Mass mortality of pen shell Atrina maura (Bivalvia: Pinnidae) due to abrupt population increase of tunicate (Distaplia sp.) in a subtropical bay, Mexico

Highlights

• Protection of Atrina maura increased substrate availability facilitating an abrupt population growth of tunicate Distaplia. cf. stylifera.

• The coverage of D. cf. stylifera, salinity, sea surface temperature and dissolved oxygen concentration were related with A. maura mass mortality.

• Coverage of the tunicate D. cf. stylifera decreased from 2016 to 2017 likely associated with storms that decreased salinity.

• Increased distance among pen shell banks and harvesting at the first signs of tunicate population growth can avoid significant economic losses.

Abstract

The present study analyses the coverage of epibiont Distaplia cf. stylifera (Ascidiacea: Holozoidae) and five environmental variables (Sal, SST, DO, sea surface Chl-a concentration and pH) as potential factors to explain a mass mortality event in a restored population of the pen shell Atrina maura (Bivalvia: Pinnidae) in a subtropical bay of the Gulf of California, Mexico. Annual autumn surveys in 2015, 2016 and 2017 (Nov–Dec) and an additional summer survey in 2016 (Jun) showed that the tunicate was first observed at low densities in a few sampling sites during 2015 and rapidly expanded along the pen shell banks in 2016. Tunicate manual removal was carried out in two small areas during Sep-Nov 2016 and Jan–Mar 2017. The mass mortalities of A. maura detected in 2016 and 2017 resulted in a high economic loss for regional fishers. A Generalised additive model (GAM) indicated that the substrate provided by A. maura was the only significant factor associated to the rapid expansion (measured as the proportion of coverage) of D. cf. stylifera. Paradoxically, the recovery success in the A. maura population increased substrate availability for the tunicate epibiont, facilitating an abrupt and fast colonisation process on the pen shell banks, resulting in A. maura mass mortality events in 2016 and 2017. Our model predicts that D. cf. stylifera coverage effects begin to occur when the density of A. maura is > 47 inds./250 m². A second GAM demonstrated that the main driver of A. maura mortality was ascidian coverage, and salinity, SST and DO were secondary driver factors. We concluded that the density of dead A. maura increases when the coverage of D. cf. stylifera is >8%, salinity >37.3 PSU, SST <26.9 °C and DO > 5.06 mg O₂/L. Early harvesting of A. maura to decrease substrate availability at the first signs of D. cf. stylifera population growth can avoid significant economic losses in the future.

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.