Ocean wave observation utilizing motion records of seabirds
Introduction
The ocean environment is a critical factor affecting the ecology of marine animals. Climate change and the rise in extreme climatic events have resulted in increasing recognition of the importance of evaluating climatic effects on animals at multiple levels (Bellard et al., 2012, Chmura et al., 2018). For seabirds, ocean waves, defined as the three-dimensional movement of the sea surface, are an important factor affecting foraging ecology in terms of prey visibility (Clay et al., 2020, Dunn, 1973, Nevitt et al., 2008) and visual recruitment to ephemeral flocks (Haney et al., 1992). Indeed, under extreme high wave conditions, the disturbed surface may prevent seabirds from detecting fish underwater. Seabirds need to run on the sea surface to take off after resting or foraging (Norberg and Norberg, 1971), which is known to be an energetically costly activity (Weimerskirch et al., 2000); therefore, taking-off from the sea surface is also greatly influenced by ocean waves. Furthermore, ocean waves play an important role in building the ocean wind shear layer, which is assumed to be used by many types of soaring seabirds (Bousquet et al., 2017, Richardson, 2011). Thus, ocean waves are expected to play a role in the visual foraging and flight tactics of seabirds. However, while sea winds have been well studied for their key role in the movement and foraging ecology of seabirds (Goto et al., 2017, Weimerskirch et al., 2016, Weimerskirch et al., 2012, Weimerskirch and Prudor, 2019), no study has attempted to quantitatively examine the effects of wave conditions on seabirds. To evaluate and predict the effect of climate change on the behavioral ecology of seabirds, relationships between seabirds in the open sea and ocean waves (e.g., foraging efficiency) must be examined in greater detail than in the few existing studies (Clay et al., 2020, Nevitt et al., 2008).
The major barrier for studying the relationship between ocean waves and seabirds is the paucity of fine-scale information on ocean waves. Although ocean wave parameters, including wave height, period, and direction, are important for the safety of the shipping and fishery industries (Ardhuin et al., 2019, Caires et al., 2005, Quartly and Kurekin, 2020), ocean wave observation networks still suffer from large data gaps compared to observation networks of other parameters, such as the Argo temperature/salinity profiling float (Wong et al., 2020). Owing to the recently developed remote sensing systems, satellite-borne radar altimeters can estimate wave properties around the world. Oceanographic observation buoys dispersed across global oceans provide in-situ observational data on ocean waves. However, satellite telemetry still suffers from limited spatial sampling; most satellite altimeters have a sampling cycle of 10–35 days (Ardhuin et al., 2019) and are restricted to measuring only the wave height (Caires et al., 2005). The observation network of buoys also has spatial gaps in some parts of the global ocean, particularly in the Southern Ocean and the tropics (Ardhuin et al., 2019).
To compensate for spatiotemporal observation gaps, there is a need to develop new low-cost platforms to observe ocean waves globally (Ardhuin et al., 2019). Although the paucity of ocean wave networks, which can easily overlook particular ocean events (Ardhuin et al., 2019), is a significant issue for improving forecast accuracy for marine safety and understanding air-sea interactions (Quartly and Kurekin, 2020), it is also an obstacle for evaluating the effect of ocean waves on marine animals. To study how ocean waves affect seabird ecology, fine-scale (time and spatial) wave information, which reflect the actual experience of seabirds, is necessary, and large spatiotemporal averaged or forecasted values are helpful but generally not reliable enough, considering local wave conditions change rapidly on a daily or hourly scale.
During the last decade, the field of biological science using animal-borne data loggers, known as biologging, has enabled scientists to expand their research with the development of miniaturized devices (Wilmers et al., 2015). Beyond the field of biology, biologging has facilitated the collection of environmental variables, such as ocean water temperature, salinity, ocean winds, and ocean currents, from unobservable places using animals with extensive locomotion ability (Charrassin et al., 2008, Goto et al., 2017, Harcourt et al., 2019, Roquet et al., 2014, Sánchez-Román et al., 2019, Yoda et al., 2014, Yonehara et al., 2016). However, despite the demands for integrated ocean observation and improved ocean knowledge (Villas Bôas et al., 2019), a comprehensive observation of ocean wave parameters using animals has not yet been performed (Cazau et al., 2017). In this study, a simple but unique method for estimating ocean waves from global navigation satellite system (GNSS) motion records of seabirds floating on the sea surface is demonstrated. GNSS, specifically the global positioning system (GPS), is one of the most commonly used sensors for wave observation buoys to collect sea surface displacement. Although differential GPS, which requires an additional GPS reference station onshore, is the major GPS positioning method used for wave observation in the past, the feasibility of a wave monitoring buoy mounting single-GPS (stand-alone positioning) receiver, which does not require an additional shore station, has been demonstrated (DeVries et al., 2003, Harigae et al., 2004). Single-GPS wave observation buoys are now used in a manner similar to traditional buoys (DeVries et al., 2003, Harigae et al., 2004, Herbers et al., 2012, Villas Bôas et al., 2019). Therefore, with the appropriate usage, a single-GPS receiver mounted on a seabird would be sufficiently reliable to collect wave conditions experienced by seabirds in the open sea, as long as seabirds remain on the sea surface.
The aim of this study was to evaluate the possibility of bird-based wave observations and to examine the preference of seabirds under various wave conditions. In this study, data recorders equipped with a high time-resolution GPS receiver (five positional fixes every second) were used. Recorders were deployed on the backs of two species of seabirds, streaked shearwater (Calonectris leucomelas; mean body mass, 0.6 kg) and wandering albatross (Diomedea exulans, 9.1 kg), to record the passive motion derived from ocean waves when they sat on the sea surface. These species were chosen because they are known to have floating time on the sea surface during foraging trips (Shaffer et al., 2001, Yoda et al., 2014). They are also known to seize prey at the sea surface and rarely make deep dives (Cherel and Weimerskirch, 1999, Matsumoto et al., 2012, Prince et al., 1994). Moreover, since wandering albatrosses inhabit annual high wave areas in the Southern Hemisphere (Suryan et al., 2008), their preference for waves is of interest, and it also enables us to collect and examine a large range of wave heights. Wave parameters (height, period, and direction) were calculated from the motion records, and the accuracy of bird-based wave parameters was first examined by comparing the wave observation buoy and streaked shearwaters. We then added data from wandering albatrosses and further validated them using hindcast models. Finally, it was determined whether a wave height preference of seabirds exists, and the impact of ocean waves on seabird behavior was discussed using an example of wave height distribution experienced by wandering albatrosses in the southern Indian Ocean.
Section snippets
Recorder characters and validation of the recorder’s performance
The recorders used in this study were Ninja-scan (Little Leonardo, Japan), which was configured to record 3D GPS positions and Doppler velocity (5 Hz), triaxial acceleration and angular velocity (100 Hz), temperature (6 Hz), pressure (6 Hz), and geomagnetism (6 Hz). There are two types of Ninja-scans with different battery masses (Naruoka et al., 2021). Small Ninja-scans weighed 28 g, which corresponds to less than 5% of the body mass of streaked shearwater and are expected to record for 7 h.
Availability of animal-borne recorders for ocean wave observations
Prior to mounting recorders on seabirds, the ability of a single-GPS receiver to record wave movement was tested by attaching it to a wave observation buoy. The vertical wave motion (vertical displacement) obtained from the high-pass filtered GPS altitude record (100 min) of the attached recorder closely fitted the record of the wave observation buoy (Fig. S1A in the Supplementary Data). The regression slope between the buoy and recorder was 1.035 (99% CI: 1.027–1.043), and the Pearson’s R was
Wave observations utilizing seabirds
This study demonstrates that it is possible to use floating seabirds equipped with loggers to measure ocean waves. The mean error of the bird-based wave observation and its standard deviation compared to the buoy fall within the accuracy requirement range for the wave observation (∼0.1–0.5 m for height, ∼0.1–1 s for wave period, and 10° for wave direction) (Ardhuin et al., 2019, WMO, 2018), indicating the reliable accuracy of bird-based wave observations. Some measurement results of the wave
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Tatsuo Abe, Takanori Abe, Masaaki Hirano, Takanori Suzuki, Aran Garrod, Sei Yamamoto, Julien Collet, Timothée Poupart, and all the members of the research vessel “Shinsei-Maru” and the research station of Crozet Islands for their support during the fieldwork. We appreciated fruitful comments from Kagari Aoki and Chihiro Kinoshita. We also thank Michihiko Suzuki, Koichiro Ikeda, Takashi Mukai, and Taichi Sakamoto for developing the Ninja-scan. The field studies were financially
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