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and/or inappropriate data interpretation (Popper and pressure changes, leading to tissue damage. The sec- Hastings, 2009). ond is when the solubility of gas in the blood and The lack of data is related to the considerable other fluids changes with pressure, thereby increas- difficulty in doing experiments on effects of pile ing when pressure increases and decreasing when driving under conditions in which the investigators pressure decreases. The swim bladder in the abdom- could not control the stimulus. In most pile driving inal cavity of most fish species is critical for buoy- studies to date, fishes were exposed to actual pile ancy control (as well as hearing and sound production driving operations. However, the frequency, mag- in some species). Changes in external pressure may nitude, and other aspects of the pile driving were cause rapid and substantial changes in the volume of controlled by the construction engineers and not the the swim bladder, causing its walls to move exces- investigators. Consequently, investigators did not sively and/or rupture. A ruptured swim bladder com- have control of any factors needed to understand and promises the fishes' swimming performance, thereby quantify the effects of pile driving on fishes (Popper increasing the risk for further injury or predation be- and Hastings, 2009). cause it cannot maintain buoyancy. A swim bladder The ideal pile driving experiments would enable that changes in size rapidly (whether it bursts or not) the investigators to fully control the pile driving can result in damage to nearby tissues. operation and define parameters such as number of In addition to the presence of a swim bladder in strikes, intervals between strikes, and sound inten- most species, fishes have gasses dissolved in their sity. However, this is generally not feasible in the blood and body tissues. At decompression, the amount field. At the same time, it is imperative that quantifi- of gas that can remain in solution decreases. When gas able data be obtained on the effects of pile driving leaves solution, it forms bubbles in the blood and body on fishes so that scientists, industry representatives, tissues. The presence of these bubbles increases the and regulators can make science-based assessments pressure in the vessels and, in the case of veins in of potential harm to fishes from a specific pile driv- particular, can cause their rupture. Gas bubbles in a ing operation. fish's circulatory system can disrupt the function or One suggested approach to circumvent the issue damage vital organs such as the heart, gills, kidney, of control of signal parameters has been to replicate gonads, and brain. The most severe effects, such as pile driving sounds in the laboratory. However, this bubbles in the gills or heart, may result in immedi- has not been possible until now because the sounds ate death at exposure from pile driving sounds. Even need to be far more intense than those producible by if an injury is not immediately Mortal, there may be even the best of underwater projectors. Further, even delayed mortality resulting from injury processes if such sounds could be produced in the laboratory, such as hemorrhaging, or there may be indirect mor- they might be sufficiently loud as to prevent humans tality resulting from predation if fish performance from being anywhere near the experiment for fear is decreased. of personal injury. Most important, any pile driving sounds used in the laboratory must be accurate rep- resentations of actual pile driving strikes and not just Study Rationale sounds that are very loud. Origin of Current Interim Criteria To date, the only regulation of the sound levels Potential Effects of Pile Driving Sounds from pile driving activities are interim physiological on Fish injury onset criteria being used for pile driving pro- Pile driving impulsive sound may produce sev- jects on the U.S. west coast. These levels were estab- eral types of effects on fishes. The one addressed lished in 2008 by a group of state agencies on the west here is referred to as barotrauma, or damage result- coast working in collaboration with the National ing from rapid change in pressure that directly Marine Fisheries Service (NMFS) and the U.S. Fish affects the body gases and thus affects body tissues. and Wildlife Service offices in that region (Wood- More specifically, two changes of gases in the body bury and Stadler, 2008; Stadler and Woodbury, of fish can lead to injury. The first is when free gas 2009). The interim criteria were peak sound pressure in the swim bladder, or in bubbles in the blood and (SPLpeak) of 206 dB re 1 Pa and a cumulative sound tissues of fishes expands and contracts during rapid exposure level (SELcum) of 187 dB re 1 Pa2s for 5
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fishes above 2 g and a SELcum of 183 dB re 1 Pa2s Recent Studies Relevant to Interim Criteria for fishes below 2 g. However, the agreement specif- Subsequently to setting the U.S. west coast ically designated the criteria as interim, and the interim criteria, Ruggerone et al. (2008) investi- agencies were committed to "review the science gated the effects of pile driving exposure on caged periodically and revise the threshold and cumulative yearling Coho salmon (Oncorhynchus kisutch) mea- levels as needed to reflect current information" suring approximately 90121 mm in fork length (Stadler and Woodbury, 2009). (FL, weight not given). Fish were placed in cages The NMFS also recognized that there is a "reset- near the piles being driven and exposed to sound ting" of SELcum after 12 hours of non-exposure from 1,627 strikes over a 4.3-hour period. Peak (Stadler and Woodbury, 2009). Thus, the SELcum for sound pressure levels were as high as 208 dB re a fish during a pile driving operation is reset to 0 for 1 Pa, and SELss reached 179 dB re 1 Pa2s, leading the next set of exposures if there is a 12-hour period to a SELcum of approximately 207 dB re 1 Pa2s. The between the end of the first pile driving exposure study used controls, and there were no reported and the start of the next. This "resetting" was specific for recovery from temporary effects to the hearing effects on body tissues. However, this study did not of exposed fish, not barotrauma. permit test fish the opportunity to fill their swim In preparation for the 2008 decision, the Califor- bladders prior to exposure; therefore, the study nia Department of Transportation (Caltrans) asked results are not applicable to coho salmon in the wild. a group of internationally known investigators to Absence of acclimation to neutral buoyancy prior to review the literature on effects of sound on fishes exposure to changes in pressure effectively removes and to make recommendations on possible criteria. changes in the volume of the swim bladder as a source This resulted in two memos (Popper et al., 2006; of barotrauma either to the swim bladder or other tis- Carlson et al., 2007) that examined the best available sues and organs that may be affected by changes in science and then proposed interim criteria based on swim bladder volume (i.e., fish would be protected those data. In the 2006 memo, Popper et al., (2006) from barotrauma damage). developed a strong case for using a single-strike In a study at Mad River, California, juvenile sound exposure level (SELss) of 187 dB re 1 Pa2s steelhead salmon (Oncorhynchus mykiss), measur- and a SPLpeak of 208 dB re 1 Pa. This was the first ing 55117 mm FL and weighing 1.4917.43 g, attempt to use dual-criteria to protect fishes from were exposed to pile driving signals at different dis- physiological injury resulting from exposure to pile tances (ranging from about 35 m to 150 m) from the driving. The dual-criteria was adopted by the authors, source (Caltrans, 2010a, 2010b). The juvenile salmon and later by NMFS, with the idea that the SELss value were exposed to peak SPLs ranging from 169 to confines the total acoustic energy fishes may experi- 188 dB re 1 Pa and SELcum ranging from 179 to 194 ence by exposure to a single impulsive sound, while dB re 1 Pa2s. the peak sound pressure level protects fishes from an The Mad River study was well designed and had especially strong excursion in pressure within the appropriate controls, properly performed pathology, sound impulse. and appropriate recordings of received sound levels. Carlson et al. (2007) used additional data to that On-site necropsies and histopathology results showed available to Popper et al. (2006) to propose SELcum no mortality and no tissue damage that could be values for onset of tissue damage that depended on related to pile driving to fish exposed to SELcum as fish mass. Carlson et al. (2007) suggested that for high as 194 dB 1 Pa2s, and no statistically signifi- fishes above 2 g (small larvae), the SELcum value for cant differences between experimental and control non-auditory tissue damage should be 190 dB re animals were detected (Caltrans, 2010b). Higher 1 Pa2s, and for fishes below 1 g, they suggested an sound levels were not used, but considering that there SELcum of 183 dB re 1 Pa2s. Carlson and his col- were no differences in tissue effects between exposed leagues made the important point that as fishes get and control, it is reasonable to suggest that injury larger the exposure value must be increased further. onset is at sound levels above 194 dB re 1 Pa2s Most pertinently, Carlson et al. (2007) recom- SELcum, and likely well above this level. mended a conservative value of 197 dB SELcum for In yet another study, Houghton et al. (2010) fishes above 8 g, and a value above 213 dB SELcum exposed 133 caged juvenile coho salmon (Onco- for fishes over 200 g. rhynchus kisutch) measuring approximately 6