Dr. Urzúa-Osorio, Ángel

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.

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.

The integrated biochemical condition (IBC) of gonads is closely related to the reproductive success of highly migratory marine species. The IBC of gonads can be influenced not only by size and/or age, but also by environmental conditions. Here, female swordfish, Xiphias gladius, that migrate to temperate regions with a marked seasonality (e.g., the Southeastern Pacific Ocean, SEPO) were compared in relation to the IBCs (lipids, proteins, glucose and, fatty acid profiles) of their gonads; individuals with two body size ranges and distinct degrees of sexual maturity were evaluated, and considered as: small and/or virginal (SV: <170 cm lower jaw fork-length (LJFL), oocyte size (OS) <0.08 mm) vs large and/or maturing females (LM: >190 cm LJFL, OS >0.133 mm). This comparison was conducted in two environmentally contrasting seasons (winter vs spring). Our results showed that the gonadosomatic index (GSI) was significantly higher in LM than SV. Lipid contents varied significantly between seasons and body sizes. The highest lipid concentrations were recorded in the spring in large females. No significant differences were found when comparing the protein and glucose contents of the two evaluated seasons or body size ranges of the studied females. In turn, the fatty acid (FA) profiles of female gonads significantly varied for both seasons and body size ranges. A high content of saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs) and poly-unsaturated fatty acids (PUFAs) were recorded in female gonads in the spring. The SFAs C16:0 and C18:0, the MUFA C18:1n9, and the essential PUFA C22:6n3 were the main contributors to the observed differences between spring and winter. These results could be used as indicators of the nutritional condition and health status of swordfish individuals. Hence, the IBC of female swordfish gonads have great potential to aid in estimating survival rates and stock abundances of this species. The integration of this information constitutes an asset in fishery management models with an ecosystem approach.

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 systems deliver nutrient-rich water into coastal ecosystems, influencing primary productivity and potentially altering seaweed-herbivore interactions. Upwelling bottom-up effects on distinct trophic levels are wellknown. However, their influence on seaweed biomolecules and on algae-herbivore interactions and growth are less known. The aim of this study was threefold: i) to compare physical-chemical characteristics and nutrient levels in the water of upwelling (U) and downwelling (DU) zones, ii) to quantify their influence on the content of protein and carbohydrates in seaweed tissues of representative U and DU locations, and iii) to experimentally assess their effect on the feeding behavior and growth of a prominent intertidal herbivore, the sea urchin Loxechinus albus. Waters from U zones showed lower temperatures and pH, and higher phosphate concentrations than those from downwelling zones. Similarly, the tissue of seaweeds from a U location had significantly more proteins and carbohydrates than those from a DU location. The origin location of the sea urchins had a significant influence on consumption and growth rates: in general, those coming from a site with U conditions consumed and grew more than those coming from DU conditions. The quality of the algae was a significant factor on consumption rates, although in the case of preference trials, this factor interacted with sea urchin origin location. Our results show that the availability and quality of the food in upwelling zones has an influence on herbivore-seaweed direct interactions. However, these interactions and the growth of the sea urchins were also related to the coastal site and conditions from which the sea urchins came from. These results are relevant considering the expected impact of climate change on the world's oceans, and the importance of U zones as thermal (cold water) refuges for marine ectotherms.

Marine-derived nutrients (MDN) contained in gametes (mature eggs and sperm), carcasses and metabolic wastes from anadromous migratory salmon can transfer energy and materials to fresh water, thereby affecting the structure and function of stream ecosystems. This is crucial among ecosystems where humans have mediated biological invasions by propagating non-native species. Previous studies have demonstrated that consumption of MDN from salmon can benefit both native and invasive resident fishes. Yet, a more detailed understanding of the transfer of biomolecules with important physiological functions such as ω-3 highly unsaturated fatty acids (HUFAs) have received less attention among researchers. Here we demonstrate that consumption of MDN contained in invasive Chinook salmon eggs transfers ω-3 HUFAs (e.g., EPA and DHA) to resident invasive rainbow trout in a river food web. We conducted a field study in river sections previously identified as spawning areas for Chinook salmon in the Cisnes River, Patagonia. Rainbow trout were sampled around salmon spawning areas before, during, and after the salmon spawning season. Additionally, we collected tissue from different food web resources and components of different origin (e.g., primary producers, aquatic and terrestrial items) from the Cisnes River system. Analyses of stomach contents of trout were performed in conjunction with analyses of both lipid content and fatty acid profiles of trout tissue and food web components. Chinook salmon eggs showed higher content of ω-3 HUFAs, especially EPA (31.08 ± 23.08 mg g DW−1) and DHA (27.50 ± 14.11 mg g DW−1) than either freshwater or terrestrial components (0–6.10 mg g DW−1 both EPA and DHA). We detected marked shifts in the fatty acid profile (~six-fold increase in EPA and DHA) of trout following consumption of Chinook salmon eggs. Our findings suggest that MDN via consumption of salmon eggs by resident rainbow trout may positively influence resident trout and likely contribute to gauge synergistic interactions between invaders on receiving ecosystems of Patagonia.

In marine invertebrates, the bioenergetic fuel available for fundamental physiological processes (growth, reproduction) may present intra-individual variability depending on the storage organ, sex and state of sexual maturity. This variability is considered relevant information for fishery management. In the squid Dosidicus gigas, an important fishery resource, we analyzed adult males (immature vs. mature) and females (immature I vs. immature II) off the coast of Chile. Their bioenergetic fuel (protein, glucose, lipid and fatty acid content-FAs) was quantified in different organs of the body (digestive gland, gonad and mantle). When comparing the organs of males at both stages of maturity, a greater amount of glucose and lipids were observed in the digestive gland than in the gonad and mantle, while a higher protein content was recorded in the gonad. In turn, the same tendency of biochemical variations among the organs was observed for the female at both stages. Regarding the FA profiles of the analyzed organs, the digestive gland had the highest mean proportion of FAs. However, no significant differences were observed related to sex and sexual maturity. According to the multivariate analyses for both sexes and maturity stages, the FA profiles of the mantle and gonad showed overlap and a high similarity, while the profile of the digestive gland was completely dissimilar. Our findings indicate that D. gigas from Chilean coastal waters showed, mainly in the digestive gland, high levels of all biochemical constituents, which are obtained through food and stored in their organs as bioenergetic fuel, and may then be used for the subsequent process of migration and reproduction in oceanic waters.