Icelandic herring-eating killer whales feed at night
Herring-eating killer whales debilitate herring with underwater tail slaps and likely herd herring into tighter schools using a feeding-specific low-frequency pulsed call (‘herding’ call). Feeding on herring may be dependent upon daylight, as the whales use their white underside to help herd herring; however, feeding at night has not been investigated. The production of feeding-specific sounds provides an opportunity to use passive acoustic monitoring to investigate feeding behaviour at different times of day. We compared the acoustic behaviour of killer whales between day and night, using an autonomous recorder deployed in Iceland during winter. Based upon acoustic detection of underwater tail slaps used to feed upon herring we found that killer whales fed both at night and day: they spent 50% of their time at night and 73% of daytime feeding. Interestingly, there was a significant diel variation in acoustic behaviour. Herding calls were significantly associated with underwater tail slap rate and were recorded significantly more often at night, suggesting that in low-light conditions killer whales rely more on acoustics to herd herring. Communicative sounds were also related to underwater tail slap rate and produced at different rates during day and night. The capability to adapt feeding behaviour to different light conditions may be particularly relevant for predator species occurring in high latitudes during winter, when light availability is limited.
Investigating top predator behaviour is essential for a full understanding of the ecosystem they inhabit and the role that they play in it. Indeed, marine predator’s behaviours are influenced by diverse intrinsic and extrinsic factors. Prey abundance and distribution vary spatially within the water column, i.e. in depth, but also with time, either on short timescales, such as diel migration, or on longer scales, such as seasonal migration. Such diverse use of the water column by prey, both spatially and temporally, should influence the diving and foraging patterns and behaviour of their predators (e.g. Baird et al. 2005; Friedlaender et al. 2009; Arranz et al. 2011; Friedlaender et al. 2013; Samarra and Miller 2015). Day-night differences in light availability may also affect predator–prey interactions. For example, fish catchability may increase in the absence of light, either during night or at depth (Casey and Myers 1998). Thus, light availability could impact the foraging behaviour of marine predators. For example, Miller et al. (2010) revealed day-night differences in the diving behaviour of mammal-eating killer whales that were most likely explained by day–night ecological differences, such as differences in prey detectability due to ambient light or changes in prey behaviour.
Herring (Clupea harengus) is an important prey species for a number of marine predators, and it undertakes both diel and seasonal migrations. Throughout the year herring migrates between overwintering, spawning and feeding grounds (Holst et al. 2004) with concurrent changes in its behaviour, such as school size, preferred depth and density (Nøttestad et al. 2004). In addition, preferred depth also changes throughout the day, with a diel migration from deeper waters during the day to the surface layer during the night (Dommasnes et al. 1994; Huse and Ona 1996). In Iceland and Norway, killer whales (Orcinus orca) feed upon herring using a coordinated strategy to gather the herring and then slapping the prey ball with their tail to debilitate the fish (Similä and Ugarte 1993; Simon et al. 2005, 2007). These underwater tail slaps consist of multiple pulses over a short duration of ~300 ms with source levels of 186 ± 5.4 dB re. 1 μPa at 1 m across a broadband frequency range centred at 46.1 ± 22.3 kHz (Simon et al. 2005).
Killer whale groups produce unique and stable repertoires of stereotyped pulsed calls that differ between groups (Ford 1989, 1991) but are generally not specific to behavioural context (Ford 1989). From well-known populations, such as in the North Pacific, killer whale finer-scale groups have been described as matrilineal units, i.e. matrilines composed of an oldest-surviving female adult with several offspring generations (Bigg et al. 1990; Baird and Whitehead 2000; Ford et al. 2000). Matriline composition and interactions vary according to killer whale ecology. Indeed, optimal foraging group sizes depend on trade-offs between the ability to detect prey and the probability to be detected by potential prey (Baird and Dill 1996). Within a killer whale population, matrilines that associated at least 50% of the time were considered to form a ‘pod’ (Bigg et al. 1990). Matrilines in the same pod share a unique acoustic repertoire (Ford 1989, 1991) and are genetically more closely related than matrilines from different pods (Barrett-Lennard 2000). However, different pods can share a part of their repertoire, in which case they are considered part of the same acoustic ‘clan’ (Ford 1991). Yurk et al. (2002) revealed that two acoustic clans in Alaska are two maternal lineages, strengthening the idea of vertical maternal cultural transmission of vocal repertoires. Unique pulsed calls work as vocal signature, either matriline or pod or clan, and thus contain important information during social activity with other groups (Ford 1989, 1991; Deecke et al. 2000; Miller and Bain 2000), or to maintain cohesion while hunting (Miller 2002; Lammers and Au 2003).
During feeding, herring-eating killer whales increase the rate of production of communication sounds (Van Opzeeland et al. 2005; Samarra and Miller 2015), suggesting that acoustic communication may be used to coordinate whale movements and/or help herd the herring (Similä and Ugarte 1993; Simon et al. 2007; Shapiro 2008). Call production decreases when whales feed non-cooperatively upon herring discarded from fishing boats (Van Opzeeland et al. 2005), supporting the important role of acoustic communication during coordinated feeding. Thus, we might expect that variations in feeding behaviour in different ecological contexts will be reflected in differences in acoustic behaviour, but such variations are still poorly understood.
Herring-eating killer whales off Iceland produce a feeding-specific pulsed call thought to be aimed at prey and function as an acoustic means to herd the herring (‘herding’ call; Simon et al. 2006). Feeding-specific sounds thought to be directed at prey are also produced by bottlenose dolphins when feeding upon salmon (Janik 2000) and humpback whales when bubble-net feeding on herring (Cerchio and Dahlheim 2001). These calls are similar in structure to killer whale herding calls, suggesting convergence in acoustic behaviour that would facilitate the capture of herring (Simon et al. 2006). The production of feeding-specific sounds allows investigation of feeding occurrence, as well as variations with time of day or season, using passive acoustic monitoring (e.g. Schaffeld et al. 2016).
Herding calls of Icelandic killer whales have a high intensity (estimated source levels of 169–192 dB pp re 1 μPa @ 1 m; Simon et al. 2006), a low frequency (between 400 and 1400 Hz; Samarra 2015), a lack of frequency modulation and a long (~3 s) duration (Simon et al. 2006). Similar herding calls were also recorded from herring-eating killer whales in Shetland (Deecke et al. 2011). However, herding calls are not consistently produced in all feeding events (Simon et al. 2006; Samarra 2015), and it is not clear what factors drive its production. Variations in the production of the call and in the characteristics of calls produced may suggest that the herding call is group-specific (Simon et al. 2006; Samarra 2015); however, this has not been demonstrated to date.
In previous boat-based behavioural studies on herring-eating killer whales (e.g. Similä and Ugarte 1993; Simon et al. 2005, 2006, 2007), data collection was only possible during the daytime. When feeding during the day, the whales flash their white bellies to scare the fish, herding the herring school further, and therefore killer whales may depend on daylight to catch herring (Nøttestad et al. 2002). However, given the short length, i.e. between 4 and 6 h or less, of daylight during winter in high latitude areas, such as Iceland, it appears unlikely that feeding is limited to daylight time.
In this study we contrasted the acoustic behaviour of killer whales between day and night, using an autonomous acoustic recorder deployed in an Icelandic fjord during 1 month in winter 2014. Overwintering herring gather in large aggregations in fjords during the winter months (Óskarsson et al. 2009), and killer whales are known to feed on these herring. Using acoustically detectable underwater tail slaps as a proxy of feeding activity (Simon et al. 2005, 2007; Samarra and Miller 2015), we aimed to assess whether killer whales feed at night, and how acoustic behaviour related to feeding might differ between day and night.
Materials and methods
For each file, we summed the total number of sounds of each category. We then estimated the solar angle using time and spatial coordinates, using the function solarpos (package maptools) from the software R (R Development Core Team 2015) in order to define whether each file was recorded during the day, night or civil twilight. Solar angles are estimated from the horizon, so in theory they could vary between −90° and +90°. As we considered the civil twilight, we set this period between −6° and 0°. Thus, day is defined by positive solar angles, i.e. the sun is above the horizon, and night is defined as negative angles below −6°.
In order to ensure the detectability of sounds did not vary between day and night, we compared ambient noise levels on the recorder during daytime and night-time. Additionally, we used a proxy for recording quality comparable between daytime and night-time. Due to their high intensity (source level 169–192 dB pp re 1 μPa @ 1 m), long duration (~3 s) and low frequency (400–1400 Hz, Simon et al. 2006; Samarra 2015), we assumed that herding calls could be detected from a longer distance than sounds of other categories. Thus, we assessed the quality of all herding calls in the recording periods, as a proxy for overall recording quality, by establishing whether each herding call was masked by noise or could be clearly distinguished. For that purpose, we measured the root mean square (RMS) sound pressure level (SPL) values of the recorded waveform over one-third octave bands with a custom-written script in MATLAB (The MathWorks, Natick, MA, USA). An octave band filter has been applied to both the signal-plus-noise and the noise within the extracted marked sound. The process compared the RMS SPL (dB re 1 muPa2) of calls (with overlapping background noise) to the RMS SPL of the ambient noise (without any call) a few seconds before or after each call. Then we calculated the signal-to-noise ratio (SNR) as the difference of both RMS measures (call and noise). We considered calls to be of high quality if they had peak SNR > 10 dB in at least one of the third octave bands. Finally, we compared the proportion of high quality herding calls between day and night to assess whether there were differences in recording quality between day and night. Additionally, we compared the mean RMS SPL of the ambient noise between day and night within a 200 Hz–15 kHz band, by estimating the mean difference of random RMS noise levels between the two periods.
Units of analysis
Killer whale presence in the fjord was assumed if any killer whale sound was marked within each 5-min acoustic file. Files with killer whale sounds appeared to occur in bouts. Absence of sounds could be due to true killer whale absence or because killer whales were present but not vocalising (e.g. travelling, Simon et al. 2007; Samarra and Miller 2015) or remained undetected by the recording equipment. Therefore, we conducted a bout analysis to determine the bout criterion interval (Slater and Lester 1982; Sibly et al. 1990), i.e. we aimed to objectively define a time interval threshold between files with sounds to establish a ‘presence event’. We plotted the log frequency of intervals between files with detected sounds using cftool in MATLAB and fitted the distribution with one- and two-process exponential models (Sibly et al. 1990). We observed that the best curve fit to the distribution of intervals was a two-process exponential model (r2 = 0.95). We then minimised the total time misclassified to specify the threshold (Slater and Lester 1982; Miller et al. 2004) giving us a time interval threshold of 10.8 files, i.e. any two files with killer whale sounds separated by more than 10 files (approximately 110 min) without sounds were considered two different presence events.
Each presence event was then assigned to one of two periods: day or night. All cases where the presence event continued through day into night or vice versa (8 presence events), and included twilight were removed. By removing the twilight we removed the gradient of luminosity between day and night.
Variations in sound production with feeding behaviour and day/night
To test whether sound production was related to underwater tail slaps (as a proxy of feeding activity), and whether there were differences between day and night, we used generalised linear models where the number of sounds of each category was the response variable and both the rate of underwater tail slaps per presence event, and the light period (as a categorical variable: day/night) were explanatory variables. Killer whale group composition during all presence events was unknown, thus we could not control for group identity in our analyses. Presence events were assumed to be statistically independent feeding bouts, either performed by the same or by a different group. As our response variable was a number per presence event, we used a Poisson distribution (with a log link function), and set the duration of each presence event as an offset, thus approximating a production rate (Zuur 2009). We then repeated the same model structure but added an interaction term between the two explanatory variables. We chose the better of the two models (with or without interaction) for each sound category based upon the Aikake Information Criterion (AIC) selection. Two models were considered different if their ΔAIC was higher than 2, in which case the lowest AIC defined the best model. However, if the ΔAIC was lower than 2, we selected the model with the lower degrees of freedom. In addition, we supported the models’ selection by conducting an ANOVA between the two models with and without the interaction term. We used the function anova in R, by setting a χ2 test, which allowed us to test for a significant difference between the two models. To avoid type 1 error inflation with multiple tests in our interpretation of the 6 models (one per sound category, excluding tail slaps) we applied a Bonferroni correction, by dividing the significant p value threshold by 6, so that a factor had a significant effect if its p value was lower than 0.008.
The EAR recorded a total of 5093 files, 47% during day and 46% during night. At the beginning of the recording period (22 February) sunrise occurred around 8:46 GMT (0) and sunset around 18:45 GMT (0), while at the end of the recording period (31 March) sunrise occurred around 6:30 GMT (0) and sunset around 20:22 GMT (0). From these files we extracted 3239 sounds from the first minute of 544 files (S1 Table), representing 11.5% of all recordings. From all the files with recorded sounds during the first minute, 59% were during the day, 34% during the night and 7% during twilight. Excluding recordings during twilight, we obtained 544 files with sounds, i.e. 10.7% of all recordings (63% during the day and 37% during the night).
We obtained similar mean RMS SPL of the ambient noise between day and night, with a mean difference of 1.71 ± 5.2 dB re 1 muPa2 between the two periods. Similarly, we found that 91% of herding calls (linear and nonlinear) recorded during the day and 87% of herding calls recorded during the night were of high quality, i.e. the signal-to-noise ratio in at least one 3rd-octave band was at least 10 dB. These results allowed us to consider that recording quality between day and night periods were similar. Given the high quality rate of recorded calls, we used the entire dataset without removing the lowest quality sounds, assuming that in the rare cases when lower-quality herding calls were detected, other sounds could also be representatively detected.
Diel variation in sound production
Percentages (and number) of presence events with at least one instance of each sound type
Linear herding call
Nonlinear herding call
Day (22) (number of presence events)
Night (24) (number of presence events)
Results of the generalised linear models, explaining the different sound categories in relation to tail slap rate and the light period per event, with or without interaction (Rate of tail slap:Night) and using event duration as an offset
Linear herding calls
Rate tail slap
Nonlinear herding calls
Rate tail slap
Rate tail slap
Interaction (Rate tail slap:Night)
Rate tail slap
Interaction (Rate tail slap:Night)
Rate tail slap
Interaction (Rate tail slap:Night)
Rate tail slap
Interaction (Rate tail slap:Night)
Correlation with feeding behaviour
Based upon AIC criteria and the ANOVA tests, we found that the models without interaction between the rate of underwater tail slaps and the light period better explained the production of herding calls (both linear and nonlinear), whereas for all the other sound categories the models using the interaction term were selected (S2 Table). We observed that the production of linear herding calls was significantly and positively related to the rate of underwater tail slaps, consistent with the hypothesis of the herding role of this call just before slapping the herring schools increasing feeding efficiency. However, for nonlinear herding calls no correlation was found with the rate of underwater tail slap production. As for the light period, we observed that during the night the numbers of herding calls (both linear and nonlinear) were significantly higher than during the day, for a given rate of underwater tail slap (Table 2).
The number of biphonic calls was significantly lower during the night than during the day; however, their production was significantly associated to the rate of underwater tail slap at night but not during the day (Table 2). In contrast, we observed that during the day monophonic calls and whistles were significantly and positively related to the rate of underwater tail slaps, while during the night whistles showed no correlation whereas monophonic calls were still positively related to the rate of underwater tail slap but with a much lower relationship than during the day (Table 2). Finally, high-frequency whistles were produced more often during night and had a significantly negative relationship to the rate of underwater tail slap, which was not observed during the day (Table 2).
Remote acoustic monitoring of killer whale sounds showed for the first time that Icelandic killer whales fed roughly equally both during the day and night, using underwater tail slaps as acoustic markers of feeding activity. Comparisons of sound production during day and night showed significant diel variation in acoustic behaviour, previously undocumented in herring-eating killer whales. Acoustics is the main communication channel in killer whales, so the pronounced diel variation in production of different sound categories suggests underlying changes in behaviour.
Using underwater tail slaps as a direct indicator of feeding, we observed that killer whales foraged during 77% of the day presence events and 50% of the night events. The overall difference of these percentages of feeding events between day and night was not significant (p = 0.06), albeit close to significance at 0.05. This suggests that killer whales foraged at night to a similar extent as during the day; however, we cannot rule out that significant differences could be identified with an increased sample size.
Marine mammals are adapted for low-light conditions (Peichl et al. 2001) and use acoustic senses to their maximum advantage, such as in localising prey (Norris 1968). Night-time foraging is common and often advantageous because many prey species come closer to the surface at night and are less likely to detect predators (Norris et al. 1994; Thomas and Thorne 2001; Plötz et al. 2001; Benoit-Bird and Au 2003).
For instance, several studies using bio-loggers revealed diel foraging variation in southern elephant seals, as they dove at shallower depth during the night than during daylights hours (Hindell et al. 1991; Biuw et al. 2007; Guinet et al. 2014), suggesting a migration of seals’ prey, the myctophids, to a shallower depth. Indeed, light level is most likely to induce the vertical distribution of myctophids, since southern elephant seals avoid layers in the water column where the light intensity is too high during daytime foraging as well (Jaud et al. 2012). Similarly, deploying tags on long finned pilot whales, Baird et al. (2002) revealed diel variation of pilot whales foraging behaviour feeding on squid, but in contrast they observed very shallow dives during the day but deep dives at night. This was presumably because the whales could only hunt at night when squid came closer to the surface and spent daytime hours resting or socialising at the surface. Similar studies have also been conducted among baleen whales. For example, Friedlaender et al. (2009) observed that North West Atlantic humpback whales fed at the surface during the day, whereas at nigh they fed near the bottom, which correlated with the diel migration of their prey, the sand lance.
Predators that target herring in high latitudes during winter, when daylight is very short, such as killer whales, likely face selective pressures to adjust their foraging strategies to successfully capture their prey despite changes in the prey’s behaviour. Variations in herring schooling behaviour depending on light availability (Blaxter and Batty 1987) may lead to changes in their predators’ foraging strategies. We found that killer whales produced sounds from every category during feeding events during both day and night, but that the production of linear herding calls was higher at night and positively associated with the rate of underwater tail slaps. This result is in agreement with previous suggestions of the function of herding calls to herd the herring (Simon et al. 2006). The lack of light at night may make it more difficult to herd herring into schools because killer whales cannot use their white undersides to scare and herd the fish as they do during the day (Similä and Ugarte 1993). Thus, killer whales may significantly increase the production of herding calls at night to deal with the lack of light as tools to assist the herding of herring. However, we also noticed a short period during the night (between midnight and 3 am) that killer whale have produced some linear herding call without any tail slap production. This absence of co-occurrence between both sounds may reveal a feeding failure. During the middle of the night, at the darkest period, herring might be more disperse (Blaxter and Batty 1987), making killer whales’ foraging harder.
Variation in daytime vs night-time acoustic behaviour during feeding can be related not only to the amount of light, but also to differences in herring behaviour. Herring perform diel vertical migrations, rising closer to the surface at night (Dommasnes et al. 1994; Huse and Ona 1996). Our study area was rather shallow (max depth about 40 m), but still the diel variation in the depth distribution of prey may have caused changes in the hunting tactics and therefore acoustic behaviour of killer whales. Variations in herring schooling behaviour depending on light conditions have also been reported: herring was less active and less likely to form schools in darkness (Blaxter and Batty 1987), which may affect killer whale foraging tactics and calling behaviour. If so, the effort to herd herring might increase during night-time with an increase in herding call production in order to stimulate the anti-predatory schooling behaviour of the fish.
In contrast to the typical ‘herding’ calls, nonlinear herding calls were produced without any relation to the underwater tail slap rate, suggesting that they might have a different function. Nonlinear herding calls might be more effective than linear herding calls in herding herring in the absence of light, as they reach a larger range of frequencies that could match herring of diverse body sizes and swim-bladder resonant frequencies. In other species, nonlinear calls are produced predominantly by specific age-classes, such as juveniles, and can be a non-adaptive by-product of the physics of the sound production mechanism (Fitch et al. 2002). Future work will be necessary to investigate if this is the case in killer whales as well.
As killer whales were acoustically active and foraged both at night and during the day, we assessed how each sound category was associated with feeding context and whether it was used similarly during the day and at night. At night biphonic calls were positively related to feeding attempts, while monophonic calls were positively correlated with the rate of underwater tail slaps during the day. These results are in agreement with previous studies, which showed that killer whales have high rates of sound production during feeding (Simon et al. 2007; Samarra and Miller 2015). Day-night variation in correlation with underwater tail slap rate may suggest different functional roles of these sound categories. In the North Pacific fish-eating killer whales, biphonic calls have higher source levels (Miller 2006) and are more directional (Miller 2002) than monophonic calls. Together with their increased usage in the contexts of pod mixing (Filatova et al. 2009, 2013), this suggests that biphonic calls are used to track the position of family members, while monophonic calls are close-range intra-group contact signals (Filatova et al. 2009). Icelandic killer whales produced more biphonic calls during the day than during night, but they were related to the underwater tail slap rates only during the night. This result could reflect the possibility that their directionality allowed the whales to acoustically track the orientations and movements of each other in darkness in the context of a coordinated hunt (Miller 2002; Lammers and Au 2003). Although herring-eating killer whales in Iceland also increase the use of biphonic calls during daytime feeding (Samarra and Miller 2015), their use in other behavioural contexts in our dataset may have explained the lack of a significant relationship with tail slap rate.
Whistles appeared positively correlated with the rate of underwater tail slaps both during the day and night. Whistles are characterised by high frequencies and low sound pressure levels (Miller 2006), and so are considered to be important in close-range communication, such as during social interaction (Riesch et al. 2006, 2008). Simon et al. (2007) also showed increased whistle production during feeding activity for Icelandic killer whales. Therefore, we could assume that whistles may play a role in coordinated foraging.
In Iceland, killer whales are acoustically active while foraging and socialising but not while travelling (Simon et al. 2007; Samarra and Miller 2015). Thus, during “non-feeding” activities (i.e. presence events with calls and/or whistles but no underwater tail slaps) killer whales were most likely to be socialising, but without any acoustic marker we cannot confirm any behaviour. Only high-frequency whistles produced at night appeared to be possibly specific to the “non-feeding” activity. However, this has to be interpreted with caution since it is likely that our sample of high-frequency whistles is not representative of the entire repertoire produced due to sampling frequency constraints.
Acoustic markers of feeding behaviour (such as echolocation or buzz production) allow for the monitoring of diel foraging behaviours. Many studies have revealed increases in foraging activity at night for odontocetes, based upon passive acoustic monitoring (e.g. harbour porpoises: Todd et al. 2009; Yangtze finless porpoises: Wang et al. 2014; beaked whales: McDonald et al. 2009; deep diving odontocetes in Hawaii: Au et al. 2013). Indeed, for species that produce feeding-specific sounds, passive acoustic monitoring can be an extremely useful tool to understand habitat use, diel and seasonal behavioural patterns. Here, we show that acoustic markers of feeding activity produced by herring-eating killer whales can be reliably used for passive acoustic monitoring.
In conclusion, we have revealed that night-time foraging occurs in herring-eating killer whales and likely represents a substantial amount of killer whale food intake during winter in Iceland. This contrasts with reports for other fish-eating killer whales that appear to forage mostly during the day, with reduced activity levels at night (Baird et al. 2005). Our study brings new evidence of the importance of night-time foraging, suggesting that detailed research into this behaviour is essential to fully understand predator–prey relationships, and that passive acoustic monitoring is a powerful tool to more fully assess these interactions. Our results indicate that Icelandic killer whales have adapted their diel feeding activity to optimise their foraging success.
We would like to thank all the people involved in the field work for their help in collecting this data, as well as Gísli Ólafsson from Láki Tours for logistical support. We are also grateful to S. Isojunno, P. Wensveen, M. Neves and J. Vaquié-Garcia for their help in data processing. This study was funded by an Icelandic Research Fund (i. Rannsóknasjóður) START Postdoctoral Fellowship for FIPS, and was supported by a Marie Curie Fellowship for OAF. Field research was carried in compliance with local regulations and under an institutional permit provided by the Ministry of Fisheries of Iceland.
This study was funded by an Icelandic Research Fund (i. Rannsóknasjóður, Grant No. 120248042) and supported by a Marie Curie Fellowship.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain studies with human participants by any of the authors.
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