Hematology and Plasma Chemistry Reference

Intervals for Cultured Tilapia (Oreochromis Hybrid)

Terry C. Hrubec, DVM, PhD; Jenifer L. Cardinale, DVM; Stephen A. Smith, DVM, PhD

Abstract: Tilapia are a commonly aquacultured fish yet little is known about their normal physiology and
response to disease. In this study we determined the results of complete hematologic (n = 40) and plasma bio-
chemical profiles (n = 63) in production tilapia (Oreochromis hybrids). The fish were raised in recirculating
systems with a high stocking density (120 g/L), and were in the middle of a 15-month production cycle. Blood
was analyzed using standard techniques, and reference intervals were determined using nonparametric meth-
ods. Non-production tilapia (n = 15) from low-density tanks (4 g/L) also were sampled; the clinical chemistry
results were compared to reference intervals from the fish raised in high-density tanks. Differences were noted
in plasma protein, calcium and phosphorus concentrations, such that reference intervals for high-den-sity
production tilapia were not applicable to fish raised under different environmental and management con-
ditions. (Vet Clin Pathol 2000;29:7-12)

Key Words: Clinical chemistry, fish, hematology, reference intervals, tilapia

◆
Tilapia are the second most commonly cultured fish in the
world,1,2 and are a food staple in many parts of Africa, Asia
and South America. Tilapia consumption has increased in
the United States, where it is the fourth most commonly
cultured food fish. Aquaculture of tilapia, as with other
species of finfish, is adversely affect-ed by production
related disorders and infectious dis-eases.1 Unfortunately,
there are few diagnostic tools available to veterinarians and
fish health professionals to evaluate disease in fish. Many
of the clinical tools used to evaluate mammalian health are
not developed for use in fishes. As the aquaculture industry
expands, there is an increasing need for improved
diagnostic methods. Hematology and clinical chemistry
analysis, although not used regularly in fish medicine, can
provide sub-stantial diagnostic information once reference
values are established. In this study, we determined
reference inter-vals for hematologic and plasma chemistry
analytes in cultured tilapia. We also evaluated clinical
chemistry results from a small group of tilapia raised under
differ-ent culture conditions. To our knowledge, this is the
first study to determine complete hematologic and clinical
chemistry results for tilapia, and to report the values as
reference intervals suitable for diagnostic use.
Materials and Methods
Production tilapia (Oreochromis nilotica O. mossam-bicus
O. aureus hybrids) were maintained indoors in 8 high-
density (120 g/L) tanks (10,220 L) at Virginia Tech’s
Aquaculture Center.The fish, in the middle of their pro-
duction cycle (mean weight 240 g, mean length 22 cm),
were fed a commercial tilapia feed (Southern States,
Richmond, VA, USA) at 4% of body weight per day. Tanks
received a 12% fresh water exchange per day. Water quality
was monitored daily and was considered acceptable for
high-density production systems (Table 1). Each of the 8
tanks was sampled once, with 10 fish per tank bled for
biochemical analysis and 10 fish bled for hematologic
analysis. Fish with any gross abnormal-ity were not
included in the study. Careful netting and handling was
implemented to minimize stress. Fish were rapidly netted,
anesthetized in aerated buffered tricaine methanesulfonate
(MS-222, Sigma Chemical Co. St. Louis, MO, USA) and
bled with a needle and syringe from the caudal vessels. The
blood was placed in tubes containing either lithium heparin
for chemistry analysis, or EDTA for hematologic analysis.
Any hemo-lyzed, clotted or insufficient volume samples
were dis-carded. After sampling, fish were placed in a
separate tank of fresh water for recovery.
Blood in heparinized tubes was centrifuged imme-
diately at 14,000 g for 5 minutes. The plasma was col-
lected and frozen at –10°C until all fish were sampled.
Plasma samples were analyzed using an automated dry
chemistry system (Kodak Ektachem 700, Eastman Kodak
Co., Rochester, NY, USA) for total protein, albu-min,
creatinine, ammonia, total bilirubin, cholesterol, sodium,
chloride, potassium, calcium, magnesium and phosphorus
concentrations, and alkaline phosphatase

From the Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinary Medicine, Virginia
Polytechnic Institute and State University, Blacksburg, VA 24061. Address correspondence to Dr. Hrubec (thrubec@vt.edu).

Vol. 29 / No. 1 / 2000 Veterinary Clinical Pathology Page 7

 Tilapia Hematology and Plasma Chemistry Values

Table 1. Mean water quality values for high-density (120 Table 2. Plasma chemistry reference intervals for hybrid
g/L) and low-density (4.3 g/L) tilapia production systems. tilapia (n = 63) raised in high-density production systems.

Parameter High Density Low Density Analyte Reference Interval Median

Temperature (°C) 29.9 26.7 Total Protein (g/dL) 2.9-6.6 3.9
pH 7.4 7.5 Albumin (g/dL) 1.3-2.6 1.8

NH3 non-ionized (mg/L) 0.020 0.004 Globulins (g/dL) 1.6-4.2 2.1

NO2-N (mg/L) 0.36 0.01 Creatinine (mg/dL) 0.1-0.5 0.2

70 3 Ammonia (µg/dL) 111-414 249

NO3-N (mg/L)
Alkalinity (mg/L)* 105.0 34.2 Total bilirubin (mg/dL) 0.0-0.3 0.2
† 281.0 51.3 ALP (U/L) 15-39 22
Hardness (mg/L)
AST (U/L) 9-102 26
Dissolved oxygen (mg/L) 9.4 ND
Sodium (mEq/L) 139-160 151
Turbidity (NTU) 9 ND
Potassium (mEq/L) 3.5-5.4 4.3
*Alkalinity is a measure of the buffering capacity of the water.
† Chloride (mEq/L) 128-142 136
Hardness is the sum of the calcium and magnesium ions
in the water. ND = not determined Calcium (mg/dL) 13.6-69.4 31.0
Magnesium (mg/dL) 1.9-3.5 2.5
(ALP) and aspartate aminotransferase (AST) activities. Phosphorus (mg/dL) 5.5-22.1 9.1
Globulins were calculated from the difference between total
Glucose (mg/dL) 30-69 46
protein and albumin values.
Blood from the EDTA tubes was drawn into micro- Cholesterol (mg/dL) 110-318 189
hematocrit tubes and the PCV was determined after
ALP = alkaline phosphatase; AST = aspartate aminotransferase
centrifugation for 5 minutes at 10,000 g. Plasma pro-tein
was determined with a clinical refractometer using plasma
from the microhematocrit tube. The total RBC count was thrombocyte clumping (< 4 cells clumped) were used for
determined manually with a Neubauer hemacytometer differential counts. If thrombocyte clumping was more
using Natt-Herrick’s solution as a dilu-ent stain.3 Slight severe, the samples were discarded. Leukocyte size was
thrombocyte clumping prevented accurate enumeration of a measured in 10 WBC of each type, in 10 different fish, to
combined WBC + thrombo-cyte count on the give a range of diameters for each cell type. Hemoglobin
hemacytometer. Blood smears were made within 45 was determined, using the cyanomethemoglobin method
minutes of sample collection, stained with Wright-Giemsa, (Sigma). Prior to reading the absorbance, hemo-globin test
and used to determine the WBC + thrombocyte count, samples were centrifuged to remove dis-persed nuclear
differential WBC counts, and cell size estimates. material. The RBC, MCV, MCH, and MCHC were
Percentages of RBC and WBC + throm-bocytes were calculated by standard formulas.
determined by counting 1,500 cells. The WBC + Reference intervals were determined following the
thrombocyte percentage was multiplied by the RBC count guidelines proposed by the National Committee for Clinical
from the hemacytometer to determine the WBC +
Laboratory Standards (NCCLS).7 As suggested in these
thrombocyte absolute count. For the differential count,
WBC and thrombocytes were counted until 200 WBC were guidelines, outliers were determined using the 1/3 ratio
enumerated on blood smears, and the per-centages of each difference/range ratio. Two hematologic values and one
WBC type and of thrombocytes were multiplied by the total biochemical value were identified as outliers and were
WBC + thrombocyte count to obtain absolute differential deleted. Remaining values were then ranked, and the high
cell counts. Thrombocyte numbers were subtracted from the and low 2.5% were discarded. The range of the remaining
WBC + thrombocyte count to obtain a total WBC count. values provided the reference interval.
This method of man-ually determining total WBC and Plasma chemistry values from 15 non-production
tilapia (mean weight 350 g) were compared to reference
differential counts has been recommended for avian4 and
intervals determined for the production fish. Non-pro-
fish5 blood because nucleated RBC prevent accurate duction fish conditions were characterized by lower
enumeration using automated analysis.6 Only smears with stocking density (4.3 g/L), lower feeding rate of the
mild

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 Hrubec, Cardinale, Smith

Table 3. Plasma chemistry results for hybrid tilapia (n = 15) Table 4. Hematology reference intervals for hybrid tilapia
raised in low-density systems compared to reference intervals (n = 40) raised in high-density production systems.
from tilapia raised in high-density systems (see Table 2).

Analyte Reference Interval Median

Analyte Range* Median Compared to
PCV (%) 27-37 33
Ref. Intervals (n)
Low Within High Hemoglobin (g/dL) 7.0-9.8 8.2
Total protein (g/dL) 2.3-3.6 2.9 7 8 0 MCV (fL) 115-183 135.7
Albumin (g/dL) 1.0-1.6 1.2 9 6 0 MCH (pg) 28.3-42.3 34.9
Globulins (g/dL) 1.3-2.1 1.6 6 9 0 MCHC (g/dL) 22-29 25.7
Creatinine (mg/dL) 0.2-1.1 0 0 14 1 Plasma protein (g/dL) 4.8-7.8 6.1
Total bilirubin (mg/dL) 0.0-0.1 0 0 15 0 6 1.91-2.83 2.31
RBC (X 10 /µL)
ALP (U/L) 16-38 26 0 15 0 WBC (/µL) 21,559-154,690 75,659
AST (U/L) 5-124 18 1 13 1
Small lymphocytes (/µL) 6,776-136,390 61,164
Sodium (mEq/L) 140-156 150 0 15 0
Large lymphocytes (/µL) 2,852-30,833 10,720
Potassium (mEq/L) 3.2-4.3 3.9 2 13 0
Neutrophils (/µL) 557-9,873 1,805
Chloride (mEq/L) 136-147 141 0 10 5
Monocytes (/µL) 400-4,286 1,520
Calcium (mg/dL) 10.5-19.0 11.8 14 1 0
Eosinophils (/µL) 35-1,645 334
Magnesium (mg/dL) 2.3-2.8 2.5 0 15 0
TLC (/µL) 35-4,336 972
Phosphorus (mg/dL) 3.5-7.2 4.6 13 2 0
Thrombocytes (/µL) 25,068-85,216 52,762
Glucose (mg/dL) 39-96 52 0 13 2
TLC = thrombocyte-like cell
Cholesterol (mg/dL) 64-299 156 2 13 0

*Minimum-maximum values
ALP = alkaline phosphatase; AST = aspartate aminotransferase
same diet (1% of body weight per day), greater fresh water
exchange rate (35% per day) and, consequently, more
optimal water quality (Table 1). Fish were sam-pled and the
blood was processed as described for fish raised in high-
density tanks.
and thrombocytes. The RBC were nucleated, oblong cells
measuring 7.0 12.9 µm in size. Nuclei stained purple and
cytoplasm stained reddish-gray. Immature RBC, or
polychromatophilic RBC, had a blue-grey tinge to the usual
eosinophilic cytoplasm; these cells were included in RBC
counts.
Cell morphology

Results Six types of WBC were distinguished and counted: small

Analyses
Reference intervals for plasma chemistry analytes were
summarized (Table 2). Plasma chemistry values from non-
production tilapia were summarized and com-pared to
reference intervals from production tilapia (Table 3).
Protein concentrations in tilapia raised in high-density
systems were slightly higher, while calci-um and
phosphorus levels were much higher com-pared to fish in
low-density systems.
Reference intervals for hematology analytes were
summarized (Table 4). As in other species of fish, there
were three types of circulating blood cells: RBC, WBC
lymphocytes, large lymphocytes, neutrophils, monocytes,
eosinophils and thrombocyte-like cells (TLC) (Figures 1-6).
Small lymphocytes ranged from 4.6 to 5.0 µm in diameter,
and had dark purple, round to oval, condensed nuclei with
clumped chromatin. Small lymphocyte cytoplasm was deep
blue and often consist-ed of only a thin rim encircling the
nucleus. Large lym-phocytes measured 5.7 to 6.4 µm in
diameter, and had round nuclei that were larger and had a
more open chromatin pattern than small lymphocytes.
Large lym-phocyte cytoplasm was more deeply basophilic
and abundant than that of small lymphocytes. Both small
and large lymphocytes had high N:C ratios. Frequently,
lymphocytes had cytoplasmic pseudopods and azurophilic
cytoplasmic granules.

Vol. 29 / No. 1 / 2000 Veterinary Clinical Pathology Page 9

 Tilapia Hematology and Plasma Chemistry Values

Figure 1. Small lymphocyte (SL), large lymphocyte (LL), Figure 4. Eosinophil (E) with an eccentric nucleus and moderate num-
and a thrombocyte (T). Thrombocytes can be distinguished ber of eosinophilic granules. A small lymphocyte (SL) is also present.
from lym-phocytes by the highly condensed nucleus and Photograph taken with a didymium filter. Wright-Giemsa. Bar = 10 µm.
grey cytoplasm. Wright-Giemsa. Bar = 10 µm.

Figure 5. Eosinophil (E) with a large number of granules. A

throm-bocyte (T) with a slightly indented nucleus and one
Figure 2. Monocyte (M) with an indented nucleus and vacuoles.
with a seg-mented nucleus (insert) are present. Photograph
Wright-Giemsa. Bar = 10 µm. taken with a didymium filter. Wright-Giemsa. Bar = 10 µm.

Figure 3. Neutrophil (N) with an irregular cytoplasmic Figure 6. Thrombocyte-like-cell (TLC), thrombocyte (T) and a small
border. A small lymphocyte (SL) and a thrombocyte (T) lymphocyte (SL). The TLC can be distinguished by a more open
are also present. The insert depicts a neutrophil with a nucleus and more abundant grey cytoplasm than is seen in either
bean shaped nucleus. Wright-Giemsa. Bar = 10 µm. the thrombocyte or lymphocyte. Wright-Giemsa. Bar = 10 µm.

Page 10 Veterinary Clinical Pathology Vol. 29 / No. 1 / 2000

 Hrubec, Cardinale, Smith
Monocytes measured 9.4 to 10.7 µm in diameter and
had round or indented, eccentric nuclei with an open
chromatin pattern (Figure 2). Monocyte cytoplasm was
deeply basophilic and often contained clear, punc-tate,
cytoplasmic vacuoles. Neutrophils were 9.6 to 10.8 µm in
diameter, and had round, oval or reniform nuclei with an
open chromatin pattern (Figure 3). Neutrophil cytoplasm
was stippled, gray to lightly basophilic, and had occasional
vacuoles and basophilic, intracytoplas-mic inclusion bodies.
Cytoplasmic borders were irregu-lar. Eosinophils were 5.7
to 6.7 µm in diameter, and had round, light purple, often
eccentric nuclei with open chromatin (Figures 4, 5).
Eosinophil cytoplasm was lightly basophilic and contained
eosinophilic granules ranging from small and few to large
and numerous. The eosinophil granules occasionally
obscured the nucleus. Thrombocyte-like cells were clearly
identified in WBC differentials as a distinct cell type
(Figure 6). The TLC were larger (5.6 to 7.2 µm diameter)
and had a less con-densed nuclear chromatin pattern than
thrombocytes. The cytoplasm of TLC was pale gray,
slightly stippled and more abundant than that of
thrombocytes. Throm-bocytes (counted separately from
WBC) were 4.7 to 5.5 µm in diameter, and had very dark,
dense, purple nuclei that were round, polygonal or
segmented (Figures 1, 3, 5, 6). Thrombocyte cytoplasm was
clear to slightly basophilic, and occasionally vacuolated.
In a few fish, large cells with extremely blue cyto-
plasm were rarely noted. These cells were considered
undifferentiated blast cells; due to their immaturity, we
were unable to morphologically determine the cell line. The
blast cells were not included in cell counts.
Discussion
Although tilapia are the second most frequently cul-tured
fish in the world, there are surprisingly few reports of
normal blood values. In addition, published values are
severely limited by low fish numbers or by the few analytes
measured.8-10 Compared with previ-ously reported values,
our results were similar for most analytes. 8-10 Terao and
Ogawa8 reported much higher mean concentrations of
cholesterol (567 mg/dL), glu-cose (408 mg/dL) and
creatinine (4.3 mg/dL). Hussein et al 10 obtained slightly
lower values for PCV (20%), hemo-globin concentration
(6.0 g/dL) and RBC count (1.31 x106/µL) than those in our
study. Haniffa and Vijayarani9 reported even lower PCV
(10%), hemoglobin (3.7 g/dL) and RBC (0.90 x10 6/µL)
values.These differences may be due to the fact that the
production fish in our study were hybrids of parental
species used in previous stud-ies.The earlier studies are of
limited use for comparison and diagnostic purposes because
too few fish were sampled and the fish populations were
not well
Vol. 29 / No. 1 / 2000 Veterinary Clinical Pathology
defined.
Leukocyte numbers reported for one parent species, O.
mossambicus,9 were similar to those for Oreochromis
hybrids reported herein. Additionally, WBC types and
morphology in this study were similar to those described
for O. mossambicus.11 In O. mossam-bicus, three
granulocyte types were distinguished by ultrastructural
observation. Two granulocytes repre-sented the neutrophils
and eosinophils seen by light microscopy, while the third
granulocyte was unidenti-fied by light microscopy. This
third cell type may be the TLC described here. The TLC is
a distinct cell type that has been observed and described in
other fish species.12 The cells were first described in hybrid
striped bass, in which they superficially resembled
thrombocytes; they were termed TLC to distinguish them
from other unidentified cells. The function and origin of
TLC were not determined. In tilapia, TLC appeared similar
to a small neutrophil with lighter cytoplasm. Because TLC
were identified in all individual tilapia, as well as in other
fish species, the cell probably represents a matu-rational
stage of one of the WBC, although the cell’s lin-eage and
function remain unknown.
Distinguishing lymphocytes from thrombocytes can be
difficult; however, in our laboratory we do a number of
procedures to help ensure cells are identi-fied correctly,
including routine repetitions of differen-tial counts, and
having more than one person repeat the differential counts.
While these measures do not always ensure the cells are
accurately identified, they do pro-vide consistency. The
high WBC and lymphocyte counts were consistent with
values obtained in our laboratory for other fish species
raised in high-density recircula-tion systems, including
hybrid striped bass, yellow perch and tilapia (unpublished
observations).12 Leukocyte counts in these same species
maintained under low production densities are lower by
40% to 50%.12 Fish in high-density production systems are
exposed constantly to high bacterial loads in the water and
less than optimal water quality, factors which may influence
WBC counts.
When reference intervals for production tilapia were
compared to clinical chemistry values obtained from tilapia
raised in low-density tanks, there were notable differences
in protein, calcium and phosphorus concentrations. Protein
concentrations in tilapia raised in high-density systems
were slightly higher, while cal-cium and phosphorus levels
were much higher com-pared to fish in low-density
systems. Similar differ-ences in blood values were observed
in hybrid striped bass raised in high-density production
systems,13 although the differences in calcium and
phosphorus values were greater in these tilapia.The reason
for high-er calcium and phosphorus values is unknown, but
is
Page 11
 Tilapia Hematology and Plasma Chemistry Values
probably an effect of water quality or stocking density,
since the two groups of tilapia were from the same stock
source and were fed the same diets. Water hardness was
much higher in production fish tanks compared to the low-
density tanks, and may have influenced blood calcium
levels.Total protein, albumin, and globulin con-centrations
in fish from high-density, recirculating sys-tems may be
influenced by the characteristic high organic load and
bacterial count, which could have induced a generalized
immune response.
Calculation of reference intervals as ± 2 SD from the
mean is valid only when blood values follow a nor-mal
distribution. It is incorrect to assume that biological
parameters are distributed normally, therefore non-
parametric methods are more accurate for determining
reference intervals.14 Techniques to properly determine
reference intervals have been established by the NCCLS, 7
and suggestions for their use and interpreta-tion have been
discussed.15 Unfortunately, reference values are not used on
a routine basis in fish medicine, and the number of studies
in which reference intervals have been determined for fish
species is limited. The majority of blood values determined
for fishes have been reported as mean ± SD. As for
mammals, refer-ence intervals should be determined for
different pop-
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Page 12 Veterinary Clinical Pathology
ulations of fish within a single species, since culture
conditions and environmental variables can markedly affect
blood values.12,13,16,17 As demonstrated in our com-parison
of blood values from tilapia in high and low-density
systems, reference intervals developed in high-density
production tilapia are not applicable to fish raised under
different environmental and management conditions.
As the aquaculture industry expands, tools to mon-itor
the health status of fish using standardized non-lethal and
inexpensive methods will be needed. Evaluation of
hematologic and blood chemistry ana-lytes will enhance the
culture of fish by facilitating early detection of infectious
disease and identification of sub-lethal conditions affecting
production performance. This, in turn, will contribute to
more specific, timely and effective disease treatments in the
future. ◊
Acknowledgements
The authors thank Butch Kukanich for technical assistance, and
the staff and students of the Virginia Tech Aquaculture Center,
particularly Brian Brazil, for the culture and mainte-nance of the
tilapia used in this study. This project was fund-ed in part by the
Office of Research and Graduate Studies at the Virginia-Maryland
Regional College of Veterinary Medicine.
10. Hussein SY, El-Nasser MA, Ahmed SM. Comparative studies on
the effect of the herbicide atrazine on freshwater fish Oreochromis
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of Oreochromis mossambicus. J Fish Biol 1989;33:747-756.
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hematologic reference intervals between culture system and type
of hybrid striped bass. Am J Vet Res 1996;57:618-623.
13. Hrubec TC, Smith SA, Robertson JL, et al. Blood biochemical
reference intervals for sunshine bass (Morone chrysops Morone
saxatilis) in three culture systems. Am J Vet Res 1996; 57:624-627.
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used on the resulting estimate of normal range. Clin Chem
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comments. Vet Clin Pathol 1998;27:102-106.
16. Hrubec TC, Robertson JL, Smith SA. Effects of temperature on
hematologic and serum biochemical profiles of hybrid striped bass
(Morone chrysops X Morone saxatilis). Am J Vet Res 1997;58:126-
130.
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Vol. 29 / No. 1 / 2000