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Benitez, S., Duarte, C., Opitz, T., Lagos, N. A., Pulgar, J. M., Vargas, C. A., et al. (2017). Intertidal pool fish Girella laevifrons (Kyphosidae) shown strong physiological homeostasis but shy personality: The cost of living in hypercapnic habitats. Mar. Pollut. Bull., 118(1-2), 57–63.
Abstract: Tide pools habitats are naturally exposed to a high degree of environmental variability. The consequences of living in these extreme habitats are not well established. In particular, little it is known about of the effects of hypercanic seawater (i.e. high pCO(2) levels) on marine vertebrates such as intertidal pool fish. The aim of this study was to evaluate the effects of increased pCO(2) on the physiology and behavior in juveniles of the intertidal pool fish Girella laevifrons. Two nominal pCO(2) concentrations (400 and 1600 patm) were used. We found that exposure to hypercapnic conditions did not affect oxygen consumption and absorption efficiency. However, the lateralization and boldness behavior was significantly disrupted in high pCO(2) conditions. In general, a predator-risk cost of boldness is assumed, thus the increased occurrence of shy personality in juvenile fishes may result in a change in the balance of this biological interaction, with significant ecological consequences. (C) 2017 Elsevier Ltd. All rights reserved.
Keywords: Carbon dioxide; Hypercapnic conditions; Physiology; Behavior; Intertidal pool; Fish
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Labra, F. A., San Martin, V. A., Jahnsen-Guzman, N., Fernandez, C., Zapata, J., Garcia-Huidobro, M. R., et al. (2022). Metabolic rate allometry in intertidal mussels across environmental gradients: The role of coastal carbonate system parameters in mediating the effects of latitude and temperature. Mar. Pollut. Bull., 184, 114149.
Abstract: We assess the role of direct and indirect effects of coastal environmental drivers (including the parameters of the carbonate system) on energy expenditure (MR) and body mass (M) of the intertidal mussel, Perumytilus pur-puratus, across 10 populations distributed over 2800 km along the Southern Eastern Pacific (SEP) coast. We find biogeographic and local variation in carbonate system variables mediates the effects of latitude and temperature on metabolic rate allometry along the SEP coast. Also, the fitted Piecewise Structural Equation models (PSEM) have greater predictive ability (conditional R2 = 0.95) relative to the allometric scaling model (R2 = 0.35). The largest standardized coefficients for MR and M were determined by the influence of temperature and latitude, followed by pCO2, pH, total alkalinity, and salinity. Thus, physiological diversity of P. purpuratus along the SEP coast emerges as the result of direct and indirect effects of biogeographic and local environmental variables.
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Lagos, N. A., Benitez, S., Duarte, C., Lardies, M. A., Broitman, B. R., Tapia, C., et al. (2016). Effects of temperature and ocean acidification on shell characteristics of Argopecten purpuratus: implications for scallop aquaculture in an upwelling-influenced area. Aquac. Environ. Interact., 8, 357–370.
Abstract: Coastal upwelling regions already constitute hot spots of ocean acidification as naturally acidified waters are brought to the surface. This effect could be exacerbated by ocean acidification and warming, both caused by rising concentrations of atmospheric CO2. Along the Chilean coast, upwelling supports highly productive fisheries and aquaculture activities. However, during recent years, there has been a documented decline in the national production of the native scallop Argopecten purpuratus. We assessed the combined effects of temperature and pCO(2)-driven ocean acidification on the growth rates and shell characteristics of this species farmed under the natural influence of upwelling waters occurring in northern Chile (30 degrees S, Tongoy Bay). The experimental scenario representing current conditions (14 degrees C, pH similar to 8.0) were typical of natural values recorded in Tongoy Bay, whilst conditions representing the low pH scenario were typical of an adjacent upwelling area (pH similar to 7.6). Shell thickness, weight, and biomass were reduced under low pH (pH similar to 7.7) and increased temperature (18 degrees C) conditions. At ambient temperature (14 degrees C) and low pH, scallops showed increased shell dissolution and low growth rates. However, elevated temperatures ameliorated the impacts of low pH, as evidenced by growth rates in both pH treatments at the higher temperature treatment that were not significantly different from the control treatment. The impact of low pH at current temperature on scallop growth suggests that the upwelling could increase the time required for scallops to reach marketable size. Mortality of farmed scallops is discussed in relation to our observations of multiple environmental stressors in this upwelling-influenced area.
Keywords: Calcification; Shell growth; Scallop farming; Upwelling; Chile
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Lagos, N. A., Benitez, S., Grenier, C., Rodriguez-Navarro, A. B., Garcia-Herrera, C., Abarca-Ortega, A., et al. (2021). Plasticity in organic composition maintains biomechanical performance in shells of juvenile scallops exposed to altered temperature and pH conditions. Sci. Rep., 11(1), 24201.
Abstract: The exposure to environmental variations in pH and temperature has proven impacts on benthic ectotherms calcifiers, as evidenced by tradeoffs between physiological processes. However, how these stressors affect structure and functionality of mollusk shells has received less attention. Episodic events of upwelling of deep cold and low pH waters are well documented in eastern boundary systems and may be stressful to mollusks, impairing both physiological and biomechanical performance. These events are projected to become more intense, and extensive in time with ongoing global warming. In this study, we evaluate the independent and interactive effects of temperature and pH on the biomineral and biomechanical properties of Argopecten purpuratus scallop shells. Total organic matter in the shell mineral increased under reduced pH (similar to 7.7) and control conditions (pH similar to 8.0). The periostracum layer coating the outer shell surface showed increased protein content under low pH conditions but decreasing sulfate and polysaccharides content. Reduced pH negatively impacts shell density and increases the disorder in the orientation of calcite crystals. At elevated temperatures (18 degrees C), shell microhardness increased. Other biomechanical properties were not affected by pH/temperature treatments. Thus, under a reduction of 0.3 pH units and low temperature, the response of A. purpuratus was a tradeoff among organic compounds (biopolymer plasticity), density, and crystal organization (mineral plasticity) to maintain shell biomechanical performance, while increased temperature ameliorated the impacts on shell hardness. Biopolymer plasticity was associated with ecophysiological performance, indicating that, under the influence of natural fluctuations in pH and temperature, energetic constraints might be critical in modulating the long-term sustainability of this compensatory mechanism.
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Lardies, M. A., Caballero, P., Duarte, C., & Poupin, M. J. (2021). Geographical Variation in Phenotypic Plasticity of Intertidal Sister Limpet's Species Under Ocean Acidification Scenarios. Front. Mar. Sci., 8, 647087.
Abstract: Ocean Acidification (OA) can have pervasive effects in calcifying marine organisms, and a better understanding of how different populations respond at the physiological and evolutionary level could help to model the impacts of global change in marine ecosystems. Due to its natural geography and oceanographic processes, the Chilean coast provides a natural laboratory where benthic organisms are frequently exposed to diverse projected OA scenarios. The goal of this study was to assess whether a population of mollusks thriving in a more variable environment (Talcaruca) would present higher phenotypic plasticity in physiological and morphological traits in response to different pCO(2) when compared to a population of the same species from a more stable environment (Los Molles). To achieve this, two benthic limpets (Scurria zebrina and Scurria viridula) inhabiting these two contrasting localities were exposed to ocean acidification experimental conditions representing the current pCO(2) in the Chilean coast (500 mu atm) and the levels predicted for the year 2100 in upwelling zones (1500 (mu atm). Our results show that the responses to OA are species-specific, even in this related species. Interestingly, S. viridula showed better performance under OA than S. zebrina (i.e., similar sizes and carbonate content in individuals from both populations; lower effects of acidification on the growth rate combined with a reduction of metabolism at higher pCO2). Remarkably, these characteristics could explain this species' success in overstepping the biogeographical break in the area of Talcaruca, which S. zebrina cannot achieve. Besides, the results show that the habitat factor has a strong influence on some traits. For instance, individuals from Talcaruca presented a higher growth rate plasticity index and lower shell dissolution rates in acidified conditions than those from Los Molles. These results show that limpets from the variable environment tend to display higher plasticity, buffering the physiological effects of OA compared with limpets from the more stable environment. Taken together, these findings highlight the key role of geographic variation in phenotypic plasticity to determine the vulnerability of calcifying organisms to future scenarios of OA.
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Manriquez, P. H., Jara, M. E., Torres, R., Mardones, M. L., Lagos, N. A., Lardies, M. A., et al. (2014). Effects of ocean acidification on larval development and early post-hatching traits in Concholepas concholepas (loco). Mar. Ecol.-Prog. Ser., 514, 87–103.
Abstract: Larval stages represent a bottleneck influencing the persistence of marine populations with complex life cycles. Concholepas concholepas is a gastropod species that sustains the most important small-scale artisanal fisheries of the Chile-Peru Humboldt Coastal current system. In this study, newly-laid egg capsules of C. concholepas collected from 3 localities along the Chilean coast were used to evaluate the potential consequences of projected near-future ocean acidification (OA) on larval development and early post-hatching larval traits. We compared hatching time, hatching success and early survivorship of encapsulated larvae reared under contrasting average levels of pCO(2): 382 (present-day), ca. 715 and ca. 1028 μatm CO2 (levels expected in near-future scenarios of OA). Moreover, we compared morphological larval traits such as protoconch size, thickness and statolith size at hatching. Some of the developmental traits were negatively affected by pCO(2) levels, source locality, female identity, or the interaction between those factors. Meanwhile, the effect of pCO(2) levels on morphological larval traits showed significant interactions depending on differences among egg capsules and females. Our results suggest that OA may decouple hatching time from oceanographic processes associated with larval transport and reduce larval survivorship during the dispersive phase, with a potential impact on the species' population dynamics. However, the results also show geographic variability and developmental plasticity in the investigated traits. This variation may lead to an increased acclimatization ability, facilitate the persistence of natural populations and mitigate the negative effects that OA might have on landings and revenues derived from the fishery of this species.
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Martel, S. I., Fernandez, C., Lagos, N. A., Labra, F. A., Duarte, C., Vivanco, J. F., et al. (2022). Acidification and high-temperature impacts on energetics and shell production of the edible clam Ameghinomya antiqua. Front. Mar. Sci., 9, 972135.
Abstract: Warming and ocean acidification are currently critical global change drivers for marine ecosystems due to their complex and irreversible effects on the ecology and evolution of marine communities. Changes in the chemistry and the temperature of the ocean impact the biological performance of marine resources by affecting their energy budget and thus imposing energetic restrictions and trade-offs on their survival, growth, and reproduction. In this study, we evaluated the interplaying effects of increased pCO(2) levels and temperature on the economically relevant clam Ameghinomya antiqua, an infaunal bivalve inhabiting a wide distributional range along the coast of Chile. Juvenile clams collected from southern Chile were exposed to a 90-day experimental set-up emulating the current and a future scenario projeced to the end of the current century for both high pCO(2)/low-pH and temperature (10 and 15 degrees C) projected for the Chilean coast. Clams showed physiological plasticity to different projected environmental scenarios without mortality. In addition, our results showed that the specimens under low-pH conditions were not able to meet the energetic requirements when increased temperature imposed high maintenance costs, consequently showing metabolic depression. Indeed, although the calcification rate was negative in the high-pCO(2) scenario, it was the temperature that determined the amount of shell loss. These results indicate that the studied clam can face environmental changes for short-term periods modifying energetic allocation on maintenance and growth processes, but with possible long-term population costs, endangering the sustainability of an important benthic artisanal fisheries resource.
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Navarro, J. M., Duarte, C., Manriquez, P. H., Lardies, M. A., Torres, R., Acuna, K., et al. (2016). Ocean warming and elevated carbon dioxide: multiple stressor impacts on juvenile mussels from southern Chile. ICES J. Mar. Sci., 73(3), 764–771.
Abstract: The combined effect of increased ocean warming and elevated carbon dioxide in seawater is expected to have significant physiological and ecological consequences at many organizational levels of the marine ecosystem. In the present study, juvenile mussels Mytilus chilensis were reared for 80 din a factorial combination of two temperatures (12 and 16 degrees C) and three pCO(2) levels (380, 700, and 1000 μatm). We investigated the combined effects of increasing seawater temperature and pCO(2) on the physiological performance (i.e. feeding, metabolism, and growth). Lower clearance rate (CR) occurred at the highest pCO(2) concentration (1000 μatm) compared with the control (380 μatm) and with the intermediate concentration of pCO(2) (700 μatm). Conversely, CR was significantly higher at 16 degrees C than at 12 degrees C. Significant lower values of oxygen uptake were observed in mussels exposed to 1000 μatm pCO(2) level compared with those exposed to 380 μatm pCO(2). Scope for growth (SFG) was significantly lower at the highest pCO(2) concentration compared with the control. Mussels exposed to 700 μatm pCO(2) did not show significantly different SFG from the other two pCO(2) treatments. SFG was significantly higher at 16 degrees C than at 12 degrees C. This might be explained because the experimental mussels were exposed to temperatures experienced in their natural environment, which are within the range of thermal tolerance of the species. Our results suggest that the temperature rise within the natural range experienced by M. chilensis generates a positive effect on the processes related with energy gain (i.e. feeding and absorption) to be allocated to growth. In turn, the increase in the pCO(2) level of 1000 μatm, independent of temperature, adversely affects this species, with significantly reduced energy allocated to growth (SFG) compared with the control treatment.
Keywords: high CO2; multiple stressors; mussels; ocean warming; scope for growth; thermal window
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Ramajo, L., Marba, N., Prado, L., Peron, S., Lardies, M. A., Rodriguez-Navarro, A. B., et al. (2016). Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification. Glob. Change Biol., 22(6), 2025–2037.
Abstract: Future ocean acidification (OA) will affect physiological traits of marine species, with calcifying species being particularly vulnerable. As OA entails high energy demands, particularly during the rapid juvenile growth phase, food supply may play a key role in the response of marine organisms to OA. We experimentally evaluated the role of food supply in modulating physiological responses and biomineralization processes in juveniles of the Chilean scallop, Argopecten purpuratus, that were exposed to control (pH similar to 8.0) and low pH (pH similar to 7.6) conditions using three food supply treatments (high, intermediate, and low). We found that pH and food levels had additive effects on the physiological response of the juvenile scallops. Metabolic rates, shell growth, net calcification, and ingestion rates increased significantly at low pH conditions, independent of food. These physiological responses increased significantly in organisms exposed to intermediate and high levels of food supply. Hence, food supply seems to play a major role modulating organismal response by providing the energetic means to bolster the physiological response of OA stress. On the contrary, the relative expression of chitin synthase, a functional molecule for biomineralization, increased significantly in scallops exposed to low food supply and low pH, which resulted in a thicker periostracum enriched with chitin polysaccharides. Under reduced food and low pH conditions, the adaptive organismal response was to trade-off growth for the expression of biomineralization molecules and altering of the organic composition of shell periostracum, suggesting that the future performance of these calcifiers will depend on the trajectories of both OA and food supply. Thus, incorporating a suite of traits and multiple stressors in future studies of the adaptive organismal response may provide key insights on OA impacts on marine calcifiers.
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Ramajo, L., Prado, L., Rodriguez-Navarro, A. B., Lardies, M. A., Duarte, C. M., & Lagos, N. A. (2016). Plasticity and trade-offs in physiological traits of intertidal mussels subjected to freshwater-induced environmental variation. Mar. Ecol.-Prog. Ser., 553, 93–109.
Abstract: Environmental gradients play an important role in shaping geographic variability in coastal marine populations. Thus, the ability of organisms to cope with these changes will depend on their potential to acclimatize, or adapt, to these new environmental conditions. We investigated the spatial variability in biological responses shown by Perumytilus purpuratus mussels collected from 2 intertidal areas experiencing contrasting freshwater input influences (river-influenced vs. marine conditions). To highlight the role of plasticity and adaptive potential in biological responses, we performed a reciprocal-transplant experiment and measured relevant phenotypic traits including mortality, growth, calcification, metabolism, and chemical composition of the shell periostra cum. We determined that mussels exposed to river-influenced conditions had increased metabolic rates and reduced growth rates, as compared to mussels experiencing marine conditions (p < 0.05). While the energy investment strategies of the 2 local populations resulted in similar net calcification rates, these rates decreased significantly when mussels were transplanted to the river-influenced site. Stressful conditions at the river-influenced site were evidenced by decreased survivorship across treatments. Freshwater inputs modify the organic composition of the shell periostracum through a significant reduction in polysaccharides. Although our field experiment did not identify specific environmental factors underlying these contrasting phenotypic changes, the results imply that plasticity plays a strong role when P. purpuratus is exposed to some combination of natural (e.g. salinity) and anthropogenic influences (e.g. pollution), and that the lack of exposure to freshwater may promote less tolerant mussels with greater potential for local adaptation.
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Ramajo, L., Rodriguez-Navarro, A. B., Duarte, C. M., Lardies, M. A., & Lagos, N. A. (2015). Shifts in shell mineralogy and metabolism of Concholepas concholepas juveniles along the Chilean coast. Mar. Freshw. Res., 66(12), 1147–1157.
Abstract: Along the west coast of South America, from the tropical zone to the Patagonian waters, there is a significant latitudinal gradient in seawater temperature, salinity and carbonate chemistry. These physical-chemical changes in seawater induce morphological and physiological responses in calcifying organisms, which may alter their energy budget and calcification processes. In this study, we study the organism energy maintenance (i.e. metabolic rate) and mineralogical composition of the shell of the juvenile marine snails Concholepas concholepas (Gastropoda: Muricidae), collected from benthic populations located similar to 2000km apart, varies across geographic regions along the Chilean coast. We found that in juvenile snails, the calcite:aragonite ratio in the pallial shell margin (i.e. newly deposited shell) increase significantly from northern to southern populations and this increase in calcite precipitation in the shell of juveniles snails was associated with a decrease in oxygen consumption rates in these populations. Our result suggests that calcite secretion may be favoured when metabolic rates are lowered, as this carbonate mineral phase might be less energetically costly for the organism to precipitate. This result is discussed in relation to the natural process such as coastal upwelling and freshwater inputs that promote geographic variation in levels of pH and carbonate saturation state in seawater along the Chilean coast.
Keywords: calcium carbonate; metabolism; ocean acidification; temperature
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Torres, R., Manriquez, P. H., Duarte, C., Navarro, J. M., Lagos, N. A., Vargas, C. A., et al. (2013). Evaluation of a semi-automatic system for long-term seawater carbonate chemistry manipulation. Rev. Chil. Hist. Nat., 86(4), 443–451.
Abstract: The assessment of the effects of Ocean Acidification (OA) on marine life has received increasing attention in recent marine research. On a mesocosmic scale, the CO2 levels in seawater can be manipulated to evaluate experimentally the consequences of OA on marine organisms (vertebrates and invertebrates). An ideal manipulation of carbonate chemistry should mimic exactly the changes to carbonate chemistry, which will occur in years to come. Although some methods have been described in the literature, here we describe in detail a simple, robust and inexpensive system to produce CO2-enriched seawater by bubbling the seawater with air-CO2 mixtures. The system uses mass flow controllers (MFC) to blend atmospheric air with pure CO2 to produce two pCO(2) levels. The air-CO2 mixtures are delivered continuously to seawater equilibration reservoirs, and simultaneously to an infrared CO2 analyser to verify CO2 levels in the air-CO2 mixture delivered to the equilibration tanks. We monitored both pH and total alkalinity in the equilibration reservoirs over a period of one year in order to document the long-term performance of this system for simulating the future carbonate chemistry of seawater in a coastal laboratory. System performance was sufficient to maintain three contrasting (e.g., 397, 709 and 1032 matm) and relatively constant (the coefficient of variability was 11 %, 9 % and 9 % respectively) seawater pCO(2) during a year-long monitoring.
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Vargas, C. A., Lagos, N. A., Lardies, M. A., Duarte, C., Manriquez, P. H., Aguilera, V. M., et al. (2017). Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol., 1(4), 7 pp.
Abstract: Global stressors, such as ocean acidification, constitute a rapidly emerging and significant problem for marine organisms, ecosystem functioning and services. The coastal ecosystems of the Humboldt Current System (HCS) off Chile harbour a broad physical-chemical latitudinal and temporal gradient with considerable patchiness in local oceanographic conditions. This heterogeneity may, in turn, modulate the specific tolerances of organisms to climate stress in species with populations distributed along this environmental gradient. Negative response ratios are observed in species models (mussels, gastropods and planktonic copepods) exposed to changes in the partial pressure of CO2 (p(CO2)) far from the average and extreme P-CO2 levels experienced in their native habitats. This variability in response between populations reveals the potential role of local adaptation and/or adaptive phenotypic plasticity in increasing resilience of species to environmental change. The growing use of standard ocean acidification scenarios and treatment levels in experimental protocols brings with it a danger that inter-population differences are confounded by the varying environmental conditions naturally experienced by different populations. Here, we propose the use of a simple index taking into account the natural p(CO2) variability, for a better interpretation of the potential consequences of ocean acidification on species inhabiting variable coastal ecosystems. Using scenarios that take into account the natural variability will allow understanding of the limits to plasticity across organismal traits, populations and species.
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