Decreasing body size is associated with reduced calving probability in critically endangered North Atlantic right whales.

Body size is key to many life-history processes, including reproduction. Across species, climate change and other stressors have caused reductions in the body size to which animals can grow, called asymptotic size, with consequences for demography. A reduction in mean asymptotic length was documented for critically endangered North Atlantic right whales, in parallel with declines in health and vital rates resulting from human activities and environmental changes. Here, we tested whether smaller body size was associated with lower reproductive output, using a state-space model for individual health, survival and reproduction that quantifies the mechanistic links between these processes. Body size (as represented by the cube of length) was strongly associated with a female's calving probability at each reproductive opportunity. This relationship explained 62% of the variation in calving among reproductive females, along with their decreasing health (20%). The effects of decreasing mean body size on reproductive performance are another concerning indication of the worsening prospects for this species and many others affected by environmental change, requiring a focus of conservation and management interventions on improving conditions that affect reproduction as well as reducing mortality.

Bottlenose dolphin mothers modify signature whistles in the presence of their own calves.

Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this "motherese," or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother-offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.

Anthropogenic noise impairs cooperation in bottlenose dolphins.

Understanding the impact of human disturbance on wildlife populations is of societal importance,1 with anthropogenic noise known to impact a range of taxa, including mammals,2 birds,3 fish,4 and invertebrates.5 While animals are known to use acoustic and other behavioral mechanisms to compensate for increasing noise at the individual level, our understanding of how noise impacts social animals working together remains limited. Here, we investigated the effect of noise on coordination between two bottlenose dolphins performing a cooperative task. We previously demonstrated that the dolphin dyad can use whistles to coordinate their behavior, working together with extreme precision.6 By equipping each dolphin with a sound-and-movement recording tag (DTAG-37) and exposing them to increasing levels of anthropogenic noise, we show that both dolphins nearly doubled their whistle durations and increased whistle amplitude in response to increasing noise. While these acoustic compensatory mechanisms are the same as those frequently used by wild cetaceans,8,9,10,11,12,13 they were insufficient to overcome the effect of noise on behavioral coordination. Indeed, cooperative task success decreased in the presence of noise, dropping from 85% during ambient noise control trials to 62.5% during the highest noise exposure. This is the first study to demonstrate in any non-human species that noise impairs communication between conspecifics performing a cooperative task. Cooperation facilitates vital functions across many taxa and our findings highlight the need to account for the impact of disturbance on functionally important group tasks in wild animal populations.

Managing the effects of multiple stressors on wildlife populations in their ecosystems: developing a cumulative risk approach.

Assessing cumulative effects of human activities on ecosystems is required by many jurisdictions, but current science cannot meet regulatory demands. Regulations define them as effect(s) of one human action combined with other actions. Here we argue for an approach that evaluates the cumulative risk of multiple stressors for protected wildlife populations within their ecosystems. Monitoring effects of each stressor is necessary but not sufficient to estimate how multiple stressors interact to affect wildlife populations. Examining the mechanistic pathways, from cellular to ecological, by which stressors affect individuals can help prioritize stressors and interpret how they interact. Our approach uses health indicators to accumulate the effects of stressors on individuals and to estimate changes in vital rates, driving population status. We advocate using methods well-established in human health and integrating them into ecosystem-based management to protect the health of commercially and culturally important wildlife populations and to protect against risk of extinction for threatened species. Our approach will improve abilities to conserve and manage ecosystems but will also demand significant increases in research and monitoring effort. We advocate for increased investment proportional to the economic scale of human activities in the Anthropocene and their pervasive effects on ecology and biodiversity.

Understanding the combined effects of multiple stressors: A new perspective on a longstanding challenge.

Wildlife populations and their habitats are exposed to an expanding diversity and intensity of stressors caused by human activities, within the broader context of natural processes and increasing pressure from climate change. Estimating how these multiple stressors affect individuals, populations, and ecosystems is thus of growing importance. However, their combined effects often cannot be predicted reliably from the individual effects of each stressor, and we lack the mechanistic understanding and analytical tools to predict their joint outcomes. We review the science of multiple stressors and present a conceptual framework that captures and reconciles the variety of existing approaches for assessing combined effects. Specifically, we show that all approaches lie along a spectrum, reflecting increasing assumptions about the mechanisms that regulate the action of single stressors and their combined effects. An emphasis on mechanisms improves analytical precision and predictive power but could introduce bias if the underlying assumptions are incorrect. A purely empirical approach has less risk of bias but requires adequate data on the effects of the full range of anticipated combinations of stressor types and magnitudes. We illustrate how this spectrum can be formalised into specific analytical methods, using an example of North Atlantic right whales feeding on limited prey resources while simultaneously being affected by entanglement in fishing gear. In practice, case-specific management needs and data availability will guide the exploration of the stressor combinations of interest and the selection of a suitable trade-off between precision and bias. We argue that the primary goal for adaptive management should be to identify the most practical and effective ways to remove or reduce specific combinations of stressors, bringing the risk of adverse impacts on populations and ecosystems below acceptable thresholds.

The multi-dimensional nature of vocal learning.

How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav.60, 1-11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci.4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Measuring auditory cortical responses in Tursiops truncatus.

Auditory neuroscience in dolphins has largely focused on auditory brainstem responses; however, such measures reveal little about the cognitive processes dolphins employ during echolocation and acoustic communication. The few previous studies of mid- and long-latency auditory-evoked potentials (AEPs) in dolphins report different latencies, polarities, and magnitudes. These inconsistencies may be due to any number of differences in methodology, but these studies do not make it clear which methodological differences may account for the disparities. The present study evaluates how electrode placement and pre-processing methods affect mid- and long-latency AEPs in (Tursiops truncatus). AEPs were measured when reference electrodes were placed on the skin surface over the forehead, the external auditory meatus, or the dorsal surface anterior to the dorsal fin. Data were pre-processed with or without a digital 50-Hz low-pass filter, and the use of independent component analysis to isolate signal components related to neural processes from other signals. Results suggest that a meatus reference electrode provides the highest quality AEP signals for analyses in sensor space, whereas a dorsal reference yielded nominal improvements in component space. These results provide guidance for measuring cortical AEPs in dolphins, supporting future studies of their cognitive auditory processing.

When the human brain goes diving: using near-infrared spectroscopy to measure cerebral and systemic cardiovascular responses to deep, breath-hold diving in elite freedivers.

Continuous measurements of haemodynamic and oxygenation changes in free living animals remain elusive. However, developments in biomedical technologies may help to fill this knowledge gap. One such technology is continuous-wave near-infrared spectroscopy (CW-NIRS)-a wearable and non-invasive optical technology. Here, we develop a marinized CW-NIRS system and deploy it on elite competition freedivers to test its capacity to function during deep freediving to 107 m depth. We use the oxyhaemoglobin and deoxyhaemoglobin concentration changes measured with CW-NIRS to monitor cerebral haemodynamic changes and oxygenation, arterial saturation and heart rate. Furthermore, using concentration changes in oxyhaemoglobin engendered by cardiac pulsation, we demonstrate the ability to conduct additional feature exploration of cardiac-dependent haemodynamic changes. Freedivers showed cerebral haemodynamic changes characteristic of apnoeic diving, while some divers also showed considerable elevations in venous blood volumes close to the end of diving. Some freedivers also showed pronounced arterial deoxygenation, the most extreme of which resulted in an arterial saturation of 25%. Freedivers also displayed heart rate changes that were comparable to diving mammals both in magnitude and patterns of change. Finally, changes in cardiac waveform associated with heart rates less than 40 bpm were associated with changes indicative of a reduction in vascular compliance. The success here of CW-NIRS to non-invasively measure a suite of physiological phenomenon in a deep-diving mammal highlights its efficacy as a future physiological monitoring tool for human freedivers as well as free living animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

Shining new light on sensory brain activation and physiological measurement in seals using wearable optical technology.

Sensory ecology and physiology of free-ranging animals is challenging to study but underpins our understanding of decision-making in the wild. Existing non-invasive human biomedical technology offers tools that could be harnessed to address these challenges. Functional near-infrared spectroscopy (fNIRS), a wearable, non-invasive biomedical imaging technique measures oxy- and deoxyhaemoglobin concentration changes that can be used to detect localized neural activation in the brain. We tested the efficacy of fNIRS to detect cortical activation in grey seals (Halichoerus grypus) and identify regions of the cortex associated with different senses (vision, hearing and touch). The activation of specific cerebral areas in seals was detected by fNIRS in responses to light (vision), sound (hearing) and whisker stimulation (touch). Physiological parameters, including heart and breathing rate, were also extracted from the fNIRS signal, which allowed neural and physiological responses to be monitored simultaneously. This is, to our knowledge, the first time fNIRS has been used to detect cortical activation in a non-domesticated or laboratory animal. Because fNIRS is non-invasive and wearable, this study demonstrates its potential as a tool to quantitatively investigate sensory perception and brain function while simultaneously recording heart rate, tissue and arterial oxygen saturation of haemoglobin, perfusion changes and breathing rate in free-ranging animals. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Toothed whale auditory brainstem responses measured with a non-invasive, on-animal tag.

Empirical measurements of odontocete hearing are limited to captive individuals, constituting a fraction of species across the suborder. Data from more species could be available if such measurements were collected from unrestrained animals in the wild. This study investigated whether electrophysiological hearing data could be recorded from a trained harbor porpoise (Phocoena phocoena) using a non-invasive, animal-attached tag. The results demonstrate that auditory brainstem responses to external and self-generated stimuli can be measured from a stationary odontocete using an animal-attached recorder. With additional development, tag-based electrophysiological platforms may facilitate the collection of hearing data from freely swimming odontocetes in the wild.

Auditory oddball responses in Tursiops truncatus.

Two previous studies suggest that bottlenose dolphins exhibit an "oddball" auditory evoked potential (AEP) to stimulus trains where one of two stimuli has a low probability of occurrence relative to another. However, they reported oddball AEPs at widely different latency ranges (50 vs 500 ms). The present work revisited this experiment in a single dolphin to report the AEPs in response to two tones each assigned probabilities of 0.2, 0.8, and 1 across sessions. The AEP was further isolated from background EEG using independent component analysis, and showed condition effects in the 40-60 ms latency range.

Effects of 3 Tesla magnetic resonance imaging exposure on the behavior and orientation of homing pigeons Columba livia domestica.

Homing pigeons (Columba livia domestica) were used to test whether clinical magnetic resonance (MR) imaging disrupts orientation of animals that sense the earth's magnetic field. Thirty young pigeons were randomly separated into three groups (n = 10/group). Two groups were anaesthetized and exposed to either a constant (no sequence) or a varying (gradient echo and echo planar sequences) magnetic field within a 3 Tesla MR unit for 15 minutes. The control group was not exposed to the MR field but shared all other aspects of the procedure. One day later, animals were released from a site they had never visited, 15 km from the home loft. Three weeks after the procedure, animals were released from a different unfamiliar site 30 km from the loft. Measured variables included the time to disappear from sight (seconds), vanishing bearing (angle), and the time interval from release to entering the home loft (hours). On first release, the group exposed to varying field gradients during image acquisition using 2 different standard sequences showed more variability in the vanishing bearing compared to the other groups (p = 0.0003 compared to control group), suggesting interference with orientation. Other measures did not show significant differences between groups. On second release, there were no significant differences between groups. Our results on homing pigeons show that regular clinical MR imaging exposure may temporarily affect the orientation of species that have magnetoreception capabilities. If exposure to MR imaging disrupted processes that are not specific to magnetoreception, then it may affect other species and other capabilities as well.

On the use of the Lloyd's Mirror effect to infer the depth of vocalizing fin whales.

The interference between the direct path and the sea surface reflection of a signal as measured by a receiver is called Lloyd's Mirror effect (LME). It results in a frequency-dependent interference pattern that can be observed in a spectrogram. LME depends on the receiver depth, signal source depth, signal frequency, and slant range between source and receiver. Knowing three of these parameters a priori, LME can be used to estimate the third parameter, such as source depth. Here, the work in Pereira et al. (2016) was expanded to estimate the depth of a vocalizing fin whale recorded by an ocean-bottom seismometer (OBS). In Pereira et al. (2016), the depth of a vocalizing fin whale was inferred by manually comparing spectrograms of LME transmission loss models with observed LME. This study developed an automated procedure to perform the same task using the LME interference pattern observed in the spectrograms of the hydrophone and the vertical channel of the OBS. The results show that the joint use of the two channels was the best approach to estimate a source depth using LME. LME provides a non-intrusive approach for estimating the depth at which a fin whale was vocalizing.

Fin whale acoustic presence and song characteristics in seas to the southwest of Portugal.

Fin whales were once abundant in the seas to the southwest of Portugal, but whaling activities decreased their numbers considerably. Acoustic data from ocean bottom seismometers provide an opportunity to detect fin whales from their notes, data that would otherwise be logistically challenging and expensive to obtain. Based on inter-note interval and frequency bandwidth, two acoustic patterns produced by fin whales were detected in the study area: pattern 1, described from fin whales in the Mediterranean Sea, and pattern 2, associated with fin whales from the northeast North Atlantic Ocean (NENA). NENA fin whales travel into the western Mediterranean Sea, but the Mediterranean population has not been documented to travel regularly into the NENA. In this study, 11 months of acoustic data recorded southwest of Portugal in the NENA were used to characterize 20-Hz fin whale notes into these patterns. Pattern 2 was the most common and occurred mostly in November-January. Pattern 1 occurred less frequently and mostly in September-December, February and April, which suggested a limited excursion of whales from the Mediterranean Sea. There were also occasions when the two patterns were recorded simultaneously. Results suggest that fin whales from the NENA and Mediterranean Sea might mix in the area during part of the year.

Flash and grab: deep-diving southern elephant seals trigger anti-predator flashes in bioluminescent prey.

Bioluminescence, which occurs in approximately 80% of the world's mesopelagic fauna, can take the form of a low-intensity continuous glow (e.g. for counter-illumination or signalling) or fast repetitions of brighter anti-predatory flashes. The southern elephant seal (SES) is a major consumer of mesopelagic organisms, in particular the abundant myctophid fish, yet the fine-scale relationship between this predator's foraging behaviour and bioluminescent prey remains poorly understood. We hypothesised that brief, intense light emissions should be closely connected with prey strikes when the seal is targeting bioluminescent prey that reacts by emitting anti-predator flashes. To test this, we developed a biologging device containing a fast-sampling light sensor together with location and movement sensors to measure simultaneously anti-predator bioluminescent emissions and the predator's attack motions with a 20 ms resolution. Tags were deployed on female SES breeding at Kerguelen Islands and Península Valdés, Argentina. In situ light levels in combination with duration of prey capture attempts indicated that seals were targeting a variety of prey types. For some individuals, bioluminescent flashes occurred in a large proportion of prey strikes, with the timing of flashes closely connected with the predator's attack motion, suggestive of anti-predator emissions. Marked differences across individuals and location indicate that SES do exploit bioluminescent organisms but the proportion of these in the diet varies widely with location. The combination of wideband light and acceleration data provides new insight into where and when different prey types are encountered and how effectively they might be captured.

Fear of Killer Whales Drives Extreme Synchrony in Deep Diving Beaked Whales.

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.

Dynamic biosonar adjustment strategies in deep-diving Risso's dolphins driven partly by prey evasion.

Toothed whales have evolved flexible biosonar systems to find, track and capture prey in diverse habitats. Delphinids, phocoenids and iniids adjust inter-click intervals and source levels gradually while approaching prey. In contrast, deep-diving beaked and sperm whales maintain relatively constant inter-click intervals and apparent output levels during the approach followed by a rapid transition into the foraging buzz, presumably to maintain a long-range acoustic scene in a multi-target environment. However, it remains unknown whether this rapid biosonar adjustment strategy is shared by delphinids foraging in deep waters. To test this, we investigated biosonar adjustments of a deep-diving delphinid, the Risso's dolphin (Grampus griseus). We analyzed inter-click interval and apparent output level adjustments recorded from sound recording tags to quantify in situ sensory adjustment during prey capture attempts. Risso's dolphins did not follow typical (20logR) biosonar adjustment patterns seen in shallow-water species, but instead maintained stable repetition rates and output levels up to the foraging buzz. Our results suggest that maintaining a long-range acoustic scene to exploit complex, multi-target prey layers is a common strategy amongst deep-diving toothed whales. Risso's dolphins transitioned rapidly into the foraging buzz just like beaked whales during most foraging attempts, but employed a more gradual biosonar adjustment in a subset (19%) of prey approaches. These were characterized by higher speeds and minimum specific acceleration, indicating higher prey capture efforts associated with evasive prey. Thus, tracking and capturing evasive prey using biosonar may require a more gradual switch between multi-target echolocation and single-target tracking.

A taxonomy for vocal learning.

Humans and songbirds learn to sing or speak by listening to acoustic models, forming auditory templates, and then learning to produce vocalizations that match the templates. These taxa have evolved specialized telencephalic pathways to accomplish this complex form of vocal learning, which has been reported for very few other taxa. By contrast, the acoustic structure of most animal vocalizations is produced by species-specific vocal motor programmes in the brainstem that do not require auditory feedback. However, many mammals and birds can learn to fine-tune the acoustic features of inherited vocal motor patterns based upon listening to conspecifics or noise. These limited forms of vocal learning range from rapid alteration based on real-time auditory feedback to long-term changes of vocal repertoire and they may involve different mechanisms than complex vocal learning. Limited vocal learning can involve the brainstem, mid-brain and/or telencephalic networks. Understanding complex vocal learning, which underpins human speech, requires careful analysis of which species are capable of which forms of vocal learning. Selecting multiple animal models for comparing the neural pathways that generate these different forms of learning will provide a richer view of the evolution of complex vocal learning and the neural mechanisms that make it possible. This article is part of the theme issue 'What can animal communication teach us about human language?'

Signal-specific amplitude adjustment to noise in common bottlenose dolphins (Tursiops truncatus).

Anthropogenic underwater noise has increased over the past century, raising concern about the impact on cetaceans that rely on sound for communication, navigation and locating prey and predators. Many terrestrial animals increase the amplitude of their acoustic signals to partially compensate for the masking effect of noise (the Lombard response), but it has been suggested that cetaceans almost fully compensate with amplitude adjustments for increasing noise levels. Here, we used sound-recording DTAGs on pairs of free-ranging common bottlenose dolphins (Tursiops truncatus) to test (i) whether dolphins increase signal amplitude to compensate for increasing ambient noise and (ii) whether adjustments are identical for different signal types. We present evidence of a Lombard response in the range 0.1-0.3 dB per 1 dB increase in ambient noise, which is similar to that of terrestrial animals, but much lower than the response reported for other cetaceans. We found that signature whistles tended to be louder and with a lower degree of amplitude adjustment to noise compared with non-signature whistles, suggesting that signature whistles may be selected for higher output levels and may have a smaller scope for amplitude adjustment to noise. The consequence of the limited degree of vocal amplitude compensation is a loss of active space during periods of increased noise, with potential consequences for group cohesion, conspecific encounter rates and mate attraction.

Evidence for discrimination between feeding sounds of familiar fish and unfamiliar mammal-eating killer whale ecotypes by long-finned pilot whales.

Killer whales (KW) may be predators or competitors of other cetaceans. Since their foraging behavior and acoustics differ among populations ('ecotypes'), we hypothesized that other cetaceans can eavesdrop on KW sounds and adjust their behavior according to the KW ecotype. We performed playback experiments on long-finned pilot whales (Globicephala melas) in Norway using familiar fish-eating KW sounds (fKW) simulating a sympatric population that might compete for foraging areas, unfamiliar mammal-eating KW sounds (mKW) simulating a potential predator threat, and two control sounds. We assessed behavioral responses using animal-borne multi-sensor tags and surface visual observations. Pilot whales barely changed behavior to a broadband noise (CTRL-), whereas they were attracted and exhibited spyhops to fKW, mKW, and to a repeated-tonal upsweep signal (CTRL+). Whales never stopped nor started feeding in response to fKW, whereas they reduced or stopped foraging to mKW and CTRL+. Moreover, pilot whales joined other subgroups in response to fKW and CTRL+, whereas they tightened individual spacing within group and reduced time at surface in response to mKW. Typical active intimidation behavior displayed to fKW might be an antipredator strategy to a known low-risk ecotype or alternatively a way of securing the habitat exploited by a heterospecific sympatric population. Cessation of feeding and more cohesive approach to mKW playbacks might reflect an antipredator behavior towards an unknown KW ecotype of potentially higher risk. We conclude that pilot whales are able to acoustically discriminate between familiar and unfamiliar KW ecotypes, enabling them to adjust their behavior according to the perceived disturbance type.