Shifts in maternal foraging strategies during pregnancy promote offspring health and survival in a marine top predator.

The success of maternal foraging strategies during the rearing period can greatly impact the physiology and survival of dependent offspring. Surprisingly though, little is known on the fitness consequences of foraging strategies during the foetal period. In this study, we characterized variation in maternal foraging strategy throughout pregnancy in a marine top predator (South American fur seal, Arctocephalus australis), and asked if these shifts predicted neonatal health and postnatal survival. We found that during early pregnancy all pregnant females belonged to a single, homogenized foraging niche without evident clusters. Intriguingly though, during late pregnancy, individual fur seal mothers diverged into two distinct foraging niches characterized by a benthic-nearshore and a pelagic-offshore strategy. Females that shifted towards the benthic-nearshore strategy gave birth to pups with greater body mass, higher plasmatic levels of glucose and lower levels of blood urea nitrogen. The pups born to these benthic females were eight times more likely to survive compared to females using the pelagic-offshore foraging strategy during late pregnancy. These survival effects were mediated primarily by the impact of foraging strategies on neonatal glucose independent of protein metabolic profile and body mass. Benthic-nearshore foraging strategies during late pregnancy potentially allow for the greater maternal transfer of glucose to the foetus, leading to higher chances of neonatal survival. These results call for a deeper understanding of the balance between resource acquisition and allocation provided by distinct foraging polymorphisms during critical life-history periods, and how this trade-off may be adaptive under certain environmental conditions.

Lower marine productivity increases agonistic interactions between sea lions and fur seals in Northern Pacific Patagonia.

Interspecific interactions are key drivers of individual and population-level fitness in a wide range of animals. However, in marine ecosystems, it is relatively unknown which biotic and abiotic factors impact behavioral interactions between competing species. We assessed the impact of weather, marine productivity, and population structure on the behavioral agonistic interactions between South American fur seals (SAFSs), Arctocephalus australis, and South American sea lions (SASLs), Otaria byronia, in a breeding colony of SAFS. We hypothesized that agonistic interactions between SAFSs and SASLs respond to biotic and abiotic factors such as SAFS population structure, marine productivity, and weather. We found that SASL and SAFS interactions almost always resulted in negative impacts on the social structure or reproductive success of the SAFS colony. SASL adult males initiated stampedes of SAFS and/or abducted and predated SAFS pups. Adult SAFS males abundance and severe weather events were negatively correlated with agonistic interactions between species. However, proxies for lower marine productivity such as higher sea surface temperature and lower catches of demerso-pelagic fish were the most important predictors of more frequent agonistic interactions between SAFS and SASL. Under the current scenario of decline in marine biomass due to global climate change and overfishing, agonistic interactions between competing marine predators could increase and exacerbate the negative impacts of environmental change in these species.

Towards understanding the effects of oceanic plastic pollution on population growth for a South American fur seal (Arctocephalus australis australis) colony in Chile.

Entanglement of pinnipeds with plastic debris is an emerging conservation and animal welfare issue worldwide. However, the origins and long-term population level consequences of these entanglements are usually unknown. Plastic entanglement could produce a combination of wounds, asphyxiation, or inability to feed that results in the death of a certain percentage of individuals from the total population. In this research, we report on the consequent effect of plastic entanglement on population growth demographics in a South American fur seal (Arctocephalus australis australis) colony on Guafo Island, southern Chile. Using a stochastic matrix population model structured according to age and sex, and assuming an otherwise stable population, we explored population growth rates under five scenarios with differing rates of entanglement: A) a zero rate of plastic entanglement, B) entanglement rates (number of entangled individuals as a proportion of the total number of individuals) as observed in our study population (overall entanglement ratio of 1.2 × 10-3); and for the other scenarios, entanglement ratios as reported in the literature for other pinniped colonies around the world: C) 3.04 × 10-3, D) 4.42 × 10-2, and E) 8.39 × 10-2. Over the 30 years forecasting period and starting with a population size of ∼2950 individuals, the population growth rate was lower under all scenarios with rates of entanglement greater than zero (scenarios B-E). In comparison with scenario A, at the end of the 30-year period forecasted, we calculated a projected decrease in population size of between 20.34% (scenario B) and 91.38% (scenario E). These results suggest that even the lowest levels of entanglement in pinnipeds as reported in the literature might have significant effects over time on population-level dynamics. Our research offers potential insight when devising policy for the management and limitation of plastic pollution in the oceans, and indeed for the conservation and management policy of affected marine species. Furthermore, whilst there are some limitations to our methodology, it offers a straightforward and potentially useful approach for the standardized prediction of impacts at a population level of different rates of plastic pollution and entanglement and could be applied in distinct populations of the same species around the world.

Monitoring the occurrence of microplastic ingestion in Otariids along the Peruvian and Chilean coasts.

Repeated reports of microplastic pollution in the marine pinniped diet have emerged in the last years. However, only few studies address the drivers of microplastics presence and the potential implications for monitoring microplastic pollution in the ocean. This study monitored their in the scats (N = 205) of four pinniped species/subspecies at five different locations in the southern Pacific Ocean (Peru and Chile). Samples from all rookeries contained microplastics, and overall, 68% of the examined scats contained fragments/fibers, mostly blue colored. We confirmed that 81.5% of the fragments/fibers were anthropogenic in origin , but only 30% were polymers. Scats from Juan Fernández Archipelago presented higher microplastic concentrations than continental rookeries. Also, the common diet in each location may influence the levels found in the samples. This study presents a useful non-invasive technique to track plastic pollution in top predator diets as bioindicators for future surveillance/management plans applied to different location.

The influence of microplastics pollution on the feeding behavior of a prominent sandy beach amphipod, Orchestoidea tuberculata (Nicolet, 1849).

Pollution by microplastics has become a global threat affecting coastal habitats such as sandy beaches and their resident macrofauna. The goal of this study was to assess the influence of microplastics on the feeding behavior and growth rate of a widespread sandy beach amphipod, Orchestoidea tuberculata. These organisms were exposed to artificial food prepared with Poly(styrene-co-divinylbenzene) microspheres (8 µm particle size) at 3 different concentrations (0%, 5% and 10%). The amphipods consumed significantly more food when the concentration of microplastics was 0% and significantly less when the concentration was 10%, both in trials in which they had a choice (preference experiments) and those in which they did not have a food choice. In contrast to this, the amphipod's absorption efficiency and estimated growth rates were not significantly affected by the concentration of microplastics. Combined, these results indicate that high microplastics concentrations (e.g. 10%) cause a reduction in the amphipod's consumption rates and, indirectly, may affect the role of this species as a main consumer of stranded seaweeds in sandy beaches ecosystems.

Parasitism Elicits a Stress Response That Allocates Resources for Immune Function in South American Fur Seals (Arctocephalus australis).

Parasites can cause chronic stress in some animal species, and this type of stress response has been associated with adverse consequences for the host. In order to know whether parasitism elicited a stress response associated with decreased host fitness, hookworm (Uncinaria sp.) infection was studied in a colony of South American fur seals (Arctocephalus australis) in which hookworms infect nearly all pups born in a reproductive season. A parasite-free group was generated by treating a subset of pups with an antiparasitic drug before they developed patent hookworm infection. Stress and metabolic hormones, energy balance, and humoral and cellular immune parameters were measured in this group and hookworm-infected pups. Hookworms elicited a marked increase in plasma cortisol levels in fur seal pups. These hookworm-infected pups were able to maintain constant glucose levels, despite losing body mass over the course of infection potentially because of increased protein catabolism. Infected pups were able to mount an effective immune response against the parasite and eliminated hookworms from the intestine, recovering partial body mass lost as a result of hookworm infection at the end of the study period. As shown in previous studies, adequate glucose levels are critical for proper T lymphocyte reactivity, and it is possible that, through activation of a stress response, energy can be readily available for immune response against the parasite contributing to early recovery from infection. Although there are potential fitness costs to mounting a sustained stress response, these could also be adaptive and promote survival during critical life-history stages.

The contrasting hidden consequences of parasitism: Effects of a hematophagous nematode (Uncinaria sp.) in the development of a marine mammal swimming behavior.

Parasites are an important part of ecosystems, playing a critical role in their equilibrium. However, the consequences of parasitism beyond the direct effects associated with disease and mortality are not completely understood. This gap in knowledge is in part due to the difficulties to isolate the effect of single parasite species on physiological and behavioral traits in natural systems.The South American fur seal (Arctocephalus australis)-hookworm (Uncinaria sp.) interaction offers an ideal system to overcome these difficulties and study the behavioral and physiological effects of parasites in their hosts.Hookworms cause stunted growth and anemia in pinniped pups, which could affect early life active behaviors such as swimming. The aim of this study was to determine the effects of hookworms (Uncinaria sp.) on the development of swimming capabilities in A. australis through physiological and ethological analyses.Higher parasite burden was associated with reduced growth rates and lower blood hemoglobin concentrations, whereas scaled body mass and blood hemoglobin levels had an important positive effect on the water activity of the pups. However, antihookworm treatment did not affect the level of water activity of the pups, and pups with high hookworm burden increased their time budget in water. This was probably related to lower maternal attendance in heavily parasitized pups, leaving these pups more time to perform water activities. Therefore, pups with heavy hookworm burden, despite having decreased growth rates and blood hemoglobin concentrations, compensated for their handicap in physiological traits related to swimming by spending more time in the water.This work offers new insights to understand the contrasting effects of parasites on aquatic organisms, and the compensatory mechanisms employed by infected animals to avoid the worst consequences of parasitism.

Immune-mediated hookworm clearance and survival of a marine mammal decrease with warmer ocean temperatures.

Increases in ocean temperature are associated with changes in the distribution of fish stocks, and the foraging regimes and maternal attendance patterns of marine mammals. However, it is not well understood how these changes affect offspring health and survival. The maternal attendance patterns and immunity of South American fur seals were assessed in a rookery where hookworm disease is the main cause of pup mortality. Pups receiving higher levels of maternal attendance had a positive energy balance and a more reactive immune system. These pups were able to expel hookworms through a specific immune mediated mechanism and survived the infection. Maternal attendance was higher in years with low sea surface temperature, therefore, the mean hookworm burden and mortality increased with sea surface temperature over a 10-year period. We provide a mechanistic explanation regarding how changes in ocean temperature and maternal care affect infectious diseases dynamics in a marine mammal.

The life history strategy of a fur seal hookworm in relation to pathogenicity and host health status.

The strategies that parasites use to exploit their hosts can lead to adverse effects on human and animal populations. Here, we describe the life cycle, epidemiology, and consequences of hookworm (Uncinaria sp.) disease in South American fur seals (Arctocephalus australis), and propose that hookworm adaptation to fur seal life history traits has led to maximizing transmission at high levels of parasite-induced anemia and mortality. Fur seal pups acquire hookworms during their first days of life through their mothers' colostrum and most adult hookworms are expelled from the pups' intestine 30-65 days later. This gives hookworms little time to feed and reproduce. However, despite reaching high within-host densities, female hookworms do not decrease egg output, therefore pups with high hookworm burden contribute disproportionately to parasite egg shedding. These heavily infected pups also suffer severe anemia and high levels of hookworm-induced mortality. Alternative strategies to maximize total egg shedding and/or transmission, such as increased environmental survival of larval stages or avoidance of clearance, have not been developed by this hookworm. We propose that fur seal hookworms exploit a live fast-die young life history strategy, which translates to the highest levels of host anemia and mortality recorded among hookworms.

Kelp and dolphin gulls cause perineal wounds in South American fur seal pups (Arctocephalus australis) at Guafo Island, Chilean Patagonia.

During five reproductive seasons, we documented the presence, extent and origin of perineal wounds in South American fur seal pups (Arctocephalus australis) on Guafo Island, Northern Chilean Patagonia. The seasonal prevalence of perineal wounds ranged from 5 to 9%, and new cases were more common at the end of the breeding season (February), when pups were on average two months old and were actively expelling hookworms (Uncinaria sp). Histologically, wounds corresponded to marked ulcerative lymphoplasmacytic and histiocytic dermatitis with granulation tissue and mixed bacterial colonies. In 2015 and 2017, kelp gulls (Larus dominicanus) and dolphin gulls (Leucophaeus scoresbii) were observed picking and wounding the perineal area of marked pups. This behaviour occurred more frequently after the pups' defecation, when sea gulls engaged in consumption of pups' faeces. The affected pups usually had moderate to marked hookworm infections along with bloody diarrhoea and anaemia. Pups with severe wounds (23% of affected animals) had swollen perineal areas and signs of secondary systemic bacterial infection. We propose that seagulls on Guafo Island have learned to consume remains of blood and parasites in the faeces of pups affected by hookworm infection, causing perineal wounds during this process. We conclude that this perineal wounding is an unintentional, occasional negative effect of an otherwise commensal gull-fur seal relationship.

Is the feeding type related with the content of microplastics in intertidal fish gut?

Microplastics pollution is a growing global concern that affects all aquatic ecosystems. Microplastics in the environment can be in the form of fibers and/or particles, being the former the most abundant in the marine environment, representing up to 95% of total plastics. The aim of this work was to compare the content of microplastics among intertidal fish with different feeding type. Our results show that omnivorous fish presented a higher amount of microplastic fibers than registered in herbivores and carnivores. Moreover, lower condition factors (K) were found in omnivorous specimens with higher microplastic content. We hypothesized that the type of feeding resulted in different microplastic ingestion, with species with wider range of food sources as omnivores with higher rates. Futures studies carried out to evaluate the biological impacts of microplastics on marine organisms, and microplastics cycling on the marine environment should consider the type of feeding of the studied species.

Hematology, Serum Chemistry, and Early Hematologic Changes in Free-Ranging South American Fur Seals ( Arctocephalus australis ) at Guafo Island, Chilean Patagonia.

The establishment of clinical pathology baseline data is critical to evaluate temporal and spatial changes in marine mammal groups. Despite increased availability of studies on hematology and biochemistry of marine mammals, reference ranges are lacking for many populations, especially among fur seal species. During the austral summers of 2014 and 2015, we evaluated basic hematologic and biochemical parameters in clinically healthy, physically restrained South American fur seal ( Arctocephalus australis ) lactating females and 2-mo-old pups. We also assessed the temporal variation of hematology parameters on the pups during their first 2 mo of life. Reference ranges of lactating females were similar to those previously reported in other fur seal species. In the case of pups, reference ranges are similar to values previously reported in sea lion species. As expected, most biochemical and hematologic values differ significantly between adult females and pups. As in other otariids, South American fur seals pups are born with higher values of total red blood cells, hemoglobin, and packed cell volume, and lower numbers of total leukocytes, neutrophils, lymphocytes, and eosinophils. To the best of our knowledge, data on hematology reference values for South American fur seals has not been previously reported and is useful for continued health monitoring of this species, as well as for comparisons with other otariid groups.