香京julia种子在线播放

North Pacific minke whale (Balaenoptera acutorostrata) boing calls are commonly detected in Hawaiian waters from fall to spring, but the animals that produce them have rarely been sighted and little is known about their behavior in this area. The minke whale boing call was first detailed by Wenz (1964) using recordings from submarines operating off the coast of San Diego, California and in Hawaiian waters and also from two bottom-mounted hydrophones off the coast of Kāneʻohe, Hawaiʻi. Although it was suspected that the boing was produced by a whale species (Thompson and Friedl, 1982), it took about 40 years until the source of the boing was determined to be from a minke whale (Rankin and Barlow, 2005). Minke whales are difficult to detect visually, so passive acoustic monitoring (PAM) is an important methodology for learning about the behavior and life history of this species.

Thompson and Friedl (1982) recorded boing sounds from two bottom-mounted hydrophones off the coast of Oʻahu. They observed two calling states with distinct inter-call intervals (ICIs). They proposed that the whales produced calls with ICIs of approximately 30 s when in acoustic contact with another calling whale, and 6 min when not in acoustic contact with another calling whale, but this study was limited by a low sample size and the inability to localize calls and measure distances between individuals (Thompson and Friedl, 1982). The significance of the boing call is currently unknown. However, since humpback whales (Megaptera novaeangliae) in Hawaiian waters use song for breeding purposes (Tyack, 1981) and have a similar seasonal and spatial overlap with minke whales, past researchers have suggested that the minke whale boing is also a mating call (Oswald et al., 2011; Martin et al., 2015), but this hypothesis is yet to be tested. Learning more about the calling rate of whales in different contexts can help us better understand the function of calls in whale behavior.

The central North Pacific boing call produced by minke whales in Hawaiian waters (as opposed to the eastern North Pacific boing call, which has a slightly different pulse repetition rate and call duration) has an onset transient component followed by a long call (mean duration of 2.6 sec) with both frequency and amplitude modulation (Rankin and Barlow, 2005). The 1,350 to 1,440 Hz band contains the majority of energy from the boing call with 115 Hz pulse repetition rate harmonic bands (Wenz, 1964; Rankin and Barlow, 2005; Martin et al., 2015). The peak frequency in this band has been termed the dominant signal component (DSC) (Martin, 2009), and has been identified as a feature to attribute calls to individual whales in some situations (Martin et al., 2013).

The life history of minke whales that spend time in Hawaiian waters is unknown, but acoustic detections and visual sightings in other areas can give clues about their migratory patterns. In the Chukchi Sea, Delarue et al. (2012) detected a small number of central North Pacific boings in the early fall (n=44), and boings resembling the eastern North Pacific type in the late summer and fall (n=10). In the North Pacific, pulse trains and downsweep calls have been documented in the presence of minke whales during the summer in Cormorant Channel, British Columbia, Canada which is likely a feeding area (Nikolich and Towers, 2020). Minke whales sighted off Vancouver Island and central British Columbia often have scars characteristic of cookiecutter sharks (Isistius brasiliensis) which are only in tropical and subtropical waters (Towers et al., 2013). Based on these observations and acoustic detections, the minke whales detected in Hawaiian waters probably migrate north to arctic or subarctic waters to feed, similar to the migration patterns of other large baleen whales.

In addition to helping us understand whale behavior, calling rate, or cue rate, is a necessary variable for PAM cue-rate-based density estimation (Marques et al., 2009). Visual surveys are currently the primary method to estimate marine mammal abundance, but minke whales are difficult to see due to their small size, minimal surface cues, and tendency to be alone, and so it is very challenging to estimate their abundance precisely (Zerbini et al., 2006). In addition, the visual ship-based surveys for marine mammals in Hawaiian waters are usually conducted during summer and fall, and since minke whales are rarely visually or acoustically detected during this time, no total abundance estimate exists for minke whales in this region (Carretta et al., 2014). Quantifying the minke whale cue rate and the variables that influence it may make it possible to estimate the abundance of minke whales using PAM for applications when tracking individuals is not possible.

In this paper, we investigate the hypothesis proposed by Thompson and Friedl (1982) that minke whales call more rapidly when closer to other calling minke whales. We recorded and localized boing calls off of Kauaʻi, Hawaiʻi between fall and spring for 5 years, and spatio-temporally grouped these localized calls into acoustic tracks. Using these tracks, we quantified individual minke whale ICIs and modeled ICI as a function of distance to the nearest tracked calling conspecific. This paper summarizes the calling behavior of minke whales using 36,033 boing calls from 509 tracks.

Between August 2012 and July 2017, 599 days of data were recorded on each hydrophone. During this time, 2,245 individual minke whale tracks were observed and contained 223,732 calls. Of these tracks, 509 were located within the focal area at least part of the time and so were included as “focal tracks”. The subset of focal tracks contained 36,033 localized calls. Although we recorded throughout the year, minke whale boing vocalizations were only present between October and May ( Figure 3 ). The increase in recording effort from collecting long-term data at the 6 kHz sample rate (initiated in August 2014) is evident from the lower cyan bars in Figure 3 starting in September 2014.

Manual review of 5% of the 509 focal tracks (26 tracks) resulted in a mean missed localization rate of 4.6%. We noted that missed calls were almost always detected on 8 or more hydrophones, but were sometimes discarded by the automated localization process because the least square error value exceeded the user-defined threshold. No false localizations were noted in the manual review process. Relaxing the least square error threshold would result in fewer missed localizations, but would come at the expense of false localizations that can confuse the tracking algorithm. The 4.6% missed localization rate was acceptable and did not affect the outcome of determining the behavioral state, as demonstrated by the stress test dataset (details presented with the modeling results).

Minke whale boing ICIs followed a bimodal distribution (gray bars, Figure 4 ). Two calling states based on ICI were identified by the HMM and their probability density functions followed the observed ICI distribution well (blue and teal curves, Figure 4 ). Whales in State 1 had an mean ICI of approximately 6.85 min and whales in State 2 had an mean ICI of approximately 0.63 min ( Table 1 ).

We compared three different time windows to search for the nearest calling conspecific. The 30 min time window performed the best, followed by 20 min, and 10 min, which all performed better than the null model that tested the hypothesis that minke whale inter-call interval was not a function of distance to the nearest neighbor ( Table 2 ). Because the inter-call interval changed by an order of magnitude between State 1 and State 2, these results were not sensitive to occasional missed localizations along a track. In the stress test dataset, 30% of calls were randomly dropped from a track, but the model ranking and stationary state probability trend remained the same (although the ICIs for the two states increased, as expected since there were fewer calls).

The probability of a minke whale being in State 1 and calling at a nominal rate increased as its distance to the nearest calling conspecific increased and the probability of a minke whale being in State 2 and calling at a rapid rate increased as its distance to the nearest calling conspecific decreased ( Figure 5 ). Since each observation is a localized call, the plotted probabilities are the probability of a call being in a given state and not the length of time that a whale is in a state ( Figure 5 upper). When a whale is calling rapidly, more localizations are available for a given time than when a whale is calling nominally. Of the 36,033 localized calls that were part of focal tracks, 49% were categorized as being in State 1 and 51% were categorized as being in State 2. However, these tracked whales spent a total of 84.7 days calling nominally (State 1) and 8.0 days calling rapidly (State 2), which is equal to 91% of the time in State 1 and 9% of the time in State 2. Therefore, regardless of the distance to the closest calling conspecific, at any given time, minke whales are most likely in State 1 ( Figure 5 lower). Calling rapidly has a higher probability when whales are closer together, but it is never more likely than calling nominally.

We selected two interactions between calling minke whales to illustrate these behaviors with individual whales. The first example occurred on 7 Feb 2017 ( Figure 6 ). The minke whale that generated the primary track was calling entirely in State 1 and changed its heading and speed, and ultimately ceased calling during an encounter with a whale that generated the nearest track and was mainly in State 2. At the start of the primary track it was steadily calling and moving east-southeast, and had a distant nearest neighbor that was outside the search area. The whale that generated the track labeled as the “nearest track” in Figure 6 started calling at 18:31 UTC, almost an hour and 15 min after the start of the primary track. When the nearest track started calling it was 11.8 km away from the primary track and it quickly switched into State 2 and traveled southeast. At about the same time, the primary track turned to a south-southeast heading and increased its median speed before it stopped calling. While both animals were calling, the distance between the primary track and the nearest track varied between 10.8–11.8 km.

The second example of an interaction between two calling minke whales occurred on 8 Nov 2013 ( Figure 7 ). During this encounter, the minke whale that generated the primary track switched to a rapid calling behavioral state when the whale that generated the nearest track and was also calling rapidly headed towards it. At the start of these tracks, the primary track was traveling southwest and the nearest track was traveling northeast and then north, with the distance between the two tracks decreasing. The primary track switched to calling mainly in State 2 at 6:27 UTC (indicated by arrow in Figure 7 ) when the whales were about 6.9 km apart. At the same time, the nearest track’s heading became more northeast, a reciprocal heading of the primary track. Before the tracks intersected, the whales paused calling for 36 min (primary track) and 15 min (nearest track). The nearest track started calling again first and was traveling northwest. When the primary track started calling it was about 2.7 km southwest of the nearest track and milled in that area while still calling in State 2. The nearest track then turned and headed south towards the primary track. The whale generating the primary track ceased calling when the nearest track was 900 m away.

Minke whales were more likely to call at an increased calling rate when in close proximity to another calling minke whale. They increased their calling rate by an order of magnitude between State 1 and State 2. Converting the ICIs reported in the Results section, the mean calling rate for State 1 was 8.7 calls/whale/hour and the mean calling rate for State 2 was 95.2 calls/whale/hour. The overall mean calling rate for minke whales on PMRF was 15.7 calls/whales/hour. Since calling rate is dependent on distance to the nearest neighbor, calling rate would be expected to be higher in areas where minke whale density is higher and lower in areas where minke whale density is lower.

The findings in this paper add complication to PAM cue-rate-based density estimation since calling rate is needed and is dependent on the number of animals in an area. In contrast, using PAM tracks of localized calls for a census-type density estimation (counting the number of tracks) is less complicated than density estimation methods using only calling rate, but is only available in places where the number and spacing of hydrophones allow for tracking (requirements for tracking are discussed in detail in Nosal, 2013; Helble et al., 2015). For researchers that are unable to localize and track calls, this work provides information on minke whale calling dynamics that are important to consider when studying calling behavior and density estimation. Although we present a cue rate for minke whale boing calls in this paper, this rate should be applied with caution to density estimation equations because we also found that calling rate is density dependent. In addition, this calling rate is based only on regularly vocalizing animals and we do not know the proportion of silent minke whales. Due to the complicated use of vocalizations by mysticetes, deploying multiple hydrophones to track animals may allow for more accurate PAM-based density estimation. Then the “cue” would be a track and the “cue rate” would be related to the probability of tracking a whale, which could be estimated with passive acoustic tagging studies. However, these tagging studies might show that the probability of acoustically tracking whales is also density dependent, which was shown with humpback whales migrating off the coast of Australia by Noad et al. (2017). Even so, deploying multiple hydrophones to localize and track whales is likely more stable for density estimation because it is easier to define a study area and tracking is less impacted by changes in calling rate.

Martin et al. (2015) hypothesized that the minke whale boing call is a mating call. Since minke whales increase their calling rate when in close proximity to other calling minke whales, we are hypothesizing that the boing call also communicates territoriality when the calling rate increases. Minke whales might call slowly to advertise their position and keep space between other vocalizing whales. When another whale gets too close, they begin to call rapidly, possibly as a sign of aggression. Territoriality is expressed acoustically in many other animal taxa. For example, territorial male Galápagos sea lions (Zalophus wollebaeki) and greater sac-winged bats (Saccopteryx bilineata) both increased their vocalization rates as the density of conspecifics around them increased (Kunc and Wolf, 2008; Eckenweber and Knörnschild, 2013). Other species including male green frogs (Rana clamitans) and ring-billed gulls (Larus delawarensis) use a specific call type to signal aggression and produced those calls when intruders entered their territory (Wells, 1978; Southern, 1981).

The minke whale boing call might have a dual purpose of being a mating call and a territorial call. Other species also use the same calls for both aggression and mating. Anurans, birds, and even fish species have been observed to produce the same calls while defending their territory from an intruder as they would if they were trying to attract a mate, although their calling rate may help signify the intent in these different scenarios (e.g. Wiewandt, 1969; Wingfield, 1994; Borgia and Coleman, 2000; Vasconcelos et al., 2010; Baker et al., 2012). However, aggression and mating may not be independent events. Species that use vocalizations to simultaneously deter competitors and attract mates include male midwife toads (Alytes obstetricans and Alytes cisternasii), red deer (Cervus elaphus), and fallow bucks (Dama dama) (McComb, 1991; Bosch and Márquez, 1996; McElligott and Hayden, 1999). These previous studies have used the proximity of non-calling conspecifics (specifically female conspecifics) to help determine the significance of calls, but in our study, we only know the positions of vocal whales and do not know how non-vocal whales are behaving and whether they are attracted or repelled from the boing calls.

Even if vocalizations are associated with mating behavior, their purpose may not be to attract mates. Sometimes other humpback whale males have approached singers, but singers have also been observed to sing when alone and when escorting mother-calf pairs (e.g. Darling and Bérubé, 2001; Smith et al., 2008). Male-male interactions were not always agonistic and Darling and Bérubé (2001) suggested that they might help in social ordering. Similar to minke whales, singing humpbacks might also change their singing behavior when in close proximity to another singing male and often stop singing if the approach gets very close, regardless of whether or not the other male is singing (Darling and Bérubé, 2001; Smith et al., 2008; Cholewiak et al., 2018). Our understanding of baleen whale behavior has advanced more slowly than other taxa due to their vast communication space and difficulties with visual observations, but studies like these can help to increase our knowledge of these protected species.

Although the seasonality of the minke whale boing in Hawaiian waters is similar to that of male songs from humpback whales and fin whales (Balaenoptera physalus) (e.g. Guazzo et al., 2020; Helble et al., 2020a), no biopsies have been collected from calling minke whales to provide evidence of their sex (unlike with humpback and fin whales, e.g. Darling and Bérubé, 2001; Croll et al., 2002; Smith et al., 2008). In other taxa, both males and females have been observed producing territorial calls, so our hypothesis that the minke whale call is used to signal aggression does not also imply the sex of the calling animals. For example, both male and female little blue penguins (Eudyptula minor) defended nest sites by vocalizing and/or moving toward intruders and these vocalizations may help them to signal their aggression in the low-visibility nighttime conditions when they are most active (Waas, 1991). Minke whales also live in low-visibility conditions, so vocalizations are more effective than visual signals to communicate a message over long distances. Since territoriality and aggression are associated with mating in many taxa, it is possible that the minke whale boing functions as a mating call when emitted at the lower calling rate and as a territorial or aggressive call at the higher calling rate.

An alternative hypothesis for the minke whale boing call is that this call is a social call not used for mating, and whales are increasing their calling rate to better communicate location and maintain cohesion with another nearby minke whale. The rarity of boing calls reported at higher latitudes during the summer and fall (Delarue et al., 2012) in potential feeding areas suggests that if the boing call is a social call, it seems to be used primarily in tropical waters from fall to spring. More information about the sex of calling minke whales and the reaction of conspecifics to the boing call would help differentiate between hypotheses.

Minke whale vocal activity is likely influenced by other factors not tested in this analysis. If the boing call is part of mating behavior, then calling behavior may be influenced by hormone levels and time of year (proposed for humpback whales by Clark and Clapham, 2004; Vu et al., 2012; Vu et al., 2014). The time of day can also affect whale behavior, including vocalization behavior (observed in gray whales (Eschrichtius robustus) by Guazzo et al., 2017). In addition, background noise level might affect the vocalization rate (Helble et al., 2020b; Guazzo et al., 2020). Minke whales might call more if noise levels are higher due to other calling conspecifics in the area or they might call more out of a defensive posture due to reduced communication space. Conversely, minke whales might call less if the communication space is reduced and they cannot hear nearby conspecifics (various responses to increased noise level are reviewed in Brumm and Zollinger, 2011). These variables should be tested with future research.

Ideally, similar studies should be performed in other locations to assess how minke whales and other species vocalize as a function of density. However, very few hydrophone set-ups currently available would be able to replicate the study described in this paper. PMRF is a unique area in that we were able to guarantee detection and localization of calling minke whales within a large (over 3,100 km²) search area. A large search area is required to be able to test for behavioral responses based on distance to a conspecific when conspecifics are spread out on the order of multiple kilometers.

In conclusion, minke whales producing boing calls in Hawaiian waters are more likely to call at a rapid rate when they are closer to other vocalizing conspecifics. Many questions still remain about the function of these boing calls, but the unique hydrophone array set-up at PMRF combined with the statistical tools applied here allowed for the analysis of more than 500 minke whale tracks containing tens of thousands of calls. Since the calling rate is dependent on the distance to the nearest neighbor, the calling rate would be expected to be higher in areas where the density of minke whales is higher and lower in areas where the density of minke whales is lower, adding complication to density estimation using passive acoustic monitoring. Despite this added difficulty when estimating abundance, these findings provide new information about minke whale calling behavior on what is probably a breeding area.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://seamap.env.duke.edu/dataset/2190.

Ethical review and approval was not required for the animal study because this study was conducted using passive acoustic monitoring of wild animals with underwater microphones (i.e. hydrophones) and has no impact on animals’ lifecycle.

CM and SM formulated the idea for this study and CM performed the initial analysis. CM, SM, BM, and EH collected the data. GA and BM programmed the detection, classification, and localization algorithms. GA managed and post-processed the data. SM developed the initial tracking algorithm and CM, GA, and SM tuned the tracking algorithm for minke whale boings. ID assisted with the HMM statistical analysis. CM, RG, and TH validated and analyzed the data and wrote the draft manuscript. All authors discussed the results and contributed to the final manuscript.

This research was supported by Commander, U.S. Pacific Fleet (Code N465JR, AwardNumber N0007020WR0EP8F) and tool development utilized for this analysis was supported by the U.S. Navy’s Living Marine Resources Program (Award Number N0002520WR0141R).

The authors thank the personnel at PMRF, especially Eliseo Boloson, Mike Dick, Jim Hager, Robin Higuchi, Bryson Kurokawa, Jon Winsley, and Jeffrey Yates, for obtaining recordings of acoustic data, as without the acoustic data this type of analysis would not be possible.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.