Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Intraspecific variation in diel patterns of rocky reef use suggests temporal partitioning in Port Jackson sharks

Nathan Charles Bass https://orcid.org/0000-0002-5815-1392 A E , Joanna Day A B , Tristan L. Guttridge C , Nathan A. Knott D and Culum Brown A
+ Author Affiliations
- Author Affiliations

A Macquarie University, Department of Biological Sciences, North Ryde, NSW 2109, Australia.

B Taronga Institute of Science and Learning, Taronga Conservation Society Australia, Mosman, NSW 2088, Australia.

C Saving the Blue, Cooper City, FL 33328, USA.

D NSW Department of Primary Industries, Fisheries Research, 4 Woollamia Road, Huskisson, NSW 2540, Australia.

E Corresponding author. Email: nathancbass@mail.com

Marine and Freshwater Research - https://doi.org/10.1071/MF20204
Submitted: 29 June 2020  Accepted: 26 March 2021   Published online: 13 May 2021

Journal Compilation © CSIRO 2021 Open Access CC BY-NC

Abstract

Limited information exists about the temporal residency patterns of marine predators, especially at the individual level. Temporal partitioning of resources can reduce intra-specific competition, but this has seldom been examined in predators in marine ecosystems. Here, we used 8 years of acoustic telemetry data from 27 receivers deployed in a large coastal embayment to examine the temporal residency of 51 Port Jackson sharks (Heterodontus portusjacksoni), during their breeding season. We found that the residency lengths of male and female Port Jackson sharks on breeding reefs differed throughout the breeding season, with males showing longer residency at the start of the season and females showing longer residency at the end of the season. Port Jackson sharks also showed a 24-h or diel periodicity in their detection patterns. Although the majority of individuals were nocturnal, a small proportion of sharks was detected more frequently during the day, possibly to reduce competition for resources. Surprisingly, there was no difference in the sex ratio nor the size of diurnal and nocturnal individuals. This study provides long-term insight into the temporal residency patterns of mesopredatory sharks at a breeding site and, more broadly, our results highlight the importance of studying temporal variation at the individual level in movement ecology studies.

Keywords: elasmobranchs, marine, ecology.


References

Alanärä, A., Burns, M. D., and Metcalfe, N. B. (2001). Intraspecific resource partitioning in brown trout: the temporal distribution of foraging is determined by social rank. Journal of Animal Ecology 70, 980–986.
Intraspecific resource partitioning in brown trout: the temporal distribution of foraging is determined by social rank.Crossref | GoogleScholarGoogle Scholar |

Austin, D., Bowen, W. D., and McMillan, J. I. (2004). Intraspecific variation in movement patterns: modeling individual behaviour in a large marine predator. Oikos 105, 15–30.
Intraspecific variation in movement patterns: modeling individual behaviour in a large marine predator.Crossref | GoogleScholarGoogle Scholar |

Barnett, A., Abrantes, K. G., Seymour, J., and Fitzpatrick, R. (2012). Residency and spatial use by reef sharks of an isolated seamount and its implications for conservation. PLoS One 7, e36574.
Residency and spatial use by reef sharks of an isolated seamount and its implications for conservation.Crossref | GoogleScholarGoogle Scholar | 23284819PubMed |

Bass, N. C. (2012). Social networking and site fidelity in Port Jackson sharks (Heterodontus portusjacksoni). B.Mar.Sc.(Hons) Thesis, Macquarie University, Sydney, NSW, Australia.

Bass, N. C., Mourier, J., Knott, N. A., Day, J., Guttridge, T., and Brown, C. (2017). Long-term migration patterns and bisexual philopatry in a benthic shark species. Marine and Freshwater Research 68, 1414–1421.
Long-term migration patterns and bisexual philopatry in a benthic shark species.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Mächler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bergmüller, R., and Taborsky, M. (2010). Animal personality due to social niche specialisation. Trends in Ecology & Evolution 25, 504–511.
Animal personality due to social niche specialisation.Crossref | GoogleScholarGoogle Scholar |

Bessudo, S., Soler, G. A., Klimley, A. P., Ketchum, J. T., Hearn, A., and Arauz, R. (2011). Residency of the scalloped hammerhead shark (Sphyrna lewini) at Malpelo Island and evidence of migration to other islands in the Eastern Tropical Pacific. Environmental Biology of Fishes 91, 165–176.
Residency of the scalloped hammerhead shark (Sphyrna lewini) at Malpelo Island and evidence of migration to other islands in the Eastern Tropical Pacific.Crossref | GoogleScholarGoogle Scholar |

Brown, C., and Irving, E. (2014). Individual personality traits influence group exploration in a feral guppy population. Behavioral Ecology 25, 95–101.
Individual personality traits influence group exploration in a feral guppy population.Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., Anderson, D. R., and Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.
AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons.Crossref | GoogleScholarGoogle Scholar |

Byrnes, E. E., and Brown, C. (2016). Individual personality differences in Port Jackson sharks Heterodontus portusjacksoni. Journal of Fish Biology 89, 1142–1157.
Individual personality differences in Port Jackson sharks Heterodontus portusjacksoni.Crossref | GoogleScholarGoogle Scholar | 27228221PubMed |

Campbell, H. A., Watts, M. E., Dwyer, R. G., and Franklin, C. E. (2012). V-Track: software for analysing and visualising animal movement from acoustic telemetry detections. Marine and Freshwater Research 63, 815–820.
V-Track: software for analysing and visualising animal movement from acoustic telemetry detections.Crossref | GoogleScholarGoogle Scholar |

Carlson, J. K., Heupel, M. R., Bethea, D. M., and Hollensead, L. D. (2008). Coastal habitat use and residency of juvenile Atlantic sharpnose sharks (Rhizoprionodon terraenovae). Estuaries and Coasts 31, 931–940.
Coastal habitat use and residency of juvenile Atlantic sharpnose sharks (Rhizoprionodon terraenovae).Crossref | GoogleScholarGoogle Scholar |

Castro, J. I. (2000). The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands. Environmental Biology of Fishes 58, 1–22.
The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and the Bahama Islands.Crossref | GoogleScholarGoogle Scholar |

Chapman, D. D., Feldheim, K. A., Papastamatiou, Y. P., and Hueter, R. E. (2015). There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annual Review of Marine Science 7, 547–570.
There and back again: a review of residency and return migrations in sharks, with implications for population structure and management.Crossref | GoogleScholarGoogle Scholar | 25251267PubMed |

Chesson, P. (2000). Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31, 343–366.
Mechanisms of maintenance of species diversity.Crossref | GoogleScholarGoogle Scholar |

Clarke, C., Lea, J. S. E., and Ormond, R. F. G. (2011). Reef-use and residency patterns of a baited population of silky sharks, Carcharhinus falciformis, in the Red Sea. Marine and Freshwater Research 62, 668–675.
Reef-use and residency patterns of a baited population of silky sharks, Carcharhinus falciformis, in the Red Sea.Crossref | GoogleScholarGoogle Scholar |

Collatos, C., Abel, D. C., and Martin, K. L. (2020). Seasonal occurrence, relative abundance, and migratory movements of juvenile sandbar sharks, Carcharhinus plumbeus, in Winyah Bay, South Carolina. Environmental Biology of Fishes 103, 859–873.
Seasonal occurrence, relative abundance, and migratory movements of juvenile sandbar sharks, Carcharhinus plumbeus, in Winyah Bay, South Carolina.Crossref | GoogleScholarGoogle Scholar |

Conrath, C. L., and Musick, J. A. (2010). Residency, space use and movement patterns of juvenile sandbar sharks (Carcharhinus plumbeus) within a Virginia summer nursery area. Marine and Freshwater Research 61, 223–235.
Residency, space use and movement patterns of juvenile sandbar sharks (Carcharhinus plumbeus) within a Virginia summer nursery area.Crossref | GoogleScholarGoogle Scholar |

Cote, J., Clobert, J., Brodin, T., Fogarty, S., and Sih, A. (2010). Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 365, 4065–4076.
Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations.Crossref | GoogleScholarGoogle Scholar | 21078658PubMed |

Day, J., Clark, J. A., Williamson, J. E., Brown, C., and Gillings, M. (2019). Population genetic analyses reveal female reproductive philopatry in the oviparous Port Jackson shark. Marine and Freshwater Research 70, 986–994.
Population genetic analyses reveal female reproductive philopatry in the oviparous Port Jackson shark.Crossref | GoogleScholarGoogle Scholar |

de Souza, D. C., Vieira, L. D., and da Silva Castro, A. L. (2018). Territoriality and home range of red legged seriema (Cariama cristata). Ornitologia Neotropical 29, 101–105.

Dhellemmes, F., Finger, J. S., Laskowski, K. L., Guttridge, T. L., and Krause, J. (2020). Comparing behavioural syndromes across time and ecological conditions in a free-ranging predator. Animal Behaviour 162, 23–33.
Comparing behavioural syndromes across time and ecological conditions in a free-ranging predator.Crossref | GoogleScholarGoogle Scholar |

Economakis, A. E., and Lobel, P. S. (1998). Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environmental Biology of Fishes 51, 129–139.
Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Ferguson, A. M., Harvey, E. S., Taylor, M. D., and Knott, N. A. (2013). A herbivore knows its patch: luderick, Girella tricuspidata, exhibit strong site fidelity on shallow subtidal reefs in a temperate marine park. PLoS One 8, e65838.
A herbivore knows its patch: luderick, Girella tricuspidata, exhibit strong site fidelity on shallow subtidal reefs in a temperate marine park.Crossref | GoogleScholarGoogle Scholar | 23741515PubMed |

Field, I. C., Meekan, M. G., Speed, C. W., White, W., and Bradshaw, C. J. A. (2011). Quantifying movement patterns for shark conservation at remote coral atolls in the Indian Ocean. Coral Reefs 30, 61–71.
Quantifying movement patterns for shark conservation at remote coral atolls in the Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Finger, J. S., Dhellemmes, F., Guttridge, T. L., Kurvers, R. H., Gruber, S. H., and Krause, J. (2016). Rate of movement of juvenile lemon sharks in a novel open field, are we measuring activity or reaction to novelty? Animal Behaviour 116, 75–82.
Rate of movement of juvenile lemon sharks in a novel open field, are we measuring activity or reaction to novelty?Crossref | GoogleScholarGoogle Scholar |

Finger, J. S., Guttridge, T. L., Wilson, A. D. M., Gruber, S. H., and Krause, J. (2018). Are some sharks more social than others? Short-and long-term consistencies in the social behavior of juvenile lemon sharks. Behavioral Ecology and Sociobiology 72, 17.
Are some sharks more social than others? Short-and long-term consistencies in the social behavior of juvenile lemon sharks.Crossref | GoogleScholarGoogle Scholar |

Fingerle, A., Larranaga, N., and Steingrímsson, S. Ó. (2016). Density-dependent diel activity in stream‐dwelling Arctic charr Salvelinus alpinus. Ecology and Evolution 6, 3965–3976.
Density-dependent diel activity in stream‐dwelling Arctic charr Salvelinus alpinus.Crossref | GoogleScholarGoogle Scholar | 27247761PubMed |

Fox, J., and Weisberg, S. (2019). ‘An R Companion to Applied Regression’, 3rd edn. (Sage: Thousand Oaks, CA, USA.)

Frick, L. H., Reina, R. D., and Walker, T. I. (2009). The physiological response of Port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity. North American Journal of Fisheries Management 29, 127–139.
The physiological response of Port Jackson sharks and Australian swellsharks to sedation, gill-net capture, and repeated sampling in captivity.Crossref | GoogleScholarGoogle Scholar |

Garla, R. C., Chapman, D. D., Shivji, M. S., Wetherbee, B. M., and Amorim, A. F. (2006). Habitat of juvenile Caribbean reef sharks, Carcharhinus perezi, at two oceanic insular marine protected areas in the southwestern Atlantic Ocean: Fernando de Noronha Archipelago and Atol das Rocas, Brazil. Fisheries Research 81, 236–241.
Habitat of juvenile Caribbean reef sharks, Carcharhinus perezi, at two oceanic insular marine protected areas in the southwestern Atlantic Ocean: Fernando de Noronha Archipelago and Atol das Rocas, Brazil.Crossref | GoogleScholarGoogle Scholar |

Gervais, C. (2019). Physiological responses of developing Port Jackson sharks to predation and elevated temperatures. Ph.D. Thesis, Macquarie University, Sydney, NSW, Australia.

Guttridge, T. L., Gruber, S. H., Krause, J., and Sims, D. W. (2010). Novel acoustic technology for studying free-ranging shark social behaviour by recording individuals’ interactions. PLoS One 5, e9324.
Novel acoustic technology for studying free-ranging shark social behaviour by recording individuals’ interactions.Crossref | GoogleScholarGoogle Scholar | 20174465PubMed |

Heupel, M. R., Semmens, J. M., and Hobday, A. J. (2006). Automated acoustic tracking of aquatic animals: scales, design and deployment of listening station arrays. Marine and Freshwater Research 57, 1–13.
Automated acoustic tracking of aquatic animals: scales, design and deployment of listening station arrays.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C., Harcourt, R. G., and Otway, N. M. (2006). Observation of localised movements and residence times of the wobbegong shark Orectolobus halei at Fish Rock, NSW, Australia. Cybium 30, 103–111.

Jacoby, D. M., Busawon, D. S., and Sims, D. W. (2010). Sex and social networking: the influence of male presence on social structure of female shark groups. Behavioral Ecology 21, 808–818.
Sex and social networking: the influence of male presence on social structure of female shark groups.Crossref | GoogleScholarGoogle Scholar |

Jacoby, D. M., Fear, L. N., Sims, D. W., and Croft, D. P. (2014). Shark personalities? Repeatability of social network traits in a widely distributed predatory fish. Behavioral Ecology and Sociobiology 68, 1995–2003.
Shark personalities? Repeatability of social network traits in a widely distributed predatory fish.Crossref | GoogleScholarGoogle Scholar |

Judson, O. P. (1994). The rise of the individual-based model in ecology. Trends in Ecology & Evolution 9, 9–14.
The rise of the individual-based model in ecology.Crossref | GoogleScholarGoogle Scholar |

Kadar, J., Ladds, M., Mourier, J., Day, J., and Brown, C. (2019). Acoustic accelerometry reveals diel activity patterns in premigratory Port Jackson sharks. Ecology and Evolution 9, 8933–8944.
Acoustic accelerometry reveals diel activity patterns in premigratory Port Jackson sharks.Crossref | GoogleScholarGoogle Scholar | 31462992PubMed |

Kadri, S., Metcalfe, N. B., Huntingford, F. A., and Thorpe, J. E. (1997). Daily feeding rhythms in Atlantic salmon II: size-related variation in feeding patterns of post-smolts under constant environmental conditions. Journal of Fish Biology 50, 273–279.
Daily feeding rhythms in Atlantic salmon II: size-related variation in feeding patterns of post-smolts under constant environmental conditions.Crossref | GoogleScholarGoogle Scholar |

Kelly, M. L., Murray, E. R., Kerr, C. C., Radford, C. A., Collin, S. P., Lesku, J. A., and Hemmi, J. M. (2020). Diverse activity rhythms in sharks (Elasmobranchii). Journal of Biological Rhythms 35, 476–488.
Diverse activity rhythms in sharks (Elasmobranchii).Crossref | GoogleScholarGoogle Scholar | 32525441PubMed |

Lei, J., and Booth, D. T. (2017). Intraspecific variation in space use of a coastal population of lace monitors (Varanus varius). Australian Journal of Zoology 65, 398–407.
Intraspecific variation in space use of a coastal population of lace monitors (Varanus varius).Crossref | GoogleScholarGoogle Scholar |

Luongo, S. M., and Lowe, C. G. (2018). Seasonally acclimated metabolic Q 10 of the California horn shark, Heterodontus francisci. Journal of Experimental Marine Biology and Ecology 503, 129–135.
Seasonally acclimated metabolic Q 10 of the California horn shark, Heterodontus francisci.Crossref | GoogleScholarGoogle Scholar |

Matich, P., and Heithaus, M. R. (2015). Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia 178, 347–359.
Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas).Crossref | GoogleScholarGoogle Scholar | 25669454PubMed |

Matich, P., Kiszka, J. J., Heithaus, M. R., Le Bourg, B., and Mourier, J. (2019). Inter-individual differences in ontogenetic trophic shifts among three marine predators. Oecologia 189, 621–636.
Inter-individual differences in ontogenetic trophic shifts among three marine predators.Crossref | GoogleScholarGoogle Scholar | 30796523PubMed |

McLaughlin, R. H. (1969). The ecology of heterodont sharks. Ph.D. Thesis, University of New South Wales, Sydney, NSW, Australia.

McLaughlin, R. H., and O’Gower, A. K. (1971). Life history and underwater studies of a heterodont shark. Ecological Monographs 41, 271–289.
Life history and underwater studies of a heterodont shark.Crossref | GoogleScholarGoogle Scholar |

Meese, E. N., and Lowe, C. G. (2020). Active acoustic telemetry tracking and tri-axial accelerometers reveal fine-scale movement strategies of a non-obligate ram ventilator. Movement Ecology 8, 8.
Active acoustic telemetry tracking and tri-axial accelerometers reveal fine-scale movement strategies of a non-obligate ram ventilator.Crossref | GoogleScholarGoogle Scholar | 32071719PubMed |

Mourier, J., Bass, N. C., Guttridge, T. L., Day, J., and Brown, C. (2017). Does detection range matter for inferring social networks in a benthic shark using acoustic telemetry? Royal Society Open Science 4, 170485.
Does detection range matter for inferring social networks in a benthic shark using acoustic telemetry?Crossref | GoogleScholarGoogle Scholar | 28989756PubMed |

Mulcahy, D. M. (2003). Surgical implantation of transmitters into fish. ILAR Journal 44, 295–306.
Surgical implantation of transmitters into fish.Crossref | GoogleScholarGoogle Scholar | 13130160PubMed |

Munroe, S. E. M., Simpfendorfer, C. A., and Heupel, M. R. (2016). Variation in blacktip shark movement patterns in a tropical coastal bay. Environmental Biology of Fishes 99, 377–389.
Variation in blacktip shark movement patterns in a tropical coastal bay.Crossref | GoogleScholarGoogle Scholar |

Papastamatiou, Y. P., Lowe, C. G., Caselle, J. E., and Friedlander, A. M. (2009). Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90, 996–1008.
Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll.Crossref | GoogleScholarGoogle Scholar | 19449694PubMed |

Papastamatiou, Y. P., Bodey, T. W., Friedlander, A. M., Lowe, C. G., Bradley, D., Weng, K., Priestley, V., and Caselle, J. E. (2018). Spatial separation without territoriality in shark communities. Oikos 127, 767–779.
Spatial separation without territoriality in shark communities.Crossref | GoogleScholarGoogle Scholar |

Peel, L. R., Collin, S. P., and Hart, N. S. (2020). Retinal topography and spectral sensitivity of the Port Jackson shark (Heterodontus portusjacksoni). The Journal of Comparative Neurology 528, 2831–2847.
Retinal topography and spectral sensitivity of the Port Jackson shark (Heterodontus portusjacksoni).Crossref | GoogleScholarGoogle Scholar | 32227480PubMed |

Powter, D. M., and Gladstone, W. (2009). Habitat-mediated use of space by juvenile and mating adult Port Jackson sharks, Heterodontus portusjacksoni, in Eastern Australia. Pacific Science 63, 1–14.
Habitat-mediated use of space by juvenile and mating adult Port Jackson sharks, Heterodontus portusjacksoni, in Eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Ruf, T. (1999). The Lomb-Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biological Rhythm Research 30, 178–201.
The Lomb-Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series.Crossref | GoogleScholarGoogle Scholar |

Ryan, L. A., Meeuwig, J. J., Hemmi, J. M., Collin, S. P., and Hart, N. S. (2015). It is not just size that matters: shark cruising speeds are species-specific. Marine Biology 162, 1307–1318.
It is not just size that matters: shark cruising speeds are species-specific.Crossref | GoogleScholarGoogle Scholar |

Sims, D. W. (2003). Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free‐ranging sharks. Journal of Fish Biology 63, 53–73.
Tractable models for testing theories about natural strategies: foraging behaviour and habitat selection of free‐ranging sharks.Crossref | GoogleScholarGoogle Scholar |

Speed, C. W., Field, I. C., Meekan, M. G., and Bradshaw, C. J. (2010). Complexities of coastal shark movements and their implications for management. Marine Ecology Progress Series 408, 275–293.
Complexities of coastal shark movements and their implications for management.Crossref | GoogleScholarGoogle Scholar |

Speed, C. W., Meekan, M. G., Field, I. C., McMahon, C. R., Stevens, J. D., McGregor, F., Huveneers, C., Berger, Y., and Bradshaw, C. J. (2011). Spatial and temporal movement patterns of a multi-species coastal reef shark aggregation. Marine Ecology Progress Series 429, 261–275.
Spatial and temporal movement patterns of a multi-species coastal reef shark aggregation.Crossref | GoogleScholarGoogle Scholar |

Speed, C. W., Meekan, M. G., Field, I. C., McMahon, C. R., Harcourt, R. G., Stevens, J. D., Babcock, R. C., Pillans, R. D., and Bradshaw, C. J. A. (2016). Reef shark movements relative to a coastal marine protected area. Regional Studies in Marine Science 3, 58–66.
Reef shark movements relative to a coastal marine protected area.Crossref | GoogleScholarGoogle Scholar |

Spiegel, O., Leu, S. T., Bull, C. M., and Sih, A. (2017). What’s your move? Movement as a link between personality and spatial dynamics in animal populations. Ecology Letters 20, 3–18.
What’s your move? Movement as a link between personality and spatial dynamics in animal populations.Crossref | GoogleScholarGoogle Scholar | 28000433PubMed |

Swadling, D. S., Knott, N. A., Rees, M. J., Pederson, H., Adams, K. R., Taylor, M. D., and Davis, A. R. (2020). Seagrass canopies and the performance of acoustic telemetry: implications for the interpretation of fish movements. Animal Biotelemetry 8, 8.
Seagrass canopies and the performance of acoustic telemetry: implications for the interpretation of fish movements.Crossref | GoogleScholarGoogle Scholar |

Swanson, A., Arnold, T., Kosmala, M., Forester, J., and Packer, C. (2016). In the absence of a “landscape of fear”: How lions, hyenas, and cheetahs coexist. Ecology and Evolution 6, 8534–8545.
In the absence of a “landscape of fear”: How lions, hyenas, and cheetahs coexist.Crossref | GoogleScholarGoogle Scholar | 28031805PubMed |

Wearmouth, V. J., and Sims, D. W. (2008). Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Advances in Marine Biology 54, 107–170.
Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications.Crossref | GoogleScholarGoogle Scholar | 18929064PubMed |

Wearmouth, V. J., and Sims, D. W. (2010). Sexual segregation in elasmobranchs. Biologia Marina Mediterranea 17, 236–239.

Whitney, N. M., Lear, K. O., Gaskins, L. C., and Gleiss, A. C. (2016). The effects of temperature and swimming speed on the metabolic rate of the nurse shark (Ginglymostoma cirratum, Bonaterre). Journal of Experimental Marine Biology and Ecology 477, 40–46.
The effects of temperature and swimming speed on the metabolic rate of the nurse shark (Ginglymostoma cirratum, Bonaterre).Crossref | GoogleScholarGoogle Scholar |

Wickham, H. (2016). ‘ggplot2: Elegant Graphics for Data Analysis.’ (Springer-Verlag: New York, NY, USA.)

Wu, Y., Wang, H., Wang, H., and Feng, J. (2018). Arms race of temporal partitioning between carnivorous and herbivorous mammals. Scientific Reports 8, 1713.
Arms race of temporal partitioning between carnivorous and herbivorous mammals.Crossref | GoogleScholarGoogle Scholar | 29379083PubMed |

Zollner, P. A., and Lima, S. L. (1999). Search strategies for landscape-level interpatch movements. Ecology 80, 1019–1030.
Search strategies for landscape-level interpatch movements.Crossref | GoogleScholarGoogle Scholar |

Zupcic-Moore, J. R., Ruiz-Cooley, R. I., Paliza, O., Koch, P. L., and McCarthy, M. D. (2017). Using stable isotopes to investigate foraging variation and habitat use of sperm whales from northern Peru. Marine Ecology Progress Series 579, 201–212.
Using stable isotopes to investigate foraging variation and habitat use of sperm whales from northern Peru.Crossref | GoogleScholarGoogle Scholar |