfish)
for the ith m on th and the jth tim e period s, X I and X 2 are
the p roportions o f Pacific co d and rock so le in the catch,
a m and atory observer p rogram m e. R e c ord s c ontain the
w eigh t, nu m bers, and length freq u en cies o f Pacific hali­
and a and ß are m o d e l intercept param eters for the
m onth and tim e period m o d ifyin g th e overall m ean [â .
but, n u m b er o f crabs, total catch w e ig h t, and w eigh t by
T h e logarithm ic transform ation o f the by-catch data
groundfish sp ecies. R e c ord s also contain inform ation
abou t trawl op e r a tio n s such as gear type, d a te , locatio n ,
n o rm alized the distribution o f the errors. W e fitted the
full m od el and tested for differen ces in the m o d e l slopes
and tim e o f set and retrieval o f the nets. D a y hauls are
th o se set and retrieved b e tw e e n sunrise and su n set, and
b e tw e e n m o n th and tim e o f the day periods as w ell as for
differences b e tw e e n the m e a n s. A p p ly in g day param ­
eters o f the m o d e l to g e th e r with night catch proportions
and com parin g the results with e stim a tes o b ta in e d from
night p aram eters, w e w ere able to estim ate m onth ly
night hauls are th o se taken after e v en in g twilight and
b efo re m orning twilight. H auls e xten d in g from day to
night perio d s w ere classified as transitional.
C om p arison o f day and night rates used an analysis o f
covariance ( A N C O V A ) (Z ar, 1984), w h ere by-catch
rates are a fun ction o f the catch c o m p o sitio n . T h e
analysis used the G en er a liz e d Linear Interactive M o d e l­
ling (G L IM ) System (R o y a l Statistical S ociety 1987).
T h e proportions o f Pacific co d and rock sole in the catch
w ere incorp orated as covariates, and m on th (January to
M ay) and tim e period o f the day w ere inclu ded as fixed
factors. W alle y e p ollock , an im portant c o m p o n e n t o f
the catch, w as not in cluded as a covariate be c au se Pacific
c o d and p o llo ck are collinearly related in th e se fisheries
63 "
U.S. line
R u s s ia n li n e
522
D is p u te d
a re a
514
521
-
513
5 50
522
511
G u l f o f Alaska
53 “
165”
160"
Figure 1. Regulatory areas in the Bering Sea/Alcutian Islands.
Data for the analysis were taken from the stippled area o f Area
212
p(|t| > 1.108) > 0.2; T ann er crab: p(|t| > 0 .8 9 1 ) > 0 .2 ).
T hu s, for further analysis w e c o m b in e d the transition
and night c ategories. O b se r v ed m e an by-catch o f the
com b in e d data for the three prohibited sp ec ies was
higher during night hours (Fig. 2 ). R esu lts o f the
A N C O V A using day and night-tim e c a tegories sh o w e d
that three-w ay interactions b e tw e en Pacific c o d , m onth
and day/night periods w ere not significant at an a level o f
0.05 (F 4 i 3 7 d = 2.152; p = 0 .0 7 2 ), nor b e tw e e n rock so le ,
m onth and day/night period s (F 4, 137() = 1.961; p =
day/night period ( F L!378 = 2.575; p = 0 .1 0 9 ). T h ese
results a llo w ed us to perform an A N C O V A (intercep ts)
using c o m m o n slo p e s ( b l and b2) m o d e ls. R esu lts from
518
511.
C om p arison o f the param eter estim ates o f the three time
ca teg ories (ß-,) in fitting the full by-catch m od el revealed
that by-catch rates o f halibut and the crab sp ec ies in the
transition category w ere not significantly different from
the night rates (halibut: p(|t| >: 0 .8 1 6 ) > 0.2; king crab:
(F-t. 1378 = 1-653; p = 0 .1 5 9 ), Pacific co d and day/night
period ( F t, i378 = 2.729; p = 0 .0 9 9 ), and rock sole and
517
55 °
175 °
Results
0 .0 9 8 ). T w o -w a y interaction b e tw e e n Pacific c o d and
m onth w as not significant (F 4 i378 = 1.846; p = 0 .1 1 8 ),
nor w ere the interactions b e tw e e n rock sole and m onth
5 1 2 511
530
540
savings o f prohib ited sp ecies by-catch that w o u ld be
obtain ed if the night catch es o f fisheries un der con sid er­
ation w ere harvested during day hours.
the A N C O V A indicated that by-catch rates vary by time
o f the day (p = 0 .0 0 4 ), by m onth (p < 0 .0 0 0 5 ). and with
the proportion in the catch o f Pacific c o d (p < 0.0 005 )
and rock so le (p < 0 .0 0 0 5 ). T h e interaction b e tw e en
m onth and tim e o f the day w as not significant (p > 0 .25)
0.3<D
Q)
<D
C
c
o
c
o
c.
C
C
o
0 .2 -
O)
0
cc
0)
2
n
2
o
CD
S, 0.5
c
C
C
CO
*
I-
100i
40i
King crab
C/)
CD
O)
LU
3
CL
c
Q_
O
C/3
£}
CO
O
X
Total catch
UJ
3
O
3
-Q
30
o
LU
g 20
O
eo
Tanrter crab
Pacific cod
O
Figure 2. Observed mean by-catch rates o f the prohibited specics, and catch per hour o f groundfish and prohibited species in Area
511, 1990.
(T able 1). A Filliben test (F illiben, 1975) p erform ed on
the o rdered m o d e l residuals indicated n o e v id en ce
against assum ing norm al distribution o f the errors (Filli­
ben coefficient = 0.9 989 , p < 0 .0 5).
Inspection o f the param eter estim ates o f the c o m m o n
slop es m od el incorporating m o n th , time o f the day, and
proportions o f cod and rock so le , sh ow s that the inter­
cept o f the m o d e l is increased during night hours over
the day intercept (Table 1). Thu s, since the slopes
rem ain the sam e during the tw o tim e p eriod s, halibut bycatch rates for a given catch sp ecies c o m p o sitio n are
higher at night than during the day. W e estim ated
potential savings obtain ed by fishing during day hours by
using param eters in T able 1 and catch c o m p o sitio n . The
results indicated that if night catches w ere taken during
the day, the by-catch rates w ou ld be red uced by 16.2%
in January, 16.4% in February, 17.4% in M arch, 35.4%
in A p ril, and 15.2% in M ay.
R esu lts o f the A N C O V A on the by-catch data o f the
tw o crab sp ecies sh o w e d similar results to th o se obta in ed
from the halibut data. Three- and tw o-w ay interactions
b e tw e e n the covariates and factors w ere non-significant
(p > 0.1 in all cases). This allo w ed us to perform the
A N C O V A using c o m m o n slop es m od els. R esu lts from
the A N C O V A on the king crab data using the c o m m o n
slo p e s m o d e l r eve aled that day and night by-catch rates
are significantly different from each oth er (p < 0.0005)
Table 1. Results o f analysis o f covariance o f the by-catch rate
(Y ) o f Pacific halibut for the cffect o f month (January to April),
and time o f the day (night and day) accounting for the
proportion o f Pacific cod (X I ) and rock sole (X2). Covariates,
factors, and interactions are assessed simultaneously, with each
effect adjusted for all other effects in the model.
Source o f variation
Month
Day/night
Rock sole
Cod
Month, day/night
Residual
SS
DF
F
P
178.80
8.44
61.37
87.02
2.613
1426.8
4
1
1
1
4
1389
43.525
8.173
61.367
87.016
0.635
< 0 .0 0 0 5
< 0 .0 0 4
< 0 .0005
< 0 .0 0 0 5
> 0 .2 5
Parameter estimates for the m odel including significant
variables Yy = ft + a, + $ + b l X l + b2X2
1
2
3
4
5
6
7
8
Estimate
s.c.
Parameter
1.680
-0 .2 9 5 6
-0 .6 8 0 9
-0.3 8 5 4
0.3978
0.1659
2.047
1.189
0.1003
0.1017
0.1124
0.0983
0.0911
0.0578
0.2555
0.1232
^ (January, day)
a2 (February, day)
a3 (March, day)
a 4 (April, day)
a 5 (May, day)
ß2 (night)
Rock sole (covariate) ( b l)
Pacific cod (covariate) (b2)
u \ and ß \ arc constrained to 0. Standard errors o f the
intercept ai and ßj are o f the difference between the corre­
sponding factor levels and ft.
213
and that the night intercept is increased o v e r the day
intercept. A ll o th er variables w ere significant in d e te r ­
m ining by-catch (p < 0 .0 0 0 5 ). W e e stim ated rate re­
du ctions as b efore. R a tes could be red uced by 17.2% in
January, 20.8% in February, 28.7% in M arch, 26.4% in
A p ril, and 19.0% in M ay. R esu lts from the A N C O V A
using the red u ced m o d e l on the T an n er crab data indi­
Discussion and conclusion
B y-catch rates o f prohibited sp ecies in the w a lley e p o l­
lock and Pacific cod bo tto m trawl fisheries in the Bering
Sea w ere fo u n d to b e higher during the day than during
night hours. Increase in halibut and crab by-catch rates
at night is probably the result o f the beh av iou r o f the
cated that day and night by-catch rates are significantly
different from each o th e r (p < 0 .0 0 5 ) and that the night
intercept is in creased ov e r the day intercept. W e esti­
sp ec ies involved in the bo tto m trawl fisheries. T he
relative abu nd ance o f the groundfish (m ainly w a lleye
m a ted rate reductions to be 31.9% in January, 34.9% in
February, 37.7% in M arch, 34.4% in A p ril, and 39.4%
in May.
By-catch rates are d eterm in ed by the relative abu n­
dan ce o f prohib ited sp ec ies and groundfish in the catch.
Catch per unit effort ( c .p .u .e . in to n n es/h ) o f groundfish
d ecreases significantly at night: p(|t| S: 2.7 2 4 ) < 0.005
night, se e m in gly b e c a u se sp ecies m igrate tow ards the
surface during the night. O b serva tion s o f cod migrating
to m idw ater at night (i.e . B e a m ish , 1966; T uruk , 1973)
support this hyp othesis. H o w e v e r , m o v e m e n t in the
for all m o n th (Fig. 2). In particular c .p .u .e . o f Pacific cod
d ecreases during the night: p(|t|
2
: 1.953) < 0.0 5 for all
m onth s. L o w e r c .p .u .e . o f the groundfish catch during
night suggests that fish are less available or v ulnerable to
the net near the se a b e d during those hours. L o w e r
availability is c on sisten t w ith h yd roacoustic o b ser ­
vations in the B ering Sea that the tw o main sp ec ies in the
catch, Pacific c o d and w a lley e p o llo ck , rise o ff the
b o tto m during the night (E . P. N u n n a lle e , pers. c o m m .,
N M F S , Se attle). A l s o , catch rates o f c o d ( G a d u s m o rhua L .) in b o tto m trawl surveys have b e e n rep orted to be
higher by day (E n ga s and Sold a i, 1992). H alib u t, king
crab and T an n er crab, c .p .u . e .s by m on th are co n sist­
ently higher at night (Fig. 2 ), although the differences
b e tw e e n th e tw o tim e periods are not significant (p(|t| >
0.5 4 3 ) > 0.5; p(|t| > 1.528) > 0.1; p(|t| > 1.679) > 0.1).
pollock and Pacific co d ) on bo tto m d e c re a se s during the
op p o site direction has also b e e n ob ser v e d . Turuk (1973)
d e m o n strated that the direction o f the migration is
related to the c o d diet: w h en fe ed in g o n actively sw im ­
m ing prey, co d d e sc e n d during the day and a scen d at
night; if benth ic organism s p r ed om in ate in the diet the
o p p o site is true. A lth o u g h Pacific co d diet exhibits much
diversity, in the study area this sp ec ies fe e d s primarily on
pelagic fish such as ju v e n ile p ollock (B r o d e u r and
Livingston, 1988).
Proh ib ited s p e c ie s’ c .p .u .e . are con sisten tly, although
not significantly, higher at night. H ig h er halibut c .p .u .e .
in kg I T 1 is related to higher proportion o f large fish in
night catch es. W e sp ecu late that during the day large fish
are m ore likely to avoid the nets. T his is in a greem en t
with the su ggestion that vision is the pred o m in a n t sense
used in av oid an ce reaction w h e n a fish is app ro ach ed by
a trawl (W a rdle, 1986). W alsh (1991) dem on strated
higher e sc a p e m en t o f large flounders (plaice and yello w tail) under the g round gear during the day than during
H ig h er c .p .u .e . can be du e to increased vulnerability or
availability o f prohib ited sp ecies near the se a b e d during
night hours. W e o b ser v e d that len gth freq uency distri­
b u tio n s o f halibut by-catch during day and night hours
sh o w significant d ifferences (K o lm o g o r o v -S m ir n o v tw osam p les te st p o f Z < 0 .0 0 0 1 ). T h e te n d e n c y is to find
higher proportio ns o f fish larger than 50 cm in night
hauls than in day hauls. It is possible that fish vuln er­
ability ch a n ges b e tw e e n dark and light period s beca use
large halibut are m or e likely to avoid the nets during
night hours. T h e night increase in crab c .p .u .e . is c o n ­
sistent with o b serva tio n s o f crab p o d d in g activity. D e w
(1989) rep orted o n diel activity cycles and foraging
dynam ics o f king crab in the general area o f this study.
W e p r o p ose that high catch rates at night are gen erated
by fishing w h e n crabs are active and highly aggregated.
Irrespective o f the origin o f d ifferences in by-catch
rate, it is clear that savings m ay b e o b ta in e d in the
light periods. N o inform ation w as accessible to us to
investigate diel ch a n ges in availability. N e v e r th e le s s,
the groundfish fishing se a so n s and increase the harvest
o f their allow a n ces. From the N O R P A C data and infor­
W alsh (1991) rep orted n o e v id e n c e o f ch an ges o f avail­
m ation provided by Jerry B erger (pers. c o m m ., N M F S ,
ability o f A m e ric a n plaice or yellow tail flounder in
relation to light intensity. T h e variation o f the crab
for Pacific cod and w a lley e fisheries and the total halibut
fisheries co n sid e r ed in this study by avoiding fishing
during dark hours. A v o id in g night fishing m ay e xten d
Seattle), w e estim ated that for A r e a 511 the total harvest
sp ec ies, c .p .u .e . b e tw e e n day and night periods m ay be
by-catch are around 50 000 and 500 to n n e s respectively.
du e to differences n o te d in beh av iou r b e tw e e n a period
o f diurnal rest and o n e o f nocturnal foraging, as n o te d by
This is about 10% o f the entire b o tto m trawl harvest and
halibut by-catch o f the Bering Sea. B a se d on the data
D e w (1989) in king crabs. N octurnal aggregations result
in po d s, w hich are accu m ulation s o f several hundred to
several thou san d crabs. It is c o n ceivab le that nocturnal
activity may increase availability co m p ar ed with the day
situation w h en crab are resting in a hiding site.
from the 1990 fishing sea son in A r e a 5 11, day-on ly
fishing can red uce total halibut by-catch by 13% . C o n ­
versely, for the sa m e am ou n t o f by-catch taken in the
214
area, day fishing w o u ld allow 13% m o re o f the g r o u n d ­
fish harvest. D a y -o n ly fishing w ou ld result in 13% sav­
ings o f king crab by-catch in num bers, and 16% savings
o f T ann er crabs. In m any instances a change in m a n a g e ­
m ent strategies d e sign e d to protect a particular prohi­
bited sp ec ies, such as im posin g fishing se ason s or closin g
specific areas to harvest, can be to the detrim ent o f other
prohibited sp ecies. D a y -o n ly fishing in the Bering Sea o f
the fisheries c o n sid ered , h o w ev e r , appears to reduce
concurrently the by-catch rates o f Pacific halibut, king
crab, and T a n n er crabs.
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