Peer-Reviewed Studies on the Effects of Anthropogenic Noise on Marine Invertebrates: From Scallop Larvae to Giant Squid

Chapter on proceedings of conference "the Effects of Noise on Aquatic Life II" published as a book by Springer (pp 17-26

Tracking the kinematics of caudal-oscillatory swimming : a comparison of two on-animal sensing methods

Funding: Marie Sklodowska Curie Career Integration Grant and by The Marine Alliance for Science and Technology for Scotland (MASTS).Studies of locomotion kinematics require high-resolution information about body movements and the specific acceleration (SA) that these generate. On-animal accelerometers measure both orientation and SA but an additional orientation sensor is needed to accurately separate these. Although gyroscopes can perform this function, their power consumption, drift and complex data processing make them unattractive for biologging. Lower power magnetometers can also be used with some limitations. Here, we present an integrated and simplified method for estimating body rotations and SA applicable to both gyroscopes and magnetometers, enabling a direct comparison of these two sensors. We use a tag with both sensors to demonstrate how caudal-oscillation rate and SA are adjusted by a diving whale in response to rapidly changing buoyancy forces as the lungs compress while descending. Both sensors gave similar estimates of the dynamic forces demonstrating that magnetometers may offer a simpler low-power alternative for miniature tags in some applications.PostprintPeer reviewe

Sperm whale predator-prey interactions involve chasing and buzzing, but no acoustic stunning

Field work in Norway was funded by the Carlsberg Foundation and the National Danish Research Council to PTM. The NMFS study was funded by the U.S. Mineral Management Service. MJ is funded by the Marine Alliance for Science and Technology, Scotland, and by a Marie Curie Career Integration Grant. MW was funded by the Danish Council for Independent Research, Natural Science and NAS is currently funded by a EU Horizon 2020 MSC Fellowship.The sperm whale carries a hypertrophied nose that generates powerful clicks for long-range echolocation. However, it remains a conundrum how this bizarrely shaped apex predator catches its prey. Several hypotheses have been advanced to propose both active and passive means to acquire prey, including acoustic debilitation of prey with very powerful clicks. Here we test these hypotheses by using sound and movement recording tags in a fine-scale study of buzz sequences to relate the acoustic behaviour of sperm whales with changes in acceleration in their head region during prey capture attempts. We show that in the terminal buzz phase, sperm whales reduce inter-click intervals and estimated source levels by 1-2 orders of magnitude. As a result, received levels at the prey are more than an order of magnitude below levels required for debilitation, precluding acoustic stunning to facilitate prey capture. Rather, buzzing involves high-frequency, low amplitude clicks well suited to provide high-resolution biosonar updates during the last stages of capture. The high temporal resolution helps to guide motor patterns during occasionally prolonged chases in which prey are eventually subdued with the aid of fast jaw movements and/or buccal suction as indicated by acceleration transients (jerks) near the end of buzzes.Publisher PDFPeer reviewe

Gait switches in deep-diving beaked whales : biomechanical strategies for long-duration dives

Work in the Canary Islands was funded by the Office of Naval Research and the National Oceanographic Partnership Program (NOPP), by a consortium consisting of the Canary Islands Government, the Spanish Ministry of Environment and the Spanish Ministry of Defense and by the European environmental funding LIFE-INDEMARES program for the inventory and designation of the Natura 2000 network in marine areas of the Spanish territory, headed by Fundacion Biodiversidad, with additional support from the Cabildo Insular of El Hierro. Fieldwork in the Ligurian Sea was funded by NOPP. Research in the Gully was funded by the Strategic Environmental Research and Development Program (SERDP) programs RC-2113 and RC-2337. L.M.M.L. was funded by a ‘la Caixa’ Fellowship within the 2010 UK Framework Programme. N.A.d.S. was funded for this study by ONR and by the EU FP7 Marie Curie project SOUNDMAR. M.J. was funded by a Marie Curie Career Integration Grant, and from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.Diving animals modulate their swimming gaits to promote locomotor efficiency and so enable longer, more productive dives. Beaked whales perform extremely long and deep foraging dives that probably exceed aerobic capacities for some species. Here, we use biomechanical data from suction-cup tags attached to three species of beaked whales (Mesoplodon densirostris, N = 10; Ziphius cavirostris, N = 9; and Hyperoodon ampullatus, N = 2) to characterize their swimming gaits. In addition to continuous stroking and stroke and-glide gaits described for other diving mammals, all whales produced occasional fluke-strokes with distinctly larger dorsoventral acceleration, which we termed 'type-B' strokes. These high-power strokes occurred almost exclusively during deep dive ascents as part of a novel mixed gait. To quantify body rotations and specific acceleration generated during strokes we adapted a kinematic method combining data from two sensors in the tag. Body rotations estimated with high-rate magnetometer data were subtracted from accelerometer data to estimate the resulting surge and heave accelerations. Using this method, we show that stroke duration, rotation angle and acceleration were bi-modal for these species, with B-strokes having 76% of the duration, 52% larger body rotation and four times more surge than normal strokes. The additional acceleration of B-strokes did not lead to faster ascents, but rather enabled brief glides, which may improve the overall efficiency of this gait. Their occurrence towards the end of long dives leads us to propose that B-strokes may recruit fast-twitch fibres that comprise similar to 80% of swimming muscles in Blainville's beaked whales, thus prolonging foraging time at depth.PostprintPeer reviewe

Single-click beam patterns suggest dynamic changes to the field of view of echolocating Atlantic Spotted Dolphins (Stenella frontalis) in the wild

The study was funded by frame grants from the Danish Natural Science Foundation to P.T.M. and M.W., and by the National Oceanographic Partnership Programme via a research agreement between La Laguna University (N.A.d.S.) and the Woods Hole Oceanographic Institution (M.J.). F.H.J. was supported by the Danish Council for Independent Research | Natural Sciences, and is currently funded by a postdoctoral fellowship from the Carlsberg FoundationEcholocating animals exercise an extensive control over the spectral and temporal properties of their biosonar signals to facilitate perception of their actively generated auditory scene when homing in on prey. The intensity and directionality of the biosonar beam defines the field of view of echolocating animals by affecting the acoustic detection range and angular coverage. However, the spatial relationship between an echolocating predator and its prey changes rapidly, resulting in different biosonar requirements throughout prey pursuit and capture. Here, we measured single-click beam patterns using a parametric fit procedure to test whether free-ranging Atlantic spotted dolphins (Stenella frontalis) modify their biosonar beam width. We recorded echolocation clicks using a linear array of receivers and estimated the beam width of individual clicks using a parametric spectral fit, cross-validated with well-established composite beam pattern estimates. The dolphins apparently increased the biosonar beam width, to a large degree without changing the signal frequency, when they approached the recording array. This is comparable to bats that also expand their field of view during prey capture, but achieve this by decreasing biosonar frequency. This behaviour may serve to decrease the risk that rapid escape movements of prey take them outside the biosonar beam of the predator. It is likely that shared sensory requirements have resulted in bats and toothed whales expanding their acoustic field of view at close range to increase the likelihood of successfully acquiring prey using echolocation, representing a case of convergent evolution of echolocation behaviour between these two taxa.PostprintPeer reviewe

Condición corporal del calderón de aleta corta (Globicephala macrorhynchus) en el Suroeste de Tenerife a partir de fotogrametría.

La estima de la condición corporal de los animales es fundamental para monitorizar el estado de salud de sus poblaciones. Debido a la dificultad de medir animales salvajes de gran tamaño, la condición corporal de cetáceos en libertad ha sido poco estudiada. En el presente estudio registramos video de alta calidad en 4K con un vehículo aéreo no tripulado o dron (DJI Inspire 1 Profesional equipado con cámara Zenmuse) para obtener imágenes aéreas cenitales de ejemplares de calderón tropical (Globicephala macrorhynchus) en su hábitat natural en el Suroeste de Tenerife, con el objetivo de estimar la longitud absoluta de los individuos así como su condición corporal. La estima de la longitud y amplitud de cada individuo (en píxeles) se realizó con el programa paint.net; su condición corporal fue estimada a partir de la división de su amplitud entre su longitud. Se realizaron un total de 5 vuelos, con una duración total de 13 min y 10 s, en los que se registraron un total de 8 individuos. La longitud media de los animales fue 3,1 m (SD = 1,18, rango = 2,35 - 5,83). La amplitud media, medida justo por detrás de la aleta dorsal, de los animales fue 0,5 m (SD = 0,42, rango = 0,32 - 1,54). La calidad de las imágenes se evaluó utilizando una escala del 1 al 3 (de mejor a peor calidad), siendo el 25% de calidad 1, 50% de calidad 2 y 25% de calidad 3. La media del índice de condición corporal fue de 0,15 (SD = 0,016, rango 0,13 - 0,27), siendo la talla media de los individuos con índice corporal por encima de la media de (N = 6) 2,57 m, mientras que los animales con índice corporal por debajo de la media tuvieron una talla media de 4,65 m (N = 2). Los resultados indican que, los individuos de menor tamaño poseen un mayor índice de condición corporal y en general éste disminuye con el desarrollo a estado adulto del individuo, en relación a los costes derivados de la reproducción, alimentación y/o cuidado aloparental en los individuos adultos. El estudio a largo plazo de la condición corporal de los individuos, permitirá monitorizar el estado de conservación de esta población, así como su comparación con poblaciones existentes en zonas con menor actividad humana, a efectos de identificar posibles factores de impacto.<br /

Sperm whale echolocation behaviour reveals a directed, prior-based search strategy informed by prey distribution

The fieldwork was funded by a grant from the Carlsberg Foundation to B. Møhl and ONR, SERDP and FNU grants to MJ, PJOM and PTM. PJOM was supported by a Royal Society Fellowship, NAS by the International Campus of Excellence of the Canary Islands, MJ by the Marine Alliance for Science and Technology for Scotland and AF partly by project CETOBAPH (grant number CGL2009-1311218).Predators make foraging decisions based upon sensory information about resource availability, but little is known about how large, air-breathing predators collect and use such information to maximize energy returns when foraging in the deep sea. Here, we used archival tags to study how echolocating sperm whales (Physeter macrocephalus) use their long-range sensory capabilities to guide foraging in a deep-water habitat consisting of multiple, depth-segregated prey layers. Sperm whales employ a directed search behaviour by modulating their overall sonar sampling with the intention to exploit a particular prey layer. They forage opportunistically during some descents while actively adjusting their acoustic gaze to sequentially track different prey layers. While foraging within patches, sperm whales adjust their clicking rate both to search new water volumes as they turn and to match the prey distribution. This strategy increases information flow and suggests that sperm whales can perform auditory stream segregation of multiple targets when echolocating. Such flexibility in sampling tactics in concert with long-range sensing capabilities apparently allow sperm whales to efficiently locate and access prey resources in vast, heterogeneous, deep water habitats.PostprintPeer reviewe

Beaked whales echolocate on prey

Author Posting. © Royal Society, 2004. This article is posted here by permission of Royal Society for personal use, not for redistribution. The definitive version was published in Biology Letters 271: Supplement 6 (2004): S383-S386, doi:10.1098/rsbl.2004.0208.Beaked whales (Cetacea: Ziphiidea) of the genera Ziphius and Mesoplodon are so difficult to study that they are mostly known from strandings. How these elusive toothed whales use and react to sound is of concern because they mass strand during naval sonar exercises. A new non-invasive acoustic recording tag was attached to four beaked whales (two Mesoplodon densirostris and two Ziphius cavirostris) and recorded high-frequency clicks during deep dives. The tagged whales only clicked at depths below 200 m, down to a maximum depth of 1267 m. Both species produced a large number of short, directional, ultrasonic clicks with no significant energy below 20 kHz. The tags recorded echoes from prey items; to our knowledge, a first for any animal echolocating in the wild. As far as we are aware, these echoes provide the first direct evidence on how free-ranging toothed whales use echolocation in foraging. The strength of these echoes suggests that the source level of Mesoplodon clicks is in the range of 200-220 dB re 1 μPa at 1 m. This paper presents conclusive data on the normal vocalizations of these beaked whale species, which may enable acoustic monitoring to mitigate exposure to sounds intense enough to harm them.Tag development was funded by a Cecil H. and Ida M. Green Award and the US Office of Naval Research. Fieldwork was funded by the Strategic Environmental Research and Development Program (SERDP) under program CS-1188, the Packard Foundation, and the Council of Environment of the Canary Islands, and was supported by University of La Laguna, BluWest, SACLANT Undersea Research Centre, and the Government of El Hierro

Fear of killer whales drives extreme synchrony in deep diving beaked whales

Canary Islands: ONR grants N00014-16-1-2973 and N00014-16-1-3017, and the Spanish Central Government Plan Nacional DeepCom CTM2017-88686-P. PLT was supported by ONR grant N00014-18-1-2062 and PLT and MJ acknowledge the support of the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) in the completion of this study. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. FV and fieldwork at the Azores were supported by ONR grants N00014-15-1-2341 and N00014-17-1-2715 and by the Dutch Research Council (award number 016.Veni.181.086). NAS, PA and JA were funded for writing this paper by Ramon y Cajal, Agustín de Bethencourt and FPU grants from the Spanish Ministry and Cabildo de Tenerife, respectively.Fear of predation can induce profound changes in the behaviour and physiology of prey species even if predator encounters are infrequent. For echolocating toothed whales, the use of sound to forage exposes them to detection by eavesdropping predators, but while some species exploit social defences or produce cryptic acoustic signals, deep-diving beaked whales, well known for mass-strandings induced by navy sonar, seem enigmatically defenceless against their main predator, killer whales. Here we test the hypothesis that the stereotyped group diving and vocal behaviour of beaked whales has benefits for abatement of predation risk and thus could have been driven by fear of predation over evolutionary time. Biologging data from 14 Blainville’s and 12 Cuvier’s beaked whales show that group members have an extreme synchronicity, overlapping vocal foraging time by 98% despite hunting individually, thereby reducing group temporal availability for acoustic detection by killer whales to <25%. Groups also perform a coordinated silent ascent in an unpredictable direction, covering a mean of 1 km horizontal distance from their last vocal position. This tactic sacrifices 35% of foraging time but reduces by an order of magnitude the risk of interception by killer whales. These predator abatement behaviours have likely served beaked whales over millions of years, but may become maladaptive by playing a role in mass strandings induced by man-made predator-like sonar sounds.Publisher PDFPeer reviewe

Spatio-temporal variation in click production rates of beaked whales : implications for passive acoustic density estimation

T.A.M. was funded under Grant No. N000141010382 from the Office of Naval Research (LATTE project) and thanks support by CEAUL (funded by FCT - Fundação para a Ciência e a Tecnologia, Portugal, through the project UID/MAT/00006/2013). M.P.J. was funded by a Marie Curie Career Integration Grant and M.P.J. and P.L.T. were funded by MASTS (The Marine Alliance for Science and Technology for Scotland, a research pooling initiative funded by the Scottish Funding Council under grant HR09011 and contributing institutions). L.S.H. thanks the BRS Bahamas team that helped collect the Bahamas data, and A. Bocconcelli. D.H. and L.T. were funded by the Office of Naval Research (Award No. N00014-14-1-0394). N.A.S. was funded by an EU-Horizon 2020 Marie Slodowska Curie fellowship (project ECOSOUND). DTAG data in the Canary Islands were collected with funds from the U.S. Office of Naval Research and Fundación Biodiversidad (EU project LIFE INDEMARES) with permit from the Canary Islands and Spanish governments.Passive acoustic monitoring has become an increasingly prevalent tool for estimating density of marine mammals, such as beaked whales, which vocalize often but are difficult to survey visually. Counts of acoustic cues (e.g., vocalizations), when corrected for detection probability, can be translated into animal density estimates by applying an individual cue production rate multiplier. It is essential to understand variation in these rates to avoid biased estimates. The most direct way to measure cue production rate is with animal-mounted acoustic recorders. This study utilized data from sound recording tags deployed on Blainville's (Mesoplodon densirostris, 19 deployments) and Cuvier's (Ziphius cavirostris, 16 deployments) beaked whales, in two locations per species, to explore spatial and temporal variation in click production rates. No spatial or temporal variation was detected within the average click production rate of Blainville's beaked whales when calculated over dive cycles (including silent periods between dives); however, spatial variation was detected when averaged only over vocal periods. Cuvier's beaked whales exhibited significant spatial and temporal variation in click production rates within vocal periods and when silent periods were included. This evidence of variation emphasizes the need to utilize appropriate cue production rates when estimating density from passive acoustic data.PostprintPeer reviewe