In Situ Occurrence, Prevalence and Dynamics of Parvilucifera Parasitoids During Recurrent Blooms of the Toxic Dinoflagellate Alexandrium Minutum
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ORIGINAL RESEARCH published: 31 August 2017 doi: 10.3389/fmicb.2017.01624 In situ Occurrence, Prevalence and Dynamics of Parvilucifera Parasitoids during Recurrent Blooms of the Toxic Dinoflagellate Alexandrium minutum Elisabet Alacid *, Albert Reñé, Jordi Camp and Esther Garcés Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain Dinoflagellate blooms are natural phenomena that often occur in coastal areas, which in addition to their large number of nutrient-rich sites are characterized by highly restricted hydrodynamics within bays, marinas, enclosed beaches, and harbors. In these areas, massive proliferations of dinoflagellates have harmful effects on humans and the ecosystem. However, the high cell density reached during blooms make them vulnerable to parasitic infections. Under laboratory conditions parasitoids are able to exterminate an entire host population. In nature, Parvilucifera parasitoids infect the toxic dinoflagellate Edited by: Alexandrium minutum during bloom conditions but their prevalence and impact remain Télesphore Sime-Ngando, unexplored. In this study, we evaluated the in situ occurrence, prevalence, and dynamics Centre National de la Recherche (CNRS), France of Parvilucifera parasitoids during recurrent blooms of A. minutum in a confined site in the Reviewed by: NW Mediterranean Sea as well as the contribution of parasitism to bloom termination. Catharina Alves-de-Souza, Parvilucifera parasitoids were recurrently detected from 2009 to 2013, during seasonal University of North Carolina at outbreaks of A. minutum . Parasitic infections in surface waters occurred after the Wilmington, United States 4 5 −1 Lourdes Velo Suarez, abundance of A. minutum reached 10 –10 cells L , suggesting a density threshold French Research Institute for beyond which Parvilucifera transmission is enhanced and the number of infected cells Exploitation of the Sea, France increases. Moreover, host and parasitoid abundances were not in phase. Instead, there *Correspondence: Elisabet Alacid was a lag between maximum A. minutum and Parvilucifera densities, indicative of a [email protected] delayed density-dependent response of the parasitoid to host abundances, similar to the temporal dynamics of predator-prey interactions. The highest parasitoid prevalence Specialty section: This article was submitted to was reached after a peak in host abundance and coincided with the decay phase of the Aquatic Microbiology, bloom, when a maximum of 38% of the A. minutum population was infected. According a section of the journal to our estimates, Parvilucifera infections accounted for 5–18% of the total observed Frontiers in Microbiology A. minutum mortality, which suggested that the contribution of parasitism to bloom Received: 06 May 2017 Accepted: 10 August 2017 termination is similar to that of other biological factors, such as encystment and grazing. Published: 31 August 2017 Keywords: phytoplankton, plankton, protist, harmful algal blooms, Perkinsids, parasitism, infection flux Citation: Alacid E, Reñé A, Camp J and Garcés E (2017) In situ Occurrence, INTRODUCTION Prevalence and Dynamics of Parvilucifera Parasitoids during In the last decades, toxic and harmful planktonic protist species have been the focus of scientific Recurrent Blooms of the Toxic Dinoflagellate Alexandrium minutum. and public attention due to their environmental, economic, and public health impacts in coastal Front. Microbiol. 8:1624. areas, which are of major importance for food production ( Zingone and Enevoldsen, 2000 ). Around doi: 10.3389/fmicb.2017.01624 200 species belonging to diverse groups of marine microalgae, including dinoflagellates, diatoms, Frontiers in Microbiology | www.frontiersin.org 1 August 2017 | Volume 8 | Article 1624 Alacid et al. In situ Parvilucifera Occurrence and Dynamics pelagophytes, raphydophytes, and prymnesiophytes, have been and kill several genera of dinoflagellates, including noxious identified as potentially harmful. Of these, about 90 species, species, and their very strong virulence and high prevalence have mainly those of dinoflagellates, are potentially toxic ( Zingone and been demonstrated in laboratory experiments and in the field Enevoldsen, 2000; Hallegraeff et al., 2003 ). (Coats and Park, 2002; Chambouvet et al., 2008 ). Thus, some In the Mediterranean Sea, harmful algal blooms (HABs) authors have proposed the use of parasitoids as biological control commonly occur in areas with restricted hydrodynamics, agents for bloom mitigation ( Norén et al., 1999; Erard-Le Denn such as bays, lagoons, harbors, beaches, and estuaries. These et al., 2000 ). However, little is known about the specificity of coastal proliferations are an emerging problem whose frequency these parasites or the potential unintended side effects on other has increased in response to the intensive urbanization and dinoflagellate populations ( Anderson, 2009 ). The mechanisms recreational use of the Mediterranean shoreline, which has underlying host specificity are also not well understood, as intra- resulted in nutrient-rich (semi-) confined areas with low and inter-species variability may depend on host phylogeny turbulence levels. These areas constitute a unique environment (Chambouvet et al., 2008 ) and/or the specific genetic features that favors HAB formation by several planktonic protist of the host and parasite. Both will determine the outcome of species ( Garcés and Camp, 2012 ). For example, the worldwide infection ( Råberg et al., 2014; Turon et al., 2015; Alacid et al., distributed Alexandrium minutum is responsible for outbreaks 2016 ). of paralytic shellfish poisoning in humans and for the high A few studies have addressed the interaction between parasites mortality of wild and cultured aquatic fauna ( Anderson et al., and their dinoflagellate hosts in the marine environment in 2012 ). It also forms recurrent blooms along the Catalan coast order to assess the impact of parasitism in natural communities. (NW Mediterranean Sea) ( Vila et al., 2001, 2005; Bravo et al., Modeling studies have shown that, under certain conditions, 2008 ), which includes a large number of harbors and suffers parasitism may have a greater impact than grazing with respect from huge nutrient inputs from inland sources ( Vila et al., to dinoflagellate population dynamics ( Montagnes et al., 2008; 2001; Garcés et al., 2003; Bravo et al., 2008 ). However, many Salomon and Stolte, 2010; Jordi et al., 2015 ). In the field, the physical, chemical, and biological factors are involved in bloom prevalence of Amoebophyra parasites in dinoflagellate blooms development, persistence, and termination ( Garcés and Camp, is usually moderate to high ( Coats et al., 1996; Chambouvet 2012 ). While most studies on HAB dynamics have focused on et al., 2008; Alves-de-Souza et al., 2012; Velo-Suárez et al., 2013 ) bottom-up factors, recent investigations have demonstrated a but under some conditions is the main cause of dinoflagellate role for the top-down control exerted by biotic factors, such as mortality. In the case of Parvilucifera , although its high parasitism and grazing ( Coats et al., 1996; Johansson and Coats, abundance has been correlated with a reduction in the relative 2002; Calbet et al., 2003; Chambouvet et al., 2008; Montagnes abundance of A. minutum in short-lasting blooms ( Blanquart et al., 2008 ). et al., 2016 ), field studies on the prevalence of Parvilucifera Parasitism on marine dinoflagellates by eukaryotic parasitoids infections, their impact on natural host populations, and the is mainly due to members of the globally distributed genera contribution of infection to bloom termination are lacking. Parvilucifera and Amoebophrya (Alveolata) ( Park et al., 2004 ). The main goals of this study were: (i) to determine the timing The life cycle of these two parasitoids is, for the most part, of Parvilucifera parasitoid occurrence in Arenys de Mar harbor, similar. Infection begins when a free-living zoospore penetrates a confined area in the NW Mediterranean Sea; (ii) to assess host- a host cell, where it develops into a trophocyte that enlarges parasitoid dynamics during a bloom of the toxic dinoflagellate while feeding on the host by completely digesting its cell contents. A. minutum ; and (iii) to quantify the impact and contribution of The trophocyte nucleus then divides, and transforms into a Parvilucifera spp. parasitism to bloom termination. The present sporocyte to produce zoospores. Finally, the newly produced work constitutes the first record of the impact of Parvilucifera zoospores are released into the marine environment to find parasitoids in the field. a new host ( Jephcott et al., 2016 ). However, whereas after infection by Parvilucifera the host stops swimming and sinks MATERIALS AND METHODS immediately ( Alacid et al., 2015 ), dinoflagellates parasitized by Amoebophrya continue swimming until late stages of the Study Area infection cycle ( Park et al., 2002 ). Moreover, the sporangium of Arenys de Mar harbor (41 ◦ 34.30 N and 2 ◦ 32.40 E) is located on Parvilucifera is non-motile, unlike Amoebophrya , which forms the coast of Catalonia (NE Spain), in the NW Mediterranean Sea a highly motile vermiform stage before spreading its zoospores (Figure 1 ). Fishing and leisure are the main human activities in (Fritz and Nass, 1992 ). Consistent with the features of their the harbor. The harbor measures 0.4 km 2, has a depth ranging infection cycle, marine environmental molecular surveys have from 1 m at confined sites to 6 m at the entrance, and