Ontogenetic changes in energy expenditure and resting behaviour of humpback whale mother–calf pairs examined using unmanned aerial vehicles
Ditte D. Ejrnæs
A and Kate R. Sprogis A B C
+ Author Affiliations
- Author Affiliations
A Zoophysiology, Department of Biology, Aarhus University, C. F. Møllers Allé 3, Aarhus C 8000, Denmark.
B Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 90 South Street, Perth, WA 6150, Australia.
C Corresponding author. Email: kate.sprogis@bio.au.dk
Wildlife Research 49(1) 34-45 https://doi.org/10.1071/WR20186
Submitted: 31 October 2020 Accepted: 19 March 2021 Published: 17 June 2021
Abstract
Context: Baleen whale calves rapidly increase in size and improve locomotion abilities, while on their low-latitude breeding ground, allowing them to undertake a successful migration to high-latitude feeding grounds.
Aims: We investigated energy expenditure and resting behaviour of humpback whale (Megaptera novaeangliae) mother–calf pairs in regard to changes in calf length on an undisturbed breeding/resting ground off Exmouth Gulf, Western Australia.
Methods: Data were collected from August to October in 2018 and 2019 on lactating mothers that were predominantly resting on the surface with their calf. Focal follows on mother–calf pairs (n = 101) were conducted using an unmanned aerial vehicle to obtain detailed video of behaviours and respirations (23.7 h). Body length measurements of individual whales were calculated from aerial still frames.
Key results: Results on calves ranging in length from ~4–8 m demonstrated that calf respiration rate decreased with an increase in calf length and increased with presence of activity (P < 0.001). Calf inter-breath intervals became longer in duration with an increase in calf length (P < 0.01). Calf activity level and resting behaviour remained constant, with calves logging for 53% of the time their mothers were logging. Maternal respiration rate remained low and did not differ with respect to maternal or calf length.
Conclusions: Results highlighted the importance of resting grounds for energy preservation, which benefits the calves’ rapid growth before migration to polar waters.
Implications: Findings from the present largely undisturbed population serve as a baseline for understanding the impacts of anthropogenic disturbance on resting behaviour and energy expenditure in humpback whale mother–calf pairs globally.
Keywords: respiration, stress, migration, locomotion, growth, energetics, development, anthropogenic impacts.
References
Alava, J. J., Jiménez, P. J., Fair, P. A., and Barrett-Lennard, L. (2019). First record of a live-stranded killer whale (Orcinus orca) in coastal Ecuador and insights on killer whale occurrence in Ecuadorian waters. Aquatic Mammals 45, 106–115.| First record of a live-stranded killer whale (Orcinus orca) in coastal Ecuador and insights on killer whale occurrence in Ecuadorian waters.Crossref | GoogleScholarGoogle Scholar |
Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour 49, 227–267.
| Observational study of behavior: sampling methods.Crossref | GoogleScholarGoogle Scholar | 4597405PubMed |
Andrews-Goff, V., Bestley, S., Gales, N. J., Laverick, S. M., Paton, D., Polanowski, A. M., Schmitt, N. T., and Double, M. C. (2018). Humpback whale migrations to Antarctic summer foraging grounds through the southwest Pacific Ocean. Scientific Reports 8, 12333.
| Humpback whale migrations to Antarctic summer foraging grounds through the southwest Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 30120303PubMed |
Barber, N. (1991). Play and energy regulation in mammals. The Quarterly Review of Biology 66, 129–147.
| Play and energy regulation in mammals.Crossref | GoogleScholarGoogle Scholar | 1891590PubMed |
Bejder, M., Johnston, D. W., Smith, J., Friedlaender, A., and Bejder, L. (2016). Embracing conservation success of recovering humpback whale populations: evaluating the case for downlisting their conservation status in Australia. Marine Policy 66, 137–141.
| Embracing conservation success of recovering humpback whale populations: evaluating the case for downlisting their conservation status in Australia.Crossref | GoogleScholarGoogle Scholar |
Bejder, L., Videsen, S. K. A., Hermannsen, L., Simon, M., Hanf, D., and Madsen, P. T. (2019). Low energy expenditure and resting behaviour of humpback whale mother–calf pairs highlights conservation importance of sheltered breeding areas. Scientific Reports 9, .
| Low energy expenditure and resting behaviour of humpback whale mother–calf pairs highlights conservation importance of sheltered breeding areas.Crossref | GoogleScholarGoogle Scholar | 31439909PubMed |
Bestley, S., Andrews-Goff, V., van Wijk, E., Rintoul, S. R., Double, M. C., and How, J. (2019). New insights into prime Southern Ocean forage grounds for thriving Western Australian humpback whales. Scientific Reports 9, .
| New insights into prime Southern Ocean forage grounds for thriving Western Australian humpback whales.Crossref | GoogleScholarGoogle Scholar | 31831763PubMed |
Burnham, K. P., and Anderson, D. R. (2002). ‘Model selection and multimodel inference: a practical information-theoretic approach.’ 2nd edn. (Springer.)
Cartwright, R., and Sullivan, M. (2009a). Associations with multiple male groups increase the energy expenditure of humpback whale (Megaptera novaeangliae) female and calf pairs on the breeding grounds. Behaviour 146, 1573–1600.
| Associations with multiple male groups increase the energy expenditure of humpback whale (Megaptera novaeangliae) female and calf pairs on the breeding grounds.Crossref | GoogleScholarGoogle Scholar |
Cartwright, R., and Sullivan, M. (2009b). Behavioral ontogeny in humpback whale (Megaptera novaeangliae) calves during their residence in Hawaiian waters. Marine Mammal Science 25, 659–680.
| Behavioral ontogeny in humpback whale (Megaptera novaeangliae) calves during their residence in Hawaiian waters.Crossref | GoogleScholarGoogle Scholar |
Cartwright, R., Newton, C., West, K. M., Rice, J., Niemeyer, M., Burek, K., Wilson, A., Wall, A. N., Remonida-Bennett, J., Tejeda, A., Messi, S., and Marcial-Hernandez, L. (2016). Tracking the development of muscular myoglobin stores in mysticete calves. PLoS One 11, e0145893.
| Tracking the development of muscular myoglobin stores in mysticete calves.Crossref | GoogleScholarGoogle Scholar | 26788728PubMed |
Cartwright, R., Venema, A., Hernandez, V., Wyels, C., Cesere, J., and Cesere, D. (2019). Fluctuating reproductive rates in Hawaii’s humpback whales, Megaptera novaeangliae, reflect recent climate anomalies in the North Pacific. Royal Society Open Science 6, .
| Fluctuating reproductive rates in Hawaii’s humpback whales, Megaptera novaeangliae, reflect recent climate anomalies in the North Pacific.Crossref | GoogleScholarGoogle Scholar | 31032006PubMed |
Cerchio, S., Strindberg, S., Collins, T., Bennett, C., and Rosenbaum, H. (2014). Seismic surveys negatively affect humpback whale singing activity off Northern Angola. PLoS One 9, .
| Seismic surveys negatively affect humpback whale singing activity off Northern Angola.Crossref | GoogleScholarGoogle Scholar | 24618836PubMed |
Chittleborough, R. G. (1965). Dynamics of two populations of the humpback whale, Megaptera novaeangliae (Borowski). Australian Journal of Marine and Freshwater Research 16, 33–128.
| Dynamics of two populations of the humpback whale, Megaptera novaeangliae (Borowski).Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Rasmussen, M., and Lusseau, D. (2013). Whale watching disrupts feeding activities of minke whales on a feeding ground. Marine Ecology Progress Series 478, 239–251.
| Whale watching disrupts feeding activities of minke whales on a feeding ground.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Rasmussen, M., and Lusseau, D. (2014). Inferring energy expenditure from respiration rates in minke whales to measure the effects of whale watching boat interactions. Journal of Experimental Marine Biology and Ecology 459, 96–104.
| Inferring energy expenditure from respiration rates in minke whales to measure the effects of whale watching boat interactions.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Dujon, A. M., Sprogis, K. R., Arnould, J. P. Y., and Bejder, L. (2016a). Noninvasive unmanned aerial vehicle provides estimates of the energetic cost of reproduction in humpback whales. Ecosphere 7, .
| Noninvasive unmanned aerial vehicle provides estimates of the energetic cost of reproduction in humpback whales.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Rojano-Doñate, L., Madsen, P. T., and Bejder, L. (2016b). Noise levels of multi-rotor unmanned aerial vehicles with implications for potential underwater impacts on marine mammals. Frontiers in Marine Science 3, 1–9.
| Noise levels of multi-rotor unmanned aerial vehicles with implications for potential underwater impacts on marine mammals.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Vivier, F., Charlton, C., Ward, R., Amerson, A., Burneli, S., and Bejder, L. (2018). Maternal body size and condition determine calf growth rates in southern right whales. Marine Ecology Progress Series 592, 267–281.
| Maternal body size and condition determine calf growth rates in southern right whales.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Nielsen, M. L. K., Charlton, C., Bejder, L., and Madsen, P. T. (2020a). Southern right whales show no behavioral response to low noise levels from a nearby unmanned aerial vehicle. Marine Mammal Science 36, 953–963.
| Southern right whales show no behavioral response to low noise levels from a nearby unmanned aerial vehicle.Crossref | GoogleScholarGoogle Scholar |
Christiansen, F., Sprogis, K. R., Gross, J., Castrillon, J., Warick, H. A., Leunissen, E., and Nash, S. B. (2020b). Variation in outer blubber lipid concentration does not reflect morphological body condition in humpback whales. The Journal of Experimental Biology 223, .
| Variation in outer blubber lipid concentration does not reflect morphological body condition in humpback whales.Crossref | GoogleScholarGoogle Scholar | 32661113PubMed |
Derville, S., Torres, L. G., Albertson, R., Andrews, O., Baker, C. S., Carzon, P., Constantine, R., Donoghue, M., Dutheil, C., Gannier, A., Oremus, M., Poole, M. M., Robbins, J., and Garrigue, C. (2019). Whales in warming water: assessing breeding habitat diversity and adaptability in Oceania’s changing climate. Global Change Biology 25, 1466–1481.
| Whales in warming water: assessing breeding habitat diversity and adaptability in Oceania’s changing climate.Crossref | GoogleScholarGoogle Scholar |
Dolphin, W. F. (1987). Dive behavior and estimated energy expenditure of foraging humpback whales in southeast Alaska. Canadian Journal of Zoology 65, 354–362.
| Dive behavior and estimated energy expenditure of foraging humpback whales in southeast Alaska.Crossref | GoogleScholarGoogle Scholar |
Eisenmann, P., Fry, B., Holyoake, C., Coughran, D., Nicol, S., and Bengtson Nash, S. (2016). Isotopic evidence of a wide spectrum of feeding strategies in southern hemisphere humpback whale baleen records. PLoS One 11, e0156698.
| Isotopic evidence of a wide spectrum of feeding strategies in southern hemisphere humpback whale baleen records.Crossref | GoogleScholarGoogle Scholar | 27244081PubMed |
Félix, F. (2004). Assessment of the level of surface activity in humpback whales during the breeding season. The Latin American Journal of Aquatic Mammals 3, 25–36.
| Assessment of the level of surface activity in humpback whales during the breeding season.Crossref | GoogleScholarGoogle Scholar |
Félix, F., Muñoz, M., Falconí, J., Botero, N., and Haase, B. H. (2011). Entanglement of humpback whales in artisanal fishing gear in Ecuador. The Journal of Cetacean Research and Management 3, 285–290.
| Entanglement of humpback whales in artisanal fishing gear in Ecuador.Crossref | GoogleScholarGoogle Scholar |
Fiori, L., Martinez, E., Bader, M. K. F., Orams, M. B., and Bollard, B. (2020). Insights into the use of an unmanned aerial vehicle (UAV) to investigate the behavior of humpback whales (Megaptera novaeangliae) in Vava’u, Kingdom of Tonga. Marine Mammal Science 36, 209–223.
| Insights into the use of an unmanned aerial vehicle (UAV) to investigate the behavior of humpback whales (Megaptera novaeangliae) in Vava’u, Kingdom of Tonga.Crossref | GoogleScholarGoogle Scholar |
Goldbogen, J. A., Calambokidis, J., Croll, D. A., Harvey, J. T., Newton, K. M., Oleson, E. M., Schorr, G., and Shadwick, R. E. (2008). Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. The Journal of Experimental Biology 211, 3712–3719.
| Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge.Crossref | GoogleScholarGoogle Scholar | 19011211PubMed |
Harkness, P., and Sprogis, K. R. (2021). Silver gull harassment of humpback whales in Exmouth Gulf, Western Australia. Marine and Freshwater Research 72, 584–592.
| Silver gull harassment of humpback whales in Exmouth Gulf, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Irvine, L., and Salgado-Kent, C. (2019). The distribution and relative abundance of marine mega-fauna, with a focus on humpback whales (Megaptera novaeangliae), in Exmouth Gulf, Western Australia, 2018. Attachment 2J Humpback Whale Aerial Survey Report. Subsea 7, Exmouth, WA, Australia.
Irvine, L. G., Thums, M., Hanson, C. E., McMahon, C. R., and Hindell, M. A. (2017). Quantifying the energy stores of capital breeding humpback whales and income breeding sperm whales using historical whaling records. Royal Society Open Science 4, .
| Quantifying the energy stores of capital breeding humpback whales and income breeding sperm whales using historical whaling records.Crossref | GoogleScholarGoogle Scholar | 28405350PubMed |
Irvine, L. G., Thums, M., Hanson, C. E., McMahon, C. R., and Hindell, M. A. (2018). Evidence for a widely expanded humpback whale calving range along the Western Australian coast. Marine Mammal Science 34, 294–310.
| Evidence for a widely expanded humpback whale calving range along the Western Australian coast.Crossref | GoogleScholarGoogle Scholar |
Jenner, K. C. S., and Jenner, M. N. (2005). Distribution and abundance of humpback whales and other mega-fauna in Exmouth Gulf, Western Australia, during 2004/2005. Prepared for Straits Salt Pty Ltd.
Jenner, K. C. S., Jenner, M. N., and McCabe, K. A. (2001). Geographical and temporal movements of humpback whales in Western Australian waters. The APPEA Journal 41, 749–765.
| Geographical and temporal movements of humpback whales in Western Australian waters.Crossref | GoogleScholarGoogle Scholar |
Kleiber, M. (1932). Body size and metabolism. Hilgardia Journal of Agricultural Science 6, 315–353.
Kriete, B. (1995). Bioenergetics in the killer whale, Orcinus orca. PhD Thesis, University of British Colombia, Canada.
Lockyer, C. (2007). All creatures great and smaller: a study in cetacean life history energetics. Journal of the Marine Biological Association of the United Kingdom 87, 1035–1045.
| All creatures great and smaller: a study in cetacean life history energetics.Crossref | GoogleScholarGoogle Scholar |
Lomac-MacNair, K., Zoidis, A. M., Anderson, M., and Blees, M. (2018). Humpback whale calf vulnerability to small-vessel collisions; assessment from underwater videography in Hawaiian waters. Journal of Coastal Sciences 5, 28–36.
Mann, J., and Smuts, B. (1999). Behavioral development in wild bottlenose dolphin newborns (Tursiops sp.). Behaviour 136, 529–566.
| Behavioral development in wild bottlenose dolphin newborns (Tursiops sp.).Crossref | GoogleScholarGoogle Scholar |
Moon, K. (2018). ggiraphExtra: make interactive ‘ggplot2’. Extension to ‘ggplot2’ and ‘ggiraph’. Available at https://cran.r-project.org/package=ggiraphExtra
Naessig, P. J., and Lanyon, J. M. (2004). Levels and probable origin of predatory scarring on humpback whales (Megaptera novaeangliae) in east Australian waters. Wildlife Research 31, 163–170.
| Levels and probable origin of predatory scarring on humpback whales (Megaptera novaeangliae) in east Australian waters.Crossref | GoogleScholarGoogle Scholar |
Narazaki, T., Isojunno, S., Nowacek, D. P., Swift, R., Friedlaender, A. S., Ramp, C., Smout, S., Aoki, K., Deecke, V. B., Sato, K., and Miller, P. J. O. (2018). Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance. PLoS One 13, e0200287.
| Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance.Crossref | GoogleScholarGoogle Scholar | 30001369PubMed |
Nielsen, M. L. K., Sprogis, K. R., Bejder, L., Madsen, P. T., and Christiansen, F. (2019). Behavioural development in southern right whale calves. Marine Ecology Progress Series 629, 219–234.
| Behavioural development in southern right whale calves.Crossref | GoogleScholarGoogle Scholar |
Pack, A. A., Herman, L. M., Spitz, S. S., Hakala, S., Deakos, M. H., and Herman, E. Y. K. (2009). Male humpback whales in the Hawaiian breeding grounds preferentially associate with larger females. Animal Behaviour 77, 653–662.
| Male humpback whales in the Hawaiian breeding grounds preferentially associate with larger females.Crossref | GoogleScholarGoogle Scholar |
Pitman, R. L., Totterdell, J. A., Fearnbach, H., Ballance, L. T., Durban, J. W., and Kemps, H. (2015). Whale killers: prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia. Marine Mammal Science 31, 629–657.
| Whale killers: prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2018). R: a language and environment for statistical computing. Available at http://www.r-project.org/
Rasmussen, K., Palacios, D. M., Calambokidis, J., Saborío, M. T., Dalla Rosa, L., Secchi, E. R., Steiger, G. H., Allen, J. M., and Stone, G. S. (2007). Southern hemisphere humpback whales wintering off Central America: Insights from water temperature into the longest mammalian migration. Biology Letters 3, 302–305.
| Southern hemisphere humpback whales wintering off Central America: Insights from water temperature into the longest mammalian migration.Crossref | GoogleScholarGoogle Scholar | 17412669PubMed |
Rojano-Doñate, L., McDonald, B. I., Wisniewska, D. M., Johnson, M., Teilmann, J., Wahlberg, M., Højer-Kristensen, J., and Madsen, P. T. (2018). High field metabolic rates of wild harbour porpoises. The Journal of Experimental Biology 221, .
| High field metabolic rates of wild harbour porpoises.Crossref | GoogleScholarGoogle Scholar | 30523043PubMed |
Roos, M. M. H., Wu, G. M., and Miller, P. J. O. (2016). The significance of respiration timing in the energetics estimates of free-ranging killer whales (Orcinus orca). The Journal of Experimental Biology 219, 2066–2077.
| The significance of respiration timing in the energetics estimates of free-ranging killer whales (Orcinus orca).Crossref | GoogleScholarGoogle Scholar |
Salgado-Kent, C., Jenner, K. C. S., Jenner, M. N., Bouchet, P., and Rexstad, E. (2012). Southern hemisphere Breeding Stock D humpback whale population estimates from North West Cape, Western Australia. The Journal of Cetacean Research and Management 12, 29–38.
Smith, J. N., Kelly, N., Childerhouse, S., Redfern, J. V., Moore, T. J., and Peel, D. (2020). Quantifying ship strike risk to breeding whales in a multiple-use marine park: the Great Barrier Reef. Frontiers in Marine Science 7, 67.
| Quantifying ship strike risk to breeding whales in a multiple-use marine park: the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Smultea, M., Fertl, D., Bacon, C., Moore, M., James, V., and Wursig, B. (2017). Cetacean mother-calf behavior observed from a small aircraft off southern California. Animal Behavior and Cognition 4, 1–23.
| Cetacean mother-calf behavior observed from a small aircraft off southern California.Crossref | GoogleScholarGoogle Scholar |
Špinka, M., Newberry, R. C., and Bekoff, M. (2001). Mammalian play: training for the unexpected. The Quarterly Review of Biology 76, 141–168.
| Mammalian play: training for the unexpected.Crossref | GoogleScholarGoogle Scholar | 11409050PubMed |
Sprogis, K. R., Bejder, L., Hanf, D., and Christiansen, F. (2020a). Behavioural responses of migrating humpback whales to swim-with-whale activities in the Ningaloo Marine Park, Western Australia. Journal of Experimental Marine Biology and Ecology 522, .
| Behavioural responses of migrating humpback whales to swim-with-whale activities in the Ningaloo Marine Park, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Sprogis, K. R., Videsen, S. K. A., and Madsen, P. T. (2020b). Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching. eLife 9, .
| Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching.Crossref | GoogleScholarGoogle Scholar | 32539930PubMed |
Stevick, P. T., Neves, M. C., Johansen, F., Engel, M. H., Judith, A., Marcondes, M. C. C., and Carlson, C. (2011). A quarter of a world away: female humpback whale moves 10000 km between breeding areas. Biology Letters 7, 299–302.
| A quarter of a world away: female humpback whale moves 10000 km between breeding areas.Crossref | GoogleScholarGoogle Scholar | 20943678PubMed |
Szabo, A., and Duffus, D. (2008). Mother–offspring association in the humpback whale, Megaptera novaeangliae: following behaviour in an aquatic mammal. Animal Behaviour 75, 1085–1092.
| Mother–offspring association in the humpback whale, Megaptera novaeangliae: following behaviour in an aquatic mammal.Crossref | GoogleScholarGoogle Scholar |
Tackaberry, J. E., Cade, D. E., Goldbogen, J. A., Wiley, D. N., Friedlaender, A. S., and Stimpert, A. K. (2020). From a calf’s perspective: humpback whale nursing behavior on two US feeding grounds. PeerJ 8, .
| From a calf’s perspective: humpback whale nursing behavior on two US feeding grounds.Crossref | GoogleScholarGoogle Scholar | 32181052PubMed |
Thomas, P. O., and Taber, S. M. (1984). Mother-infant interaction and behavioral development in southern right whales, Eubalaena australis. Behaviour 88, 42–60.
| Mother-infant interaction and behavioral development in southern right whales, Eubalaena australis.Crossref | GoogleScholarGoogle Scholar |
Thomas, P. O., Reeves, R. R., and Brownell, R. L. (2016). Status of the world’s baleen whales. Marine Mammal Science 32, 682–734.
| Status of the world’s baleen whales.Crossref | GoogleScholarGoogle Scholar |
Videsen, S. K. A., Bejder, L., Johnson, M., and Madsen, P. T. (2017). High suckling rates and acoustic crypsis of humpback whale neonates maximise potential for mother–calf energy transfer. Functional Ecology 31, 1561–1573.
| High suckling rates and acoustic crypsis of humpback whale neonates maximise potential for mother–calf energy transfer.Crossref | GoogleScholarGoogle Scholar |
Villagra, D., García-Cegarra, A., Gallardo, D. I., and Pacheco, A. S. (2021). Energetic effects of whale-watching boats on humpback whales on a breeding ground. 7, .
| Energetic effects of whale-watching boats on humpback whales on a breeding ground.Crossref | GoogleScholarGoogle Scholar |
Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L. D., Francois, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T. L., Miller, E., and Bache, S. M. (2019). Welcome to the tidyverse. Journal of Open Source Software 4, 1686.
| Welcome to the tidyverse.Crossref | GoogleScholarGoogle Scholar |
Williams, R., and Noren, D. P. (2009). Swimming speed, respiration rate, and estimated cost of transport in adult killer whales. Marine Mammal Science 25, 327–350.
| Swimming speed, respiration rate, and estimated cost of transport in adult killer whales.Crossref | GoogleScholarGoogle Scholar |
Yazdi, P., Kilian, A., and Culik, B. M. (1999). Energy expenditure of swimming bottlenose dolphins (Tursiops truncatus). Marine Biology 134, 601–607.
| Energy expenditure of swimming bottlenose dolphins (Tursiops truncatus).Crossref | GoogleScholarGoogle Scholar |
Zoidis, A. M., and Lomac-MacNair, K. S. (2017). A note on suckling behavior and laterality in nursing humpback whale calves from underwater observations. Animals (Basel) 7, 51.
| A note on suckling behavior and laterality in nursing humpback whale calves from underwater observations.Crossref | GoogleScholarGoogle Scholar |
Zoidis, A. M., Lomac-MacNair, K. S., Chomos-Betz, A. E., Day, A. J., and McFarland, A. S. (2014). Effects of sex, seasonal period, and sea state on calf behavior in Hawaiian humpback whales (Megaptera novaeangliae). Aquatic Mammals 40, 44–58.
| Effects of sex, seasonal period, and sea state on calf behavior in Hawaiian humpback whales (Megaptera novaeangliae).Crossref | GoogleScholarGoogle Scholar |
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M. (2009). ‘Mixed effects models and extensions in ecology with R.’ (Springer: New York, NY, USA.)
Zuur, A. F., Ieno, E. N., and Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.
| A protocol for data exploration to avoid common statistical problems.Crossref | GoogleScholarGoogle Scholar |
