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Abstract

Fish caught from piers are an important part of the recreational fishery and are not routinely monitored for phycotoxins. Species taken in this catch are often different from those obtained in the commercial catch further offshore, and diets of pier-caught fish may differ from those of offshore species, resulting in different toxin exposure. Here we report preliminary results from a study on diatom toxins in the recreational fish catch, using data collected from 4 July 2001 to 15 December 2001 at the Santa Cruz Municipal Wharf, a heavily fished coastal pier in California. A variety of frequently caught fish species were taken by hook-and-line from the Santa Cruz Wharf and tested for the diatom toxin domoic acid (DA). Fish viscera and muscle tissue were analyzed separately using High Performance Liquid Chromatography methods. DA was detected in fish viscera but not in fish muscle tissue. DA in fish viscera coincided with the appearance of elevated cell counts of species of the DA-producing diatom, Pseudo-nitzschia australis, and with DA in the water column. DA was detected almost exclusively in white croaker, Genyonemus lineatus, and to a lesser extent in staghorn sculpin, Leptocottus armatus. Although the DA levels in these two fish species were comparatively low (<3 μ μ μ μ μg/g tissue), the bloom of toxic species was comparatively modest at the time. Given the much higher toxin levels encountered in the region at other times, it is likely that these two species could achieve much larger toxin loads during the more intensive blooms of toxic Pseudo-nitzschia that occur most years in Monterey Bay. The relationship between toxin levels in the water column and in fish tissue is discussed, as well as the relationship between food habits and the accumulation of domoic acid in white croaker.
CALIFORNIA FISH AND GAME
California Fish and Game 91(3):179-192 2005
179
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY
SPENCER E. FIRE1
Ocean Sciences Department
University of California at Santa Cruz
Santa Cruz, CA 95064
E-mail: sfire@ucsc.edu
MARY W. SILVER
Institute of Marine Sciences
University of California at Santa Cruz
Santa Cruz, CA 95064
ABSTRACT
Fish caught from piers are an important part of the recreational fishery
and are not routinely monitored for phycotoxins. Species taken in this
catch are often different from those obtained in the commercial catch
further offshore, and diets of pier-caught fish may differ from those of
offshore species, resulting in different toxin exposure. Here we report
preliminary results from a study on diatom toxins in the recreational fish
catch, using data collected from 4 July 2001 to 15 December 2001 at the
Santa Cruz Municipal Wharf, a heavily fished coastal pier in California. A
variety of frequently caught fish species were taken by hook-and-line from
the Santa Cruz Wharf and tested for the diatom toxin domoic acid (DA). Fish
viscera and muscle tissue were analyzed separately using High
Performance Liquid Chromatography methods. DA was detected in fish
viscera but not in fish muscle tissue. DA in fish viscera coincided with the
appearance of elevated cell counts of species of the DA-producing diatom,
Pseudo-nitzschia australis, and with DA in the water column. DA was
detected almost exclusively in white croaker, Genyonemus lineatus, and
to a lesser extent in staghorn sculpin, Leptocottus armatus. Although the
DA levels in these two fish species were comparatively low (<3 μμ
μμ
μg/g
tissue), the bloom of toxic species was comparatively modest at the time.
Given the much higher toxin levels encountered in the region at other times,
it is likely that these two species could achieve much larger toxin loads
during the more intensive blooms of toxic Pseudo-nitzschia that occur
most years in Monterey Bay. The relationship between toxin levels in the
water column and in fish tissue is discussed, as well as the relationship
between food habits and the accumulation of domoic acid in white croaker.
INTRODUCTION
The occurrence of harmful algal blooms (HABs) in the coastal marine environment
has been shown to pose a serious threat to marine organisms, fisheries, and public
1Current Address: Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL
34236.
CALIFORNIA FISH AND GAME
180
health. Of particular concern in California’s Monterey Bay are HABs caused by diatoms
of the genus Pseudo-nitzschia. Some species of Pseudo-nitzschia in the Bay can
produce the potent neurotoxin domoic acid (DA). DA is harmful to a variety of marine
organisms as well as humans and is the causative agent of amnesic shellfish poisoning
(ASP) in humans. DA poisoning has no known antidote and its symptoms include
vomiting, seizures, disorientation, and death (Truelove and Iverson 1994). ASP was
first documented in Canada in 1987 when 3 people died and over 100 others suffered
adverse, short-term neurological effects after eating cultured blue mussels, Mytilus
edulis, contaminated with DA produced by Pseudo-nitzschia (Perl et al. 1990). This
incident led to the current regulatory limit of 20 μg/g DA in seafood, the level at or above
which the flesh is considered unsafe for human consumption by the Food and Drug
Administration (FDA). In 1991, DA from a toxic bloom of Pseudo-nitzschia was
responsible for the deaths of over a 100 seabirds in Monterey Bay (Work et al. 1993).
In 1998, 70 California sea lions, Zalophus californianus, exhibited characteristic
symptoms, with more than half of these later dying as a result of DA poisoning (Lefebvre
et al. 1999). DA has also been detected in commercially important marine organisms
and has been the cause of several fishery closures in California due to contamination
of seafood products (G. Langlois, California Department of Health Services, personal
communication).
To protect the fishing industry and consumers of the catch, DA monitoring has
focused understandably on commercial species. Now that DA has been identified as
a public health risk, species such as anchovy, Engraulis mordax, and sardine,
Sardinops caeruleus, are sometimes monitored for toxins in California, especially
during blooms of Pseudo-nitzschia (G. Langlois, personal communication). However,
little is known about the effects of DA on fish taken in the recreational or subsistence
fisheries and on the associated public health hazards. Fish caught from piers are an
important part of recreational and subsistence fisheries and are mostly unmonitored
for phycotoxins.
Relatively little is known about the pier fishing community. Fishing from a public
pier or wharf requires no permit or license in California, and thus can not be readily
tracked by the usual method used to quantify recreational fishers (i.e. the licensing
process). Those who fish from piers and other “man-made structures”, however,
represent about 11% of the total marine recreational fishers in California (estimate from
RecFIN data)2. The absolute numbers of marine recreational fishers in the state is
unknown, but their catch is often considered to be highly significant, both relative to
commercial operations and because of their economic impact on regional communities
(Coleman et al. 2004). Species taken in a pier fishery are often different from those
targeted in the offshore recreational catch and in the commercial fishery, and species
in the pier catch frequently may be species of lower value, as suggested by market price
when those same species are commercially available in markets (RecFIN2, Starr et al.
2RecFIN (Recreational Fisheries Information Network). Pacific States Marine Recreational
Fisheries Monitoring Database (data on recreational fish catches in California are available
up to December, 2003). <http://www.psmfc.org/recfin/>
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 181
2002). Thus species in the pier catch have not been the focus of much attention.
Additionally, the diets of nearshore fish may lead to toxin exposure that is different from
that of species taken offshore, because of differences in prey availability in the
nearshore subtidal zone as compared with prey availability offshore. The fishing
community that uses piers also may have consumption patterns different from other
recreational fishers. For example, the majority of pier fishers in California are represented
by a variety of ethnic groups who consume up to 90% of their catch and thus are
subsistence fishers; in fact, those of Asian and Latino descent consume three times
the recommended amount of fish (PEHAB 2003)3. Furthermore, among certain ethnic
groups of pier fishers, it is a common practice to consume the whole fish, including
viscera. This practice may further increase the possibility of DA exposure, since the
toxin tends to be concentrated mostly in viscera (Lefebvre et al. 2002).
Routes by which algal toxins move through marine food webs are still relatively
poorly understood. Planktivorous fish such as sardine and anchovy, probably the best
known DA vectors, can feed directly on planktonic diatoms and tend to be contaminated
with DA only during Pseudo-nitzschia blooms, as expected of a water soluble toxin
(Lefebvre et al. 2002). These planktivorous fish have sufficiently fine gill rakers to
directly filter toxic Pseudo-nitzschia from the water and thus can contain very high
levels in their viscera during toxic Pseudo-nitzschia blooms: values greater than 1800
μg/g have been detected in anchovy in Monterey Bay (Lefebvre et al. 2002). Nearshore,
shallow-water fish such as those caught from piers can utilize a wide variety of prey,
not only pelagic but also benthic species. Such prey, for example, could include
invertebrates such as mussels, clams, and sand crabs, which can directly filter out toxic
plankton and have been shown to have detectable DA loads (Perl et al. 1990, Wekell
et al. 1994, Ferdin et al. 2002). Additional fish prey may include invertebrate detritivores
and deposit-feeders like polychaete worms, which would become contaminated with
DA when they consume DA-rich flocculate matter that settles from surface Pseudo-
nitzschia blooms to depth (Buck and Chavez 1994). Additionally some benthic fish may
directly consume contaminated pelagic detritus when it reaches the sea floor. If routes
exist for DA to enter the food webs of fish caught in pier-based fisheries, then pier
fishers may also be at risk.
As researchers attempt to better understand HAB effects, it has become
necessary to study how DA moves through the food web from diatoms to higher trophic
level organisms. This study will examine the potential exposure to DA of pier fishers
and whether consumption of pier-caught fish poses a public health threat. The
objective of this study was to determine whether DA toxins are present in the catch of
fishes taken recreationally from piers in Monterey Bay and to ascertain the relative roles
of different trophic pathways by which DA may transit in shallow marine food webs.
The Santa Cruz wharf was selected as a study site because it is the second most heavily
fished ocean pier in California (RecFIN2, data for 2001-2003) and it was the only
California pier where water samples were routinely obtained for quantitative
3PEHAB (Public and Environmental Health Advisory Board). Consumption of Contaminated
Fish. Sept. 2003. <http://www.cchealth.org/prevention/coalitions/pehab/fishReport.pdf>.
CALIFORNIA FISH AND GAME
182
measurements of toxic algal abundance and DA water concentrations during the study
period (see below). For this study, data were collected during summer and fall months,
a time at which DA blooms commonly occur in central California (Kudela et al.,
submitted). Samples of fish and water were taken from this site over a 6-month period
and analyzed for the presence of DA using High Performance Liquid Chromatography
(HPLC-UV).
METHODS
Sample Collection
A sample set of fish was obtained from California’s Monterey Bay at the Santa
Cruz municipal wharf from 4 July 2001 to 15 December 2001, a period that included a
relatively modest toxic Pseudo-nitzschia australis event. Fish were sampled 1-2 times
per week during the study interval, yielding 1-10 individuals per sampling event. All
fish were caught from 0600 hours to 1000 hours using common hook and line methods,
the typical local fishing technique. Specimens were pooled for analysis from the
seaward end (8-10 m water depth) and the middle of the pier (3-5 m water depth), places
where local fishers typically position themselves. Upon capture, the standard length
(SL) of each specimen was taken and each fish was identified to species level. The fish
were then immediately stored in ice until transferred to a -20 ºC freezer where they were
stored until dissected.
In order to determine the local availability of DA sources for fish during the
study interval, water samples were also collected during the July 2001 to 15 December
2001 period. Sea water (SW) samples were taken on a weekly basis from the Santa Cruz
wharf for DA analysis by HPLC. SW samples were collected from the surface at the
seaward end of the pier using a bucket. Sample water was filtered after collection
through a glass fiber filter (Gelmon GF/F) using low vacuum pressure. Five hundred
ml of water was filtered from each sample, and was kept frozen at -20 ºC until extraction
for DA. Counts of the toxic cells were also obtained from the same water samples, as
described in Lefebvre et al. (2002).
Preparation Of Viscera And Muscle Tissue Extracts
DA from viscera and muscle tissue samples was extracted following procedures
described in Lefebvre et al. (1999) and Hatfield et al. (1994). DA was analyzed from whole
viscera (including all organs in the intracoelomic cavity) for all fish taken. DA was
analyzed in muscle tissue only in specimens in which visceral DA was detected.
Samples were prepared and analyzed within 3 weeks. In order to minimize post-mortem
leakage of DA from the digestive tract, fish were kept frozen until processed and whole
viscera were removed from fish without thawing. Muscle tissue samples were taken
from the posterior dorsal side of the fish near the tail to avoid regions where DA may
have diffused from the digestive tract (Lefebvre et al. 2001). Aliquots taken from the
same species of fish on the same day were pooled before extraction. Whole viscera were
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 183
removed from fish and homogenized with mortar and pestle. A 4-g subsample of the
homogenate was added to 16 ml of 50% methanol and homogenized for 2 minutes at
highest setting with homogenizer probe. The homogenate was then sonicated for 2
minutes in a sonicator bath, followed by centrifugation for 20 minutes at 4000 × g. The
supernatant was then vacuum-filtered through a 1.0 μm polycarbonate filter, in
preparation for solid-phase extraction.
Solid-Phase Extraction of Viscera And Muscle Tissue
Solid-phase extraction was performed on all samples using JT Baker strong
anion exchange (SAX) cartridges. SAX columns were first conditioned with 6 ml of
Nanopure water, 3 ml of 100% MeOH, and 3 ml of 50% MeOH. Two ml of sample filtrate
was passed through the column, followed by 5 ml of wash solution (1:9 MeCN:H2O).
DA in the column was eluted with 5 ml of eluting solution (0.5M NaCl in 10% MeCN),
then analyzed by HPLC. Efficiency of extraction was 83.6 ± 5.7% (n = 3) for whole viscera
and 78.2 ± 11.3% for muscle tissue. Method detection limits were 1.5 ppm for viscera
and 1.6 ppm for muscle tissue.
Water Sample Preparation
DA was extracted and derivatized from water samples using procedures outlined
in Wright and Quilliam (1995). Filters were homogenized in 10% methanol and ground
using a Teflon pestle at 250 rpm, followed by sonication for 3 minutes. Samples were
then centrifuged for 1 minute at 4000 rpm and supernatant was filtered through a 0.22
μm filter.
Two hundred μl of filtered sample extract was added to 50 μl of borate buffer, 10 μl
of dihydrokainic acid (DHK) internal standard, and 250 μl of 9-Fluorenylmethoxy-
chloroformate (FMOC-Cl) reagent solution, then vortexed for 45 seconds. The sample
was then washed three times with 500 μl of ethyl acetate to remove excess FMOC-Cl.
Derivatized samples were run on HPLC for DA analysis.
High-Performance Liquid Chromatography
DA from samples of whole viscera and muscle tissue was measured using a
Hewlett-Packard 1090 HPLC instrument. The HPLC was equipped with a diode array
detector set at 242 nm with a bandwidth of 10 nanometers (nm). Analysis was done
using an isocratic elution profile. A reference signal was set at 450 nm with a bandwidth
of 10 nm. The HPLC was equipped with a Vydac reverse-phase C18 column (catalog
#201TP52, 21 × 25 mm; Separations Group, Hesperia, Calif.) and a Vydac guard column
(particle size 5 μm). The mobile phase used was 90% H2O, 10% MeCN, 0.1% TFA and
was run at a flow rate of 0.3 ml/min. Prior to analysis, the solvent was degassed with
helium for 10 minutes. All injections were 20 μl each. Samples had a 15-minute run time.
Using DACS-1C domoic acid standard, a calibration curve was generated using
standards of 0.15, 0.3, 0.5, 1.0, 2.0, 4.0, 8.0, and 16.0 ppm (r = 0.99). The lowest detectable
CALIFORNIA FISH AND GAME
184
standard was 0.15 ppm. The instrument limit of detection (the concentration
corresponding to three times the SD of the signal from the lowest detectable standard)
was 0.1 ppm. Spike and recovery experiments using DA standards yielded 83 ± 4.7%
and 78 ± 11.3% efficiency for viscera and muscle tissue samples, respectively.
SW samples were analyzed for DA using a Hewlett-Packard 1090 HPLC, equipped
with a Hewlett-Packard 1046A programmable fluorescence detector (FLD). The FLD
was set at 264 nm excitation and 313 nm emission with a photomultiplier gain of 13. The
analysis was done using an isocratic elution profile. The HPLC was equipped with a
Vydac reverse-phase C18 column and a Vydac guard column (particle size 5 μm). The
mobile phase used was 60% H2O, 40% MeCN, 0.1% TFA and was run at a flow rate of
0.2 ml/min. Prior to analysis, the solvent was degassed with helium for 10 minutes. All
injections were 5 μl each. Samples had a 30-minute run time. FMOC-Cl was used as
a fluorescent tag for DA analysis of all water samples.
Using DACS-1C domoic acid standard, a calibration curve was generated using
standards of 5, 10, 25, 50, 100, and 250 nanograms (ng)/ml (r = 0.99). The lowest
detectable standard was 5 ng/ml. The instrument limit of detection was 1.4 ng/ml. Spike
and recovery experiments using DA standards yielded 84 ± 7% efficiency.
Chemical Reagents
Reagents used for calibration standards and spike/recovery calculations included
DACS-1C certified DA standard (National Research Council of Canada, Institute for
Marine Biosciences, 1411 Oxford Street, Halifax, NS, Canada), and Sigma DA reagent
(90% pure). Standards were stored under refrigeration in the dark. Optima grade
methanol, acetonitrile, ethyl acetate, analytical grade NaCl, and trifluoroacetic acid were
obtained from Fisher Scientific (Pittsburgh, PA). DHK was used as an internal standard
and FMOC-Cl was used as a fluorescing reagent for detection of amino acids (Aldrich
Chemical Co. Milwaukee, WI). Milli-Q water was used in preparation of solutions.
RESULTS
The sample set consisted of 115 specimens, representing 12 different species
of fish. The most abundant species caught was white croaker, Genyonemus lineatus,
accounting for 23% of the total catch during the sampling period (Table 1). Also
abundant were juvenile and adult shiner surfperch, Cymatogaster aggregata (22%),
juvenile bocaccio, Sebastes paucispinis (21%), and juvenile and adult staghorn
sculpin, Leptocottus armatus (14%). These fish were common in the catch of most
fishers at the wharf at the time. Toward the end of the sampling period, the catch
consisted mainly of white croaker and staghorn sculpin.
HPLC analysis of whole viscera detected DA contamination in white croaker on four
separate catch dates and in staghorn sculpin on one date (Table 2). DA levels in white
croaker ranged from 2.0 to 2.8 μg/g tissue. The DA level detected in staghorn sculpin
was 2.1 μg/g. DA was not detected in the muscle tissue of either fish. All other species
of fish in the sample set showed no detectable amounts of DA (Table 2). (While the
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 185
Table 1. Frequency of occurrence of fish captured at Santa Cruz Pier (n = 120), 4 July to
15 December 2001.
% of sample set
White croaker, Genyonemus lineatus 23
Shiner surfperch, Cymatogaster aggregata 22
Bocaccio, Sebastes paucispinis 21
Staghorn sculpin, Leptocottus armatus 14
Pacific sardine, Sardinops caeruleus 11
Walleye surfperch, Hyperprosopon argenteum 5
Striped surfperch, Embiotoca lateralis < 1
Silver surfperch, Hyperprosopon ellipticum < 1
Pile perch, Rhacochilus vacca < 1
Pacific mackerel, Scomber japonicus < 1
Jacksmelt, Atherinopsis californiensis < 1
Black perch, Embiotoca jacksoni < 1
Table 2. Distribution of DA detected in fish muscle tissue and viscera
Viscera DA Muscle DA
Date Species nSL (cm) (μg/g) (μg/g)
Pre- 7/4/2001 white croaker 1 14.0 0
Bloom 7/4/2001 bocaccio 1 12.0 0
7/4/2001 black perch 1 14.5 0
7/13/2001 bocaccio 2 10.0-12.0 0
7/13/2001 walleye surfperch 4 12.0-13.0 0
7/21/2001 staghorn sculpin 1 16.5 0
7/21/2001 shiner surfperch 4 8.0-8.5 0
7/21/2001 pile perch 1 17.5 0
8/3/2001 pacific sardine 5 18.0-19.0 0
8/10/2001 bocaccio 1 14.5 0
8/11/2001 pacific sardine 3 19.0-21.0 0
8/11/2001 jacksmelt 1 17.0 0
8/18/2001 pacific sardine 5 18.0-23.0 0
8/18/2001 pacific mackerel 1 24.0 0
8/21/2001 white croaker 2 11.0-17.0 2.4 0
8/25/2001 shiner surfperch 4 9.0-12.0 0
8/25/2001 walleye surfperch 1 17.5 0
8/25/2001 striped surfperch 1 14.0 0
8/31/2001 shiner surfperch 6 9.0-9.5 0
9/10/2001 white croaker 2 11.0-16.0 0
9/10/2001 bocaccio 8 10.0-13.0 0
9/13/2001 shiner surfperch 6 9.0-10.5 0
9/19/2001 shiner surfperch 4 10.0-11.0 0
CALIFORNIA FISH AND GAME
186
HPLC method used in this study is not as sensitive as other methods used to detect
DA, it can be used to reliably detect tissue burdens $$
$$
$1.5 μg/g, well below the regulatory
limit for human consumption. What is not known at present is the effects of chronic
low level exposures to DA).
The collection period coincided with a toxic algal, Pseudo-nitzschia australis,
bloom in Monterey Bay. Cell counts for this bloom reached 1.6 × 104 cells/L at the Santa
Cruz wharf. DA was detected in SW samples during this period reaching concentrations
of 339 ng/l at the Santa Cruz wharf.
DISCUSSION
The contamination of pelagic food webs by DA has been well-established in
Monterey Bay. The northern anchovy appears to be a particularly important vector
of the toxin (Lefebvre et al. 2002). In May 1998, a large-scale California sea lion stranding
9/19/2001 bocaccio 5 9.0-10.0 0
9/24/2001 staghorn sculpin 4 13.5-14 0
9/28/2001 staghorn sculpin 1 12.0 0
10/2/2001 white croaker 2 13.0-20.0 0
During 10/10/2001 white croaker 6 12.0-16.0 2.8 0
Bloom 10/17/2001 shiner surfperch 2 10.0-11.0 0
10/17/2001 bocaccio 5 10.0-11.0 0
10/17/2001 walleye surfperch 1 16.0 0
10/23/2001 staghorn sculpin 1 12.0 0
10/23/2001 silver surfperch 1 15.0 0
10/26/2001 white croaker 1 6.0 0
10/26/2001 staghorn sculpin 1 16.0 0
Post- 10/29/2001 white croaker 3 12.0-16.0 2.4 0
Bloom 10/29/2001 staghorn sculpin 3 11.0-14.0 0
11/2/2001 white croaker 3 10.0-16.5 2 0
11/2/2001 staghorn sculpin 1 12.5 2.1 0
11/2/2001 bocaccio 3 10.5-11.0 0
11/9/2001 staghorn sculpin 1 13.0 0
11/13/2001 white croaker 2 16.0-18.0 0
11/17/2001 white croaker 2 17.0 0
11/17/2001 staghorn sculpin 2 15.0 0
11/21/2001 white croaker 1 15.0 0
11/21/2001 staghorn sculpin 2 12.0-15.0 0
12/4/2001 white croaker 1 18.0 0
12/15/2001 white croaker 1 15.0 0
Viscera DA Muscle DA
Date Species nSL (cm) (μg/g) (μg/g)
Table 2 (continued)
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 187
event along the central California coast resulted in the deaths of 47 animals and
coincided with a toxic bloom of P. australis in the region (Gulland 19994, Scholin et al.
2000). DA was later identified as the probable causative agent in this event (Lefebvre
et al. 1999), vectored by the anchovies. During the course of this study, 16 sea lions
were found stranded along the central California coast (two of these in Santa Cruz
County), and these were confirmed to be contaminated with DA (F. Gulland, Director
of Veterinary Science, The Marine Mammal Center, personal communication).
Commercially-caught sardines landed in the bay during this period and analyzed by the
California Department of Health Services, contained DA at concentrations reaching 51
μg/g (Langlois 2002)5. However, most of the fish taken in this pier study were not
pelagic, but benthic-feeding fish. Much less is known about the DA contamination of
benthic food webs than of pelagic food webs and thus about the potential risk to the
human population of consuming bottom fish.
The DA detected in white croaker (2.0-2.8 μg/g) and in staghorn sculpin (2.1 μg/g)
was well below the FDA regulatory limit of 20 μg/g. However, DA levels detected in
Santa Cruz water during the associated Pseudo-nitzschia event were modest in
comparison to levels detected in the region during typical blooms (e.g., Walz et al. 1994,
Scholin et al. 2000). Since the event that occurred during this study was relatively
modest, it is reasonable to expect much higher DA levels in fish during major blooms.
Furthermore, DA values detected in water at other Monterey Bay sites during the same
bloom are typically much higher than those detected at the Santa Cruz wharf (M. Silver,
unpublished), possibly explaining the higher DA concentrations found in sardines
from the commercial catch. Indeed, for the bloom described in this study, DA levels
in Santa Cruz water were an order of magnitude lower than those detected at a more
southerly site in the bay (S. Fire and M. Silver, unpublished). It is also important to note
that the HPLC-UV detection limits here are rather high and that DA may in fact have
been present in low concentrations in other fish analyzed in this study.
An intriguing aspect of this study is the presence of DA in white croaker and
staghorn sculpin when it was not measurable in other species during the toxic Pseudo-
nitzschia event. Although several other species of fish were caught during times when
DA was found in water samples, they did not have detectable levels of DA. During the
3-week bloom period there were six species of fish sampled, and only white croaker
contained measurable DA levels (Table 2). Four out of the five samples contaminated
with DA during the study period were from white croaker, suggesting that this species
is somewhat unique among pier fish in its ability to accumulate the toxin. Such results
are not totally unexpected, however, as this species is known to accumulate a variety
of toxins available in other nearshore settings (e.g. Greenfield et al. 2003)
4Gulland, F. 1999. Domoic acid toxicity in California sea lions stranded along the central
California coast, May-October 1998. NOAA Tech. Memo. NMFS-OPR-8. USA National
Marine Fisheries Service, U.S. Department of Commerce.
5Langlois, G. W. 2002. Marine Biotoxin Monitoring Program annual report 2001. California
Dept. of Health Services, Division of Drinking Water and Environmental Health. Berkeley,
CA.
CALIFORNIA FISH AND GAME
188
The feeding habits of white croaker may explain its DA contamination. According
to Ware (1979)6, white croaker exhibits “euryphagous [feeding] habits and is capable
of utilizing all available food resources” in the area. Foraging individuals apparently
suck up sediment in order to ingest prey items (Ware 1979)6. This species’ broad diet
is dominated by epifaunal and infaunal invertebrates. Adult white croaker (over 100
mm length) forage mainly on deposit feeding polychaetes, detrital feeding
macrocrustaceans and have even been observed to eat “large amounts of green algae,
Ulva and Enteromorpha, and amorphous flocculent matter” (Ware 1979)6. In this
study, 96% of white croaker individuals sampled were over 100 mm SL and thus were
considered adults. It seems plausible that this euryphagous feeding behavior may be
responsible for the accumulation of DA in white croaker. The contamination pathway
for this species of fish could be either the flocculent detrital matter or the organisms
that consume it. Given that other crustacean-feeding fish were sampled at the same time
as white croaker and only one date of staghorn sculpin was DA-toxic, this suggests
that it may be a detrital pathway and not an invertebrate pathway.
DA-contaminated fish also were caught before, during and immediately following
the bloom. White croaker viscera contained toxin on two dates during the week
following the bloom, and staghorn sculpin viscera had measurable DA levels on one
date during that week (Table 2). During the post-bloom period, P. australis, like some
other diatoms, can flocculate and settle through the water column (Buck and Chavez
1994) including to shallow, nearshore sediments in Monterey Bay (R. Kvitek, California
State University, Monterey Bay and V. Welborn, University of California, Santa Cruz,
personal communication). This influx of detrital material becomes available to benthic
populations, and may provide a DA source to benthic consumers even after the surface
bloom is gone. The feeding habits of staghorn sculpin may be an explanation for its
DA contamination, as they are somewhat similar to those of white croaker. As
suggested above, benthic invertebrates may be the mechanism of DA transfer in this
case as well. According to Barry et al. (1996), adults of staghorn sculpin consume mainly
“small shore crabs, gammarid amphipods … and macroalgae”. Small individuals fed on
smaller, less mobile prey such as gammarid amphipods, harpacticoid copepods, and
polychaete worms (Barry et al. 1996). Indeed, the small shore crab, Emerita analoga,
has been shown to contain high levels of DA during HABs (Ferdin et al. 2002, Goldberg
20037).
Shiner surfperch and bocaccio were nearly as abundant as white croaker, and more
abundant than staghorn sculpin in the sample set, but showed no detectable levels of
DA. This may have been due to differences in feeding habits and/or due to their take
occurring primarily before the bloom began. Catches of shiner surfperch and bocaccio
were frequent during the beginning of the sampling period but had become infrequent
6Ware, R. R. 1979. The food habits of white croaker Genyonemus lineatus and an infaunal
analysis near areas of waste discharge in outer Los Angeles Harbor. M.A. Thesis, California
State Univ., Long Beach, 113 p.
7Goldberg, J.D. 2003. Domoic acid in the benthic food web of Monterey Bay, California.
Master’s Thesis, California State University Monterey Bay, CA. 44 p.
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 189
by the time the bloom peaked. Moreover, even if present, juvenile bocaccio of the size
collected are already piscivorous and no longer feed on benthic invertebrates (M. Carr,
Professor, University of California at Santa Cruz, personal communication). Shiner
surfperch feeds mainly on epifaunal worms (Armandia brevis and other polychaetes)
and crustaceans such as harpacticoid copepods and gammarid amphipods (Barry et
al. 1996). The four most abundant fish in this study have several prey items in common,
but there may be some other mechanism at work to bring DA into contact with white
croaker, such as the consumption of sediment as part of its feeding behavior. It is
possible that the ingestion of flocculated algal cells and DA-contaminated detritus
during feeding could make this species more likely to become toxic. The high
abundance of white croaker in the catch relative to other species during the bloom
period may be another explanation for it exhibiting most of the DA contamination.
The relationship between the appearance of DA in croaker with that of DA and toxic
Pseudo-nitzschia in the water is not yet clear from the results of this study, given the
relatively short duration of the project and the low levels of toxin in the water and fish
viscera. A surprising result of this preliminary study, however, was the detection of
DA in white croaker on 21 August, almost 2 months before the bloom began. If such
a result is found again, the mismatch could indicate the presence of DA reservoirs in
sediments or in prey items during non-bloom times at concentrations high enough to
contaminate benthic populations. Some organisms, such as sardine and anchovy, are
found to be toxic only when DA is present in the water column (Lefebvre et al. 2001).
However, there is evidence that some other organisms can retain DA long after bloom
conditions subside: razor clams are toxic up to 86 days after removal from their natural
environment to the laboratory (Horner et al. 1993, Wekell et al. 1994). The mechanism
by which this water soluble toxin is retained is not yet understood. Very recently,
Goldberg (2003)7 found a benthic echiurid worm, Urechis caupo, to be toxic whenever
sampled in the bay, suggesting some unusually effective method for retaining the toxin
or, alternately, access to environmental reservoirs of the toxin heretofore undetected.
Similar retention of DA in prey organisms of white croaker could explain DA contamination
during periods when DA is not detectable in the water column.
The levels of DA found in white croaker and staghorn sculpin viscera were below
20 μg/g (Tables 2), the level considered unsafe for human consumption. However, the
fact that white croaker contained DA on four dates during the sampling period suggests
the possibility of a potential hazard to the recreational and subsistence fishery.
Although most fishermen hold little regard for this species, it is popular with certain
ethnic groups, especially in the Asian community (Love et al. 1984). In fact, fish cake
plants that processed up to 4000 lb of white croaker per day sold their product
exclusively to Asian communities in Los Angeles (Love et al. 1984). During the
sampling period for this study, fishers of Asian descent were observed to take and keep
them in their catch and expressed their intent to consume them (S. Fire, personal
observation). Today, white croaker is still fished all over Monterey Bay throughout the
year and represents 4% of the catch at the Santa Cruz Wharf in the last 3 years for which
data are available (RecFIN2, data for 2001-2003) During this same period, this species
represented ~7% of the pier catch in the state (RecFIN)2.
CALIFORNIA FISH AND GAME
190
White croaker did not always contain DA during the fall 2001 bloom, however, and
when it did, it was found only in the viscera. Although DA was not detected in the
muscle tissue of any fish, it is not an uncommon practice to consume whole fish,
including viscera. This practice could represent the greatest hazard to fishers. Clearly,
it is advisable to remove all viscera from white croaker before consumption, even when
a harmful algal bloom is not in evidence.
In light of these data, public health may be a concern when involving the pier fisher
community. The Environmental Protection Agency states that subsistence fishers rely
on noncommercial fish as a major source of protein, and do so for a greater portion of
the year than other fishers (US EPA 1994)8. Studies have found that fish consumption
rates were higher for Asians, African-Americans, Native Americans, and other ethnic
groups and the parts of the fish eaten by these groups varied as well (OEHHA 2001)9.
In the event that fish such as white croaker become contaminated with DA during a
moderate to severe algal bloom, certain groups of pier fishers may be consuming levels
of the toxin that may approach or exceed FDA levels. Furthermore, these fishers who
already may be at risk may be exposed to this risk for longer periods of time in comparison
to other types of fishers.
CONCLUSIONS
The presence of DA in the viscera of commonly caught pier fish establishes a
potential public health risk to pier fishers. Some of these fish contain detectable levels
of phycotoxins even during low-level algal blooms, suggesting the possibility for
higher levels of intoxication during severe blooms. Individuals who fish for sport or
as a means to provide food for their families may put themselves at risk for this toxin
when taking fish close to toxic bloom events, especially if their catch includes white
croaker and staghorn sculpin. This risk may be compounded by the practice of
consuming fish that have not been gutted, essentially when eating the organs that
concentrate toxins. Until more is known about the trophic transfer of DA from
phytoplankton to fish, and about which species of nearshore fish are susceptible to
DA-contamination, the subsistence and recreational fisheries should be alerted to the
potential health risk of consuming these species.
ACKNOWLEDGMENTS
The authors thank R. Antrobus, K. Bruland, M. Carr, D. Casper, S. Coale, S. Dovel,
R. Franks, R. Kudela, K. Lefebvre, C. O’Halloran, C. Pomeroy, S. Singaram, and V.
8U.S. EPA (1994). Guidance for Assessing Chemical Contaminant Data for Use in Fish
Advisories, Vol. II: Risk Assessment and Fish Consumption Limits. Office of Water. U.S.
Environmental Protection Agency. Washington, DC: Document No. EPA 823-B-94-004.
9OEHHA (Office of Environmental Health Hazard Assessment). Chemicals in fish: Consumption
of fish and shellfish in California and the United States. Oct. 2001. <http://www.oehha.org/
fish/pdf/Fishconsumptionrpt.pdf>.
DOMOIC ACID IN THE SANTA CRUZ WHARF FISHERY 191
Welborn of University of California at Santa Cruz (UCSC), and J. Goldberg of California
State University, Monterey Bay for lab assistance, training, specimen collection, and
helpful discussions. W. Van Buskirk (Pacific States Marine Fisheries Commission,
Portland, Oregon) provided key instruction in the acquisition of the RecFIN data.
Support was provided by the Myers Oceanographic and Marine Biology Trust Fund,
Friends of Long Marine Lab (UCSC), and the Toxic Substance Research and Teaching
Program (UC) to S. Fire, , and NOAA/ECOHAB Award NA960P0476 and the University
of California California Coastal Environmental Quality Initiative 01TCEQI071088 to M.
Silver.
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Received: 31 March 2004
Accepted: 2 February 2005
... pelicans, cormorants; [16]), marine mammals (e.g. sea lions, seals, dolphins, whales; [17]), and marine fish [18,19] to toxic and sublethal doses of domoic acid. ...
... DA permeates marine food webs and has been detected in multiple pelagic and benthic fish and invertebrate species (Lelong et al. 2012a, Trainer et al. 2012. Although the toxin has been quantified in molluscs such as bivalve mussels (Bates et al. 1989, Horner and Postel1993, Amzil et al. 2001), clams (Martinet al. 1990, Wekell et al. 1994, Blanco et al. 2010 (Ferdin et al. 2002, Costa et al. 2003), krill (Bargu et al. 2002), and shrimp (Kvitek et al. 2008; and approximately 20 species of fish (Bucket al. 1992, McGinness et al. 1995, Sierra-Beltnin et al. 1997, Lefebvre et al. 2002a,b, Costa and Garrido 2004, Fire and Silver 2005, Vigilant and Silver 2007, Del Rio et al. 2010, none of these organisms have been shown to have overt excitotoxic behavioural effects as a result of consuming DA. In fact, increasing evidence suggests that fish, the most potent vectors of DA to marine mammals and birds, are not affected by DA and do not exhibit excitotoxic behaviour during typical toxic Pseudo-nitzschia blooms in spite of accumulating high levels of the toxin in the GI tract (Lefebvre et al. 2012b ). ...
... Langlois pers. comm.), yet DA has been found in fishes at locations where anglers fish (Fire & Silver 2005). Thus, humans may be exposed to DA through consumption of not only shellfish but also recreationally caught finfish. ...
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Domoic acid (DA) is a neurotoxin that causes amnesic shellfish poisoning, and fish are recognized vectors of DA to marine fauna. However, the exposure of anglers through consumption of DA-contaminated fish is unknown. We measured DA in 11 fish species targeted by Santa Cruz Wharf (SCW) anglers in Monterey Bay, California, USA, and surveyed anglers regarding their fish consumption patterns. In addition, we used California mussel Mytilus californianus DA data provided by the state of California and our measurements of DA in seawater to examine the associations between DA in fish viscera versus in mussels and seawater. DA was detected in the viscera of 7 fish species commonly consumed by anglers, and toxin uptake in fishes varied according to their diet. DA was almost entirely in the viscera, with low DA concentrations detected in muscle tissue. The majority of anglers (58% of 565) reported consuming their catch, with a small fraction ingesting the viscera. Total DA concentrations in fish decreased significantly after 11 mo storage at -20 degrees C. DA concentration in seawater and California mussels was correlated with DA in the viscera of some but not all fish groups. We conclude that SCW anglers who consume their catch are exposed to asymptomatic DA doses, and that exposure is a function of the species and parts consumed, as well as storage methods and DA levels in the seawater when the fish are caught.
... After the first DA poisoning event in Monterey Bay, CA in 1991, with northern anchovies (Engraulis mordax) found to be the DA vector (Lefebvre et al., 1999;Scholin et al., 2000), researchers identified additional DA vectors on the US west coast: e.g., mussels (Mytilus californianus), razor clams (Siliqua patula), Dungeness crabs (Cancer magister), mole crabs (Emerita analoga), and krill (Euphausica pacifica and Thysanoessa spinifera (Loscutoff, 1992;Wohlgeschaffen et al., 1992;Langlois et al., 1993;Horner and Postel, 1993;Lund et al., 1997;Lefebvre et al., 1999;Bargu et al., 2002. An increasing number of fish have also found to contain DA, including northern anchovies, Pacific sardines, sand dabs, white croaker, sculpins, and menhaden (Lefebvre et al., 1999(Lefebvre et al., , 2002aFire and Silver, 2005;Del Rio et al., 2010). In some blooms, Pseudo-nitzschia is the overwhelmingly dominant phytoplankton. ...
Chapter
Toxic algal blooms are occurring on a more frequent basis and have been shown to cause harm in higher trophic levels. The diatom toxin domoic acid, produced by the genus Pseudo-nitzschia, has been shown to be responsible for the contamination of shellfish, zooplankton, and fish around the world. Contaminations have impacted various economical markets as well. These primary consumers (vectors) have a variety of responses to blooms of toxic phytoplankton species ranging from avoidance to ingestion of the algae. To define their role in toxin transfer, it is necessary to know their position in the food web and their response to toxic food species. If the toxin is transferred via these vectors, it can cause a serious intoxication in humans, marine birds, and mammals. KeywordsDomoic acid- Pseudo-nitzschia -Shellfish-Zooplankton-Fish-Primary consumers-Vectors-Food web-Harmful algal blooms-Amnesic shellfish poisoning
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