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.

Marine trophodynamics refer to the transfer of energy from prey to predators. In marine invertebrates and fishes, the nutrients obtained through the consumption of food and/or prey are stored as energy reserves in certain tissues and/or organs including the liver, muscle, or gonads, and that these are subsequently used as bioenergetic fuel for highly energy-demanding fundamental physiological processes. In the southern Humboldt Current System, the interaction between two highly migratory resources and top species has been observed: the swordfish (Xiphias gladius) and its prey the jumbo squid (Dosidicus gigas). Because of this trophic interaction, these species store large amounts of energy (as lipids and fatty acids) in their main organs. However, how the fatty acid profile varies in the various organs of the predator and its prey is still unknown, as is its potential use as trophic biomarkers and the ecophysiological role it plays. Our results showed a moderate similarity between the fatty acid profile of the digestive gland of D. gigas with the profiles of the liver, gonad, and muscle of X. gladius, particularly with fatty acids: palmitic (C16:0), stearic (C18:0), oleic (C18:1n9), gadoleic (C20:1), EPA (C20:5n3), and DHA (C22:6n3). Our findings on the use of fatty acids as biomarkers of the interaction between two highly migratory species in the southern Humboldt System may reveal the degree of preference swordfish have for preying on jumbo squid, particularly through the consumption of the digestive gland. In both species, a high bioenergetic fuel content characterized by a predominance of saturated, monounsaturated, and polyunsaturated fatty acids may be necessary to sustain the high energy costs involved in their migratory and reproductive processes in the Humboldt Current system.

The traceability of fish species and their resulting food products is essential to maintain the global supply of these goods, allowing us to distinguish and reconstruct the origin and history of their production chain. One way to trace food is through biochemical determinations, which aid in identifying their geographical origin quickly. This study analyzed the fatty acid (FA) profiles of highly migratory fishery resource species (HMRS) from the Southeastern Pacific Ocean (SEPO), and their use as potential tools to determine the geographic origin and nutritional condition of these marine resources. The fatty acids (FAs) presented in fillet or muscle tissue of 18 HMRS were measured as FA methyl esters by gas chromatography. Our results reveal that the swordfish Xiphias gladius presented the greatest variety of FAs, strongly characterized by the presence of saturated, monounsaturated, and polyunsaturated FAs. A similar trend of high diversity in all classes of FAs was observed in tuna species (i.e., Thunnus alalunga; T. albacares; T. obesus), oilfish (Ruvettus pretiosus) and escolar fish (Lepidocybium flavobrunneum). In turn, Lampris guttatus, Makaira indica, and Tetrapturus audax presented an intermediate variety of FAs and the highest amount of saturated and monounsaturated FAs of the evaluated species. Finally, Luvarus imperialis, Coryphaena hippurus and the sharks (Lamna nasus; Alopias vulpinus; Prionace glauca; Isurus oxyrinchus; Sphyrna zygaena) presented a low diversity of FAs, with only saturated FAs strongly predominating. Regarding the total concentration of FAs, the highest average values were recorded in X. gladius, L. flavobrunneum and R. pretiosus. The present study revealed notable differences in the FA compositions of the muscle of diverse HMRS from the SEPO off the coast of Chile, with the swordfish showing the healthiest FAs (i.e., mono and polyunsaturated) for human consumption. The data on FAs collected for HMRS could be used as a reference to characterize the FA profiles of other fisheries in the SEPO (e.g., coastal pelagic fishes). In an ecosystem approach, our findings help us to understand how essential nutrients (i.e., FA biomolecules) are transferred through the marine food web in the SEPO, revealing the diet type and/or feeding habits of HMRS considered as top predators. Furthermore, identifying the FA profiles of fishery resources at a spatial level provides crucial information for their management and conservation, particularly in those resources that are overexploited and also have a critical nutritional importance for human consumption.

Parasites can alter the reproductive performance of their hosts, and to avoid or mitigate the resulting fitness loss, hosts may increase their current reproductive output to compensate for the future loss due to the parasitic infection. Fecundity compensation can be exploited by parasites for their own transmission (exploitation of host compensatory responses by parasites). However, this phenomenon has rarely been reported in second intermediate hosts of trematodes and its mechanisms and consequences largely unexplored. Along the east coast of the South Pacific, the second intermediate host, the mollusk Fissurella crassa, has been observed to display higher muscular foot, greater shell length and weight, and a higher gonadosomatic index when parasitized by metacercariaes of Proctoeces humboldti compared to non-parasitized hosts. In this study, we examined the histology, biochemistry (glucose, lipids, and proteins), and levels of sex hormones (estradiol and progesterone) in both parasitized and non-parasitized female individuals of F. crassa. Our findings revealed that the gonad of parasitized limpets had a higher density of oocytes, but these had a smaller individual area. Additionally, the gonadal tissue of parasitized limpets exhibited lower glucose content but higher lipid content. Notably, the levels of progesterone increased with parasite intensity. These results suggest that F. crassa possesses the ability to compensate for the negative effects of parasites by increasing the number of oocytes through biochemical and hormonal mechanisms. Our study contributes to the limited research on the impact of metacercariae on the reproduction of second intermediate hosts. Furthermore, we discuss how these changes in parasitized limpets could benefit parasite transmission.

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.

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.

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 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.

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.

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.