Mass mortality of pen shell Atrina maura (Bivalvia: Pinnidae) due to abrupt population increase of tunicate (Distaplia sp.) in a subtropical bay, Mexico
Introduction
Pen shells of the genus Atrina have a high commercial value and, both living or dead, provide substrate and shelter for motile species and for the settling of invertebrate larvae (Munguia, 2004; 2007). Tunicates commonly inhabit as epibionts of bivalves, competing for food and in some cases causing death of the bivalves due to suffocation (Petersen, 2007). When tunicates invade bivalve farms, they can decrease body mass and/or population growth, weaken the shell or cause mass mortality events, resulting in further economic losses (Góngora-Gómez et al., 2016; Lins and Rocha, 2020). Tunicate overpopulation frequently affects mussel and oyster farms. Multiple peaks of abundance of several tunicate species were observed in Prince Edward Island (Canada), starting with Styela clava Herdman, 1881 in 1997, followed by Botryllus schlosseri Pallas, 1766 in 2001, Botrylloides violaceus Oka, 1927 in 2002 and Ciona intestinalis (Linnaeus, 1767) in 2004 (Ramsay et al., 2008). Although the colonial botryllids (B. schlosseri and B. violaceus) did not cause an evident negative ecological impact, S. clava and C. intestinalis competed for food and space with the farmed mussels (Thompson and MacNair, 2004; Comeau et al., 2015). The presence of solitary tunicate species competes with the mussels increasing between 30% and 47% the clearance rate per area compared to mussels without epibiont tunicates (Comeau et al., 2015). Overall, mussels with epibiont tunicates were considerably less efficient at retaining the picophytoplankton component than mussels without tunicates (Comeau et al., 2015). Seventeen tunicates species were observed in commercial shellfish farms during 10-years’ monitoring research in Brazil. Styela plicata (Lesueur, 1823) and Didemnum perlucidum Monniot F., 1983 were the most abundant tunicate species with the potential to become a threat to shellfish populations (Rocha et al., 2009). Ten out of thirteen species of the encrusting organisms on commercial oyster Crassostrea gigas (Thunberg, 1793) farms were exotic or even invasive ascidians in a temperate bay of Baja California, Mexico (Rodríguez and Ibarra-Obando, 2009). Ascidians colonised 40% of the C. gigas population after one year of monthly observation being positively correlated with sea water temperature (Rodríguez and Ibarra-Obando, 2009). Thus, climatic conditions appear to control ascidian population growth. The ascidian Polyclinum constellatum Savigny, 1816 also colonised several oyster farms on the east coast of the Gulf of California (Tovar-Hernández et al., 2010; 2013).
A natural population of the pen shell Atrina maura Sowerby, 1786 represents an economically relevant income for regional fishers of Ensenada de La Paz, a subtropical bay located on the southwest coast of the Gulf of California, Mexico (Fig. 1a–c) (Camacho-Mondragón et al., 2008; 2012; Camacho-Mondragón, 2009). A relocation programme within Ensenada de La Paz between 2011 and 2014 was carried out to restore the functionality and recovery of the previously 24 km2 overexploited banks of A. maura. This programme successfully increased the A. maura population from 74,706 pen shells in 2011 to 1,121,749 in 2014 (NOS, 2015). The present study documents an abrupt population increase of the epibiont tunicate Distaplia cf. stylifera (Kowalevsky, 1874) that resulted in a mass mortality event of the pen shell A. maura in 2016.
The aim of the present study was to investigate the effect of D. cf. stylifera population growth on the density of A. maura before, during and after a mass mortality event of A. maura first observed during summer 2016. Two hypotheses were tested to determine the main mechanistic cause of the abrupt increase in the D. cf. stylifera population size and its effects on the mortality of the A. maura population at Ensenada de La Paz, Baja California Sur, Mexico. The first hypothesis was to test if A. maura density (substrate availability) rather than environmental conditions (sea surface temperature, salinity, dissolved oxygen, pH, and sea surface Chlorophyll-a concentration) was the most relevant cause of D. cf. stylifera population growth on natural communities of A. maura. The second tested hypothesis was to determine the main biological and environmental factors related to the mortality of A. maura. An understanding of the tunicate coverage process and pen shell mortality will help to prevent such economically catastrophic events in the future and suggest improvements or alternative strategies to control tunicate populations on naturally occurring mollusc banks.
Section snippets
Area of study
A natural population of the pen shell A. maura covering an area of ~24 km2 in Ensenada de La Paz (24°07′59″ N, −110°25′1″ W) was monitored in a shallow habitat < 10 m depth along the tidal channel and shallower depths > 0.5 m in the inner areas exposed at low tide. Ensenada de La Paz sea floor has sandy to muddy-silty sediments and is connected to the Bahía de La Paz by a ~1 km wide channel (Espinoza, 1977) (Fig. 1a–c). The region has a semi-desert climate with rainfall mainly during summer
Results
Pilot observations of the A. maura population during autumn 2011, 2012, 2013 and 2014 did not show the presence of epibiont D. cf. stylifera (data not shown), which was first observed in low abundance in autumn 2015. An abrupt increase of the tunicate population during summer 2016 resulted in a massive mortality event of the A. maura population.
Discussion
Following the recovery of the economically valuable population of A. maura after several years of an active and successful restoration programme without harvesting at a subtropical bay, an abrupt and fast colonisation of the tunicate D. cf. stylifera resulted in a mass mortality event of the pen shell banks. Our results indicate that the main factors behind the abrupt growth of the tunicate during summer 2016 was, paradoxically, related to the availability of substrate provided by the pen
Conclusion
The image that emerges from our analysis is that the success in the recovery of the pen shell population was actually the main driver behind the explosive growth of the ascidian population, which resulted in a mass mortality event of the pen shells and major economic loss for fishers. The tunicate removal efforts carried out (177 MT wet weight extracted) was expensive, time consuming, spatially extremely limited, and it was overall ineffective. The tropical storms and hurricanes that seasonally
Author statement
Betzabé Moreno-Dávila: Methodology, developed formal data analysis, Writing – original draft. Leonardo Huato-Soberanis: Study design methodology, Formal analysis, Writing – original draft. Jaime Gómez-Gutiérrez, Teresa Alcoverro, Carlos Sanchez, Eduardo F. Balart: Writing – review & editing, Study design. Silvia Ramírez-Luna: Sampling design and Field sampling.
Funding
This work was supported by CONACyT 421011/263861 PhD scholarship to BBMD. JGG is an EDI-IPN, COFAA-IPN and JGG, CS and EFBP are SNI fellows.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We gratefully acknowledge Noroeste Sustentable A.C. (NOS) for granting us access to their database, and Organización de Pescadores al Rescate de la Ensenada (OPRE) for the intensive work of annual surveys of Atrina maura density and Distaplia cf. stylifera area coverage during 2011–2017. Also, to Rosana M. Rocha (Universida de Federal do Paraná, Brazil) for her support in the taxonomic identification of the ascidian species and her valuable comments. We deeply thank the critics and comments
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