Bubbles and Whale Strandings

The end of March saw the stranding of 19 adult pilot whales on Noordhoek beach on the western side of the Cape Peninsula, South Africa (see the News24 article). The strandings are the second on this particular beach in recent years, with 55 false killer whales beaching themselves in 2009. There are deep public divisions about what to do in such circumstances. Some want the animals to be “left alone”, and for “nature to take its course”. Others desperately want the animals saved, and bemoan the euthanisation of the whales. Despite this intense public interest (the authorities had to close off the area to keep the fascinated public at bay), the debate as to the causes of cetacean strandings still rages within the global scientific literature.

A stranded pilot whale on Noordhoek Beach, South Africa (see News24)

 The truth is that we simply do not know exactly what causes cetaceans (the scientific term given to whales and dolphins) to strand. Some papers suggest navigational disorientation due to anomalies in the magnetic field of a certain area is the cause of strandings. Because cetaceans utilise the magnetic field of the earth to navigate, a disruption in this system may cause the animals to “get lost” and head towards shore. Another theory is that the tight social groups of whales and dolphins is a cause – if one individual, especially if it is the ‘leader’ of a social group, becomes ill or injured the others will follow it when it beaches. An emerging explanation is that the increased ‘noise pollution’ in the ocean leads to a breakdown in the communication between whales, causing confusion and strandings. A more sinister follow on from that theme is that intense noises created by humans underwater (such as military sonar or underwater mining explosions) results in internal damage to the animals.

A mass stranding of pilot whales (from http://www.smh.com.au/news)

There is no doubt that anthropogenic (man-made) sounds have increased dramatically over the past century, due to the industrialisation of the world’s oceans. Shipping traffic, commercial activity such as oil drilling and exploration, research and military sources have all added to the din below the waves. I have had the privilege to listen to hydrophone recordings taken recently in False Bay of South Africa, and it has stuck me just how noisy it is down there – not just due to natural sounds of the waves and the dolphin dawn chorus, but because of boat traffic. We are particularly sensitive to the effects of pollution we can actually see – a seal entangled and drowned in an old net, an albatross hooked on a long line hook. But we also need to take into account those aspects of pollution we cannot see and how that affects the world around us.

Noise pollution frequencies in the ocean. Note how the noise generated by shipping falls right over the frequency band used by baleen whales to communicate; and how intense the frequencies of sonar are in comparison (from http://www.wired.com)

Sound travels a lot further and faster in water than in air, and marine mammals in particular utilize this very effectively for communication, hunting and orientation. It should be no surprise then that anthropogenic disturbances in the underwater realm have a marked impact on the physiology and behaviour of animals sensitive to sound. The issue needs to become a major conservation concern because it involves human behaviour influencing the behaviour of other organisms and in some cases, harming them. For example, baleen whales communicate by low frequency calls which happen to be on the same frequency band as the increasing ambient noise from shipping traffic (see Tyack, 2008). Does this decrease the range over which the whales communicate? Does it mask their calls or even confuse them? The effects of anthropogenic sounds on cetaceans in particular range from call silencing, displacement and temporary hearing loss to physiological injury of the hearing canal, internal bleeding and stranding. The effect is dependent on the level of noise (the intensity, amplitude and frequency). The most intense anthropogenic sound source comes from seismic exploration and sonar utilised by the military. 

 

An advert by the Whale and Dolphin Conservation Society (see www.wdcs.org/stop/pollution/)

Jepson and his colleagues published a brief communication in Nature in 2003 which discusses the impacts of military sonar on marine mammals. Even though it is not a recent publication, the intense public interest created in light of the recent strandings calls for the examination of the paper. In 2002, fourteen beaked whales were stranded in the Canary Islands (off the coast of Spain) close to where a mid-frequency military sonar exercise had been conducted.  The animals were dissected (as most stranded whales are, including those stranded at Noordhoek), and these autopsies revealed that the animals had not died of illness. However, there was widespread vascular congestion (the overfilling and swelling of the veins with blood as a result of an obstruction in the vessel) as well as prominent, widespread capillary haemorrhages due to the blocking of the blood vessels by blood clots and air bubbles. These bubbles in the blood vessels were also present in several vital organs. These bubbles and the associated damage of organs are usually associated with severe decompression sickness (the bends). If a human diver rises too quickly to the surface, dissolved gases come out of the blood and form bubbles inside the body as the pressure increases again. Cetaceans (deep diving beaked whales in particular) were thought to have physiological adaptations to cope with pressure changes as they dive, such as exhaling before diving or collapsing of lungs. Jepson et al (2003) argue that the formation of these bubbles may be due to changes in the diving behaviour these animals because of the sound disturbance, such as ascending from depth too quickly. It has also been suggested that sonar pulses force dissolved gas in the blood out of solution through changing pressures. These Canary Island strandings are not unique in the presence of bubble-associated tissue injury. Strandings around the world have revealed gas bubbles in blood vessels and gas-filled cavities in the functional parts of the vital organs. The liver was most affected, with gas-filled cavities taking up between 5 and 90% of the volume of the organ. These cavities are not filled with the bacteria associated with the decomposition of a body, and are therefore caused by something before death. 

So, what did cause the strandings of those pilot whales on the beautiful beach in Noordhoek? Necropsies are still taking place, and I look forward to the publication of the results. Until then, we will continue to ponder the deaths of these magnificent creatures. Was it natural? Or was it, once again, the fault of humans?

Psychiatric drugs and Fish

Psychiatric drugs used to alter behaviour in humans that find their way into aquatic systems are doing just that – altering the behaviour of the vertebrates in those systems. See the full paper here.

There is an increasing awareness and concern over the pollution of aquatic systems by pharmaceutical drugs worldwide. Anxiolytic drugs are commonly used to treat anxiety in humans, but when they enter the waterways in waste water, they are still biochemically active. This means that they persist in the system, especially since they are resistant to photodegredation (the decomposition of a compound by radiant energy from the sun). Although studies have been conducted into the effects of these chemical toxins on the biology of these systems (ecotoxicological studies), little is actually know about the ecological effects this pollution may have. Brodin et al (2013) have shown that exposure to these toxins change the behaviour and feeding rate of wild European perch – the fish show evidence of increased activity, decreased ‘sociality’ and a higher feeding rate. All these behaviours are considered important ecologically and evolutionarily because they affect how the fish interact, survive and reproduce. A change in these behaviours can lead to a change in the entire functioning of the ecosystem.

A brilliantly coloured European Perch (http://www.fishandfly.com)

This is the first study that actively shows changes in behaviour of organisms (in this case, fish) exposed to these toxins. Even though the concentrations in the natural environment are low, they are still there and are having an effect. There was a higher concentration of the drug in the tissue muscle of the fish than in the surrounding waters which indicated bioaccumulation, and leads to thoughts on the potential impacts this will have on those who consume the fish. The changes in behaviour induced by these toxins influence the aquatic community composition and thus, system function. This puts additional pressure on ecosystems already under stress from development, water extraction and other sources of pollution. It may impact the resilience of these systems to change, putting vulnerable systems at further risk along with the ecosystem services and goods these systems provide. We have to protect our freshwater sources and systems.

Fish behavioural responses to two concentrations (low: 1.8μg litre ^-1; high: 9108μg litre ^-1) of dissolved oxzazpam

compared to control treatment (08μg litre ^-1). (a) Activity, measured as level of swimming over 10 minutes (b) Boldness, measured as willingness to enter a new area during trial time (900s) (c) Sociability, measured as amount of time (seconds) spent close to another group. The error bars show standard error, and statistically significant differences between pre- and post-treatment is given by * (*p<0.05 or **p<0.001)  

[Brodin et al (2013) Science 338:814]

This study is no doubt an important one – the pollution of our freshwater systems is of major concern in the face of an increasing human population and potential future water shortages due to climate change. The study screened Swedish stream surface waters and found concentrations of oxazepam, a common anxiolytic drug, in both treated waters and in a mid-sized stream into which treated water flows. The fact that there are pharmaceutical products in these systems and that these are affecting the organisms in them can have major consequences in the potential usability of that water. No one wants to use water with psychiatric drugs still present in it! This also has major consequences for how we treat waste water, especially since these anxiolytic drugs remain biochemically active and do not decompose naturally, and thus continue to produce effects if taken into the body. The fact that these concentrations are comparable to those found in European and American waters should be cause for concern. The high demand for water in First World countries will no doubt spill over to the already water stressed Third World, with potential humanitarian issues. Pharmaceutical companies need to be made aware of this pollution, and incentives need to be devised to manufacture drugs with some foresight into where they will end up at the end of the chain. 

The strengths of this study include the neat and clean experimental design, as well as the utilisation of previously tried and tested techniques for quantifying behavioural change. However, the conclusions drawn by this study can be questioned - the concentrations of anxiolytic drugs the experimental fish were exposed were far higher than the concentrations reported out in the field. For example, the concentrations of oxazepam in Swedish streams were found to be 0.73 μg per litre in treated wastewater, and 0.58 μg per litre in a midsized stream receiving the input of treated water. Despite this, the experiment exposed fish to a “low” treatment concentration of 1.8 μg per litre, more than double that found in the wastewater effluent. The “high” exposure was at an impossible 910 μg per litre – of course the fish were going to show behavioural changes at such high dosages! There is no possible scenario where the concentrations of anxiolytic drugs will reach that level through wastewater input. 

Despite the shortcomings, this study has implications for my work as an ecologist - there is now a new factor to be considered when observing behaviour and ecosystem interactions. There are currently no studies of this sort here in South Africa, and so we don’t know what the implications of this may be on our systems. There is also no indication of the effects of this type of pollution on marine systems, but as most water systems lead to the ocean and as a large number of wastewater systems empty into the global ocean there must be some evidence, we just haven’t looked for it yet. Does the bioaccumulation of pharmaceutical products, as well as mercury, impact top marine predators such as tuna and sharks, and should we thus be cautious of consuming such fish? We do know however that anxiolytic drugs are not the only pharmaceuticals entering our waterways – the impacts of one such drug, oxazepam, on behaviour of European perch should alarm us all the more when we consider that there is a cocktail of pharmaceutical products found in waters worldwide, and that these may have direct compounding effects on behaviour and ecosystem function. The presence of pharmaceutical products in our water can be predicted to increase as they become more available for the growing human population, and thus new protocols must be implemented to determine the full impact these toxins have on our environment and ourselves.