Underwater Calls Research Articles

First paired observations of sexual behavior and calls in wild leopard seals

Little is known about the reproductive biology of the leopard seal (Hydrurga leptonyx), a Southern Ocean predator. Here we observed sexual behavior in wild leopard seals in Laguna San Rafael, Chile during a 2 h courtship interaction between a female and male. The female was hauled out on ice, mostly lying still (69% of the time) or moving (19%). The male was mostly under water (87%) or at the water’s surface (11%). The female made seven in-air calls (i.e., thump pulse, noseblast, blast, growl). The male produced 65 underwater calls (i.e., low- and high-double trills, unidentified trills). The underwater calls appeared to be directed toward the female. After the primary male vocalized for an hour, one or two unidentified leopard seals briefly swam near the female. After leaving the area, we heard underwater calls for another 8 h. The next day, the primary male was hauled out on ice with a swollen genital opening. The male was bleeding from a laceration caudal to the preputial opening, suggesting the male attempted to mate and that the female, or another seal, was responsible for the injury. Together, we find that leopard seal courtship involves a suite of behavioral and acoustic behaviors by both sexes, both in air and under water. This is the first description of leopard seal sexual behavior in the wild. Our study also provides the first evidence that leopard seals mate in South America.

Male spiny frogs enter the underwater battlefield with loose skin exhibiting enhanced penetration of capillaries into the epidermis

The skin has multiple functions, and capillaries can penetrate the epidermis to shorten the diffusion path while allowing maintenance of overall epidermal thickness for nonrespiratory roles. However, a method for quantifying the capillary penetration extent is lacking. Such a method may facilitate making comparisons and detecting associations, potentially making the extent a useful variable in biological studies. We quantified the extent as the ratio of the average minimum thickness of epidermis overlying each capillary to the average epidermal thickness along a skin section and then explored its performance in the Emei mustache toad, Leptobrachium boringii, a species in which breeding males with loose skin call and fight each other with maxillary spines underwater. The ratio showed informative associations with other variables, such as perfused capillary density. It displayed small intragroup variation and could be more sensitive than other variables in revealing structural differences in the skin. The ratio estimates were lowest and were correlated with epidermal and stratum compactum thicknesses in breeding males, i.e., a covariation but not reinforcement against stabbing, constituting early evidence consistent with the increased extensibility of loose skin conferring a defensive advantage during combat in amphibians. In addition, our results lead to the hypothesis that high hemoglobin density along subepidermal capillaries favors the maintenance of low blood partial oxygen pressure and hence increases cutaneous oxygen uptake. We also provide evidence supporting the new idea that the cooccurrence of loose skin and underwater calling found in some frogs can be explained by the latter benefiting from a large functional respiratory surface area. Awareness of the usefulness of the ratio may promote its application and the quantification of the penetration. Regarding exchange surface design, these findings for L. boringii imply a case in which looseness increases surface area as well as prevents damage.

Waterproof breathable multifunctional flexible sensor for underwater tactile sensing and ammonia gas monitoring

Flexible wearable multifunctional sensors play a vital role in health monitoring, electronic skin, and hazardous gas detection. While combining excellent sensing performance, it is still a challenge to prepare an electronic device with practical properties to increase wearing comfort and adaptability to harsh environments. Herein, we present a multifunctional sensor based on PA6 composite fibers, exhibiting outstanding sensitivity to different external stimuli. For the tactile sensor, we have successfully adjusted the sensitivity and linear range by introducing a spacer layer to improve the linearity by 21.6 times. Benefiting from its intricate and rich fiber structure, the multi-layer fiber-based ammonia sensor has a high sensitivity and a lower detection limit. The multifunctional sensor leverages the dual properties of its outer hydrophobic PA6/PS composite fibers and inner hygroscopic PA6 nanofibers, effectively bolstering its resistance to humidity. Furthermore, the breathability and waterproofness make the sensor promising for rainfall monitoring, underwater pulse/behavior monitoring, etc. Notably, a wireless underwater monitoring system has been designed, confirming the feasibility of underwater calling for help, further demonstrating the potential applicability of our work in the underwater communication.

Diversity of Underwater Vocalizations in Chinese Soft-Shelled Turtle (Pelodiscus sinensis).

Sound communication is important for underwater species. The wild population of the Chinese soft-shelled turtle (Pelodiscus sinensis) is listed as vulnerable. However, its vocalization, which can serve as the basis for ecological and evolutionary research, has not been studied. Here, we performed underwater recordings of 23 Chinese soft-shelled turtles of different ages and sexes and identified 720 underwater calls. The turtle calls were manually divided into 10 call types according to visual and aural inspection properties. The similarity test indicated that the manual division was reliable. We described the acoustic properties of the calls and the statistical analysis showed that the peak frequency of calls was significantly different between adult females and males, and also between subadults and adults. Similar to other aquatic turtles that prefer to live in deep water, Chinese soft-shelled turtles have a high vocal diversity and many harmonic calls, indicating that this highly aquatic species developed a variety of vocalizations to enhance their underwater communication, which helped them adapt to the complex and dim underwater environment. Furthermore, the turtles showed a tendency for vocalization to become more diverse with age.

Evaluation of Pure Titanium Welded Joints Produced by Underwater Friction Stir Welding

Underwater friction stir welding (UWFSW) is an advancement of conventional friction stir welding, which is performed in air. The need for welding underwater calls for more information to be explored in the welding of different materials. The aim of this research is to investigate the UWFSW of 2 mm titanium sheet joints for their tensile and microstructural properties and compare them with the results of friction stir welding (FSW) performed in air. Also, nondestructive tests, such as radiography and dye penetrant tests, were carried out to identify the occurrence of any weld defects. The rotational speed of the FSW tool and its travelling speed were considered process parameters, while other parameters like the tilt angle of the tool, shape of the tool pin, etc. were kept constant. The results show that the welded joints with higher strengths were achieved at a lower travelling speed of 140 mm/min at a rotational speed of 400 and 500 rpm in FSW and UWFSW, respectively. The mechanical properties such as yield strength, tensile strength, and hardness are improved in UWFSW when compared with conventional FSW due to the proper mixing of the metal and effective cooling due to the water environment. In underwater FSW, the improved YS and TS values are observed, which are 95.9% and 75.1% of the base metal values, respectively, when the tool rotational speed is 400 rpm and the travelling speed is 140 mm/min. However, the elongation % is much lower in both FSW and UWFSW when compared with the base metal. These results are supported by microstructure and nondestructive test outcomes.

Quantification of underwater calling and foraging activities in the African clawed frog Xenopus laevis

Abstract Aquatic anuran species are difficult to detect and observe and this is a major limit to the study of their behaviour and ecology. This habit limits the direct monitoring of sexual and foraging activity, and the investigation of how environmental factors influence their expression as well as how individuals allocate time between competing activities. We investigated this issue in Xenopus laevis, a mostly aquatic frog that forages and emits calls underwater. This model species in biology has been extensively studied in the lab but its behaviour in nature remains poorly described. We carried out a study in a pond during the breeding season in the French invasive range. We recorded underwater vocal activity as a proxy for sexual activity using a hydrophone, set food-baited traps to quantify foraging activity, and recorded environmental conditions (moonlight intensity, temperature and rainfall) over two lunar cycles. We found that individuals engage in these two activities during the breeding season. At the peak of the breeding period, vocal activity was expressed during the day. The investment in reproduction (calling activity) may reduce the time allocated to foraging on a circadian scale. The two activities seem to be partitioned depending on moonlight intensity, with a stronger effect on males. Foraging activity decreased and vocal activity increased when moonlight intensity increased. We also observed a negative effect of temperature and a positive effect of rainfall on vocal activity only. Our method is promising to monitor the activity of other aquatic anurans.

Vocal Behavior in Spotted Seals (Phoca largha) and Implications for Passive Acoustic Monitoring

Passive acoustic methods enable remote monitoring of marine species and habitats. These methods can be applied to investigate distribution and abundance of populations, to evaluate behavioral and physiological states of individuals, and to inform management efforts for animals that live in hard-to-reach places. Spotted seals (Phoca largha) inhabit high-latitude, light-limited sub-Arctic and Arctic waters and move seasonally with unstable sea ice. They are high trophic level predators vulnerable to changing conditions associated with environmental warming. At present, an incomplete characterization of the spotted seal vocal repertoire limits our ability to monitor this species acoustically. Captive studies can inform passive acoustic efforts by describing fundamental features of species-typical vocalizations emitted by known individuals. These features include acoustic parameters as well as developmental, seasonal, and sex-specific patterns in vocal behavior. Here, we studied several male spotted seals in captivity from age 6 months through adulthood (10 years). Vocal behavior was scored daily and opportunistically recorded. The production of underwater calls emerged during sexual maturation, at age 4. To evaluate vocal repertoire and fine-scale temporal patterns of sound production in adult seals, an underwater acoustic recorder was continuously deployed with two seals at age 7 years. The spotted seals produced at least eight distinctive underwater call types with dominant energy below 1 kHz. The amplitude of the most common vocalization was ∼140 dB re 1 μPa (sound pressure level at 1 m). There was a marked peak in vocal activity in springtime, prior to onset of the annual molt. This period coincided with increased aggressive behavior, presence of a notable musky odor, and urogenital swelling indicative of heightened reproductive status. These results from developing male spotted seals reared in human care confirm the production of recognizable, stereotypic underwater calls associated with the breeding season. Description of vocal behavior improves knowledge of this species’ biology, and informs the potential use of autonomous acoustic recorders to track the presence and movements of free-ranging spotted seals in remote habitats.

Resonance plays a secondary role in amplifying underwater vocalizations of Weddell seals (Leptonychotes weddellii)

AbstractDuring the breeding season, male Weddell seals (Leptonychotes weddellii) defend underwater territories using high amplitude trill vocalizations (some >190 dB re 1 μPa‐m). The source‐filter theory states that the characteristics of vocalizations are a product of both the sound produced at the source and the effects of soundwave reflection within the vocal tract. This study aimed to determine the relative influence of reflection (resonance). Weddell seal trills (tonal descending frequency sweeps ranging from >20 to <0.1 kHz) offered a unique opportunity to look for resonance in the spectral patterns, appearing as periodic peaks in amplitude over short frequency intervals. Additionally, distributions of frequencies with absolute maximum amplitude (FMA) were tested against random distributions to look for frequencies where FMAs occur more frequently than by chance. All methods exhibited evidence of resonance at 0.45–0.56 and 2.25–2.83 kHz. These frequencies would resonate in closed‐at‐both‐ends tubes with lengths of 32–40 and 6–8 cm, respectively. These lengths approximate the likely sizes of the trachea and larynx or pharynx respectively. The amplitudes of the underwater calls of Weddell seals primarily result from the amplitude generated by the sound source in the larynx with some additional amplitude associated with resonance in the vocal tract.

Underwater calling behavior in two high‐altitude frog species

AbstractUnderwater calls of frogs are poorly documented, probably because they are usually weak and difficult to detect out of water because the impedance contrast at the water–air interface limits sound transmission. The tympanic middle ear and vocal sacs, which may not be essential for underwater acoustic communication, are often reduced in high‐elevation anurans. In addition to the Andean Telmatobius and Sierra Nevada Rana sierrae, many other highland frog species may vocalize underwater rather than be mute as previously thought. We report evidence from the eastern Tibetan Plateau supporting this speculation. In two species of the megophryid genus Scutiger, breeding males emitted trill‐like calls in series under submerged rocks at elevations of approximately 3700 m a.s.l. Because the few high‐elevation anurans known to vocalize underwater are all highly aquatic, this strategy is possibly used because the signal receivers usually remain in water during the breeding season. The finding of underwater calling in Scutiger characterized by reduced middle ears was partly guided by co‐occurrence of loose skin and underwater vocalization in some frog species and constitutes another independent case of such co‐occurrence. We suggest that the presence/absence of loose skin folds should be routinely included in the morphological descriptions of anurans, because an increased surface/volume ratio facilitates effective cutaneous respiration that is required for metabolically costly underwater behaviors which are usually cryptic to human observers.

In-air and underwater sounds of hooded seals during the breeding season in the Gulf of St. Lawrence.

The hooded seal is a migratory species inhabiting the North Atlantic. Passive acoustic monitoring (PAM) conducted over spatial scales consistent with their known and potential habitat could provide insight into seasonal and spatial occurrence patterns of this species. Hooded seal airborne and underwater acoustic signals were recorded during the breeding season on the pack ice in the Gulf of St. Lawrence in March 2018 to better characterize their acoustic repertoire (notably underwater calls). In-air and underwater signals were classified into 12 and 22 types, respectively. Signals produced by males through the inflation and deflation of the proboscis and septum were the predominant sounds heard on the ice surface. Five of the 22 underwater signals were proboscis and septum noises. The remaining underwater signals (17) were categorized as voiced calls and further analyzed using two classification methods. Agreement with the initial subjective classification of voiced calls was high (77% for classification tree analysis and 88% for random forest analysis), showing that 12-13 call types separated well. The hooded seal's underwater acoustic repertoire is larger and more diverse than has been previously described. This study provides important baseline information necessary to monitor hooded seals using PAM.

Underwater hearing and communication in the endangered Hawaiian monk seal Neomonachus schauinslandi

Hawaiian monk seals are among the most endangered marine mammals and the most basal of the phocid seals. The auditory biology of monk seals is compelling from behavioral, evolutionary, and conservation perspectives, but we presently lack substantive bioacoustic information for this species, with no formal descriptions of underwater vocalizations and limited data concerning hearing. These seals have been isolated for more than 10 million yr and have auditory structures differing from those of related species. Additionally, unlike other aquatically mating phocids, monk seals breed asynchronously and are not known to produce social calls in water. To address existing knowledge gaps, we trained a mature male Hawaiian monk seal to perform a psychophysical task while submerged. Detection thresholds were measured for narrowband sounds across the frequency range of hearing. We also conducted a year-round characterization of the seal’s spontaneous underwater vocalizations. This individual demonstrated best hearing between 0.2 and 33 kHz, with a lower high-frequency roll-off than that of related species. Hearing at all frequencies was less sensitive than in other true seals. Despite the absence of conspecifics, the seal regularly produced 6 different underwater calls with energy below 1 kHz. Calling patterns reflected a period of annual reproductive activity lasting about 6 mo, coincident with elevated testosterone levels. This study presents the first examination of underwater vocalizations in Hawaiian monk seals, provides insight into the auditory abilities of this species and the evolution of underwater hearing among phocids, and enables improved assessments of noise effects on these vulnerable seals.

Auditory biology of bearded seals (Erignathus barbatus)

Bearded seals (Erignathus barbatus) have a circumpolar Arctic distribution and are closely associated with unstable pack ice, spending nearly all of their lives in remote habitats. As a result, their biology and behavior remain largely unknown. With respect to sensory biology, bearded seals—like other marine mammals—rely on acoustic cues to support a range of vital behaviors. Acoustic monitoring from moored instrumentation has revealed a rich repertoire of underwater calls associated with the breeding season. However, the ability of bearded seals to perceive sound has never been investigated. In this study, species-typical auditory profiles were obtained from two young male bearded seals trained to cooperate in a go/no-go sound detection paradigm. Hearing thresholds were measured for underwater tonal sounds at frequencies between 0.1 and 61 kHz, in quiet conditions and in the presence of octave-band masking noise. The bearded seals displayed sensitive underwater hearing with peak sensitivity near 50 dB re 1 µPa and a broad frequency range of best hearing extending from approximately 0.3 to 45 kHz. Additionally, the two seals performed particularly well compared to other mammals when detecting target signals embedded within background noise; critical ratios ranged from 12 to 30 dB between 0.1 and 25.6 kHz. These findings improve understanding of the acoustic ecology of bearded seals, inform best management practices related to anthropogenic noise in Arctic habitats, and provide insight into comparative auditory capabilities within the lineage of phocid seals.

Vocal behavior in spotted seals (Phoca largha)

Captive studies can inform passive acoustic monitoring efforts by describing fundamental features of species-typical vocalizations emitted by known individuals. These include acoustic parameters as well as developmental, seasonal, and sex-based patterns in vocal behavior. Here, two male spotted seals were studied in captivity from age 3 months through 8 years. Vocal behavior was scored daily and opportunistically recorded. The production of underwater calls emerged with presumed sexual maturity (age 4). To evaluate vocal repertoire and fine-scale temporal patterns of sound production in adult seals, an underwater acoustic recorder was continuously deployed with these seals at age 7–8 years. The spotted seals produced a variety of underwater calls—including roars, knocks, and moans—with dominant energy below 1 kHz. There was a marked annual peak in vocal activity in spring, prior to the yearly molt. This period coincided with increased aggressive behavior and musky odor indicative of heightened reproductive activity. These results from developing male spotted seals, obtained in the absence of conspecific females, confirm the production of recognizable, stereotypic underwater calls associated with the breeding season. These findings can be used to inform the use of autonomous acoustic recorders to track the presence and movements of free-ranging seals in remote habitats.

The co‐occurrence of loose skin and underwater calling in frogs—further evidence from Amolops ricketti and its implications

AbstractUnderwater vocalizations of frogs are usually inaudible to the human ear and have been poorly documented. Some authors believe that they are more common than currently recognized, yet there have been no new records at the genus level for nearly 30 years. I report on the recordings of underwater calling by the ranid species Amolops ricketti (Boulenger, 1899) from a mountain stream in southern China. Males emitted 2.2–3.5 calls per minute under submerged rocks, which were inaudible to the human ear. Most of the recorded calls lasted 0.73–2.09 s and contained a weak initial note with fewer pulses (1–5) and one to three subsequent notes (3–13 pulses each) repeated at a rate of 0.82–1.99 notes·s−1, with an internote interval lasting 0.36–1.19 s. The dominant frequency of calls ranged from 2.1 to 3.0 kHz, and the notes exhibited increasing intensity and slight upward frequency modulation. Comparisons between individuals of different sexes and breeding stages reveal that the loose skin of the flanks and thighs is a male nuptial trait in A. ricketti. The finding extends the phylogenetic distribution of underwater vocalization to a distinct lineage and constitutes another instance of loose‐skin frogs calling underwater, which can also been identified in Pelobates (Pelobatidae), Leptobrachium (Megophryidae), Telmatobius (Telmatobiidae), Rana italica and Rana sakuraii (Ranidae). These independent cases may allow the proposal of an evolutionary correlation of the two traits in anurans, as a large surface/volume ratio facilitates high levels of cutaneous respiration required for the effective performance of underwater calling. An awareness of this possibility may aid in increasing our understanding of the natural history of anurans.

The underwater vocal complexity of seals (Phocidae) is not related to their phylogeny

Closely related mammalian species often make similar vocalizations, but this is not so with the underwater calls of the true seals. Some seal species have diverse underwater vocal repertoires, whereas others only make pulsed calls. Vocal complexity scores of underwater calls of 13 seal species were compared with their phylogeny and life-history traits. Waveform types, repertoire sizes, repetition and rhythm patterns, and frequency and duration measures (15 attributes, scaled 0 to 1) were summed to give a vocal complexity score. The lowest complexity group use low frequency, burst pulse or irregular waveforms and have small repertoires. The intermediate group have both sinusoidal and noisy waveforms, songs, and a single rhythm pattern in repeated element calls. The most complex group have large repertoires, sinusoidal and noisy waveforms, songs, and two or more rhythm patterns in repeated element calls. There is no evidence of a relationship between phylogeny and vocal complexity. The low vocal complexity species are serially monogamous, do not form breeding groups, breed on beaches or pack ice, and are subject to higher predation risk. Species with higher vocal complexity are promiscuous or polygamous, form breeding groups on pack or landfast ice, and have a lower predation risk.

Clear diel patterns in breeding calls of harbor seals (Phoca vitulina) at Hornby Island, British Columbia, Canada

During the breeding season, male harbor seals (Phoca vitulina Linnaeus, 1758) produce underwater calls for sexual advertisement. The daily and seasonal timing of these calls is influenced by female availability (i.e., tidal haul-out patterns, foraging behavior, and oestrus cycle). Therefore, temporal patterns of male calling can provide clues about patterns of female behavior. We collected underwater recordings during the 2014 breeding season at Hornby Island, British Columbia, Canada, and examined the relationships of light level, progression of breeding season, and tide relative to call presence or absence and calling rate. Calls were 15 times more likely to occur at night than during the day. Nocturnal peaks in calling rate have been observed in other harbor seal populations and have been attributed to tidal haul-out patterns and nocturnal foraging of females. In this study, tide level did not have a significant effect on calling rate, and female foraging behavior was not monitored. One acoustic observation of mammal-eating killer whale (Orcinus orca (Linnaeus, 1758)) calls was followed by 48 h of decreased calling rate. We infer that predation risk influences the temporal pattern of male calling at this location and suggest further study to support this hypothesis.

Airborne and underwater acoustic repertoire of hooded seals (Cystophora cristata): Cornerstone for acoustic monitoring

The hooded seal is a migratory species inhabiting the North Atlantic. They whelp and breed during mid- to late March on pack ice near Jan Mayen Island, in the Davis Strait, off the northeastern Newfoundland coast, and in the Gulf of St. Lawrence. After breeding, hooded seals return to the pack ice off eastern Greenland to moult during June and July, and then they disperse broadly for summer and fall before returning to their respective breeding areas. Passive acoustic monitoring conducted over spatial scales consistent with known and potential habitat of the hooded seal could add insight into seasonal, diel, and spatial occurrence patterns of this species. To better characterize its acoustic repertoire (notably underwater calls), airborne and underwater acoustic signals of hooded seals were recorded during their breeding season on the pack ice in the Gulf of St. Lawrence from 12 to 17 March 2018. Hood and septum noises were the predominant sounds heard from males on the ice surface. Hooded seal underwater acoustic repertoire is larger and more diverse than has been previously described. Using the dataset from an extended acoustic monitoring program along Canada’s East Coast, some clues are provided about the seasonal distribution of hooded seals.

Calling underwater is a costly signal: size-related differences in the call rates of Antarctic leopard seals.

It is proposed that where sexually selected vocal communication is an honest signal, the call production rate is predicted to change throughout the breeding season. Male leopard seals call underwater for many hours each day over their three- to four-month breeding season, and it is hypothesized that a decrease in calling rate would be associated with the declining body condition of smaller males. The calling rates of leopard seals were measured (N = 49 recordings) and compared between seals of different size classes throughout the breeding season. Male leopard seals produce their calls at more stable rates as they become larger. In this study, larger male leopard seals adopted a strategy of consistent underwater calling throughout the breeding season, whereas there was a breakdown in the calling stereotypy of the smaller males at its height. Toward the end of the breeding season, the smaller seals produced fewer calls in shortened calling bouts, and they took more rest periods. Therefore, underwater calling may represent an honest signal in the leopard seal. For marine mammals that call underwater, the production of repetitive sequences advertises the breath-holding ability of the caller to the listeners, and this ability may be related to male stamina and endurance, thus representing an honest signal that could be widespread in other species.

Silent sounds in the Andes: underwater vocalizations of three frog species with reduced tympanic middle ears (Anura: Telmatobiidae:Telmatobius)

Underwater vocalization in anurans is restricted to a few, distantly related species. In some of them, sound is transmitted through tympanic and extra-tympanic pathways. Members of the Andean genus Telmatobius Wiegmann, 1834 lack a tympanic membrane, and earlier reports assumed the absence of vocalizations in the genus. We recorded underwater vocalizations and examined the middle-ear morphology in three species of Telmatobius with different lifestyles: Telmatobius oxycephalus Vellard, 1946 (semiaquatic, riverine); Telmatobius hintoni Parker, 1940 (markedly aquatic, riverine); Telmatobius culeus (Garman 1876) (fully aquatic, lacustrine). Males emit underwater calls, which in the three species are simple and stereotyped; they consist of a repeated train of notes, with a low fundamental frequency (309–941 Hz). In each of the three species, the tympanic membrane is absent and the tympanic cavity is extremely reduced or absent, whereas the opercular system is well developed. Our data, along with prior knowledge in other species of anurans, suggest that the species examined here probably perceived sound through extra-tympanic pathways. Given the limited knowledge about underwater calling in anurans, Telmatobius seems a logical candidate to study the functional and evolutionary bases of underwater hearing and tympanic middle-ear reduction in anurans.

Through-ice communication by Weddell seals (Leptonychotes weddellii) is possible

Based on prior knowledge of the in-air hearing thresholds of seals at the time, Terhune (Polar Biol 27:810–812, 2004) suggested that Weddell seals (Leptonychotes weddellii) likely could not hear underwater calls, while they were on the ice. However, recent data on phocid hearing thresholds in the air reveal that seals have much lower detection thresholds than previously thought. A re-analysis of the situation using the lower hearing threshold data finds that many of the Weddell seal underwater calls, especially those with high-frequency components, will be audible to seals resting on the ice. Territorial males vocally defending territories under the ice during the breeding season may also be communicating with females on the ice directly above them. This communication may facilitate later mating success of those males.