Heliyon 5 (2019) e01979 Contents lists available at ScienceDirect Heliyon journal homepage: www.heliyon.com Spatiotemporal distribution of paralytic shellfish poisoning (PSP) toxins in shellfish from Argentine Patagonian coast Leilen Gracia Villalobos a,*, Norma H. Santinelli b, Alicia V. Sastre b, German Marino c, Gaston O. Almandoz d,e a Centro para el Estudio de Sistemas Marinos (CESIMAR-CONICET), Boulevard Brown 2915 (U9120ACD), Puerto Madryn, Argentina b Instituto de Investigacion de Hidrobiología, Facultad de Ciencias Naturales y Ciencias de la Salud, Universidad Nacional de la Patagonia San Juan Bosco, Gales 48 (U9100CKN), Trelew, Argentina c Direccion Provincial de Salud Ambiental, Ministerio de Salud de la Provincia del Chubut, Ricardo Berwin 226 (U9100CXF), Trelew, Argentina d Division Ficología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n (B1900FWA), La Plata, Argentina e Consejo Nacional de Investigaciones Científicas y Tecnicas (CONICET), Av. Rivadavia 1917 (C1033AAV), Buenos Aires, Argentina ARTICLE INFO ABSTRACT Keywords: Harmful algal blooms (HABs) have been recorded in the Chubut Province, Argentina, since 1980, mainly asso- Environmental science ciated with the occurrence of paralytic shellfish poisoning (PSP) toxins produced by dinoflagellates of the genus Aquatic ecology Alexandrium. PSP events in this area impact on fisheries management and are also responsible for severe human Marine biology intoxications by contaminated shellfish. Within the framework of a HAB monitoring program carried out at Environmental risk assessment several coastal sites along the Chubut Province, we analyzed spatiotemporal patterns of PSP toxicity in shellfish Environmental toxicology – Toxicology during 2000 2011. The highest frequency of mouse bioassays exceeding the regulatory limit for human con- Alexandrium catenella sumption was detected in spring and summer, with average values of up to 70% and 50%, respectively. By Harmful algal blooms contrast, a lower percentage of positive bioassays (2–8%) or no toxicity at all was usually detected during autumn Monitoring programmes and winter. The most intense PSP events were usually observed between November and January, with values of À Bivalves up to 4,000 μg STX eq 100 g 1, and showed a marked interannual variability both in their magnitude and Mouse bioassays location. In addition, a severe PSP outbreak was recorded during autumn, 2009, at Camarones Bay, with toxicity À values of up to 14,000 μg STX eq 100 g 1. The scallop Aequipecten tehuelchus showed significantly higher toxicity values compared to other shellfish species in SJG and SMG, suggesting a lower detoxification capacity. Our results contribute to the understanding of HABs dynamics on the Argentine Patagonian coast. 1. Introduction face and neck), headache, dizziness and nausea, to more severe symptoms such as incoherent speech, a progression of altered percep- Public health problems arising directly or indirectly as a result of tion to the arms and legs, a progressive loss in limb coordination and harmful algal blooms (HABs) are of widespread occurrence. Paralytic general weakness. Respiratory distress may also occur, as a conse- shellfish poisoning (PSP) toxins are part of a family of highly potent quence of muscular paralysis progressing through the whole body, and neurotoxins (i.e. saxitoxin and analogs) mainly produced by di- death may be the outcome of PSP by respiratory paralysis (Rossini and noflagellates of the genera Alexandrium, Gymnodinium, and Pyrodinium Hess, 2010). (Etheridge, 2010). The impacts of PSP outbreaks include human in- Marine bivalves, such as mussels, clams, oysters and scallops, accu- toxications and death from contaminated shellfish or fish, loss of wild mulate PSP toxins in their tissues, which makes them potentially toxic to and cultured seafood resources, impairment of tourism and recreational vertebrates, including humans (Estrada et al., 2007). The bio- activities, alterations of marine trophic structure, and death of marine accumulation in filter-feeding bivalves and the subsequent transfer mammals, fish, and seabirds (Anderson et al., 2012). through the food web results in potentially fatal human illnesses, which The symptoms in humans range from altered perception (burning or have become a widespread public health problem especially along the tingling sensation and numbness of the lips, which can spread to the Pacific and Atlantic coasts of North America, in Central and South * Corresponding author. E-mail address: [email protected] (L. Gracia Villalobos). https://doi.org/10.1016/j.heliyon.2019.e01979 Received 8 March 2019; Received in revised form 28 May 2019; Accepted 17 June 2019 2405-8440/© 2019 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). L. Gracia Villalobos et al. Heliyon 5 (2019) e01979 America, the western European coasts, Japan, Southeast Asia, South 2. Method Africa, New Zealand, and Australia (Kacem et al., 2015). On the Argentine coast, the first PSP outbreak was documented in the 2.1. Study area description Valdes Peninsula in 1980, associated with a bloom of the species Alex- andrium catenella (as A. tamarense)(Carreto et al., 1986). Since then, The study area includes the Chubut Province coast, between 42 and blooms of Alexandrium catenella have been recurrently observed along 46 S, i.e. Northern Patagonia, Argentina (Fig. 1). The San Matías Gulf the Argentine coast, causing human intoxications and death from (SMG) is the largest of the three northern Patagonian gulfs (18,000 km2) contaminated shellfish, loss of seafood resources, and death of marine and presents two well defined areas separated by a frontal system fauna (Montoya et al., 2018, and references therein). In particular, (Amoroso and Gagliardini, 2010). In contrast, the San Jose Gulf (SJG), human poisonings and deaths were reported in northern Patagonia in subelliptic in outline and semi-enclosed, is the smallest (817 km2) and 1985 due to consumption of contaminated bivalve molluscs in Engano~ shallowest (mean depth 30 m, maximum 80 m) of the northern Patago- Bay (Vecchio et al., 1986; Santinelli et al., 2002), and a new PSP outbreak nian gulfs. The Nuevo Gulf (NG) is a roughly elliptical, semi-enclosed occurred in 1988 in Nueva Bay (Nuevo Gulf) (Esteves et al., 1992; San- body of water (2,500 km2) in communication with the southwestern tinelli et al., 2002). In order to mitigate the negative effects of PSP events Atlantic Ocean through a 17 km wide strait (Rivas and Beier, 1990). The on human health, shellfish fisheries, aquaculture and tourism, a regular Engano~ Bay (EB) is an area of exposed coast between 43 150 0200 S and monitoring program was initiated in the Chubut Province in 2000. An 43 220 4100 S, spreading to the south of the Chubut River estuary. The intense A. catenella bloom was recorded in the Northern Patagonian gulfs Chubut River has an average discharge in the bay in the order of 50 m3 À À in 2011, and then expanded southwards to Camarones Bay and San Jorge s 1, with maximums that can exceed 200 m3 s 1 (Commendatore et al., À Gulf. Toxin concentrations in mussels reached 3,980 μg STX eq 100 g 1, 1996). causing human poisonings and one fatality in Caleta Hornos, close to Southwards, the Camarones Bay (CB) is located at 44480 S and covers Camarones Bay (Baulde, 2011), associated with harvesting in forbidden a coastal marine area of approximately 52 km2. Finally, the San Jorge period. Gulf (SJgeG) is a semi-open basin of the Argentine Sea located approxi- The most significant fishery resource in the Chubut Province is a mately between 45 and 47 S that covers a total area of 39,340 km2 metapopulation of the Tehuelche scallop (Aequipecten tehuelchus) located (Fernandez, 2006). in the San Jose gulf (Amoroso and Gagliardini, 2010; Amoroso et al., 2011). However, the ribbed mussel (Aulacomya atra), the blue mussel 2.2. Shellfish sampling (Mytilus platensis) and the clam (Ameghinomya antiqua) also support important regional fisheries in the Northern Patagonian gulfs. Shellfish toxicity data from 2000 to 2011 was acquired within the Despite the impact of PSP events on public health and fisheries in framework of the HAB and Shellfish Toxicity Monitoring Program carried Northern Patagonia (Chubut Province), studies on the spatial and tem- out in Chubut coastal waters since the year 2000, as part of the Provincial poral patterns of shellfish toxicity are still lacking. Here, we analyze re- Plan for Prevention and Control of Red Tides established by the Secre- sults obtained within the framework of the monitoring program along the taría de Pesca. coast of Chubut (Northern Patagonia, 42–46 S) during the period The dataset contains a total of 1,702 toxicity records for 21 sampling 2000–2011. We used a subset of 1,702 mouse bioassay analysis focusing sites, distributed approximately between 42–46S and 64–67300W on spatial and seasonal variability to interannual patterns of timescales. (Fig. 1). Sampling was carried out monthly, although there was a lower Fig. 1. Map of the study area and location of sampling sites in Northern Patagonia, Argentina. 2 L. Gracia Villalobos et al. Heliyon 5 (2019) e01979 sampling frequency in the first years of monitoring (2000–2004). spatiotemporal distribution analysis of toxicity in shellfish species and Shellfish samples were collected from harvested beds and removed the interspecific differences in San Jose and San Matías gulfs were from subtidal sand beds and from the substrate by diving at 5–25 m of assessed by the non-parametric Kruskal–Wallis and Mann Whitney depth. analysis of variance, and post-hoc Tukey's range test. The analyzed shellfish species included Tehuelche scallops (Aequi- The spatiotemporal distribution map of PSP outbreaks was performed pecten tehuelchus), clams (Ameghinomya antique), mussels (Mytilus pla- using QGIS software (QGIS 1.8.0-Lisboa, 2012). tensis), ribbed mussels (Aulacomya atra), Geoduck clams (Panopea abbreviata) and razor clams (Ensis macha).