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Changes in the Acoustic Behavior of Gray Whales Eschrichtius Robustus in Response to Noise

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Changes in the Acoustic Behavior of Gray Whales Eschrichtius Robustus in Response to Noise Vol. 31: 227–242, 2016 ENDANGERED SPECIES RESEARCH Published October 31 doi: 10.3354/esr00759 Endang Species Res Contribution to the Theme Section ‘21st century paradigms for measuring and managing the effects of OPEN anthropogenic ocean noise’ ACCESS Changes in the acoustic behavior of gray whales Eschrichtius robustus in response to noise Marilyn Dahlheim1,*, Manuel Castellote2,3 1Alaska Fisheries Science Center, Marine Mammal Laboratory, 7600 Sand Point Way NE, Seattle, Washington 98115, USA 2Joint Institute for the Study of the Atmosphere and Ocean (JISAO), University of Washington, 3737 Brooklyn Avenue NE, Seattle, Washington 98105, USA 3Alaska Fisheries Science Center, Marine Mammal Laboratory, 7600 Sand Point Way NE, Seattle, Washington 98115, USA ABSTRACT: Gray whales Eschrichtius robustus, while engaged in underwater signaling, circum- vented noise in their environment by altering the structure and timing of their calls. Acoustic responses of whales to both naturally occurring and artificially increased levels of noise were documented during sound playback experimentation in San Ignacio Lagoon, Baja California Sur, Mexico. Nine acoustic parameters were examined and compared between experimental con - ditions: calling rates, call types, frequency range of calls (Hz), call peak frequencies (Hz), call received levels (dB re 1 µPa), call duration (s), percentage of calls showing frequency modulation, number of pulses per call, and call repetition rates (number of pulses s−1). Multiple acoustic strate- gies were employed by whales which enabled them to minimize the detrimental effect that noise had on their underwater signaling. When different sources of noise were added to their habitat, a corresponding increase was observed in calling rates, call received levels, frequency-modulated signals, number of pulses per call, and call repetition rates. Our results show that gray whales vary their calling behavior dependent upon the noise source, duration, and presentation. Acoustic responses to noise may also differ based on the behavioral activity of the whale (e.g. breeding, migrating, feeding) and on the habitat the whale is occupying (shallow lagoons, coastal or pelagic waters). Background noise (both natural and man-made) has a profound effect on the acoustic behavior of this coastal species and calling is modified to optimize signal transmission and recep- tion. Whether these modifications ensure that effective communication takes place in higher noise situations, without causing detrimental effects to individuals in the long term, remains to be tested. KEY WORDS: Gray whale · Acoustic behavior · Noise · Sound playback INTRODUCTION tially to levels that could threaten marine mammals on a global scale. The dramatic increase in human-generated ocean Increased noise levels have the potential to inter- noise over the last century has raised concerns about fere with or mask the acoustic signals of animals. the potential negative impact that increased noise Literature reviews on the effects of noise on animal levels may have on marine mammals (Richardson et communication report that many features of animal al. 1995, NRC 2003, 2005, Nowacek et al. 2007, signals change under increased noise levels, thereby Southall et al. 2007). Of particular concern is how reducing the detrimental effect of noise on their these increased levels of noise could potentially communication signals (e.g. Brumm & Slabbekoorn impact the low-frequency specialists such as baleen 2005, Barber et al. 2010, Bradbury & Vehrencamp whales (Clark et al. 2009). Ocean anthropogenic 2011, Shannon et al. 2016). Special attention has been noise will most likely continue to increase, poten- paid to the impact of noise on the acoustic communi- Outside the USA © The USA Government 2016. Open Access under Creative Commons by Attribution Licence. Use, distribu- *Corresponding author: [email protected] tion and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 228 Endang Species Res 31: 227–242, 2016 cation of many species, including frogs (e.g. Ten- (2009) suggested shipping noise as one of many nessen et al. 2014), birds (e.g. Parris & Schneider explanations for a long-term decrease in the funda- 2008), fish (Popper & Hastings 2009), cetaceans (e.g. mental frequency of eastern North Pacific blue whale Richardson et al. 1995), and other mammals (Rabin et Balaenoptera musculus song. Blue whales were al. 2003). A collective review of these studies sug- found to call more consistently in the presence of gests that these various taxa minimize the effects of seismic exploration noise, suggesting that this re - noise on their signaling by changes in either the sponse may represent a compensatory behavior on relative timing of their signals or in the structure of the part of the whales to the elevated ambient noise their calls. These short-term behavioral responses (Di Iorio & Clark 2010). Fin whale B. physalus improve signal detection and thus may contribute to acoustic communication was modified to compensate maintaining successful communication in noisy habi- for increased background noise by both chronic ship- tats (Slabbekoorn 2013); however, the long-term sub- ping noise and acute seismic survey noise. Blackwell lethal effects of noise on reproduction and survival et al. (2015) documented changes in bowhead whale remain poorly understood (Kight & Swaddle 2011). In Balaena mysticetus calling rates during the gradual addition to the impacts on acoustic behavior, ele- increase of seismic airgun activity in the Beaufort vated background noise can cause displacement Sea. The whales increased their calling rate until a from preferred or critical habitats (Bryant et al. 1984, plateau was reached, followed by a decrease until Dahlheim 1987, Seip et al. 2007, Castellote et al. calling ceased while noise levels continued to in - 2012). Adverse physical effects such as ear damage crease. Noise has also been shown to impact whales have also been demonstrated, as well as non-audi- by causing them to move out of the area. Castellote et tory physical effects such as physiological stress al. (2012) documented a major displacement of Medi- involving hormone responses leading to lowering of terranean fin whales by seismic survey noise that disease resistance, increased vulnerability to envi- persisted for a time period well beyond the duration ronmental stress, and hormone imbalances which of the disturbance. For gray whales Eschrichtius ro - may adversely affect reproduction (Creel et al. 2002, bus tus, surface behavioral reactions to underwater Rolland et al. 2012, Tennessen et al. 2014). noise have been directly observed for multiple activ- For marine mammals, especially cetaceans, hear- ities such as oil and gas exploration and production, ing constitutes their most important sensory process. aircraft overflights, and a variety of vessel activities A reduction in signal transmission or reception can including whale watching and dredging (Bryant et adversely affect the reproduction or even the sur- al. 1984, Malme et al. 1989, Moore & Clark 2002). vival of a given species that is dependent on such a Dahlheim (1987) documented a significant decline in sensory process. Thus, cetacean species, dependent the number of gray whales occupying Laguna San on acoustic signaling for spacing, attracting, effective Ignacio during noise playback experimentation. foraging, or alerting functions must overcome or be The gray whale, due to its preferred coastal habi- able to circumvent noise. tat, is exposed to a dynamic acoustic environment. As Several studies have shown high sensitivity to this species undergoes its annual migration from anthropogenic noise by mysticetes. The Lombard Alaska waters to the lagoons of Mexico it encounters effect, where signalers modify vocal characteristics a wide spectrum of both naturally occurring and such as level, pitch, and/or rate of signal production man-made sounds. Gray whale calls have been de - in a noisy environment to improve signal detection scribed from both the southern and northern regions (Lombard 1911), has been described for North of its habitat (Dahlheim et al. 1984, Moore & Ljung- Atlantic right whales Eubalaena glacialis (Parks et al. blad 1984), with most vocal activity occurring on the 2011), and humpback whale Megaptera novaean- southern breeding and calving grounds. Within the gliae (Dunlop et al. 2014). Parks et al. (2007) exam- shallow waters of Laguna San Ignacio, calls of gray ined both short-term and long-term behavioral whales most likely are heard and used by con- responses in calls produced by North Atlantic right specifics within a 5–6 mile (8–9.7 km) distance. The whales and South Atlantic right whales E. australis in distance over which different calls are produced and the presence of low-frequency noise. In high noise heard most likely varies in different coastal habitats. situations, right whales were documented to shift to a Throughout the species’ range, the function of their higher average fundamental frequency and call at a calls is unknown. Given grey whales’ limited call lower rate. The study indicated that right whales may repertoire (i.e. 6 call types) and frequency range of shift call frequency to compensate for increased the calls (40 Hz to 4 kHz) (Dahlheim et al. 1984, band-limited background noise. McDonald et al. Moore & Ljungblad 1984), what, if any, strategies Dahlheim & Castellote: Gray whale acoustic response to noise 229 could
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