Impact of preparation method on gonad domoic acid levels in the scallop, Pecten maximus (L.)

doi:10.1016/S1568-9883(03)00025-8

Harmful Algae

Volume 2, Issue 3, August 2003, Pages 215-222

https://doi.org/10.1016/S1568-9883(03)00025-8 Get rights and content

Abstract

The king scallop, Pecten maximus (L.), fishery is a valuable economic resource in the UK, and is reliant on supplying premium “roe-on” processed scallops to the continental market. A considerable degree of variability is observed in domoic acid (DA) levels among individual P. maximus and their body components, which complicates the management of the fishery during amnesic shellfish poisoning (ASP) events. This study examined the impact of professional processing and three differing laboratory preparation techniques on final gonadal DA levels. DA analysis was conducted using a LC–MS/MS procedure. The results demonstrate that different methods of preparation can significantly alter gonadal toxicities in scallops from the same site, and the extent to which DA within the digestive loop, which passes through the gonad, contributes to total gonadal DA. Mean gonadal toxicity attributed to the digestive loop contents was estimated at 4.7–24.7 μg DA g⁻¹. Despite large individual variations in toxin levels; in scallops with elevated gonadal toxicities resulting from higher digestive loop content toxicity, the effect of flushing out the contents of the digestive loop significantly reduced the DA content of the tissue and lowered the frequency of individuals harbouring levels above the 20 μg DA g⁻¹ statutory safety limit. Removal of the digestive loop contents can potentially result in an 87% decrease in gonadal DA burden. Furthermore, the method applied by professional processors effectively removed the contents of the digestive loop and reduced gonadal DA to levels comparable with the laboratory techniques. Deliberate contamination with scallop mucus did not increase gonadal DA levels. The extent of toxin variation resulting from differing gonad preparations demonstrates the need to standardize scallop tissue preparation techniques during ASP events. Consequently, detailed protocols aimed at minimizing the contamination of edible components should be developed and adhered to by both processing facilities and monitoring bodies.

Introduction

The king scallop (Pecten maximus (L.)), fishery is a valuable economic resource in the UK, and is principally exploited by scallop dredgers, which account for 97% of UK landings. An estimated 95% of the king scallops are processed as an adductor muscle and gonad “roe-on” product for the continental market, of which 60% is distributed as premium chilled product and 40% frozen (Denton, 1999).

In July 1999, P. maximus harbouring the amnesic shellfish poisoning (ASP) toxin, domoic acid (DA), in gonadal tissue at levels above the statutory limit (20 μg DA g⁻¹) were detected across areas of northern and western Scotland. This prompted a widespread closure of the king scallop fishery which persisted for more than 10 months. During the height of the incident the ban covered in excess of 19,000 square miles, to date the largest fisheries closures resulting from a harmful algal bloom (HAB) (Campbell and Kelly, 2001). The pennate diatom Pseudo-nitzschia australis was indicated as a potential causative agent of scallop toxicification, on the basis of its dominance within the phytoplankton and confirmation of its DA production capability in culture (Campbell et al., 2001). ASP events have occurred each year in Scotland since then, resulting in financial hardship for scallop dredging, diving and cultivation industries.

A considerable degree of variation in DA level is encountered among individual P. maximus and their body components. Despite this, DA loading of the tissues follows a predictable rank order: all other tissue (digestive gland (hepatopancreas), mantle tissue and gills) > gonad > adductor (Arevalo et al., 1998, Campbell et al., 2001, Hess et al., 2001). Toxin levels within all other tissue account for 99% of the total DA burden and are consistently an order of magnitude over the statutory 20 μg DA g⁻¹ limit. Thus during ASP events the consumption P. maximus digestive glands, mantles and gills would pose a high risk to public health. However, in Pectinids, a loop of intestine passes directly through the gonad (Purchon, 1977). The digestive loop in P. maximus can represent up to 6% of the gonadal volume (Mackie, 1986) and the contents therefore have the potential to contribute to gonadal toxicity.

DA levels in gonad tissue are generally lower than the statutory 20 μg DA g⁻¹ limit. However, the concentration of DA in gonad tissue can vary by an order of magnitude and DA levels above the statutory (20 μg DA g⁻¹) safety level are regularly detected (Campbell et al., 2001). Consequently, strict regulatory regimes are now compulsory for the safe marketing of “roe-on” scallops. A total ban on harvesting is invoked when whole scallop toxicity exceeds 250 μg DA g⁻¹. Scallops from a fishing box with whole animal toxicities in the range from 20 to >250 μg DA g⁻¹ can only be landed to a processor, having shown that the median gonadal toxicity is not greater than 4.6 μg DA g⁻¹, which ensures that individuals with gonadal toxicities above 20 μg DA g⁻¹ are not harvested at a 99% confidence level (Fryer et al., 2001). Adductor muscle toxicity contributes negligible amounts to the total body burden, and levels never exceed the statutory limit, even when toxin levels are extremely high in all other tissue (Campbell et al., 2001).

The high individual variation in toxicities, and particularly the occurrence of DA in the gonad at levels above the regulatory limit, complicates the management of the king scallop fishery during ASP events. The variance of DA toxicity in scallop tissue may be attributed to one of, or a combination of three sources: (1) natural variation in tissue toxicity (Shumway and Cembella, 1993); (2) variable contamination of the tissue from toxic body components, during “shucking” and dissection; (3) analytical error. Characterizing variation in toxin levels is necessary both for ecological considerations and for the development of sound management protocols (Whyte et al., 1993). Given the extent to which digestive material can contaminate edible tissues, the potential to reduce the DA burden by appropriate preparation of gonad tissue should be established. The objectives of this study were to (a) examine the impact of professional processing and three different laboratory preparation techniques on final gonadal toxin levels, (b) evaluate the significance of the toxin content in the digestive loop running through the scallop gonad on final gonadal DA level and (c) assess scallop mucus as a potential source of DA contamination.

Section snippets

Sampling

In October 2000, and after obtaining a dispensation order from the Food Standards Agency (FSA) Scotland to fish, 80 specimens of adult P. maximus (shell height >90 mm, “market size”) were collected by SCUBA divers from each of fisheries boxes J9 (Jura), SM15 and SM16 (Sound of Mull) (sites 1, 2 and 3, respectively, Table 1). These locations are routinely used for monitoring ASP toxin levels by the FSA Biotoxin Monitoring Program and were chosen as a result of previous consistently high DA levels

Gonad wet weight

Normality and homoscedasticity were achieved by applying a log₁₀ transformation to the raw data. Significant differences were found among the mean gonad wet weights (g) of scallops from each site (F=140.4, P=<0.001, d.f.=2228). Individuals from site 3 had a significantly greater mean gonad wet weight than individuals from sites 1 and 2, and the mean gonad wet weight was greater in individuals from site 2 than 1. However, there was no significant difference in mean gonad size after the scallops

Discussion

The levels and variability of DA found in the gonad tissue of P. maximus in the present study are consistent with those of previous studies (Arevalo et al., 1998, Campbell et al., 2001, Hess et al., 2001).

The results demonstrate that DA contamination can be derived from the digestive loop contents. The mean level of gonadal toxicity attributed to the digestive loop contents was estimated at 4.7–24.7 μg DA g⁻¹. The digestive loop descends from the stomach sac and passes through the digestive gland

Acknowledgements

We thank Colin Campbell and Mull Marine Services for the sample collection and Loch Fyne Seafarms for processing the scallops. This study was funded by The Highlands and Islands Enterprise and The Highland Council.

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The pennate diatom Pseudo-nitzschia is globally distributed genus containing several species that produce domoic acid, a potent neurotoxin (Hasle, 2002). Toxic blooms of Pseudo-nitzschia have resulted in the deaths of humans (Bates et al., 1989), sea birds (Fritz et al., 1992), and marine mammals (Fire et al., 2011; Scholin et al., 2000; Silvagni et al., 2005), as well as the closures of commercial fisheries (e.g. Campbell et al., 2003). The abundance of Pseudo-nitzschia in the GOM has been increasing since the 1950s due to increased nutrient loading from the Mississippi River (Parsons and Dortch, 2002), and several toxic blooms have been recorded in the area in the last two decades (Dortch et al., 1997; Liefer et al., 2013, 2009; Macintyre et al., 2011).
The diatom genus Pseudo-nitzschia is a common component of phytoplankton communities in the Gulf of Mexico and is potentially toxic as some species produce the potent neurotoxin domoic acid. The impact of oil and chemical dispersants on Pseudo-nitzschia spp. and domoic acid production have not yet been studied; preliminary findings from a mesocosm experiment suggest this genus may be particularly resilient. A toxicological study was conducted using a colony of Pseudo-nitzschia sp. isolated from a station off the coast of Louisiana in the Gulf of Mexico. The cultures were exposed to a water accommodated fraction (WAF) of oil and a diluted chemically enhanced WAF (DCEWAF) which was a mix of oil and dispersant (20:1). Exposure to WAF induced a lag phase but did not inhibit growth rates once in exponential growth. Cultures grown in DCEWAF did not experience a lag phase but had significantly lower growth rates than the Control and WAF cultures. The cellular quota of domoic acid was higher in cultures treated with DCEWAF and WAF relative to their control values, and half of the domoic acid had leaked out of the cells into the surrounding seawater in the DCEWAF cultures while all the domoic acid remained inside the cells in WAF-treated cultures. These results suggest that the presence of oil could lead to toxic blooms, but that the application of dispersant could decrease bioaccumulation of domoic acid through the food web.
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Taking this into account, the elimination of the DG by means of selective evisceration would not substantially reduce toxicity. In P. maximus, in which selective evisceration is used, different studies have demonstrated that the digestive gland contains more than 90% of the toxin, but only contributes less than 10% to the total body weight (Arévalo et al., 1998; Blanco et al., 2002a; Campbell et al., 2001, 2003). Therefore, their anatomical distribution of DA has allowed the establishment of the European Decision 2002/226/EC, which allows the harvesting and marketing of eviscerated scallops under specific conditions.
In northern Chile, domoic acid (DA) has been detected in several bivalve species. In Mesodesma donacium, one of the most important commercial species for local fishermen, no information is available on depuration, or on the anatomical distribution of this toxin and its potential use as a palliative measure to minimize the consequences of ASP outbreaks. Deputation of DA is very fast in M. donacium, and can be adequately described by means of a two-compartment model. The estimated rates for the first and second compartments were 1.27 d⁻¹ and 0.24 d⁻¹, respectively, with a transfer rate between compartments of 0.75. Having high depuration rates protects this species from being affected by Pseudo-nitzschia blooms for an extended period of time. Taking this into account, the time in which the bivalves are unsafe for consumers is very short, and therefore the economic losses that could result by the DA outbreaks in local fisheries should be moderate. In relation to anatomical distribution, at least during the uptake phase, the toxin was evenly distributed within the soft tissues, with a total toxin burden corresponding to 27%, 32% and 41% for Digestive Gland (DG), Foot (FT) and Other Body Fractions (OBF), respectively. Since the contribution of each organ to the toxin concentration is a function of both weight contribution and toxin burden, the pattern of toxin distribution showed the following trend: “all other body fractions” (OBF) > Foot (FT) > Digestive Gland (DG). Thus, the highest concentration of DA, with a contribution close to 72%, corresponds to the edible tissues (OBF + FT), while the DG (non-edible tissue) only contributes the remaining 28%. Consequently, in view of the anatomical distribution of domoic acid in M. donacium, the elimination of the digestive gland does not substantially reduce the toxicity of the final product and therefore selective evisceration would not improve their quality for human consumption.
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This capacity was suggested for C. gigas (Jones et al., 1995), but is lacking or limited in Pecten maximus (Blanco et al., 2002a). Therefore, visceral tissues (including the digestive gland) may account for 94–99% of the toxin burden in DA-contaminated P. maximus (Blanco et al., 2002a, 2006; Campbell et al., 2003; Bogan et al., 2007), 93% in M. edulis (Grimmelt et al., 1990), but only 70% in C. virginica (Roelke et al., 1993) during the toxin uptake phase. Toxin kinetics may be affected by the body size of contaminated organisms.
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2007, Harmful Algae
Amnesic shellfish poisoning (ASP) has proved problematic in Irish king scallop, Pecten maximus fisheries necessitating restrictions on the sale of fresh scallops (in-shell), which achieve a higher market price than frozen processed product. An investigation of variability in domoic acid (DA) concentration in king scallop from 69 sampling sites within a limited area off the southeast coast of Ireland was performed. Variation in DA concentration was examined in the whole area, within smaller sub-areas, with size, age, and water depth. Mean DA concentrations in whole scallop ranged from 6.5 to 154.3 μg g⁻¹, with an overall mean of 40.6 ± 30.8 μg g⁻¹. The concentration in gonad exceeded 20 μg g⁻¹ in 17 sites and in adductor muscle in 3 sites. Significant differences in DA concentration were detected between scallops from different sampling stations. Whole scallop tissue and individual scallop tissues with the exception of gonad, exhibited significant negative correlations with water depth. Highest DA concentrations were recorded in inshore, shallow sites and lowest DA concentrations in deeper offshore waters. Significant positive correlations between DA concentration in hepatopancreas and scallop size were exhibited at inshore sites but not at offshore sites. High inter-animal and spatial variability in toxin concentration demonstrated the importance of a reliable sampling protocol for the management of ASP outbreaks to ensure public safety and to avoid unnecessary fishery closures.

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Harmful Algae

Abstract

Introduction

Section snippets

Sampling

Gonad wet weight

Discussion

Acknowledgements

References (15)

Sequestering and putative biotransformation of Paralytic shellfish toxins by the scallop Placopecten magellanicus: seasonal and spatial scales in natural populations

J. Exp. Mar. Biol. Ecol.

ASP in king scallops

Shellfish News

Distribution of domoic acid in king scallop (Pecten maximus) populations, from the West Coast of Scotland

J. Shellfish Res.

Determination and confirmation of the amnesic shellfish poisoning toxin, domoic acid, in shellfish from Scotland by liquid chromatography and mass spectrometry

J. AOAC Int.

Cited by (16)

Growth dynamics and domoic acid production of Pseudo-nitzschia sp. in response to oil and dispersant exposure

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Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health

Toxin production and temperature-induced morphological variation of the diatom Pseudo-nitzschia seriata from the Arctic

Domoic acid uptake and elimination kinetics in oysters and mussels in relation to body size and anatomical distribution of toxin

Spatial variability of domoic acid concentration in king scallops Pecten maximus off the southeast coast of Ireland