Cumulative Effects of Multiple Stressors

Potential Cumulative Effects of Multiple Stressors

While it is difficult to quantify or characterize individual stressors, it is even more difficult to quantify the potential impacts that a combination of stressors, either concurrently or sequentially, would have on CI beluga recovery. Exposure to any given stressor at a sub-lethal level may predispose individual belugas to greater susceptibility to mortality or long-term effects (e.g., reproductive failure) from other stressors.

Anything that affects the probability of reproduction or survival of an individual affects that individual’s fitness. Death can also result from different combinations and intensities of multiple stressors. Because body condition (one measure of health) varies among individual whales, deaths observed from the cumulative effects of multiple stressors are likely to occur over a period of time rather than as a single instantaneous event as progressively less robust individuals succumb. However, peaks in mortalities are likely to be associated with periods of greatest stress, such as over winter or during the birthing/nursing season. Environmental factors can also interact with other factors to impact beluga whale health. For example, a reduction in availability of preferred, high-lipid prey, such as salmon, will reduce individual body condition, increasing susceptibility to parasites, disease, and predation, and possibly reduce reproductive potential. Also, a period of restricted food access can cause belugas to use their fat reserves, resulting in the short-time release into the blood stream of contaminants that may have bioaccumulated in that tissue (Couillard et al. 2008a; Couillard et al. 2008b).

Cumulative impacts have been a long-standing issue in the debate over noise effects on marine mammals (Clark et al. 2009). The additive effects of multiple noise sources, as well as the combination of noise and other stressors, are of particular concern, but this field remains poorly understood (NRC 2005, Kuczaj 2007).

Cumulative effects include synergistic effects in which two stressors interact to cause greater harm than the sum of the effects of the individual component stressors. This is particularly relevant for marine mammals, including CI belugas, because potential cumulative effects are not well-understood in marine mammals generally and in CI belugas specifically. However, available scientific data, discussed below, highlights the concerns surrounding these potential cumulative effects, some of which are tied to stressors that are present in CI beluga habitat (e.g., chemicals, noise, presence of predators). For example, there is the potential for synergistic effects occurring as a result of co-exposure to certain chemical pollutants and noise. Ototoxins are substances that temporarily or permanently damage hearing. These chemicals can be absorbed through the respiratory tract, the skin, or the gastrointestinal tract. Understanding the effects of these compounds on the hearing of marine mammals is limited; however, hearing deficits have been established in cetaceans, including belugas, which were treated with aminoglycosides, a class of antibiotics known to be ototoxic (Finneran et al. 2005). When exposure to ototoxic chemicals is combined with exposure to noise, hearing loss is exacerbated by increasing both the breadth and severity of permanent threshold shifts; hearing loss can even occur at subtoxic chemical and sub-traumatic noise levels when neither exposure to the chemical nor noise would cause hearing loss in isolation (Steyger 2009). The synergistic effect of noise and organic solvents is more serious after repeated exposure at lower levels (Steyger 2009).

The synergistic effect between certain chemical pollutants and noise is of increasing concern in the marine environment, especially in coastal areas where chemical pollutants are concentrated. Well-known chemicals that, when combined with excessive noise exposure, can have synergistic effects on hearing in humans include organic solvents (e.g., paint, adhesive solvents, or fuel fumes), some insecticides, heavy metals like lead and mercury, and some clinical drugs known to impact hearing (e.g., aminoglycoside antibiotics). It has been shown that the physiological impact can exponentially increase if the individual is concurrently or sequentially exposed to these chemicals and noise. For example, loud noise and solvent inhalation by dockyard workers has proven to generate a hearing deficit five times stronger than the one generated just by the loud noise exposure (Sliwinska-Kowalska et al. 2004). Jet fuel vapor inhalation and jet noise exposure led to permanent hearing loss in laboratory rats; however, when rats were exposed to the same concentration of jet fuel but not exposed to noise, no effects on hearing were detected (Fechter et al. 2007). To our knowledge, these synergistic effects have not yet been described in marine mammals. However, the fact that CI beluga habitat is surrounded by many human activities that generate chemicals known to impact hearing (e.g., jet fuel from the airplane activity around the Inlet) and the fact that CI beluga habitat is noisy, raises the concern of potential synergistic effects on CI belugas from chemicals in the water and noise.

Another example of synergistic effects of multiple stressors is the toxicity among various contaminants that augment each other, whereas individual exposure to the same concentrations of those contaminants may yield little to no detectable effect (De Guise et al. 1998). There are well-documented examples of multiple stressors in terrestrial species that individually have little impact, but, when combined, can have major, negative, synergistic impacts that may cause death. For example, two studies (Relyea and Mills 2001; Relyea 2003) reviewed in Sih et al. (2004) found that several species of North American tadpoles exposed to the common pesticide carbaryl at a concentration only one-third of the recommended level suffered 10% mortality. However, when only the smell of a predatory newt was added, tadpole mortality increased to 80%, meaning that the introduction of the predator’s smell somehow increased the lethality of carbaryl eightfold. This synergistic effect was even more pronounced with bullfrog tadpoles: carbaryl alone caused only 2% mortality (indistinguishable from carbaryl-free controls), but when combined with the smell of predatory newts caused 92% mortality, a 46-fold amplification. This work showed that adding the stressor (the perceived risk of predation) to sublethal concentrations of carbaryl unexpectedly increased tadpole mortality, and the drastic increase in mortality did not require that actual predation take place.

In Chester Creek, a stream draining urban areas in Anchorage and directly discharging into Cook Inlet, the pesticide carbaryl was detected in high concentrations. This broad-spectrum insecticide, widely used throughout the Cook Inlet Basin to control spruce bark beetles, was detected in 79% of the samples from this creek (Glass et al. 2004) with concentrations as great as 0.33 µg/L. Fifteen percent of the samples had carbaryl levels that exceeded drinking water standards and Canadian guidelines (Canadian Council of Ministers of the Environment, 2009) for the protection of freshwater aquatic life (0.2 µg/L). Therefore, CI belugas in upper Cook Inlet near Chester Creek, and potentially in other streams with urban and residential watersheds, could be exposed to high levels of carbaryl. Since contaminants (e.g., the pesticide carbaryl) and predators (e.g., transient killer whales) may co-occur in the preferred beluga habitat, a potential for synergistic effects may exist, if, like in the case of the tadpoles, the contaminants make the exposed belugas more susceptible to predation. We note, however, that a direct comparison cannot be made between tadpoles and belugas, and we do not have information about the level of exposure to, or absorption of, carbaryl by CI belugas. Nevertheless, these studies underscore the possibility that CI belugas might be at risk from the negative synergistic effects as a result of co- exposure to anthropogenic noise, widespread pollutants, and the presence of transient killer whales (e.g., detecting their presence acoustically without the need of actual physical encounters).

Climate change can also amplify the effects of some contaminants as climate-driven changes in temperature, pH, and salinity can alter contaminant toxicity and bioavailability (Schiedek et al. 2007). For example, the half-life of the pesticide malathion increases substantially under a lower pH, suggesting increased persistence of this contaminant under expected conditions of climate- driven ocean acidification (Relyea 2004). Malathion serves here as an example of how contaminant toxicity may change as the climate changes. There is no evidence to suggest that this pesticide, with low toxicity for mammals, short half-life in water (2–18 days), and low level of use in Alaska, is a threat to CI belugas.

Relative Concern

Predicting cumulative effects is extraordinarily difficult, as it requires knowledge of a myriad of contextual factors for each exposure (e.g., acoustic exposure; contaminant exposure; predatory exposure), and synergistic effects can be very unpredictable (Wright et al. 2007). Because susceptibility varies among individuals in a population and because mortalities may be dispersed over time, factors contributing to cumulative effects are difficult to detect, making mitigation of these effects challenging. Stressors related to the current small population size of CI belugas, when combined with anticipated trends of increased anthropogenic impacts, can increase the likelihood of co-occurring and interacting multiple stressors that may combine effects to the detriment of the CI belugas’ recovery.

Moreover, stress resulting from anthropogenic noise, a threat of high relative concern, needs to be evaluated in combination with other stressors because noise has been demonstrated as a component of harmful synergistic effects in several animals and humans (Steyger 2009). Given the increase of human activities in Cook Inlet and the presence of contaminants in Cook Inlet and CI belugas, the trend for and likelihood of cumulative effects is increasing over time. Cumulative effects are categorized as a threat of high relative concern for CI belugas due to the following: 1) multiple stressors occur year-round and throughout range of CI belugas; 2) uncertainty regarding the magnitude of future cumulative effects; 3) uncertainty over the mechanisms of existing and future cumulative effects (including synergistic effects, if any); 4) difficulty in detecting impacts attributable to cumulative mechanisms; and 5) difficulty in effectively mitigating cumulative effects due to the occurrence of multiple stressors.