Juvenile social play predicts adult reproductive success in male bottlenose dolphins.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.

Acoustic monitoring of artificial reefs reveals Atlantic cod and weakfish spawning and presence of individual bottlenose dolphins.

The artificial reefs in New York's waters provide structure in areas that are typically flat and sandy, creating habitat for a multitude of species as an area to spawn, forage, and reside. Passive acoustic data collected on the Fire Island and Shinnecock artificial reefs between 2018 and 2022 detected spawning-associated calls of weakfish (Cynoscion regalis) and Atlantic cod (Gadus morhua), as well as the presence of individual bottlenose dolphins (Tursiops truncatus) through their signature whistles. Weakfish and Atlantic cod were more vocally active on the Fire Island reef, where Atlantic cod grunts peaked during a new moon phase in December, and weakfish spawning experienced variable peaks between mid-July and mid-August on both reefs. Fifty-seven individual bottlenose dolphins were identified, with whistle repeats ranging from seconds to years apart. Passive acoustic monitoring allows for simultaneous collection of information on multiple species at different trophic levels as well as behavioral information that helps managers understand how these animals utilize these habitats, which can lead to improved conservation measures.

Dolphin social phenotypes vary in response to food availability but not the North Atlantic Oscillation index.

Social behaviours can allow individuals to flexibly respond to environmental change, potentially buffering adverse effects. However, individuals may respond differently to the same environmental stimulus, complicating predictions for population-level response to environmental change. Here, we show that bottlenose dolphins (Tursiops truncatus) alter their social behaviour at yearly and monthly scales in response to a proxy for food availability (salmon abundance) but do not respond to variation in a proxy for climate (the North Atlantic Oscillation index). There was also individual variation in plasticity for gregariousness and connectedness to distant parts of the social network, although these traits showed limited repeatability. By contrast, individuals showed consistent differences in clustering with their immediate social environment at the yearly scale but no individual variation in plasticity for this trait at either timescale. These results indicate that social behaviour in free-ranging cetaceans can be highly resource dependent with individuals increasing their connectedness over short timescales but possibly reducing their wider range of connection at longer timescales. Some social traits showed more individual variation in plasticity or mean behaviour than others, highlighting how predictions for the responses of populations to environmental variation must consider the type of individual variation present in the population.

Cooperation increases bottlenose dolphins' (Tursiops truncatus) social affiliation.

Dolphins live in a fission-fusion society, where strong social bonds and alliances can last for decades. However, the mechanism that allows dolphins to form such strong social bonds is still unclear. Here, we hypothesized the existence of a positive feedback mechanism in which social affiliation promotes dolphins' cooperation, which in turn promotes their social affiliation. To test it, we stimulated the cooperation of the 11 dolphins studied by providing a cooperative enrichment tool based on a rope-pulling task to access a resource. Then we measured the social affiliation [simple ratio index (SRI)] of each possible pair of dolphins and evaluated whether it increased after cooperation. We also evaluated whether, before cooperation, pairs that cooperated had a higher SRI than those that did not cooperate. Our findings showed that the 11 cooperating pairs had significantly stronger social affiliation before cooperation than the 15 non-cooperating pairs. Furthermore, cooperating pairs significantly increased their social affiliation after cooperation, while non-cooperating pairs did not. As a result, our findings provide support to our hypothesis, and suggest that the previous social affiliation between dolphins facilitates cooperation, which in turn promotes their social affiliation.

Dolphins reduce hearing sensitivity in anticipation of repetitive impulsive noise exposures.

The auditory steady-state response (ASSR) was continuously measured in two bottlenose dolphins during impulse noise exposures to determine whether observed head movements coincided with actual changes to auditory system sensitivity. Impulses were generated by a seismic air gun at a fixed inter-pulse interval of 10 s. ASSR amplitudes were extracted from the instantaneous electroencephalogram using coherent averaging within a sliding analysis window. A decline in ASSR amplitude was seen during the time interval between air gun impulses, followed by an elevation in ASSR amplitude immediately after each impulse. Similar patterns were not observed during control trials where air gun impulses were not generated. The results suggest that the dolphins learned the timing of the impulse noise sequences and lowered their hearing sensitivity before each impulse, presumably to lessen the auditory effects of the noise. The specific mechanisms responsible for the observed effects are at present unknown.

Dolphin conditioned hearing attenuation in response to repetitive tones with increasing level.

All species of toothed whales studied to date can learn to reduce their hearing sensitivity when warned of an impending intense sound; however, the specific conditions under which animals will employ this technique are not well understood. The present study was focused on determining whether dolphins would reduce their hearing sensitivity in response to an intense tone presented at a fixed rate but increasing level, without an otherwise explicit warning. Auditory brainstem responses (ABRs) to intermittent, 57-kHz tone bursts were continuously measured in two bottlenose dolphins as they were exposed to a series of 2-s, 40-kHz tones at fixed time intervals of 20, 25, or 29 s and at sound pressure levels (SPLs) increasing from 120 to 160 dB re 1 µPa. Results from one dolphin showed consistent ABR attenuation preceding intense tones when the SPL exceeded ∼140-150 dB re 1 µPa and the tone interval was 20 s. ABR attenuation with 25- or 29-s intense tone intervals was inconsistent. The second dolphin showed similar, but more subtle, effects. The results show dolphins can learn the timing of repetitive noise and may reduce their hearing sensitivity if the SPL is high enough, presumably to "self-mitigate" the noise effects.

Forward masking in a bottlenose dolphin Tursiops truncatus: dependence on azimuthal positions of the masker and test sources.

Forward masking was investigated by the auditory evoked potentials (AEP) method in a bottlenose dolphin Tursiops truncatus using stimulation by two successive acoustic pulses (the masker and test) projected from spatially separated sources. The positions of the two sound sources either coincided with or were symmetrical relative to the head axis at azimuths from 0 to ± 90°. AEPs were recorded either from the vertex or from the lateral head surface next to the auditory meatus. In the last case, the test source was ipsilateral to the recording side, whereas the masker source was either ipsi- or contralateral. For lateral recording, AEP release from masking (recovery) was slower for the ipsi- than for the contralateral masker source position. For vertex recording, AEP recovery was equal both for the coinciding positions of the masker and test sources and for their symmetrical positions relative to the head axis. The data indicate that at higher levels of the auditory system of the dolphin, binaural convergence makes the forward masking nearly equal for ipsi- and contralateral positions of the masker and test.

Dynamic body acceleration as a proxy to predict the cost of locomotion in bottlenose dolphins.

Estimates of the energetic costs of locomotion (COL) at different activity levels are necessary to answer fundamental eco-physiological questions and to understand the impacts of anthropogenic disturbance to marine mammals. We combined estimates of energetic costs derived from breath-by-breath respirometry with measurements of overall dynamic body acceleration (ODBA) from biologging tags to validate ODBA as a proxy for COL in trained common bottlenose dolphins (Tursiops truncatus). We measured resting metabolic rate (RMR); mean individual RMR was 0.71-1.42 times that of a similarly sized terrestrial mammal and agreed with past measurements that used breath-by-breath and flow-through respirometry. We also measured energy expenditure during submerged swim trials, at primarily moderate exercise levels. We subtracted RMR to obtain COL, and normalized COL by body size to incorporate individual swimming efficiencies. We found both mass-specific energy expenditure and mass-specific COL were linearly related with ODBA. Measurements of activity level and cost of transport (the energy required to move a given distance) improve understanding of the COL in marine mammals. The strength of the correlation between ODBA and COL varied among individuals, but the overall relationship can be used at a broad scale to estimate the energetic costs of disturbance and daily locomotion costs to build energy budgets, and investigate the costs of diving in free-ranging animals where bio-logging data are available. We propose that a similar approach could be applied to other cetacean species.

Tag-based estimates of bottlenose dolphin swimming behavior and energetics.

Current estimates of marine mammal hydrodynamic forces tend to be made using camera-based kinematic data for a limited number of fluke strokes during a prescribed swimming task. In contrast, biologging tag data yield kinematic measurements from thousands of strokes, enabling new insights into swimming behavior and mechanics. However, there have been limited tag-based estimates of mechanical work and power. In this work, we investigated bottlenose dolphin (Tursiops truncatus) swimming behavior using tag-measured kinematics and a hydrodynamic model to estimate propulsive power, work and cost of transport. Movement data were collected from six animals during prescribed straight-line swimming trials to investigate swimming mechanics over a range of sustained speeds (1.9-6.1 m s-1). Propulsive power ranged from 66 W to 3.8 kW over 282 total trials. During the lap trials, the dolphins swam at depths that mitigated wave drag, reducing overall drag throughout these mid- to high-speed tasks. Data were also collected from four individuals during undirected daytime (08:30-18:00 h) swimming to examine how self-selected movement strategies are used to modulate energetic efficiency and effort. Overall, self-selected swimming speeds (individual means ranging from 1.0 to 1.96 m s-1) tended to minimize cost of transport, and were on the lower range of animal-preferred speeds reported in literature. The results indicate that these dolphins moderate propulsive effort and efficiency through a combination of speed and depth regulation. This work provides new insights into dolphin swimming behavior in both prescribed tasks and self-selected swimming, and presents a path forward for continuous estimates of mechanical work and power from wild animals.

Understanding across the senses: cross-modal studies of cognition in cetaceans.

Cross-modal approaches to the study of sensory perception, social recognition, cognition, and mental representation have proved fruitful in humans as well as in a variety of other species including toothed whales in revealing equivalencies that suggest that different sensory stimuli associated with objects or individuals may effectively evoke mental representations that are, respectively, object based or individual based. Building on established findings of structural equivalence in the form of spontaneous recognition of complex shapes across the modalities of echolocation and vision and behavior favoring identity echoic-visual cross-modal relationships over associative echoic-visual cross-modal relationships, examinations of transitive inference equivalencies from initially learned associations of visual and acoustic stimuli, and recent work examining spontaneous cross-modal social recognition of individual identity across acoustic and gustatory chemical modalities (i.e., the equivalence relationships among an individual's characteristics), we examine the history, utility and implications for cross-modal research in cetacean cognition. Drawing from research findings on bottlenose dolphins and beluga whales as well as other species we suggest future directions for cetacean cross-modal research to further illuminate understanding how structural and individual sensory equivalencies lead to object-centered and individual-centered mental representations, as well as to explore the potential for practical applications related to cetacean conservation.

Context-dependent and seasonal fluctuation in bottlenose dolphin (Tursiops truncatus) vocalizations.

A fundamental question in animal behaviour is the role of vocal communication in the regulation of social interactions in species that organise themselves into social groups. Context dependence and seasonality in vocalizations are present in the communication of many species, although very little research has addressed this dependence in marine mammals. The study presented here examined variations in the rate at which free-ranging dyads of bottlenose dolphins emit social-signals in an effort to better understand the relationship between vocal communication and social context. The results demonstrate that changes in the social-signal production in bottlenose dolphins are related to the sex of the partner, mating season and social affiliation between the components of the dyad. In a context of foraging behaviour on the same feeding ground, mixed (male-female) dyads were found to emit more pulsed burst sounds during the mating season. Another relevant aspect of the study seems to be the greater production of agonistic social-signals in the dyads formed by individuals with a lower degree of social affiliation. Overall, this study confirms a clear relationship between dyad composition and context-specific social-signals that could reflect the motivational state of individuals linked to seasonal changes in vocal behaviour.

Classification of simulated complex echoes based on highlight time separation in the bottlenose dolphin (Tursiops truncatus).

Previous studies suggested that dolphins perceive echo spectral features on coarse (macrospectrum) and fine (microspectrum) scales. This study was based on a finding that these auditory percepts are, to some degree, dependent on the dolphin's ∼250-µs auditory temporal window (i.e., "critical interval"). Here, two dolphins were trained to respond on passively detecting a simulated "target" echo complex [a pair of echo "highlights" with a characteristic 120-µs inter-highlight interval (IHI)]. This target had unique micro- and macrospectral features and was presented among "distractor" echoes with IHIs from 50 to 500 µs (i.e., microspectra) and various highlight durations (i.e., macrospectra). Following acquisition of this discrimination task, probe echo complexes with the macrospectrum of the target but IHIs matching the distractors were infrequently presented. Both dolphins initially responded more often to probes with IHIs of 80-200 µs. Response strategies diverged with increasing probe presentations; one dolphin responded to a progressively narrower range of probe IHIs while the second increased response rates for probes with IHIs > 250 µs. These results support previous conclusions that perception of macrospectra for complex echoes is nonconstant as the IHI decreases below ∼100 µs, but results approaching and exceeding 250 µs-the temporal window upper boundary-were more ambiguous.

Output compensation of auditory brainstem responses in dolphins and sea lions.

Cochlear dispersion causes increasing delays between neural responses from high-frequency regions in the cochlear base and lower-frequency regions toward the apex. For broadband stimuli, this can lead to neural responses that are out-of-phase, decreasing the amplitude of farfield neural response measurements. In the present study, cochlear traveling-wave speed and effects of dispersion on farfield auditory brainstem responses (ABRs) were investigated by first deriving narrowband ABRs in bottlenose dolphins and California sea lions using the high-pass subtractive masking technique. Derived-band ABRs were then temporally aligned and summed to obtain the "stacked ABR" as a means of compensating for the effects of cochlear dispersion. For derived-band responses between 8 and 32 kHz, cochlear traveling-wave speeds were similar for sea lions and dolphins [∼2-8 octaves (oct)/ms for dolphins; ∼3.5-11 oct/ms for sea lions]; above 32 kHz, traveling-wave speed for dolphins increased up to ∼30 oct/ms. Stacked ABRs were larger than unmasked, broadband ABRs in both species. The amplitude enhancement was smaller in dolphins than in sea lions, and enhancement in both species appears to be less than reported in humans. Results suggest that compensating for cochlear dispersion will provide greater benefit for ABR measurements in species with better low-frequency hearing.

Breeding program in rehabilitated bottlenose dolphins (Tursiops truncatus gephyreus) from the Southwestern Atlantic Ocean.

Tursiops truncatus gephyreus is only found in the inshore waters of the Southwestern Atlantic Ocean. They are organized in small socially, structured groups, which lead to low genetic variability and high anthropogenic threats. Currently, the information about their reproductive biology and management is still insufficient. Thus, this study aims to present novel information recorded for 20 years regarding reproductive parameters in a small population of captive T. t. gephyreus. Three of the animals involved were found stranded in La Plata River estuary and, the other two were born at the oceanarium. Thirteen semen evaluations showed high-quality semen with a low percentage of sperm abnormalities. Twelve pregnancies and parturitions were observed. There was a clear calving seasonality during austral spring and summer. The duration of phase-2 of labor was approximately 80 min, being the caudal presentation the most frequent. The average inter-birth interval (IBI) was about 33 months. This is the first report that closely monitored parturition, IBI, and seminal evaluation in this species. Information gathered during this program will allow the development of adequate conservation plans for free-ranging populations.

Contextual impacts on individual and synchronous breathing rate variations in three captive odontocete groups.

Breathing rates are often collected both in the wild and in captivity to inform on cetaceans' internal state. However, few studies have investigated the effect of various factors on this breathing rate. We investigated the variations of individual and synchronous breathing rates depending on individual features (species, sex, age), displayed behavior, social parameters (social grouping), and environmental parameters (diurnal variation, presence of enrichment, unusual events, and presence of visitors in three groups of captive odontocetes (Yangtze finless porpoises, Neophocaena asiaeorentalis asiaeorientalis, East-Asian finless porpoises, Neophocaena asiaeorentalis sunameri, bottlenose dolphins, Tursiops truncatus). Both individual and synchronous breathing rates were the highest when animals engaged in energetic or social behaviors. Individual breathing rate decreased but synchronous breathing rate increased with the presence of enrichment. Both rates increased during unusual events (e.g., pool cleaning, presence of a diver in the pool, noise, transport) and when public was present for Yangtze finless porpoises. Finally, synchronous breathing rate increased for Yangtze finless porpoises when experiencing social separation. We suggest that individual and synchronous breathing rates are useful parameters to measure, both in wild and captive animals, to obtain information on their arousal/stress state. However, these rates should be interpreted with caution and should be used together with other parameters to allow more accurate inferences.

RESPIRATORY CHANGES IN STRANDED BOTTLENOSE DOLPHINS (TURSIOPS TRUNCATUS).

Lung function (breath duration, respiratory flow [V̇], and tidal volume [VT]), and end-expiratory O2 were measured in 19 adult bottlenose dolphins (Tursiops spp.) while at rest in water or beached for up to 10 min. The results show that inspiratory VT, expiratory VT, or inspiratory V̇ did not differ on land or in water. The average expiratory V̇ for all dolphins on land decreased by 16%, and the expiratory and total breath durations increased by 5% and 4%, respectively, compared with in water. There were temporal changes observed during beaching, where expired and inspired VT and inspired V̇ decreased by 13%, 16%, and 9%, respectively, after 10 min on land. These data suggest that dolphins compensate for the effect of gravity by adjusting respiration to maintain alveolar ventilation and gas exchange, but during extended durations, the increased work of breathing may impede ventilation and gas exchange. Continuous monitoring of lung function and gas exchange may help prevent long-term damage during out-of-water medical procedures, optimize animal transport conditions, and improve survival during stranding events.

Acoustic coordination by allied male dolphins in a cooperative context.

Synchronous displays are hallmarks of many animal societies, ranging from the pulsing flashes of fireflies, to military marching in humans. Such displays are known to facilitate mate attraction or signal relationship quality. Across many taxa, synchronous male displays appear to be driven by competition, while synchronous displays in humans are thought to be unique in that they serve a cooperative function. Indeed, it is well established that human synchrony promotes cooperative endeavours and increases success in joint action tasks. We examine another system in which synchrony is tightly linked to cooperative behaviour. Male bottlenose dolphins form long-lasting, multi-level, cooperative alliances in which they engage in coordinated efforts to coerce single oestrus females. Previous work has revealed the importance of motor synchrony in dolphin alliance behaviour. Here, we demonstrate that allied dolphins also engage in acoustic coordination whereby males will actively match the tempo and, in some cases, synchronize the production of their threat vocalization when coercing females. This finding demonstrates that male dolphins are capable of acoustic coordination in a cooperative context and, moreover, suggests that both motor and acoustic coordination are features of coalitionary behaviour that are not limited to humans.

The rate of cochlear compression in a dolphin: a forward-masking evoked-potential study.

The "active" cochlear mechanism of hearing manifests in the cochlear compression. Investigations of compression in odontocetes help to determine the frequency limit of the active mechanism. The compression may be evaluated by comparison of low- and on-frequency masking. In a bottlenose dolphin, forward masking of auditory evoked potentials to tonal pips was investigated. Measurements were performed for test frequencies of 45 and 90 kHz. The low-frequency maskers were - 0.25 to - 0.75 oct relative the test. Masking efficiency was varied by masker-to-test delay variation from 2 to 20 ms, and masker levels at threshold (MLTs) were evaluated at each of the delays. It was assumed that low-frequency maskers were not subjected or little subjected to compression whereas on-frequency maskers were subjected equally to the test. Therefore, the compression rate was assessed as the slope of low-frequency MLT dependence on on-frequency MLT. For the 90-kHz test, the slopes were 0.63 and 0.18 dB/dB for masker of - 0.25 and - 0.5 oct, respectively. For the 45 kHz test, the slopes were 0.69 and 0.39 dB/dB for maskers of - 0.25 and - 0.5 oct. So, compression did not decay at the upper boundary of the hearing frequency range in the dolphin.

Whistling is metabolically cheap for communicating bottlenose dolphins (Tursiops truncatus).

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 (Tursiops truncatus) 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 O2 consumption rate (V̇O2 ), 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 V̇O2  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 (P>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 startle reflex in echolocating odontocetes: basic physiology and practical implications.

The acoustic startle reflex is an oligo-synaptic reflex arc elicited by rapid-onset sounds. Odontocetes evolved a range of specific auditory adaptations to aquatic hearing and echolocation, e.g. the ability to downregulate their auditory sensitivity when emitting clicks. However, it remains unclear whether these adaptations also led to changes of the startle reflex. We investigated reactions to startling sounds in two bottlenose dolphins (Tursiops truncatus) and one false killer whale (Pseudorca crassidens). Animals were exposed to 50 ms, 1/3 octave band noise pulses of varying levels at frequencies of 1, 10, 25 and 32 kHz while positioned in a hoop station. Startle responses were quantified by measuring rapid muscle contractions using a three-dimensional accelerometer attached to the dolphin. Startle magnitude increased exponentially with increasing received levels. Startle thresholds were frequency dependent and ranged from 131 dB at 32 kHz to 153 dB at 1 kHz (re. 1 µPa). Startle thresholds only exceeded masked auditory AEP thresholds of the animals by 47 dB but were ∼82 dB above published behavioural audiograms for these species. We also tested the effect of stimulus rise time on startle magnitude using a broadband noise pulse. Startle responses decreased with increasing rise times from 2 to 100 ms. Models suggested that rise times of 141-220 ms were necessary to completely mitigate startle responses. Our data showed that the startle reflex is conserved in odontocetes and follows similar principles as in terrestrial mammals. These principles should be considered when assessing and mitigating the effects of anthropogenic noise on marine mammals.