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Atlantic herring as a dietary component for culture of Atlantic salmon
Aquaculture,
3 (1974)
369-385
@ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
ATLANTIC HERRING AS A DIETARY OF ATLANTIC SALMON
COMPONENT
FOR CULTURE
RICHARD L. SAUNDERS and EUGENE B. HENDERSON Fisheries Research Board of‘canada,
Biological Station, St. Andrews, N.B. (Canada)
(Received August 27, 1973; revised February 11, 1974)
Chopped herring was readily eaten by Atlantic salmon. Fry, parr and smolts grew well on a herring-rich diet but after long periods fry and smolts developed symptoms of nutritional deficiency which were quickly cured by omitting herring from the diet. Parr, fed herring and liver separately on alternate days, did not show ill effects. The symptoms are believed due to a high content of thiaminase in herring. Mixing herring with other thiamine-rich foods did not prevent the harmful effects in salmon, presumably owing to inactivation of the thiamine in the food mixture. It is suggested that the beneficial effects of a herring diet can be retained and the harmful effects prevented by feeding herring and some other thiaminase-free food separately during alternate periods.
INTRODUCTION Criteria for suitable foods for fish farming include nutritive value, promotion of growth and acceptance by the fish, as well as reasonable cost of the food, its ready availability and maintenance of quality during storage. This paper considers the potential of Atlantic herring (Clupcu harengus) as a diet for Atlantic salmon (Salvo s&r) with respect to some of the above criteria. It is reasonable to consider herring as a food for cultured salmon since this species is an important food item of Baltic salmon (Wiktor, 1961; Thurow, 1966) and probably of other stocks as well. Laboratory stocks of salmon fry, Parr, smolts and post-smolts fed readily on herring presented alone or mixed with beef liver or cod (Gadus morhua) muscle (Saunders and Henderson, MS 1969a, b, and c; available on request from the authors). Growth rates of the post-smolts approached those found in nature (Allen et al., 1972).
370 Herring are available in Atlantic Canada at low cost ($0.12-$0.14 per kg) in freshly caught or frozen form. However, herring has a high fat content which varies seasonally (Stoddard, MS 1968). Like other species of fishes, it may develop fat rancidity and resultant protein destruction during frozen storage (Tappel, 1965). Moreover herring contains relatively high concentrations of thiaminase, which inactivates thiamine (Neilands, 1946). A diet of herring or other marine or freshwater fishes known to have high thiaminase content has been shown to be responsible for Chastek paralysis, a dietary deficiency disease in mink (Green et al., 1937: Deutsch and Hasler, 1943). Allan (1958) describes a noninfectious disease in rainbow trout which he believes to be a vitamin deficiency disorder resulting from a diet of herring. Saunders and Henderson (MS 1969b and c) report similar adverse effects of a herring-rich diet on Atlantic salmon fry and smolts. In the present study we show that a diet of herring over a long period does lead to symptoms of dietary deficiency in Atlantic salmon; yet, when presented for shorter periods or in combination with other foods, herring may satisfy some of the criteria of a suitable fish food. MATERIALS
AND METHODS
Experiments were conducted with recently hatched fry, underyearling parr and two-year-old smolts. All were hatchery-reared and brought to the laboratory some weeks before experiments were started.
Alevins were brought to the laboratory in May and held-in fibreglass tanks with limited exchange of fresh water-until they had completed absorption of their yolk sacs and begun to eat. At this stage they are referred to as fry. Feeding was started on June 15 using freshly ground beef liver. On July 5 the fry were divided into six groups of 300. Two groups were put in fresh water (O%O), two in 6%0 salinity and two in 12%0 to allow for experiments with two diets at each of three salinities. We had determined previously that fry survived indefinitely following abrupt transfer from fresh to brackish water up to 12?& It was concluded that the lethal level for fry just after they commenced feeding is between 12 and 15%0 and that salinities between 0 and 127~ would be suitable for studies of growth over a long period. Salinities were maintained at various levels (? 1%0) by delivering fresh or salt water (30’$00) from constant-head reservoirs through drawn glass jets ground to size to give the appropriate proportions
98
96
96
I
I
I
7.8
3.7
10.7
12.8
Nov. 24 (99)
Feb. 24 (191)
May 10 (266)
June 7 (294)
98 94
98 99
I II
11.8
Oct. 26 (70) I II
98 99
I II
15.0
Sept. 21 (42)
101 100
II
I
17.9
Aug. 17 (0)
N
Temperature (“C)
Date (elapsed time)
Lot
0
(“/a,)
Salinity
12.9
11.4
9.4
8.9 8.9
8.0 8.2
6.8 7.0
5.2 5.3
Mean length (cm)
25.7
17.1
9.1
8.4 8.2
6.4 6.7
3.9 4.1
1.5 1.6
Mean weight (g)
99
99
100
100 95
100 97
100 97
100 101
N
6
14.2
12.4
9.9
9.4 9.0
8.4 8.3
7.1 7.3
5.2 5.1
Mean length (cm)
32.8
21.8
11.2
9.6 8.3
7.3 7.1
4.4 4.5
1.5 1.4
Mean weight (g)
12
97
98
98
98 96
98 100
98 100
13.2
11.8
9.6
9.2 8.7
8.3 8.1
7.0 7.1
5.1 5.0
Mean length (cm)
26.7
19.8
10.3
9.1 7.9
7.1 6.7
4.4 4.4
1.5 1.5
Mean weight (9)
and fed either liver (Lot
100 100
N
Salmon fry experiment. Mean lengths and weights of six groups reared in different salinities (0,6, 12’/,,) I) or a mixture of herring and liver (Lot II)
TABLE 1
w -1
372 of each water supply. Water temperature varied seasonally from a low of 4°C in February to a high of 18°C in August (Table I> but at any time was the same for all groups. All fry were fed beef liver from June 15 to August 24. The fry then were divided into two lots, and each lot into three groups held at 0, 6 and 12$& respectively. From August 24 onward Lot I was fed beef liver only, Lot II was fed a mixture of 50% ground, fresh or freshly frozen herring and 50% beef liver by weight. Measurements of length and weight were begun on August 17. Parr
Five groups of 110 underyearling salmon were held between December and the following June in cylindrical fibreglass tanks (l-m diameter) of flowing water with salinities of 0, 7, 15, 22 and 30?&. Salinities were maintained at the selected levels (+ ca. l%,). Temperature followed the seasonal cycle for the freshwater supply but at any time was the same (+ 0.2”C) for all groups. Finely chopped fresh herring and chopped beef liver were fed separately on alternate d,ays. The parr accepted herring more readily than liver and as a consequence consumed far more herring than liver during the experiment. Smelts
Stocks of two-year-old pat-r were brought to the laboratory in late winter and held in fresh water in cylindrical fibreglass tanks (1.8-m diameter). Water inlets together with submersible electric pumps at the periphery of each tank maintained a current speed of ca. 14 cm/set near the periphery. This current elicited a positive rheotactic response in the salmon; feeding was enhanced by dispersal of the fish throughout the tank and by constant motion of the food particles. Separate experiments were conducted during successive years beginning in June and April. In the first experiment, four groups of 95 smolts each were taken from freshwater holding tanks on June 24 and placed in separate 1.8-m tanks in which the salinity was raised within 3 days to 7, 15, 22 and 30%~ respectively. A fifth group was held in fresh water. The fish were fed to satiety two or three times daily, depending on water temperature. The diet for the first experiment was a mixture of ground beef liver, fresh herring and Purina trout chow (42.5-42.5-15% by weight) ground to a paste. Herring was excluded from the food mixture after November 20.
313 In the second experiment, five groups of 100 smolting salmon were put in water of the same salinities as used in the previous experiment. The diet from April 1 to April 22 was a mixture of equal parts of beef liver and cod fillets. A liver-cod-trout chow mixture (42.5-42.5-1570 by weight) was used from April 22 onward. In addition, a duplicate group (7-A) held at 7YG was fed the herring-liver-trout chow mixture to confirm the observation in the previous experiment that a diet containing herring caused symptoms of nutritional deficiency and mortalities. Temperature during both experiments followed the natural seasonal cycle for the freshwater supply but at any time was the same (+ O.?_“C) for all groups (Tables III, V). Food rations were weighed,to permit calculation of food conversion efficiency. Food was offered until the fish allowed it to sink to the bottom of the tank, which was taken as an indication that they were satiated. Gross conversion efficiency was calculated in terms of wet weight as weight gain by a group during the period weight of food gven dunng the period
x loo
Composition of the food can be expected to vary with different batches, and seasonally owing to changing carbohydrate, fat and protein contents of fish. The following percent dry weights from one analysis serve to show differences among the foods used: liver, 30.2; cod, 18.2; herring, 38.2 ‘and trout chow 9 1.9%. Fuller details on effects of salinity and temperature on the growth of salmon at various developmental stages are in unpublished teclmical reports (Saunders and Henderson, MS 1969a, b, and c). Some of those data are included here to make possible a fuller understanding of dietary effects. RESULTS
Both lots of fry fed readily accepted their respective foods. There were few mortalities in any group between mid-August and later October. During November there was an increase in mortalities among the herringfed groups (Lot II). Mortality rate increased directly with increase in salinity. Few of the liver-fed fry died during the period. Mortalities in the two lots between October 29 and March 4 were as follows:
374
Salinity (Ym) 0
6 12
Lot 1 (liver) (%) 3 0 2
Lot II (herring-liver) (%) 45 63 73
It was clear that inclusion of herring in the diet of fry for a period over 3 months resulted in heavy mortality. In view of the similar, low mortality rates among groups in Lot I, and increasing mortality with increased salinity in Lot II, it appears that increased salinity aggravated the adverse effect of the herring diet in Lot II. There was no indication of sizedependent mortality. Mean lengths and weights were essentially the same among groups when the fish were measured for the first time (Table I). There was little difference in growth, rates between liver-fed and herring-fed groups between August 17 and October 26. Between October 26 and November 24, growth rates of the herring-fed groups fell slightly below those of the comparable liver-fed groups (Table I). This coincided with a period of heavy mortality in the herring-fed groups. Further comparisons of growth between Lots I and II were discontinued; because of the differential mortality rates, herring-fed fish were not measured after November 24. Parr
This experiment was designed to show the effects of salinity on presmolt growth during the winter and spring. Although diet was not a variable, the experiment provided data on the-effects of feeding a diet ih which herring predominated over a long period. There were few or no mortalities among the 0,7 and 15Ym groups during the experiment (Table II). Slightly higher mortalities occurred in the 22%~~group until April 8, when 50 fish died after this group was accidentally subjected to 30%0 salinity. In the 300~ group, on the other hand, there were many deaths until March 10 after which few pan- died. Most of the smaller individuals had died by this time and the survivors were mostly large Parr, apparently well able to withstand the higher salinity. There were no indications of adverse effects from the herring-rich diet. Growth rates of the 0, 7 and 15%0 groups were similar during the experiments (Table II). No growth advantage was indicated at any of these salinity levels, nor were there salinity-dietary interactions as occurred for salmon fry: However, growth rates in 227~ were considerably lower, although mortalities in this group were of the same order as those in lower
5.9
4.1
4.2
4.8
1.7
10.3
Jan. 7 (34)
Feb. 11 (69)
March 10 (97)
April 8 (126)
May 6 (154)
May 25
100
104
109
109
109
109
110
104
103
18.2
17.8
20.1
24.8
3.1 101
102
102
107
17.7
18.5
110
13.8
2.1
11.8
11.6
11.6
11.3
10.5
* Total length; all other lengths are fork lengths. ** 52 fish died on April 8: salinity accidentally increased to 30°/,0 while fish were recovering from anaesthetic.
(173)
8.2
W
N
Mean weight
N
Mean length (cm)
7
(oloo)
0
Salinity
Temperature
1”C)
Dec. 4 (0)
Date
20.3
22.4
26.6
2.0
12.4
13.4
111
111
1 11
11
19.6
2.0
11
111
N
11
18.9
15.3
62)
Mean weight
19.5
1.8
1.6
10.8
Mean length (cm )
15
13.3
12.4
11.9
11.7
11.7
11.5
43
45**
22.5
26.5
9-l
101
105
106
108
N
18.8
18.9
18.5
18.1
15.3
(9)
(cm) 10.9
Mean weight
Mean length
22
Salmon parr experiment. Mean length and weights of 5 groups reared in different salinities (0, 7, 15, 22, 30’/,& and fed herring and liver separately on alternate days
TABLE II
13.4
12.0
11.3
11.1
11.0
10.9
10.6
W
Mean weight Mean
28.4
20.5
15.8
15.7
15.5
15.4
14.3
length (cm)
28
29
32
34
46
67
110
N
30
14.1
13.3
13.4*
12.5
12.2
11.8
11.0
Mean length (cm)
31.8
25.8
22.9
21.6
20.2
18.0
16.0
Mean weight W
376 salinities and fresh water. Clearly, 22% was above the upper limit of salinity which was suitable for growth of parr IO-12 cm long at the temperatures experienced during the experiment. There was a sharp rise in growth rates during the period April 8 to May 6 when temperatures rose from 5 to 8°C. By late May, most of the larger individuals were becoming silvery and had low condition factor and other external appearances of smolts. Smolts
Growth among the five groups in the first experiment generally was directly related to salinity (Table III; Fig.1). From June through July mean lengths and weights differed little among the salinity groups. By the ,600
:
IO-
D
‘i
6-
;
t
6-
: 4-
J ‘J
‘A’S 0
1’ i
300
36
3
36 F
6
.I
/ II
32!-
A
.- Fresh o:24-
//
;22-
x
x
7%
o-
15%.
I-
22%.
A-
30%.
Water
Salinity
J
.
20-
0
16-
/ x
I6 J
’
J
’
A
’
I
’
N’
D
J
’
F
’
Fig.1. Mean lengths and weights of smolts and post-smelts in relation to salinity. Mean temperature among groups plotted for each measuring date. All fish were fed a herring-beef liver-trout chow mixture.
31.7
32.3
33.0
42
36
34
7.5
3.6
3.0
Nov. 26 (155)
Jan. 26 (216)
Feb. 25
(246)
55
56
397.6
419.7
58
381.9
88
30.8
69
I 1.7
Oct. 26 (124)
346.8
93
244.2
27.7
73
14.3
Sept. 24 (92)
94
162.1
25.0
75
15.5
Aug. 24 (61)
94
101.1
95
15.8
July 24 (30)
21.3
16.9
96
13.2
June 24 (0)
94
Mean length (cm)
N
Date (elapsed time)
47.0
7 N
0
Salinity (%,)
34.1
44
44
455.1
45
70
86
89
92
99
N
453.0
458.3
32.9
33.7
369.4
3 1.4
283.9
183.6
25.6
28.6
112.4
47.7
Mean weight W
21.8
16.9
MeaIl length (cm)
15
Mean length and weight of 5 groups reared in different
Mean weight W
Temperature CC)
Salmon smelt and post-smelt experiment. I&-herring-trout chow mixture
TABLE 111
35.8
35.3
34.2
32.2
29.0
25.9
22.1
16.9
Mean length (cm)
541.9
535.7
506.9
389.2
293.2
191.7
113.6
48.6
Mean weight (9)
salinities (0,7, 15,22,
49
49
49
77
90
91
94
99
N
22
508.7
515.8
35.5
435.3
358.2
261.1
173.9
110.7
46.3
Mean weight (9)
35.0
33.1
31.5
28.4
25.5
21.9
16.8
Mean length (cm)
30’6,) and fed a
56
56
58
88
91
91
94
95
N
30
37.a
36.6
35.1
32.6
29.4
25.6
21.5
16.7
Mean length (cm)
572.5
574.4
542.0
410.7
304.6
184.6
104.6
46.0
Mean weight W
w
378 end of August mean lengths and weights for all groups in brackish and salt water were greater than those for the freshwater group. The 15 and 307~ fish were significantly longer and heavier (P < 0.01) than the 07m fish on October 26. At the end of the experiment all except the 7o/oo were significantly larger than the O$?&,fish. Food conversion efficiencies for the period July 24 to October 26 differed little among groups at a given time. There was little difference in efficiency within groups at different times (Table IV). Percentage efficiencies ranged from 28 to 34 and averaged about 32. TABLE IV Food conversion efficiency of post-smolt salmon reared at various salinities. All fish were fed liver-herring-trout chow mixture Interval
July 24Aug. 24 Aug.25 Sept.24 Sept. 25Oct. 26
Salinity PI&l)
Temperature PC) Mean
Range
0
7
15
22
30
15.9
15.5-16.5
0.32
0.31
0.33
0.28
0.32
15.3
15.9-14.2
0.33
0.34
0.36
0.30
0.33
13.1
14.3-11.8
0.32
0.28
0.29
0.36
0.29
Mean
0.32
0.31
0.33
0.31
0.31
There were no obvious adverse effects of the herring diet until early October. At that time many of the fish in 0, 7 and 157~ appeared abnormal. Fish lost equilibrium and often rested on their sides on the tank bottom. These fish still attempted and usually succeeded in feeding. There were few deaths; those occurring were probably hastened by secondary causes such as loss of scales and erosion of the skin through chafing on the tank bottom. On November 20 the percentages of such abnormal fish in different salinities were: Salinity (%G ) % of abnormal fish
0
7
15
22
30
64
21
18
4
3
Although incidence of the problem was inversely related to salinity, there were three distinct levels; 64% in fresh water, about 20% in 7 and 1.57~ and about 4% in 22 and 30%0. Herring was excluded from the diet after November 20. New outbreaks ceased and some of the affected fish recovered.
379 In the second smolt experiment, herring-fed fish were included (group 7-A) to confirm the observation that adverse effects were related to a diet rich in herring. Growth rates in this group at first equalled and later exceeded those of the other 7%0 fish, as well as most of the other salinity groups (Table V; Fig.2). However, it was obvious in early October that the herring-fed fish were abnormal. By late November, 20% of them either had lost equilibrium or died. None of the fish in the other groups (codliver-trout chow diet) were similarly affected. Although the herring-fed fish in the second experiment were larger in June than the corresponding groups in the first experiment, these groups had similar growth patterns during the experiments conducted during successive years. At no time was the condition factor of the herring-fed fish markedly different from that of the other groups.
35 33 -
‘IE v
29-
f
27-
0.
7 X.
0. I-
15%. 22 x.
b-
30
Salinity
i
/ I
--
l-7X.A
-
:,” 25-
Weight
23r
.’ * L
E
300 .
w
x.
I 21
100
1
X-X
19
17 IS
L
-0 :-
A
(
I
M
1
J
I
1
1
J
A
S
I
0
I
N
D
Months
Fig. 2. Mean lengths and weights of smolting salmon, smolts, and post-smolts in relation to salinity. Mean temperature among groups plotted for each measuring date. The 7-A group was given a herring-beef liver-trout chow mixture throughout the experiment. The other groups were fed a cod-liver mixture from April l-26 and cod-liver-trout chow mixture thereafter.
5.0
7.8
10.2
15.3
17.5
16.3
15.6
12.8
9.9
7.1
May 13 (42)
June 3 (63)
July 8 (98)
Aug. 12 (133)
Sept. 2 (154)
Sept. 23 (175)
Oct. 21 (203)
Nov. 10 (223)
Dec. 7 (250)
4.4
April 22 (21)
(0)
April 1
(elapsed time)
Date
57
57
60
64
70
79
84
99
100
100
100
33.6
32.8
31.8
29.9
28.1
25.8
21.7
18.8
17.1
15.9
15.5
483.9
456.9
406.4
316.6
242.3
177.0
100.2
67.6
53.8
45.0
41.2
(8)
57
57
59
65
70
80
98
100
100
100
100
N
Mean weight
N
Mean length (cm)
7
(%o)
PC)
0
Salinity
Temp.
32.9
32.2
31.2
29.2
27.5
25.8
22.7
19.1
17.1
15.9
15.5
Mean length (cm)
449.6
423.6
376.6
284.2
221.1
171.9
116.3
72.1
54.7
45.2
40.9
Mean weight (8)
53
54
58
63
68
80
96
99
100
100
100
N
7-A
33.6
32.9
31.9
29.9
28.9
27.2
23.1
19.2
17.2
16.1
15.5
(cm)
Mean length
_
471.4
447.1
398.4
297.8
259.9
204.0
128.3
73.6
57.0
48.0
41.5
Mean weight fg)
57
57
60
65
68
80
97
100
100
100
100
N
15
32.6
32.0
31.0
29.1
27.4
25.3
22.5
19.1
17.1
15.9
15.4
km)
Mean length
423.2
409.3
357.9
278.0
224.3
161.5
114.5
72.7
54.7
45.7
40.9
Mean weight (9)
57
57
60
64
70
79
97
100
100
100
100
N
22
Salmon smelt and post-smelt experiment. Mean length and weight of six groups reared in different salinities (0, 7, 15, 22, 304b,). The 7-A group was fed a he&g-live-trout chow diet throughout the experiment. The other groups were fed a cod-liver mixture from April 1-26 and a cod-liver-trout chow mixture thereafter
TABLE V
32.2
31.5
30.5
28.6
26.9
25.2
22.3
19.1
17.2
15.9
15.4
MeZUl length (cm)
417.5
393.5
342.0
261.9
204.2
160.5
111.3
73.6
55.5
45.9
40.8
Mean weight (9)
29.5
29.9
57
28.3
26.5
25.0
23.7
22.0
18.8
17.0
15.9
15.5
Mean length (cm)
57
57
62
67
78
96
100
100
100
100
N
30
318.6
309.7
262.9
192.7
156.0
126.9
104.0
70.5
54.2
45.5
41.3
Mean weight (8)
w cc 0
381 Food conversion efficiency was strongly affected by diet. Following addition of trout chow to the cod and liver mixture on April 26, there was approximately a 30% increase in conversion efficiency in all groups on that diet. The herring-liver-trout chow group (7-A) had the highest mean value for the period April to December and the highest value during six of the ten intervals (Table VI). The conversion efficiency values for the TABLE VI Food conversion efficiency of smolting salmon, smolts, and post-smolts at various salinities. Diets for various groups as described in Table V Temperature P0
Salinity P/c@)
Interval
Mean
Range
0
I
I-A
15
22
30
April 1 -April 22 April 23-May 13 May 14-June 3 June 4-July 8 July 9-Aug. 12 Aug. 13-Sept. 2 Sept. 3-Sept. 23 Sept. 24-Oct. 21 Oct. 22-Nov. 10 Nov. 11 -Dec. 7
4.1 6.2 8.9 13.0 16.9 17.3 15.8 13.7 11.3 8.2
4.2- 5.0 5.1- 7.8 7.6-10.2 10.3-15.6 15.2-18.0 18.0-16.2 16.0-15.2 15.6-12.6 12.8- 9.9 9.7- 7.0
0.19 0.32 0.29 0.22 0.30 0.29 0.26 0.23 0.23 0.14
0.22 0.32 0.31 0.27 0.22 0.25 0.23 0.23 0.20 0.14
0.33 0.28 0.27 0.34 0.32 0.36 0.27 0.32 0.23 0.14
0.23 0.32 0.34 0.25 0.21 0.30 0.21 0.22 0.24 0.07
0.23 0.32 0.32 0.31 0.21 0.24 0.23 0.23 0.23 0.11
0.20 0.33 0.32 0.22 0.13 0.20 0.17 0.21 0.17 0.05
Mean
0.25
0.24
0.29
0.24
0.24
0.20
herring-fed fish from July 9 to October 21 were similar to those of the 7%0 group as well as the other salinity groups during a comparable period in the first smolt experiment (Table IV). The mean for all groups (exclu&ng 7-A) for the period April l-22 was 21%. During the next 41 days the mean increased to 32%, presumably owing to the addition of trout chow in the diet. Although the groups other than that fed on herring had high conversion efficiency values during early summer, these values did not remain high during late summer and autumn as did those of the herring-fed fish. There did not appear to be any correlation between conversion efficiency and salinity during the summer. However, efficiency decreased more in the 30”/00 and 22%~ groups than in the others during autumn. DISCUSSION
Results of our experiment showed that finely chopped herring and beef liver are readily eaten by Atlantic salmon fry. Furthermore, growth of fry
382 fed this diet over a period of 2-3 months was equal to or greater than that attained on beef liver alone over a comparable period. Protracted feeding on the herring-rich diet, however, led to reduced growth rate and many deaths among the fry. This can be attributed to the herring component of the diet, since deaths were few in the liver-fed groups. Coble (1966) reported only slight or no adverse effects of feeding raw American smelt (Osmerus mordax) to lake trout (Salvelinus namaycush). Like herring, smelt have a high thiaminase content (Neilands, 1947). Trout feeding on smelt grew as well as or better than those fed a more balanced diet. In view of our results, Coble’s fish, which were on a smelt diet less than two months, may not have had time to develop disease symptoms or show reduced growth rates in the shorter period. The most likely explanation for these results is the demonstration by Neilands (1947) that herring has a high content of thiaminase which inactivates thiamine (vitamin Bi ). It is unlikely that spoilage of the herring and resultant destruction of essential dietary components were associated with the symptoms and deaths observed, since the herring was obtained fresh at frequent intervals during the experiment. Further support for suspecting thiaminase as the causative factor, and not the effects of herring spoilage, is the fact that mixing beef liver with the herring did not ameliorate the situation. The same explanation applies to the smolt experiment wherein the diet containing herring led to symptoms which were quickly reversible after herring was excluded from the mixture. We suggest that during mixing and storage of herring with liver, cod fillets or trout chow, the thiaminase in herring acts on any thiamine in the other foods. Support for this suggestion is given in the parr experiment in which herring and liver were fed separately on alternate days. In that experiment the fish ate far more herring than beef liver over a six-month period and showed none of the previously described symptoms. In an extensive series of experiments with captive harp seals (Phoca groenlandica) Geraci (1972) induced thiamine deficiency by feeding herring and smelts (Osmerus mordqx) without thiamine administration. The seals developed a thiamine deficiency which was sometimes fatal. Feeding of autoclaved herring did not lead to death of the seals in spite of some evidence of thiamine deficiency. Geraci found that seals maintained on a herring diet could be kept alive and free, of disease symptoms if given an oral dosage of thiamine administered 2 h before regular feeding. Our feeding of herring and beef liver on alternate days seems to have accomplished the same effect in salmon Parr. In view of Geraci’s (1972) results with autoclaved herring as a diet for seals, a similar procedure might be effective when using herring as a salmon food. However, cooking herring to deactivate thiaminase would be inconvenient and would add to opera-
383 tional costs. Moreover, our results indicate that autoclaving herring may be an unnecessary precaution if some other food is occasionally substituted for the herring. On the basis of our experiments, we suggest that Atlantic salmon can be fed fresh herring for various periods, from two to five months depending on the size of the salmon, without ill effects. Herring is an important food of Baltic salmon (Wiktor, 1961) and probably of other stocks as well. However, Baltic herring may not have high thiaminase levels (Lieck and Agren, 1944). Salmon in the sea may be able to tolerate a diet of herring for a time and benefit from its growth promoting effects if they are able to leave it for a time and feed on organisms less rich in thiaminase. In our final smolt experiment, the fish given the herring-liver-trout chow misture grew faster for some months than those given the cod-liver-trout chow mixture. The harmful effects of herring might have been avoided and the beneficial effects retained if we had fed the fish on alternate days or weeks with herring and liver, or some other food low in thiaminase, instead of mixing the two ingredients and thereby destroying thiamine in the liver. From our experience in these and other (unpublished) feeding experiments with Atlantic salmon, brook trout (Salvelinus fontinalis) and rainbow trout (Salmo gairdneri), we suggest that fresh herring can be used to advantage, when available at a low price, as a food with good growth promoting qualities. This practice of using readily available, low cost fish or fish scraps is used successfully in some salmon and rainbow trout producing plants in Norway (Saunders, 1973). We, suggest a feeding regime wherein chopped fresh herring and some commercial food (or thiaminasefree fish) are given for alternate periods to maximize the growth promoting effects of the herring while guarding against the symptoms of deficiency which often follow long-term feeding with herring. We did not determine proximate compositions of the rations or fish. Therefore, we can not evaluate growth and food conversion efficiency on an isocaloric basis. Had we taken into account energy densities of the rations, the growth resulting from different rations could be more completely understood. For example, herring is richer in fat and therefore more energy dense than cod. .Addition of trout chow to the cod-liver ration resulted in increased gross conversion efficiency, presumably owing to an increased energy density. Addition of trout chow to a herring ration may have effected an energy dilution. That growth rate was directly related to salinity in the first experiment with smolts and inversely related in the second one (Fig. 1, 2) appeared to result from differences in diet. In the experiment wherein all groups were fed herring, there was clearly a beneficial effect of high salinity which gave
384
higher growth rates and fewer mortalities than in lower salinities. In view of the beneficial effects of a moderately high salinity (305’20) while herring were being used as food, we suggest that the sea water may have provided needed thiamine. Indeed, both lake waters (Hutchinson, 1957) and marine coastal waters (Natarajan and Dugdale, 1966) contain thiamine in seasonally varying amounts. Coble (1966) suggests that lake trout may be able to feed on smelt containing thiaminase but not suffer thiamine deficiency since lake water contains thiamine. The fewer mortalities and higher growth rates in higher salinities possibly resulted from higher concentrations of thiamine in sea water than in fresh water. Salmon in the sea or those being reared in sea water may get sufficient thiamine from the environment to compensate for a thiamine destructive factor in their diet. ACKNOWLEDGEMENTS
We are greateful to Miss Mary Holmes for help during the experiments and to Messrs. K.R. Allen, A. Sreedharan, G. Fawkes and Dr. J.K. Lindsey for assistance with computer programming and analysis of data. Drs. D.W. McLeese and D.J. Wildish gave helpful suggestions for the manuscript. REFERENCES AIlan, I.R.H. (1958) Anaemic disease in rainbow trout. Cons. Perm. Int. Explor. Mer Annu. Biol., 13: 233.
Allen, K.R., Saunders, R.L., and Elson, P.F. (1972) Marine growth of Atlantic salmon (Sulmo salar) in the Northwest Atlantic. .I. Fish. Res. Bd Can., 29: 1373- 1380. Coble, D.W. (1966) Effects of adiet of raw smelt on lake trout. Can. Fish Cult., No. 36: 27-34. Deutsch, H.F. and Hasler, A.D. (1943) Distribution of a vitamin B, destructive enzyme in fish. Proc. Sot. Exp. Biol. Med., 53: 63-65. Geraci, J.R. (1972) Experimental thiamine deficiency in captive harp seals, Phoca groenlandica, induced by eating herring, Clupea harengus, and smelts, Osmsus mordax. Can. J. Zool., 50: 179-195.
Green, R.G., Evans, C.A. and Carlson, W.E. (1937) A summary of Chastek paralysis studies. Minn. Wildl. Dis. Invest., 3: 173-177. Hutchinson, C.E. (1957) A Treatise on Limnology. Vol I. Geography, Physics and Chemistry. Wiley, New York, N.Y. p. 897-898. Lieck, H. and Agren, G. (1944) On the occurrence of a thiamin inactivating factor in some species of Swedish fish. Acta Physiol. &and., 8: 203-214. Natarajan, K.V. and Dugdale, R.C. (i966) Bioassay and distribution of thiamine in the sea. Limnol. Oceanogr., ll(4): 621-629. Neilands, J.B. (1947) Thiaminase in aquatic animals of Nova Scotia. J. Fish. Res. Bd Can., 7: 94-99.
Saunders, R.L. and Henderson, relation to salinity. Fish. Res. Saunders, R.L. and Henderson, relation to salinity. Fish. Res.
E.B. (MS 1969a) Survival and growth of Atlantic salmon parr in Bd Can. Tech. Rep., No. 147. E.B. (MS 1969b) Survival and growth of Atlantic salmon fry in Bd Can. Tech. Rep. No. 148.
385 Saunders, smelts Saunders, Stoddard,
R.L. and Henderson, E.B., (MS 1969~) Growth of Atlantic salmon smelts and postin relation to salinity, temperature and diet. Fish. Res Bd Can. Tech. Rep., No. 149. R.L. (1973) Salmonid aquaculture in Norway. Atl. Salmon J., No. l(1973): 8-13. J.H. (MS 1968) Fat contents of Canadian Atlantic herring. Fish. Res. Bd Can. Tech.
Rep., No. 79.
Tappel, A.L. (1965) Oxidative reactions and enzymes. In: R. Kreuzer (Editor), The Technology of Fish Utilization, Contributions from Research. Fishing News (Books), London, pp. 129-134. Thurow, F. (1966) Beitrage zur Biologie und Bestandskunde des Atlantischen Lachses (Salmo solar L.). Ostsee Ber. Dtsche Wiss. Komm. Meeresforsch., 18: 223-379. Wiktor, K. (1961) Food investigations on salmon and sea trout in southeastern Baltic. Cons. Perm. Int. Explor. MerAnnu.
Biol., 16: 251-252.
3 (1974)
369-385
@ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
ATLANTIC HERRING AS A DIETARY OF ATLANTIC SALMON
COMPONENT
FOR CULTURE
RICHARD L. SAUNDERS and EUGENE B. HENDERSON Fisheries Research Board of‘canada,
Biological Station, St. Andrews, N.B. (Canada)
(Received August 27, 1973; revised February 11, 1974)
Chopped herring was readily eaten by Atlantic salmon. Fry, parr and smolts grew well on a herring-rich diet but after long periods fry and smolts developed symptoms of nutritional deficiency which were quickly cured by omitting herring from the diet. Parr, fed herring and liver separately on alternate days, did not show ill effects. The symptoms are believed due to a high content of thiaminase in herring. Mixing herring with other thiamine-rich foods did not prevent the harmful effects in salmon, presumably owing to inactivation of the thiamine in the food mixture. It is suggested that the beneficial effects of a herring diet can be retained and the harmful effects prevented by feeding herring and some other thiaminase-free food separately during alternate periods.
INTRODUCTION Criteria for suitable foods for fish farming include nutritive value, promotion of growth and acceptance by the fish, as well as reasonable cost of the food, its ready availability and maintenance of quality during storage. This paper considers the potential of Atlantic herring (Clupcu harengus) as a diet for Atlantic salmon (Salvo s&r) with respect to some of the above criteria. It is reasonable to consider herring as a food for cultured salmon since this species is an important food item of Baltic salmon (Wiktor, 1961; Thurow, 1966) and probably of other stocks as well. Laboratory stocks of salmon fry, Parr, smolts and post-smolts fed readily on herring presented alone or mixed with beef liver or cod (Gadus morhua) muscle (Saunders and Henderson, MS 1969a, b, and c; available on request from the authors). Growth rates of the post-smolts approached those found in nature (Allen et al., 1972).
370 Herring are available in Atlantic Canada at low cost ($0.12-$0.14 per kg) in freshly caught or frozen form. However, herring has a high fat content which varies seasonally (Stoddard, MS 1968). Like other species of fishes, it may develop fat rancidity and resultant protein destruction during frozen storage (Tappel, 1965). Moreover herring contains relatively high concentrations of thiaminase, which inactivates thiamine (Neilands, 1946). A diet of herring or other marine or freshwater fishes known to have high thiaminase content has been shown to be responsible for Chastek paralysis, a dietary deficiency disease in mink (Green et al., 1937: Deutsch and Hasler, 1943). Allan (1958) describes a noninfectious disease in rainbow trout which he believes to be a vitamin deficiency disorder resulting from a diet of herring. Saunders and Henderson (MS 1969b and c) report similar adverse effects of a herring-rich diet on Atlantic salmon fry and smolts. In the present study we show that a diet of herring over a long period does lead to symptoms of dietary deficiency in Atlantic salmon; yet, when presented for shorter periods or in combination with other foods, herring may satisfy some of the criteria of a suitable fish food. MATERIALS
AND METHODS
Experiments were conducted with recently hatched fry, underyearling parr and two-year-old smolts. All were hatchery-reared and brought to the laboratory some weeks before experiments were started.
Alevins were brought to the laboratory in May and held-in fibreglass tanks with limited exchange of fresh water-until they had completed absorption of their yolk sacs and begun to eat. At this stage they are referred to as fry. Feeding was started on June 15 using freshly ground beef liver. On July 5 the fry were divided into six groups of 300. Two groups were put in fresh water (O%O), two in 6%0 salinity and two in 12%0 to allow for experiments with two diets at each of three salinities. We had determined previously that fry survived indefinitely following abrupt transfer from fresh to brackish water up to 12?& It was concluded that the lethal level for fry just after they commenced feeding is between 12 and 15%0 and that salinities between 0 and 127~ would be suitable for studies of growth over a long period. Salinities were maintained at various levels (? 1%0) by delivering fresh or salt water (30’$00) from constant-head reservoirs through drawn glass jets ground to size to give the appropriate proportions
98
96
96
I
I
I
7.8
3.7
10.7
12.8
Nov. 24 (99)
Feb. 24 (191)
May 10 (266)
June 7 (294)
98 94
98 99
I II
11.8
Oct. 26 (70) I II
98 99
I II
15.0
Sept. 21 (42)
101 100
II
I
17.9
Aug. 17 (0)
N
Temperature (“C)
Date (elapsed time)
Lot
0
(“/a,)
Salinity
12.9
11.4
9.4
8.9 8.9
8.0 8.2
6.8 7.0
5.2 5.3
Mean length (cm)
25.7
17.1
9.1
8.4 8.2
6.4 6.7
3.9 4.1
1.5 1.6
Mean weight (g)
99
99
100
100 95
100 97
100 97
100 101
N
6
14.2
12.4
9.9
9.4 9.0
8.4 8.3
7.1 7.3
5.2 5.1
Mean length (cm)
32.8
21.8
11.2
9.6 8.3
7.3 7.1
4.4 4.5
1.5 1.4
Mean weight (g)
12
97
98
98
98 96
98 100
98 100
13.2
11.8
9.6
9.2 8.7
8.3 8.1
7.0 7.1
5.1 5.0
Mean length (cm)
26.7
19.8
10.3
9.1 7.9
7.1 6.7
4.4 4.4
1.5 1.5
Mean weight (9)
and fed either liver (Lot
100 100
N
Salmon fry experiment. Mean lengths and weights of six groups reared in different salinities (0,6, 12’/,,) I) or a mixture of herring and liver (Lot II)
TABLE 1
w -1
372 of each water supply. Water temperature varied seasonally from a low of 4°C in February to a high of 18°C in August (Table I> but at any time was the same for all groups. All fry were fed beef liver from June 15 to August 24. The fry then were divided into two lots, and each lot into three groups held at 0, 6 and 12$& respectively. From August 24 onward Lot I was fed beef liver only, Lot II was fed a mixture of 50% ground, fresh or freshly frozen herring and 50% beef liver by weight. Measurements of length and weight were begun on August 17. Parr
Five groups of 110 underyearling salmon were held between December and the following June in cylindrical fibreglass tanks (l-m diameter) of flowing water with salinities of 0, 7, 15, 22 and 30?&. Salinities were maintained at the selected levels (+ ca. l%,). Temperature followed the seasonal cycle for the freshwater supply but at any time was the same (+ 0.2”C) for all groups. Finely chopped fresh herring and chopped beef liver were fed separately on alternate d,ays. The parr accepted herring more readily than liver and as a consequence consumed far more herring than liver during the experiment. Smelts
Stocks of two-year-old pat-r were brought to the laboratory in late winter and held in fresh water in cylindrical fibreglass tanks (1.8-m diameter). Water inlets together with submersible electric pumps at the periphery of each tank maintained a current speed of ca. 14 cm/set near the periphery. This current elicited a positive rheotactic response in the salmon; feeding was enhanced by dispersal of the fish throughout the tank and by constant motion of the food particles. Separate experiments were conducted during successive years beginning in June and April. In the first experiment, four groups of 95 smolts each were taken from freshwater holding tanks on June 24 and placed in separate 1.8-m tanks in which the salinity was raised within 3 days to 7, 15, 22 and 30%~ respectively. A fifth group was held in fresh water. The fish were fed to satiety two or three times daily, depending on water temperature. The diet for the first experiment was a mixture of ground beef liver, fresh herring and Purina trout chow (42.5-42.5-15% by weight) ground to a paste. Herring was excluded from the food mixture after November 20.
313 In the second experiment, five groups of 100 smolting salmon were put in water of the same salinities as used in the previous experiment. The diet from April 1 to April 22 was a mixture of equal parts of beef liver and cod fillets. A liver-cod-trout chow mixture (42.5-42.5-1570 by weight) was used from April 22 onward. In addition, a duplicate group (7-A) held at 7YG was fed the herring-liver-trout chow mixture to confirm the observation in the previous experiment that a diet containing herring caused symptoms of nutritional deficiency and mortalities. Temperature during both experiments followed the natural seasonal cycle for the freshwater supply but at any time was the same (+ O.?_“C) for all groups (Tables III, V). Food rations were weighed,to permit calculation of food conversion efficiency. Food was offered until the fish allowed it to sink to the bottom of the tank, which was taken as an indication that they were satiated. Gross conversion efficiency was calculated in terms of wet weight as weight gain by a group during the period weight of food gven dunng the period
x loo
Composition of the food can be expected to vary with different batches, and seasonally owing to changing carbohydrate, fat and protein contents of fish. The following percent dry weights from one analysis serve to show differences among the foods used: liver, 30.2; cod, 18.2; herring, 38.2 ‘and trout chow 9 1.9%. Fuller details on effects of salinity and temperature on the growth of salmon at various developmental stages are in unpublished teclmical reports (Saunders and Henderson, MS 1969a, b, and c). Some of those data are included here to make possible a fuller understanding of dietary effects. RESULTS
Both lots of fry fed readily accepted their respective foods. There were few mortalities in any group between mid-August and later October. During November there was an increase in mortalities among the herringfed groups (Lot II). Mortality rate increased directly with increase in salinity. Few of the liver-fed fry died during the period. Mortalities in the two lots between October 29 and March 4 were as follows:
374
Salinity (Ym) 0
6 12
Lot 1 (liver) (%) 3 0 2
Lot II (herring-liver) (%) 45 63 73
It was clear that inclusion of herring in the diet of fry for a period over 3 months resulted in heavy mortality. In view of the similar, low mortality rates among groups in Lot I, and increasing mortality with increased salinity in Lot II, it appears that increased salinity aggravated the adverse effect of the herring diet in Lot II. There was no indication of sizedependent mortality. Mean lengths and weights were essentially the same among groups when the fish were measured for the first time (Table I). There was little difference in growth, rates between liver-fed and herring-fed groups between August 17 and October 26. Between October 26 and November 24, growth rates of the herring-fed groups fell slightly below those of the comparable liver-fed groups (Table I). This coincided with a period of heavy mortality in the herring-fed groups. Further comparisons of growth between Lots I and II were discontinued; because of the differential mortality rates, herring-fed fish were not measured after November 24. Parr
This experiment was designed to show the effects of salinity on presmolt growth during the winter and spring. Although diet was not a variable, the experiment provided data on the-effects of feeding a diet ih which herring predominated over a long period. There were few or no mortalities among the 0,7 and 15Ym groups during the experiment (Table II). Slightly higher mortalities occurred in the 22%~~group until April 8, when 50 fish died after this group was accidentally subjected to 30%0 salinity. In the 300~ group, on the other hand, there were many deaths until March 10 after which few pan- died. Most of the smaller individuals had died by this time and the survivors were mostly large Parr, apparently well able to withstand the higher salinity. There were no indications of adverse effects from the herring-rich diet. Growth rates of the 0, 7 and 15%0 groups were similar during the experiments (Table II). No growth advantage was indicated at any of these salinity levels, nor were there salinity-dietary interactions as occurred for salmon fry: However, growth rates in 227~ were considerably lower, although mortalities in this group were of the same order as those in lower
5.9
4.1
4.2
4.8
1.7
10.3
Jan. 7 (34)
Feb. 11 (69)
March 10 (97)
April 8 (126)
May 6 (154)
May 25
100
104
109
109
109
109
110
104
103
18.2
17.8
20.1
24.8
3.1 101
102
102
107
17.7
18.5
110
13.8
2.1
11.8
11.6
11.6
11.3
10.5
* Total length; all other lengths are fork lengths. ** 52 fish died on April 8: salinity accidentally increased to 30°/,0 while fish were recovering from anaesthetic.
(173)
8.2
W
N
Mean weight
N
Mean length (cm)
7
(oloo)
0
Salinity
Temperature
1”C)
Dec. 4 (0)
Date
20.3
22.4
26.6
2.0
12.4
13.4
111
111
1 11
11
19.6
2.0
11
111
N
11
18.9
15.3
62)
Mean weight
19.5
1.8
1.6
10.8
Mean length (cm )
15
13.3
12.4
11.9
11.7
11.7
11.5
43
45**
22.5
26.5
9-l
101
105
106
108
N
18.8
18.9
18.5
18.1
15.3
(9)
(cm) 10.9
Mean weight
Mean length
22
Salmon parr experiment. Mean length and weights of 5 groups reared in different salinities (0, 7, 15, 22, 30’/,& and fed herring and liver separately on alternate days
TABLE II
13.4
12.0
11.3
11.1
11.0
10.9
10.6
W
Mean weight Mean
28.4
20.5
15.8
15.7
15.5
15.4
14.3
length (cm)
28
29
32
34
46
67
110
N
30
14.1
13.3
13.4*
12.5
12.2
11.8
11.0
Mean length (cm)
31.8
25.8
22.9
21.6
20.2
18.0
16.0
Mean weight W
376 salinities and fresh water. Clearly, 22% was above the upper limit of salinity which was suitable for growth of parr IO-12 cm long at the temperatures experienced during the experiment. There was a sharp rise in growth rates during the period April 8 to May 6 when temperatures rose from 5 to 8°C. By late May, most of the larger individuals were becoming silvery and had low condition factor and other external appearances of smolts. Smolts
Growth among the five groups in the first experiment generally was directly related to salinity (Table III; Fig.1). From June through July mean lengths and weights differed little among the salinity groups. By the ,600
:
IO-
D
‘i
6-
;
t
6-
: 4-
J ‘J
‘A’S 0
1’ i
300
36
3
36 F
6
.I
/ II
32!-
A
.- Fresh o:24-
//
;22-
x
x
7%
o-
15%.
I-
22%.
A-
30%.
Water
Salinity
J
.
20-
0
16-
/ x
I6 J
’
J
’
A
’
I
’
N’
D
J
’
F
’
Fig.1. Mean lengths and weights of smolts and post-smelts in relation to salinity. Mean temperature among groups plotted for each measuring date. All fish were fed a herring-beef liver-trout chow mixture.
31.7
32.3
33.0
42
36
34
7.5
3.6
3.0
Nov. 26 (155)
Jan. 26 (216)
Feb. 25
(246)
55
56
397.6
419.7
58
381.9
88
30.8
69
I 1.7
Oct. 26 (124)
346.8
93
244.2
27.7
73
14.3
Sept. 24 (92)
94
162.1
25.0
75
15.5
Aug. 24 (61)
94
101.1
95
15.8
July 24 (30)
21.3
16.9
96
13.2
June 24 (0)
94
Mean length (cm)
N
Date (elapsed time)
47.0
7 N
0
Salinity (%,)
34.1
44
44
455.1
45
70
86
89
92
99
N
453.0
458.3
32.9
33.7
369.4
3 1.4
283.9
183.6
25.6
28.6
112.4
47.7
Mean weight W
21.8
16.9
MeaIl length (cm)
15
Mean length and weight of 5 groups reared in different
Mean weight W
Temperature CC)
Salmon smelt and post-smelt experiment. I&-herring-trout chow mixture
TABLE 111
35.8
35.3
34.2
32.2
29.0
25.9
22.1
16.9
Mean length (cm)
541.9
535.7
506.9
389.2
293.2
191.7
113.6
48.6
Mean weight (9)
salinities (0,7, 15,22,
49
49
49
77
90
91
94
99
N
22
508.7
515.8
35.5
435.3
358.2
261.1
173.9
110.7
46.3
Mean weight (9)
35.0
33.1
31.5
28.4
25.5
21.9
16.8
Mean length (cm)
30’6,) and fed a
56
56
58
88
91
91
94
95
N
30
37.a
36.6
35.1
32.6
29.4
25.6
21.5
16.7
Mean length (cm)
572.5
574.4
542.0
410.7
304.6
184.6
104.6
46.0
Mean weight W
w
378 end of August mean lengths and weights for all groups in brackish and salt water were greater than those for the freshwater group. The 15 and 307~ fish were significantly longer and heavier (P < 0.01) than the 07m fish on October 26. At the end of the experiment all except the 7o/oo were significantly larger than the O$?&,fish. Food conversion efficiencies for the period July 24 to October 26 differed little among groups at a given time. There was little difference in efficiency within groups at different times (Table IV). Percentage efficiencies ranged from 28 to 34 and averaged about 32. TABLE IV Food conversion efficiency of post-smolt salmon reared at various salinities. All fish were fed liver-herring-trout chow mixture Interval
July 24Aug. 24 Aug.25 Sept.24 Sept. 25Oct. 26
Salinity PI&l)
Temperature PC) Mean
Range
0
7
15
22
30
15.9
15.5-16.5
0.32
0.31
0.33
0.28
0.32
15.3
15.9-14.2
0.33
0.34
0.36
0.30
0.33
13.1
14.3-11.8
0.32
0.28
0.29
0.36
0.29
Mean
0.32
0.31
0.33
0.31
0.31
There were no obvious adverse effects of the herring diet until early October. At that time many of the fish in 0, 7 and 157~ appeared abnormal. Fish lost equilibrium and often rested on their sides on the tank bottom. These fish still attempted and usually succeeded in feeding. There were few deaths; those occurring were probably hastened by secondary causes such as loss of scales and erosion of the skin through chafing on the tank bottom. On November 20 the percentages of such abnormal fish in different salinities were: Salinity (%G ) % of abnormal fish
0
7
15
22
30
64
21
18
4
3
Although incidence of the problem was inversely related to salinity, there were three distinct levels; 64% in fresh water, about 20% in 7 and 1.57~ and about 4% in 22 and 30%0. Herring was excluded from the diet after November 20. New outbreaks ceased and some of the affected fish recovered.
379 In the second smolt experiment, herring-fed fish were included (group 7-A) to confirm the observation that adverse effects were related to a diet rich in herring. Growth rates in this group at first equalled and later exceeded those of the other 7%0 fish, as well as most of the other salinity groups (Table V; Fig.2). However, it was obvious in early October that the herring-fed fish were abnormal. By late November, 20% of them either had lost equilibrium or died. None of the fish in the other groups (codliver-trout chow diet) were similarly affected. Although the herring-fed fish in the second experiment were larger in June than the corresponding groups in the first experiment, these groups had similar growth patterns during the experiments conducted during successive years. At no time was the condition factor of the herring-fed fish markedly different from that of the other groups.
35 33 -
‘IE v
29-
f
27-
0.
7 X.
0. I-
15%. 22 x.
b-
30
Salinity
i
/ I
--
l-7X.A
-
:,” 25-
Weight
23r
.’ * L
E
300 .
w
x.
I 21
100
1
X-X
19
17 IS
L
-0 :-
A
(
I
M
1
J
I
1
1
J
A
S
I
0
I
N
D
Months
Fig. 2. Mean lengths and weights of smolting salmon, smolts, and post-smolts in relation to salinity. Mean temperature among groups plotted for each measuring date. The 7-A group was given a herring-beef liver-trout chow mixture throughout the experiment. The other groups were fed a cod-liver mixture from April l-26 and cod-liver-trout chow mixture thereafter.
5.0
7.8
10.2
15.3
17.5
16.3
15.6
12.8
9.9
7.1
May 13 (42)
June 3 (63)
July 8 (98)
Aug. 12 (133)
Sept. 2 (154)
Sept. 23 (175)
Oct. 21 (203)
Nov. 10 (223)
Dec. 7 (250)
4.4
April 22 (21)
(0)
April 1
(elapsed time)
Date
57
57
60
64
70
79
84
99
100
100
100
33.6
32.8
31.8
29.9
28.1
25.8
21.7
18.8
17.1
15.9
15.5
483.9
456.9
406.4
316.6
242.3
177.0
100.2
67.6
53.8
45.0
41.2
(8)
57
57
59
65
70
80
98
100
100
100
100
N
Mean weight
N
Mean length (cm)
7
(%o)
PC)
0
Salinity
Temp.
32.9
32.2
31.2
29.2
27.5
25.8
22.7
19.1
17.1
15.9
15.5
Mean length (cm)
449.6
423.6
376.6
284.2
221.1
171.9
116.3
72.1
54.7
45.2
40.9
Mean weight (8)
53
54
58
63
68
80
96
99
100
100
100
N
7-A
33.6
32.9
31.9
29.9
28.9
27.2
23.1
19.2
17.2
16.1
15.5
(cm)
Mean length
_
471.4
447.1
398.4
297.8
259.9
204.0
128.3
73.6
57.0
48.0
41.5
Mean weight fg)
57
57
60
65
68
80
97
100
100
100
100
N
15
32.6
32.0
31.0
29.1
27.4
25.3
22.5
19.1
17.1
15.9
15.4
km)
Mean length
423.2
409.3
357.9
278.0
224.3
161.5
114.5
72.7
54.7
45.7
40.9
Mean weight (9)
57
57
60
64
70
79
97
100
100
100
100
N
22
Salmon smelt and post-smelt experiment. Mean length and weight of six groups reared in different salinities (0, 7, 15, 22, 304b,). The 7-A group was fed a he&g-live-trout chow diet throughout the experiment. The other groups were fed a cod-liver mixture from April 1-26 and a cod-liver-trout chow mixture thereafter
TABLE V
32.2
31.5
30.5
28.6
26.9
25.2
22.3
19.1
17.2
15.9
15.4
MeZUl length (cm)
417.5
393.5
342.0
261.9
204.2
160.5
111.3
73.6
55.5
45.9
40.8
Mean weight (9)
29.5
29.9
57
28.3
26.5
25.0
23.7
22.0
18.8
17.0
15.9
15.5
Mean length (cm)
57
57
62
67
78
96
100
100
100
100
N
30
318.6
309.7
262.9
192.7
156.0
126.9
104.0
70.5
54.2
45.5
41.3
Mean weight (8)
w cc 0
381 Food conversion efficiency was strongly affected by diet. Following addition of trout chow to the cod and liver mixture on April 26, there was approximately a 30% increase in conversion efficiency in all groups on that diet. The herring-liver-trout chow group (7-A) had the highest mean value for the period April to December and the highest value during six of the ten intervals (Table VI). The conversion efficiency values for the TABLE VI Food conversion efficiency of smolting salmon, smolts, and post-smolts at various salinities. Diets for various groups as described in Table V Temperature P0
Salinity P/c@)
Interval
Mean
Range
0
I
I-A
15
22
30
April 1 -April 22 April 23-May 13 May 14-June 3 June 4-July 8 July 9-Aug. 12 Aug. 13-Sept. 2 Sept. 3-Sept. 23 Sept. 24-Oct. 21 Oct. 22-Nov. 10 Nov. 11 -Dec. 7
4.1 6.2 8.9 13.0 16.9 17.3 15.8 13.7 11.3 8.2
4.2- 5.0 5.1- 7.8 7.6-10.2 10.3-15.6 15.2-18.0 18.0-16.2 16.0-15.2 15.6-12.6 12.8- 9.9 9.7- 7.0
0.19 0.32 0.29 0.22 0.30 0.29 0.26 0.23 0.23 0.14
0.22 0.32 0.31 0.27 0.22 0.25 0.23 0.23 0.20 0.14
0.33 0.28 0.27 0.34 0.32 0.36 0.27 0.32 0.23 0.14
0.23 0.32 0.34 0.25 0.21 0.30 0.21 0.22 0.24 0.07
0.23 0.32 0.32 0.31 0.21 0.24 0.23 0.23 0.23 0.11
0.20 0.33 0.32 0.22 0.13 0.20 0.17 0.21 0.17 0.05
Mean
0.25
0.24
0.29
0.24
0.24
0.20
herring-fed fish from July 9 to October 21 were similar to those of the 7%0 group as well as the other salinity groups during a comparable period in the first smolt experiment (Table IV). The mean for all groups (exclu&ng 7-A) for the period April l-22 was 21%. During the next 41 days the mean increased to 32%, presumably owing to the addition of trout chow in the diet. Although the groups other than that fed on herring had high conversion efficiency values during early summer, these values did not remain high during late summer and autumn as did those of the herring-fed fish. There did not appear to be any correlation between conversion efficiency and salinity during the summer. However, efficiency decreased more in the 30”/00 and 22%~ groups than in the others during autumn. DISCUSSION
Results of our experiment showed that finely chopped herring and beef liver are readily eaten by Atlantic salmon fry. Furthermore, growth of fry
382 fed this diet over a period of 2-3 months was equal to or greater than that attained on beef liver alone over a comparable period. Protracted feeding on the herring-rich diet, however, led to reduced growth rate and many deaths among the fry. This can be attributed to the herring component of the diet, since deaths were few in the liver-fed groups. Coble (1966) reported only slight or no adverse effects of feeding raw American smelt (Osmerus mordax) to lake trout (Salvelinus namaycush). Like herring, smelt have a high thiaminase content (Neilands, 1947). Trout feeding on smelt grew as well as or better than those fed a more balanced diet. In view of our results, Coble’s fish, which were on a smelt diet less than two months, may not have had time to develop disease symptoms or show reduced growth rates in the shorter period. The most likely explanation for these results is the demonstration by Neilands (1947) that herring has a high content of thiaminase which inactivates thiamine (vitamin Bi ). It is unlikely that spoilage of the herring and resultant destruction of essential dietary components were associated with the symptoms and deaths observed, since the herring was obtained fresh at frequent intervals during the experiment. Further support for suspecting thiaminase as the causative factor, and not the effects of herring spoilage, is the fact that mixing beef liver with the herring did not ameliorate the situation. The same explanation applies to the smolt experiment wherein the diet containing herring led to symptoms which were quickly reversible after herring was excluded from the mixture. We suggest that during mixing and storage of herring with liver, cod fillets or trout chow, the thiaminase in herring acts on any thiamine in the other foods. Support for this suggestion is given in the parr experiment in which herring and liver were fed separately on alternate days. In that experiment the fish ate far more herring than beef liver over a six-month period and showed none of the previously described symptoms. In an extensive series of experiments with captive harp seals (Phoca groenlandica) Geraci (1972) induced thiamine deficiency by feeding herring and smelts (Osmerus mordqx) without thiamine administration. The seals developed a thiamine deficiency which was sometimes fatal. Feeding of autoclaved herring did not lead to death of the seals in spite of some evidence of thiamine deficiency. Geraci found that seals maintained on a herring diet could be kept alive and free, of disease symptoms if given an oral dosage of thiamine administered 2 h before regular feeding. Our feeding of herring and beef liver on alternate days seems to have accomplished the same effect in salmon Parr. In view of Geraci’s (1972) results with autoclaved herring as a diet for seals, a similar procedure might be effective when using herring as a salmon food. However, cooking herring to deactivate thiaminase would be inconvenient and would add to opera-
383 tional costs. Moreover, our results indicate that autoclaving herring may be an unnecessary precaution if some other food is occasionally substituted for the herring. On the basis of our experiments, we suggest that Atlantic salmon can be fed fresh herring for various periods, from two to five months depending on the size of the salmon, without ill effects. Herring is an important food of Baltic salmon (Wiktor, 1961) and probably of other stocks as well. However, Baltic herring may not have high thiaminase levels (Lieck and Agren, 1944). Salmon in the sea may be able to tolerate a diet of herring for a time and benefit from its growth promoting effects if they are able to leave it for a time and feed on organisms less rich in thiaminase. In our final smolt experiment, the fish given the herring-liver-trout chow misture grew faster for some months than those given the cod-liver-trout chow mixture. The harmful effects of herring might have been avoided and the beneficial effects retained if we had fed the fish on alternate days or weeks with herring and liver, or some other food low in thiaminase, instead of mixing the two ingredients and thereby destroying thiamine in the liver. From our experience in these and other (unpublished) feeding experiments with Atlantic salmon, brook trout (Salvelinus fontinalis) and rainbow trout (Salmo gairdneri), we suggest that fresh herring can be used to advantage, when available at a low price, as a food with good growth promoting qualities. This practice of using readily available, low cost fish or fish scraps is used successfully in some salmon and rainbow trout producing plants in Norway (Saunders, 1973). We, suggest a feeding regime wherein chopped fresh herring and some commercial food (or thiaminasefree fish) are given for alternate periods to maximize the growth promoting effects of the herring while guarding against the symptoms of deficiency which often follow long-term feeding with herring. We did not determine proximate compositions of the rations or fish. Therefore, we can not evaluate growth and food conversion efficiency on an isocaloric basis. Had we taken into account energy densities of the rations, the growth resulting from different rations could be more completely understood. For example, herring is richer in fat and therefore more energy dense than cod. .Addition of trout chow to the cod-liver ration resulted in increased gross conversion efficiency, presumably owing to an increased energy density. Addition of trout chow to a herring ration may have effected an energy dilution. That growth rate was directly related to salinity in the first experiment with smolts and inversely related in the second one (Fig. 1, 2) appeared to result from differences in diet. In the experiment wherein all groups were fed herring, there was clearly a beneficial effect of high salinity which gave
384
higher growth rates and fewer mortalities than in lower salinities. In view of the beneficial effects of a moderately high salinity (305’20) while herring were being used as food, we suggest that the sea water may have provided needed thiamine. Indeed, both lake waters (Hutchinson, 1957) and marine coastal waters (Natarajan and Dugdale, 1966) contain thiamine in seasonally varying amounts. Coble (1966) suggests that lake trout may be able to feed on smelt containing thiaminase but not suffer thiamine deficiency since lake water contains thiamine. The fewer mortalities and higher growth rates in higher salinities possibly resulted from higher concentrations of thiamine in sea water than in fresh water. Salmon in the sea or those being reared in sea water may get sufficient thiamine from the environment to compensate for a thiamine destructive factor in their diet. ACKNOWLEDGEMENTS
We are greateful to Miss Mary Holmes for help during the experiments and to Messrs. K.R. Allen, A. Sreedharan, G. Fawkes and Dr. J.K. Lindsey for assistance with computer programming and analysis of data. Drs. D.W. McLeese and D.J. Wildish gave helpful suggestions for the manuscript. REFERENCES AIlan, I.R.H. (1958) Anaemic disease in rainbow trout. Cons. Perm. Int. Explor. Mer Annu. Biol., 13: 233.
Allen, K.R., Saunders, R.L., and Elson, P.F. (1972) Marine growth of Atlantic salmon (Sulmo salar) in the Northwest Atlantic. .I. Fish. Res. Bd Can., 29: 1373- 1380. Coble, D.W. (1966) Effects of adiet of raw smelt on lake trout. Can. Fish Cult., No. 36: 27-34. Deutsch, H.F. and Hasler, A.D. (1943) Distribution of a vitamin B, destructive enzyme in fish. Proc. Sot. Exp. Biol. Med., 53: 63-65. Geraci, J.R. (1972) Experimental thiamine deficiency in captive harp seals, Phoca groenlandica, induced by eating herring, Clupea harengus, and smelts, Osmsus mordax. Can. J. Zool., 50: 179-195.
Green, R.G., Evans, C.A. and Carlson, W.E. (1937) A summary of Chastek paralysis studies. Minn. Wildl. Dis. Invest., 3: 173-177. Hutchinson, C.E. (1957) A Treatise on Limnology. Vol I. Geography, Physics and Chemistry. Wiley, New York, N.Y. p. 897-898. Lieck, H. and Agren, G. (1944) On the occurrence of a thiamin inactivating factor in some species of Swedish fish. Acta Physiol. &and., 8: 203-214. Natarajan, K.V. and Dugdale, R.C. (i966) Bioassay and distribution of thiamine in the sea. Limnol. Oceanogr., ll(4): 621-629. Neilands, J.B. (1947) Thiaminase in aquatic animals of Nova Scotia. J. Fish. Res. Bd Can., 7: 94-99.
Saunders, R.L. and Henderson, relation to salinity. Fish. Res. Saunders, R.L. and Henderson, relation to salinity. Fish. Res.
E.B. (MS 1969a) Survival and growth of Atlantic salmon parr in Bd Can. Tech. Rep., No. 147. E.B. (MS 1969b) Survival and growth of Atlantic salmon fry in Bd Can. Tech. Rep. No. 148.
385 Saunders, smelts Saunders, Stoddard,
R.L. and Henderson, E.B., (MS 1969~) Growth of Atlantic salmon smelts and postin relation to salinity, temperature and diet. Fish. Res Bd Can. Tech. Rep., No. 149. R.L. (1973) Salmonid aquaculture in Norway. Atl. Salmon J., No. l(1973): 8-13. J.H. (MS 1968) Fat contents of Canadian Atlantic herring. Fish. Res. Bd Can. Tech.
Rep., No. 79.
Tappel, A.L. (1965) Oxidative reactions and enzymes. In: R. Kreuzer (Editor), The Technology of Fish Utilization, Contributions from Research. Fishing News (Books), London, pp. 129-134. Thurow, F. (1966) Beitrage zur Biologie und Bestandskunde des Atlantischen Lachses (Salmo solar L.). Ostsee Ber. Dtsche Wiss. Komm. Meeresforsch., 18: 223-379. Wiktor, K. (1961) Food investigations on salmon and sea trout in southeastern Baltic. Cons. Perm. Int. Explor. MerAnnu.
Biol., 16: 251-252.