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Discovery of Sound in the Sea
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Strandings

The term stranding refers to an aquatic animal, especially a marine mammal, landing on a beach or in shallow water, dead or sometimes alive, and probably in distress. Observations as far back as Aristotle and illustrations from the Middle Ages show us that marine mammals have been stranding for millennia.

Drawing of a stranded whale in Katwijk, the Netherlands, in 1598.
Drawing of a stranded whale in Katwijk, the Netherlands, in 1598. Image courtesy of World News Network.

In the U.S. alone, about 1,000 cetaceans and 2,500 pinnipeds strand annually. Some animals strand live and are returned to sea. Others die at sea or on shore. Animals may strand singly or in groups. When 3 or more animals strand together in time and place, it is called a mass stranding. Some species, such as pilot whales, mass strand fairly often. Whether strandings are single or mass, strandings are a concern for conservationists and biologists. Determining the cause of a stranding or death of a stranded animal is difficult. Scientists must reconstruct what happened, but have little or no information about the animal’s history or the circumstances that preceded the stranding. On average, a cause of death can be determined in only about half of all stranding cases.

Bar graph showing the total number of cetacean and pinniped strandings in the U.S. from 1992-2002
Total number of strandings of cetaceans (yellow bars) and pinnipeds (blue bars) in the U.S. each year from 1992-2002. Data provided by Janet E. Whaley and Teri K. Rowles, NOAA Marine Mammal Health and Stranding Response Program.

One controversial and unresolved issue is how the use of military sonar relates to strandings, particularly strandings of some species of beaked whales [1] [2] [3]. Mass strandings of beaked whales are rare; a review of all beaked whale strandings from 1874 to 2004 found only 136 mass stranding events [3]. This study ranked each stranding by the quantity and quality of data available in order to determine whether a correlation existed between use of naval sonar and the strandings. They found only 12 stranding events for which there was evidence that naval activity and a stranding coincided in space and time. These events had three consistent features: (1) the stranding locations were less than 80 km from the 1,000-m depth contour (that is, where deep water occurs near shore); (2) 8 out of the 12 stranding events occurred in areas where beaked whale mass strandings had previously been reported; and (3) all 12 events included Cuvier’s beaked whales (Ziphius cavirostris), a species that does not commonly mass strand. Another analysis examining the correlation between sonar use and beaked whale mass strandings found that strandings were correlated with naval activity in the Mediterranean and Caribbean seas, but not off the coasts of Japan, the eastern United States, and southern California [4]. This suggests that there are locations with certain characteristics that may contribute to stranding events.

Because reported mass stranding events involving beaked whales coincided closely in time and space with military exercises by several nations that used sonar, it is important to understand what role sound may have played in these strandings. Although these strandings are closely related to the operation of military sonars in time and location, the mechanism by which the sonars might have caused the strandings is still not explained. In two well-documented cases, there is sufficient information about the sonar operations, the times and locations of the strandings, and the nature of the injuries to the animals to determine that multiple sonar and multi-ship exercises with sonar contributed to the strandings. These events occurred in Greece (1996) and the Bahamas (2000). In two of the remaining mass stranding events that coincided with naval sonar activities (Madeira and Portugal in May 2000 and the Canary Islands in 2002), there is insufficient information about the timing and location of the strandings vs. naval activity to make a strong association, however necropsies that were performed (described below) on some of the animals found injuries similar to those seen in the Bahamian cases. There are currently few scientific publications that describe and discuss these strandings, and many of these publications were released without independent scientific review. Nevertheless, these reports about the four stranding events, discussed below, can help us understand ways in which scientists think that the use of sonar may have resulted in the strandings.

Map showing the locations of the four best-documented beaked whale strandings that coincided with military activities involving the use of sonars.
Locations of the four best-documented beaked whale strandings that coincided with military activities involving the use of sonars. Two minke whales also stranded during the incident in the Bahamas in 2000.


Overview of the Stranding Events
Greece 1996: In May, 1996, twelve Cuvier's beaked whales stranded along 38 kilometers of the Greek coastline in the Mediterranean Sea [5]. This stranding coincided with a nearby military exercise conducted by the SACLANT Centre, a scientific research organization associated with the North Atlantic Treaty Organization (NATO). The exercise used sonars at frequencies of 450-700 Hz and 2.8-3.3 kHz. This incident is described in both a NATO report [6] and in a published scientific paper [5]. The stranding responders in the area did not have enough equipment or skilled personnel to perform necropsies at the time and did not obtain the necessary tissue samples to determine the cause of death.

Bahamas 2000: Fourteen beaked whales, one spotted dolphin, and two minke whales were reported stranded in the Northern Bahamas Islands on March 15 and 16, 2000. Six beaked whales and 1 spotted dolphin died during this event. The strandings coincided in time (within a 36-hour period) and in space (along a 240-km arc) with the passage of five U.S. Navy ships taking part in an exercise that also used mid-frequency (1-10 kHz) sonars. The incident has been described in a preliminary report issued jointly by the U.S. Navy and the National Marine Fisheries Service [1] and a peer-reviewed publication of the necropsy results [7]. The stranded animals that died were examined for injuries by scientists and veterinarians [7] [8]. The spotted dolphin stranded on the opposite side of the island chain from the beaked whales and was found to be malnourished with evidence of chronic, debilitating disease in multiple major organs. It was decided that this animal’s stranding was a coincidence and was not related to the mass stranding event. In contrast, the beaked whales that stranded were all in good condition with no evidence of significant disease, but blood was found in and around the ears in several of the animals. The reports concluded that the animals died from hyperthermia when they beached (overheating due to their inability to perspire and cool the body) and that they did not die from the bleeding seen in the heads, but the blood deposits were an unusual, previously unreported observation.

Madeira 2000: Three Cuvier’s beaked whales mass stranded near Madeira, Portugal between 10 and 14 May 2000 [9]. A fourth animal was reported floating in the water by a fisherman, but it did not come ashore. A NATO naval exercise off Portugal started just one day prior to the stranding (from May 9 to May 14, 2000). The head of one beaked whale was in adequate condition to be examined [8]. It was found to have blood in and around the eyes, ears, and brain. This animal and another that were also examined on site were also found to have lung hemorrhaging.

Canary Islands 2002: In September, 2002, a mass stranding of fourteen beaked whales occurred in the Canary Islands. This stranding began about four hours after the start of a nearby NATO naval exercise involving ships of many nations that were using several types of mid-frequency sonar. The details of the sonar transmissions that occurred are not available. Ten of the stranded animals were found to have gas bubbles and hemorrhages in several organs [10] [11].

Hypotheses
A number of explanations have been proposed for the observed injuries in the animals that stranded in the areas of sonar exercises. These tentative explanations, called hypotheses need to be tested through experiments and checked for consistency in any further observations in order to determine whether they are correct.

Acoustic resonance: One proposed hypothesis that was ultimately found to be unlikely was that hemorrhages occurred because some air-filled tissues (such as the lungs and head sinuses) resonated when exposed to the sonars, causing blood vessels nearby to rupture. For resonance-related motion to cause injury, the tissues would need to move at very large amplitudes. NOAA held a workshop in 2003 to discuss the effects of acoustic resonance in cetaceans (for more information see Report of the Workshop on Acoustic Resonance as a Source of Tissue Trauma in Cetaceans). The workshop concluded that acoustic resonance at the received sound levels and frequencies [12] would have caused tissue movements in the nanometer range, which is far too small to cause injury. Further, key air spaces in the animals examined did not contain hemorrhages. Even more important, because of similarities in lung and sinus structures among toothed whale species, resonance should have damaged most of the species in the vicinity, but only beaked whales stranded.

Decompression Sickness: Another hypothesis that has been proposed to explain the gas bubbles and tissue damage observed in the strandings in the Canary Islands is that the animals experienced decompression sickness (DCS) [10] [11]. Scientists suggested that beaked whales might have changed their diving pattern in response to the sounds and come to the sea surface faster than normal, causing bubbles to form in their tissues. Some tests have been carried out to determine the probability that this hypothesis is correct. Data from bottlenose dolphins show that rapidly diving animals may accumulate nitrogen in their muscles. The same model of nitrogen accumulation was applied to the diving behavior of the northern bottlenose whale, a beaked whale, and a blue whale, a baleen whale [13]. Their results suggested that in long dives, supersaturation levels as much as 300% might occur. In addition, other studies suggest that if animals stay at the surface longer than normal or otherwise change their diving behavior, they might increase their risk for decompression sickness [14] [15] [16] [17]. However, a study of a trained bottlenose dolphin that completed 10-12 dives to depths of 30, 50, 70, or 100 m showed no indication of gas bubbles or elevated blood nitrogen levels, not supporting the hypothesis that nitrogen accumulates during repetitive dives [13]. This hypothesis is still being debated and more research is needed to evaluate it.

The hypotheses about bubbles in the bodies being related to DCS overlook the fact that bubbles form fairly rapidly in any animal that has recently dived and dies, so bubbles in a body are not sufficient evidence to diagnose DCS. DCS is a complex syndrome with many components that result in the injury or death of the diver. Bubbles are just part, but not all, of that mechanism. The evidence in the stranded animals is not consistent with DCS’s characteristic set of symptoms and its known mechanisms for injury. In many cases the bubbles reported in the whales are too large or are found in the wrong organs for DCS. Even more important, none of these hypotheses explains a key element of the strandings, which are why beaked whales are the one group that strands.

The gas bubbles and tissue damage that have been observed could have resulted from many causes, some that are not related to sound [2]. A recent report has found degeneration in the bones of sperm whale specimens collected over the last 111 years [18]. Scientists hypothesized that this degeneration is due to bubble formation associated with DCS unrelated to sound exposure. However, these scientists did not consider the possibility that diseases like arthritis or infections may have caused the abnormal appearance in any of these bones. Thus, the decompression sickness hypothesis has not been fully tested as an explanation for observations in the bones of sperm whales, and is not considered a fully explored or accepted explanation of mass strandings.

Diffusion: Another hypothesis put forth to explain the cause of tissue damage is that sound causes bubbles to form or expand in tissues that are supersaturated with nitrogen. One way this could happen is through a process called rectified diffusion [19]. In this case, sound causes small bubbles, which normally exist in the blood and tissues, to grow larger. It is unlikely that this process caused the tissue damage observed in the Bahamas stranding because the levels of sound exposure required to produce rectified diffusion experimentally are greater than were possible from the sonars by several orders of magnitude. This does not eliminate the possibility that static diffusion occurred, but to date, this mechanism has not been explored or determined to be sufficient to produce tissue damage in marine mammals [13] [2] [20].

Environmental Conditions: Research into the acoustic sources and transmission of sound in areas in which the Greece, Bahamas, Madeira, and Canary strandings occurred showed three common characteristics [21]. First, in each location, there is deep water close to land, such as submarine canyons. Second, the sources transmitted series of sound pulses at depths shallower than 10 m (33 ft) while moving at speeds of 2.6 m/s (5.1 kts) or more. Finally, since sound speed is dependent on water depth and temperature, some of the transmitted sound remained near the surface and decreased in level more slowly than would be the case under other conditions. Whether these acoustic characteristics influenced the probability that beaked whales detected the sounds, increased the effects of the sounds through greater propagation, or were not relevant remains unclear. The fact that there are common and relatively unique ocean characteristics in the areas of these four stranding events means that they may be worth considering, and that avoiding exercises in areas that are similar may help reduce the risk of stranding from future naval sonar activity.

Behavioral Response: Another hypothesis suggests that the strandings may have more to do with a number of reactions and sensitivities of this group of animals, such as disturbances in their foraging areas that cause unique behavioral reactions, rather than a direct physical cause related to sound-induced injury from sonar specifically.

Scientists are investigating this hypothesis with a series of studies of the behavioral responses of beaked whales to the playback of certain sounds. The first two phases took place at the Navy’s Atlantic Undersea Test and Evaluation Center (AUTEC) Range off Andros Islands, Bahamas, and the third phase was in the Mediterranean Sea. The AUTEC Range includes several hydrophones on the seafloor that can detect vocalizing animals. Scientists also went out in small vessels to attach tags to animals in order to record their dives and movements. A total of 16 acoustic tags were attached to individuals of four cetacean species over the three studies. Significant advances in understanding basic diving and vocal behavior were made and nine controlled exposures were conducted using simulated military, mid-frequency sonar sounds, killer whale calls, and “control” noise. During the AUTEC studies, researchers found that when tagged Blainville’s beaked whales were exposed to all three sounds during deep foraging dives, they stopped echolocating and slowly ascended while moving away from the sound source [22]. The whales reacted to the killer whale calls at much lower sound levels than they did for the sonar and control noise. However, they did not react to the anthropogenic sounds at the same level as they did for sounds of potentially lethal predators.

The next phase is a five-year project off southern California Additional studies are needed to identify whether these initial observations are generally applicable in other circumstances, and to extend studies to previously untested species such as large baleen whales, seals, and sea lions.

Future Research
Much more scientific research is needed to understand why a relationship in time and location exists between some beaked whale mass strandings and the use of multiple, mid-frequency sonars in critical areas [2]. At present, we still do not have an answer. Science is an evolving process and future work may help us further understand what we are observing.