Dr. Urzúa-Osorio, Ángel

The physical-chemical variability of coastal upwelling creates a mosaic of environmental conditions that affect different levels of biological organization. Understanding the mechanisms that organisms use to cope with this variability is critical for addressing the challenges that climate change imposes on coastal ecosystems. This study integrates information on transcriptomic traits, metabolic performance, and the quantity of organic biomolecules in the intertidal fish Girella laevifrons from four locations with varying upwelling intensities. The results show that fish from locations with stronger upwelling intensity have higher levels of glucose, lipids, and proteins in their muscle tissue, in addition to better physiological performance compared to fish from sites with weaker upwelling intensity. Transcriptomic analyses revealed that genes associated with multicellular development and oxygen metabolism are more highly expressed in sites with stronger upwelling intensity, whereas genes related to protein ubiquitination are more expressed in sites with weaker upwelling intensity. In response to the mosaic of upwelling intensities (SAM-SST), and in-situ temperature, nutrients and oxygen variation observed in field, fish showed differential responses, suggesting local adaptations process that maximize ecological success in these areas with different physical-chemical conditions. Future studies should consider the integration of molecular tools to better understand the responses of organisms to environmental variability as upwelling intensities. This will help elucidate the complex interactions between environmental factors and biological responses, providing insights into how marine organisms might adapt to changing conditions. Understanding these mechanisms is essential for predicting the impacts of climate change on coastal ecosystems and for developing effective conservation and management strategies. The integration of transcriptomic data with metabolic and physiological performance measures offers a comprehensive approach to studying the adaptive responses of marine organisms to their dynamic environments considering the future responses in face to predict global change.

In this brief, non-exhaustive essay, we review major adaptive changes in reproductive and developmental traits of decapod crustaceans, which have passed through evolutionary transitions from ancestral life in coastal marine environments to brackish, limnic, polar, or deep-sea habitats. Two major approaches can be recognised in studies of life-history evolution, focussing on: (1) developmental changes in adaptive physiological or biochemical traits of successive ontogenetic stages, comparing, for instance, osmoregulatory capabilities in larvae, juveniles, and adults (“ontogeny of adaptations” perspective); (2) adaptive changes in the modes of reproduction and development, e.g., enhanced maternal energy investment in egg production, abbreviated, non-feeding larval development (“adaptations in ontogeny”). Using both scientific approaches, Christoph D. Schubart has significantly contributed to our understanding of evolutionary transitions in crustaceans. In our essay, we pay particular attention to the significance of nutritional selection factors in relation to presumably adaptive developmental, physiological, and biochemical traits in different life-history stages. In this context, we highlight the key roles of lipids and carotenoid pigments, in particular of essential polyunsaturated fatty acids (PUFAs) and astaxanthin. While PUFAs and other lipid compounds have received wide scientific attention, we propose that future studies should further analyse also the potential role of astaxanthin and other essential carotenoids.

In coastal Antarctic environments, glacial meltwater changes the nutrients and physicochemical parameters in the water column. Consequently, top-down cascading effects are triggered throughout the food web, which can affect the bioenergetic condition of benthic invertebrates and their coupling processes between energy levels and flows throughout the marine food web. In this study, two benthic polychaetes (Maldane sarsi antarctica and Notomastus latericeus), exposed to the impact of glacial melting over a broad time scale, were used to evaluate the effect of glacial meltwater on their bioenergetic condition through the integrated analysis of: i) their biochemical composition; ii) fatty acid profiles and iii) total energy contents. The findings indicate that glacial meltwater has a direct effect on the bioenergetic condition of polychaetes. In areas where glacial meltwater has a significant impact, N. latericeus showed higher levels of proteins and glucose, but lower levels of lipids. On the other hand, M. sarsi antarctica exhibited decreased protein content with increasing glacial meltwater impact. M. sarsi antarctica presented varying levels of lipids across different sites, with the highest concentrations observed in areas with moderate impact. Both species showed a reduction in fatty acids with increasing glacial meltwater impact. Additionally, M. sarsi antarctica individuals from highly impacted areas had lower energy levels than those from less impacted areas, while N. latericeus had higher energy levels in the most impacted site. This information enables the development of a framework for assessing the impact of climate change using glacial meltwater and the integrated bioenergetics of key benthic polychaeta as a proxy. Therefore, identifying how glacial meltwater affects their bioenergetic condition helps us understand how climate change could affect trophic interactions, structure, and energy flows in the Antarctic marine food web.

The producer of paralytic shellfish toxin (PST), Alexandrium catenella, is one of the main generators of HABs in the coasts of Chile. Its presence produces ecological and economic damage, directly affecting filter feeding organisms, and indirectly to other organism through the trophic chain. The objective of this research was to identify the effect of a toxic diet on the energetic and reproductive parameters of the carnivorous snail Chorus giganteus. Two groups of snails were used, one fed with toxic prey (bivalves fed with A. catenella), and the other fed with non-toxic prey. Both treatments were maintained under these conditions for 63 days, then, elemental composition (C, N) and energy content were estimated, and fecundity parameters were analyzed. The results indicate that snails fed with toxic prey had a lower percentage of C and C/N ratio. The energy content was significantly lower in intoxicated snails. Regarding fecundity parameters, a higher number of egg-masses were produced by toxic snails, however, only 62% of these showed embryonic development, with 57% hatching success. A negative relationship was identified between the mean PST concentration, quantified in snails, and the number of egg-masses produced per aquarium. In the aquarium where the snails had highest average PST concentration (1200 ± 820 μg STX.2HCL eq. Kg− 1) there was no oviposition, while egg-masses were only produced by snails in aquaria where the average concentration did not exceed 360 ± 160 μg STX.2HCL eq. Kg− 1. It is likely that, with low levels of accumulated PST, C. giganteus activates its oviposition process as a response to toxin-induced stress, generating a higher energy expenditure supported by a redirection of its reserves. However, when the intoxication presents higher levels, the reproductive process could be inhibited, similar to what has been identified in other molluscs.

The bioenergetic status of fishes has been used to study their physiological responses to temporal changes at interannual scales. We evaluated the physiological responses of swordfish at an interannual scale from the El Niño Southern Oscillation (ENSO): warm phase “El Niño” in 2015 to the cold phase “La Niña” in 2017 and under neutral conditions as well in 2019. Herein, muscle samples from females and males were analyzed to evaluate the bioenergetic status from their biochemical constituents (L: lipids, P: proteins and G: glucose, E: total energy, and FAs: fatty acid profile), elemental composition (C: carbon, N: nitrogen, H: hydrogen), and nutritional indices (L:P, C:N, DHA/C18:1n-3, DHA/C16:0 and ω3/ω6 FAs). The physiological response of swordfish showed an interaction between the year and sex. Herein, the L and E showed similar trends, with the lowest female values found in 2015 and the highest in 2019. Contrary, males showed their highest values in 2015 and lowest in 2019. FA profile differed among years and highlighted significant differences between females and males in 2019. Although the female L:P and C:N ratios were lower in 2015 than in 2017, a decreasing trend in these ratios was found from 2017 to 2019. Moreover, DHA/C18:1n-3, DHA/C16:0 and ω3/ω6 showed higher ratios in females than males in 2019. Our results coincide with the beginning of the ENSO phases; it is therefore likely that the swordfish diet changed in response to the disturbances in environmental conditions. Furthermore, the degree of individual dietary specialization found under the neutral conditions could indicate differences in the feeding behaviors of males vs. females, which may be an adaptive strategy in this species. These findings will aid in understanding the bioenergetic status of swordfish under different climatic scenarios and the current global warming, providing relevant information for the management of this resource.

Upwelling oceanographic phenomenon is associated with increased food availability, low seawater temperature and pH. These conditions could significantly affect food quality and, in consequence, the growth of marine species. One of the most important organismal traits is somatic growth, which is highly related to skeletal muscle. In fish, skeletal muscle growth is highly influenced by environmental factors (i.e. temperature and nutrient availability) that showed differences between upwelling and downwelling zones. Nevertheless, there are no available field studies regarding the impact of those conditions on fish muscle physiology. This work aimed to evaluate the muscle fibers size, protein content, gene expression of growth and atrophy-related genes in fish sampled from upwelling and downwelling zones. Seawater and fish food items (seaweeds) samples were collected from upwelling and downwelling zones to determine the habitat's physical-chemical variations and the abundance of biomolecules in seaweed tissue. In addition, white skeletal muscle samples were collected from an intertidal fish to analyze muscular histology, the growth pathways of protein kinase B and the extracellular signal-regulated kinase; and the gene expression of growth- (insulin-like growth factor 1 and myosin heavy-chain) and atrophy-related genes (F-box only protein 32 and muscle RING-finger protein-1). Upwelling zones revealed higher nutrients in seawater and higher protein content in seaweed than samples from downwelling zones. Moreover, fish from upwelling zones presented a greater size of muscle fibers and protein content compared to downwelling fish, associated with lower protein ubiquitination and gene expression of F-box only protein 32. Our data indicate an attenuated use of proteins as energy source in upwelling conditions favoring protein synthesis and muscle growth. This report shed lights of how oceanographic conditions may modulate food quality and fish muscle physiology in an integrated way, with high implications for marine conservation and sustainable fisheries management.

Swordfish (Xiphias gladius), a highly migratory fishery resource of great importance in the Southeastern Pacific Ocean (SEPO), is a species with late sexual maturation, high longevity, and a large body size that spawns and reproduces several times throughout its adulthood. In the present study, we hypothesized that the Biochemical-Ecological Composition (BEC) of the gonad (measured as the lipid, protein, glucose, and energy contents) and its bio-stoichiometric ratios (lipid/protein: L/P; lipid/ glucose: L/G) would be influenced by both female body size (lower jaw fork length in cm, LJFL: <180, 180–260, >260) and time (trimesters: 1,2,3; years: 2017, 2019). Our results revealed that in relation to their body size, female swordfish gonads varied significantly in their BEC, but not in their L/P and L/G ratios during their quarterly development within an annual cycle. These variations in the BEC were noticeable in females of medium (180–260) and larger (>260) sizes. Particularly, as the year progressed, females stored significant amounts of energy during their trophic migration, made evident by the increase in the lipid and protein contents of the gonads, which reached maximum levels towards the end of the year, during the second and third trimesters. These high energy reserves can be used for the reproduction during the last trimester of the year (i.e. austral spring–summer), when the warm temperature and high productivity in the SEPO are optimal for the successful development of oocytes. Future studies considering an ecosystem approach should analyze the classes of lipids and types of fatty acids that are involved in the reproduction of this species, and how they are acquired through the consumption of lipid-rich prey, and subsequently metabolized to be used in reproduction and during early ontogeny.

Microplastics are a widespread environmental contaminant. Although detrimental effects on aquatic organisms are well documented, little is known about the long-term effects of microplastic exposure to filter-feeding organisms at ecologically realistic levels. This study investigates the effects of environmentally relevant concentrations of polyethylene micro beads ranging in size from 3 to 30 μm, on the physiology and energetics of a coastal filter-feeding crab Petrolisthes laevigatus. We evaluated the impact of microplastics by exposing P. laevigatus to two different concentrations and exposure times: i) a chronic exposure for five months at 250 particles L−1, and ii) an acute exposure for 48 h at 20,800 particles L−1, ~80 times higher than the chronic exposure. The results showed that only chronic exposures elicited negative effects on the coastal crab in both, metabolic and physiological parameters. Our findings demonstrate a strong correlation between the ingestion rate and weight loss, even at low concentrations, the crabs exhibited severe nutritional damage as a result of long-term microplastic exposure. By contrast, acute exposure revealed no significant effects to the crabs, a possible explanation for this being short-term compensatory responses. These results suggest that environmentally relevant concentrations of microplastics are harmful to marine organisms, and they should be evaluated during realistic temporal scales, as their effects strongly dependent on the exposure time. Our results also suggest that the effects of microplastics have been likely underestimated to date, due to the dominance of short-term exposures (acute) reported in the current literature.

The estuarine crab Hemigrapsus crenulatus has a wide distribution range along the coast of the South Pacific Ocean (from 20 °S to 53 S°). This decapod is abundant in these coastal and estuarine habitats and plays a key ecological role as prey of the snook fish (Eleginops maclovinus) and kelp gull (Larus dominicanus). Its diet consists of detritus, dead fish, and crustaceans, and the macroalgae Ulva sp. In response to contrasting environmental conditions and anthropogenic impacts along the Chilean coast, H. crenulatus may present intraspecific variations in its reproductive traits and changes in the elemental composition of its embryos, directly affecting its biological fitness. Along the Chilean coast, female individuals were collected during late spring 2019 and early summer 2020 (from November 2019 to February 2020) in six areas of Chile (north: Tongoy (30°S); south-central: Lenga (36°S), Tubul (37°S); south austral: Calbuco (41°S), Castro (42°S), Quellón (43°S). The environmental conditions (i.e. sea surface temperature, precipitation and chlorophyll α) present during each sampling event were also recorded. We evaluated the reproductive parameters of females (fecundity, reproductive output (RO)) as well as their body size (carapace width and dry weight), volume, water content, dry weight, elemental composition (carbon, hydrogen, nitrogen: CHN), and finally the energy content of their embryos. Our results indicated that the environmental conditions of the sea water temperature, precipitation (proxy of water salinity) and chlorophyll α (proxy of food availability) have direct effects on the reproductive parameters of females and the characteristics of their embryos. We observed a low fecundity and high RO in Calbuco and Quellón, where precipitation was high (i.e. diluted salinity) and temperatures and productivity was low. For embryo traits, the highest values of volume and water content were observed in female crabs from the estuarine areas (i.e. Tongoy, Lenga, Tubul), values much higher than those found in the internal sea of Chile (i.e. Calbuco, Castro, Quellón). For the elemental composition, we observed high nitrogen levels and a low C:N proportion in embryos from female crabs from Lenga (a nitrogen enriched area). Fluctuating environmental variables among localities proved to modulate intraspecific variations in females and embryos of H. crenulatus, revealing different reproductive strategies, particularly in the quality and energy investment per embryo, which subsequently influenced successful embryogenesis and larval survival.

The temporal dynamics of energy reserves are associated with the physiological processes (i.e., reproduction) in marine fishes, in which storage organs play a key role for efficient energy investment. We evaluated the temporal (i.e., seasons) and intra-individual (i.e., organs) dynamics of adult female swordfish (Xiphias gladius) during its feeding period off the Chilean coast in the southeastern Pacific Ocean (SEPO). The biochemical composition (i.e., lipids, proteins, and glucose), energy content and fatty acid profile of the muscle, liver and gonad were evaluated during the austral autumn, winter, and spring. Our results showed principally an intra-individual effect in both the muscle and liver in the autumn and spring. Herein, a trend of higher amounts of lipids and total energy were found in the muscle, while the liver showed greater protein and glucose contents. Consequently, the muscle showed a higher saturated, monounsaturated, and polyunsaturated fatty acid contents than the liver. Although the gonad showed no significant temporal effect in the lipids and proteins contents, an increasing trend of each biochemical constituent, fatty acid group and gonadosomatic index were found from autumn to winter. Consistently, the glucose and total energy content as well Fulton's condition factor were significantly higher in winter. These findings reflect the spatial-temporal physiological dynamic of swordfish based on the storage of energy reserves in different organs during its feeding period. In this way, the products obtained from swordfish could have an added value depending on the season and capture zone, which could benefit the exploitation and regulation measures of this resource under an ecological approach of conservation and sustainability in the SEPO.