www.elsevier.nlrlocateraqua-online
Effect of dietary histamine supplementation on
growth and tissue amine concentrations in blue
shrimp Litopenaeus stylirostris
Mireya Tapia-Salazar
a, Trevor K. Smith
b, Andrew Harris
b,
Denis Ricque-Marie
a,), Lucia-Elizabeth Cruz-Suarez
aa
Programa Maricultura, Facultad de Ciencias Biologicas, Uni´ Õersidad Autonoma de Nue´ Õo Leon, Cd.´
UniÕersitaria, Apdo. Postal F-56, San Nicolas de los Garza, NueÕo Leon 66450, Mexico´
b
Department of Animal and Poultry Science, UniÕersity of Guelph, Guelph, Ontario, Canada N1G 2W1
Received 4 April 2000; received in revised form 31 July 2000; accepted 1 August 2000
Abstract
Recent studies have shown that feeding diets supplemented with fish meal containing high levels of biogenic amines to shrimp reduced growth and feed consumption. An improvement in growth, however, has been found in shrimp fed a diet supplemented with histamine and cadaverine. The objective of the current experiment was to provide more information about the effect of dietary histamine on the growth of blue shrimp Litopenaeus stylirostris and the impact on biogenic amine concentration in shrimp tissues. Six experimental diets were manufactured and supplemented with histamine at 0, 600, 1200, 2400, 3600 and 4800 mg kgy1 and tested in a
feeding trial for 28 days. Histamine supplementation did not have any effect on feed consumption,
Ž .
feed conversion ratio or survival. Weight gain fitted a quadratic dose response curve P-0.05 ,
y1 Ž
with maximum values at 1200 and 2400 mg kg of dietary histamine weight gain being 8.8%
.
higher than for the control , and lower growth at higher doses. Spermidine concentration in whole shrimp tissue increased linearly with dietary histamine supplementation. It was concluded that dietary histamine supplementation at the levels tested does not have any negative effect on shrimp performance. Moreover, an improvement in weight gain was observed when histamine was supplemented at moderate levels.q2001 Elsevier Science B.V. All rights reserved.
Keywords: Histamine; Shrimp; Growth performance; Feeding and nutrition; Toxicity
)Corresponding author. Tel.:q52-8-3526380; fax:q52-8-3526380.
Ž .
E-mail address: drique@ccr.dsi.uanl.mx D. Ricque-Marie .
0044-8486r01r$ - see front matterq2001 Elsevier Science B.V. All rights reserved. Ž .
1. Introduction
Amines are synthesized by animal and plant cells, but are also produced by
Ž .
microbiological activity Stratton et al., 1991 . Histamine is a heterocyclic compound
Ž .
formed by the decarboxylation ofL-histidine Ten-Brink et al., 1990 . The presence of this compound in foods or feedstuffs at high levels is considered to be toxic and ingestion causes effects such as mortality, decreased weight gain and feed consumption
Ž .
in chickens Harry et al., 1975; Osuna, 1985 . Histamine is used as a quality criterion for fish meals manufactured principally from warmwater species, such as anchovy,
mack-Ž .
erel and sardine Pike and Hardy, 1997 . The effect of dietary amines on fish is unclear.
Ž . Ž .
Cowey and Cho 1992 and Fairgrieve et al. 1998 reported a decrease in feed
Ž y1.
consumption of rainbow trout fed diets supplemented with putrescine 13.3 g kg and
Ž y1. Ž . Ž .
histamine 2 g kg . Watanabe et al. 1987 and Fairgrieve et al. 1994 , however, observed that dietary histamine supplementation caused intestinal damage, but did not
Ž .
affect feed intake or weight gain. Cruz-Suarez et al. 1996 reported reduced feed intake, lower weight gain and increased mortalities when fish meals rich in biogenic amines
Žcadaverine, putrescine and histamine were included to shrimp diets. Tapia-Salazar et. Ž .
al. 1998 , however, demonstrated that dietary supplementation with biogenic amines
Žhistamine, cadaverine, putrescine and tyramine did not affect feed conversion ratio or.
survival of shrimp. Weight gain and feed consumption increased, moreover, with dietary
Ž y1. Ž y1.
histamine 559 mg kg plus cadaverine 620 mg kg supplements. The aim of the current study was to provide further information about the effects of dietary histamine on growth of blue shrimp Litopenaeus stylirostris and the impact on tissue amine concentrations.
2. Material and methods
2.1. Experimental diets
Ž .
A basal diet was formulated Table 1, unsupplemented diet to meet the nutritional
Ž .
requirements for blue shrimp as recommended by Akiyama et al. 1991 . A series of test
Ž w x
diets containing graded levels of histamine dihydrochloride 2- 4-imidazolyl
eth-. Ž .
ylamine Sigma, St. Louis, MO was prepared by supplementing the basal diet with 600, 1200, 2400, 3600 and 4800 mg kgy1. Each diet was analysed to determine
Ž . Ž . Ž
moisture A.O.A.C., 1990, method 920.36 , protein Tecator, 1987 , lipid Tecator,
. Ž . Ž .
1983 , ash A.O.A.C., 1990, method 942.05 , fibre AOAC, 1990, method 962.09 and
Ž .
carbohydrate calculated by difference concentrations. Diet stability was tested by
Ž y1.
immersing 5 g diet samples in seawater 268C, 35 g l for 1 h according to Aquacop
Ž1978 , using six replicates for each diet. Dietary histamine content was determined.
Ž .
before and after the leaching test at Inual-Tepual Laboratory Santiago, Chile by HPLC
ŽTable 2 according to Seiler and Knodgen 1978 ..
¨
Ž .2.2. Feeding trial
Ž .
Table 1
Fundacion Chile. Moisture 7.2%, protein 70.5%, lipid 8.4%, ash 14%, sand 0.1%, chlorides 2.3%, free
y1 Ž . y1
fatty acids 4.6%, histamine 545 mg kg , Total Volatile Nitrogen TVN 105 mg N 100g .
b
INVE Baasrode, Belgium: Ascorbic acid 60 000 mg kgy1, ascorbyl polyphosphate 60 000 mg kgy1,
retinol 4000 IU gy1, menadione 16 000 mg kgy1, thiamin 24 000 mg kgy1, cholecalciferol 3200 IU gy1,
0.36%, crude ash 27.2%, crude fiber 0.21%.
d
was fed to five replicated groups of 10 shrimp housed in a fibreglass tank 50 shrimp per
.
treatment . Tank working water volume was 8 l and 42% of this volume was changed once a day to maintain water quality; these tanks were held in 500 ly1 tanks to maintain
a constant temperature. Water parameters were: temperature 288C; salinity 35 g ly1; pH w x y1 w x y1 w y1x y1 w y1x
Histamine concentration in the experimental diets mg kg as free base
Histamine supplemented Before leaching After leaching
The daily feed ration was calculated initially as 10%, the biomass of each tank and the amount was then reduced accordingly for each tank to minimize the amount of
Ž .
uneaten feed. The shrimp were fed two times per day 12:00 and 17:00 . The first meal accounted for 50% of the total daily ration and was completely consumed before next feeding in most cases. In the second feeding period, the remainder of the feed was
Ž .
offered. Uneaten feed was determined visually the next day 07:00 before cleaning the tank. Uneaten feed ranged between 0% and 10% of the total feed offered daily, the most frequent value being 5%.
Weight gain, feed consumption, feed conversion ratio and survival were calculated
wŽ
for each tank using the following formulas: %weight gains final weightyinitial
. x Ž . 28 wŽ
weightrinitial weight =100; individual feed consumption g sSis1 feed given on
. x
day iyuneaten feedrnumber of shrimp on day i ; feed conversion ratiosindividual
Ž . Ž . Ž . wŽ
feed consumption grindividual mean increase in weight g ; survival rate % s final
. x
number of shrimprinitial number of shrimp =100 .
2.3. Determination of polyamine concentrations in shrimp tissues
On completion of the feeding trial, the shrimp were deprived of food for 24 h before sampling. All the shrimp in the tank were sampled and the pool was considered as an experimental unit. Hepatopancreas tissue was removed from each shrimp. The shrimp samples were lyophilized, vacuum packed and stored at y808C until analysed. His-tamine, cadaverine, putrescine, spermidine and spermine were analysed by HPLC
Ž .
according to the method described by Tapia-Salazar et al. 2000 .
2.4. Statistical analyses
A random block design was used and the treatments were compared by orthogonal
Ž . Ž .
contrasts Zar, 1974 using SAS software 1987 . Fitness of the response with a linear or quadratic model was considered significant when PF0.05.
3. Results
3.1. Experimental diets
The chemical composition of the experimental diets was 8"0.2% moisture, 41"
0.4% protein, 9.3"0.1% lipid and 8.6"0.5% ash. The loss of dry matter after 1 h of immersion in seawater was 5.9"0.3%. Histamine values for the experimental diets
Ž .
approximated calculated values Table 2 . After the leaching test, histamine levels were reduced by 54% for the control diet and 72–75% for the supplemented diets.
3.2. Feeding trial
Feed consumption, feed conversion ratio and survival values were not significantly
Ž .
Table 3
Shrimp performance during the feeding trials
y1 a b b b b
Ž . Ž . Ž . Ž . Ž .
Histamine supplemented mg kg FW g FC g WG % FCR S %
0 0.44 0.68 490 1.88 100
600 0.42 0.69 462 2.04 94
1200 0.47 0.70 532 1.78 92
2400 0.48 0.70 535 1.77 100
3600 0.44 0.67 490 1.79 98
4800 0.43 0.66 472 1.89 92
Pooled SD 0.04 0.04 49.21 0.15 8.72
Significance
Linear NS NS NS NS NS
Quadratic P-0.05 NS P-0.05 NS NS
Ž .
FWsfinal weight; FCsfeed consumption grshrimpr28 days ; WGsweight gain; FCRsFeed conversion ratio; Sssurvival; SDsstandard deviation; NSsnot significant.
a
ns50.
b
ns5.
feed. The feed conversion ratio ranged between 1.77 and 2.04. A quadratic effect was observed on weight gain with a maximum for shrimp fed 1200 and 2400 mg histamine
y1 Ž .
kg of diet. This was an 8.8% increase in weight gain compared to controls Fig. 1 . Survival for shrimp fed all diets was over 92% and mortality was not related to dietary reatment.
3.3. Polyamine concentration in shrimp tissues
The polyamine concentration in shrimp tissues are given in Table 4. Cadaverine, spermidine and spermine were detected. Concentrations in hepatopancreas were higher
Table 4
Ž y1 .
Shrimp tissue polyamine concentrations mg mg of dry sample as homogenized
y1 a b
Ž .
Histamine supplemented mg kg Body Hepatopancreas
Cad Spd Spm Cad Spd Spm
0 5.7 14.2 83.7 57.1 287.2 161.7
600 3.1 13.0 74.6 48.6 267.0 161.6
1200 5.6 13.9 76.8 57.9 288.3 157.8
2400 5.6 14.2 85.4 78.8 272.7 147.7
3600 5.8 15.4 81.7 46.0 271.9 142.2
4800 4.2 15.7 82.2 41.2 260.5 137.9
Pooled SD 1.8 2.9 15.6 50 77.8 40.5
Significance
Linear NS P-0.05 NS NS NS NS
Quadratic NS NS NS NS NS NS
Cadscadaverine; Spdsspermidine; Spmsspermine; NSsnot significant; SDsstandard deviation.
a Ž Ž . .
ns10 five samples pooled by tank per diet and two injections per sample .
b Ž .
ns5 five samples per diet and one injection per sample .
than those in the body. Histamine and putrescine concentrations were below the
Ž y1.
detection limit 50 pmol ml . Spermidine concentration in whole body increased linearly with dietary histamine supplementation.
4. Discussion
Ž . Ž .
Cowey and Cho 1992 and Fairgrieve et al. 1998 have reported decreases in feed
Ž y1.
intake in rainbow trout fed diets supplemented with putrescine 13.3 g kg and
Ž y1. Ž . Ž .
histamine 2 g kg . Watanabe et al. 1987 and Fairgrieve et al. 1994 did not
Ž y1.
observe any effect of histamine supplementation 1000 to 10 000 mg kg but observed
Ž .
intestinal damage. Tapia-Salazar et al. 1998 reported an increase in feed consumption
Ž y1. Ž y1.
of small L. stylirostris fed histamine 559 mg kg plus cadaverine 620 mg kg . In the current experiment, no effect of histamine was observed on feed intake.
Ž y1.
The feeding of a diet supplemented with dietary histamine 4000 mg kg to chicks
Ž .
has been shown to depress growth and cause gizzard lesions Harry and Tucker, 1976 .
Ž .
The effect of dietary histamine on rainbow trout is not clear. Watanabe et al. 1987 observed that supplementation with 70 mg kgy1 improved net protein utilization and
Ž .
protein efficiency ratio. Fairgrieve et al. 1994 , however, reported intestinal damage of rainbow trout fed 2000 mg kgy1, although growth was not affected. Feeding diets
Ž
supplemented with fish meal containing moderate levels of biogenic amines resulting in dietary concentrations of 367, 173, 100, 56 and 30 mg kgy1 for histamine, cadaverine,
.
putrescine, tyramine and phenylalanine, respectively; Cruz-Suarez et al., 1996 or pure
Ž y1
amines histamineqcadaverine, dietary concentrations 559 and 620 mg kg ,
respec-. Ž .
tively to shrimp L.Õannamei and L. stylirostris resulted in an increase in weight gain
ŽTapia-Salazar et al., 1998 . In the current experiment, the growth response of shrimp.
response at dietary concentrations of 1200 and 2400 mg kgy1 diet. This response is in accord with the slight growth improvements found in previous experiments at lower dietary concentrations. The lack of growth improvement at the 600 mg kgy1 concentra-tion in the present case can be attributed to the inherent variability of different experimental groups.
High mortalities have been observed in poultry with dietary histamine
supplementa-Ž .
tion Harry et al., 1975; Osuna, 1985 . Survival in rainbow trout was not affected by
Ž .
dietary histamine Watanabe et al., 1987; Fairgrieve et al., 1994, 1998 . In the current experiment, we observed that histamine supplementation had no influence on shrimp mortality. Toxicity of histamine may be greater in poultry than in fish and shrimp.
Ž
It has been observed that tissues with high metabolic activity pancreas, intestine,
.
kidney and liver contain higher concentration of polyamines than tissues with lower
Ž . Ž
metabolic activity muscle due to the short half life of these tissues Bardocz et al.,
.
1993; Seidel and Scemama, 1997 . In the current experiment, putrescine, spermidine and spermine concentrations were higher in the hepatopancreas than in the whole body. This is likely due to a higher physiological activity in hepatopancreas than in other tissues such as muscle. Histamine supplementation significantly increased spermidine concen-trations in whole shrimp, although no explanation was found for a correlation between histamine and spermidine concentrations. In mammals, histamine is rapidly metabolised,
Ž .
leaves the blood stream and appears in almost all tissues as metabolites Beaven, 1978 .
Ž .
Arnould 1986 reported that carcinine synthetase can metabolize neuronal histamine and also possibly exogenous histamine in Carcinus maenas. In this experiment, his-tamine was not detected in shrimp tissues. It is possible, therefore, that the shrimp can metabolize histamine into storage or excretory forms. Unfortunately, histamine metabo-lites were not analysed in the current experiment.
5. Conclusion
It can be concluded that up to 4800 mg kgy1 of dietary histamine supplementation
does not affect feed consumption, feed conversion ratio or survival of L. stylirostris. Histamine supplementation resulted in a quadratic effect on weight gain with a maxi-mum response at 1200 and 2400 mg kgy1, but lower growth rates were seen at higher doses.
Acknowledgements
This study has been funded by Universidad Autonoma de Nuevo Leon, Mexico
´
´
ŽPAYCYT ; Ontario Ministry of Agriculture, Food and Rural Affairs OMAFRA ;. Ž .Ž .
Agricultural Adaptation Council AAC ; Hiram Walker and Sons, Windsor, Ontario; and
Ž .
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