Article Figures and data Abstract eLife digest Introduction Results Discussion Materials and methods Data availability References Decision letter Author response Article and author information Metrics Abstract 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. https://doi.org/10.7554/eLife.38432.001 eLife digest Every year off the coasts of Chile, Guafo Island becomes a nursery for South American fur seals pups. Mother fur seals leave their young on the beaches, going out at sea to hunt for fish before returning to the shore to nurse. These first few months are dangerous for young seals, with many dying because of hookworms, parasites that latch to the wall of the bowels to suck blood. However, the immune system of the pups is usually able to mount a response and fight off these parasites. Even though the pups stay on land, their lives depend on the health of the ocean that feeds their nursing mothers. In recent years, sea temperature has been rising rapidly, which modifies winds and water currents. This can set off a chain of events that results in fewer fish being available for seals and other marine mammals to eat. Researchers know that years with warmer waters are associated with changes in the pattern of the mothers’ hunting trips, more pups’ deaths, and a weaker immune system in young fur seals. However, the mechanisms that connect these different factors are still unclear. To explore this, Seguel et al. followed South American fur seals colonies on Guafo Island for several years, tracking the mothers’ trips and monitoring the health of the pups by looking at their levels of blood sugar, whether they carry hookworms, and certain elements of their immune system. Results showed that in years when the sea is warmer, fur seal mothers are gone hunting for longer: they spend less time nursing their young, which then grow slower. These young seals also have lower levels of blood sugar, and so they have less energy to create the immune response necessary to clear off parasitic worms. In fact, in years with warmer seas, almost half of the pups die from hookworm infections. The work by Seguel et al. shows that warmer oceans directly weaken the immune defenses of certain marine mammals. If temperatures keep rising, infectious diseases may kill more of these animals. Further work is now needed to explore if strategies could be developed to help seal populations, for example by treating the pups with drugs that eliminate the parasites. https://doi.org/10.7554/eLife.38432.002 Introduction Marine mammals are a diverse group of top predators highly sensitive to changes in aquatic ecosystems (Constable et al., 2014). Within this group, fur seals and sea lions (otariids) breed and give birth on land but forage at sea, alternating periods of foraging in the ocean with periods of offspring attendance and nursing on land (income breeders) (Stephens et al., 2009). Therefore, otariids, like other marine mammals, are highly sensitive to local changes in prey distribution and abundance (Trillmich et al., 1991, Constable et al., 2014, Elorriaga-Verplancken et al., 2016). One of the most important indexes of the abundance of marine mammal prey is sea surface temperature (SST) (Soto et al., 2006, Elorriaga-Verplancken et al., 2016). Warmer SST indicates reduced nutrient upwelling, which is associated with reduced primary productivity and abundance of mesopelagic marine organisms (Lewandowska et al., 2014). This decrease in food resources forces otariid females to change their foraging strategies by increasing their foraging trip lengths, resulting in decreased time spent on land with their pup (maternal attendance) (Trillmich et al., 1991, Costa, 2008). These changes in patterns of maternal attendance have been associated with decreased pup growth and increased mortality (Soto et al., 2006, Jeanniard-du-Dot et al., 2017). Regardless, the mechanisms that drive decreased survival during years with low ocean productivity have not been intensely explored beyond assuming that this results from direct mortality because of starvation. However, in some otariid populations, in years with abnormal SST, the immune competence of pups decreases (Banuet-Martínez et al., 2017), suggesting that environmental variables can affect the health of marine mammals by impairing their immune function. If these immunological changes impact offspring survival, there could be additional negative consequences between a warmer ocean, health, and survival of marine vertebrates. In some marine mammal populations, infectious diseases are one of the most significant causes of mortality among young individuals (Gulland and Hall, 2007; Spraker et al., 2007; Seguel et al., 2013). In otariids, hookworms (Uncinaria sp.) have been described in nearly all species, and while some populations suffer few adverse effects, others experience up to 70% of hookworm-related mortality being one of the most significant infectious diseases of young fur seals and sea lions (Spraker et al., 2007; Lyons et al., 2011a; Seguel et al., 2013; Seguel and Gottdenker, 2017). Fur seals are infected with hookworms (Uncinaria sp.) during their first 1–4 days of life through their mother’s colostrum (Lyons et al., 2011b; Seguel et al., 2018). These nematodes live in the small intestine where they bite the mucosa to feed on blood, causing substantial tissue damage, anemia, and death (Marcus et al., 2015, Seguel et al., 2017, Seguel et al., 2018); however, it is unclear how the host responds to this infection. Long term studies in fur seal populations show that hookworm prevalence and mortality varies over time, but the mechanisms driving these patterns are unknown (Lyons et al., 2011a; Seguel et al., 2013). In this paper, we describe how oceanographic environmental variables, via the modification of maternal care, are associated with immune-mediated parasite clearance, and survival of a marine mammal, the South American fur seal (SAFS, Arctocephalus australis). Results Hookworm disease dynamics and mortality in fur seal pups The hookworm (Uncinaria sp.) prepatent period varied from 14 to 18 days and based on the coprological analyses and necropsies of recaptured pups, the number of days a pup released hookworm eggs (infectious period) ranged from 5 to 55 days (2014–15 and 2017, mean = 25.7 ± 10.9, n = 146). Seven to 15 days before having a negative coprological test, fur seal pups experienced a decline of more than 50% in the number of eggs shed in previous exams. At this stage, pups were considered to be in a hookworm clearance state. When presenting the first negative coprological exam, they were considered to have cleared hookworm infection (Figure 1A). Between 81% to 100% of pups examined through necropsy between 2005–08 (n = 124) and 2012–17 (n = 154) had evidence of hookworm infection, and hookworm-related mortality corresponded to 13–50% of all pups found dead (n = 56, Figure 1B). Total hookworm mortality could be calculated in a subset of marked pups in 2014 (n = 38), 2015 (n = 53), and 2017 (n = 54) (Figure 1—source data 1). Hookworms killed 42.1% of pups born in 2014, 20.7% of pups born in 2015, and 24% of pups born in 2017 at Guafo Island (GLM, 2014 = 1.02 ± 0.47, Z = 2.16, p = 0.0304). Based on multimodel inference using generalized linear mixed models, pups that had higher hookworm burden, delayed hookworm clearance, and lower plasma concentration of parasite specific IgG, blood urea nitrogen, and glucose were more likely to die from hookworm disease (Figure 1C–F) (Supplementary file 1 and 2). Therefore, the most important host-related factors affecting hookworm mortality were energy balance and immune response against the parasite. The parasite-related factors affecting mortality suggested that hookworm clearance, by reducing infectious period and hookworm burden, enhanced host survival. Figure 1 Download asset Open asset Hookworm infection dynamics and predictors of hookworm mortality in South American fur seal (Arctocephalus australis) pups at Guafo Island, southern Chile. (A) Hookworm egg shedding patterns through infection stages. (B) Hookworm prevalence and mortality through different reproductive seasons (2005–08, 2012–17). (C–F) Predictors of hookworm mortality in generalized linear mixed models (GLMM) (2014, 2015, 2017) vs observed hookworm mortality. Higher hookworm burdens (GLMM, 1.47 ± 0.56, Z = 2.61, p = 0.009), longer infectious periods (GLMM, 0.17 ± 0.06, Z = 2.87, p = 0.004), and lower plasma concentrations of blood urea nitrogen (BUN) (GLMM, −0.45 ± 0.23, Z = −1.97, p = 0.049) and parasite-specific IgG (GLMM, −0.41 ± 0.17, Z = −2.45, p = 0.014) increased the probability of hookworm mortality. Raw data in: Figure 1—source data 1. https://doi.org/10.7554/eLife.38432.003 Figure 1—source data 1 Predictors of hookworm-related mortality in South American fur seal pups. https://doi.org/10.7554/eLife.38432.004 Download elife-38432-fig1-data1-v2.xlsx Hookworm clearance is immune-mediated To determine the mechanisms that drive hookworm clearance and affect host mortality, the immune response to hookworms was investigated during 2017 at different infection stages in 54 fur seal pups, and compared to 24 hookworm-free (ivermectin-treated) age-matched controls (Figures 2, 4A and B, Figure 2—source data 1). The number of peripheral blood leukocytes (lymphocytes, macrophages, neutrophils, eosinophils, and basophils) was obtained as a basic tool to indirectly measure the level of proliferation of these different immune cell types in infected and control animals. During the patent and clearance period, fur seal pups that survived infection (n = 41) experienced a significant increase in the number of peripheral blood lymphocytes (GLMM, 0.9 ± 0.003, Z = 231, p = 2.0×10−16) and basophils (GLMM, 4.8 ± 0.08, Z = 56.7, p = 2.0×10−16), and had higher numbers of these cells when compared to age-matched controls and to the pups that died from hookworm infection (Figure 2A–B). The number of neutrophils in peripheral blood was similar between controls and pups that survived but slightly lower in pups that died (n = 13) from hookworm disease (GLMM, died = −0.53 ± 0.06, Z = −8.04, p = 9.1×10−16). During the patent period, lower numbers of monocytes were found in animals that died from hookworm disease compared to controls (GLMM, died = −0.88 ± 0.11, Z = −7.64, p = 1.54×10−14), and eosinophils were higher in animals that survived when compared to controls and animals that died (GLMM, survived = 0.86 ± 0.16, Z = 5.19, p = 2.0×10−7); however, during the clearance and post-clearance periods, eosinophils (GLMM, survived = 0.26 ± 0.14, Z = 1.88, p = 0.07) and macrophages (GLMM, survived = −0.03 ± 0.09, Z = 0.36, p = 0.71) were in similar numbers in pups that survived infection and controls. Pups that cleared the infection developed medium to high levels of parasite-specific IgG, whereas the level of these antibodies was significantly lower in pups that died from hookworm infection and almost non-existent in the control group (Figure 2J–M). There was moderate to marked immunolabelling of the hookworm intestinal brush border using serum from six pups with moderate to high levels of parasite-specific IgG (23–100 arbitrary units) (Figure 2I), suggesting that anti-hookworm antibodies bind proteins located in the hookworm intestine. Figure 2 Download asset Open asset Changes in peripheral blood leukocytes and parasite-specific IgG antibodies during different phases of hookworm infection (Uncinaria sp.) in South American fur seal (Arctocephalus australis) pups (2017). (A) Pups that die from hookworm disease have lower numbers of lymphocytes during the prepatent phase compared to controls and pups that survived (Generalized linear mixed model (GLMM), lymphocytes died = −0.52 ± 0.13, Z = −4.06, p = 4.92×10−5). Pups that survive hookworm infection have higher numbers of lymphocytes during the patent (B) (GLMM, lymphocytes survived = 0.80 ± 0.13, Z = 6.04, p = 1.54×10−9) and clearance (C) (GLMM, lymphocytes survived = 0.52 ± 0.12, Z = 4.30, p = 1.74×10−5) infection phases when compared to pups that died due to hookworm infection and/or age matched controls. (E–H) Pups that clear and survive hookworm infection have markedly higher numbers of basophils during the patent (GLMM, basophils survived = 7.46 ± 1.4, Z = 5.33, p = 1.0×10−7) and clearance (GLMM, basophils survived = 6.34 ± 0.9, Z = 7.07, p = 1.5×10−12) infection phases compared to controls and pups that died from hookworm infection. (I) Fur seal pups that clear hookworm infection produce parasite-specific IgG that binds the intestinal brush border of the fur seal hookworms (Uncinaria sp.) (arrow). (J–M) Fur seal pups that clear hookworm infection have higher levels of parasite-specific IgG during the prepatent (GLMM, IgG survived = 1.78 ± 0.36, Z = 4.86, p = 1.12×10−6), patent (GLMM, IgG survived = 2.27 ± 0.25, Z = 9.067, p = 2.0×10−16), clearance (GLMM, IgG survived = 1.80 ± 0.2, Z = 9.0, p = 2.0×10−16), and post-clearance (GLMM, IgG survived = 1.87 ± 0.25, Z = 7.3, p = 3.53×10−13) infection phases compared to controls and pups that died. Asterisk indicate groups are statistically different at alpha = 0.05. p-values code: *0.01 < 0.05, **0.001 < 0.01, *** < 0.001. Raw data in: Figure 2—source data 1. https://doi.org/10.7554/eLife.38432.005 Figure 2—source data 1 Maternal attendance and health-related parameters in pups with different hookworm infection status. https://doi.org/10.7554/eLife.38432.006 Download elife-38432-fig2-data1-v2.xlsx To determine the morphological and immune cell population changes in the anatomical site of hookworm infection, sections of small intestine and mesenteric lymph nodes were collected from pups that died from hookworm disease (n = 21), pups that were undergoing clearance (n = 18), and pups that were never infected with hookworms (controls, n = 6) (Figure 3—source data 1). The small intestine mucosa, submucosa, and the mesenteric lymph nodes of pups undergoing hookworm clearance contained larger numbers of T-lymphocytes when compared to pups that died from hookworm infection or pups never infected with adult Uncinaria sp (Generalized linear models with negative binomial distribution (GLM.NB), mucosa clearance = 0.86 ± 0.11, Z = 8.312, p = 2.0×10−16, submucosa clearance = 1.08 ± 0.16, Z = 6.86, p = 7.0×10−12, mesenteric lymph node clearance = 0.78 ± 0.06, Z = 14.21, p = 2.0×10−16) (Figure 3). B-lymphocytes and plasma cells were more numerous in the mesenteric lymph node of pups clearing hookworm infection versus controls and pups dead from hookworm infection (GLM.NB, B-lymphocytes clearance = 0.29 ± 0.07, Z = 4.1, p = 4.1×10−5, plasma cell clearance = 0.59 ± 0.05, Z = 10.2, p = 2.0×10−16). Similarly, there were higher numbers of mast cells (GLM.NB, clearance = 1.14 ± 0.25, Z = 4.6, p = 4.2×10−6) and more mucus (GLM, clearance = 0.03 ± 0.003, Z = 7.84, p = 9.4×10−10) in the mucosa, and more leukocytes expressing IL-4 in the intestine (GLM.NB, clearance = 1.97 ± 0.15, Z = 12.72, p = 2.0×10−16) and mesenteric lymph node (GLM.NB, clearance = 1.57 ± 0.11, Z = 14.63, p = 2.0×10−16) of pups that cleared hookworm infection when compared to controls and pups with hookworm enteritis and bacteremia. Pups that died from hookworms, however, had larger numbers of macrophages in the intestinal submucosa (GLM.NB, mortality = 0.52 ± 0.09, Z = 5.79, p = 6.94×10−9) and mesenteric lymph nodes (GLM.NB, mortality = 0.63 ± 0.05, Z = 12.68, p = 2.0×10−16) compared to pups never infected with hookworms and pups clearing hookworm infection (Figure 3). Figure 3 Download asset Open asset Intestinal immune response in different groups of South American fur seals (Arctocephalus australis) infected with hookworms (Uncinaria sp.) and controls. During the clearance process, fur seal pups recruit numerous T-lymphocytes (CD3 stain) in the jejunum mucosa (Generalized linear models with negative binomial distribution (GLM.NB), clearance = 0.86 ± 0.11, Z = 8.312, p = 2.0×10−16) and submucosa (GLM.NB, clearance = 1.08 ± 0.16, Z = 6.86, p = 7.0×10−12). Mast cells (C-kit stain) are found in higher numbers in the intestinal mucosa of pups undergoing clearance (GLM.NB, clearance = 1.14 ± 0.25, Z = 4.6, p = 4.2×10−6). The intestinal mucosa of pups clearing hookworm infection contains a large amount of mucus (GLM, clearance = 0.03 ± 0.003, Z = 7.84, p = 9.4×10−10). Pups that die from hookworm enteritis and bacteremia (HEB) have lower numbers or proportions of these immune components but higher numbers of macrophages (IBA1 stain) in the jejunum submucosa (GLM.NB, mortality = 0.52 ± 0.09, Z = 5.79, p = 6.94×10−9). Asterisks indicate groups are statistically different at alpha = 0.05. p-values code: *0.01 < 0.05, ** <0.01. GLM.NB. Raw data: Figure 3—source data 1. https://doi.org/10.7554/eLife.38432.007 Figure 3—source data 1 Leukocyte subsets and IL-4 immunohistochemical staining in intestine and mesenteric lymph node. https://doi.org/10.7554/eLife.38432.008 Download elife-38432-fig3-data1-v2.xlsx Figure 4 Download asset Open asset Maternal attendance affects South American fur seal pup’s growth rate, energy balance, and immune response against hookworms. (A) The observed number of nursing events against predicted values of growth rate. With more nursing events pups grow faster (GLM.NB, 0.031 ± 0.006, Z = 5.53, p = 3.2×10−8). (B) Pups that survived hookworm infection had higher levels of maternal attendance (more nursing events) (GLM.NB, 0.78 ± 0.23, Z = 3.45, p = 5.5×10−4), faster growth rate (GLM.NB, 1.05 ± 0.16, Z = 6.6, p = 2.7×10−11), and higher average levels of glucose (GLM, 3.0 ± 0.5, Z = 5.9, p = 1.02×10−7) compared to pups that died from hookworm disease; however, they had similar attendance and metabolic values compared to hookworm-free (control) pups (GLM.NB, 0.01 ± 0.13, Z = 0.13, p = 0.893, and GLM, 0.71 ± 0.38, t = 1.863, p = 0.066). (C) The observed values of number of nursing events, growth rate, interaction between nursing and growth rate and hookworm burden vs. the predicted values of CD3+ lymphocytes in section of skin in response to phytohemagglutinin (PHA) challenge. Pups with more nursing events (GLM.NB, 0.098 ± 0.02, Z = 4.39, p = 1.14×10−5), faster growth rate (GLM.NB, 0.04 ± 0.004, Z = 11.3, p = 2.0×10−16), and higher hookworm burden (GLM.NB, 0.009 ± 0.004, Z = 2.56, p = 0.01) had more recruitment of T-lymphocytes. (D) A subset of pups was divided into groups of low and high response to PHA challenge at 30 days old. Pups with higher CD3 lymphocyte response had higher average levels of parasite-specific IgG (GLM.NB, 1.11 ± 0.33, Z = 3.37, p = 7.5×10−4), shorter infectious period (GLM.NB, −0.38 ± 0.12, Z = −3.06, p = 2.1×10−3), faster growth rate (GLM.NB, 0.68 ± 0.06, Z = 10.9, p = 2.0×10−16), and higher levels of maternal attendance (GLM.NB, 0.94 ± 0.13, Z = 7.04, p = 1.92×10−1). Hookworm burden was similar between the two groups (GLM.NB, low reactivity = −0.63 ± 0.37, Z = −1.67, p = 0.09). Raw data: Figure 4—source data 1 and Figure 4—source data 2. https://doi.org/10.7554/eLife.38432.009 Figure 4—source data 1 Phytohemagglutinin immune challenge in 8-wk-old pups. https://doi.org/10.7554/eLife.38432.010 Download elife-38432-fig4-data1-v2.xlsx Figure 4—source data 2 Phytohemagglutinin immune challenge in 4-wk-old pups. https://doi.org/10.7554/eLife.38432.011 Download elife-38432-fig4-data2-v2.xlsx Maternal attendance affects fur seal pup hookworm clearance Maternal attendance patterns and pup-related health parameters were assessed in the 2017 reproductive season (n = 78) (Figure 4A and B, Figure 4—source data 1). Among measured serum chemistry variables, the average level of blood glucose was the best predictor of growth rate (GLM.NB, 0.18 ± 0.03, Z = 5.9, p = 2×10−16). Among the considered external factors that could affect growth, the number of nursing events observed in a pup was the most significant predictor of growth rate, and although hookworm burden and hookworm infectious period were included in some top ranked models, their effect was not significant (Figure 4A, supplementary file 4 and 5). Additionally, there were no significant differences in growth rates between pups treated with ivermectin (n = 24) and non-treated (n = 54) (GLM.NB, 0.17 ± 0.15, Z = 1.16, p = 0.26). Nevertheless, when pups that died from hookworm disease were considered (n = 13), they had significantly slower growth rates (GLM.NB, −1.05 ± 0.16, Z = −6.6, p = 2.7×10−11) compared to pups that survived (n = 41) and pups treated with ivermectin; however, the animals that died also had the lowest levels of maternal attendance (GLM.NB, −0.78 ± 0.23, Z = −3.45, p = 5.5×10−4) (Figure 4B). Regarding the factors that affected overall immune reactivity (Figure 4C, Figure 4—source data 1), pups with more nursing events, faster growth rate, and higher hookworm burden were more likely to recruit higher numbers of T-cells (CD3+ lymphocytes) in the skin in response to (Phytohemagglutinin) PHA challenge (Figure 4C, supplementary file 5 and 6). Pups with lower parasite-specific IgG concentrations (GLMM.NB, coeff = −0.017 ± 0.002, Z = 6.54, p = 2×10−16, n = 146) and higher hookworm burden (GLMM.NB, coeff = 0.06 ± 0.022, Z = 2.78, p = 0.005, n = 146) had longer infectious periods (Supplementary file 7 and 8), suggesting that among measured immune parameters, parasite-specific IgG was the most significant factor affecting the permanence of hookworms in the intestine. Based on the PHA immune challenge performed when pups were 1-mo-old (Figure 4D, Figure 4—source data 1), animals with high T-cell response had higher levels of IgG, maternal attendance, glucose, growth rate, and shorter infectious periods at the end of the study when compared to the average levels in pups with low T-cell response (Figure 4D). However, hookworm burden was similar between the two groups (Figure 4D), suggesting, in conjunction with the previous analyses, that maternal attendance and growth rate accounted for most of the difference in T-cell reactivity between these groups. In years with high sea surface temperature there is lower maternal attendance, immune response, and increased hookworm-induced mortality SAFS females were observed more frequently arriving to the rookery from foraging trips early in the morning (2007 = 78/115, 67.8% returning events in the morning, 2017 = 87/135, 64% returning events in the morning). Foraging trip length was correlated with the number of nursing events, indicating that the more time females spend at sea makes it less likely to observe them nursing their pup (Figure 5A). In 2017, a year with SST above Guafo Island average, SAFS females (n = 21) spend more time foraging at sea compared to 2007 (n = 23), a year with SST below Guafo Island average, therefore in 2017 (n = 79) the level of maternal attendance and pup growth rate were lower than in 2007 (n = 128) (Figure 5B) (Figure 5A and B, Figure 5—source data 1). Between 2012 and 2017 (Figure 5C, Figure 5—source data 1), in years with high SST (e.g. 2014), the average concentrations of glucose, cholesterol, parasite-specific IgG, and peripheral blood lymphocytes and basophils were lower than in years with low SST (Figure 5C). Similarly, the average hookworm infectious period was shorter in years with low SST (GLM, X2 = 6.95, df = 1, p = 0.00036). Figure 5 Download asset Open asset South American fur seals foraging behavior and maternal care patterns differ between seasons. (A) The level of maternal attendance decreases as foraging trips become longer (linear regression, R2 = 0.412, p = 0.016; dashed lines represent 95% confidence intervals). (B) In a year with sea surface temperature (SST) below the historic Guafo Island average (2007), fur seal females foraging trips are shorter when compared to the mean foraging trip duration during a year with SST temperature above the historical average (2017) (unpaired T-test, t = 5.133, df = 42, p < 0.0001). Additionally, maternal attendance and pup growth rate in 2007 were higher than attendance and growth rates in 2017 (maternal attendance index: unpaired T-test, t = 2.060, df = 244, p = 0.04; growth rate: unpaired T-test, t = 2.85, df = 66, p = 0.0058). (C) Between 2012 and 2017 the mean values of glucose, cholesterol, parasite-specific IgG, peripheral blood lymphocytes and basophils followed an inverse pattern with mean SST at Guafo Island. In 2013, a year with low SST, pups had, on average, higher levels of glucose, cholesterol, parasite-specific IgG, lymphocytes and basophils when compared to the mean values of other reproductive seasons (Kruskal-Wallis with Dunn’s multiple comparison tests, Kruskal-Wallis statistic = 73.2–114.6, mean rank diff. = 63.98–203.8, p < 0.0001–0.023). In 2014, with the highest mean SST over the last 15 y at Guafo Island, fur seal pups had the lowest mean values of these metabolic and immune parameters (Kruskal-Wallis with Dunn’s multiple comparison tests, Kruskal-Wallis statistic = 73.2–114.6, mean rank diff. = −230.83,–83.4, p < 0.0001–0.017). (Asterisks indicate mean is significantly different from means of other seasons). Raw data in: Figure 5—source data 1 and Figure 5—source data 2. https://doi.org/10.7554/eLife.38432.012 Figure 5—source data 1 Maternal attendance and growth rates in 2007 and 2017. https://doi.org/10.7554/eLife.38432.013 Download elife-38432-fig5-data1-v2.xlsx Figure 5—source data 2 Immune and metabolic parameters in South American fur seal pups between 2012 and 2017. https://doi.org/10.7554/eLife.38432.014 Download elife-38432-fig5-data2-v2.xlsx Over a 10-y period (2005–08, 2012–17) (Figure 6, Figure 6—source data 1 and 2), there was a significant positive correlation between mean hookworm burdens of necropsied pups and SST (Linear regression, Ad-R2 = 0.86, p < 0.001), and between hookworm mortality and SST (Ad-R2 = 0.56, p = 0.016); however, in the case of hookworm prevalence at necropsy the correlation with SST was not significant (Figure 6, supplementary file 9–11) (Ad-R2 = 0.29, p = 0.064). A similar but negative correlation existed between the same hookworm epidemiological parameters and average chlorophyll-a concentrations (Figure 6). Figure 6 Download asset Open asset Correlation between oceanographic parameters (sea surface temperature and chlorophyll-a) and hookworm disease dynamics in South American fur seals (Arctocephalus australis) at the Chilean Patagonia (2005–08, 2012–17). (A) Hookworm prevalence, burden, and mortality increase in years with warmer sea surface temperature (Linear regressions. Hookworm prevalence, Ad-R2 = 0.29, p = 0.064. Hookworm burden, Ad-R2 = 0.86, p < 0.001. Hookworm mortality, Ad-R2 = 0.56, p = 0.016). Hookworm prevalence, burden, and mortality decrease in some years with higher primary productivity (Second order polynomial regressions. Hookworm prevalence, Ad-R2 = 0.46, p = 0.046. Hookworm burden, Ad-R2 = 0.29, p < 0.123. Hookworm mortality, Ad-R2 = 0.70, p = 0.005). Dashed lines represent 95% confidence intervals. Raw data: Figure 6—source data 1 and Figure 6—source data 2. https://doi.org/10.7554/eLife.38432.015 Figure 6—source data 1 Sea surface temperature data for Guafo Island. https://doi.org/10.7554/eLife.38432.016 Download elife-38432-fig6-data1-v2.xlsx Figure 6—source data 2 Hookworm prevalence, burden, and mortality in South American fur seal pups at Guafo Island. https://doi.org/10.7554/eLife.38432.017 Download elife-38432-fig6-data2-v2.docx Discussion Hookworm disease causes significant mortality in SAFSs in the Chilean Patagonia and represents one of the most significant causes of death among pups (Seguel et al., 2013; Seguel et al., 2018). However, in some years, hookworm-induced mortality decreases significantly. We showed that variations in hookworm disease morbidity and mortality are associated with specific changes in the immune response against the parasite. Additionally, maternal care was the most important external factor affecting immune response and hookworm clear