Harmful algal blooms expose southern right whales to domoic acid and can potentially cause endocrine alterations

Dr. Alejandro Fernández Ajó, OSU Department of Fisheries, Wildlife, & Conservation Sciences, Geospatial Ecology of Marine Megafauna Lab

Rises in ocean temperatures can lead to multiple alterations in marine ecosystems, including the increase and the frequency of Harmful Algal Blooms (HABs). HABs are characterized by the rapid growth of toxin-producing species of algae that can be harmful to people, animals, and the local ecology, even causing death in severe cases. Species of marine diatom within the genus Pseudo-nitzschia and Nitzschia can form HABs when they produce domoic acid (DA), a potent neurotoxin responsible for amnesic shellfish poisoning (D’Agostino et al., 2018, 2017).

Figure 1. Southern right whale (E. australis) mother and calf swimming at the gulfs of Peninsula Valdes, Argentina, during a phytoplankton bloom. Photo: Mariano Sironi / Instituto de Conservacion de Ballenas de Argentina.

During HABs, DA is transferred to higher organisms through the pelagic food web and is accumulated by intermediate vectors, such as copepods, euphausiids (i.e., krill), shellfish, and fish. As this neurotoxin affects top predators, DA poisoning poses a risk to the safety and health of humans and wildlife. This neurotoxin has caused mortality in many marine mammal species, including both pinnipeds and cetaceans (Gulland 1999; Lefebvre et al. 1999; Fire et al. 2010, 2021; Broadwater et al. 2018). In addition, the exposure to DA constitutes a stressor that may affect glucocorticoids (hormones involved in the stress response) concentrations.

The glucocorticoids (GCs; cortisol and corticosterone) are adrenal steroid hormones that maintain the essential functions of metabolism and energy balance in mammals. GCs can increase sharply in response to environmental stressors to elicit physiological and behavioral adaptations by individuals to support survival (Sapolsky et al. 2000; Bornier et al. 2009). However, with the chronic exposure to a stressor, this relationship can reverse, with GCs sometimes declining below its baseline levels (Dickens and Romero, 2013; Fernández Ajó et al., 2018). Moreover, DA can interfere with the stress response in mammals, and cause alterations in their physiological response. DA is an excitatory amino acid analog of glutamate (Pulido 2008), a well-known brain neurotransmitter that play an important role in the activation of the adrenal axis (which in turn regulate the production and secretion of the GCs) and regulate many of the pituitary hormones involved in the stress response (Brann and Mahesh 1994; Johnson et al. 2001). Hence, monitoring GC levels in marine mammals can be a potential useful metric for assessing the physiological impacts of exposure to DA.

Glucocorticoids are traditionally measured in plasma, but given that plasma sampling from free-ranging large whales is currently impossible, alternative sample types such as fecal samples, among others, can be utilized to quantify GCs in large whales (Ajó et al., 2021; Burgess et al., 2018, 2016; Fernández Ajó et al., 2020, 2018; Hunt et al., 2019, 2014, 2006; Rolland et al., 2017, 2005)(Figure 2). The analyses of fecal glucocorticoid metabolites (fGCm) is particularly useful for endocrine assessments of free-swimming whales, with several studies showing that fGCm correlate in meaningful ways with presumed stressors. For example, high levels of fGCm in North Atlantic right whales (NARW, Eubalaena glacialis) and in gray whales (Eschrichtius robustus) correlate with poor body condition (Hunt et al., 2006; Lemos et al., 2021), and fGCm increases were associated with whale entanglements and ship strikes (i.e., Lemos et al., 2020; Rolland et al., 2017).

Figure 2. Alternative samples types can be used to study hormones in large whales. 1-2-3 are sample types that can be obtained from free-living whales and provide a more instantaneous and acute measurement of the whales´ physiology. 4-5 can be obtained at necropsy when the whale is found dead at the beach and provide an integrated measure of the whale physiology that can expand through years or even the lifespan of an individual.

In Península Valdés, Argentina, southern right whales (SRW, E. australis) gather in large numbers to mate and nurse their calves during the austral winter months (Bastida and Rodríguez, 2009). SRWs are capital breeders, largely fasting during the breeding season and instead relying on stored blubber fuel reserves. However, they can occasionally feed on calanoid copepods (D’Agostino et al., 2018, 2016), particularly during the phytoplankton blooms that are dominated by diatoms of the genus Pseudo-nitzschia (Sastre et al. 2007; D’Agostino et al. 2015, 2018). Therefore, feeding SRWs in Península Valdés temporally overlap with these Pseudo-nitzschia blooms (D’Agostino et al. 2018, 2015) and represents a test case for assessing the relationship of DA exposure with GC levels (Figure 3).

Figure 3. Southern right whale (E. australis) skim feeding at the Peninsula Valdes breeding ground. Photo: Lucas Beltranino.

In our recent scientific publication (D’Agostino et al. 2021), we investigate SRW exposure to DA at their breeding ground in Peninsula Valdes and assessed its effects on fecal glucocorticoid concentrations. Although the sample size of this study is unavoidably small due to the difficulties of obtaining fecal samples from whales at their calving grounds where defecation is infrequent, we observed significantly lower fGCm in samples from whales exposed to DA (Figure 4). Our results agree with findings from a previous study in California sea lions (Zalophus californianus) exposed to DA, where these authors found a significant association of DA exposure with reduced serum cortisol (Gulland et al., 2009), which can be tentatively attributed to abnormal function of the adrenal axis due to the exposure.

Figure 4. Fecal glucocorticoid metabolite levels in southern right whales exposed (YES, solid triangles) and not-exposed (NO, open circles) to DA. Left panel: immunoreactive fecal corticosterone metabolites. Right panel: immunoreactive fecal cortisol metabolites. Hormone concentrations are expressed in ng of immunoreactive hormone per gram of dry fecal sample. Significant differences between groups are denoted with an asterisk (P<0.05). The black solid line indicates the mean for each group, and in parenthesis is the sample size for each group. Adapted from D’Agostino et al. 2021.

If ingestion of toxins produced by phytoplankton can result in long-term suppression of baseline GCs, whales and marine mammals in general, could suffer reduced ability to cope with additional stressors. The adrenal function is essential to maintain circulating blood glucose and other aspects of metabolism within normal bounds. Additionally, the ability to elevate GCs facilitates energy mobilization to physiologically cope with a stressful event and to initiate appropriate behavioral responses (i.e., flee from predators, heal wounds). Various toxicants have been shown to reduce adrenal function across taxa (Romero and Wingfield, 2016) and could have negative consequences on the ability of cetaceans to respond and adapt to ongoing environmental and anthropogenic changes. Compounding this problem, whales are exposed to an increasing number of stressors from multiple sources and with cumulative effects and they need to be able to physiologically respond to continue to reproduce and survive.

To our knowledge, this study provides the first quantification of fGCm levels in whales exposed to DA; and we hope this effort starts a growing dataset to which other researchers can add. Sampling and analysis of non-traditional matrices, such as feces, blubber, baleen and others, would likely increase sample sizes and thus our understanding of the interrelationships among DA exposure and age, sex, and reproductive status of cetaceans. Given that chronic exposure to DA could alter the capacity of animals to respond to stress, and indications that HABs are becoming more frequent and intense world-wide (Van Dolah 2000; Masó et al. 2006; Erdner et al. 2008), we believe that research evaluating the health status of marine mammal populations should include the assessment of stress physiology relative to natural and anthropogenic stressors including exposure to toxicants.

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