Assessment of risks produced by extreme events on commercially important bivalves

Resumo

One of the consequences of the global change predicted by the climatic models is an increase in the frequency of the occurrence of extreme events such as heat waves and torrential rains. Among such models, the regional climatic projections of the Fifth Report of Evaluation of the IPCC and of the project EURO-CORDEX show that in the atlantic coast of Europe there will be very likely more frequent heat waves, longer in duration and greater in intensity, as well as increases in the intensity and frequency of extreme precipitations by 2099 (Christensen et al. 2013; Jacob et al. 2014). These modifications in the climate affect species and modify coastal habitats. In particular, the pronounced fluctuations in salinity and temperature during the extreme events can have significant impacts on the biogeochemical processes in the water and in the sediments, affecting physiological condition and metabolic function of species (Ringwood and Keppler 2002; Grilo et al. 2011; Parada et al. 2012). Given their ecological and socioeconomic importance, negative effects of climate change in coastal marine ecosystems, especially estuaries, are a major focus of interest. Potential dramatic impacts of climate change include changes in structure and functioning of communities including provision of ecosystem services (Harley et al. 2006; Grilo et al. 2011). Depending on the conditions of each site and of the moment in which the stress conditions happen, the effects can be of different intensity. Environmental stress may also drive episodes of mass mortality depending on the species, life cycle or spatio-temporal context (Garrabou et al. 2009; Grilo et al 2011). This is of special concern when the affected species support important fisheries (Parada et al. 2012; Macho et al. 2016) with huge socioeconomic costs (de Coo 2008). The largest artisanal fishery in Spain in terms of landings and employability is developed in Galicia, NW Iberian Peninsula (Macho et al. 2013; www.pescadegalicia.com). The native clams Ruditapes decussatus (Linnaeus, 1758) (almeixa fina) and Venerupis corrugata (Gmelin, 1791) (ameixa babosa), the introducided Ruditapes philippinarum (Adams and Reeve, 1850) (almeixa xaponesa) and the cockle Cerastoderma edule (Linnaeus, 1758) represented in the last years almost 80% of the total bivalve landings and more than 85% of the market value for bivalves (www.pescadegalicia.com). These species are clearly fundamental for the success of the intertidal and low subtidal artisanal shellfisheries. They are also important components of the sedimentary ecosystem (Macho et al. 2016). Although diverse studies have investigated the characteristics of these species, few studies have dealt with the ecophysiological effects of extreme events. It is known that the four species differ in their reproductive and life cycle (Villaba et al. 1993; Rodríguez-Moscoso e Arnaiz 1998; Delgado e Pérez-Camacho 2007; Molares et al. 2008). For example, C. edule is a fast-growing species with a scattered spawning, while R. decussatus presents a slower growth rate and has massive spawnings. The optimal environmental conditions also differ between species. While V. corrugata has a low tolerance to oscillations in salinity (reaching almost 100% mortality at salinities as low as 10) and temperature (Molares et al. 2008), R. decussatus is more resistant because it can tolerate short periods of low salinity down to 6, although it still cannot survive longer periods at salinities below 20 (Molares et al. 2008). The optimal temperature for R. decussatus is aproximately 20 °C, and above 27 °C it starts showing stress signals (Sobral and Widdows 1997). In occasions in which ambient temperature rises above 35 °C, great mortality rates of this species are registered (Sobral e Widdows 1997). The optimum salinity range for C. edule is 20-25, with critical values below 10 (Verdelhos et al. 2015). Mortality episodes (up to 60%) due to temperature are also associated with the development of the pathogen Perkinsus spp. (Molares et al. 2008). The Asiatic clam R. philippinarum was introduced because its growth rate is elevated and is considered resistant to environmental changes, although it presents some degree of mortality after 6 days of exposure to low salinity below 14, reducing metabolic activity at temperatures above 25 ℃ (Kang et al. 2016; Nie et al. 2016). Previous research by our research group investigated the resistance of the three clam species to temperatures typical of heat waves registered in the rias and the results indicated that R. philippinarum was more resistant compared to the two native species (Macho et al. 2016). As a consequence, the abundance of these fishery resources is very variable, depending of the conditions of each ria and shellfish bed (river outflow, type of sediment, degree of exposure...) and of climate. For example, the proximity of the shellfish beds to river mouths, most times related to the productivity due to the organic matter input, increases the risk due to extreme events of low salinity. The ability of estuarine species to respond to salinity variations through different behavioural and physiological mechanisms may determine the maintenance of populations, and this is relatively unknown, particularly in the context of climate change. Besides, it is expected that at the the Galician rias latitude, as across the southern European coast, heatwaves will increase in duration and frequency, impacting coastal ecosystems. Especially, intertidal organisms that already live near their tolerance limits and those organisms with lower mobility inhabiting sediments will be the most affected by abrupt changes of temperature. They may, however, bury deeper to mitigate the effects of heat. For these reasons, modifications in physiology and behaviour of these species are expected. Generally, shellfish beds that are located in the inner part of the rias and appear in elevated areas respect to the tidal level, with longer exposure time outside water, are likely more sensitive to the effects of extreme events. The studied species, both native and introduced, are natural habitants of estuaries and, therefore, are used to cope with natural variations within their tolerance ranges, at individual or population level. The reiteration of extreme events may put in danger their resistance with consequences for the productivity of shellfish beds. Field data validate the variability in abundances of species. The strongest precipitation events from the last decades were registered in the autumn-winter of 2000-2001, which drove into massive mortality episodes of bivalves in shellfish beds. Such events were so strong that prevented those resources from being exploited during an entire year (Parada e Molares 2008). In the subsequent years, more periods of heavy rain were registered. For example, the conditions derived from heavy rains in the winter of 2013-2014 caused a great mortality of clams in beds of Ría de Vigo, Ría de Arousa and Ría de Pontevedra (Mariño, Pereira, Pastoriza, pers. obs.). These events produced evident economic loses and, as a response, the development for measurements and experimental plans to recover the production (ex: Parada et al. 2006). However, the environmental stress not only provokes mortality in the short term, but can also induce sublethal effects in bivalves. For example, reducing the growth or physiological condition and development and reproductive output, or increasing the vulnerability to disease or predation (Petes et al. 2007; Sanford 2002; Wang et al. 2011). Whereas a greater vulnerability to predators can translate into an increase in mortality at medium and long term, smaller growth rates potentially increase the time for bivalves to reach commercial size. Moreover, a lower reproductive development reduces the production of released gametes causing a lower recruitment, with further consequences on the replenishment of shellfish beds (Beukema and Dekker 2005). Such fluctuations facilitated the progressive introduction of the Manila clam in the shellfish beds, which is, at present, the most cultivated bivalve species worldwide (FAO 2018). Due to this change in the productivity of species, it is important to understand how extreme events can affect both the native and introduced species in the present and predicted conditions in the near future along the Galician coast. The evidence in literature suggests that the introduced species may be more resistant and that, some of the native species may have reduced its area of distribution (Sobral and Widdows 1997; Aranguren et al. 2014; Macho et al. 2016). The general hypothesis of this thesis is that the effects of extreme phenomena of low salinities and high temperatures related to climate change will be greater for species living preferentially in the middle intertidal than those in the deeper intertidal. In addition, stress due to these events will have stronger negative effects on native species than on the introduced one. This thesis investigated the main stressors produced by extreme events, with proven potential to affect bivalve species throughout the seasons. Heavy rains that can increase in fall, winter, or spring and heat waves during the summer were reproduced in laboratory conditions at each season. The results obtained were related to the known reproductive stage of the species and to their different life strategies and ecophysiological traits. The first chapter addresses the main aspects related to frequent climatic phenomena known and projected by climatological models, which affect shellfish beds. Descriptions of the main expected changes in relation to global climate change and the possible impact on marine ecosystems are presented. Moreover,similar predictions and implications for shellfish in Galicia are detailed. A brief description of the history and organization of the practice of artisanal shellfish in Galicia is offered, as well as a description of the main catch patterns of the species studied. The second chapter details the results of three laboratory experiments where the response of the four species to low salinity events was determined. Specifically, the short-term sublethal effects of different salinity variations occurring in shellfish beds, whose intensity depends mainly on the proximity of beds to river mouths, were investigated. Physiological (growth potential or Scope for Growth, SFG) and behavioural responses (valve closure and burrowing activity) were measured. To measure and quantify the responses, bivalves were first exposed to simulated tidal cycles and salinities similar to those found on field. Specifically, four salinity ramps (variation from 5 to 20, 10 to 25, 15 to 30 and one control without variation, with natural salinity) were reproduced for six consecutive days. In addition, the experiment was repeated under the same conditions at three different times of the year (autumn, winter and spring), in order to be able to relate the responses to the state of reproductive development of each species. The overall response was the same for all species under the lowest salinities (5, 10, and 15), showing a sharp reduction in filtering activity, due to generalized valve closure during the higher stress, which led to a similar reduction in SFG, and in parallel of the re-burrowing capacity. Results were more differentiated between species when measured after salinity recovery on each of the ramps (20, 25, and 30). While C. edule was the most affected species in autumn, showing no recovery despite having higher SFG compared to the venerids, R. decussatus was more resistant in all seasons despite having the lowest SFG compared to the rest of species. In winter, V. corrugata was the one that showed the highest vulnerability due to lower SFG at lower salinities. All species showed a pattern of compensation in spring that led to nonrecovery of individuals. Burrowing capacity followed patterns similar to those of the SFG in autumn and winter, but differed in spring, when recovery was the general pattern. Decreased re-burrowing capacity at low salinities during stress observed to some extent in all species may increase vulnerability to predation. The results suggest that differential responses of lower activity over time could be related to the physiological condition and habitat preferences of each species and should be taken into account for future management plans, in the context of climate change. The results also serve to drive a discussion on the usefulness of calculating SFG as an index to assess salinity stress in adult bivalves and the possibility of varying the frequency and duration of stress in future research, as well as analysing the effects in conjunction with other variables, such as the amount of food available or the acidification of water, which may affect the growth of bivalve shells. The third chapter details the results of a laboratory experiment in which the response of the four species of bivalves to events of high atmospheric temperatures was determined. Heatwaves can produce high sediment temperatures if low tides coincide with maximum daily temperatures. Similar to low salinity experiments, physiological (SFG) and behavioural responses (valve closure and re-burrowing activity) were measured. Mortality was also measured and analysed, as notable percentages were recorded in some of the species. Specifically, the lethal and sublethal effects of heat during low tide in the laboratory were investigated by replicating temperature rises experienced in the intertidal, recorded in shallow sediments at a depth of approximately 2 cm (20 ℃ -control-, 27 ℃, 32 ℃ and 37 °C) for four consecutive days. In addition, the diffusion of heat to the burial depth of each species was estimated to get an idea of the actual temperature that each species can experience. The effect of temperatures was analysed by calculating the exposure as degree hours above 22 °C, because it is considered that not only the maximum exposure temperatures affect the physiology of the species, but also the duration of the exposure (Jones et al. 2009; Mislan et al. 2014). After only two days of exposure during low tides, C. edule and V. corrugata suffered significant mortality in the two treatments of higher temperatures, and also the most dramatic decrease in their SFG, in addition to the reduction in burrowing activity. After four days under stress, all species had negative SFG at the highest exposures, and mortality continued to increase in varying proportions for both C. edule and V. corrugata, and surprisingly also for R. philippinarum, which during exercise suffered a massive spawning. At the time of recovery, species showed compensation in their filtration rates to higher exposures, particularly C. edule. These effects of temperature on mortality, growth potential, and burrowing capacity can increase the time to achieve commercial size and exposure to predators and can clearly leave all species negatively affected. In particular, V. corrugata, which has its distribution center at lower intertidal and subtidal levels, and C. edule, which lives more superficially in sediment can be the most affected. It is very likely that the projected increase in heat wave intensity and frequency will affect these key species in intertidal shellfish beds, changing ecosystem functioning and fisheries management strategies. The results also serve to drive a discussion on the usefulness of using SFG as an index to assess temperature stress in adult bivalves, or the calculation of degree hours to consider acumulated exposure. Besides, it is discused the possibility of varying the frequency and duration of stress in future research, as well as analysing the effects in conjunction with other variables, such as salinity, food availability or acidification. The fourth chapter details the results of a laboratory experiment in which the resistance to predators of three of the studied species (V. corrugata, C. edule, R. philippinarum) subjected to low salinity stress was determined. Bivalves in their early life stages suffer a high mortality due to depredation. It was investigated whether stress due to low salinity could negatively affect populations. To do this, groups of bivalves buried in sediment were exposed to low salinities (5, 10 and 30 –control-) for two consecutive days and then exposed to one of the two most common types of predators on shellfish beds, namely the crab Carcinus maenas (Linnaeus, 1758) and the gastropod mollusc Bolinus brandaris (Linnaeus, 1758), which is a non-native species present in some shellfish beds in Galicia for decades. Both are known voracious bivalve consumers (Bañón et al. 2008, 2019; Smallegange and van der Meer 2003). Two types of choice experiments were performed: 1) one offering each predator the same prey species previously exposed to one of the three salinities, and 2) the other offering each predator all three species of prey at the same time previously exposed to one of the three salinities. Consumption of both predators and predatory behaviour of C. maenas was measured (e.g., handling time, rejections, consumption rate). Predation rates and behaviour differed among predators, with B. brandaris being more generalist than C. maenas. However, both predators clearly consumed more prey when stressed (salinities 5 and 10) than non-stressed prey. The overall consumption of the native species C. edule and V. corrugata was greater than that of R. philippinarum, probably due to its vulnerability to low salinity and its physical traits that favour the predator (ex: thinner shell, presence of gaps in the valves). Increased rainfall may therefore alter salinity gradients in shellfish beds and affect the dynamics of bivalve populations by changing predator-prey interactions. In this case, the results serve to drive a discussion about the usefulness of the different behavioural variables measured to analyse the predation risk in bivalves. In the fifth chapter, the results were related to the historical records of catches presented in the introduction, trying to respond to variations in each of the species and relating the results to the available literature. Furthermore, the main results were synthesised to be presented in conceptual models that can serve as a tool for the management of these resources, and as a basis to produce predictive models relating this eco-physiological information with the conditions that can be found in each bed depending on the climatic conditions. Additionally, a series of recommendations and ideas are given for future lines of research derived from the results obtained and the main conclusions of the experiments carried out are summarised.