Mobile animal groups provide some of the most compelling examples of self-organization in the natural world. While field observations of songbird flocks wheeling in the sky or anchovy schools fleeing ...from predators have inspired considerable interest in the mechanics of collective motion, the challenge of simultaneously monitoring multiple animals in the field has historically limited our capacity to study collective behaviour of wild animal groups with precision. However, recent technological advancements now present exciting opportunities to overcome many of these limitations. Here we review existing methods used to collect data on the movements and interactions of multiple animals in a natural setting. We then survey emerging technologies that are poised to revolutionize the study of collective animal behaviour by extending the spatial and temporal scales of inquiry, increasing data volume and quality, and expediting the post-processing of raw data.
This article is part of the theme issue ‘Collective movement ecology’.
Cetaceans represent an evolutionary peak in terms of their cognitive capacities, complex communication systems and their structured, multilevel societies. However, the difficulty of observing their ...behaviour underwater means that studying whale and dolphin sociality in the wild poses some significant methodological challenges.
Traditionally, playback experiments have been used to explore aspects of communication and cognition in whales and dolphins, particularly with trained animals under human care. However, while these studies have provided major breakthroughs in our understanding of cetacean social cognition, it is difficult to know whether these findings generalize to wild animals.
In recent years, new state‐of‐the‐art technology (drones and non‐invasive sound and movement tags) have revolutionized the field of marine mammal behaviour, providing unparalleled information on the fine‐scale behaviour of individuals in the wild. Here, we review the state of the field, combining published studies with our own extensive experience, to demonstrate how these new technologies fundamentally change the behavioural metrics that we are able to measure; allowing us to move from categorical observations to quantifying fine‐scale changes in movement, activity and vocal behaviour.
We discuss how conducting playback experiments alongside these new technologies combines rigorous experimental design with strong ecological validity and increased reproducibility and can be adapted for many social species, setting the standard for high‐calibre, field‐based experiments that explore animal social cognition in the wild.
Toothed whales (Cetacea, odontoceti) use biosonar to navigate their environment and to find and catch prey. All studied toothed whale species have evolved highly directional, high-amplitude ...ultrasonic clicks suited for long-range echolocation of prey in open water. Little is known about the biosonar signals of toothed whale species inhabiting freshwater habitats such as endangered river dolphins. To address the evolutionary pressures shaping the echolocation signal parameters of non-marine toothed whales, we investigated the biosonar source parameters of Ganges river dolphins (Platanista gangetica gangetica) and Irrawaddy dolphins (Orcaella brevirostris) within the river systems of the Sundarban mangrove forest. Both Ganges and Irrawaddy dolphins produced echolocation clicks with a high repetition rate and low source level compared to marine species. Irrawaddy dolphins, inhabiting coastal and riverine habitats, produced a mean source level of 195 dB (max 203 dB) re 1 µPapp whereas Ganges river dolphins, living exclusively upriver, produced a mean source level of 184 dB (max 191) re 1 µPapp. These source levels are 1-2 orders of magnitude lower than those of similar sized marine delphinids and may reflect an adaptation to a shallow, acoustically complex freshwater habitat with high reverberation and acoustic clutter. The centroid frequency of Ganges river dolphin clicks are an octave lower than predicted from scaling, but with an estimated beamwidth comparable to that of porpoises. The unique bony maxillary crests found in the Platanista forehead may help achieve a higher directionality than expected using clicks nearly an octave lower than similar sized odontocetes.
Abstract
Large-scale offshore wind farms are a critical component of the worldwide climate strategy. However, their developments have been opposed by the fishing industry because of concerns ...regarding the impacts of pile driving vibrations during constructions on commercially important marine invertebrates, including bivalves. Using field-based daily exposure, we showed that pile driving induced repeated valve closures in different scallop life stages, with particularly stronger effects for juveniles. Scallops showed no acclimatization to repetitive pile driving across and within days, yet quickly returned to their initial behavioral baselines after vibration-cessation. While vibration sensitivity was consistent, daily pile driving did not disrupt scallop circadian rhythm, but suggests serious impacts at night when valve openings are greater. Overall, our results show distance and temporal patterns can support future mitigation strategies but also highlight concerns regarding the larger impact ranges of impending widespread offshore wind farm constructions on scallop populations.
Toothed whales are apex predators varying in size from 40-kg porpoises to 50-ton sperm whales that all forage by emitting high-amplitude ultrasonic clicks and listening for weak returning echoes 1, ...2. The sensory field of view of these echolocating animals depends on the characteristics of the biosonar signals and the morphology of the sound generator, yet it is poorly understood how these biophysical relationships have shaped the evolution of biosonar parameters as toothed whales adapted to different foraging niches. Here we test how biosonar output, frequency, and directivity vary with body size to understand the co-evolution of biosonar signals and sound-generating structures. We show that the radiated power increases twice as steeply with body mass (P ∝ M1.47 ± 0.25) than expected from typical scaling laws of call intensity 3, indicating an evolutionary hyperallometric investment into sound production structures that may be driven by a strong selective pressure for long-range biosonar. We find that biosonar frequency scales inversely with body size (F ∝ M−0.19 ± 0.03), resulting in remarkably stable biosonar beamwidth that is independent of body size. We discuss why the three main hypotheses for inverse frequency scaling in animal communication signals 3–5 do not explain frequency scaling in toothed whale biosonar. We instead propose that a narrow acoustic field of view, analogous to the fovea of many visual predators, is the primary evolutionary driver of biosonar frequency in toothed whales, serving as a spatial filter to reduce clutter levels and facilitate long-range prey detection.
•Toothed whales have evolved four different biosonar signals for echolocating prey•Larger whales echolocate with higher output levels and at lower click rates•Inverse frequency scaling leads to a highly narrow field of view across species
Jensen et al. analyze scaling of echolocation parameters in toothed whales. They show that large species use lower frequency and higher source levels for longer prey detection range. In contrast, species have converged on remarkably similar beamwidth, suggesting that a narrow field of view drives inverse frequency scaling in cetacean biosonar.
Toothed whales depend on sound for communication and foraging, making them potentially vulnerable to acoustic masking from increasing anthropogenic noise. Masking effects may be ameliorated by higher ...amplitudes or rates of calling, but such acoustic compensation mechanisms may incur energetic costs if sound production is expensive. The costs of whistling in bottlenose dolphins (
) have been reported to be much higher (20% of resting metabolic rate, RMR) than theoretical predictions (0.5-1% of RMR). Here, we address this dichotomy by measuring the change in the resting O
consumption rate (
), a proxy for RMR, in three post-absorptive bottlenose dolphins during whistling and silent trials, concurrent with simultaneous measurement of acoustic output using a calibrated hydrophone array. The experimental protocol consisted of a 2-min baseline period to establish RMR, followed by a 2-min voluntary resting surface apnea, with or without whistling as cued by the trainers, and then a 5-min resting period to measure recovery costs. Daily fluctuations in
were accounted for by subtracting the baseline RMR from the recovery costs to estimate the cost of apnea with and without whistles relative to RMR. Analysis of 52 sessions containing 1162 whistles showed that whistling did not increase metabolic cost (
>0.1, +4.2±6.9%) as compared with control trials (-0.5±5.9%; means±s.e.m.). Thus, we reject the hypothesis that whistling is costly for bottlenose dolphins, and conclude that vocal adjustments such as the Lombard response to noise do not represent large direct energetic costs for communicating toothed whales.
The costs of predation may exert significant pressure on the mode of communication used by an animal, and many species balance the benefits of communication (e.g. mate attraction) against the ...potential risk of predation. Four groups of toothed whales have independently evolved narrowband high-frequency (NBHF) echolocation signals. These signals help NBHF species avoid predation through acoustic crypsis by echolocating and communicating at frequencies inaudible to predators such as mammal-eating killer whales. Heaviside's dolphins (Cephalorhynchus heavisidii) are thought to exclusively produce NBHF echolocation clicks with a centroid frequency around 125 kHz and little to no energy below 100 kHz. To test this, we recorded wild Heaviside's dolphins in a sheltered bay in Namibia. We demonstrate that Heaviside's dolphins produce a second type of click with lower frequency and broader bandwidth in a frequency range that is audible to killer whales. These clicks are used in burst-pulses and occasional click series but not foraging buzzes. We evaluate three different hypotheses and conclude that the most likely benefit of these clicks is to decrease transmission directivity and increase conspecific communication range. The expected increase in active space depends on background noise but ranges from 2.5 (Wenz Sea State 6) to 5 times (Wenz Sea State 1) the active space of NBHF signals. This dual click strategy therefore allows these social dolphins to maintain acoustic crypsis during navigation and foraging, and to selectively relax their crypsis to facilitate communication with conspecifics.
Investigations of collective movement and animal communication have often followed distinct, though complementary, trajectories. Both subfields are deeply concerned with how information flows between ...individuals and shapes subsequent behaviour. Collective movement has largely focused on the dynamics of passive, cue‐mediated group coordination, while animal communication has primarily examined the content and function of active dyadic signal exchanges in sender–receiver frameworks. However, in many social groups, network‐wide signalling and collective movement decisions are tightly linked.
Here we discuss opportunities afforded by using multi‐sensor tracking tags to simultaneously monitor the fine‐scale movements and vocalisations of entire social groups. We highlight how such data can elucidate the role of vocal signals in individual and collective movement while illuminating the structures of entire vocal‐interaction sequences at previously unexamined timescales and across entire communication networks.
We identify practical and analytical challenges associated with these new tools and datasets, and present avenues for addressing them. We specifically address issues associated with the deployment and synchronisation of multiple tags, the processing and interpretation of resulting multidimensional datasets, and the benefits of combining tag‐based data collection with experimental approaches.
Finally, we argue that a comparative approach employing consistent methodologies across a range of environments, populations and systems is needed to shed light on the evolutionary ecology of communication and collective behaviour.
Studying sound production at different developmental stages can provide insight into the processes involved in vocal ontogeny. Humpback whales (Megaptera novaeangliae) are a known vocal learning ...species, but their vocal development is poorly understood. While studies of humpback whale calves in the early stages of their lives on the breeding grounds and migration routes exist, little is known about the behavior of these immature, dependent animals by the time they reach the feeding grounds. In this study, we used data from groups of North Atlantic humpback whales in the Gulf of Maine in which all members were simultaneously carrying acoustic recording tags attached with suction cups. This allowed for assignment of likely caller identity using the relative received levels of calls across tags. We analyzed data from 3 calves and 13 adults. There were high levels of call rate variation among these individuals and the results represent preliminary descriptions of calf behavior. Our analysis suggests that, in contrast to the breeding grounds or on migration, calves are no longer acoustically cryptic by the time they reach their feeding ground. Calves and adults both produce calls in bouts, but there may be some differences in bout parameters like inter-call intervals and bout durations. Calves were able to produce most of the adult vocal repertoire but used different call types in different proportions. Finally, we found evidence of immature call types in calves, akin to protosyllables used in babbling in other mammals, including humans. Overall, the sound production of humpback whale calves on the feeding grounds appears to be already similar to that of adults, but with differences in line with ontogenetic changes observed in other vocal learning species.
Odontocetes produce a range of different echolocation clicks but four groups in different families have converged on producing the same stereotyped narrow band high frequency (NBHF) click. In ...microchiropteran bats, sympatric species have evolved the use of different acoustic niches and subtly different echolocation signals to avoid competition among species. In this study, we examined whether similar adaptations are at play among sympatric porpoise species that use NBHF echolocation clicks. We used a six-element hydrophone array to record harbour and Dall's porpoises in British Columbia (BC), Canada, and harbour porpoises in Denmark. The click source properties of all porpoise groups were remarkably similar and had an average directivity index of 25 dB. Yet there was a small, but consistent and significant 4 kHz difference in centroid frequency between sympatric Dall's (137±3 kHz) and Canadian harbour porpoises (141±2 kHz). Danish harbour porpoise clicks (136±3 kHz) were more similar to Dall's porpoise than to their conspecifics in Canada. We suggest that the spectral differences in echolocation clicks between the sympatric porpoises are consistent with evolution of a prezygotic isolating barrier (i.e., character displacement) to avoid hybridization of sympatric species. In practical terms, these spectral differences have immediate application to passive acoustic monitoring.
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