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.
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Gaitan-Espitia, J. D., Bacigalupe, L. D., Opitz, T., Lagos, N. A., Timmermann, T., & Lardies, M. A. (2014). Geographic variation in thermal physiological performance of the intertidal crab Petrolisthes violaceus along a latitudinal gradient. J. Exp. Biol., 217(24), 4379–4386.
Abstract: Environmental temperature has profound effects on the biological performance and biogeographical distribution of ectothermic species. Variation of this abiotic factor across geographic gradients is expected to produce physiological differentiation and local adaptation of natural populations depending on their thermal tolerances and physiological sensitivities. Here, we studied geographic variation in whole-organism thermal physiology of seven populations of the porcelain crab Petrolisthes violaceus across a latitudinal gradient of 3000 km, characterized by a cline of thermal conditions. Our study found that populations of P. violaceus show no differences in the limits of their thermal performance curves and demonstrate a negative correlation of their optimal temperatures with latitude. Additionally, our findings show that high-latitude populations of P. violaceus exhibit broader thermal tolerances, which is consistent with the climatic variability hypothesis. Interestingly, under a future scenario of warming oceans, the thermal safety margins of P. violaceus indicate that lower latitude populations can physiologically tolerate the ocean-warming scenarios projected by the IPCC for the end of the twenty-first century.
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Garcia-Huidobro, M. R., Poupin, M. J., Urrutia, C., Rodriguez-Navarro, A. B., Grenier, C., Vivanco, J. F., et al. (2021). An intrapopulational study of organic compounds and biomechanical properties of the shell of the Antarctic bivalve Laternula elliptica (P. P. King, 1832) at King George Island. Polar Biol., 44, 1343–1352.
Abstract: Laternula elliptica is a key bivalve species and widely distributed around the Antarctic continent. This bivalve has been the study subject in several studies centered on ecological, physiological, biochemical, and behavioral patterns. However, little is known about the chemistry and the biomechanical properties of the shells of this mollusk. Here, we present the first report of the intra-population variability in the organic composition and mechanical properties of L. elliptica shells. Further, we analyze different morphological traits and their association with the metabolism of a population of L. elliptica from King George Island, Western Antarctic Peninsula. The summer metabolic rates and the hepatosomatic index values indicate good health conditions of this clam's population. Shell periostracum chemistry is quite similar to bivalves from temperate regions, but the relative amount of protein increased ca. five-fold in shells of L. elliptica. The microhardness is approximately 32% lower than in bivalves from temperate regions. Our characterization of the L. elliptica shells suggests that periostracum chemistry could be specially fitted to avoid shell carbon exposure to dissolution (e.g., in corrosive acidified seawater). In contrast, the reduction in shell hardness may result from prioritizing behavioral (burial) and shell repairing strategies to confront biological (predators) and physical disturbances (e.g., ice scouring). Similar studies in other Antarctic mollusks will help understand the role of shell structure and function in confronting projected climate changes in the Antarctic ocean.
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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.
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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., Arias, M. B., Poupin, M. J., Manriquez, P. H., Torres, R., Vargas, C. A., et al. (2014). Differential response to ocean acidification in physiological traits of Concholepas concholepas populations. J. Sea Res., 90, 127–134.
Abstract: Phenotypic adaptation to environmental fluctuations frequently occurs by preexisting plasticity and its role as a major component of variation in physiological diversity is being widely recognized. Few studies have considered the change in phenotypic flexibility among geographic populations in marine calcifiers to ocean acidification projections, despite the fact that this type of study provides understanding about how the organism may respond to this chemical change in the ocean. We examined the geographic variation in CO2 seawater concentrations in the phenotype and in the reaction norm of physiological traits using a laboratory mesocosm approach with short-term acclimation in two contrasting populations (Antofagasta and Calfuco) of the intertidal snail Concholepas concholepas. Our results show that elevated pCO(2) conditions increase standard metabolic rates in both populations of the snail juveniles, likely due to the higher energy cost of homeostasis. juveniles of C concholepas in the Calfuco (southern) population showed a lower increment of metabolic rate in high-pCO(2) environments concordant with a lesser gene expression of a heat shock protein with respect to the Antofagasta (northern) population. Combined these results indicate a negative effect of ocean acidification on whole-organism functioning of C. concholepas. Finally, the significant Population x pCO(2) level interaction in both studied traits indicates that there is variation between populations in response to high-pCO(2) conditions. (C) 2014 Elsevier BM. All rights reserved.
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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.
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Osores, S. J. A., Lagos, N. A., Martin, V. S., Manriquez, P. H., Vargas, C. A., Torres, R., et al. (2017). Plasticity and inter-population variability in physiological and life-history traits of the mussel Mytilus chilensis: A reciprocal transplant experiment. J. Exp. Mar. Biol. Ecol., 490, 1–12.
Abstract: Geographically widespread species must cope with environmental differences between habitats. Information concerning geographic variations in response to climate variability is critical because many morphological, life history and physiological traits show variation across space. Reciprocal transplant experiments have shown to be relevant to evaluate the role of phenotypic plasticity and potential local adaptation in ecophysiological responses when coping with environmental variability. In this study, we characterize through reciprocal transplant experiments the reaction norms of morphological, biochemical, physiological and life-history traits between two intertidal populations of the socioeconomically important mussel Mytilus chilensis, inhabiting contrasting local environments (estuarine vs coastal habitats). We found a gradient in phenotypic plasticity with plastic trait responses in metabolic, ingestion and clearance rates, and in HsP(70) gene expression, and some traits with responses more canalized as growth and calcification rates. This emphasizes that responses not only vary across different local populations but also in different traits in M. chilensis, thus it is difficult to establish an overall trend of the responses at integrated organismal level. Moreover, the synergistic interaction of factors such as salinity and carbonate system parameters evaluated make it necessary to study the response at the population level with emphasis on benthic species important in aquaculture. Finally, field studies such as this one are useful for documenting the patterns of traits variation that occur in nature, identifying possible causes of such variation, and generating testable hypotheses for future controlled experiments. (C) 2017 Elsevier B.V. All rights reserved.
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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.
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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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