Frants H. Jensen How do social delphinids use sound for mediating group interactions, and how will increasing ocean noise affect these processes? When Jacques Cousteau first coined the sea the “silent world” in his famous 1956 documentary, it was a consequence of taking an air-adapted ear into water, rather than a reflection of the state of the ocean. Sound in fact propagates both 4.5 times faster and with much less attenuation underwater, whereas light attenuates quickly at depth, leading many marine animals to rely extensively on sound. Cetaceans, many of which are often thought of as highly social animals, exploit these favourable conditions to achieve long-range acoustic communication and even to echolocate for food. Yet as global shipping intensifies and humans further develop and exploit coastal and offshore marine areas, we change the acoustic environment, and we are now starting to appreciate how profoundly these changes may affect aquatic life. But while we can model how increasing noise affects signal detection and communication range, we do not yet understand the function of many cetacean communication signals and the functional ranges over which they are needed. In this project, postdoc Frants Jensen investigates how social toothed whales coordinate activities and behaviours and how acoustic information flow helps mediate critical social interactions to better predict effects on cetaceans as underwater noise increases. He does so by working on a small population of long-finned pilot whales in the Strait of Gibraltar, an intense shipping area where well-known groups of pilot whales are found year-round and can be easily reached by boat. A Highly Social, Deep-Diving Delphinid FIGURE 1: Instrumentation of pilot whales using carbon-fiber pole. Photo by F. H. Jensen under NMFS permit number 14241 to P. Tyack. Instrumentation of Pilot Whales Digital acoustic recording tags record sound, movement and depth for up to 24 hours at a time from a single tagged individual. Researchers use light carbon fiber poles to instrument animals with tags that are held on to the animals with four small suction cups. A programmable release and VHF radio beacon facilitates retrieval. Long-finned pilot whales are highly successful marine predators that dive up to one kilometre into the ocean in pursuit of their cephalopod prey. These highly social animals generally live in stable matrilineal groups characterised by a high degree of natal philopatry, meaning that offspring generally stay within the groups that they are born into. Like other social animals, they depend on group members for navigating many ecological challenges: Among other group benefits, pilot whales band together to harass and chase away killer whales as a likely social defence mechanism against predators (De Stephanis), and they rely extensively on alloparental care of young, where other group members care for or even nurse dependent young (Whitehead). They are a highly acoustic species with a rich vocal repertoire of sounds that include echolocation clicks, rapid series of clicks called burst pulses, and a variety of long-range tonal whistles or calls. Long-finned pilot whales are an ideal model organism to understand the role of acoustic signals in mediating behavioural interactions, partly due to their gregarious nature, but also because their relatively curious nature allows for easier instrumentation with state of the art biologging tags that record depth, vocalisations and movement of tagged individuals. Uniquely to these efforts, the team instruments multiple pilot whales within the same group with acoustic tags to analyse and track acoustic interactions and information flow within moving animal social groups. FIGURE 2: A female pilot whale and her juvenile calf instrumented with acoustic and movement recording tags. Photo by F. H. Jensen under NMFS permit number 14241 to P. Tyack. Listening In on an Echolocating Top Predator Toothed Whale Nasal Sound Production Toothed whales have evolved two independent air-driven sound generators, termed phonic lips, in their nasal passages. Pressurising these allow animals to produce echolocation clicks, whistles, and even complex calls with two independent components. The system is self-contained, and air is recycled intermittently, ensuring that toothed whales can keep echolocating throughout dives up to several hours. Toothed whales use echolocation to gather information about their environment and to find and capture prey. During prey capture, all toothed whales speed up their biosonar to gather more rapid feedback on prey location while simultaneously decreasing amplitude and widening the sonar beam to decrease the risk of prey escape responses taking them outside of the highly directional biosonar beam. Acoustic tags are particularly strong methods for studying the ecology of these predators as it allows us to tap directly into the sensory system of the predator itself and detect individual foraging attempts in situ from wild animals. In the Strait of Gibraltar, pilot whales spend periods of time resting or travelling at the surface, interspersed with bouts of concentrated foraging activity. When foraging, animals generally dive to the bottom at 500-1000 m depth, presumably targeting squid and other cephalopods as evidenced from stomach contents of stranded animals. Foraging bouts are concentrated especially during periods of rising tide and therefore higher bottom current. Exploiting these oceanographic changes help increase prey encounter rates and therefore foraging efficiency during deep dives. FIGURE 3: Spectrogram of a long-finned pilot whale echolocation sequence, showing an initial period of low-rate, broadband search clicks and then a transition to rapid clicks (that seemingly merge together in spectrogram) during prey capture attempt. Intense Group Coordination The study has revealed that long-finned pilot whales exhibit a very high degree of coordination in both movement at the surface and foraging at depth within groups. Simultaneously tagged group members often surface together and synchronise shallow foraging dives with one another, and they also embark on deep foraging dives together. This foraging synchrony is much higher for animals that remain tightly associated in small subgroups at the surface, indicating that preferential association in heterogeneous social groups extends into foraging dives. This tight synchrony may at first appear counterintuitive, since group members foraging at the same time would compete for the same prey at depth. However, using the echolocation clicks of the animals themselves, it is possible to track the distance between multiple simultaneously tagged animals and demonstrate that these carefully timed foraging dives do not reflect cooperative foraging, but rather a type of distributed foraging where animals pay attention to location of conspecifics (likely by eavesdropping on echolocation clicks) and actively seek to avoid overlapping their search trajectories. “These behavioural interaction rules decrease foraging competition and increase the total group foraging performance.” - Frants H. Jensen. FIGURE 4: A foraging dive of a long-finned pilot whale, showing a descent phase, a bottom phase with frequent foraging attempts (yellow circles) and an ascent phase with a few sparse foraging attempts. Acoustic Signals Used for Animal Coordination To achieve this extensive coordination over long time scales and over changing spatial scales that can exceed thousands of meters, long-finned pilot whales employ a variety of dedicated communication signals. During long resting or travelling periods at the surface, they primarily use complex tonal calls with two independent frequency contours similar to the songs of some songbirds. “At present, we are testing how information is encoded in these calls, and what information can be derived from them, for example about identity or social group of the caller, and how they are used to mediate collective decisions within a social group.” - Frants H. Jensen. These are the types of signals most often looked at when evaluating how noise impacts detection range, and they are also often used when animals are separated over long distances. However, during foraging dives, they depend on a suite of other signals that are primarily low-amplitude or directional signals, seemingly to help coordinate foraging dive timing. Since coordinating activities is a common problem for many social animals, these less studied acoustic signals may be more important than recordings with hydrophones near whales have previously suggested, and they reflect how versatile the communication system of toothed whales may be. FIGURE 5: Reconstruction of 3-d trajectories for simultaneously tagged long-finned pilot whale trio, demonstrating distributed foraging at depth (yellow), and reunion calls during ascent (red). What it Means to Receive the Grant from the Carlsberg Foundation “With the grant from the Carlsberg Foundation, I was given the opportunity to learn from the rich academic environment at Princeton University and from three leading research groups on ecology and collective behaviour. This has been crucial not only to forming new collaborations, but also to start off new joint research projects, one of which has already received further support from the Carlsberg Foundation.” - Frants H. Jensen. Relevant References Jensen, F. H., J. Marrero Perez, M. Johnson, N. Aguilar Soto and P. T. Madsen. 2011. Calling under pressure: short-finned pilot whales make social calls during deep foraging dives. Proceedings of the Royal Society B 278:3017-3025. Jensen, F. H., M. Wahlberg, K. Beedholm, M. Johnson, N. A. De Soto and P. T. Madsen. 2015. Single-click beam patterns suggest dynamic changes to the field of view of echolocating Atlantic spotted dolphins (Stenella frontalis) in the wild. The Journal of Experimental Biology 218:1314-1324. Pérez, J. M., F. H. Jensen, L. Rojano-Doñate and N. Aguilar De Soto. 2016. Different modes of acoustic communication in deep-diving short-finned pilot whales (Globicephala macrorhynchus). Marine Mammal Science: DOI: 10.1111/mms.12344. Fact box 1: Instrumentation of Pilot Whales Johnson and Tyack, 2003, Jensen et al. 2011 Fact box 2: Toothed Whale Nasal Sound Production, Madsen, P. T., F. H. Jensen, D. Carder and S. Ridgway. 2012. Dolphin whistles: a functional misnomer revealed by heliox breathing. Biology Letters 8:211-213. Jensen, F. H., J. Marrero Perez, M. Johnson, N. Aguilar Soto and P. T. Madsen. 2011. Calling under pressure: short-finned pilot whales make social calls during deep foraging dives. Proceedings of the Royal Society B 278:3017-3025.