Frontiers reaches 6.4 on Journal Impact Factors

Original Research ARTICLE

Front. Mar. Sci., 17 July 2017 | https://doi.org/10.3389/fmars.2017.00220

S.O.S. Pinna nobilis: A Mass Mortality Event in Western Mediterranean Sea

Maite Vázquez-Luis1*, Elvira Álvarez1, Agustín Barrajón2, José R. García-March3, Amalia Grau4,5, Iris E. Hendriks6,7, Santiago Jiménez8, Diego Kersting9,10, Diego Moreno2, Marta Pérez10, Juan M. Ruiz11, Jordi Sánchez12, Antonio Villalba13,14 and Salud Deudero1
  • 1Centro Oceanográfico de Baleares, Instituto Español de Oceanografía, Palma de Mallorca, Spain
  • 2Agencia de Medio Ambiente y Agua, Consejería de Medio Ambiente y Ordenación del Territorio, Almería, Spain
  • 3Instituto de Investigación en Medio Ambiente y Ciencia Marina, Universidad Católica de Valencia, Alicante, Spain
  • 4Laboratori d'Investigacions Marines i Aqüicultura, Illes Balears, Spain
  • 5Instituto de Investigaciones Agroambientales y de Economía del Agua (INAGEA), Palma de Mallorca, Spain
  • 6Global Change Department, Mediterranean Institute for Advanced Studies (CSIC-UIB), Instituto Mediterráneo de Estudios Avanzados, Esporles (Mallorca), Spain
  • 7Departamento de Biología, Universitat de les Illes Balears, Palma de Mallorca, Spain
  • 8Instituto de Ecología Litoral, Alicante, Spain
  • 9Section Paleontology, Institute of Geological Sciences, Freie Universität Berlin, Berlin, Germany
  • 10Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain
  • 11Instituto Español de Oceanografía, Centro Oceanográfico de Murcia, Murcia, Spain
  • 12SUBMON - Serveis Ambientals Marins, Barcelona, Spain
  • 13Centro de Investigacións Mariñas, Consellería do Mar, Xunta de Galicia, Vilanova de Arousa, Spain
  • 14Departamento de Ciencias de la Vida, Universidad de Alcalá, Alcalá de Henares, Spain

A mass mortality event (MME) impacting the bivalve Pinna nobilis was detected across a wide geographical area of the Spanish Mediterranean Sea (Western Mediterranean Sea) in early autumn 2016. Underwater visual censuses were conducted across several localities separated by hundreds of kilometers along the Spanish Mediterranean coasts and revealed worrying high mortality rates reaching up to 100% in the center and southernmost coasts of the Iberian Peninsula including Balearic Islands. Populations on the northern coasts of the Spanish Mediterranean Sea seemed to be unaffected (Catalonian region). Histological examination of affected individuals revealed the presence of a haplosporidan-like parasite within the digestive gland being probably the pathogen that causes this mortality. The present MME has spread rapidly, causing high mortality rates in infected populations. Taking into account the degree of impact, the geographic extent, and the high probability that the infection is still in a spreading phase, this might be considered the largest MME ever registered for P. nobilis up to date, forcing this emblematic bivalve into a critical viability status over hundreds of kilometers of coast.

Introduction

The Pinnidae family Leach 1819 (order Ostreida, Lemer et al., 2016) is a taxonomic family of large saltwater bivalves commonly known as pen shells or fan mussels. They are filter-feeding molluscs with a long triangular shape with the apex of the shell anchored in the substrate by byssus threads. The shells reach 15–35 cm length, exceptionally up to 120 cm (Schultz and Huber, 2013). This family includes two genera (Pinna and Atrina, Lemer et al., 2014) with 61 species described worldwide (WoRMS, 2014). Most of the species are distributed in the Indo-Pacific area, with some inhabiting the Caribbean Sea, West Africa, Mediterranean Sea, North East Atlantic, and West America. In the Mediterranean Sea, the endemic bivalve Pinna nobilis Linnaeus 1758 is distributed at depths ranging from 0.5 to 60 m being the largest bivalve of this sea (Zavodnik et al., 1991; Butler et al., 1993). In the twentieth century, P. nobilis populations have greatly declined due to anthropogenic activities, including recreational and commercial fishing, ornamental harvesting, and accidental killing by anchoring, bottom nets and trawlers (Vicente and Moreteau, 1991; Richardson et al., 2004; Katsanevakis, 2007; Hendriks et al., 2013; Deudero et al., 2015; Vázquez-Luis et al., 2015). At the present time, this species is legally protected under Annex II of the Barcelona Convention (SPA/BD Protocol 1995), Annex IV of the EU Habitats Directive (EU Habitats Directive 2007), and Spanish Catalog of Threatened Species (Category: Vulnerable, Royal Decree 139/2011). Mass mortality events (hereafter MMEs) represent demographic catastrophes that can affect simultaneously all life stages (Lande, 1993). Recently the magnitudes of MMEs are changing among animal taxa, with increases for birds, marine invertebrates, and fishes (Fey et al., 2015). Analyzing the impact of these events at appropriate scales (spatial and temporal) and biological organization levels (species, populations, communities) is crucial to accurately anticipate future changes in marine ecosystems and propose adapted management and conservation plans (Pairaud et al., 2014). Some MME on bivalve molluscs are consequence of a disease caused by parasites and has been widely studied for commercial bivalve molluscs (Peters, 1988; Elston et al., 1992; Barber, 2004). Among Pinnids, high mortality rates of Atrina pectinata (60–90%) and Atrina lischkeana (with rates exceeding 60%) have been observed as a consequence of virus-like parasites (Maeno et al., 2006, 2012). Regarding Pinna nobilis the existence of one parasite which affects the gonads causing the castration of the animal has been observed (de Gaulejac, 1993). However, studies on diseases or parasites among Pinnids are scarce.

In early autumn 2016 (end September and beginning October 2016) an abnormally high mortality of P. nobilis individuals was detected almost simultaneously at several points in the Spanish Mediterranean Sea (south-western Mediterranean Sea) separated by hundreds of kilometers. The main aim of this paper is to provide a comprehensive report on the extent of a P. nobilis MME in the SW Mediterranean Sea by providing data on its geographical scale, intensity, depth range, the cause and the timing of the event in the different impacted areas. Finally, we want to raise the alarm to neighboring countries of the Mediterranean Sea.

Materials and Methods

Study Areas

This study encompasses a large geographical scale covering the main habitat for P. nobilis (Posidonia oceanica seagrass meadows) but also other habitats such as Cymodocea nodosa seagrass meadows, rocky shores, coastal lagoons, maërl beds, and detritic bottoms. Different research groups involved in the study of the species have conducted censuses to estimate the extent of the event and the mortality rates in the impacted populations at a national level (Spanish Mediterranean Sea). In some cases, affected populations have been studied over the last decade by scientists of various research institutes. Visual censuses were carried out between September 2016 and June 2017 among 137 localities along the Spanish coast (Figure 1) and more than 1,600 individuals of pen shells have been registered. Moreover, several diving centers and recreational divers have been contacted (citizen science) in order to obtain widespread information about the current status of the P. nobilis population throughout the study area.

FIGURE 1
www.frontiersin.org

Figure 1. Extent of the mass mortality event on Pinna nobilis in western Mediterranean Sea. White dots indicate the sampling localities from September 2016 to June 2017, red shading, mortality of 100% of individuals censed; shaded orange, mortality between 90 and 99% of individuals censed; and green shading, no mass mortality detected. Question marks are places where there are P. nobilis populations but it has not been possible to carry out censuses to evaluate the state of the populations in the frame of the MME. *Individuals isolated due to being at their distribution limit: aOnly four living specimens in Algeciras Bay; and bOne living specimen.

Impact Assessment of P. nobilis Mortality Event

Data on mortality impact was obtained by both rapid assessments and detailed surveys in monitoring localities (non-destructive surveys). In both types of surveys, number of living, dead and affected (detection of diseased individuals when possible) individuals were recorded to obtain the percentage of the P. nobilis population belonging to each state. Additional information such as depth, habitat type, density of individuals, and total area surveyed were also registered when possible. Affected but still living individuals were clearly differentiated, since they present mantle retraction (i.e., not reaching the edge of the valve), a lack of response to stimuli, and slow closing of the valves. Samples of sick and healthy specimens have been collected and histopathological analyses have been carried out in order to identify the agent that could be blamed for the MME. Collection of P. nobilis individuals (both sick and healthy specimens) were conducted under permission of “Servei de Protecció d'Espècies” and “Cabrera National Park,” both of “Conselleria de Media Ambient, Agricultura i Pesca.” A total of 24 individuals from 2 localities separated tens of kilometers were sampled (Andratx and Cabrera National Park (Balearic Islands): 23 and 1 respectively). Samples were fixed in 10% buffered formalin for at least a week, embedded in paraplast, sectioned at 4 μm and routine hematoxilin/eosine stained for light microscope examination.

Results

By the end of September and beginning October 2016 a great mortality of individuals of Pinna nobilis was detected across several locations along Spanish Mediterranean Sea (Figure 1). The first observations of mortality were reported on the 28th September, 4th and 5th October in the southern and south-east of Iberian Peninsula (Andalusia, Region of Murcia and southern Valencia Community) and Balearic Islands (Formentera and Ibiza). By the third week of October, mortalities close to 90% were detected in almost all the populations under study in the above mentioned localities. In Mallorca the first warnings of anomalous mass mortalities were produced in mid-November 2016. The same pattern was found few months later (March 2017) in populations inhabiting the rest of the Balearic Islands (Menorca and Cabrera) reaching mortalities rates over 90% in the different populations. During March to June 2017, many localities in the above mentioned areas were revisited and the obtained results showed that mortality rates reached in all cases 100%. Regarding Chafarinas Islands located in the Alboran Sea off the coast of Morocco mortalities of 90% have been detected but this mortality event does not seem to be recent. Affected individuals were found independently of depth, habitat type or size-age (juveniles and adults) of the pen shell individual. In the Columbretes Islands Marine Reserve (located in the north of Valencia Community), populations were unaffected in November 2016. In the same way, data from P. nobilis populations inhabiting the northernmost part of the Spanish Mediterranean Sea (Catalonia) obtained in September 2016, showed that these populations were not affected. The most recent data in the area (April-June 2017), corresponding to the populations of the Alfacs Bay in Delta del Ebro (Natural Park), the Medes Islands marine reserve and Cadaqués, indicates that populations in those areas have not been impacted at least for the moment. The congeneric species P. rudis, which shares habitat with P. nobilis in many of the surveyed areas, seems to be unaffected by the mortality.

Gross signs of sick pen shells, Pinna nobilis, were unspecific but include, gaping, slow closing and loss of force of the valves, mantle recession, emaciation and the occurrence of abundant large vesicles full of liquid on the visceral mass. Histological examination revealed the presence of a haplosporidan-like parasite (unknown species, under study) (Figure 2) within the digestive gland in the 2 studied localities (in 23 of the 24 individuals analyzed); and in a third locality separated hundreds of kilometers (Darriba, 2017). Numerous plasmodia and sporogonic stages, as well as mature ellipsoidal spores with a lid, were found in the epithelium of digestive tubules. In advanced infected individuals of P. nobilis, the epithelium of all the digestive tubules was completely occupied by stages of the parasite; the epithelium height of digestive tubules was reduced, thus resulting in wider lumen. A heavy inflammatory host response was associated with infection, with serious infiltration of the connective tissue of the digestive gland by host hyaline hemocytes. Since food absorption takes place in the digestive gland, a heavy occupation of its epithelium with the parasite should cause severe organ dysfunction, likely leading to host starvation.

FIGURE 2
www.frontiersin.org

Figure 2. Digestive gland of P. nobilis. Mature ellipsoidal uninucleate spores were found in the epithelia of digestive tubules (A). A heavy inflammatory host response, with infiltration of the connective tissue by hyaline hemocytes, was associated with infection (B). Note that the epithelium height of the digestive tubules was reduced, resulting in a wider lumen.

Discussion

The results presented here allow us to infer that a mass mortality event (MME) has affected the populations of P. nobilis in a large area of the Spanish Mediterranean Sea (Western Mediterranean Sea) and removing in most cases 100% of pen shell population. Although the proportion of the animal population removed during an MME remains the most widespread approach for defining a MME (Young, 1994; Reed et al., 2003; Garrabou et al., 2009; Ameca et al., 2012), only 9.6% of published MMEs reported information on how MMEs affect population sizes (Fey et al., 2015). This lack of data limits the ability to resolve temporal patterns in the population-level consequences of MMEs. However, reported MMEs frequently remove a substantial proportion of animal populations, including up to 100% of the population (Fey et al., 2015). In our case, given that P. nobilis presents the highest population densities in the central Spanish Mediterranean Sea (Southern Catalonia, Valencia Community, Murcia and the Balearic Islands; Guallart and Templado, 2012; Prado et al., 2014) and that in many of those areas the population has suffered a drastic decline close to 100%, it is estimated that the P. nobilis population could have been reduced by more than 90% at the national level (Spanish Mediterranean). In the case of the Balearic Islands, the Valencian Community and the Murcia Region some emblematic and long-studied localities for this species were found, such as Tabarca Marine Reserve in Alicante (Garcia-March et al., 2016), the Cabrera National Park in the Balearic Islands (Vázquez-Luis et al., 2014; Deudero et al., 2015) and Isla Grosa Natural Park in Murcia Region (Ruiz et al., 2016) with no individual alive to date. Taking into account that many of the most relevant populations at national level have been impacted by the MME, the consequences in the distribution, potential recovery, and therefore in the viability of the species are unknown and alarming, since most of the populations were already fragmented (Guallart and Templado, 2012). This degree of regression of the Spanish population of 90% should allow a change in the cataloging of the species at the national level from “Vulnerable” to “Endangered” or “Critically Endangered.”

The haplosporidan-like parasite detected in moribund individuals is highly probably causing this MME, however samples are still being analyzed and there may be other related causes. Regarding the possible origin of the parasite as it has been pointed out by Darriba (2017), it is impossible to asseverate if this parasite is new infecting P. nobilis or if is an old symbiont that has changed leading to a mortality outbreak. Other haplosporidan species, such as Haplosporidium nelsoni and Bonamia spp., have been responsible for bivalve mass mortalities world-wide (Arzul and Carnegie, 2015). Considering the vast geographic spreading, parasite eradication does not seem feasible because historical attempts to eradicate bivalve mollusk parasites from marine open areas have failed; intermediate or reservoir hosts and parasite long-term resistant stages could contribute to parasite staying even if the specimens of the host species are thoroughly removed from affected areas (Grizel et al., 1986; van Banning, 1991). Therapeutic measures in the open marine environment should also be discarded. Therefore, only prevention measures can be applied. Caution must be taken avoiding the movement of specimens of the species between zones (zoning) and minimizing the risks of infection by transporting parasite infective stages (vessels, equipment, etc.). In the short-term, the possibility of the existence of resistant specimens must be explored; resistance to this infection could be crucial to develop restoration programs using resistant strains produced through selective breeding (Dégremont et al., 2015). It is as well of high importance to search for potentially survived juveniles in the impacted areas as the present MME occurred after spawning of P. nobilis, which was observed from May to July in Balearic Islands (Deudero et al., 2017). Additionally, neighboring non-affected populations should be periodically monitored to detect a further spread of the parasite infection.

This unprecedented P. nobilis MME has spread very rapidly and has caused high percentages of mortality in infected populations. Taking the degree of impact into account, the geographic extent, and the fact that the event is ongoing, this might be considered the largest MME ever registered for P. nobilis, but also among Pinnids worldwide (Maeno et al., 2006, 2012). The possibility that environmental factors mediate in the speed and direction of propagation should be taken into account, since the effect is concentrated only in the South, Southeast and Balearics (e.g., currents) at the moment. Nonetheless, the parasite has progressed over months, therefore can continue spreading across the Mediterranean basin. P. nobilis is characterized by high longevity and slow population dynamics with low population replenishment. This event may produce severe consequences, not only in the viability of the affected populations, but, due to the large geographical area impacted, the consequences could be disastrous for the species at least at a Mediterranean sub-basin level. We suggest that neighboring countries urgently adopt monitoring plans to detect drastic population reductions and identify resistant individuals, to ensure an acceptable level of genetic variability in possible future restocking programs.

Author Contributions

MV, EA, AB, JG, AG, IH, SJ, DK, DM, MP, JR, JS, AV, and SD conducted field work or laboratory analyses and help with writing and revision of the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer VB and handling Editor declared their shared affiliation, and the handling Editor states that the process nevertheless met the standards of a fair and objective review.

Acknowledgments

The authors are very grateful to “División para la Protección del Mar” (M° de Agricultura y Pesca, Alimentación y Medio Ambiente-MAPAMA); we thanks also to F. Garfella, G. Follana, M. Maldonado, J. M. Remón, J. De la Rosa, M. Fernández-Casado, M. C. Arroyo, and M. S. Vivas for providing sick specimens and/or visual census data. MV is supported by a postdoctoral contract co-funded by the Regional Government of the Balearic Islands and the European Social Fund 2014–2020. EA was also supported by a Personal Técnico de Apoyo contract (PTA2015-10829-I) funded by the Spanish Ministry of Economy and Competiveness. JG is supported by the project “The study, protection and possible breeding of pen shell (Pinna nobilis) in the Boka Kotorska Bay” funded by the Alberto II of Monaco Foundation. IH is supported by grant RYC-2014-15147, co-funded by the Conselleria d'Innovació, Recerca i Turisme of the Balearic Government (Pla de ciència, tecnologia, innovació i emprenedoria 2013-2017) and the Spanish Ministry of Economy, Industry and Competitiveness. MP was supported by the Spanish Ministry of Science and Innovation (project RECCAM CTM2013-48027-C3-1-R. JR is supported by the Regional Government of Murcia and the European Fishery Found.

References

Ameca, Y., Juárez, E. I., Mace, G. M., Cowlishaw, G., and Pettorelli, N. (2012). Natural population die offs: causes and consequences for terrestrial mammals. Trends Ecol. Evol. 27, 272–277. doi: 10.1016/j.tree.2011.11.005

CrossRef Full Text | Google Scholar

Arzul, I., and Carnegie, R. B. (2015). New perspective on the haplosporidian parasites of molluscs. J. Invertebr. Pathol. 131, 32–42. doi: 10.1016/j.jip.2015.07.014

PubMed Abstract | CrossRef Full Text | Google Scholar

Barber, B. J. (2004). Neoplastic diseases of commercially important marine bivalves. Aquat. Living Resour. 17, 449–466.

Butler, A., Vicente, N., and Gaulejac, B. (1993). Ecology of the pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Mar. Life 3, 37–45.

Google Scholar

Darriba, S. (2017). First haplosporidan parasite reported infecting a member of the Superfamily Pinnoidea (Pinna nobilis) during a mortality event in Alicante (Spain, Western Mediterranean). J. Invertebr. Pathol. 148, 14–19. doi: 10.1016/j.jip.2017.05.006

PubMed Abstract | CrossRef Full Text | Google Scholar

de Gaulejac, B. (1993). Étude Écophysiologique du Mollusque Bivalve Méditerranéen Pinna nobilis L.: Reproduction; Croissance; Respiration. Ph.D. thesis, Université d'Aix-Marseille III, Marseille, 220.

Dégremont, L., Garcia, C., and Allen, S. K. (2015). Genetic improvement for disease resistance in oysters: a review. J. Invertebr. Pathol. 131, 226–241. doi: 10.1016/j.jip.2015.05.010

PubMed Abstract | CrossRef Full Text | Google Scholar

Deudero, S., Grau, A., Vázquez-Luis, M., Álvarez, E., Alomar, C., and Hendriks, I. E. (2017). Reproductive investment of the pen shell Pinna nobilis Linnaeus, 1758 in Cabrera National Park (Spain). Mediterr. Mar. Sci. 10, 1–14. doi: 10.12681/mms.1645

CrossRef Full Text | Google Scholar

Deudero, S., Vázquez-Luis, M., and Álvarez, E. (2015). Human stressors are driving coastal benthic long-lived sessile fan mussel Pinna nobilis population structure more than environmental stressors. PLoS ONE 10:e0134530. doi: 10.1371/journal.pone.0134530

PubMed Abstract | CrossRef Full Text | Google Scholar

Elston, R. A., Moore, J. D., and Brooks, K. (1992). Disseminated neoplasia of bivalve molluscs. Rev. Aquat. Sci. 6, 405–466.

Google Scholar

Fey, S. B., Siepielskic, A. M., Nussléd, S., Cervantes-Yoshidad, K., Hwand, J. L., Huberd, E. R., et al. (2015). Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. Proc. Natl. Acad. Sci. U.S.A. 112, 1083–1088. doi: 10.1073/pnas.1414894112

PubMed Abstract | CrossRef Full Text | Google Scholar

Garcia-March, J. R., Jiménez, S., Sanchis, M. A., Monleon, S., Lees, J., Surge, D., et al. (2016). In situ biomonitoring shows seasonal patterns and environmentally mediated gaping activity in the bivalve, Pinna nobilis. Mar. Biol. 163, 1–12. doi: 10.1007/s00227-016-2812-3

CrossRef Full Text | Google Scholar

Garrabou, J., Coma, R., Bensoussan, N., Bally, M., Chevaldonne, P., Cigliano, M., et al. (2009). Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Chang. Biol. 15, 1090–1103. doi: 10.1111/j.1365-2486.2008.01823.x

CrossRef Full Text | Google Scholar

Grizel, H., Bachère, E., Mialhe, E., and Tigé, G. (1986). “Solving parasite-related problems in cultured molluscs,” in Parasitoloy, Quo vadit? Proceedings of the 6th International Congress of Parasitology, ed M. J. Howell (Canberra: Australian Academy of Science), 301–308.

Google Scholar

Guallart, J., and Templado, J. (2012). Pinna nobilis. En: VV.AA., Bases ecológicas preliminares para la conservación de las especies de interés comunitario en España: Invertebrados. Madrid: Ministerio de Agricultura, Alimentación y Medio Ambiente.

Hendriks, I. E., Tenan, S., Tavecchia, G., Marba, N., Jorda, G., Deudero, S., et al. (2013). Boat anchoring impacts coastal populations of the pen shell, the largest bivalve in the Mediterranean. Biol. Conserv. 160, 105–113. doi: 10.1016/j.biocon.2013.01.012

CrossRef Full Text | Google Scholar

Katsanevakis, S. (2007). Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): a generalized additive modelling approach. Mar. Biol. 152, 1319–1331. doi: 10.1007/s00227-007-0781-2

CrossRef Full Text | Google Scholar

Lande, R. (1993). Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142, 911–927.

Google Scholar

Lemer, S., Buge, B., Bemis, A., and Giribert, G. (2014). First molecular phylogeny of the circumtropical bivalve family Pinnidae (Mollusca, Bivalvia): evidence for high levels of cryptic species diversity. Mol. Phylog. Evol. 75, 11–23. doi: 10.1098/rspb.2016.0857

PubMed Abstract | CrossRef Full Text | Google Scholar

Lemer, S., González, V. L., Bieler, R., and Giribet, G. (2016). Cementing mussels to oysters in the pteriomorphian tree: a phylogenomic approach. Proc. R. Soc. B 283:20160857.

PubMed Abstract | Google Scholar

Maeno, Y., Suzuki, K., Yurimoto, T., Kiyomoto, S., Fuseya, R., Fujisaki, H., et al. (2012). Laboratory and field studies on gill and kidney associated virus in the pen shell Atrina lischkeana (Mollusca: Bivalvia). Bull. Eur. Assess. Fish Pathol. 32, 78.

Google Scholar

Maeno, Y., Yurimoto, T., Nasu, H., Ito, S., Aishima, N., Matsuyama, T., et al. (2006). Virus-like particles associated with mass mortalities of the pen shell Atrina pectinata in Japan. Dis Aquat Org. 71, 169–173. doi: 10.3354/dao071169

PubMed Abstract | CrossRef Full Text | Google Scholar

Pairaud, I. L., Bensoussan, N., Garreau, P., Faure, V., and Garrabou, J. (2014). Impacts of climate change on coastal benthic ecosystems: assessing the current risk of mortality outbreaks associated with thermal stress in NW Mediterranean coastal areas. Ocean Dynamics 64, 103–115. doi: 10.1007/s10236-013-0661-x

CrossRef Full Text | Google Scholar

Peters, E. C. (1988). Recent investigations on the disseminated sarcomas of marine bivalve molluscs. Am. Fish Soc. Spec. Publ. 18, 74–92.

Prado, P., Caiola, N., and Ibáñez, C. (2014). Habitat use by a large population of Pinna nobilis in shallow waters. Sci. Mar. 78, 555–565. doi: 10.3989/scimar.04087.03A

CrossRef Full Text | Google Scholar

Reed, D., O'Grady, J., Ballou, J., and Frankham, R. (2003). The frequency and severity of catastrophic die-offs in vertebrates. Anim. Conserv. 6, 109–114. doi: 10.1017/S1367943003003147

CrossRef Full Text | Google Scholar

Richardson, C. A., Peharda, M., Kennedy, H., Kennedy, P., and Onofri, V. (2004). Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determined from Mg:Ca and Sr:Ca shell profiles. J. Exp. Mar. Biol. Ecol. 299, 1–16. doi: 10.1016/j.jembe.2003.08.012

CrossRef Full Text | Google Scholar

Ruiz, J. M., Bernardeau-Esteller, J., García-Muñoz, M. R., and Ramos Segura, A. (2016). Red de seguimiento de las praderas de P. oceanica y cambio climático de la Región de Murcia: 2004-2015. Instituto Español de Oceanografía, Centro Oceanográfico de Murcia. Available online at: http://www.repositorio.ieo.es/e-ieo/handle/10508/10139

Schultz, P. W., and Huber, M. (2013). Revision of the worldwide Recent Pinnidae and some remarks on fossil European Pinnidae. Acta Conch. 13, 1–164.

van Banning, P. (1991). Observations on bonamiosis in the stock of the European flat oyster, Ostrea edulis, in the Netherlands, with special reference to the recent developments in Lake Grevelingen. Aquaculture 93, 205–211. doi: 10.1016/0044-8486(91)90232-V

CrossRef Full Text | Google Scholar

Vázquez-Luis, M., Borg, J. A., Morell, C., Banach-Esteve, G., and Deudero, S. (2015). Influence of boat anchoring on Pinna nobilis: a field experiment using mimic units. Mar. Freshw. Res. 66, 786–794. doi: 10.1071/MF14285

CrossRef Full Text | Google Scholar

Vázquez-Luis, M., March, D., Álvarez, E., Álvarez-Berastegui, D., and Deudero, S. (2014). Spatial distribution modelling of the endangered bivalve Pinna nobilis in a Marine Protected Area. Mediterr. Mar. Sci. 15, 626–634. doi: 10.12681/mms.796

CrossRef Full Text | Google Scholar

Vicente, N., and Moreteau, J. C. (1991). “Statust of Pinna nobilis L. en Méditerranée (Mollusque Eulamellibranche),” in Les Espèces Marines à Protèger en Méditerranée, eds C. F. Boudouresque, M. Avon, and M. Garvez (Marseille: GIS Posidonie Publ.), 159–168.

WoRMS (2014). World Register of Marine Species 2014. Available online at: http://www.marinespecies.org at VLIZ (Accessed 2014-10-20).

Young, T. (1994). Natural die-offs of large mammals - implications for conservation. Conserv. Biol. 8, 410–418. doi: 10.1046/j.1523-1739.1994.08020410.x

CrossRef Full Text | Google Scholar

Zavodnik, D., Hrs-Brenko, M., and Legac, M. (1991). “Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea,” in Les Espèces Marines à Protéger en Méditerranée, eds C. F. Boudouresque, M. Avon, and V. Gravez (Marseille: Gis Posidonie Publ.), 169–178.

Keywords: Pinna nobilis, Pinnidae, bivalve, mass mortality events, parasite, Haplosporida, Pinna rudis

Citation: Vázquez-Luis M, Álvarez E, Barrajón A, García-March JR, Grau A, Hendriks IE, Jiménez S, Kersting D, Moreno D, Pérez M, Ruiz JM, Sánchez J, Villalba A and Deudero S (2017) S.O.S. Pinna nobilis: A Mass Mortality Event in Western Mediterranean Sea. Front. Mar. Sci. 4:220. doi: 10.3389/fmars.2017.00220

Received: 09 May 2017; Accepted: 27 June 2017;
Published: 17 July 2017.

Edited by:

Stelios Katsanevakis, University of the Aegean, Greece

Reviewed by:

Lotfi Rabaoui, Tunis El Manar University, Tunisia
Paolo Magni, Consiglio Nazionale Delle Ricerche (CNR), Italy
Vasileios Bakopoulos, University of the Aegean, Greece

Copyright © 2017 Vázquez-Luis, Álvarez, Barrajón, García-March, Grau, Hendriks, Jiménez, Kersting, Moreno, Pérez, Ruiz, Sánchez, Villalba and Deudero. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Maite Vázquez-Luis, maite.vazquez@ba.ieo.es