RESEARCH ARTICLE Frequency, Magnitude, and Possible Causes of Stranding and Mass-Mortality Events of the Beach Clam Tivela mactroides (Bivalvia: Veneridae) Alexander Turra1, Maíra Pombo1, Marcelo Petracco2*, Eduardo Siegle1, Mariana Fonseca3, Márcia R. Denadai1,3 1 Instituto Oceanográfico, Universidade de São Paulo, São Paulo, São Paulo, Brazil, 2 Faculdade de Oceanografia, Instituto de Geociências, Pós-Graduação em Ecologia, Universidade Federal do Pará, Belém, Pará, Brazil, 3 Centro Universitário Módulo, Caraguatatuba, São Paulo, Brazil * [email protected] OPEN ACCESS Abstract Citation: Turra A, Pombo M, Petracco M, Siegle E, Stranding combined with mass-mortality events of sandy-beach organisms is a frequent but Fonseca M, Denadai MR (2016) Frequency, little-understood phenomenon, which is generally studied based on discrete episodes. The Magnitude, and Possible Causes of Stranding and frequency, magnitude, and possible causes of stranding and mass-mortality events of the Mass-Mortality Events of the Beach Clam Tivela mactroides (Bivalvia: Veneridae). PLoS ONE 11(1): trigonal clam Tivela mactroides were assessed based on censuses of stranded individuals, e0146323. doi:10.1371/journal.pone.0146323 every four days from September 2007 through December 2008, in Caraguatatuba Bay, Editor: Fabiano L. Thompson, Universidade Federal southeastern Brazil. Stranded clams were classified as dying (closed valves did not open do Rio de Janeiro, BRAZIL when forced) or dead (closed valves were easily opened). Information on wave parameters Received: December 23, 2014 and the living intertidal clam population was used to assess possible causes of stranding. This fine-scale monitoring showed that stranding occurred widely along the shore and year- Accepted: December 16, 2015 round, with peaks interspersed with periods of low or no mortality. Dead clams showed Published: January 8, 2016 higher mean density than dying individuals, but a lower mean shell length, attributed to a Copyright: © 2016 Turra et al. This is an open higher tolerance to desiccation of larger individuals. Wave height had a significant negative access article distributed under the terms of the relationship to the density of dying individuals, presumed to be due to the accretive nature Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any of low-energy waves: when digging out, clams would be more prone to be carried upward medium, provided the original author and source are and unable to return; while larger waves, breaking farther from the beach and with a stron- credited. ger backwash, would prevent stranding in the uppermost areas. This ecological finding Data Availability Statement: The data are available highlights the need for refined temporal studies on mortality events, in order to understand at https://datadryad.org/resource/doi:10.5061/dryad. them more clearly. Last, the similar size structure of stranded clams and the living popula- 402rr. tion indicated that the stranded individuals are from the intertidal or shallow subtidal Funding: This study was supported by the Fundação zone, and reinforces the ecological and behavioral components of this process, which de Apoio à Pesquisa do Estado de São Paulo (FAPESP, Proc. no. 05/60041-6). We also thank have important ecological and socioeconomic implications for the management of this FAPESP for the “Programa Jovem Pesquisador em population. Centro Emergente” grant awarded to M.R.D. (FAPESP Proc. no. 06/57575-1). Logistical support was provided by the Instituto Costa Brasilis – Desenvolvimento Sócio-Ambiental and also by the Centro Universitário Módulo. PLOS ONE | DOI:10.1371/journal.pone.0146323 January 8, 2016 1/13 Mass-Mortality Events of the Beach Clam Tivela mactroides Competing Interests: The authors have declared Introduction that no competing interests exist. Stranding and mass mortality on the shore are common events for many invertebrate groups, and their frequency, extent, and duration have been increasingly reported in recent decades [1–3]. These events are attributed to several factors, such as storms, positive sea-temperature anomalies, parasitism, harmful algal blooms, and hypoxia [1,2,4–12]. Despite the ecological importance of these processes, data on the frequency and magnitude of stranding and mass- mortality events of invertebrates are generally limited in time, probably because of the sudden and generally episodic occurrence of this phenomenon [2,3,13], for sandy-beach clams in par- ticular [2,9,10,13–17]. Mass mortality of sandy-beach clams has important ecological implica- tions because it can affect the density of these frequently dominant populations, altering the structure of the benthic community [18,19], as well as the organisms that rely on this food source [20]. In extreme cases, mass mortality can decimate clam populations along their geo- graphical range, as reported for the yellow clam Mesodesma mactroides and the surf clam M. donacium [9,11,21–23]. In addition, in view of the high importance of sandy-beach clams in recreational and artisanal fisheries of developing countries in South America, mass-mortality events of these organisms can be socioeconomically significant [18,22,24–26]. The trigonal clam Tivela mactroides is an important sandy-beach species, both economically and ecolog- ically [20,27–34]. It has a wide distribution from Venezuela to Brazil (Pará to Santa Catarina states) and in the West Indies [35]. This suspension-feeder inhabits the intertidal and subtidal zones of sandy beaches, where it is often the dominant macrofaunal component [28,36–38]. The trigonal clam frequently reaches high abundance in Venezuelan beaches, where it is an important resource of artisanal fisheries [28,30,31]. On these tropical beaches, no studies of mass mortality of the trigonal clam have been conducted, although there are brief notes on observations made under conditions of strong winds and waves [28]. The population of the tri- gonal clam living in the intertidal zone of sandy beaches in Caraguatatuba Bay, southeastern Brazil, has continuous recruitment, high individual growth and mortality rates, and reaches high levels of density, biomass and secondary production [32,33]. On several occasions, large numbers of stranded clams were observed in the intertidal zone of these beaches, and these mass strandings were presumed to be related to population density-dependent processes such as individual growth and mortality rates [32]. Also for this population, an assessment of har- vesting intensity showed that under ordinary conditions, the amount of clams harvested yearly is about 25 tons. The same study showed that the mass-mortality events are also socioeconomi- cally important, since a decrease in harvesting was attributed partly to these events [34]. The authors suggested that the foul odor and unpleasant sight caused by the stranded and dead clams were responsible for a decrease in recreational use of the beaches in Caraguatatuba Bay. Mass-mortality events can have dramatic effects on fishing and management of natural resources [11,22]. Moreover, some physical changes related to global climate change can increase the frequency and severity of mass-mortality episodes on sandy beaches [9,11]. In view of these considerations, assessment of mortality events of T. mactroides is a crucial step in managing populations of this species. Among the many possible causes of mortality are aspects of the population dynamics such as overpopulation, competition for resources, and parasitism, but also physical features, since these clams live under harsh conditions, depending largely on the characteristics of the sedi- ment where they burrow and on the wave energy across the shore [9,11,17,32]. Wave energy has a high potential to transport sediment as well as individual clams, while the sediment con- ditions may favor or preclude their burrowing and survival [39]. In fact, shoreward passive migration of small-sized clams was hypothesized to explain spatial partitioning between small (subtidal) and large (intertidal and shallow subtidal) individuals [37]. PLOS ONE | DOI:10.1371/journal.pone.0146323 January 8, 2016 2/13 Mass-Mortality Events of the Beach Clam Tivela mactroides The present study aimed to shed some light on stranding and mass-mortality events of these beach clams, by assessing their frequency, magnitude and possible causes for the popula- tion of T. mactroides in Caraguatatuba Bay. A comprehensive study was carried out on stranded individuals, both dying and dead, at a 4-day temporal scale during 15 months. The concomitant physical and biological conditions were assessed in relation to the stranding events. Given the general importance of hydrodynamics for mortality events on sandy beaches [40], wave parameters were considered in order to test the hypothesis that these are related to the number or size of stranded individuals. Similarly, the data for intertidal-living buried indi- viduals, obtained by Turra et al. [32], were also included as a potential factor influencing the structure of stranded individuals, i.e., if the density or size of the stranded clams is related to the respective parameters of the buried intertidal individuals. Material and Methods Study area and sampling The coastline of Caraguatatuba Bay (23°37’S to 23°44’S and 45°24’W to 45°26’W) in southeast- ern Brazil is about 16 km long and is uninterrupted by physical barriers. The sandy beaches in the study area have a gentle slope (1/33-1/41 m), a wide surf zone (ca 150 m), fine to very fine sand (0.8–1.12 mm), and waves predominantly with a period of 6 s and height of 0.4 m [32,33,37]. The mortality of Tivela mactroides was assessed in a 4-km area of the central-southern por- tion of the bay. This area was selected because intertidal densities of this clam are higher in this part of the bay [32,37]. Sampling was carried out under license granted by the Instituto Brasi- leiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA-DIREN No. 08/2001), at four-day intervals from September 8, 2007 to December 3, 2008.