- Email: [email protected]
Greenland halibut (Reinhardtius hippoglossoides) off Southern Labrador and Northeastern Newfoundland (Northwest Atlantic) feed primarily on capelin (Mallotus villosus)
211
Netherlands Journal of Sea Research 29 (1-3): 211-222 (1992)
GREENLAND HALIBUT (REINHARDTIUSHIPPOGLOSSOIDES)OFF SOUTHERN LABRADOR AND NORTHEASTERN NEWFOUNDLAND (NORTHWEST ATLANTIC) FEED PRIMARILY ON CAPELIN (MALLOTUSVlLLOSUS) W.R. BOWERING* and G.R. LILLY* Department of Fisheries and Oceans, P.O. Box 5667, St. John's, Newfoundland, Canada AIC 5Xl ABSTRACT Stomachs were collected from 10 300 Greenland halibut (Reinhardtius hippoglossoides) caught during the autumns of 1981, 1982 and 1984 on the continental shelf and upper slope off southern Labrador and northeastern Newfoundland (northwest Atlantic). Examination revealed strong similarity among years in the percentage of stomachs which were empty (42 to 48%), the average degree of stomach fullness, and the prey spectrum. Small ( < 2 0 cm) Greenland halibut preyed mainly on small crustaceans and cephalopods, medium-sized (20 to 69 cm) individuals preyed primarily on capelin (Mallotus villosus), and large ( > 6 9 cm) individuals preyed on a variety of demersal fish, particularly redfish (Sebastes sp.) and Greenland halibut. An abrupt change in diet at about 64 to 69 cm was related to changes in both feeding habit and geographic distribution. The quantity of capelin in the stomachs was greatest on Hamilton Bank and on or near the coastal shelf off southern Labrador and northeastern Newfoundland. Medium-sized Greenland halibut were not highly aggregated in those areas where they were most successful in finding capelin. Preliminary estimates of daily and annual prey consumption indicate that Greenland halibut is an important predator of capelin. 1. INTRODUCTION This paper describes the food of Greenland halibut (Reinhardtius hippoglossoides) on the continental shelf and upper slope off southern Labrador and northeastern Newfoundland in the northwest Atlantic (northwest Atlantic Fisheries Organization (NAFO) Div. 2J3K, Fig. 1). The Greenland halibut is one of the major demersal species in this area. During the period 1981-84 it contributed 7 to 13% of the annual catch of groundfish and represented 10 to 20% of the *Authorship equal
trawlable biomass estimated from annual bottomtrawl surveys conducted by the Department of Fisheries and Oceans, Canada. Despite its abundance and commercial importance, its role in the trophic interactions in this area is poorly known. Studies of the food of Greenland halibut in the eastern Atlantic (HAUG & GULLIKSEN, 1982), off Greenland (SMIDT, 1969; DE GROOT, 1970) and in the Bering Sea (ALTON et al., 1988; YANG & LIVINGSTON, 1988) have shown that this species feeds predominantly on plankton when it is small and changes to nekton, mainly fish, as it gets larger. It seldom takes invertebrates that stay on the bottom. CHUMAKOV & PODRAZHANSKAYA (1986) found that the most frequently occurring prey off Labrador and eastern Newfoundland were small fish, notably myctophids, capelin (Mallotus villosus) and sand lance (Ammodytes sp.), and various crustaceans, notably the northern shrimp (Pandalus borealis). Their data were aggregated over very broad geographic areas (NAFO Subareas 2 and 3) and provided prey composition by weight for only a small number of fish. LEAR (1970) provided quantitative stomach content data for Trinity Bay on the east coast of Newfoundland, where the dominant prey during the late 1960's was capelin. We expand upon earlier studies in the northwest Atlantic by providing stomach content data by weight with relatively fine size and spatial resolution for the whole offshore region of NAFO Div. 2J3K. We also provide an estimate of the weight of major prey taxa in the stomachs of the population at the time of sampling, and use published information on daily ration to estimate the annual consumption of capelin. Acknowledgements.--We wish to thank the many scientists and technicians who participated in collection of the Greenland halibut stomachs. We also thank C. Butt, H. Collins and P. Bemister for examining the stomach contents, and D. Porter, D. Davis and C. Butt for help in preparing the figures. Several anonymous reviewers provided useful comments on the manuscript.
212
W.R BOWERING & G.R. LILLY
56
ii :i
.6
,
-~
53
54
,
52
,
,
r~
i
51
,
i
50
~--
i
.\.
2H
L" - H A ; R R ] S Q N 55 -'-'~-- L BANK,
• L
:~:..:-... ~,..T~
~'~ "
L,:I /
54
~
"<%Z...
j~"
55
0///
"~
COASTLINE 200 rn ...... 400 m ................ 800 ~ ___ _
-
.
@ LABRADOR
~,~' "~ / P ~
54
i!
B
.
53
2J
BELLE ISLE i 52i___
J
BANK
c • .
i /
3K
ST ANTHONY
.
SHEEF
51 y . ~ /
FUNK SLAND DEEP
GRAY,~ " ~ ~LrSLAt~D ~ - " ~HEPL F
<~
IVEBTE
51
FUNK SLAND
BANK
-~
-50 .
.
.
.
..
FOG0
2 ~ 1 ~
NEWFOUNDLAND 49
. 58
. 57
-
. 56
55
. 54
. 53
52
51
50
JLLE-- . . . . 49 49 48
Fig. 1. Map of study area, showing major physiographic features and NAFO Divisions. 2. METHODS AND MATERIALS 2.1. STUDY AREA The study area in NAFO Div. 2J3K encompasses 189 508 km 2 on the southern Labrador Shelf, the northeast Newfoundland Shelf, and the adjacent continental slope to a depth of 1000 m (Fig. 1). The continental shelf in this area is broad and deep; 80% of the survey area is deeper than 200 m, and 24% is within 301 to 400 m. Hamilton Bank in the northwest has an extensive plateau less than 200 m in depth, whereas Belle Isle Bank and Funk Island Bank to the south have only small areas shallower than 200 m. Depths greater than 400 m occur in the saddles between Harrison, Hamilton and Belle Isle Banks, and landward of the Belle Isle and Funk Island Banks. The Labrador Current flows southeastward over the shelf and keeps temperatures low ( S M I T H et al.,
1937). The cold intermediate layer of the current is deepest and coldest toward the coast, and temperatures below 0°C are found to depths of about 200 m in many years (PETRIE et al., 1988). Maximum bottom temperatures in the survey area are usually about 4oC. 2.2. STOMACH COLLECTIONS AND EXAMINATION Greenland halibut were caught during random depthstratified bottom-trawl surveys by the R.V. 'Gadus Atlantica' during the autumns of 1981, 1982 and 1984 (Table 1). The locations and sizes of the 58 strata are provided by DOUBLEDAY (1981). In 1981 and 1982 there were two consecutive trips which fished depths of 100 to 1000 m in Div. 2J and 200 to 1000 m in Div. 3K. In 1984 there were three consecutive trips, and depths between 100 and 200 m in northwestern Div. 3K (St. Anthony Shelf and Grey Islands Shelf) were
FOOD OF GREENLAND HALIBUT
213
TABLE 1 Information on stomach collections from Greenland halibut caught during surveys by the R.V. 'Gadus Atlantica' in NAFO Div. 2J3K in 1981, 1982 and 1984. a Number of fishing sets, number of sets in which Greenland halibut were caught, and number of sets from which stomachs were collected; b Number of stomachs collected, and percentage of total catch.
Year
trip numbers
sampling period
number of setsa
number of stomachsb
1981 1982 1984
58-59 71-72 101-103
Nov. 14-Dec. 13 Oct. 30-Dec. 8 Oct. 27-Dec. 5
224 (216) (194) 303 (295) (286) 262 (249) (205)
2915 (27) 4424 (29) 2970 (18)
Total
789 (760) (685)
added to the survey. Depths of 100 to 200 m in southern Div. 3K (Baie Verte Shelf and Fogo Shelf) were not surveyed. In all years, fishing was conducted on a 24-h basis. Greenland halibut were caught in at least 95% of the fishing tows in each year (Table 1). We intended to collect stomachs from a stratified-random sample of up to 3 fish per 5-cm length-group from the catch of every tow. However, stomachs were collected from only 82 to 97% of the tows in which Greenland halibut were caught in each year. Nevertheless, the sampling protocol resulted in the collection of stomachs from 18 to 29% of the total catch in each year, and ensured that sampling was well distributed with respect to predator size and geographic distribution. Stomachs were not collected from fish which showed signs of regurgitation, such as food in the mouth or a flaccid stomach. Stomachs were individually tagged and excised, and fixed and preserved in 4% formaldehyde solution in seawater prior to examination of their contents in the laboratory. Examination involved separation of food items into taxonomic categories. Fish and decapod crustaceans were identified to species, but other groups were combined into higher order taxa. Items in each taxon were placed briefly on absorbent paper to remove excess liquid, and then counted and weighed to the nearest 0.1 g. Whenever digestive condition permitted, fish prey were measured to the nearest mm total length. 2.3. DATA ANALYSIS The relative importance of individual prey taxa was assessed with indices of occurrence, number and weight (CLARK, 1985) and a stomach fullness index. The mean partial fullness index for prey i (PFli) was calculated as:
10309
m TFI= ~. PFI i i=1 where m is the number of prey categories. TFI values as high as 20 were calculated for individual fish. Each index has its advantages and limitations, depending on the question addressed (HYSLOP, 1980). We used the partial fullness index to examine variability related to Greenland halibut size, trawling site and year of sampling, because it emphasizes the weight of specific prey in relation to predator size. For brevity, we have illustrated the influence of predator size and geographic location using only data collected in 1982, the year when fishing intensity was highest and stomach sampling was most successful (Table 1). Observations in 1981 and 1984 were very similar. We estimated the total weight of specific prey in the stomachs of the Greenland halibut population at the time of sampling (WPt) as k 10 WPt= ~, S t~ s,/ ' Us' V~s,l,t s =1 /=1 where/V is the mean number caught per tow, U is the number of sampling units (total area of stratum divided by the area covered by a standard tow), IN is the mean weight of prey, s is the index of stratum, I is the index of 10-cm length group, and t is the index of prey taxon. The number of strata (k) was 56 in 1981, 54 in 1982, and 55 in 1984. All Greenland halibut longer than 89 cm were combined into a single length group. 3. RESULTS 3.1. STOMACH FULLNESS AND PREY SPECTRUM
PFli=!
~ Wii . 104 n J =1 Lj 3
where W/j is the weight of prey i in fish j, Lj is the length of fish j, and n is the number of fish in the sample. Mean total fullness index (TFI) was calculated as:
There was strong similarity among years in the percentage of stomachs which were empty (42 to 48%), the average degree of total stomach fullness (1.41 to 1.44), the prey composition, and the relative importance of individual taxa (Table 2). Fish were the major
214
W.R. BOWERING & G.R. LILLY
TABLE 2 Prey items from stomachs of Greenland halibut caught off northeastern Newfoundland and southern Labrador during autumns of 1981, 1982, and 1984. ( - indicates absence; + indicates presence but percentage <0.05 or PFI <0.005.)
Occurrence (%) 1981 1982 1984
Number (%) 1981 1982 1984
Weight (%)
Mean PFI
1981 1982 1984
1981 1982 1984
Invertebrata (misc.)
0.9
0.4
0.9
0.6
0.3
0.8
0.2
+
0.1
+
+
+
Cephalopoda
4.1
1.7
1.4
2.8
1.3
1.1
2.0
0.6
1.3
0.07
0.04
0.03
26.4 8.8 4.7 1.2 1.0
16.7 3.6 2.9 + 0.8
17.9 5.7 1.5 1.4
34.6 14.5 6.9 1.4 0.9
30.5 10.8 7.8 + 1.0
26.7 10.9 1.9
1.9 0.1 0.1
1.7 + 0.2
1.7 0.1 +
0.06 0.02 0.01
0.04 0.01 +
0.05 0.02 +
--
+
+
--
+
+
--
1.7
+
+
+
+
+
+
Pandalus borealis 3.6 Others + unidentified 5.2 Others + unidentified 4.4
4.8 5.0 1.1
5.0 4.5 2.0
4.0 3.9 3.0
5.4 4.5 0.9
5.9 4.4 1.8
1.0 0.6 0.1
1.1 0.4 +
1.0 0.5 +
0.02 0.01 0.01
0.02 0.01 +
0.02 0.01 +
-
0.2
+
0.2
+
-
0.4
+
Crustacea (total) Hyperiidae Gammaridea Mysidacea Euphausiacea Natantia
Selachii
+
-
+
38.7 18.9 1.2
42.6 23.1 0.1
42.7 21.9 0.9
62.0 41.3 1.5
68.0 45.6 0.1
71.3 45.3 1.0
95.8 46.2 0.6
96.6 45.9 +
95.9 38.0 0.8
1.29 0.89 0.01
1.35 0.99 +
1.32 0.86 0.02
0.4 1.5 Others + unidentified Macrouridae 0.4 Anarhichadidae 0.1 Zoarcidae 0.7 Sebastes sp. 1.6 Pleuronectidae
0.5 0.6 0.1 0.1 0.6 1.6
0.6 1.9 + 0.3 0.2 0.2 3.0
0.2 3.1 0.3 0.1 0.4 1.1
0.4 0.6 0.1 + 0.1 1.3
0.5 2.4
5.1 4.5
5.6 0.6
6.5 0.9
0.02 0.06
0.03 0.01
0.03 0.03
0.2 0.1 0.2 2.3
3.8 0.7 5.9 13.1
1.3 1.0 7.5 11.3
1.2 0.9 1.1 21.6
0.01 + 0.02 0.05
0.01 + 0.03 0.05
0.01 + 0.01 0.09
1.1 1.0 0.3 15.9
1.6 0.7 0.4 15.5
1.1 0.8 0.3 11.8
0.9 0.9 0.2 17.4
1.3 0.6 0.3 17.1
8.6 1.4 0.2 5.8
9.7 3.5 0.5 9.6
10.4 1.6 1.7 10.3
0.05 0.01 + 0.16
0.04 0.01 + 0.19
0.06 0.01 0.01 0.21
1.6
0.7
0.1
1.2
0.6
Pisces (total)
Mallotus villosus Myctophidae Gadidae
Gadus morhua Boreogadus saida
Reinhardtius hippoglossoides
1.4 Others + unidentified 1.1 Others 0.4 Unidentified 14.3 Unidentified + miscellaneous
1.6
Length: mean minimum maximum
-
_
+
--
+
1.42
Total Number of stomachs Percent empty
+
2915 4424 41.5 44.1 45 8 101
45 12 110
_
+
1.44
+
+
1.41
2970 48.1 48 12 105
prey, contributing 62 to 71% of the prey by number, a b o u t 9 6 % of the total prey weight, and 91 to 9 4 % of the total fullness index. The d o m i n a n t fish was capelin, which occurred in o n l y 19 to 2 3 % of the stomachs but contributed 39 to 4 6 % of the total prey weight. Arctic cod (Boreogadus saida) was far less important. Various d e m e r s a l fish, including redfish (Sebastes sp.), G r e e n l a n d halibut and Atlantic cod (Gadus
morhua), occurred in small n u m b e r s but w e r e m o d e r ately important in terms of weight. Skates occurred rarely. Several crustaceans, particularly northern shrimp (Pandalus borealis) and hyperiid and g a m marid a m p h i p o d s , were present in relatively high n u m b e r s but contributed little weight. To study the influence of depth of collection, we g r o u p e d the fish into four categories by depth: the
F O O D OF G R E E N L A N D H A L I B U T
215
TABLE 3 Prey items from stomachs of Greenland halibut caught on the continental shelf (landward of the 400 m isobath at the shelf break) and from three depth zones on the upper slope. Values are mean partial fullness indices. ( - indicates absence; + indicates presence but PFI <0.005.)
Shelf 1981 Invertebrata (misc.)
1982
Slope (Years combined) 1984
401-600
601-800
801-1000
+
+
+
+
+
+
Cephalopoda
0.06
0.04
0.02
0.01
0.18
0.23
Crustacea (total) Hyperiidae Gammaridea Mysidacea Euphausiacea Natantia
0.07 0.02 0.01 + +
0.05 0.01 0.01 + +
0.06 0.02 + +
+ + + + +
0.02 + +
0.01 +
0.02 0,01 0,01
0.02 0.01 +
0.02 0.01 +
+ + +
0.02 +
0.01 -
+
+
Pandalus borealis Others + unidentified Others + unidentified Selachii Pisces (total)
Mallotus villosus Myctophidae Gadidae
Gadus morhua Boreogadus saida Others + unidentified Macrouridae Anarhichadidae Zoarcidae Sebastes sp. Pleuronectidae
Reinhardtius hippoglossoides Others + unidentified Others Unidentified Unidentified + miscellaneous Total Number of stomachs Percent empty Length: mean minimum maximum
+
-
-
-
1.32 0.96 0.01
1.37 1.01 +
1.38 0.94 0.02
1.61 0.88 0.01
0.64 0.14 0.02
0.43 0.02
0.02 0.06 + + 0.02 0.01
0.03 0.02 + + 0.03 0.04
0.03 0.03 + + + 0.01 0.04
0.02 + 0.08 + 0.02 0.49
0.07 + 0.06 0.07 0.18
0.03 0.05 0.13
0.05 0.01 + 0.18
0.04 0.02 + 0.19
0.07 0.01 + 0.23
+ 0.13
0.01 + + 0.09
0.05 0.15
+
+
0.01
+
+
1.45
1.45
1.46
1.63
0.84
0.68
2603 39.1
4147 43.2
2567 45.2
441 53.1
316 69.0
228 72.4
42 8 101
44 12 110
45 12 105
64 21 102
59 32 97
58 37 100
c o n t i n e n t a l s h e l f l a n d w a r d of t h e 4 0 0 m i s o b a t h at t h e s h e l f b r e a k , a n d t h r e e d e p t h z o n e s on t h e u p p e r c o n t i n e n t a l s l o p e (Table 3). T h e fish s a m p l e d on t h e s l o p e w e r e l a r g e r t h a n t h o s e f r o m t h e shelf. T h e freq u e n c y of e m p t y s t o m a c h s i n c r e a s e d with d e p t h , a n d t h e a v e r a g e total f u l l n e s s i n d e x d e c l i n e d with d e p t h , e x c e p t f o r a s m a l l rise in t h e 4 0 0 to 6 0 0 m interval. C a p e l i n w a s t h e d o m i n a n t p r e y at d e p t h s to 6 0 0 m. H y p e r i i d s , n o r t h e r n s h r i m p , Arctic c o d a n d G r e e n -
-
l a n d h a l i b u t w e r e p r e y e d u p o n p r i m a r i l y o n t h e shelf, whereas cephalopods, macrourids and redfish were p r e y e d u p o n m a i n l y on t h e slope. 3.2. I N F L U E N C E O F PREDATOR SIZE In 1982 t h e total f u l l n e s s i n d e x p e a k e d in t h e 25 to 29 cm l e n g t h g r o u p , d e c l i n e d to a m i n i m u m in t h e 55 to 59 cm l e n g t h g r o u p , a n d i n c r e a s e d to a n o t h e r p e a k
216
W.R. B O W E R I N G
2.5
in the 80 to 84 cm length group (Fig. 2). Partial fullness indices for cephalopods and hyperiid amphipods were low for all predator size groups, but were highest in very small specimens ( < 20 cm). Predation on fish was distinctly size-related, with an abrupt change at about 65 to 69 cm from feeding on capelin to feeding on various groundfish. The decline in the total fullness index in the middle of the size range was less pronounced in 1981 and 1984, but otherwise the patterns were similar.
CROUNDFISH
F'.'.'.'.':I CAPEUN n u OTHER RSH I ~ UNID. RSH CEPHALOPODS u HYPERIIDS
X L,=J
2.0 V} (/}
'Z"
& G.R. LILLY
1.5
_J _J
1.0 I-n,-
0.5 .'.:.:::,-::~,:.~::.." 0.0
Fig. 2. Stomach contents in relation to predator length (5-cm length groups) for Greenland halibut collected on the southern Labrador and Northeast Newfoundland Shelves in 1982. The number of stomachs in each length group is shown at the top.
B4 -14
-24
-34
-44
-54
-64
-74
-84
LENGTH (CM)
57
:~ - - ' 55~-,e'
56
~ .... i "
,-
55
54
55
52
51
49
4856
CAPEL/N~,4~STOMACHS
i ~.~.:..
~'
50
55
X NIL
"-
io
0 '
54
,
iI
52
53
•
i:
I I :~
"
"i =
I •o ,
51
' "
52
×
.p
i Ol
~:,
@ .
., •
•
"
~.
... 50
)
,~ 49
.
58
57
56
•
~:~
O•
/ .
.
55
.
.
.
9J
"
54
'
55
52
51
50
49
49
4B
Fig. 3. Mean partial fullness index (PFI) for capelin in stomachs of Greenland halibut (25-64 cm only) by tow in 1982.
FOOD OF GREENLAND HALIBUT
3.3. SPATIAL VARIABILITY
stomach was available. Both variables were transformed (Iogl0(x+l)). There was weak association in 1982 (Pearson correlation coefficient r=0.34, P<0.001, N=286), but not in 1981 (r=0.03, P=0.69, N=190) and 1984 (r=0.07, P=0.31, N=203). In 1982 the capelin were found in largest quantities in stomachs of Greenland halibut from Hamilton Bank and the inner shelf off southern Labrador and northeastern Newfoundland (Fig. 3), whereas the largest catches of medium-sized Greenland halibut were taken in the deep basins of the shelf (Fig. 4). Similar distribution patterns were found in 1981 and 1984.
The Greenland halibut which preyed most intensely on capelin were medium-sized (roughly 20 to 69 cm). Did these Greenland halibut aggregate in areas of high capelin density? The distribution of capelin at the time of the surveys is not known from an independent source. Capelin were caught as a bycatch in the surveys (CARSCADDEN et al., 1989), but these catches are thought to provide no more than a broad overview of capelin distribution, because a nil catch is likely even when capelin are present. As an alternative, we used the mean partial fullness index for capelin in stomachs of Greenland halibut (25 to 64 cm only) from each tow as a measure of how successful the Greenland halibut were in finding capelin, and compared this with the number of medium-sized Greenland halibut caught in each tow. Analysis was restricted to those tows from which at least one 58 56
~
57 ~-T
56
56
r-
r
3.4. WHY DO LARGE GREENLAND HALIBUT NOT FEED ON CAPELIN? Large (> 69 cm) Greenland halibut tended not to feed on capelin (Fig. 2). To determine if this was because they did not co-occur with capelin, we plotted the
54
i
--
55
52
r
51
T
'
).::;>: ......... ~-\;: ""
,'
"1
W,,...
::::~
ook I ~F
S
-"
~v,~r •
250
48 56
,,+ i..a ':." "
i
55
54
• •
Ill
, •
I/.I.
"~
.
55
•
llll
52
r
". ' , ," •
dr." •
'll
1~
• @~ "_~ w'.
."x
•
500
%
°-
•
•
I w -'i
I f~--"--i~i / ~ <~<.-/-e'/
56
,
NIL
" .
""
V
57
49
r
~
'k." t ' , ,
~
~
,, ~/,7
5B
X
',~l" :: e e 'I'm:". • "~& . . , %, • O • i ~ ' " ~t o ',, " , . a l O ::k.• ¢_ ~ g " ..
W
50
-:""
"
%
.~-
'
NUMBER PER TOW
' m":~.:::.
~:~-/1", "t' '" I
217
It
w
~52 •
. ,'~ :," ....
4~,
::e±_
"4/(
51
50
49
48
Fig. 4. Catch (number) of medium-sized (20-69 cm) Greenland halibut by tow in 1982.
218
W.R. BOWERING & G.R. LILLY
56
58 . %
57 i
56 r
,
56
,
,
54 I
53
52 i
~:'~....... 55 ~'-
×" ×
50 f
49
4856
NUMBER PEB TOW
'
X
- .. _
X~X,,/ '
,...• . ~ , L~ 54
51 1
?
,i
.,
55
•
54
t
I t l i ~ ~
NIL
>-
~
53
~I I I
452
.,
.o6 i
51 i
.~_ ; , x , ~ ~
x
~::~ ,~ t~ xIIxt ~,
i
50
"""
,:o
't 49 ,58
57
56
. . . . . . 55 54
~
~
.~
/
" 55
,~
52
51
', 50
s 40
49
48
Fig. 5. Catch (number) of large (>69 cm) Greenland halibut by tow in 1982. geographic distribution of large Greenland halibut and compared it with the geographic distribution of capelin in stomachs of smaller Greenland halibut (25 to 64 cm only). In 1982 the large Greenland halibut tended to occur on the upper continental slope and in the deep water of the saddles, particularly Hawke Saddle (Fig. 5). Thus, many were outside the areas of highest capelin availability (Fig. 3). However, some overlap occurred, particularly on the outer slope of Hamilton Bank. To determine if large Greenland halibut tended not to feed on capelin even when capelin were available, we selected from all three years those tows in which the mean PFI for capelin in stomachs of 25 to 64 cm Greenland halibut was greater than 1.0, the number of stomachs on which the PFI for capelin was based was greater than 4, and the catch of Greenland halibut longer than 69 cm was greater than 5. We combined the data from the 28 tows so selected, and found that even though the
Greenland halibut in the length-range 20 to 64 cm fed intensively on capelin (PFI values of 3 to 4), the Greenland halibut longer than 69 cm fed primarily on groundfish (Fig. 6). This observation was not affected by small variations in the criteria for selection of tows. 3.5. WEIGHT OF PREY IN STOMACHS OF THE POPULATION OF GREENLAND HALIBUT In estimating the weight of prey in the stomachs of the Greenland halibut population at the time of sampling, we grouped the prey into four taxa: invertebrates, capelin, groundfish, and other fish. Unidentified fish were allocated to the three fish categories in proportion to the weight of the three categories in each combination of stratum and length group. In 1982 the major consumers of capelin were Greenland halibut in the 30 to 59 cm range, whereas the major consumers of groundfish were in the 70 to
FOOD OF GREENLAND HALIBUT
5.0
13
21
38
33
61
57
I
I
I
I
I
I
X ~'~ f-3 4 . 0 Z
77 74- 77 58 I
I
I
64- 51
I
I
F~ I ~ ~
~
(/) (Y)
1
54 I
44 72 I
GROUNDFISH CAPELIN OTHER F~SH UNID. FISH CEPHALOPODS HYPERIIOS OTHER
"
3500 3000
F/T///A
INVERT.
=~--
OTHER
FISH
I:';.:';.:';.:1 GROUNDFISH C,o o x ~
CAPELIN
2500 ::::::::::::::::::::::::::
,,, 5.0 Z d d ::3
219
iii,!iiiii!ii!;!i:j i
(/) 2000 Z 0 I-- 1500
2.0
.--I
1000 p.-
.~ 1.0 a.
5OO
0.0
24 -14
-24
-34
-44
-54
-64
-74
0 1981
84
LENGTH (CM) length groups) for Greenland halibut collected in 28 tows selected for a high PFI for capelin and the occurrence of more than 5 large Greenland halibut. The number of stomachs is shown at the top. 89 cm length-range (Table 4). The total weight of prey estimated to be in the stomachs increased from 1938 tons in 1981 to 3270 tons in 1984 (Fig. 7), in part because of an increase in the mean catch of Greenland halibut per tow (BOWERING et al., 1990). Capelin contributed 62 to 73% of the total weight. TABLE 4 The weight (tons) of specific prey categories in the stomachs of 10-cm length groups of the Greenland halibut population at the time of sampling in 1982. capelin 0.0
1984-
YEAR
Fig. 6. Stomach contents in relation to predator length (5-cm
Greenland halibut inverlength group tebrates
1982
ground fish
other fish
0.0
0.0
1-9
0.0
10-19 20-29 30-39 40-49 50-59 60-69 70-79 80-89 >89
1.1 11.8 8.6 23.2 23.3 3.1 1.8 9.8 0.4
0.2 98.9 403.8 602.1 459.6 142.9 15.0 24.0 8.7
<0.1 0.3 4.7 14.9 32.7 45.5 162.9 251.7 85.2
0.0 0.3 7.0 12.0 3.5 0.1 4.1 0.0 1.2
Total
83.2
1755.3
597.9
28.2
3.6. ANNUAL CONSUMPTION BY GREENLAND HALIBUT
Fig. 7. Total weight of prey in the stomachs of the Greenland halibut population at the time of sampling each year. and there is still uncertainty about the pattern of gastric evacuation in piscivores (LILLY, 1991). YANG & LIVINGSTON (1988) estimated daily ration of Greenland halibut in the eastern Bering Sea by employing the model proposed by ELLIOTT & PERSSON (1978), parameterized with gastric evacuation data for walleye pollock (DWYER et al., 1987). We assumed that the daily rations estimated for Greenland halibut in the Bering Sea could be applied to the Greenland halibut collected off Labrador and Newfoundland if the prey types, temperatures and mean stomach content weights were similar. The major prey in both areas were fish. The weighted mean temperature at capture for Greenland halibut off Labrador and Newfoundland varied from 1.9°C in 1982 to 2.5°C in 1981. This is only slightly lower than the 2.6 to 3.0°C reported for the Bering Sea. To determine whether mean stomach content weights were similar, we first calculated mean total fullness indices for 3-hour intervals of the 24-h day. The fullness indices showed some variability, especially in the 60 to 69 cm length group (Fig. 8), but we concluded from visual inspection that there was no diel pattern. This is in agreement with the conclusion of YANG & LIVINGSTON (1988). Because no diel pattern was detected, we calculated a mean stomach content weight, as a percentage of body weight (% BW), for all stomachs in each 10-cm length group. In this we differed from YANG & LIVINGSTON (1988), who calculated mean stomach content weight (S) as: T~=~ S i l m '
We did not estimate the rate of prey consumption by Greenland halibut in each length group and stratum because information on gastric evacuation rate in this species is lacking (YANG & LIVINGSTON, 1988),
where S i is the mean stomach content weight (% BW) in each time interval (i) for a total of m intervals. We did not record individual fish weights at sea, and
220
W.R. BOWERING & G.R. LILLY
3.0 20-29 Cm
25 167
1.5
t
183
,i7 ,i6 ,i5 ,i7 ,i 2i7 i
25 20
4 0 - 4 9 Cm
362 283
325 I 365 323 337 311 3i3
°t ~10 -J
_J30 99
60-69 Cm
25 2O
101 130
15 117
I0
li5
t
li0
t
4. DISCUSSION
115
05 O0 0
followed YANG & LIVINGSTON (1988) in estimating weights from a weight-length relationship. Mean stomach content weight (% BW) was highest in small (20 to 29 cm) fish and large (80 to 89 cm) fish (Table 5). The actual values depend on the weight-length relationship used, but are similar to those estimated for Greenland halibut from the Bering Sea (Table 5). To convert stomach content weight to daily feeding rate, we took advantage of the fact that the estimated daily ration (% BW) was approximately 48% of the mean stomach content weight (% BW) for all sizes of Greenland halibut examined by YANG & LIVINGSTON (1988; their table 3). By multiplying the quantity of capelin estimated to be in the stomachs of the population (Table 4, Fig. 7) by 0.48, we estimated that the daily rate of consumption of capelin by Greenland halibut was 575, 842 and 1140 tons in 1981, 1982 and 1984 respectively. If we further assume that Greenland halibut fed on capelin at this rate for six months of the year, then annual consumption was 105, 154 and 208 thousand tons in 1981, 1982 and 1984 respectively.
:1
12 TIME(HOUR)
24
Fig. 8. Diel changes in total fullness index (mean and 950/0 confidence interval) in three length groups of Greenland halibut. Data from all three years were combined. The number above each bar is the sample size.
Our observations of the stomach contents of Greenland halibut from the southern Labrador and Northeast Newfoundland Shelves agree with reports from elsewhere that small Greenland halibut tend to feed on plankton and that larger Greenland halibut feed almost entirely in the water column and predominantly on fish (SMID'r, 1969; LEAR, 1970; YANG & LIVINGSTON, 1988). In the present study, small (<20 cm) individuals fed primarily on small crustaceans (mainly hyperiid amphipods) and cephalopods, some of
TABLE 5 The mean stomach content weight of Greenland halibut, expressed as a percentage of body weight (% B W + SE). Data from all 3 years and all times of the day were combined. N =number of stomachs, aWeight of each fish was estimated from W=0.006072 L3"°886(YANG& LIVINGSTON(1988)) bWeight of each fish was estimated from W=0.002184 L 3'3454 (BOWERING & STANSBURY(1984)); CFrom table 3 of YANG& LIVINGSTON(1988). Mean stomach content weight (% BW + SE) Labrador and Newfoundland Green/and hafibut length group
10-19 20-29 30-39 40-49 50-59 60-69 70-79 80-89
N
318 1435 1976 2639 2174 903 463 282
YANG & LIVINGSTONE BOWERING& STANSBURY (1988)a (1984)b
1.11 +0.176 2.22 ::1:0.090 2.07 + 0.069 1.56 + 0.056 1.30 _+0.061 1.24 + 0.091 1.69 + 0.143 2.35 + 0.192
1.48+0.232 2.69 + 0.109 2.32 -I-0.077 1.64 + 0.059 1.30 -I-0.061 1.19 ::t:0.087 1.56 + 0.132 2.10 _+0.171
Bedng Sea c
}
1.43
I
1.33
}
2.43
FOOD OF GREENLAND HALIBUT
which were identified as Gonatus sp. Medium-sized (20 to 69 cm) individuals fed primarily on capelin, the dominant mid-sized (10 to 18 cm) schooling planktivore in this area (CARSCADDEN, 1984). Large (>69 cm) individuals fed primarily on a variety of demersal fish larger than capelin. Northern shrimp (Pandalus borealis) were not as important as prey in Div. 2J3K as a whole as they are on commercial shrimp grounds off Labrador (BOWERING et al., 1984) and west Greenland (SMIDT, 1969). Certain species of epibenthos, notably crabs, are available to fish in this region, as is evident from their occurrence in the stomachs of cod (Gadus morhua) (LILLY, 1984, 1991), but they were rare in Greenland halibut stomachs. Greenland halibut were broadly distributed over the shelves, and were not highly aggregated in those areas where they were most successful in finding capelin. Medium-sized (20 to 69 cm) individuals were most abundant in the deep regions of the continental shelf, and large (>69 cm) individuals were most abundant in the deep water of the saddles and along the upper slope. This is in agreement with the conclusion of a more extensive study of Greenland halibut distribution (BOWERING & CHUMAKOV, 1989). The degree of overlap with capelin may be highly variable, even if Greenland halibut distribution is not variable, because the distribution of capelin at the time of the annual bottom-trawl survey varies among years (CARSCADDEN et al., 1989; LILLY, 1991), and there is evidence that capelin move from the southern Labrador region to the northeast Newfoundland region during the autumn (BAKANEV & GORCHINSKY, 1985; CARSCADDEN et al., 1987). Our estimates of the quantity of capelin and other prey consumed by Greenland halibut may be improved in several ways. The estimates of population numbers in each length group and stratum assume that the catchability coefficient of the trawl is 1.0. If the true value is less, then the population size and consumption of prey will be higher. A recent attempt to obtain population numbers from a sequential population analysis was unsuccessful (BOWERING et al., 1990). In converting stomach content data to feeding rate, we assumed that the daily rates estimated for Greenland halibut in the Bering Sea could be applied to Greenland halibut off Labrador and Newfoundland. The rates estimated for the Bering Sea fish involved many assumptions (YANG& LIVINGSTON, 1988). We require additional study into the nature of the gastric evacuation process in piscivorous fish (BROMLEY, 1988), and parameterization of gastric evacuation models with data obtained directly from Greenland halibut. We also require stomach content data at times other than late autumn. We assumed that Greenland halibut preyed on capelin for only six months each year because CHUMAKOV & PODRAZHANSKAYA (1986) reported that Greenland
221
halibut off Labrador and eastern Newfoundland (NAFO Subareas 2 and 3) fed more intensively in summer and autumn than in winter and spring. However, CHUMAKOV & PODRAZHANSKAYA(1986) also found that the intensity of feeding declined by November and December from a peak in August to October, so our estimates may be conservative for the summer period. In addition, LEAR (1970) found that Greenland halibut in Trinity Bay preyed on capelin throughout the year, with the frequency of occurrence and percentage by volume being high in the period mid-January to mid-April. Thus, Greenland halibut probably prey on capelin in the winter in Div. 2J3K if their distributions overlap, but information on this is lacking. We estimate that Greenland halibut consumed 100 to 200 thousand tons of capelin annually during the period 1981-84. We have not tried to calculate the precision of these estimates, and we recognize that many factors contribute to the accuracy, but we have tried to be conservative. Nevertheless, the present point estimates are substantial compared to hydroacoustic estimates of standing stock of capelin during the same period: viz. 94 to 1494 thousand tons from Canadian surveys and 263 to 852 thousand tons from USSR surveys (CARSCADDENet al., 1989; LILLY, 1991). Landings during this period were restricted by quota to 12 to 24 thousand tons (CARSOADDEN et al., 1989). Earlier studies have focused on cod, seals, baleen whales and sea birds as important natural predators on capelin (BROWN & NETTLESHIP, 1984; CARSCADDEN, 1984; ANDERSON & LILLY, 1985). Greenland halibut should be added to this list. 5. REFERENCES
ALTON, M.S., R.G. BAKKALA,G.E. WALTERS& P.T. MUNRO, 1988. Greenland turbot Reinhardtius hippog/ossoides of the eastern Bering Sea and Aleutian Islands region.--U.S. Department of Commerce, NOAA Technical report NMFS 71: 1-31. ANDERSON, J.T. & G.R. LILLY, 1985. Review of reported biological and technological interactions for commercial marine species of the Newfoundland region. In: R. MAHON. Towards the inclusion of fishery interactions in management advice.--Can. Tech. Rep. Fish. Aquat. Sci. 1347: 34-53. BAKANEV,Y.S.& K.V.GORCHINSKY,1985. Hydroacousticsurvey of capelin stocks in Divisions 2J3K and trawl survey of capelin prerecruits in Divisions 3KLNO in November 1 9 8 4 - January 1985.-- Northwest Atlantic Fisheries Organization, Res. Doc. 85•52, Serial No. N1001: 1-11. BOWERING, W.R. & D.E. STANSBURY,1984. Regressions of weight on length for Greenland halibut, Reinhardtius hippog/ossoides, from Canadian waters of the northwest Atlantic.--J. Northw. Atl. Fish. Sci. 5: 107-108. BOWERING,W.R. & A.K. CHUMAKOV,1989. Distribution and relative abundance of Greenland halibut (Reinhard-
222
W.R. BOWERING & G.R. LILLY
tius hippoglossoides (Walbaum)) in the Canadian northwest Atlantic from Davis Strait to the northern Grand Bank.--Fish. Res. 7: 301-327. BOWERING,W.R., D.G. PARSONS& G.R. LILLY,1984. Predation on shrimp (Pandalus borealis) by Greenland halibut (Reinhardtius hippoglossoides) and Atlantic cod (Gadus morhua) off Labrador.--ICES C.M. 1984/G:54: 1-30. BOWERING, W.R., w.a. BRODIE & J.W. BAIRD, 1990. An assessment of the Greenland halibut stock component in NAFO Subarea 2 and Divisions 3K and 3L.-Northwest Atlantic Fisheries Organization, Res. Doc. 90/51, Serial No. N1772: 1-21. BROMLEY, P.J., 1988. Gastric digestion and evacuation in whiting, Merlangius merlangus (L.).--J. Fish Biol. 33: 331-338. BROWN, R.G.B. & D.N. NETTLESHIP,1984. Capelin and seabirds in the northwest Atlantic. In: D.N. NETTLESHIP, G.A. SANGER & P.F. SPRINGER. Marine birds: their feeding ecology and commercial fisheries relationships. Proceedings of the Pacific Seabird Group Symposium, Seattle, Washington, 6-8 January, 1982: 184-194. CARSCADDEN,J.E., 1984. Capelin in the Northwest Atlantic. In: D.N. NETTLESHIP,G.A. SANGER & P.F. SPRINGER. Marine birds: their feeding ecology and commercial fisheries relationships. Proceedings of the Pacific Seabird Group Symposium, Seattle, Washington, 6-8 January, 1982: 170-183. CARSCADDEN, J., O.S. MILLER,B.S. NAKASHIMA,R. HARNUM & D.B. ATKINSON, 1987. Capelin in SA2 + Div. 3K. Canadian Atlantic Fisheries Scientific Advisory Committee, Res. Doc. 87/12: 1-37.
CARSCADDEN,J., D.S. MILLER& G.R. LILLY,1989. Capelin in SA2 + Div. 3K: results from offshore research. Canadian Atlantic Fisheries Scientific Advisory Committee, Res. Doc. 89•78: 1-44. CHUMAKOV,A.K. & S.G. PODRAZHANSKAYA,1986. Feeding of Greenland halibut (Reinhardtius hippog/ossoides) in the Northwest Atlantic.--NAFO Sci. Coun. Studies 10: 47-52. CLARK, M.R., 1985. The food and feeding of seven fish species from the Campbell Plateau, New Zealand.--New Zealand J. Mar. Freshw. Res. 19: 339-363. DOUBLEDAY,W.G., 1981. Manual on groundfish surveys in the Northwest Atlantic.--Northw. Atl. Fish. ORB., Sci. Coun. Studies 2: 7-55.
DWYER, D.A., K.M. BAILEY & P.A. LIVINGSTON,1987. Feeding habits and daily ration of walleye pollock (Theragra chalcogramma) in the eastern Bering Sea, with special reference to cannibalism.--Can. J. Fish. Aquat. Sol. 44" 1972-1984. ELLIOTT,J.M. & L. PERSSON, 1978. The estimation of daily rates of food consumption for fish.--J. Anim. Ecol. 47: 977-991. GROOT, S.J. DE, 1970. Some notes on an ambivalent behaviour of the Greenland halibut Reinhardtius hippog/ossoides (Walb.) Pisces: Pleuronectiformes.--J. Fish Biol. 2: 275-279. HAUG, T. & B. GULLIKSEN, 1982. Size, age, occurrence, growth and food of Greenland halibut, Reinhardtius hippoglossoides (Walbaum) in coastal waters of western Spitzbergen.--Sarsia 68: 293-297. HYSLOP,E.J., 1980. Stomach contents analysis - a review of methods and their application.--J. Fish Biol. 17: 411-429. LEAR, W.H., 1970. The biology and fishery of the Greenland halibut (Reinhardtius hippog/ossoides) (Walbaum) in the Newfoundland area. M.Sc. Thesis, Memorial University of Newfoundland, St. John's: 1-132. LILLY, G.R., 1984. Predation by Atlantic cod on shrimp and crabs off northeastern Newfoundland in autumn of 1977-82.--ICES C.M.1984/G:53: 1-25. - - - - , 1991. Interannual variability in predation by cod (Gac/us morhua) on capelin (Ma//otus vi/Iosus) and other prey off southern Labrador and northeastern Newfoundland.--ICES mar. Sci. Symp. 193: 133-146.
PETRIE, B., S. AKENHEAD,J. LAZIER& J. LODER, 1988. The cold intermediate layer on the Labrador and Northeast Newfoundland Shelves, 1978-86.--Northw. Atl. Fish. ORB., Sci. Coun. Studies 12: 57-69. SMIDT, E.L.B., 1969. The Greenland halibut, Reinhardtius hippoglossoides (Walb.), biology and exploitation in Greenland waters.--Meddr Danm. Fisk.-og Havunders. 6: 79-148. SMITH, E.H., F.M. SOULE & O. MOSBY,1937. The Marion and General Greene expeditions to Davis Strait and Labrador Sea, 1928-1935. Scientific results, part 2: Physical oceanography.--U.S, Treasury Dept., Coast Guard Bull. 19: 1-259. YANG, M.S. & PA. LIVINGSTON,1988. Food habits and daily ration of Greenland halibut, Reinhardtius hippog/ossoides, in the eastern Bering Sea.--Fish. Bull. 86: 675-690.
Netherlands Journal of Sea Research 29 (1-3): 211-222 (1992)
GREENLAND HALIBUT (REINHARDTIUSHIPPOGLOSSOIDES)OFF SOUTHERN LABRADOR AND NORTHEASTERN NEWFOUNDLAND (NORTHWEST ATLANTIC) FEED PRIMARILY ON CAPELIN (MALLOTUSVlLLOSUS) W.R. BOWERING* and G.R. LILLY* Department of Fisheries and Oceans, P.O. Box 5667, St. John's, Newfoundland, Canada AIC 5Xl ABSTRACT Stomachs were collected from 10 300 Greenland halibut (Reinhardtius hippoglossoides) caught during the autumns of 1981, 1982 and 1984 on the continental shelf and upper slope off southern Labrador and northeastern Newfoundland (northwest Atlantic). Examination revealed strong similarity among years in the percentage of stomachs which were empty (42 to 48%), the average degree of stomach fullness, and the prey spectrum. Small ( < 2 0 cm) Greenland halibut preyed mainly on small crustaceans and cephalopods, medium-sized (20 to 69 cm) individuals preyed primarily on capelin (Mallotus villosus), and large ( > 6 9 cm) individuals preyed on a variety of demersal fish, particularly redfish (Sebastes sp.) and Greenland halibut. An abrupt change in diet at about 64 to 69 cm was related to changes in both feeding habit and geographic distribution. The quantity of capelin in the stomachs was greatest on Hamilton Bank and on or near the coastal shelf off southern Labrador and northeastern Newfoundland. Medium-sized Greenland halibut were not highly aggregated in those areas where they were most successful in finding capelin. Preliminary estimates of daily and annual prey consumption indicate that Greenland halibut is an important predator of capelin. 1. INTRODUCTION This paper describes the food of Greenland halibut (Reinhardtius hippoglossoides) on the continental shelf and upper slope off southern Labrador and northeastern Newfoundland in the northwest Atlantic (northwest Atlantic Fisheries Organization (NAFO) Div. 2J3K, Fig. 1). The Greenland halibut is one of the major demersal species in this area. During the period 1981-84 it contributed 7 to 13% of the annual catch of groundfish and represented 10 to 20% of the *Authorship equal
trawlable biomass estimated from annual bottomtrawl surveys conducted by the Department of Fisheries and Oceans, Canada. Despite its abundance and commercial importance, its role in the trophic interactions in this area is poorly known. Studies of the food of Greenland halibut in the eastern Atlantic (HAUG & GULLIKSEN, 1982), off Greenland (SMIDT, 1969; DE GROOT, 1970) and in the Bering Sea (ALTON et al., 1988; YANG & LIVINGSTON, 1988) have shown that this species feeds predominantly on plankton when it is small and changes to nekton, mainly fish, as it gets larger. It seldom takes invertebrates that stay on the bottom. CHUMAKOV & PODRAZHANSKAYA (1986) found that the most frequently occurring prey off Labrador and eastern Newfoundland were small fish, notably myctophids, capelin (Mallotus villosus) and sand lance (Ammodytes sp.), and various crustaceans, notably the northern shrimp (Pandalus borealis). Their data were aggregated over very broad geographic areas (NAFO Subareas 2 and 3) and provided prey composition by weight for only a small number of fish. LEAR (1970) provided quantitative stomach content data for Trinity Bay on the east coast of Newfoundland, where the dominant prey during the late 1960's was capelin. We expand upon earlier studies in the northwest Atlantic by providing stomach content data by weight with relatively fine size and spatial resolution for the whole offshore region of NAFO Div. 2J3K. We also provide an estimate of the weight of major prey taxa in the stomachs of the population at the time of sampling, and use published information on daily ration to estimate the annual consumption of capelin. Acknowledgements.--We wish to thank the many scientists and technicians who participated in collection of the Greenland halibut stomachs. We also thank C. Butt, H. Collins and P. Bemister for examining the stomach contents, and D. Porter, D. Davis and C. Butt for help in preparing the figures. Several anonymous reviewers provided useful comments on the manuscript.
212
W.R BOWERING & G.R. LILLY
56
ii :i
.6
,
-~
53
54
,
52
,
,
r~
i
51
,
i
50
~--
i
.\.
2H
L" - H A ; R R ] S Q N 55 -'-'~-- L BANK,
• L
:~:..:-... ~,..T~
~'~ "
L,:I /
54
~
"<%Z...
j~"
55
0///
"~
COASTLINE 200 rn ...... 400 m ................ 800 ~ ___ _
-
.
@ LABRADOR
~,~' "~ / P ~
54
i!
B
.
53
2J
BELLE ISLE i 52i___
J
BANK
c • .
i /
3K
ST ANTHONY
.
SHEEF
51 y . ~ /
FUNK SLAND DEEP
GRAY,~ " ~ ~LrSLAt~D ~ - " ~HEPL F
<~
IVEBTE
51
FUNK SLAND
BANK
-~
-50 .
.
.
.
..
FOG0
2 ~ 1 ~
NEWFOUNDLAND 49
. 58
. 57
-
. 56
55
. 54
. 53
52
51
50
JLLE-- . . . . 49 49 48
Fig. 1. Map of study area, showing major physiographic features and NAFO Divisions. 2. METHODS AND MATERIALS 2.1. STUDY AREA The study area in NAFO Div. 2J3K encompasses 189 508 km 2 on the southern Labrador Shelf, the northeast Newfoundland Shelf, and the adjacent continental slope to a depth of 1000 m (Fig. 1). The continental shelf in this area is broad and deep; 80% of the survey area is deeper than 200 m, and 24% is within 301 to 400 m. Hamilton Bank in the northwest has an extensive plateau less than 200 m in depth, whereas Belle Isle Bank and Funk Island Bank to the south have only small areas shallower than 200 m. Depths greater than 400 m occur in the saddles between Harrison, Hamilton and Belle Isle Banks, and landward of the Belle Isle and Funk Island Banks. The Labrador Current flows southeastward over the shelf and keeps temperatures low ( S M I T H et al.,
1937). The cold intermediate layer of the current is deepest and coldest toward the coast, and temperatures below 0°C are found to depths of about 200 m in many years (PETRIE et al., 1988). Maximum bottom temperatures in the survey area are usually about 4oC. 2.2. STOMACH COLLECTIONS AND EXAMINATION Greenland halibut were caught during random depthstratified bottom-trawl surveys by the R.V. 'Gadus Atlantica' during the autumns of 1981, 1982 and 1984 (Table 1). The locations and sizes of the 58 strata are provided by DOUBLEDAY (1981). In 1981 and 1982 there were two consecutive trips which fished depths of 100 to 1000 m in Div. 2J and 200 to 1000 m in Div. 3K. In 1984 there were three consecutive trips, and depths between 100 and 200 m in northwestern Div. 3K (St. Anthony Shelf and Grey Islands Shelf) were
FOOD OF GREENLAND HALIBUT
213
TABLE 1 Information on stomach collections from Greenland halibut caught during surveys by the R.V. 'Gadus Atlantica' in NAFO Div. 2J3K in 1981, 1982 and 1984. a Number of fishing sets, number of sets in which Greenland halibut were caught, and number of sets from which stomachs were collected; b Number of stomachs collected, and percentage of total catch.
Year
trip numbers
sampling period
number of setsa
number of stomachsb
1981 1982 1984
58-59 71-72 101-103
Nov. 14-Dec. 13 Oct. 30-Dec. 8 Oct. 27-Dec. 5
224 (216) (194) 303 (295) (286) 262 (249) (205)
2915 (27) 4424 (29) 2970 (18)
Total
789 (760) (685)
added to the survey. Depths of 100 to 200 m in southern Div. 3K (Baie Verte Shelf and Fogo Shelf) were not surveyed. In all years, fishing was conducted on a 24-h basis. Greenland halibut were caught in at least 95% of the fishing tows in each year (Table 1). We intended to collect stomachs from a stratified-random sample of up to 3 fish per 5-cm length-group from the catch of every tow. However, stomachs were collected from only 82 to 97% of the tows in which Greenland halibut were caught in each year. Nevertheless, the sampling protocol resulted in the collection of stomachs from 18 to 29% of the total catch in each year, and ensured that sampling was well distributed with respect to predator size and geographic distribution. Stomachs were not collected from fish which showed signs of regurgitation, such as food in the mouth or a flaccid stomach. Stomachs were individually tagged and excised, and fixed and preserved in 4% formaldehyde solution in seawater prior to examination of their contents in the laboratory. Examination involved separation of food items into taxonomic categories. Fish and decapod crustaceans were identified to species, but other groups were combined into higher order taxa. Items in each taxon were placed briefly on absorbent paper to remove excess liquid, and then counted and weighed to the nearest 0.1 g. Whenever digestive condition permitted, fish prey were measured to the nearest mm total length. 2.3. DATA ANALYSIS The relative importance of individual prey taxa was assessed with indices of occurrence, number and weight (CLARK, 1985) and a stomach fullness index. The mean partial fullness index for prey i (PFli) was calculated as:
10309
m TFI= ~. PFI i i=1 where m is the number of prey categories. TFI values as high as 20 were calculated for individual fish. Each index has its advantages and limitations, depending on the question addressed (HYSLOP, 1980). We used the partial fullness index to examine variability related to Greenland halibut size, trawling site and year of sampling, because it emphasizes the weight of specific prey in relation to predator size. For brevity, we have illustrated the influence of predator size and geographic location using only data collected in 1982, the year when fishing intensity was highest and stomach sampling was most successful (Table 1). Observations in 1981 and 1984 were very similar. We estimated the total weight of specific prey in the stomachs of the Greenland halibut population at the time of sampling (WPt) as k 10 WPt= ~, S t~ s,/ ' Us' V~s,l,t s =1 /=1 where/V is the mean number caught per tow, U is the number of sampling units (total area of stratum divided by the area covered by a standard tow), IN is the mean weight of prey, s is the index of stratum, I is the index of 10-cm length group, and t is the index of prey taxon. The number of strata (k) was 56 in 1981, 54 in 1982, and 55 in 1984. All Greenland halibut longer than 89 cm were combined into a single length group. 3. RESULTS 3.1. STOMACH FULLNESS AND PREY SPECTRUM
PFli=!
~ Wii . 104 n J =1 Lj 3
where W/j is the weight of prey i in fish j, Lj is the length of fish j, and n is the number of fish in the sample. Mean total fullness index (TFI) was calculated as:
There was strong similarity among years in the percentage of stomachs which were empty (42 to 48%), the average degree of total stomach fullness (1.41 to 1.44), the prey composition, and the relative importance of individual taxa (Table 2). Fish were the major
214
W.R. BOWERING & G.R. LILLY
TABLE 2 Prey items from stomachs of Greenland halibut caught off northeastern Newfoundland and southern Labrador during autumns of 1981, 1982, and 1984. ( - indicates absence; + indicates presence but percentage <0.05 or PFI <0.005.)
Occurrence (%) 1981 1982 1984
Number (%) 1981 1982 1984
Weight (%)
Mean PFI
1981 1982 1984
1981 1982 1984
Invertebrata (misc.)
0.9
0.4
0.9
0.6
0.3
0.8
0.2
+
0.1
+
+
+
Cephalopoda
4.1
1.7
1.4
2.8
1.3
1.1
2.0
0.6
1.3
0.07
0.04
0.03
26.4 8.8 4.7 1.2 1.0
16.7 3.6 2.9 + 0.8
17.9 5.7 1.5 1.4
34.6 14.5 6.9 1.4 0.9
30.5 10.8 7.8 + 1.0
26.7 10.9 1.9
1.9 0.1 0.1
1.7 + 0.2
1.7 0.1 +
0.06 0.02 0.01
0.04 0.01 +
0.05 0.02 +
--
+
+
--
+
+
--
1.7
+
+
+
+
+
+
Pandalus borealis 3.6 Others + unidentified 5.2 Others + unidentified 4.4
4.8 5.0 1.1
5.0 4.5 2.0
4.0 3.9 3.0
5.4 4.5 0.9
5.9 4.4 1.8
1.0 0.6 0.1
1.1 0.4 +
1.0 0.5 +
0.02 0.01 0.01
0.02 0.01 +
0.02 0.01 +
-
0.2
+
0.2
+
-
0.4
+
Crustacea (total) Hyperiidae Gammaridea Mysidacea Euphausiacea Natantia
Selachii
+
-
+
38.7 18.9 1.2
42.6 23.1 0.1
42.7 21.9 0.9
62.0 41.3 1.5
68.0 45.6 0.1
71.3 45.3 1.0
95.8 46.2 0.6
96.6 45.9 +
95.9 38.0 0.8
1.29 0.89 0.01
1.35 0.99 +
1.32 0.86 0.02
0.4 1.5 Others + unidentified Macrouridae 0.4 Anarhichadidae 0.1 Zoarcidae 0.7 Sebastes sp. 1.6 Pleuronectidae
0.5 0.6 0.1 0.1 0.6 1.6
0.6 1.9 + 0.3 0.2 0.2 3.0
0.2 3.1 0.3 0.1 0.4 1.1
0.4 0.6 0.1 + 0.1 1.3
0.5 2.4
5.1 4.5
5.6 0.6
6.5 0.9
0.02 0.06
0.03 0.01
0.03 0.03
0.2 0.1 0.2 2.3
3.8 0.7 5.9 13.1
1.3 1.0 7.5 11.3
1.2 0.9 1.1 21.6
0.01 + 0.02 0.05
0.01 + 0.03 0.05
0.01 + 0.01 0.09
1.1 1.0 0.3 15.9
1.6 0.7 0.4 15.5
1.1 0.8 0.3 11.8
0.9 0.9 0.2 17.4
1.3 0.6 0.3 17.1
8.6 1.4 0.2 5.8
9.7 3.5 0.5 9.6
10.4 1.6 1.7 10.3
0.05 0.01 + 0.16
0.04 0.01 + 0.19
0.06 0.01 0.01 0.21
1.6
0.7
0.1
1.2
0.6
Pisces (total)
Mallotus villosus Myctophidae Gadidae
Gadus morhua Boreogadus saida
Reinhardtius hippoglossoides
1.4 Others + unidentified 1.1 Others 0.4 Unidentified 14.3 Unidentified + miscellaneous
1.6
Length: mean minimum maximum
-
_
+
--
+
1.42
Total Number of stomachs Percent empty
+
2915 4424 41.5 44.1 45 8 101
45 12 110
_
+
1.44
+
+
1.41
2970 48.1 48 12 105
prey, contributing 62 to 71% of the prey by number, a b o u t 9 6 % of the total prey weight, and 91 to 9 4 % of the total fullness index. The d o m i n a n t fish was capelin, which occurred in o n l y 19 to 2 3 % of the stomachs but contributed 39 to 4 6 % of the total prey weight. Arctic cod (Boreogadus saida) was far less important. Various d e m e r s a l fish, including redfish (Sebastes sp.), G r e e n l a n d halibut and Atlantic cod (Gadus
morhua), occurred in small n u m b e r s but w e r e m o d e r ately important in terms of weight. Skates occurred rarely. Several crustaceans, particularly northern shrimp (Pandalus borealis) and hyperiid and g a m marid a m p h i p o d s , were present in relatively high n u m b e r s but contributed little weight. To study the influence of depth of collection, we g r o u p e d the fish into four categories by depth: the
F O O D OF G R E E N L A N D H A L I B U T
215
TABLE 3 Prey items from stomachs of Greenland halibut caught on the continental shelf (landward of the 400 m isobath at the shelf break) and from three depth zones on the upper slope. Values are mean partial fullness indices. ( - indicates absence; + indicates presence but PFI <0.005.)
Shelf 1981 Invertebrata (misc.)
1982
Slope (Years combined) 1984
401-600
601-800
801-1000
+
+
+
+
+
+
Cephalopoda
0.06
0.04
0.02
0.01
0.18
0.23
Crustacea (total) Hyperiidae Gammaridea Mysidacea Euphausiacea Natantia
0.07 0.02 0.01 + +
0.05 0.01 0.01 + +
0.06 0.02 + +
+ + + + +
0.02 + +
0.01 +
0.02 0,01 0,01
0.02 0.01 +
0.02 0.01 +
+ + +
0.02 +
0.01 -
+
+
Pandalus borealis Others + unidentified Others + unidentified Selachii Pisces (total)
Mallotus villosus Myctophidae Gadidae
Gadus morhua Boreogadus saida Others + unidentified Macrouridae Anarhichadidae Zoarcidae Sebastes sp. Pleuronectidae
Reinhardtius hippoglossoides Others + unidentified Others Unidentified Unidentified + miscellaneous Total Number of stomachs Percent empty Length: mean minimum maximum
+
-
-
-
1.32 0.96 0.01
1.37 1.01 +
1.38 0.94 0.02
1.61 0.88 0.01
0.64 0.14 0.02
0.43 0.02
0.02 0.06 + + 0.02 0.01
0.03 0.02 + + 0.03 0.04
0.03 0.03 + + + 0.01 0.04
0.02 + 0.08 + 0.02 0.49
0.07 + 0.06 0.07 0.18
0.03 0.05 0.13
0.05 0.01 + 0.18
0.04 0.02 + 0.19
0.07 0.01 + 0.23
+ 0.13
0.01 + + 0.09
0.05 0.15
+
+
0.01
+
+
1.45
1.45
1.46
1.63
0.84
0.68
2603 39.1
4147 43.2
2567 45.2
441 53.1
316 69.0
228 72.4
42 8 101
44 12 110
45 12 105
64 21 102
59 32 97
58 37 100
c o n t i n e n t a l s h e l f l a n d w a r d of t h e 4 0 0 m i s o b a t h at t h e s h e l f b r e a k , a n d t h r e e d e p t h z o n e s on t h e u p p e r c o n t i n e n t a l s l o p e (Table 3). T h e fish s a m p l e d on t h e s l o p e w e r e l a r g e r t h a n t h o s e f r o m t h e shelf. T h e freq u e n c y of e m p t y s t o m a c h s i n c r e a s e d with d e p t h , a n d t h e a v e r a g e total f u l l n e s s i n d e x d e c l i n e d with d e p t h , e x c e p t f o r a s m a l l rise in t h e 4 0 0 to 6 0 0 m interval. C a p e l i n w a s t h e d o m i n a n t p r e y at d e p t h s to 6 0 0 m. H y p e r i i d s , n o r t h e r n s h r i m p , Arctic c o d a n d G r e e n -
-
l a n d h a l i b u t w e r e p r e y e d u p o n p r i m a r i l y o n t h e shelf, whereas cephalopods, macrourids and redfish were p r e y e d u p o n m a i n l y on t h e slope. 3.2. I N F L U E N C E O F PREDATOR SIZE In 1982 t h e total f u l l n e s s i n d e x p e a k e d in t h e 25 to 29 cm l e n g t h g r o u p , d e c l i n e d to a m i n i m u m in t h e 55 to 59 cm l e n g t h g r o u p , a n d i n c r e a s e d to a n o t h e r p e a k
216
W.R. B O W E R I N G
2.5
in the 80 to 84 cm length group (Fig. 2). Partial fullness indices for cephalopods and hyperiid amphipods were low for all predator size groups, but were highest in very small specimens ( < 20 cm). Predation on fish was distinctly size-related, with an abrupt change at about 65 to 69 cm from feeding on capelin to feeding on various groundfish. The decline in the total fullness index in the middle of the size range was less pronounced in 1981 and 1984, but otherwise the patterns were similar.
CROUNDFISH
F'.'.'.'.':I CAPEUN n u OTHER RSH I ~ UNID. RSH CEPHALOPODS u HYPERIIDS
X L,=J
2.0 V} (/}
'Z"
& G.R. LILLY
1.5
_J _J
1.0 I-n,-
0.5 .'.:.:::,-::~,:.~::.." 0.0
Fig. 2. Stomach contents in relation to predator length (5-cm length groups) for Greenland halibut collected on the southern Labrador and Northeast Newfoundland Shelves in 1982. The number of stomachs in each length group is shown at the top.
B4 -14
-24
-34
-44
-54
-64
-74
-84
LENGTH (CM)
57
:~ - - ' 55~-,e'
56
~ .... i "
,-
55
54
55
52
51
49
4856
CAPEL/N~,4~STOMACHS
i ~.~.:..
~'
50
55
X NIL
"-
io
0 '
54
,
iI
52
53
•
i:
I I :~
"
"i =
I •o ,
51
' "
52
×
.p
i Ol
~:,
@ .
., •
•
"
~.
... 50
)
,~ 49
.
58
57
56
•
~:~
O•
/ .
.
55
.
.
.
9J
"
54
'
55
52
51
50
49
49
4B
Fig. 3. Mean partial fullness index (PFI) for capelin in stomachs of Greenland halibut (25-64 cm only) by tow in 1982.
FOOD OF GREENLAND HALIBUT
3.3. SPATIAL VARIABILITY
stomach was available. Both variables were transformed (Iogl0(x+l)). There was weak association in 1982 (Pearson correlation coefficient r=0.34, P<0.001, N=286), but not in 1981 (r=0.03, P=0.69, N=190) and 1984 (r=0.07, P=0.31, N=203). In 1982 the capelin were found in largest quantities in stomachs of Greenland halibut from Hamilton Bank and the inner shelf off southern Labrador and northeastern Newfoundland (Fig. 3), whereas the largest catches of medium-sized Greenland halibut were taken in the deep basins of the shelf (Fig. 4). Similar distribution patterns were found in 1981 and 1984.
The Greenland halibut which preyed most intensely on capelin were medium-sized (roughly 20 to 69 cm). Did these Greenland halibut aggregate in areas of high capelin density? The distribution of capelin at the time of the surveys is not known from an independent source. Capelin were caught as a bycatch in the surveys (CARSCADDEN et al., 1989), but these catches are thought to provide no more than a broad overview of capelin distribution, because a nil catch is likely even when capelin are present. As an alternative, we used the mean partial fullness index for capelin in stomachs of Greenland halibut (25 to 64 cm only) from each tow as a measure of how successful the Greenland halibut were in finding capelin, and compared this with the number of medium-sized Greenland halibut caught in each tow. Analysis was restricted to those tows from which at least one 58 56
~
57 ~-T
56
56
r-
r
3.4. WHY DO LARGE GREENLAND HALIBUT NOT FEED ON CAPELIN? Large (> 69 cm) Greenland halibut tended not to feed on capelin (Fig. 2). To determine if this was because they did not co-occur with capelin, we plotted the
54
i
--
55
52
r
51
T
'
).::;>: ......... ~-\;: ""
,'
"1
W,,...
::::~
ook I ~F
S
-"
~v,~r •
250
48 56
,,+ i..a ':." "
i
55
54
• •
Ill
, •
I/.I.
"~
.
55
•
llll
52
r
". ' , ," •
dr." •
'll
1~
• @~ "_~ w'.
."x
•
500
%
°-
•
•
I w -'i
I f~--"--i~i / ~ <~<.-/-e'/
56
,
NIL
" .
""
V
57
49
r
~
'k." t ' , ,
~
~
,, ~/,7
5B
X
',~l" :: e e 'I'm:". • "~& . . , %, • O • i ~ ' " ~t o ',, " , . a l O ::k.• ¢_ ~ g " ..
W
50
-:""
"
%
.~-
'
NUMBER PER TOW
' m":~.:::.
~:~-/1", "t' '" I
217
It
w
~52 •
. ,'~ :," ....
4~,
::e±_
"4/(
51
50
49
48
Fig. 4. Catch (number) of medium-sized (20-69 cm) Greenland halibut by tow in 1982.
218
W.R. BOWERING & G.R. LILLY
56
58 . %
57 i
56 r
,
56
,
,
54 I
53
52 i
~:'~....... 55 ~'-
×" ×
50 f
49
4856
NUMBER PEB TOW
'
X
- .. _
X~X,,/ '
,...• . ~ , L~ 54
51 1
?
,i
.,
55
•
54
t
I t l i ~ ~
NIL
>-
~
53
~I I I
452
.,
.o6 i
51 i
.~_ ; , x , ~ ~
x
~::~ ,~ t~ xIIxt ~,
i
50
"""
,:o
't 49 ,58
57
56
. . . . . . 55 54
~
~
.~
/
" 55
,~
52
51
', 50
s 40
49
48
Fig. 5. Catch (number) of large (>69 cm) Greenland halibut by tow in 1982. geographic distribution of large Greenland halibut and compared it with the geographic distribution of capelin in stomachs of smaller Greenland halibut (25 to 64 cm only). In 1982 the large Greenland halibut tended to occur on the upper continental slope and in the deep water of the saddles, particularly Hawke Saddle (Fig. 5). Thus, many were outside the areas of highest capelin availability (Fig. 3). However, some overlap occurred, particularly on the outer slope of Hamilton Bank. To determine if large Greenland halibut tended not to feed on capelin even when capelin were available, we selected from all three years those tows in which the mean PFI for capelin in stomachs of 25 to 64 cm Greenland halibut was greater than 1.0, the number of stomachs on which the PFI for capelin was based was greater than 4, and the catch of Greenland halibut longer than 69 cm was greater than 5. We combined the data from the 28 tows so selected, and found that even though the
Greenland halibut in the length-range 20 to 64 cm fed intensively on capelin (PFI values of 3 to 4), the Greenland halibut longer than 69 cm fed primarily on groundfish (Fig. 6). This observation was not affected by small variations in the criteria for selection of tows. 3.5. WEIGHT OF PREY IN STOMACHS OF THE POPULATION OF GREENLAND HALIBUT In estimating the weight of prey in the stomachs of the Greenland halibut population at the time of sampling, we grouped the prey into four taxa: invertebrates, capelin, groundfish, and other fish. Unidentified fish were allocated to the three fish categories in proportion to the weight of the three categories in each combination of stratum and length group. In 1982 the major consumers of capelin were Greenland halibut in the 30 to 59 cm range, whereas the major consumers of groundfish were in the 70 to
FOOD OF GREENLAND HALIBUT
5.0
13
21
38
33
61
57
I
I
I
I
I
I
X ~'~ f-3 4 . 0 Z
77 74- 77 58 I
I
I
64- 51
I
I
F~ I ~ ~
~
(/) (Y)
1
54 I
44 72 I
GROUNDFISH CAPELIN OTHER F~SH UNID. FISH CEPHALOPODS HYPERIIOS OTHER
"
3500 3000
F/T///A
INVERT.
=~--
OTHER
FISH
I:';.:';.:';.:1 GROUNDFISH C,o o x ~
CAPELIN
2500 ::::::::::::::::::::::::::
,,, 5.0 Z d d ::3
219
iii,!iiiii!ii!;!i:j i
(/) 2000 Z 0 I-- 1500
2.0
.--I
1000 p.-
.~ 1.0 a.
5OO
0.0
24 -14
-24
-34
-44
-54
-64
-74
0 1981
84
LENGTH (CM) length groups) for Greenland halibut collected in 28 tows selected for a high PFI for capelin and the occurrence of more than 5 large Greenland halibut. The number of stomachs is shown at the top. 89 cm length-range (Table 4). The total weight of prey estimated to be in the stomachs increased from 1938 tons in 1981 to 3270 tons in 1984 (Fig. 7), in part because of an increase in the mean catch of Greenland halibut per tow (BOWERING et al., 1990). Capelin contributed 62 to 73% of the total weight. TABLE 4 The weight (tons) of specific prey categories in the stomachs of 10-cm length groups of the Greenland halibut population at the time of sampling in 1982. capelin 0.0
1984-
YEAR
Fig. 6. Stomach contents in relation to predator length (5-cm
Greenland halibut inverlength group tebrates
1982
ground fish
other fish
0.0
0.0
1-9
0.0
10-19 20-29 30-39 40-49 50-59 60-69 70-79 80-89 >89
1.1 11.8 8.6 23.2 23.3 3.1 1.8 9.8 0.4
0.2 98.9 403.8 602.1 459.6 142.9 15.0 24.0 8.7
<0.1 0.3 4.7 14.9 32.7 45.5 162.9 251.7 85.2
0.0 0.3 7.0 12.0 3.5 0.1 4.1 0.0 1.2
Total
83.2
1755.3
597.9
28.2
3.6. ANNUAL CONSUMPTION BY GREENLAND HALIBUT
Fig. 7. Total weight of prey in the stomachs of the Greenland halibut population at the time of sampling each year. and there is still uncertainty about the pattern of gastric evacuation in piscivores (LILLY, 1991). YANG & LIVINGSTON (1988) estimated daily ration of Greenland halibut in the eastern Bering Sea by employing the model proposed by ELLIOTT & PERSSON (1978), parameterized with gastric evacuation data for walleye pollock (DWYER et al., 1987). We assumed that the daily rations estimated for Greenland halibut in the Bering Sea could be applied to the Greenland halibut collected off Labrador and Newfoundland if the prey types, temperatures and mean stomach content weights were similar. The major prey in both areas were fish. The weighted mean temperature at capture for Greenland halibut off Labrador and Newfoundland varied from 1.9°C in 1982 to 2.5°C in 1981. This is only slightly lower than the 2.6 to 3.0°C reported for the Bering Sea. To determine whether mean stomach content weights were similar, we first calculated mean total fullness indices for 3-hour intervals of the 24-h day. The fullness indices showed some variability, especially in the 60 to 69 cm length group (Fig. 8), but we concluded from visual inspection that there was no diel pattern. This is in agreement with the conclusion of YANG & LIVINGSTON (1988). Because no diel pattern was detected, we calculated a mean stomach content weight, as a percentage of body weight (% BW), for all stomachs in each 10-cm length group. In this we differed from YANG & LIVINGSTON (1988), who calculated mean stomach content weight (S) as: T~=~ S i l m '
We did not estimate the rate of prey consumption by Greenland halibut in each length group and stratum because information on gastric evacuation rate in this species is lacking (YANG & LIVINGSTON, 1988),
where S i is the mean stomach content weight (% BW) in each time interval (i) for a total of m intervals. We did not record individual fish weights at sea, and
220
W.R. BOWERING & G.R. LILLY
3.0 20-29 Cm
25 167
1.5
t
183
,i7 ,i6 ,i5 ,i7 ,i 2i7 i
25 20
4 0 - 4 9 Cm
362 283
325 I 365 323 337 311 3i3
°t ~10 -J
_J30 99
60-69 Cm
25 2O
101 130
15 117
I0
li5
t
li0
t
4. DISCUSSION
115
05 O0 0
followed YANG & LIVINGSTON (1988) in estimating weights from a weight-length relationship. Mean stomach content weight (% BW) was highest in small (20 to 29 cm) fish and large (80 to 89 cm) fish (Table 5). The actual values depend on the weight-length relationship used, but are similar to those estimated for Greenland halibut from the Bering Sea (Table 5). To convert stomach content weight to daily feeding rate, we took advantage of the fact that the estimated daily ration (% BW) was approximately 48% of the mean stomach content weight (% BW) for all sizes of Greenland halibut examined by YANG & LIVINGSTON (1988; their table 3). By multiplying the quantity of capelin estimated to be in the stomachs of the population (Table 4, Fig. 7) by 0.48, we estimated that the daily rate of consumption of capelin by Greenland halibut was 575, 842 and 1140 tons in 1981, 1982 and 1984 respectively. If we further assume that Greenland halibut fed on capelin at this rate for six months of the year, then annual consumption was 105, 154 and 208 thousand tons in 1981, 1982 and 1984 respectively.
:1
12 TIME(HOUR)
24
Fig. 8. Diel changes in total fullness index (mean and 950/0 confidence interval) in three length groups of Greenland halibut. Data from all three years were combined. The number above each bar is the sample size.
Our observations of the stomach contents of Greenland halibut from the southern Labrador and Northeast Newfoundland Shelves agree with reports from elsewhere that small Greenland halibut tend to feed on plankton and that larger Greenland halibut feed almost entirely in the water column and predominantly on fish (SMID'r, 1969; LEAR, 1970; YANG & LIVINGSTON, 1988). In the present study, small (<20 cm) individuals fed primarily on small crustaceans (mainly hyperiid amphipods) and cephalopods, some of
TABLE 5 The mean stomach content weight of Greenland halibut, expressed as a percentage of body weight (% B W + SE). Data from all 3 years and all times of the day were combined. N =number of stomachs, aWeight of each fish was estimated from W=0.006072 L3"°886(YANG& LIVINGSTON(1988)) bWeight of each fish was estimated from W=0.002184 L 3'3454 (BOWERING & STANSBURY(1984)); CFrom table 3 of YANG& LIVINGSTON(1988). Mean stomach content weight (% BW + SE) Labrador and Newfoundland Green/and hafibut length group
10-19 20-29 30-39 40-49 50-59 60-69 70-79 80-89
N
318 1435 1976 2639 2174 903 463 282
YANG & LIVINGSTONE BOWERING& STANSBURY (1988)a (1984)b
1.11 +0.176 2.22 ::1:0.090 2.07 + 0.069 1.56 + 0.056 1.30 _+0.061 1.24 + 0.091 1.69 + 0.143 2.35 + 0.192
1.48+0.232 2.69 + 0.109 2.32 -I-0.077 1.64 + 0.059 1.30 -I-0.061 1.19 ::t:0.087 1.56 + 0.132 2.10 _+0.171
Bedng Sea c
}
1.43
I
1.33
}
2.43
FOOD OF GREENLAND HALIBUT
which were identified as Gonatus sp. Medium-sized (20 to 69 cm) individuals fed primarily on capelin, the dominant mid-sized (10 to 18 cm) schooling planktivore in this area (CARSCADDEN, 1984). Large (>69 cm) individuals fed primarily on a variety of demersal fish larger than capelin. Northern shrimp (Pandalus borealis) were not as important as prey in Div. 2J3K as a whole as they are on commercial shrimp grounds off Labrador (BOWERING et al., 1984) and west Greenland (SMIDT, 1969). Certain species of epibenthos, notably crabs, are available to fish in this region, as is evident from their occurrence in the stomachs of cod (Gadus morhua) (LILLY, 1984, 1991), but they were rare in Greenland halibut stomachs. Greenland halibut were broadly distributed over the shelves, and were not highly aggregated in those areas where they were most successful in finding capelin. Medium-sized (20 to 69 cm) individuals were most abundant in the deep regions of the continental shelf, and large (>69 cm) individuals were most abundant in the deep water of the saddles and along the upper slope. This is in agreement with the conclusion of a more extensive study of Greenland halibut distribution (BOWERING & CHUMAKOV, 1989). The degree of overlap with capelin may be highly variable, even if Greenland halibut distribution is not variable, because the distribution of capelin at the time of the annual bottom-trawl survey varies among years (CARSCADDEN et al., 1989; LILLY, 1991), and there is evidence that capelin move from the southern Labrador region to the northeast Newfoundland region during the autumn (BAKANEV & GORCHINSKY, 1985; CARSCADDEN et al., 1987). Our estimates of the quantity of capelin and other prey consumed by Greenland halibut may be improved in several ways. The estimates of population numbers in each length group and stratum assume that the catchability coefficient of the trawl is 1.0. If the true value is less, then the population size and consumption of prey will be higher. A recent attempt to obtain population numbers from a sequential population analysis was unsuccessful (BOWERING et al., 1990). In converting stomach content data to feeding rate, we assumed that the daily rates estimated for Greenland halibut in the Bering Sea could be applied to Greenland halibut off Labrador and Newfoundland. The rates estimated for the Bering Sea fish involved many assumptions (YANG& LIVINGSTON, 1988). We require additional study into the nature of the gastric evacuation process in piscivorous fish (BROMLEY, 1988), and parameterization of gastric evacuation models with data obtained directly from Greenland halibut. We also require stomach content data at times other than late autumn. We assumed that Greenland halibut preyed on capelin for only six months each year because CHUMAKOV & PODRAZHANSKAYA (1986) reported that Greenland
221
halibut off Labrador and eastern Newfoundland (NAFO Subareas 2 and 3) fed more intensively in summer and autumn than in winter and spring. However, CHUMAKOV & PODRAZHANSKAYA(1986) also found that the intensity of feeding declined by November and December from a peak in August to October, so our estimates may be conservative for the summer period. In addition, LEAR (1970) found that Greenland halibut in Trinity Bay preyed on capelin throughout the year, with the frequency of occurrence and percentage by volume being high in the period mid-January to mid-April. Thus, Greenland halibut probably prey on capelin in the winter in Div. 2J3K if their distributions overlap, but information on this is lacking. We estimate that Greenland halibut consumed 100 to 200 thousand tons of capelin annually during the period 1981-84. We have not tried to calculate the precision of these estimates, and we recognize that many factors contribute to the accuracy, but we have tried to be conservative. Nevertheless, the present point estimates are substantial compared to hydroacoustic estimates of standing stock of capelin during the same period: viz. 94 to 1494 thousand tons from Canadian surveys and 263 to 852 thousand tons from USSR surveys (CARSCADDENet al., 1989; LILLY, 1991). Landings during this period were restricted by quota to 12 to 24 thousand tons (CARSOADDEN et al., 1989). Earlier studies have focused on cod, seals, baleen whales and sea birds as important natural predators on capelin (BROWN & NETTLESHIP, 1984; CARSCADDEN, 1984; ANDERSON & LILLY, 1985). Greenland halibut should be added to this list. 5. REFERENCES
ALTON, M.S., R.G. BAKKALA,G.E. WALTERS& P.T. MUNRO, 1988. Greenland turbot Reinhardtius hippog/ossoides of the eastern Bering Sea and Aleutian Islands region.--U.S. Department of Commerce, NOAA Technical report NMFS 71: 1-31. ANDERSON, J.T. & G.R. LILLY, 1985. Review of reported biological and technological interactions for commercial marine species of the Newfoundland region. In: R. MAHON. Towards the inclusion of fishery interactions in management advice.--Can. Tech. Rep. Fish. Aquat. Sci. 1347: 34-53. BAKANEV,Y.S.& K.V.GORCHINSKY,1985. Hydroacousticsurvey of capelin stocks in Divisions 2J3K and trawl survey of capelin prerecruits in Divisions 3KLNO in November 1 9 8 4 - January 1985.-- Northwest Atlantic Fisheries Organization, Res. Doc. 85•52, Serial No. N1001: 1-11. BOWERING, W.R. & D.E. STANSBURY,1984. Regressions of weight on length for Greenland halibut, Reinhardtius hippog/ossoides, from Canadian waters of the northwest Atlantic.--J. Northw. Atl. Fish. Sci. 5: 107-108. BOWERING,W.R. & A.K. CHUMAKOV,1989. Distribution and relative abundance of Greenland halibut (Reinhard-
222
W.R. BOWERING & G.R. LILLY
tius hippoglossoides (Walbaum)) in the Canadian northwest Atlantic from Davis Strait to the northern Grand Bank.--Fish. Res. 7: 301-327. BOWERING,W.R., D.G. PARSONS& G.R. LILLY,1984. Predation on shrimp (Pandalus borealis) by Greenland halibut (Reinhardtius hippoglossoides) and Atlantic cod (Gadus morhua) off Labrador.--ICES C.M. 1984/G:54: 1-30. BOWERING, W.R., w.a. BRODIE & J.W. BAIRD, 1990. An assessment of the Greenland halibut stock component in NAFO Subarea 2 and Divisions 3K and 3L.-Northwest Atlantic Fisheries Organization, Res. Doc. 90/51, Serial No. N1772: 1-21. BROMLEY, P.J., 1988. Gastric digestion and evacuation in whiting, Merlangius merlangus (L.).--J. Fish Biol. 33: 331-338. BROWN, R.G.B. & D.N. NETTLESHIP,1984. Capelin and seabirds in the northwest Atlantic. In: D.N. NETTLESHIP, G.A. SANGER & P.F. SPRINGER. Marine birds: their feeding ecology and commercial fisheries relationships. Proceedings of the Pacific Seabird Group Symposium, Seattle, Washington, 6-8 January, 1982: 184-194. CARSCADDEN,J.E., 1984. Capelin in the Northwest Atlantic. In: D.N. NETTLESHIP,G.A. SANGER & P.F. SPRINGER. Marine birds: their feeding ecology and commercial fisheries relationships. Proceedings of the Pacific Seabird Group Symposium, Seattle, Washington, 6-8 January, 1982: 170-183. CARSCADDEN, J., O.S. MILLER,B.S. NAKASHIMA,R. HARNUM & D.B. ATKINSON, 1987. Capelin in SA2 + Div. 3K. Canadian Atlantic Fisheries Scientific Advisory Committee, Res. Doc. 87/12: 1-37.
CARSCADDEN,J., D.S. MILLER& G.R. LILLY,1989. Capelin in SA2 + Div. 3K: results from offshore research. Canadian Atlantic Fisheries Scientific Advisory Committee, Res. Doc. 89•78: 1-44. CHUMAKOV,A.K. & S.G. PODRAZHANSKAYA,1986. Feeding of Greenland halibut (Reinhardtius hippog/ossoides) in the Northwest Atlantic.--NAFO Sci. Coun. Studies 10: 47-52. CLARK, M.R., 1985. The food and feeding of seven fish species from the Campbell Plateau, New Zealand.--New Zealand J. Mar. Freshw. Res. 19: 339-363. DOUBLEDAY,W.G., 1981. Manual on groundfish surveys in the Northwest Atlantic.--Northw. Atl. Fish. ORB., Sci. Coun. Studies 2: 7-55.
DWYER, D.A., K.M. BAILEY & P.A. LIVINGSTON,1987. Feeding habits and daily ration of walleye pollock (Theragra chalcogramma) in the eastern Bering Sea, with special reference to cannibalism.--Can. J. Fish. Aquat. Sol. 44" 1972-1984. ELLIOTT,J.M. & L. PERSSON, 1978. The estimation of daily rates of food consumption for fish.--J. Anim. Ecol. 47: 977-991. GROOT, S.J. DE, 1970. Some notes on an ambivalent behaviour of the Greenland halibut Reinhardtius hippog/ossoides (Walb.) Pisces: Pleuronectiformes.--J. Fish Biol. 2: 275-279. HAUG, T. & B. GULLIKSEN, 1982. Size, age, occurrence, growth and food of Greenland halibut, Reinhardtius hippoglossoides (Walbaum) in coastal waters of western Spitzbergen.--Sarsia 68: 293-297. HYSLOP,E.J., 1980. Stomach contents analysis - a review of methods and their application.--J. Fish Biol. 17: 411-429. LEAR, W.H., 1970. The biology and fishery of the Greenland halibut (Reinhardtius hippog/ossoides) (Walbaum) in the Newfoundland area. M.Sc. Thesis, Memorial University of Newfoundland, St. John's: 1-132. LILLY, G.R., 1984. Predation by Atlantic cod on shrimp and crabs off northeastern Newfoundland in autumn of 1977-82.--ICES C.M.1984/G:53: 1-25. - - - - , 1991. Interannual variability in predation by cod (Gac/us morhua) on capelin (Ma//otus vi/Iosus) and other prey off southern Labrador and northeastern Newfoundland.--ICES mar. Sci. Symp. 193: 133-146.
PETRIE, B., S. AKENHEAD,J. LAZIER& J. LODER, 1988. The cold intermediate layer on the Labrador and Northeast Newfoundland Shelves, 1978-86.--Northw. Atl. Fish. ORB., Sci. Coun. Studies 12: 57-69. SMIDT, E.L.B., 1969. The Greenland halibut, Reinhardtius hippoglossoides (Walb.), biology and exploitation in Greenland waters.--Meddr Danm. Fisk.-og Havunders. 6: 79-148. SMITH, E.H., F.M. SOULE & O. MOSBY,1937. The Marion and General Greene expeditions to Davis Strait and Labrador Sea, 1928-1935. Scientific results, part 2: Physical oceanography.--U.S, Treasury Dept., Coast Guard Bull. 19: 1-259. YANG, M.S. & PA. LIVINGSTON,1988. Food habits and daily ration of Greenland halibut, Reinhardtius hippog/ossoides, in the eastern Bering Sea.--Fish. Bull. 86: 675-690.