Transactions of the American Fisheries Society 128:352–361, 1999
q Copyright by the American Fisheries Society 1999
An Examination of Elemental Stability in the Fin Ray of the
White Sturgeon with Laser Ablation Sampling–
Inductively Coupled Plasma–Mass Spectrometry (LAS-ICP-MS)
GEOFFREY I. VEINOTT*1
AND
R. DOUGLAS EVANS
Watershed Ecosystems Graduate Program, Trent University,
Peterborough, Ontario K9J 7B8, Canada
Abstract.—Laser ablation sampling–inductively coupled plasma–mass spectrometry (LAS-ICPMS) was used to examine the elemental composition of the opaque growth zones in the leading
ray from the pectoral fin of 10 white sturgeon Acipenser transmontanus recaptured from the Columbia River. Changes in the elemental composition were detected within 2 years after their initial
capture, with significant correlations among the concentrations of Sr, Mg, Pb, Br, Zn, Ba, Sn, Mn,
and Na in the fin rays between the two capture periods. Concentrations of K suggested that fin
ray material had been resorbed between captures and that the entire fin ray may be available for
resorption. The cause of the changes in elemental composition of the fin rays was not determined.
For this reason the use of fin rays from white sturgeon as biomonitoring structures must account
for any resorption of the fin ray with time.
The white sturgeon Acipenser transmontanus is
North America’s largest freshwater fish. It is found
in the major river systems along the Pacific coast
from the Aleutian Islands of Alaska to Monterey,
California (Scott and Crossman 1973). Because of
a reduction in population size, sacrificing large
numbers of sturgeon for scientific research is no
longer acceptable. Yet, management decisions
concerning the white sturgeon are confounded by
the lack of information on the ecology, biology,
and physiology of these fish (McCabe et al. 1993;
Parsley et al. 1993).
The leading ray (a bony structure) in the pectoral
fin is a potential source of physiological and historical environmental data that does not require
sacrificing the fish. The fin ray grows incrementally and produces optically distinct zones of bone
material. Quite simply, one translucent and one
opaque zone is deposited in the fin ray each year
(Brennan and Cailliet 1989; Rien and Beamesderfer 1994). The fin ray can, therefore, be used to
estimate the age of the fish and the year in which
an annual increment was produced. Sturgeon older
than 50 years are common, and some estimates of
age have exceeded 100 years (Scott and Crossman
1973; Rien and Beamesderfer 1994). Furthermore,
fin rays have been collected and preserved for
more than 30 years (Semakula and Larkin 1968).
* Corresponding author: [email protected]
1 Present address: Department of Environmental Sciences, Academic Link, Lakeland College, 5707-47 Avenue West, Vermilion, Alberta T9X 1K5, Canada.
Received December 11, 1997
Accepted May 4, 1998
It is possible to remove nanogram quantities of
bone material from the fin ray with a laser for
analysis by inductively coupled plasma–mass
spectrometry (ICP-MS). Therefore, by analyzing
individual growth zones, it is possible to compile
a chemical history of the fin rays dating back to
the early 1900s.
What the chemical composition of an annual
growth zone represents is still uncertain, however.
Large-scale mobilization of bone material or resorption of the fin ray after initial deposition would
limit the usefulness of the fin ray as a biomonitoring structure. Fin development and regeneration
in other fishes suggest that fin rays originate from
cells within the dermis. Specialized cells form the
organic matrix, and the mineralized phase begins
as a poorly mineralized hydroxyapatite. Eventually the mineral phase dominates and the rays develop into ossified structures (Géraudie and Landis
1982; Landis and Géraudie 1990). Subsequent layers of bone are presumed to form on the surface
of the ray at the dermis–ray interface.
Studies on the processes regulating fin ray
growth and resorption in the white sturgeon have
not been reported. Observations from magnified
images of fin rays from white sturgeon suggest that
a similar model would explain the production of
annual growth zones in these fish. Canals are visible on the outer surface and in sections of the fin
ray as hollow areas extending outward from the
core (Figure 1). Material for bone growth would
be carried to the dermis–ray interface by these
canals in the bone. The entire fin ray is permeated
by a network of lacunae and canaliculi, charac-
352
STABILITY OF WHITE STURGEON FIN RAY
353
FIGURE 1.—Photomicrograph of a portion of a fin ray cross section showing the canals within the fin ray (C)
and examples of annual growth zones (A).
teristic of cellular bone (Figure 2). Osteocytes, osteoblasts, and osteoclasts presumably occupy these
lacunae, producing and possibly remodeling the
bone, thereby changing the fin ray’s original chemical composition. The purpose of this study was
to test the hypothesis that no change in the chemical composition of the fin rays occurred after the
fin ray was originally produced.
Methods
Fin rays used in this study were collected between 1991 and 1996 by the Oregon Department
of Fish and Wildlife as part of their continuing
study of the Columbia River white sturgeon. All
fish were from two Columbia River impoundments—McNary Reservoir (river kilometers 471–
536) and John Day Reservoir (river kilometers
346–471). Fin rays were removed according to the
procedures described by Rien and Beamesderfer
(1994). All individuals used in this study were
captured twice. On first capture each individual
was tagged and a portion of one pectoral fin (right
or left) was removed. On second capture a portion
of the fin ray from the opposite (right or left) pectoral fin was removed. The second capture oc-
curred 2 years later for seven of the sturgeon, 5
years later for two sturgeon, and 6 years later for
one sturgeon for a total of ten pairs of fin rays.
The elemental composition of each fin ray was then
determined by laser ablation sampling–inductively
coupled plasma–mass spectrometry (LAS-ICPMS).
To prepare fin rays for laser sampling and to
enhance the visual appearance of the opaque and
translucent zones, fin rays were sectioned and polished. Some fin rays received as thin sections
mounted on glass slides were removed from the
slides, cleaned, and polished only. Fin rays received as thick sections were processed as follows.
Sections of fin ray 500-mm thick were removed
with an Isomet low-speed saw with a wafering
diamond blade. The sections were lightly polished
by hand with 1,200-grit lapidary film until the
opaque and translucent bands were clearly visible
under a light microscope at 403 magnification.
Sectioned fin rays were given a final buffing with
10-mm lapidary film to enhance the appearance of
the opaque and translucent zones for photographic
work and for selecting ablation sites.
Magnified images of the polished fin ray sec-
354
VEINOTT AND EVANS
FIGURE 2.—Photomicrograph of a portion of a fin ray cross section showing examples of lacunae (L), canaliculi
(C), and laser ablation sites (A).
tions were then captured by a television camera
and displayed on a computer screen. The appearance of the opaque and translucent zones was enhanced with a digital enhancement program, and
black-and-white positive images of fin ray sections
from the same fish were printed and compared.
The patterns of opaque and translucent bands from
fin ray pairs were remarkably similar with respect
to the width of the zones. As well, in all but one
pair, the number of opaque bands produced on the
second fin ray corresponded to the known time at
TABLE 1.—Laser ablation sampling–inductively coupled
plasma–mass spectrometer (LAS-ICP-MS) operating conditions.
Conditions
Value
Laser
Laser energy (J)
Repetition rate (Hz)
Number of laser shots
Q-switch delay (ms)
ICP-MS
Forward power (kV)
Plasma gas (L/min)
Auxillary gas (L/min)
Nebulizer gas (L/min)
40–45
10
50
240–250
1,050
15.0
0.80
1.0
large after initial capture. Based on the printed
images of fin ray pairs and the number of opaque
bands visible, opaque zones believed to have been
produced in the same year on both fin rays were
selected for laser sampling. Three to five opaque
growth zones (annuli) were sampled in each fin
ray and 4–10 sites were sampled in each growth
zone.
Fin ray material was sampled with a PE (Perkin
Elmer) SCIEX laser sampler (model 320) operated
in the Q-switched mode with the laser beam wavelength set at 0.266 mm. The laser beam was focused onto the specimen through a microscope and
could be observed by way of a television monitor.
Specimens were held in a closed container, and
ablated material was transported to the ICP–mass
spectrometer (MS) by a flow of argon. The LASICP-MS was optimized daily to maximize the
count rates on 88Sr and 44Ca while maintaining an
ablation crater of approximately 50 mm in diameter. Laser and ICP-MS operating conditions are
given in Table 1.
Selection of isotopes for analysis was made
based on the expected composition of the bone
material. However, only 11 elements were consistently detected in the fin rays, and data are reported
STABILITY OF WHITE STURGEON FIN RAY
TABLE 2.—Results from the multifactor repeated measures ANOVA. An asterisk (*) indicates a significant effect due to time, individual (Ind), age, or year (P , 0.05).
Isotope
Effect
Sr
Mg
Pb
Time
Ind
Age
Year
*
*
*
*
*
*
*
*
*
*
*
*
Br
*
Zn
Ba
*
*
*
*
*
*
*
*
Sn
Mn
K
Na
*
*
*
*
*
*
*
*
*
*
*
for one isotope ( 23Na, 24Mg, 39K, 44Ca, 55Mn,
64 Zn, 79 Br, 88 Sr, 120 Sn, 138 Ba, and 208 Pb) on each
of these elements.
Isotopic data acquired on a SCIEX Elan model
5000 ICP-MS were provided in the form of counts
per second for each isotope. To account for varying
ablation yields between ablation sites, the ratio of
the isotope counts to 44Ca counts was calculated
(Arrowsmith 1987; Jackson et al. 1992). To monitor daily instrument drift, a pressed pellet produced from National Institute of Standards and
Technology (NIST) standard bone meal reference
material (SRM; number 1486) was ablated at five
different sites at the start and end of each day of
analyses and immediately after any change in operating conditions. Isotope: 44Ca ratios were calculated daily and changes in isotopic ratios were
compared by t-tests. To further minimize the possible effect of daily instrument drift, fin rays were
analyzed in pairs. Each pair of fin rays represented
the right and left fin sections collected from each
sturgeon upon capture and subsequent recapture.
Generally, time between the start and finish of ablation of a pair of fin rays was less than 2 h. The
order in which each fin ray of the pair was analyzed
was randomized.
Fin rays were ablated on four different days during a 3-week period in 1996. To monitor daily
variability in concentration, a fin ray was selected
as an in-house standard, which was ablated at a
minimum of eight different sites each day. Concentrations in the in-house standard were calculated by the method discussed below, and mean
daily isotopic concentrations were compared by a
one-way analysis of variance (ANOVA).
The ICP-MS was operated in the peak hop mode
with the number of replicates set at 50 and a dwell
time of 20 ms for a total counting time of 1 s on
each isotope. Because of the appearance of apparently random outliers in LAS-ICP-MS data
(Evans et al. 1994; Outridge et al. 1996), all data
were subjected to a variation of the Grubbs test
355
for extreme outliers (Taylor 1990). Mean count
rates and SDs were calculated for each mass (N 5
50) on every ablation site, and outliers were defined as individual count rates that were greater
than 3 SDs above the mean. Data points deemed
outliers were assigned the count rate of the data
point immediately preceding them. Backgrounds
were calculated from the first two and last ten (before any ablation product reaching the plasma and
after signals returned to pre-ablation levels) replicates. Outlier- and background-corrected data
were converted to concentrations by using the
equation of Arrowsmith (1987):
I(E)
R(E)
·C(IS) 5 C(E)·
;
I(IS)
R(IS)
5
5
5
5
counts for the element of interest;
counts for the internal standard;
concentration of the internal standard;
concentration of the element of interest;
R(E) 5 element response factor for the element
of interest; and
R(IS) 5 element response factor for the internal
standard.
I(E)
I(IS)
C(IS)
C(E)
We used 44Ca, a matrix element, as the internal
standard. The mean total Ca concentration in a
sample of fin rays was determined by atomic absorption spectrometry and set at 26% by weight.
The R(E)/R(IS) or ‘‘relative sensitivity factors’’
(RSFs) were determined for the isotopes of interest
based on laser analyses of the NIST 1486 bone
meal pellet. Concentrations are reported for seven
isotopes ( 88Sr, 24Mg, 208Pb, 64Zn, 55Mn, 39K, 23Na)
as mg/kg. However, concentrations in the SRM are
not certified for 79Br, 138Ba, or 120Sn; therefore,
values for these isotopes were reported as concentrations relative to the standard and will be refereed to as ‘‘delta’’ values. Further, plots of each
isotope were examined for correlations with
opaque growth zone width. A strong correlation
observed between 24Mg concentrations and the
width of an opaque zone led to correction for the
width of the opaque zone by normalizing concentrations to the median opaque zone width. Also,
because all isotopes were expected to be in proportion to the relative abundance of the natural
isotopes, the mass superscript will not be used in
further discussions.
To determine if mean isotopic concentrations of
individual annuli differed between capture periods, a repeated-measures multifactor ANOVA was
conducted on each isotope with individual, the
356
VEINOTT AND EVANS
FIGURE 3.—Relationship between isotopic concentrations in the annual growth zones of the fin rays from the
first and second captures. Straight line has a slope of one. Concentrations are in parts per million (mg/kg) except
Br, Ba, and Sn, which are ‘‘delta’’ values; Mg values have been corrected for the width of the annual band.
year the opaque growth zone was produced (year),
and the age of an individual at the time the opaque
growth zone was produced (age) as the independent variables and the isotopic concentrations as
the dependent variables. Main factor effects only
were tested. A correlation analysis was also performed with the mean isotopic concentrations from
each growth zone to determine if a statistically
significant relationship existed between the isotopic concentrations from the two captures.
Results
Isotopic ratios determined on the in-house standard varied significantly (ANOVA, P , 0.05)
STABILITY OF WHITE STURGEON FIN RAY
357
FIGURE 3.—Continued.
from the start to finish of a day. The change in
isotopic ratios, however, was less than 2% per
hour, so error due to instrument drift was considered minimal by virtue of the sampling protocol (see Methods). Mean isotopic concentrations in the in-house standard (with the exception
of Mn) did not vary significantly among days
(ANOVA, P . 0.05). Therefore, no further efforts
were made to correct for the sequence in which
TABLE 3.—Results from the Pearson product-moment
correlation test comparing elemental concentrations in the
fin rays from the first and second captures.
Element
r
P
Sr
Mg
Pb
Br
Zn
Ba
Sn
Mn
K
Na
0.95
0.88
0.31
0.83
0.55
0.89
0.80
0.90
20.05
0.76
,0.001
,0.001
0.049
,0.001
,0.001
,0.001
,0.001
,0.001
0.769
,0.001
specimens were analyzed. Having minimized the
random errors, the multifactor ANOVA analyzed
the sources of variation of interest to this study.
All four factors (time, individual, age, and year)
were significant for Sr, Mg, Pb, Zn, Ba, and K.
Individual, age, and year were significant for Mn
and Na. Only individual was significant for Br
and Sn (Table 2).
Plots of mean isotopic concentrations in each
growth zone from the two capture periods confirmed the findings of the ANOVA (Figure 3).
Points falling below the 1–1 line in Figure 3 indicated a decrease in concentration between captures. For the isotopes with significant differences
between captures (Sr, Mg, Pb, Zn, Ba, and K), all
but Mg had more values below the 1–1 line than
above.
With the exception of K, the isotopic concentrations from the two capture periods were strongly
correlated (Table 3), suggesting that concentrations varied in a predictable manner. The K concentrations exhibited three distinct patterns within
individual fin rays: (1) a divergence of the values
358
VEINOTT AND EVANS
FIGURE 4.—Relationship between the year an annulus was produced and the K concentration in that annulus.
Each pane represents one sturgeon from this study. Circles represent data from fin rays removed during first capture,
squares represent fin ray data from the second capture. Bars indicate SE; error bars smaller than the symbol are
not shown.
between the two capture periods (Figure 4A–C);
(2) a systematic shift in concentration between
captures (Figure 4D–H); and (3) little or no change
between captures (Figure 4I, J). Within the first
two groups the direction of change in K concentrations between captures was not consistent. In
two cases (Figure 4A, D) the K concentration in
the fin rays increased between captures, but in all
STABILITY OF WHITE STURGEON FIN RAY
the other cases the K concentration in the fin rays
decreased between captures.
Discussion
Elemental analysis of bone structures such as
fin rays is different from that of otoliths because
the potential exists for resorption and mobilization
of bone after initial deposition. Despite this limitation, bone material also has many advantages.
Bone should readily incorporate trace amounts of
Pb, Sr, and Na into its crystal lattice (Vaughan
1981). Other elements may adsorb to the crystal
surface (K) or associate with the organic components of the bone (Eanes and Posner 1970). Further, bone is precipitated from materials dissolved
in the blood (Posner 1978), the elemental composition of which can be affected by the water
chemistry, diet, and a variety of stresses (Dwyer
et al. 1988; Zaprudnova 1991; Martem’yanov
1995; Roche and Bogé 1996; Wood et al. 1996).
The chemical composition of the fin rays may,
therefore, record long-term trends in environmental pollutants such as Pb or Cd, short-term exposure to high levels of toxins, a change in diet,
disease, seasonal movements, or marine migrations (Coutant 1990). Linking the chemical composition of the fin rays to such factors would provide researchers who are interested in the sturgeon’s past environmental conditions or changes
in their physiology or health with a nonlethal technique of obtaining that information. Unfortunately,
our data suggest that for some elements the composition of the fin ray is not always stable.
The greatest change in the elemental composition of the fin rays occurred with K (Figure 3).
Potassium cannot be accommodated by the crystal
lattice of the bone and either adsorbs to the surface
of the bone crystals or is found in the bone cells
(Eanes and Posner 1970). Intracellular K concentrations are generally much higher than extracellular or plasma levels (Kem and Trachewsky
1983). Therefore, areas actively involved in bone
production and resorption would contain bone
cells rich in K. Our results suggest that the amount
of bone that recently contained living cells is large
and extends well away from the dermis–bone interface. The lacunae and canaliculi in the fin rays
comprise approximately 10% of the surface area
in a fin ray section (Figure 2). Approximately 10%
of the ablation product from a recently active
growth or resorption zone would, therefore, consist of K-enriched material. The change in K between captures suggests that areas of bone can
become dormant (loss of K) or become active after
359
a period of dormancy (increase in K; Figure 4).
However, this interpretation assumes that the Kenriched cellular fluid remains trapped within the
bone and does not difuse away from the lacunae
after cell death; this assumption needs to be tested.
Changes in elemental concentration in the fin
rays might also have been caused by the removal
of the fin ray after initial capture. Bone material
has been shown to be resorbed in other fish during
scale regeneration (Weiss and Watabe 1978). The
stress of capture, or the repairing of the damaged
fin ray, might have resulted in the resorption of
fin ray material, in which case, further changes in
the elemental composition of the fin rays may not
occur. Furthermore, it seems unlikely that a continued loss or gain of elements at the rates observed here could be maintained for very long; Sr
would lose half its value after approximately 20
years and Mg would increase at about the same
rate. Yet, white sturgeon more than 100 years old
have had Sr and Mg concentrations comparable to
the fish in this study (Veinott and Evans, unpublished data). If it can be shown that further change
in the fin ray elemental composition will not occur
or that the strong correlations between captures
(Table 3) hold for longer periods at large, then
corrections could be made for the observed
changes, and past elemental concentrations could
be estimated.
The implications for the use of white sturgeon
fin rays as biomonitoring structures are twofold.
First, if the change in elemental concentration of
the fin ray is a result of the stress of capture or
the removal of the fin ray and a correction for the
initial change in concentration can be made, then
a historical record of the elements measured in this
study could be obtained from the fin ray. The information in the fin ray may then be used for addressing environmental or physiological change.
However, if the complete fin ray is available for
resorption, the use of the fin ray as a biomonitoring
structure would be severly limited.
Even if accurate historical records of the elements within the fin ray can be obtained, it is still
unclear at this time exactly what the concentration
values represent. Studies are needed on individuals
with known exposure histories to determine how
the concentrations of the various elements in the
fin rays are affected by environmental and physiological conditions. Work in this direction has
been reported for otoliths of Atlantic croaker Micropogonias undulatus (Fowler et al. 1995), but
little is known about the chemical changes within
360
VEINOTT AND EVANS
and between fin ray growth zones in freshwater
fishes.
Conclusion
The LAS-ICP-MS was used to examine the
chemical composition of the opaque growth zones
in the leading ray from the pectoral fin of the white
sturgeon. Fin rays from recaptured fish were analyzed, and the change in composition of the fin
rays with time was evaluated. In general the fin
rays lost ions during the time between captures.
However, there was a strong linear relationship
between fin ray concentrations from the two capture periods. Therefore, concentrations from the
first capture could have been predicted from the
second capture. The exception was K: examination
of K concentrations in individuals suggested that
the entire fin ray may be available for resorption.
The usefulness of white sturgeon fin rays as biomonitoring structures depends on the cause of the
change in the elemental composition of the fin ray
and whether corrections can be made to compensate for the observed changes.
Acknowledgments
We thank the Natural Sciences and Engineering
Research Council of Canada for support of G.I.V.
in the form of a doctoral fellowship and for continuing support of research by R.D.E. Thanks are
extended to Thomas Rien at the Oregon Department of Fish and Wildlife for providing the fin
rays and to Perkin-Elmer Canada for kindly donating the LA-320 laser sampler.
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