Opportunistic acoustic recordings of (potential) orangeback flying squid Sthenoteuthis pteropus in the Central Eastern Atlantic

Journal of Marine Systems 179 (2018) 31–37

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Journal of Marine Systems journal homepage: www.elsevier.com/locate/jmarsys

Opportunistic acoustic recordings of (potential) orangeback flying squid Sthenoteuthis pteropus in the Central Eastern Atlantic

T

Marian Peñaa,*, Roger Villanuevab, Alejandro Escánezc, Alejandro Arizac a b c

Instituto Español de Oceanografía, Centre oceanogràfic de Balears, Moll de Ponent s/n, Palma, Spain Institut de Ciències del Mar (CSIC), Barcelona, Spain Instituto de Oceanografía y Cambio Global, Las Palmas de Gran Canaria, Spain

A R T I C L E I N F O

A B S T R A C T

Keywords: Sthenoteuthis pteropus Behaviour Migration Mesopelagic fish Acoustics

Squids are fast swimmers that are difficult to catch by nets and to record with echosounders in the open ocean. A rare detection of orangeback flying squid Sthenoteuthis pteropus in the Central Eastern Atlantic Ocean off the coast of Senegal was accomplished during the MAFIA oceanographic survey carried out between Brazil and the Canary Islands in April 2015. Although net sampling did not yield any subadult or adult individuals, dozens were visually detected from the vessel jumping out of the water at night and displaying their characteristic dorsal photophore patch. A few squids were caught with fishing lines and identified at the species level. The acoustic echograms revealed distinctive previously unobserved acoustic echotraces that seemed to be caused by those squids, which were the only new species detected at that station (over a bottom depth ranging from 4010 to 5215 m, between 10° 45′ N 22° 41′ W and 10° 53′ N 22° 40′ W). The acoustic response and swimming behaviour shown by those echotraces reinforced this hypothesis. The (potentially) squid recordings dove rapidly (0.19 m/s to 0.48 m/s) from around 10 m below the mesopelagic fish layer, which had migrated to the subsurface at night (35 m depth), to depths of 70–95 m, and swam upward, apparently attacking fish from below. The morning squid migration to deeper waters (250–300 m) was also recorded acoustically. Downward movements of squid swimming at speeds of 0.22 m/s were calculated from the echogram, while the mesopelagic migrating fish swam at 0.27 m/s reaching 250 m depth. Sv120 − Sv38 averaged 2.7 ± 3.2 dB for the squid echotraces while the mesopelagic layer showed values of −8.8 ± 0.9 dB. These ranges agreed with values in the literature and from theoretical models. This study provides more insight into the migrating behaviour of oceanic squids, a species group that is poorly represented in the acoustic literature due to challenges in studying them.

1. Introduction

enclosed bays (Benoit-Bird and Gilly, 2012; Benoit-Bird et al., 2008; Jefferts et al., 1987; Vaughan and Recksiek, 1979). In addition, several studies have been carried out in the Pacific Ocean to estimate their scattering properties (Chen et al., 2013; Jefferts et al., 1987; Jones et al., 2009; Kang et al., 2005; Lee, 2013; Lee et al., 2012; Zhang et al., 2015). The orangeback flying squid Sthenoteuthis pteropus (Fig. 1) is an opportunistic short-lived carnivore, among the fastest growing squids (Merten et al., 2016) that inhabits the Central Eastern Atlantic Ocean between 42°N ° N and 36°S ° S and surface water temperatures ranging from 16 to 32°C ° C, usually above 20 to 22°C ° C (Jereb and Roper, 2010). In the current study, we present an analysis of opportunistic field data of a rare and difficult-to-observe event. Visual detections of flying squids coincided with new acoustic echotraces detected on echograms carried out during a survey crossing the Central Eastern Atlantic. Several indications suggested that squids were producing those acoustic

Oceanic squids have wide geographical ranges, from polar regions to the tropics (Jereb and Roper, 2010; Arkhipkin et al., 2015). Squids are ecologically important as major predators, but are also vital as the prey of valuable commercial fish species and many endangered marine animals like whales, seals, and sharks (Boyle and Rodhouse, 2005). They serve as an important trophic link between small mesopelagic organisms and top vertebrate predators (Gilly et al., 2006; Coll et al., 2013) Despite their importance in marine food webs, there is a lack of knowledge regarding their behaviour and daily rhythms (Watanabe et al., 2006). Squids are difficult to catch with nets (Clarke, 2006), which may be related to the considerable differences between the composition of trawl catches and what is found in the stomach contents of predators (Hoving et al., 2014). They are rarely detected acoustically, except for large individuals or aggregations in shallow waters or

*

Correspondence author. E-mail address: [email protected] (M. Peña).

https://doi.org/10.1016/j.jmarsys.2017.11.003 Received 8 August 2017; Received in revised form 8 November 2017; Accepted 11 November 2017 Available online 21 November 2017 0924-7963/ © 2017 Elsevier B.V. All rights reserved.

Latitude (º)

30 20 10 0 −10 −20

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−40

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3

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7

8

−30

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Africa

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Temperature, C

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Longitude (º) Fig. 2. Track with stations (white dots) followed during the MAFIA survey. Colour indicates sea surface temperature. Sthenoteuthis pteropus was recorded at station 8. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Mesopelagic fishes showed a similar migration pattern and layer properties with greater response at 38 kHz throughout the survey and, after visual inspection of the echogram, an initial discriminating mask based on volume backscattering strength (Sv, dBre re m −1) differences, was applied to separate fish from the previously unobserved echotraces. Other relevant scatterers such as krill were scarce at station 8 and are not considered. This first selection retained significant white noise (random variation) in both echograms, due to acoustic data stochasticity. A Gaussian filter (5 rows by 5 columns and 0.01 standard deviation) was then applied to remove variance, and a 3 by 3 median filter was used to remove outliers. In this way, acoustic samples belonging to the mesopelagic fish layer and the potential squid echotraces were better defined, reducing the Sv variance. We compared the resulting Sv120 − Sv38 differences to different squid species published in the literature, and with theoretical data from Myctophidae fishes following the model in Peña et al. (2014). Squid schools were extracted using the SHAPES algorithm (Coetzee, 2000) with 10 and 5 m minimum length and height respectively, and a -60 −60 dB threshold. The school parameters (height, depth, time, length, thickness, area and mean Sv) were corrected when required for beam geometry (which due to the detection angle affects several school parameters) (Diner, 2001). We also calculated the school tilt angle as the angle deviation from horizontal, to infer behaviour. The swimming vertical speed of squid and mesopelagic fish aggregations/layers were calculated from the echogram analysing analyzing the distance of descend/ascend over time. Speeds were only calculated at the two first echotraces as the last three were less-well defined less well-defined. Squid school speed was calculated from the first school at 150 m depth to the deepest one at 300 m depth. Data was processed in Echoview (Echoview, 2016) and MATLAB (MATLAB, 2017).

Fig. 1. Female Sthenoteuthis pteropus of 25 cm mantle length.

echotraces. This work tests this hypothesis based on acoustic properties and swimming behaviour. To our knowledge, this is the first recording of acoustic data showing the natural behaviour of flying squid aggregations in the open ocean. 2. Material and methods Acoustic data were recorded in April 2015 during the “Migrants and Active Flux In the Atlantic Ocean” (MAFIA) survey from the Brazilian coast to the Canary Islands on board the RV Hesperides, along the track shown in Fig. 2, alternating 24-hour 24-h navigation with 24-h stations. Mesopelagic fishes were caught by means a midwater trawl, the “Mesopelagos” net, with a mean mouth opening of 5 ×7 5 × 7 m and a total length of 58 m (more information in Olivar et al., 2017). Fishing lines were deployed at night from the vessel deck. Two CTD casts (night: 0-3000 0–3000 m and day: 0-200 0–200 m) were performed at each station using a Seabird 911Plus conductivity-temperature-depth instrument with a Seabird-43 Dissolved Oxygen Sensor and a Seapoint Chlorophyll Fluorometer Sensor. Vessel speed during stations was ∼2 knots. Surface temperature data were also downloaded from the NOAA website1. Data shown in this work were recorded at station 8 from 04:00 h to 08:00 h GMT on the 19th of April 2015 (Fig. 2), over a bottom depth ranging from 4010 to 5215 m, between 10° ° 45’ ′ N 22° ° 41’ ′ W and 10° ° 53’ ′ N 22° ° 40’ ′ W. The station took place during a new moon, and sunrise/sunset was at 6:54/19:24 h (GMT and local time). The EK60 scientific echosounder (Kongsberg Simrad AS, Kongsberg, Norway) controlled the two frequency transducers with a 2 ms pulse duration at 38 kHz (ES38-B) and 1 ms at 120 kHz (ES120-7C), both with a 7° ° beamwidth, transmitting with a 2000 and 500 W power respectively every ∼3 s. The 38 kHz pulse duration was higher in order to increment the depth with high signal-to-noise ratio. Data for the 38 kHz echograms were resampled to match the 120 kHz ping geometry. The higher signal-to noise ratio in the 38 kHz data due to higher pulse length is compensated by a reduced variance with increased sample size. This is a common procedure in fisheries acoustics (BenoitBird, 2009). Echograms were denoised using the method in Peña (2016). The standard sphere calibration procedure was performed at the end of the survey (Demer et al., 2015) with a 38.1-mm-diameter tungsten-carbide sphere positioned under the hull. Calibration parameters were added to the data upon post-processing. Temperature and salinity values were updated at each station on the echosounder settings in order to account for changes in sound speed and absorption coefficients. 1

3. Results Hundreds of individual orangeback squid were observed at station 8 from the vessel deck at night, jumping and flying above the water’s surface, and four individuals of 24, 25, 26 and 30 cm mantle length (ML) were caught with fishing lines and identified at the species level. The station at which squids were detected showed a clear oceanographic front, with surface temperatures descending from 26° C ° C at station 7 to 22° C ° C at station 9 (Fig. 2), and a maximum surface salinity (38.8 psu), 3.1 and 2.9 psu higher than the previous and following stations respectively. Squid echotraces were recorded from 04:00 h to 08:00 h GMT on the 19th of April 2015, with sea surface temperatures close to 24° C ° C and salinities between 35.7 and 35.8 psu. The cleaned echograms at 38 and 120 kHz in Fig. 3 show the previously unobserved echotraces associated with the squid. The mesopelagic fish occupied the layer closest to the subsurface (∼35 m depth) at night before migrating to deeper waters at around 7 h. Around 10 m underneath the fish layer, the

http://www.ncdc.noaa.gov/sst/griddata.php

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Fig. 3. Echograms at 38 and 120 kHz recorded at station 8 from 04:00 h to 08:00 h GMT on the 19th of April 2015, after denoising with the algorithm outlined in Peña (2016). The usual mesopelagic fish subsurface layer at night is visible at 35 m depth and the (potential) squid echotraces just below. Squids migrate downward to depths of 350–400 m forming schools earlier than the mesopelagic fishes. Colour indicates scattering values (Sv, dB re m −1). Sunrise is marked with a sun image. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

echotraces, depicted in the same figure, present downwards and upwards trajectories of −65 and 60° ° orientation. Assuming squids of 25 cm ML with a -33° −33° orientation and a TS at 120 kHz of −52.47 dB (following the model in Kang et al., 2005), the mean Sv calculated correspond to densities of 0.2 and 0.8 individuals per cubic metre at the first two subsurface echotraces and at the schools respectively. Using the EK60 sampled volumes at 35 and 300 m depth (0.23 and 2.06cubic metre m3 respectively), this converts into around 0.04 individuals per sample at 35 m depth, and 1.65 individuals within the schools. Vertical migration speeds of the squid aggregations were calculated for the first two vertical echotraces shown by the squids at the subsurface (marked as 1 and 2 in Fig. 3), on their way down and up. Speeds of 0.27 and 0.19 m/s were measured on their descent, while values of 0.48 and 0.42 m/s were measured on their ascent. Squid schools migrating down at dawn travelled at 0.22 m/s while the mesopelagic fish layer descended at 0.27 m/s.

potential squid echotraces present diving patterns, moving up and down, away from and towards the mesopelagic fish layer. There are five patterns (numbered 1 to 5 in Fig. 3) from 5:00 h to 6:35 h starting at 35 m depth and reaching 70, 95, 82, 84 and 82 m, respectively. The first two aggregations present more scattering with a Sv at 120 kHz of -59 −59 dB, while the last three present an Sv of -63 −63 dB. The echotraces evolved from ring-shaped echotraces with a close to 45° descending angle and a near vertical swimming ascension, to round aggregations at 6:35 h, just before beginning the downward migration at dawn. After migrating, squid schools seemed to remain at depths of 250-300 250–300 m. The previously unobserved acoustic echotraces were firstly extracted selecting Sv120 − Sv38ε [-5 −5, 15] dB. The fish layer remained at the Sv120 − Sv38ε [-15, -5 −15, −5] dB echogram. Fig. 4 presents the resulting echograms at 120 kHz after separating (potential) squid and fish echotraces. Mean Sv120 − Sv38 are on the right hand column of Fig. 4. Squids had mean values of Sv120 − Sv38 of 2.7 ± 3.2 2.7 ± 3.2 dB, with a clear increase with depth (0 dB at 35 m depth, and 4 dB at 300 m depth). Sv120 − Sv38 variance on the other hand decreased with depth from ≃4 dB at the subsurface to ≃1-2 1–2 dB within the schools, increasing again to 3-4 3–4 dB at ≃350 m depth. The fish layer had mean values of -8.8 ± 0.9 −8.8 ± 0.9 dB. There were small differences in Sv120 − Sv38 between the diving and the ascending sections of the subsurface echotraces, with -0.7 ± 1.4 dB and -0.5 ± 1.5 −0.7 ± 1.4 dB and −0.5 ± 1.5 dB, respectively. The left panel in Fig. 5 shows three published experimental results of TS120 − TS38 (Target strength, dBre re m −2) with mantle length and the mean Sv120 − Sv38 found in this study (0 dB at 50 m depth and 4 dB at 300 m depth). We assume that Sv120 − Sv38 ≈ TS120 − TS38. Our results are closer to Todarodes pacificus data in Kang et al. (2005). Both Dosidicus gigas and Sthenoteuthis oualaniensis results obtained respectively by Benoit-Bird et al. (2008) and Zhang et al. (2015) present negative values. The right panel in the same figure presents the estimated TS120 − TS38 values for mesopelagic fish using the theoretical model in Peña et al. (2014). Matching the observed and theoretical values was only possible by modifying the shear modulus real part of fish flesh parameter from 105 to 107 (changes in other parameter always left values in the range [−4, 0] dB). Fish with swimbladders of 1.1 cm Equivalent Spherical Ratio (ESR) present the closest values to those observed. Shapes with equal aspect ratio in both axis axes(transforming time x axis into distance in metres) of the squid echotraces are depicted in Fig. 6. Mean values of acoustic and morphological school parameters (Table 1) include squid school lengths between 42 and 95metres m, orientations of −32.5 ± 19.5 ° −32.5 ± 19.5° and mean Sv values at 120 kHz of −53.5 ± 0.5 −53.5 ± 0.5 dB. The subsurface squid

4. Discussion An opportunistic visual detection of the squid Sthenoteuthis pteropus took place at an oceanic station in the Central Eastern Atlantic close to Senegal and Cape Verde. The visual detection and identification of squid in subsurface waters concurred with previously unobserved echotraces detected on the echograms recorded at 38 and 120 kHz. A few individual squid were caught with a fishing line, having lengths between 24 and 30 cm, sizes that fall into the lower size range of mature female Sthenoteuthis pteropus (23 to 27 cm), with larger individuals maturing at 38 to 45 cm. Limits and average sizes of adult squids depend on geographic location and population variability (Zuyev et al., 2002). The first indication that the previously unobserved echotraces could be produced by this species was their novelty on the echogram; none of the other 11 stations in the survey showed similar echotrace shapes. The species caught in the nets were nevertheless similar in terms of acoustic scattering (namely mesopelagic fishes; Olivar et al., 2017). The squid aggregations observed in this study evolved from high density diving echotraces from the mesopelagic layer to depths between 70 to and 95 m to looser aggregations forming rounded shoals just before the downward migration at dawn, when they again formed tight aggregations in schools, reaching depths of 250-300 250–300 m. This subsurface behaviour has not been reported for mesopelagic fish (as far as we know), that usually remain at the surface eating during the night in a stable layer (Peña et al., 2014), but is consistent with squid hunting mesopelagic fishes from below (this is their main prey as shown in Merten et al., 2016). A similar pattern of repetitive shallow dives at 33

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−40 −45

SQUID

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Depth (m)

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Local time (h)

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120

38

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(dB)

−40 −45

50

FISH

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Depth (m)

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38

(dB)

Fig. 4. Upper panels: Acoustic echogram at 120 kHz after selecting Sv120 − Sv38 ∈ [−5, 15] (potential squid echotraces). Lower panels: Acoustic echogram at 120 kHz after selecting Sv120 − Sv38 ∈ [−15, −5] showing the mesopelagic fish layer at the subsurface. Colour indicates scattering values (Sv, dB re m −1). Right plots present the variation in Sv differences with depth for the corresponding group. Sunrise is marked with a sun image. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

patterns were also found for Dosidicus gigas in Benoit-Bird and Gilly (2012), which were associated with feeding behaviour; diving allowed squids to relocate to areas of previously undisturbed prey, adding an element of surprise when attacking fish from below minutes later. As in this study, squid aggregations did not break during feeding. On the contrary, aggregations and parallel swimming seem to be the characteristic of feeding behaviour. The echotrace types found in this study showed aggregated behaviour of well organised well-organized organisms swimming jointly both at the surface, apparently eating, and as migrating schools at dawn. Previous works showed examples of squid forming layers

night was encountered for tagged specimens of Dosidicus gigas in the Gulf of California (Gilly et al., 2006), where the diel migration was accompanied by highly variable dives throughout the night. These authors associated this high-frequency diving behaviour at night (particularly the rhythmic episodes) with foraging behaviour. Similar hunting behaviour, with rapid changes in direction, swimming both forward (head and arms forefront) and backward (fin tip forefront), were videotaped in the large mesopelagic squid Taningia danae by Kubodera et al. (2007). The lunar phase when the squids were detected coincide with the days of more night-time activity at shallower depths (50 to 100 m modal value) in Gilly et al. (2006). Related vertical

0

35

Todarodes pacificus Sthenoteuthis oualaniensis Dosidicus gigas

This study 50 m depth This study 300 m depth

0.8 cm 0.9 cm 1.0 cm 1.1 cm this study

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Mantle length (cm)

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15 -180 10 -12 -11 -10 -9 -8 -7 -6 -5 -4 -3 -2 -1 0

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TS 120-TS 38 (dB)

TS 120-TS 38 (dB)

Fig. 5. Left: TS120 − TS38 (dB) variation with length for several squid species and results found in this study. Todarodes pacificus (Kang et al., 2005), Sthenoteuthis oualaniensis (Zhang et al., 2015), and Dosidicus gigas (Benoit-Bird et al., 2008). Right: Depth and size variation of TS120 − TS38 for mesopelagic fish. The legend indicates the corresponding equivalent spherical radius (ESR) of the swimbladder. Note that values from this study are Sv differences and not TS differences, assuming both are equivalent.

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Fig. 6. Echograms of the surface diving squid echotrace numbered as 2 in Fig. 3 (left) and downward migrating squid schools at dawn (right) after transforming the x axis from ping times to distance. Colour indicates scattering values (Sv, dB re m −1). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Another indication supporting that these echotraces were produced by squids is the location of the station at a oceanographic front (temperature and salinity gradients) where squids were seen jumping out of the water. This behaviour has been tied to long horizontal migrations coupled with different oceanographic regimes, with squids moving from spawning to feeding areas (Hatanaka, 1988; Gilly et al., 2006), and has also been related to conserving energy (Muramatsu et al., 2013; O’Dor et al., 2013). Station 8 is within one of the abundance zones found for S. pteropus in Zuyev et al. (2002), who defined these areas as dynamically active zones of divergences and convergences and hydrological fronts’. The last indication of these echotraces belonging to squids is the accordance in Sv120 − Sv38 values (0 dB at the surface, 4 dB at deeper waters) with reported values of 2 dB for Todarodes pacificus (Kang et al., 2005). Cabreira et al. (2011) and Goss et al. (2001) also found positive values of TS120 − TS38 for squids around 5 dB. Mesopelagic fish layers on the other hand gave negative values all along the MAFIA survey, as well as in the Mediterranean sea Sea (Peña et al., 2014) and the southern Indian Ocean (Béhagle et al., 2017), as predicted by theoretical models. To simulate the values found for mesopelagic fish in this study (Fig. 5), the complex shear modulus of the fish tissue had to be set as 107. This is an uncertain parameter that was evaluated in Scoulding et al. (2015), which included the value used in this study. Although other squid species reported in the literature indicate negative TS120 − TS38 results (Benoit-Bird et al., 2008; Zhang et al., 2015), it may be explained based on squid length and orientation. Fluid-like animals usually show an increase in backscatter with an increase in frequency (Martin et al., 1996) as was the case in this study. However, the frequency of higher scattering is gradually lowered after a certain length, and large individuals may present higher responses at 38 kHz (Benoit-Bird et al., 2008). Zhang et al. (2015) showed a greater response at lower frequencies for small animals (7-15 7–15 cm of mantle length) and a very similar species, the purpleback squid Sthenoteuthis oualaniensis. TS depends on orientation and, as shown in Figure 7 of Kang et al. (2005), TS is higher at 38 kHz for a 24.5 cm ML squid at 0° ° orientation, but higher at 120 kHz for orientations ≥20° ° (swimming

(Madureira et al., 2005) and schools (Arakawa et al., 1998; Cabreira et al., 2011; Sauer et al., 1992; Shibata and Flores, 1972; Shikata et al., 2011). Madureira et al. (2005) identified extensive layers, only detected at night at 300-400 300–400 m depth close to the bottom, as Illex argentinus. The same species in the Patagonian shelf (Cabreira et al., 2011) or Loligo Vulgaris vulgaris in South Africa (Sauer et al., 1992) also formed schools in pre-recruit individuals, separated by sex, with different sizes, shapes and densities. Loose layers of Dosidicus gigas mixed with Merluccius productus were studied in Holmes et al. (2008) at the slope in Northern California, finding an avoidance response in hake (seen as a density decrement) when squid was present. The aggregating behaviour of Todarodes pacificus under different light conditions has also been studied in Arakawa et al. (1998), Shibata and Flores (1972) and Shikata et al. (2011) finding a close relationship between vertical distribution and irradiance intensity. Although Muramatsu et al. (2013) reported faster swimming in fish than squids due to better efficiency of tail over backwards jet propulsion, similar speeds were detected for orangeback squid and mesopelagic fishes migrating downward at dawn in this work (0.22 and 0.27 m/s respectively). Both values are within the ranges estimated for Dosidicus gigas (0.05 to 0.28 m/s) off Peru in Sakai et al. (2017) and are close to the average swimming speeds of Todarodes pacificus (0.28 m/s; Arnaya and Sano, 1990). Swimming speeds were much faster in the upwards movement of the potential squid echotraces at the subsurface (0.48 and 0.42 m/s for schools marked as 1 and 2 in Fig. 3 respectively), which resembled the fastest swimming of Todarodes pacificus (0.40 m/s; Arnaya and Sano, 1990). The estimated numerical densities were similar at the subsurface and at 300 m depths (0.2 and 0.8 individuals per cubic metre respectively) which correspond to 0.04 individuals per sample at the subsurface and 1.65 individuals within the deep migrating squid schools. These values are within the lower limit published in the literature (aggregations of 2 to 1000 individuals; NOAA, 2005). Sthenoteuthis squids form schools (usually animals of the same size) with a high degree of individual and social behavioural organization that is one of most important prerequisites for their ecological progress (Zuyev et al., 2002).

Table 1 School parameters extracted from the 120 kHz echogram. Sv38 is also provided for comparison. School

Height (m)

Depth (m)

Time (h)

Length (m)

Area (m2)

Sv38 (dB)

Sv120 (dB)

Tilt angle (°)

1 2 3 4

6.4 14.9 11.5 7.9

153 264 289 261

06:52 07:03 07:11 07:18

42.5 56.7 76.6 94.9

265.2 831.4 864.3 730.2

−54.6 −54.7 −54.0 −54.9

−53.8 −53.9 −52.9 −53.3

−36 −33 −26 −11

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References

up or down). Theoretical models are simplifications of a very complex scattering process. For squids, only mantle length is commonly considered (Arnaya et al., 1989), but recent publications have included different mantle widths, density inhomogeneities, and natural swimming position of squid appendages, e.g., arms and tentacles, obtaining more accurate results (Jones et al., 2009). The resulting peaks and nulls may explain the observed variability in the dB differences obtained for small squid species such as purpleback squid in Zhang et al. (2015) and orangeback in this study. Changes in behaviour (mainly orientation) and body properties thus have a significant effect on acoustic characteristics. As seen in this study, squid can quickly vary its orientation during feeding, modifying its scattering properties. Sv differences can be due to numerical density (number per cubic metre) or orientation variations (assuming equal length). The shapes of the subsurface echotraces were very similar, indicating similar swimming angles. A decrease in numerical density could therefore be associated with the reduction in Sv along the five subsurface echotraces, while approaching the daily migration time. Differences in Svi − Sv38 (where i are frequencies) on the other hand are often assumed to be independent to numerical density ϱ, as Sv = TS + 10 * log 10(ϱ) (Simmonds and MacLennan, 2005). Thus, by subtracting two Svi, the numerical density term 10 * log 10(ϱ) is removed. The remaining term, TSi − TS38 (for a known species and length) can then be linked to swimming angle variation, particularly for migrating schooling organisms that present well-defined, coherent orientations. The TS of a single target is influenced not only by tilt angle (angle from the horizontal), but also by the position within the beam and the yaw. However, when aggregated targets occupy the whole beam, TS from random yaw (shoaling) is not significantly different to that of fixed yaw (migrating school) (Henderson et al., 2008). According to that, only tilt angle affects the TS of an aggregation, as long as they are randomly distributed within the beam. This fact allows us to consider orientation in the 2D space defined by the echogram without taking into account the athwartship angle. Differences in tilt angle can thus be used to infer behaviour of schooling fish. Mean values of TS120 − TS38 for the potential squid echotraces in this study probably varied with depth due to behaviour (orientation) modification, with higher values in the downmigrating schools, where narrower orientation distributions are expected. Lower values at the subsurface are probably the result of averaging a range of orientations (as the squids are swimming down but also up and likely with angles in between) which is also reflected in the higher variance (∼6 dB). Smoothing and denoising of the acoustic data was key to discriminating (potential) squid and fish echotraces, removing data stochasticity, and finding the core statistical distributions.

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5. Conclusion An opportunistic visual detection of orangeback squid flying out of the water at night in the Central Eastern Atlantic coincided with previously unobserved acoustic echotraces detected on echograms. Acoustic properties, behaviour, swimming speeds and hydrography in the area are consistent with these echotraces being produced by these squid species. This manuscript provides more insight into the acoustic properties (which allow their identification on echograms) and natural behaviour of oceanic squids, a group of species that is less represented in the acoustic literature due to the difficulty in studying them. Acknowledgments The authors are grateful to the crew and technicians on board the R/ V Hesperides for their help during the survey, and to all colleagues who participated in the survey. This research was funded by Spanish Ministerio de Economía y Competitividad (MINECO) through project CTM2012-39587-C04-03. RV was financed by the MINECO project AGL2012-39077. 36

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