Although mites of the Orthohalarachne genus are common parasites of otariids, their role as agents of disease and in causing population-level mortality is unknown. In the austral summer of 2016, there was an increase in mortality among South American fur seal ( Arctocephalus australis) pups at Guafo Island, Northern Chilean Patagonia. Pups found dead or terminally ill had moderate to marked, multifocal, mucopurulent bronchopneumonia associated with large numbers of respiratory mites ( Orthohalarachne diminuata) and rare Gram-positive cocci. In lung areas less affected by bronchopneumonia, acute interstitial pneumonia with marked congestion and scant hemorrhage was evident. Bacteria from pups dying of bronchopneumonia were isolated and identified as Streptococcus marimammalium and Streptococcus canis. Respiratory mites obstructed airflow, disrupted airway epithelial lining, and likely facilitated the proliferation of pathogenic β-hemolytic streptococci, leading to severe bronchopneumonia and death of fur seal pups. An abrupt increase in sea surface temperature in Guafo Island corresponded to the timing of the bronchopneumonia outbreak. The potential role of environmental factors in the fur seal pup mortality warrants further study.
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.
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.
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.
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