Investigation into Paralytic Shellfish Toxins and Microcystins in Seabirds from Portugal
Abstract
:1. Introduction
2. Results and Discussion
2.1. Biotoxin Levels in Different Species and Tissues
2.2. Biotoxin Transfer (Putative Toxin Reservoirs), Bioaccumulation, and Biotransformation
2.3. Clinical Signs and Etiology
3. Conclusions
4. Materials and Methods
4.1. Wildlife Rehabilitation Centre and Admission Protocol
4.2. Marine and Freshwater Biotoxin Analysis
4.3. Bibliographic Search
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Admission Number | Admission Date | Place | Species (Latin Name/Common Name) | Tissue | dcSTX (µg/kg) | MCs (µg/kg) |
---|---|---|---|---|---|---|
V0048/20/A | 8 January 2020 | Portimão | Larus michahellis yellow-legged gull | Liver | 6.5 | <LOD |
Kidney | <LOD | <LOD | ||||
M1719/20 | 21 July 2020 | STP | Ichthyaetus audouinii Audouin’s gull | Liver | 6.6 | <LOD |
Kidney | <LOD | <LOD | ||||
M2527/20 | 12 October2020 | Albufeira | Morus bassanus Northern gannet | Liver | 8.7 | <LOD |
Kidney | <LOD | <LOD | ||||
V2626/20/A | 24 October 2020 | Quarteira | L. michahellis yellow-legged gull | Liver | 5.5 | <LOD |
Kidney | <LOD | <LOD | ||||
V2641/20/A | 26 October 2020 | Quarteira | Larus fuscus lesser black-backed gull | Liver | 5.6 | <LOD |
M2693/20/A | 2 November 2020 | Portimão | L. michahellis yellow-legged gull | Liver | 5.7 | <LOD |
Kidney | <LOD | <LOD | ||||
M0183/19/A | 12 March 2019 | Quarteira | L. fuscus lesser black-backed gull | Liver | <LOD | 5.8 |
M1997/19/A | 13 September 2019 | Albufeira | L. michahellis yellow-legged gull | Liver | <LOD | 5.2 |
Kidney | <LOD | <LOD | ||||
V0427/20/A | 28 February 2020 | Quelfes | L. michahellis yellow-legged gull | Liver | <LOD | 7.4 |
M0441/20/A | 2 March 2020 | Albufeira | L. michahellis yellow-legged gull | Liver | <LOD | 7.4 |
M1001/20/A | 15 May 2020 | Portimão | L. michahellis yellow-legged gull | Liver | <LOD | 7.2 |
Kidney | <LOD | <LOD | ||||
M1897/20/A | 31 July 2020 | STP | I. audouinii Audouin’s gull | Liver | <LOD | 1.6 |
M2528/20/A | 12 October 2020 | Ferragudo | L. michahellis yellow-legged gull | Cloaca | <LOD | 4.9 |
V2603/20/A | 22 October 2020 | Guia | M. bassanus Northern gannet | Kidney | <LOD | 9.6 |
Liver | <LOD | <LOD | ||||
V2617/20/A | 23 October 2020 | Tavira | M. bassanus Northern gannet | Liver | <LOD | 30.2 |
Kidney | <LOD | <LOD | ||||
V2787/20/A | 15 November 2020 | Albufeira | L. michahellis yellow-legged gull | Liver | <LOD | 4.8 |
Kidney | <LOD | <LOD | ||||
M2811/20/A | 16 November 2020 | Alvor | Calidris alba sanderling | Liver | <LOD | 27.2 |
Kidney | <LOD | <LOD |
Species (Latin Name/Common Name) | N° Individuals | PST Concentration Range (Minimum < LOQ) | Units | Analogues/Total Toxicity | Tissue | Symptoms | Necropsy | Observations | Reference |
---|---|---|---|---|---|---|---|---|---|
Alca torda/Razorbill | 5 | <LOD (5.8)–15 | µg STXeq/100 g | Total toxicity, C1, C2, GTX2, GTX3, STX | Liver | Death | Good body condition. No other significant findings | ELISA and LC-FLD | [41] |
Anas platyrhynchos/Mallard | 14 | <LOD (2)–106.3/ 3.6 | µg STXeq/100 g | Total toxicity/ dcSTX | Small intestine/Liver | Weight loss, head shaking, excessive drinking, regurgitating, wing twitching and settling, tail wagging, death | No specific abnormalities or tissue pathology | STX orally administered. dcSTX detected in the liver. Lowest lethal dose = 110 µg/kg STX, LD50% = 167 µg/kg | [53] |
Brachyramphus brevirostris/Kittlitz’s Murrelet | 9 | <LOD (56.3)–106.4 | ng/g STXeq | Total toxicity | Liver | Chick dead shortly after consuming sand lance | Good body condition. Nematode infestation in five birds. No other significant findings | ELISA, samples with lowest levels likely due to improper preservation (ethanol) | [56] |
Caracara plancus/Southern or crested caracara | 1 | 29.59 | µg STXeq/kg | GTX2/3, STX | Liver | Death | Good body condition. No other significant findings | HPLC-FLD | [55] |
Cepphus grylle/Black guillemot | 8 | <LOD (20)–41 | µg STXeq/100 g | Total toxicity | Liver | Death | Good body condition. No other significant findings | ELISA | [41] |
Fratercula cirrhata/Tufted puffin | 4 | 3.1–9.5 | ng/g STXeq | Total toxicity | Stomach and cloaca contents | Death | Emaciation. No other significant findings | ELISA. Most birds in flight feather moult. Toxins considered not the primary cause of death | [63] |
Fulmarus glacialis/Northern fulmar | 18 | <LOD (1.4)–5.9 | µg STXeq/100 g | Total toxicity | Liver | Death. Dying animals showed weakness, lethargy, drooping heads, staggering, and lack of predador avoidance | Most in poor body condition and evidence of drowning. Some with evidence of blood in gastrointestinal tract | ELISA and HPLC, C1, 2; GTX5; STX; GTX1, 4; NEO in stomach contents | [53] |
Fulmarus glacialis/Northern fulmar | 2 | 6.87 | ng/g STXeq | Total toxicity | Liver | Death | Emaciation, renal coccidiosis, bacterial pyelonephritis, dehydration with urate stasis, ureteral rupture | ELISA, highest level in bile | [58,61] |
Gavia immer/Comon loon | 2 | <LOD-7.7 | µg STXeq/100 g | Total toxicity | Liver | Death | One thin, the other in good body condition. No other significant findings | ELISA | [41] |
Gavia stellate/Red-throated loon | 1 | 6.1 | µg STXeq/100 g | Total toxicity | Digestive tract | Death | Thin. No other significant findings | ELISA, <LOD in the liver | [41] |
Gull not identified | 2 | <LOD-33.7 | µg STXeq/100 g | Total toxicity | Liver | Death | One thin, other in good body condition. No other significant findings | ELISA. A liver with <LOD analyzed by LC-FLD; toxins not detected | [41] |
Larus argentatus/Herring gull | 7 | <LOD-10 | µg STXeq/100 g | Total toxicity | Liver | Death | Good body condition, pancreatitis in one individual. No other significant findings | ELISA. A liver with <LOD analyzed by LC-FLD; toxins not detected | [41] |
Larus argentatus/Herring gull | - | 110 | µg STXeq/100 g | Total toxicity | Intestine | Death | - | HPLC | [59] |
Larus delawarensis/Ring-billed gull | 2 | 42 | µg STXeq/100 g | Total toxicity | Digestive tract | Death | Good nutritional condition. No other apparent pathological lesions | ELISA, toxins in the liver <LOD | [41] |
Larus dominicus/Kelp gull | - | 39 | nmol/g | GTX1/4 | Intestine | Death | - | HPLC-FLD. GTX4 was present in all studied tissues (intestine, stomach, liver, and kidney) | [64,65] |
Larus dominicus/Kelp gull | 8 | 15.46 | µg/kg STXeq | GTX3/2, trace levels of STX | Liver (pooled) | Death | Good body condition. No other significant findings | HPLC–FLD. Selected animals in good nutritional condition and with stomach contents for PST analysis | [55] |
Larus philadelphia/Bonaparte’s gull | 1 | 0.01, 0.02, 2.8 | µg 100 g | C1, C2, STX | Gastrointestinal contents | Death | Good nutritional condition. No other apparent pathological lesions | LC–FLD | [41] |
Melanita deglandi/White–winged scoter | 4 | <LOD (4.68)–6.4 | ng/g STXeq | Total toxicity | Liver | Death | - | ELISA | [58] |
Melanita Perspicillata/Surf scoter | 3 | <LOD-4.68 | ng/g STXeq | Total toxicity | Intestinal contents | Death | - | ELISA | [58] |
Morus bassanus/Northern gannet | 5 | <LOD (4.7)–85 | µg STXeq/100 g | Total toxicity | Liver | Death | Two of them thin, no significant findings. Highest toxin content in those with good body condition | ELISA | [41] |
Pelecanus crispus/Dalmatian pelican | 10 | 0~25 | ng/g | Total toxicity | Liver | Decreased movement before death, not opisthotonus | - | ELISA. Cylindrospermopsins and MCs also present. The highest concentration in stomach contents | [66] |
Phalacrocorax auritus/Double–crested cormorant | 19 | <LOD (4.6)–9.8 | µg STXeq/100 g | Total toxicity | Liver | Death | Good body condition for most of them, some thin. Pneumonia and aspergillosis observed in a thin hatch-year female individual. No other significant findings | ELISA. Only STX detected by LC-FLD in GI contents | [41] |
Phalacrocorax penicillatus/Brandt’s cormorant | 2 | <LOD-2.0 | ng/g STXeq | Total toxicity | Stomach contents | Death | Emaciated | ELISA. DA also detected | [58] |
Pygoscelis papua/Papua or gentoo penguin | 1 | 43 | µg STXeq/kg | GTX2/3, STX | Liver | Death | Good body condition. No other significant findings | HPLC-FLD. Selected animals in good nutritional condition and with stomach contents for PST analysis | [55] |
Rissa tridactyla/Black-legged kittiwake | 52 | <LOD (4.2)–8.8 | µg STXeq/100 g | Total toxicity, only STX | Liver | Death | Some of them were thin. No other significant findings | ELISA, LC-FLD | [41] |
Rissa tridactyla/Black-legged kittiwake | 59 | <LOD-2.7 | µg STXeq/100 g | Total toxicity | Liver | Healthy | Good nutritional condition. No other apparent pathological lesions | ELISA | [57] |
Somateria mollissima/Common eider | 3 | <LOD (5.7)–74 | µg STXeq/100 g | Total toxicity | Digestive tract | Death | One was in good body condition. Two of them were thin; one presented granulomatous myopathy and the other, pasteurellosis | ELISA, toxins in the liver <LOD, highest values in the specimen with good body condition | [41] |
Spheniscus magellanicus/ Magellanic penguin | 2 | 28–54 | µg STXeq/kg | GTX2 and 3, dcGTX2 and 3, STX, GTX1,4 at trace levels | Liver | Death | Good body condition. No other significant findings | HPLC–FLD. Selected animals in good nutritional condition and with stomach contents for PST analysis | [55] |
Sterna paradisaea/Artic tern | 11 | <LOD (2)–5.9 | µg STXeq/100 g | Total toxicity | Liver | Death, convulsion | Most in fair body condition, no significant gross or microscopic abnormalities | ELISA, HPLC. Three nestling, one adult. C1,2, dcSTX, GTX2 and 3, GTX5 also found in liver | [54] |
Thalasseus máxima/Royal tern | - | 37 | nmol/g | GTX1/4 | Intestine | Death | - | HPLC-FLD | [64,65] |
Uria aalge/Common murre | 44 | <LOD-10.8 | µg STXeq/100 g | Total toxicity | Liver | Death, reproductive failure | Emaciation. No other apparent pathological lesions | ELISA | [57] |
Uria aalge/Common murre | 16 | <LOD-1.3 | µg STXeq/100 g | Total toxicity | Upper gastrointestinal content | Healthy | Good nutritional condition. No other apparent pathological lesions | ELISA, no toxins detected in liver | [57] |
Uria aalge/Common murre | 8 | 1.4–3.9 | ppb STXeq | Total toxicity | Proventriculus or cloaca | Death | Emaciated | ELISA. Toxins not considered the primary cause of death | [62] |
Species (Latin Name/Common Name) | N° Individuals | MC Concentration Range (Minimum > LOD) | Units | Analogues | Tissue | Symptoms | Necropsy | Observations | Reference |
---|---|---|---|---|---|---|---|---|---|
Anas platyrhynchos/Mallard | 2 | 172–218 | Total MCs ng/g (dry weight) | MC-LR, [D-Leu 1]MC-LR | Liver | Lethargy, dehydration, difficulty holding head up, dry eyelids | NA | LC-MS 2 MCs may not have been the primary cause of death (botulism?) | [5] |
Anas platyrhynchos/Mallard | 3 | 31.1 | mg/g MC-LR eq | - | Liver | Depression, ataxia and paresis, rapid death | Intrahepatic hemorrhage, edema, and hepatomegaly. No other evidence of infectious disease | Mouse bioassay and commercial kit | [76] |
Coturnix japonica/Japanese quail | 5 indiv × 5 groups | 2.2–43.7 (10 days), 0.47–7.5 (30 days) | ng/g (fresh weight) | NA | Liver | No mortality or clinical signs of pathology. Increased activities of lactate dehydrogenase and a drop in blood glucose | No gross pathological changes in inner organs. Hepatic changes with the highest doses | Birds exposed to daily dose of 0.2–224.46 ng/MCs for 10 or 30 days | [71,75] |
Chroicocephalus ridibundus/Black-headed gull | 3 | 34.5 | mg/g MC-LR eq | - | Liver | Depression, ataxia and paresis, rapid death | Intrahepatic hemorrhage, edema, and hepatomegaly. No other evidence of infectious disease | Mouse bioassay and commercial kit | [76] |
Fulica atra/Coot | 9 | 75.9 | mg/g MC-LR eq | - | Liver | Depression, ataxia and paresis, rapid death | Intrahepatic hemorrhage, edema, and hepatomegaly. No other evidence of infectious disease | Mouse bioassay and commercial kit | [76] |
Pelecanus crispus/Dalmatian pelican | 10 | 0~300 | ng/g | - | Liver | Decreased movement before death, not opisthotonus | - | ELISA. Also cylindrospermopsins and STX | [66] |
Phoeniconaias minor/Lesser flamingo | 2 | 0.196 | µg/g MC-LR eq (fresh weight) | MC-LR, MC-RR, MC-LF, MC-YR | Stomach contents | Ophistotonus behaviour, convulsed position of extremities and neck in the dying phase, death | NA | Also, anatoxin-a was found | [70] |
Phoeniconaias minor/Lesser flamingo | 11 | 0.3-54.1 | 6 µg/g (wet weight) | MC-LR MC-YR MC-RR | Liver | Starvation and struggles prior to death | Emaciation, hemorrhagic lesions in the liver and muscles, enlargement of visceral organs | LC–MS/MS | [72] |
Phoenicopterus roseus/Greater flamingo | 8 | 31,100–75,900 | ng/g | - | Liver | Death | No significant findings | Mouse bioassay and commercial kit. Values corrected from original manuscript in [5], | [5,69] |
Podiceps cristatus/Great crested grebe | 6 | 53.2 | mg/g MC-LR eq | - | Liver | Depression, ataxia and paresis, rapid death | Intrahepatic hemorrhage, edema, and hepatomegaly. No other evidence of infectious disease | Mouse bioassay and commercial kit | [76] |
Podiceps nigricollis/Eared grebe | 27 | <LOD (0.06)–110 | ng/g dry weight | - | Liver | Death | - | ELISA | [74] |
Biotoxins | Samples Analyzed | Positives | Range (µg/kg) | Prevalence | Positive Organs |
---|---|---|---|---|---|
Paralytic Shellfish Toxins | 329 | 6 | 5.5–8.7 | 1.82% | Liver |
Domoic Acid | 335 | 0 | - | 0% | - |
Anatoxin-a | 315 | 0 | - | 0% | - |
Cylindrospermins | 315 | 0 | - | 0% | - |
Tetrodotoxins | 315 | 0 | - | 0% | - |
Microcystins | 315 | 11 | 1.6–30.2 | 3.49% | Liver, cloaca content, and kidney |
Month-Year | PST-Producing Phytoplankton (Alert and Interdiction Levels 500 and 1500 cells/L) | PSP Biotoxins | Observations | ||
---|---|---|---|---|---|
Density (Cells/L) | Harvesting Area | Concentration (µg STX Equiv/kg), Vector | Harvesting Area | ||
March-2019 | 40 | TAV | 84, mussel | OLH3 | >2400 (µg STX equiv/kg) determined in Venus verrucosa and Donax trunculus from Portuguese central coast (Costa de Caparica, Comporta) |
September-2019 | 160 | L7c2 | 36, mussel | L7c1 | >1500 µg STX equiv/kg) determined in Donax trunculus from Portuguese central coast (Costa de Caparica, Comporta) |
January-2020 | 160 | TAV, FUZ | 33, mussel | L7c2 | |
February-2020 | 1340 * | L7c2 | NQ | L8 | |
March-2020 | 5880 ** | TAV | 39, mussel | L7c2 | >2400 µg STX equiv/kg determined in Donax trunculus from Portuguese central coast (Costa de Caparica) |
May-2020 | 160 | LAG | NQ | NA | |
July-2020 | ND | NA | NQ | NA | |
October-2020 | ND | NA | NQ | NA | |
November-2020 | ND | NA | NQ | NA |
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Soliño, L.; Turner, A.D.; Ben-Gigirey, B.; Alexander, R.P.; Dean, K.J.; Hatfield, R.G.; Maskrey, B.H.; Casero, M.V.M. Investigation into Paralytic Shellfish Toxins and Microcystins in Seabirds from Portugal. Toxins 2025, 17, 135. https://doi.org/10.3390/toxins17030135
Soliño L, Turner AD, Ben-Gigirey B, Alexander RP, Dean KJ, Hatfield RG, Maskrey BH, Casero MVM. Investigation into Paralytic Shellfish Toxins and Microcystins in Seabirds from Portugal. Toxins. 2025; 17(3):135. https://doi.org/10.3390/toxins17030135
Chicago/Turabian StyleSoliño, Lucía, Andrew D. Turner, Begoña Ben-Gigirey, Ryan P. Alexander, Karl J. Dean, Robert G. Hatfield, Benjamin H. Maskrey, and María V. Mena Casero. 2025. "Investigation into Paralytic Shellfish Toxins and Microcystins in Seabirds from Portugal" Toxins 17, no. 3: 135. https://doi.org/10.3390/toxins17030135
APA StyleSoliño, L., Turner, A. D., Ben-Gigirey, B., Alexander, R. P., Dean, K. J., Hatfield, R. G., Maskrey, B. H., & Casero, M. V. M. (2025). Investigation into Paralytic Shellfish Toxins and Microcystins in Seabirds from Portugal. Toxins, 17(3), 135. https://doi.org/10.3390/toxins17030135