Next Article in Journal
Effects of Selenium Yeast Addition on the Growth, Intestinal Health, Immune Status and Body Composition of Juvenile Sea Cucumber Apostichopus japonicus before and after Aestivation
Next Article in Special Issue
Seasonal Occurrence of the Indian Ocean Blue Whale (Balaenoptera musculus indica) off South Coast of Sri Lanka
Previous Article in Journal
Green Composites for Maritime Engineering: A Review
Previous Article in Special Issue
Water Surface Behaviour of Irrawaddy Dolphin Orcaella brevirostris (Owen in Gray, 1866) and Influencing Factors in the Bay of Brunei, Brunei Darussalam
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JMSE
Volume 11
Issue 3
10.3390/jmse11030600
jmse-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Exfoliating Whales–Sandy Bottom Contact Behaviour of Humpback Whales

by
Jan-Olaf Meynecke
1,2,*,
Johan Gustafon
2 and
David E. Cade
3
1
Whales & Climate Research Program, Griffith University, Gold Coast 4222, Australia
2
Centre for Coastal and Marine Research, Griffith University, Gold Coast 4222, Australia
3
Hopkins Marine Station, Stanford University, Monterey Bay, Pacific Grove, CA 93950, USA
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(3), 600; https://doi.org/10.3390/jmse11030600
Submission received: 12 February 2023 / Revised: 6 March 2023 / Accepted: 8 March 2023 / Published: 12 March 2023
(This article belongs to the Special Issue Assessment of Marine Mammal Ecological Traits and Habitat Conservation)
Browse Figures
Versions Notes

Abstract

:
Cetaceans are known for their intelligence and display of complex behaviours including object use. For example, bowhead whales (Balaena mysticetus) are known to rub on rocks and some humpback whale (Megaptera novaeangliae) populations undertake lateral bottom feeding. Such underwater behaviour is difficult to observe but can play a critical role in the whales’ survival and well-being. Distinguishing social behaviours from those which serve a specific function remains challenging due to a lack of direct observations and detailed descriptions of such behaviours. A CATS (Customized Animal Tracking Solutions) suction cup tag with on board video and a 3D inertial measurement unit was deployed on three different humpback whales to assess their behaviour in the Gold Coast bay, Australia. Here, we present evidence of humpback whales (tagged and untagged individuals) performing bottom contact with prolonged rolling on sandy substrate. In addition, we showed that fish were actively feeding from the whales’ skin during this behaviour. We detail the behaviour and discuss possible drivers, with a focus on cetacean innovation, possible ectoparasite removal, and habitat preferences.

1. Introduction

The humpback whale (Megaptera novaeangliae) is a large baleen whale species that is present in all oceans [1]. They are generalist consumers with higher reproduction rates relative to other baleen whales [2,3,4]. Their ability to adapt and take advantage of available prey allowed a more complete recovery from extensive whaling in the 20th century [5]. Their comeback was celebrated as a conservation success [6] but requires ongoing conservation efforts due to increasing anthropogenic stressors [7,8]. Humpback whales are one of the most studied whale species; however, their fine scale habitat use, complex social interactions, feeding techniques, and preferences for environmental conditions are still not well understood [9]. Such information on behaviour can provide important insights into habitat preferences and inform conservation management on how to enhance species well-being [10].
The majority of observations for humpback whales and other cetaceans are derived from surface behaviour. The intelligence of cetaceans facilitates complex interactions and feeding strategies [11,12,13,14]. While such behaviour is well known for delphinids, it is less commonly described for baleen whales. However, humpback whales were seen to facilitate “trap-feeding” [14], bubble net feeding [13], interact with seaweed [15] as well as jellyfish [16]. They were also observed using their body to protect other species from killer whales (Orcinus orca) [17]. Baleen whales were also observed exhibiting behaviours, such as bottom contact, that are not associated with feeding. Aerial footage from drones showed that bowhead whales (Balaena mysticetus) were using rocks to assist with removal of skin during summer with the whales selecting their habitats based on geological and oceanographic features [12,18].
A similar activity was described for belugas (Delphinapterus leucas) undertaking active abrasion of the skin to enhance moulting by rubbing on pebble, mud, and limestone on the bottom of shallow waters [19]. Such behaviour was not documented for humpback whales but bottom contact behaviour was mentioned in a breeding area at Trinidad Island, Brazil, during visual observations from boats and while free diving. A humpback whale was observed rubbing on the sandy bottom at 35 m depth [20]. Other bottom contact behaviour reported for humpback whales was related to feeding activities and studied in more detail.
Humpback whales have developed different feeding techniques suited to environmental conditions and types of prey, e.g., bubble net feeding for fish [13] and lunge feeding on krill [21]. Lateral feeding behaviour, a technique performed by gray whales (Eschrichtius robustus) [12], is a less common behaviour for humpback whales and was first described in the Gulf of Maine where humpback whales were targeting sand lance (Ammodytes spp.) and herring (Clupea harengus) [22,23,24]. It includes one or more off-axis rolls of greater than 45°, presumably feeding along the bottom with each roll. Friedlander et al. [23] showed that the type of feeding was linked to the abundance of the prey species with whales exhibiting both bottom and surface feeding behaviour. Observations and studies were made using digital acoustic recording tags (Dtags) that provided records on audio, pitch, roll, heading, and depth [25].
Biotelemetry was used successfully in a number of studies to conduct research on subsurface behaviour with suction cup tags such as Dtags or the combined video and 3D-accelereometer CATS (Customized Animal Tracking Solutions) tags with minimal impact on the tagged individuals [26]. These tags were deployed on various species (O. orca, Balaenoptera musculus, B. bonaerensis) [27,28,29] and with different archival loggers attached (temperature, velocity, depth, sound, cameras) using poles or cross bows for deployment. For example, CATS tags were used to study suckling rates for humpback whale calves for the first time [30,31] and deployed to document minke whales in Antarctica (B. bonaerensis) [32]. They allow the assessment of type, time, and frequencies of behaviour, along with body angles, body accelerations, depth, and location. Predominantly, humpback whale tagging studies focused on breeding grounds [33], feeding grounds [34], and large scale migration [35]. Very few subsurface behaviour studies investigated resting and socialising areas or migratory corridors.
Here, we provide a previously undescribed humpback whale behaviour, sand rolling, in a resting and socialising area on the east coast of Australia using CATS tags. The function of the newly discovered behaviour is further discussed in the context of enhanced moulting or a form of socialising. Documenting these types of behaviour is relevant for conservation management and an improved understanding of the species habitat preferences [36].

2. Materials and Methods

The Gold Coast Bay is a shallow open embayment with a mean depth of 40 m located at 27° S, 153° E in southeast Queensland, Australia (Figure 1). The mouth of the bay is roughly 80 km wide from the northern tip of North Stradbroke Island to Tweed Heads at the border of Queensland and New South Wales. The opening faces east, with the bay area connected to the Coral Sea throughout its domain. The bottom substrate mainly consists of sand with some rocky reefs [37]. It is an important aggregation site where humpback whales rest, socialise, and breed [38,39], within 10 km of their migratory corridor during southern and northern migrations between June and October each year [38,40].
Whales were tagged between August 2021 and October 2022 with CATS suction cup tags (https://www.cats.is, accessed on 15 November 2022) [41]. These systems were fitted with 4 silicon suction cups; a magnesium release system; a VHF transmitter for retrieval, an integrated high-definition video (1920 × 1080 resolution) with tri-axial accelerometers and gyroscopes; magnetometers; a hydrophone and light, pressure, temperature and GPS sensors. They were used extensively on a variety of whales [28,42,43]. The magnesium release was set to release within approximately 4 hrs after tag deployment to ensure recovery within the same day from the bay area.
For the deployment of the tag, we used a 6 m rigid-hull inflatable vessel and a 5 m carbon pole. During deployment, we aimed to attach the tag near the dorsal fin to achieve a forward vision from the tag’s camera. Whales were approached slowly (<6 knots) for the deployment and dive times, behaviour and swimming speed were recorded before and after deployment by two trained observers.
Video material was analysed visually and assessed for behaviour. Sections of sand rolling were extracted to investigate duration, swim speed, dive profile, and pitch. Data were analysed using MATLAB tools developed for CATS tags [44]. Distance travelled and swim speed was calculated from a georeferenced pseudo-track [45]. Sand rolling was defined as any visible movement of whales on the ocean floor either stationary or slowly moving forward while the whale was on its back (full roll) or sideways (side roll).

3. Results

Three deployments were undertaken in August and October in 2021 and in October 2022 on the Gold Coast, Queensland, Australia (Figure 1). The first deployment (tag a) took place 8 kilometres offshore at 37 m depth lasting 388 min, the second deployment (tag b) was carried out 14 km offshore at 49 m depth with a duration of 193 min and the third deployment (tag c) took place 7 km offshore at 35 m depth and came off after 257 min (Table 1). All tagged whales were migrating south during their southern migration from breeding grounds located further north in the Great Barrier Reef.
Visual observations for the first tagged individual (tag a) lasted for one hour with 30 min before and 30 min after tag deployment. There were three whales in the pod with two adults (>10 m length) and one subadult (<10 m length). One of the larger whales was tagged. We suspected this to be a possible male given its visible scarring; however, the sex could not be determined further. The pod showed little surface activity with dive times ranging from 2 to 5 min. The average speed over the deployment period based on the calculated pseudo-track was 2.9 km/h, covering 18.8 km. The first sand rolls occurred 57 min after the deployment over a 15 min time period. It consisted of multiple rolls (five full and two side rolls) lasting between 25 s and 95 s at a depth of 47 m over what appeared to be fine sand with some rubble (Supplementary Table S1). The accompanying whale can be seen undertaking a full roll at 35 m depth an hour later (Figure 2(a1,a2)). Silver trevally (Pseudocaranx georgianus) were visibly feeding on the whale skin while the whale was rolling in the sand (Figure 3).
The second tag (Tag b) was attached to an adult whale (estimated at >12 m in length), recognised as a male in a pod of six whales consisting of a mother calf pair with an escort and two smaller sized males around 10–12 m in length, which were visually identified as males from the underwater footage. The tagged individual showed aggressive, competitive behaviour consisting of pushing competitors on the surface (motorboating) and fast, close approaches to the other whale with an attempt to follow the mother and calf pair. One individual showed signs of a fresh dorsal injury that likely resulted from body contact with the other whales. The pod was observed for over two hours and over that period, dive times consisted of 2–6 min. Head lunges and over 27 tail slaps were counted. The tagged individual was observed undertaking similar behaviour on another pod prior to deployment. The tagged whale split from the larger pod after nearly 2 h. During tag deployment, the whale covered a distance of 16.9 km at an average speed of 5.4 km/h. At least 10 common dolphins (Delphinus delphis) were also present and were observed interacting with the competing whales through close approaches for the first half of the deployment.
Sand rolling of the tagged individual and of at least one accompanying whale that can be seen rolling at the same time took place 107 min after deployment. A half roll was performed that lasted for 47 s after which the pod split (Supplementary Table S1). Rolling took place at 49 m depth on fine, sandy substrate (Figure 4).
The third tag deployment was undertaken in a pod of two adult whales estimated to be larger than 12 m in length. The pod was observed 30 min prior tag deployment and for 3 h while the tag was deployed from a vessel. Both whales were very surface active with display of courtship behaviour such as pectoral slaps and rolling (also recorded by tags gyroscope) as well as several breaches. Two hours after tag deployment, another two whales joined the pod resulting in a change of behaviour with tail slaps and tail lobbing, indicating competitive behaviour that was also captured by the tag with fast approaches of the tagged whale towards the whales that had joined. The distance covered during deployment was 19.6 km distance with an average swim speed of 4.7 km/h. About 20 min after deployment, sand rolling of the tagged animal was observed with two full rolls and three side rolls lasting 4.40 min and another side roll was performed 50 min after deployment. Both behaviours occurred in 45 m depth in fine, sandy substrate (Figure 4, Supplementary Table S1).
On all occasions of sand rolling, the whales were observed on video to be slowly moving forward with their head first into the sand followed by rolling to one side or a full roll. Even when the whales were on their back, they were slowly moving forward. The duration of a sequence of rolls consisting of four full or side rolls lasting each between 28 to 95 s took about 5 min. The average time for sand rolling was 49 s for all 14 identified rolls.
Out of 14 documented rolls, 13 were at least 150° (one roll was only 90°), and all whales displayed a lateralised preference for rolling to the right first with 12 out of 14 rolls being to the right and 2 to the left.
Skin was observed to be falling off during the process of all identified rolls. The depth range for the behaviour was found to be between 35 and 50 m depth on fine, sandy substrate. For tag a and c, juvenile silver trevally were observed feeding from the whales skin by picking it directly off the whales body.

4. Discussion

We documented and analysed sand rolling by humpback whales along their migratory corridor for a number of individuals in the context of different behavioural stages. While lateral feeding behaviour was reported for humpback whales [24], this purpose can be excluded for the observations on the Gold Coast. There was no feeding activity on camera and there was also no suitable prey available in this region on sandy bottoms.
Pinheiro et al. [20] suggested cleaning as the reason for their observation in Trinidad, Brazil. However, a detailed assessment was not possible due to observations being made from the boat and free diving. The CATS tag video and accelerometer allowed a more detailed assessment of the behaviour for a total of five individuals of which three were tagged. During the three different deployments, the sand rolling was observed in the context of socialising. The behaviour was either following courtship (tag c), competition (tag b) or other forms of socialising (tag a). Here, we posit that the whales exfoliate using the sand to assist with moulting and removal of ectoparasites such as barnacle, though alternative functions, such as social bonding or calming activity should also be explored in future work.
The individuals performing the sand rolling were all involved in social activity, albeit in a very different context. The Gold Coast Bay is known as a socialising and resting area, suggesting that this type of behaviour maybe more frequent [46]. Tag a was deployed on an individual that was moving slow at an average speed of 1.8 km/h together with two other whales. There was no competitive or aggressive behaviour observed during the boat based on visual observations or from the underwater video. In contrast, deployment of tag b, which was on a suspected male, displayed competitive and aggressive behaviour in particular for the first half of the tag deployment while with a mother calf pair and three other whales. Males are known to seek and, in some cases, harass mother–calf pairs for possible mating [47]. The individual was travelling at an average speed of 5.4 km/h. It is possible that the sand rolling minutes before the tagged whale left the pod was not just in the context of removing access skin but also part of a social interaction with at least one of the competitors visible and rolling in the sand as well.
During the first two hours of the deployment of tag c, the suspected male displayed courtship behaviour towards an accompanying whale that was later identified as a female through underwater footage. During this time, sand rolling occurred multiple times over a period of several minutes. Bottom contact socialising behaviour is known from orcas in British Columbia and Alaska where the resident community rubs on the rocky seabeds as a social activity and less likely because of skin removal [48].
Humpback whales, and other mysticetes, were reported to engage in forms of play [49,50,51]. This includes previously documented object play with seaweed [15], cargo netting and rope [51], and even jellyfish [16]. Interaction with other species were also witnessed [52]. This type of behaviour suggests complex interactions of humpback whales with their environment. It is, therefore, possible that the sand rolling is a form of play and may be exfoliation.
The first theory that sand rolling is beneficial for removal of excess skin and removal of ectoparasites seems more obvious than for undertaking this behaviour than for socialising alone. There could be potentially therapeutic benefit in ectoparasite removal and excess skin removal. This type of behaviour is also known from other cetaceans such as bowhead whales. These baleen whales were seen rubbing on rocks regularly, which likely facilitates their moulting [18]. Throughout the class, Mammalia skin care is an essential component of well-being and health. For example, terrestrial mammals such as horses [53] and other herbivores regularly undertake dust bathes [54]. Pitman et al. [55] described skin removal and moulting of cetaceans as an essential part of their migration. Whales that are unwell are often recognised by their deteriorated skin conditions [56].
All tagged individuals slowly moved forward along the sand even when rolling from side to side (Supplementary Video S1). The whales strategically moved their head and rostrum forward into the sand and the tip of the lower jaw, two areas that are known to be densely populated with ectoparasites [57]. In addition, the pectoral fins were seen to be pushed along the sandy bottom. Bio-fouling is a common problem amongst humpback whales and other larger cetaceans. There are body parts that are favourable for ectoparasites and sessile invertebrates such as the tubercles on the rostrum and flippers, and whale lice are commonly found in wounds, on pectoral fins and within ventral pleats [1,57].
In particular, in tropical and subtropical waters, barnacles attach to the whales in their early life stages. All three deployments took place during the southern migration when whales migrate from the tropical breeding grounds to their feeding ground in Antarctica. Whales need to remove barnacles frequently to avoid excessive growth that leads to drag and energy loss [1]. Humpback whales host diverse communities of skin bacteria [58] that can pose a threat for open wounds if bacteria grow in large numbers. Removing excess skin is likely a necessity to maintain a healthy bacterial skin community. Humpback whales can remove some barnacles and skin through surface activity such as breaches but not all [59].
At two deployments (tag a and c), silver trevally were observed feeding on whale skin directly from their body. We cannot exclude the possibility that whales specifically target regions where small fish are likely to feed of the whale’s skin to enhance the skin removal similar to clean stations visited by other species [60]. Other cetaceans such as bottlenose dolphins use specific corals and sponges in coral reefs to self-medicate [61]. Given the complexity of previously described behaviour for this species, it is possible that humpback whales employ additional behavioural strategies, such as the one described here, to reduce or remove bio-fouling. Undisturbed access to areas that the whales select for skin removal is important for their conservation. Coastal areas such as the Gold Coast region are subject to increased vessel traffic and noise pollution that can disrupt the whale’s behaviour.
We do need to consider the possibility that the tagged individuals wanted to remove the tag. A direct response to the tag appears unlikely as accompanying whales were observed undertaking the same behaviour and the described sand rolling did not target the location where tag was deployed. So far, other studies using suction cup tags did not describe this behaviour or an attempt to actively remove the tags [62,63]. Canning et al. [22] reported no impact from suction cup tagging with Dtags or behaviour shifts that could be linked to the tagging itself.

5. Conclusions

Documentation of innovative behaviours in humpback whales and mysticete whales in general, such as the one described here, have been increasing in recent years. It is likely that other, yet to be discovered behaviours of these charismatic species exist, which will be observed through the use of underwater camera systems and drones. New technologies such as underwater cameras with a larger field of view (e.g., 360° field-of-view composed of two lenses with a 180° field-of-view) can assist with the observation of multiple accompanying whales and provide additional data [64].
Future studies should target socialising humpback whales in similar depth range over sandy bottom to see if the behaviour of sand rolling consistently repeats. Based on the patterns recognised in the present study, it should be possible to distinguish the behaviour by tag orientation and dive profiles in future tag deployments. In particular, deployments in other similar regions such as Hervey Bay, Australia, that are known for sandy bottoms versus regions with different, e.g., rocky substrate, could add to a better understanding of the scale and specific habitat preference of this behaviour. In addition, analyses of sound prior and post sand rolling can be included in future analyses. Singing male humpback whales, for example, have a preference for shallow water (between 15–55 m depth), sandy substrates, and flat seafloors [65,66]. It is reasonable to speculate that humpback whales seek sandy substrate specifically to roll, similar to bowhead whales selecting habitat with suitable rocks for rubbing [18]. Undisturbed access to such habitats is likely important for the whale’s well-being and should be considered in whale conservation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11030600/s1, Table S1: Sand rolling frequency and duration; Video S1: Sample of sand rolling from tag b.

Author Contributions

Conceptualization, J.-O.M.; methodology, J.-O.M. and J.G.; software, D.E.C.; validation, J.-O.M., J.G. and D.E.C.; formal analysis, J.-O.M., J.G. and D.E.C.; resources, J.-O.M. and J.G.; writing—original draft preparation, J.-O.M.; writing—review and editing, J.-O.M., D.E.C. and J.G.; visualization, J.-O.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by a grant to Griffith University from a private charitable trust to the Whales & Climate Research Program www.whalesandclimate.org (accessed on 31 January 2023).

Institutional Review Board Statement

The animal study protocol was approved by the Ethics Committee of Griffith University (ENV/01/21/AEC). All research was undertaken under the permit of Queensland Permit WA0009070 and Commonwealth water permit C2016-0003 and CP2021.0002.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available on request.

Acknowledgments

The authors like to thank Wayne Phillips and supporting staff from Sea World Research & Rescue Foundation and equipment as well as outstanding technical support from CATS Customized Animal Tracking Solutions.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Clapham, P.J. The humpback whale. In Cetacean Societies, Field Studies of Dolphins and Whales; The University of Chicago: Chicago, IL, USA, 2000; pp. 173–196. [Google Scholar]
  2. Eisenmann, P.; Fry, B.; Holyoake, C.; Coughran, D.; Nicol, S.; Bengtson Nash, S. Isotopic Evidence of a Wide Spectrum of Feeding Strategies in Southern Hemisphere Humpback Whale Baleen Records. PLoS ONE 2016, 11, e0156698. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Wedekin, L.L.; Engel, M.H.; Andriolo, A.; Prado, P.I.; Zerbini, A.N.; Marcondes, M.M.C.; Kinas, P.G.; Simões-Lopes, P.C. Running fast in the slow lane: Rapid population growth of humpback whales after exploitation. Mar. Ecol. Prog. Ser. 2017, 575, 195–206. [Google Scholar] [CrossRef] [Green Version]
  4. Pallin, L.J.; Baker, C.S.; Steel, D.; Kellar, N.M.; Robbins, J.; Johnston, D.W.; Nowacek, D.P.; Read, A.J.; Friedlaender, A.S. High pregnancy rates in humpback whales (Megaptera novaeangliae) around the Western Antarctic Peninsula, evidence of a rapidly growing population. R. Soc. Open Sci. 2018, 5, 180017. [Google Scholar] [CrossRef] [Green Version]
  5. Fleming, A.; Jackson, J. Global Review of Humpback Whales (Megaptera novaeangliae). 2011. Available online: https://repository.library.noaa.gov/view/noaa/4489 (accessed on 10 January 2023).
  6. Duarte, C.M.; Agusti, S.; Barbier, E.; Britten, G.L.; Castilla, J.C.; Gattuso, J.-P.; Fulweiler, R.W.; Hughes, T.P.; Knowlton, N.; Lovelock, C.E.; et al. Rebuilding marine life. Nature 2020, 580, 39–51. [Google Scholar] [CrossRef]
  7. Calambokidis, J.; Fahlbusch, J.A.; Szesciorka, A.R.; Southall, B.L.; Cade, D.E.; Friedlaender, A.S.; Goldbogen, J.A. Differential Vulnerability to Ship Strikes Between Day and Night for Blue, Fin, and Humpback Whales Based on Dive and Movement Data From Medium Duration Archival Tags. Front. Mar. Sci. 2019, 6, 543. [Google Scholar] [CrossRef] [Green Version]
  8. Meynecke, J.-O.; Seyboth, E.; De Bie, J.; Menzel Barraqueta, J.-L.; Chama, A.; Prakash Dey, S.; Lee, S.B.; Tulloch, V.; Vichi, M.; Findlay, K.; et al. Responses of humpback whales to a changing climate in the Southern Hemisphere: Priorities for research efforts. Mar. Ecol. 2020, 41, e12616. [Google Scholar] [CrossRef]
  9. Reinke, J.; Lemckert, C.; Meynecke, J.-O. Coastal fronts utilized by migrating humpback whales, Megaptera novaeangliae, on the Gold Coast, Australia. J. Coast. Res. 2016, 75, 552–557. [Google Scholar] [CrossRef]
  10. Hazen, E.L.; Friedlaender, A.S.; Thompson, M.A.; Ware, C.R.; Weinrich, M.T.; Halpin, P.N.; Wiley, D.N. Fine-scale prey aggregations and foraging ecology of humpback whales Megaptera novaeangliae. Mar. Ecol. Prog. Ser. 2009, 395, 75–89. [Google Scholar] [CrossRef] [Green Version]
  11. Parra, G.J. Observations of an Indo-Pacific humpback dolphin carrying a sponge: Object play or tool use? Mammalia 2007, 71, 147–149. [Google Scholar] [CrossRef] [Green Version]
  12. Woodward, B.L.; Winn, J.P. Apparent lateralized behaviour in gray whales feeding off the central British Columbia coast. Mar. Mammal Sci. 2006, 22, 64–73. [Google Scholar] [CrossRef]
  13. Wiley, D.; Ware, C.; Bocconcelli, A.; Cholewiak, D.; Friedlaender, A.; Thompson, M.; Weinrich, M. Underwater components of humpback whale bubble-net feeding. Behaviour 2011, 148, 575–602. [Google Scholar]
  14. McMillan, C.J.; Towers, J.R.; Hildering, J. The innovation and diffusion of “trap-feeding,” a novel humpback whale foraging strategy. Mar. Mammal Sci. 2019, 35, 779–796. [Google Scholar] [CrossRef]
  15. Owen, K.; Dunlop, R.; Donnelly, D. Seaweed interactions by humpback whales (Megaptera novaeangliae): A form of object play? Aquat. Mamm. 2012, 38, 418. [Google Scholar] [CrossRef]
  16. Shea, B.D.; Gallagher, A.J. Humpback Whale Instigates Object Play with a Lion’s Mane Jellyfish. Oceans 2021, 2, 386–392. [Google Scholar] [CrossRef]
  17. Pitman, R.L.; Deecke, V.B.; Gabriele, C.M.; Srinivasan, M.; Black, N.; Denkinger, J.; Durban, J.W.; Mathews, E.A.; Matkin, D.R.; Neilson, J.L.; et al. Humpback whales interfering when mammal-eating killer whales attack other species: Mobbing behavior and interspecific altruism? Mar. Mammal Sci. 2017, 33, 7–58. [Google Scholar] [CrossRef]
  18. Fortune, S.M.E.; Koski, W.R.; Higdon, J.W.; Trites, A.W.; Baumgartner, M.F.; Ferguson, S.H. Evidence of molting and the function of “rock-nosing” behavior in bowhead whales in the eastern Canadian Arctic. PLoS ONE 2017, 12, e0186156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Smith, T.; Aubin, D.; Hammill, M. Rubbing behaviour of belugas, Delphinapterus leucas, in a high Arctic estuary. Can. J. Zool. 2011, 70, 2405–2409. [Google Scholar] [CrossRef]
  20. Pinheiro, F.C.F.; Pinheiro, H.T.; Siciliano, S.; Santos, R.G. Bottom contact behaviour by humpback whales in Brazilian waters: First underwater observations at Trindade Island. Mar. Biodivers. Rec. 2016, 9, 64. [Google Scholar] [CrossRef] [Green Version]
  21. Ware, C.; Friedlaender, A.S.; Nowacek, D.P. Shallow and deep lunge feeding of humpback whales in fjords of the West Antarctic Peninsula. Mar. Mammal Sci. 2011, 27, 587–605. [Google Scholar] [CrossRef]
  22. Canning, C.; Crain, D.; Eaton, T.S.; Nuessly, K.; Friedlaender, A.; Hurst, T.; Parks, S.; Ware, C.; Wiley, D.; Weinrich, M. Population-level lateralized feeding behaviour in North Atlantic humpback whales, Megaptera novaeangliae. Anim. Behav. 2011, 82, 901–909. [Google Scholar] [CrossRef]
  23. Friedlaender, A.S.; Hazen, E.L.; Nowacek, D.P.; Halpin, P.N.; Ware, C.; Weinrich, M.; Hurst, T.; Wiley, D. Diel changes in humpback whale Megaptera novaeangliae feeding behavior in response to sand lance Ammodytes spp. behavior and distribution. Mar. Ecol. Prog. Ser. 2009, 395, 91–100. [Google Scholar] [CrossRef]
  24. Hain, J.H.W.; Ellis, S.L.; Kenney, R.D.; Clapham, P.J.; Gray, B.K.; Weinrich, M.T.; Babb, I.G. Apparent bottom feeding by humpback whales on Stellwagen Bank. Mar. Mammal Sci. 1995, 11, 464–479. [Google Scholar] [CrossRef]
  25. Ware, C.; Arsenault, R.; Plumlee, M.; Wiley, D. Visualizing the Underwater Behavior of Humpback Whales. IEEE Comput. Graph. Appl. 2006, 26, 14–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Andrews, R.D.; Baird, R.W.; Calambokidis, J.; Goertz, C.E.C.; Gulland, F.M.D.; Heide-Jorgensen, M.P.; Hooker, S.K.; Johnson, M.; Mate, B.; Mitani, Y.; et al. Best practice guidelines for cetacean tagging. J. Cetacean Res. Manag. 2019, 20, 27–66. [Google Scholar] [CrossRef]
  27. Johnson, M.; Tyack, P.; Nowacek, D.; Shorter, A. A digital acoustic recording tag for measuring the response of marine mammals to sound. J. Acoust. Soc. Am. 2000, 108, 2582–2583. [Google Scholar] [CrossRef]
  28. Friedlaender, A.S.; Goldbogen, J.A.; Nowacek, D.P.; Read, A.J.; Johnston, D.; Gales, N. Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis). J. Exp. Biol. 2014, 217, 2851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Baird, R. Studying diving behavior of whales and dolphins using suction-cup attached tags. Whalewatcher 1998, 31, 3–7. [Google Scholar]
  30. Ratsimbazafindranahaka, M.N.; Huetz, C.; Andrianarimisa, A.; Reidenberg, J.S.; Saloma, A.; Adam, O.; Charrier, I. Characterizing the suckling behavior by video and 3D-accelerometry in humpback whale calves on a breeding ground. PeerJ 2022, 10, e12945. [Google Scholar] [CrossRef]
  31. Tackaberry, J.E.; Cade, D.E.; Goldbogen, J.A.; Wiley, D.N.; Friedlaender, A.S.; Stimpert, A.K. From a calf’s perspective: Humpback whale nursing behavior on two US feeding grounds. PeerJ 2020, 8, e8538. [Google Scholar] [CrossRef] [Green Version]
  32. Linsky, J.M.J.; Wilson, N.; Cade, D.E.; Goldbogen, J.A.; Johnston, D.W.; Friedlaender, A.S. The scale of the whale: Using video-tag data to evaluate sea-surface ice concentration from the perspective of individual Antarctic minke whales. Anim. Biotele. 2020, 8, 31. [Google Scholar] [CrossRef]
  33. Garrigue, C.; Clapham, P.J.; Geyer, Y.; Kennedy, A.S.; Zerbini, A.N. Satellite tracking reveals novel migratory patterns and the importance of seamounts for endangered South Pacific humpback whales. R. Soc. Open Sci. 2015, 2, 150489. [Google Scholar] [CrossRef] [Green Version]
  34. Weinstein, B.G.; Double, M.; Gales, N.; Johnston, D.W.; Friedlaender, A.S. Identifying overlap between humpback whale foraging grounds and the Antarctic krill fishery. Biol. Conserv. 2017, 210, 184–191. [Google Scholar] [CrossRef] [Green Version]
  35. Cerchio, S.; Trudelle, L.; Zerbini, A.N.; Charrassin, J.B.; Geyer, Y.; Mayer, F.X.; Andrianarivelo, N.; Jung, J.L.; Adam, O.; Rosenbaum, H.C. Satellite telemetry of humpback whales off Madagascar reveals insights on breeding behavior and long-range movements within the southwest Indian Ocean. Mar. Ecol. Prog. Ser. 2016, 562, 193–209. [Google Scholar] [CrossRef] [Green Version]
  36. Santora, J.A.; Mantua, N.J.; Schroeder, I.D.; Field, J.C.; Hazen, E.L.; Bograd, S.J.; Sydeman, W.J.; Wells, B.K.; Calambokidis, J.; Saez, L.; et al. Habitat compression and ecosystem shifts as potential links between marine heatwave and record whale entanglements. Nat. Commun. 2020, 11, 536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Chapman, D.M. Coastal erosion and the sediment budget, with special reference to the gold coast, Australia. Coast. Eng. 1980, 4, 207–227. [Google Scholar] [CrossRef]
  38. Meynecke, J.O.; Vindenes, S.; Teixeira, D. Monitoring humpback whale (Megaptera novaeangliae) behaviour in a highly urbanised coastline: Gold Coast, Australia. In Global Challenges in Integrated Coastal Zone Management; Moksness, E., Dahl, E., Støttrup, J., Eds.; Wiley: Chichester, UK, 2013; pp. 101–113. [Google Scholar]
  39. McCulloch, S.; Meynecke, J.O.; Franklin, T.; Franklin, W.; Chauvenet, A.L.M. Humpback whale (Megaptera novaeangliae) behaviour determines habitat use in two Australian bays. Mar. Freshw. Res. 2021, 72, 1251–1267. [Google Scholar] [CrossRef]
  40. Torre-Williams, L.; Martinez, E.; Meynecke, J.O.; Reinke, J.; Stockin, K.A. Presence of newborn humpback whale (Megaptera novaeangliae) calves in Gold Coast Bay, Australia. Mar. Freshw. Behav. Physiol. 2019, 52, 199–216. [Google Scholar] [CrossRef]
  41. Goldbogen, J.A.; Cade, D.E.; Boersma, A.T.; Calambokidis, J.; Kahane-Rapport, S.R.; Segre, P.S.; Stimpert, A.K.; Friedlaender, A.S. Using Digital Tags with Integrated Video and Inertial Sensors to Study Moving Morphology and Associated Function in Large Aquatic Vertebrates. Anat. Rec. 2017, 300, 1935–1941. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Goldbogen, J.A.; Friedlaender, A.S.; Calambokidis, J.; McKenna, M.F.; Simon, M.; Nowacek, D.P. Integrative Approaches to the Study of Baleen Whale Diving Behavior, Feeding Performance, and Foraging Ecology. BioScience 2013, 63, 90–100. [Google Scholar] [CrossRef] [Green Version]
  43. Savoca, M.; Czapanskiy, M.; Kahane-Rapport, S.; Gough, W.; Fahlbusch, J.; Bierlich, K.; Segre, P.; Di Clemente, J.; Penry, G.; Wiley, D.; et al. Baleen whale prey consumption based on high-resolution foraging measurements. Nature 2021, 599, 85–90. [Google Scholar] [CrossRef]
  44. Cade, D.E.; Gough, W.T.; Czapanskiy, M.F.; Fahlbusch, J.A.; Kahane-Rapport, S.R.; Linsky, J.M.J.; Nichols, R.C.; Oestreich, W.K.; Wisniewska, D.M.; Friedlaender, A.S.; et al. Tools for integrating inertial sensor data with video bio-loggers, including estimation of animal orientation, motion, and position. Anim. Biotele. 2021, 9, 34. [Google Scholar] [CrossRef]
  45. Wilson, R.P.; Liebsch, N.; Davies, I.M.; Quintana, F.; Weimerskirch, H.; Storch, S.; Lucke, K.; Siebert, U.; Zankl, S.; Müller, G.; et al. All at sea with animal tracks; methodological and analytical solutions for the resolution of movement. Deep Sea Res. Part II Top. Stud. Oceanogr. 2007, 54, 193–210. [Google Scholar] [CrossRef] [Green Version]
  46. Valani, R.; Meynecke, J.-O.; Olsen, M.T. Presence and movement of humpback whale (Megaptera novaeangliae) mother-calf pairs in the Gold Coast, Australia. Mar. Freshw. Behav. Physiol. 2020, 53, 251–263. [Google Scholar] [CrossRef]
  47. Félix, F.; Botero-Acosta, N. Distribution and behaviour of humpback whale mother–calf pairs during the breeding season off Ecuador. Mar. Ecol. Prog. Ser. 2011, 426, 277–287. [Google Scholar] [CrossRef] [Green Version]
  48. Condy, P.R.; Aarde, R.J.V.; Bester, M.N. The seasonal occurrence and behaviour of Killer whales Orcinus orca, at Marion Island. J. Zool. 1978, 184, 449–464. [Google Scholar] [CrossRef]
  49. Cartwright, R.; Sullivan, M. Behavioral ontogeny in humpback whale (Megaptera novaeangliae) calves during their residence in Hawaiian waters. Mar. Mammal Sci. 2009, 25, 659–680. [Google Scholar] [CrossRef]
  50. Zoidis, A.M.; Lomac-MacNair, K.S.; Chomos-Betz, A.E.; Day, A.J.; Sasha McFarland, A. Effects of sex, seasonal period, and sea state on calf behavior in Hawaiian humpback whales (Megaptera novaeangliae). Aquat. Mamm. 2014, 40, 44–58. [Google Scholar] [CrossRef]
  51. Deakos, M.H.; Branstetter, B.K.; Mazzuca, L.; Fertl, D.; Mobley, J.R., Jr. Two Unusual Interactions Between a Bottlenose Dolphin (Tursiops truncatus) and a Humpback Whale (Megaptera novaeangliae) in Hawaiian Waters. Aquat. Mamm. 2010, 36. [Google Scholar] [CrossRef] [Green Version]
  52. Fertl, D.; Fulling, G. Interactions between marine mammals and turtles. Mar. Turt. Newsl. 2007, 115, 4–8. [Google Scholar]
  53. Matsui, K.; Khalil, A.M.; Takeda, K.-i. Do horses prefer certain substrates for rolling in grazing pasture? J. Equine Vet. Sci. 2009, 29, 590–594. [Google Scholar] [CrossRef]
  54. Zoe, R.B.; John, K.E.M.; Wendy, C.T. Dust-bathing behaviours of African herbivores and the potential risk of inhalation of Anthrax. J. Wildl. Dis. 2018, 54, 34–44. [Google Scholar] [CrossRef] [Green Version]
  55. Pitman, R.L.; Durban, J.W.; Joyce, T.; Fearnbach, H.; Panigada, S.; Lauriano, G. Skin in the game: Epidermal molt as a driver of long-distance migration in whales. Mar. Mammal Sci. 2020, 36, 565–594. [Google Scholar] [CrossRef] [Green Version]
  56. Félix, F.; Haase, B.; Aguirre, W.E. Spondylitis in a humpback whale (Megaptera novaeangliae) from the southeast Pacific. Dis. Aquat. Org. 2007, 75, 259–264. [Google Scholar] [CrossRef] [Green Version]
  57. Rowntree, V.J. Feeding, distribution, and reproductive behavior of cyamids (Crustacea: Amphipoda) living on humpback and right whales. Can. J. Zool. 1996, 74, 103–109. [Google Scholar] [CrossRef]
  58. Apprill, A.; Mooney, T.A.; Lyman, E.; Stimpert, A.K.; Rappé, M.S. Humpback whales harbour a combination of specific and variable skin bacteria. Environ. Microbiol. Rep. 2011, 3, 223–232. [Google Scholar] [CrossRef]
  59. Félix, F.; Bearson, B.; Falconí, J. Epizoic barnacles removed from the skin of a humpback whale after a period of intense surface activity. Mar. Mammal Sci. 2006, 22, 979–984. [Google Scholar] [CrossRef]
  60. Gibson, R.; Barnes, M. Evolution and ecology of cleaning symbioses in the sea. Oceanography and Marine Biology: An Annual Review; CRC Press: Boca Raton, FL, USA, 2000; Volume 38, p. 311. [Google Scholar]
  61. Morlock, G.E.; Ziltener, A.; Geyer, S.; Tersteegen, J.; Mehl, A.; Schreiner, T.; Kamel, T.; Brümmer, F. Evidence that Indo-Pacific bottlenose dolphins self-medicate with invertebrates in coral reefs. iScience 2022, 25, 104271. [Google Scholar] [CrossRef] [PubMed]
  62. Pack, A.A.; Herman, L.M.; Spitz, S.S.; Hakala, S.; Deakos, M.H.; Herman, E.Y. Male humpback whales in the Hawaiian breeding grounds preferentially associate with larger females. Anim. Behav. 2009, 77, 653–662. [Google Scholar] [CrossRef]
  63. Herman, E.Y.; Herman, L.M.; Pack, A.A.; Marshall, G.; Shepard, C.M. When whales collide: Crittercam offers insight into the competitive behavior of humpback whales on their Hawaiian wintering grounds. Mar. Technol. Soc. J. 2007, 41, 35–43. [Google Scholar] [CrossRef]
  64. Iwata, T.; Biuw, M.; Aoki, K.; Miller, P.J.O.M.; Sato, K. Using an omnidirectional video logger to observe the underwater life of marine animals: Humpback whale resting behaviour. Behav. Process. 2021, 186, 104369. [Google Scholar] [CrossRef]
  65. Cartwright, R.; Gillespie, B.; LaBonte, K.; Mangold, T.; Venema, A.; Eden, K.; Sullivan, M. Between a rock and a hard place: Habitat selection in female-calf humpback whale (Megaptera novaeangliae) pairs on the Hawaiian breeding grounds. PLoS ONE 2012, 7, e38004. [Google Scholar] [CrossRef] [PubMed]
  66. Ona, J.; Duque, E.; Garland, E.C.; Seger, K.; Narvaez, M.; Maldonado, J.; Denkinger, J. A Giant’s Dance: Underwater Social and Vocal Behavior of Humpback Whales (Megaptera novaeangliae) Recorded on the Northern Coast of Ecuador. Aquat. Mamm. 2019, 45, 456–464. [Google Scholar] [CrossRef]
Jmse 11 00600 g001 550
Figure 1. Map of study area on the Gold Coast, Australia, and three tracks (tag a: 31 August 2021; tag b: 6 October 2021; tag c: 26 September 2022) with arrows indicating a predominantly southern direction of movement for all three deployments. The locations of sand rolling are shown by dots on top of the tracks. Bathymetry contour lines in 10 m depth intervals.
Figure 1. Map of study area on the Gold Coast, Australia, and three tracks (tag a: 31 August 2021; tag b: 6 October 2021; tag c: 26 September 2022) with arrows indicating a predominantly southern direction of movement for all three deployments. The locations of sand rolling are shown by dots on top of the tracks. Bathymetry contour lines in 10 m depth intervals.
Jmse 11 00600 g001
Jmse 11 00600 g002 550
Figure 2. Bottom contact behaviour documented with CATS camera. Screen shots showing an accompanying whale on its back during sand rolling (a1) and an accompanying whale moving its pectoral fin over the substrate from tag a (a2). Sand rolling performed by an accompanying whale during deployment of tag (b) and the tagged individual using its pectoral fin before rolling on its back from tag (c).
Figure 2. Bottom contact behaviour documented with CATS camera. Screen shots showing an accompanying whale on its back during sand rolling (a1) and an accompanying whale moving its pectoral fin over the substrate from tag a (a2). Sand rolling performed by an accompanying whale during deployment of tag (b) and the tagged individual using its pectoral fin before rolling on its back from tag (c).
Jmse 11 00600 g002
Jmse 11 00600 g003 550
Figure 3. Silver trevally (Pseudocaranx georgianus) observed near the whale when rolling in the sand for tag a and c. Screen shots from the video from tag a show the fish actively feeding off the whales’ skin and from tag c some of the fish were seen swimming close the whale.
Figure 3. Silver trevally (Pseudocaranx georgianus) observed near the whale when rolling in the sand for tag a and c. Screen shots from the video from tag a show the fish actively feeding off the whales’ skin and from tag c some of the fish were seen swimming close the whale.
Jmse 11 00600 g003
Jmse 11 00600 g004a 550Jmse 11 00600 g004b 550
Figure 4. A series of depth profiles between surface intervals for three different tagged humpback whales (tag a, b and c) performing sand rolling and their corresponding pseudo-track with pitch. The 14 sand rolls are indicated with a dot along the depth profile.
Figure 4. A series of depth profiles between surface intervals for three different tagged humpback whales (tag a, b and c) performing sand rolling and their corresponding pseudo-track with pitch. The 14 sand rolls are indicated with a dot along the depth profile.
Jmse 11 00600 g004aJmse 11 00600 g004b
Table
Table 1. Overview of three tag deployments for which sand rolling was identified. All tags were deployed near the dorsal fin facing forward. The estimate distance and average speed based on start and end of deployment shown in brackets.
Table 1. Overview of three tag deployments for which sand rolling was identified. All tags were deployed near the dorsal fin facing forward. The estimate distance and average speed based on start and end of deployment shown in brackets.
Tag IDDate TaggedTag OnTAG OFFTag on in HrsAver. Speed km/hDistance in kmNumber of Sand Rolls
a31 August 2111:3318:016:282.9 (1.8)18.8 (11.8)8
b6 October 219:4713:003:135.4 (4.6)16.9 (14.7)1
c26 September 2210:1913:594:174.7 (3.8)19.6 (16.1)5
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Meynecke, J.-O.; Gustafon, J.; Cade, D.E. Exfoliating Whales–Sandy Bottom Contact Behaviour of Humpback Whales. J. Mar. Sci. Eng. 2023, 11, 600. https://doi.org/10.3390/jmse11030600

AMA Style

Meynecke J-O, Gustafon J, Cade DE. Exfoliating Whales–Sandy Bottom Contact Behaviour of Humpback Whales. Journal of Marine Science and Engineering. 2023; 11(3):600. https://doi.org/10.3390/jmse11030600

Chicago/Turabian Style

Meynecke, Jan-Olaf, Johan Gustafon, and David E. Cade. 2023. "Exfoliating Whales–Sandy Bottom Contact Behaviour of Humpback Whales" Journal of Marine Science and Engineering 11, no. 3: 600. https://doi.org/10.3390/jmse11030600

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop