California sea lions interfere with striped marlin hunting behaviour in multi-species predator aggregations

The open ocean offers a suite of ecological conditions promoting the occurrence of multi-species predator aggregations. These mixed predator aggregations typically hunt large groups of relatively small and highly cohesive prey. However, the mechanisms and functions of these mixed predator aggregations are largely unknown. Even basic knowledge of whether the predator species' interactions are mutualistic, commensal or parasitic is typically missing. Moreover, recordings of attack and capture rates of marine multi-species predator aggregations, which are critical in understanding how and why these interactions have evolved, are almost completely non-existent owing to logistical challenges. Using underwater video, we quantified the attack and capture rates of two high-trophic level marine predators, California sea lions (Zalophus californianus) and striped marlin (Kajikia audax) attacking schools of fishes in the Southern California Current System, offshore the Baja California Peninsula. Recording over 5000 individual attacks across 13 fish schools, which varied in species, size and predator composition, we found that sea lions kleptoparasitized striped marlin hunts and reduced the frequency of marlin attacks and captures via interference competition. We discuss our results in the context of the phenotypic differences between the predator species and implications for a better understanding of multi-species predator aggregations. This article is part of the theme issue ‘Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes’.

[1]  S. Krause,et al.  Mechanisms of prey division in striped marlin, a marine group hunting predator , 2022, Communications Biology.

[2]  P. P. Olea,et al.  Temporal resource partitioning mediates vertebrate coexistence at carcasses: the role of competitive and facilitative interactions , 2022, Basic and Applied Ecology.

[3]  Josh A. Firth,et al.  Sociability as a personality trait in animals: methods, causes and consequences , 2021, Biological reviews of the Cambridge Philosophical Society.

[4]  J. Krause,et al.  Fish waves as emergent collective antipredator behavior , 2021, Current Biology.

[5]  E. González-Rodríguez,et al.  California sea lion population decline at the southern limit of its distribution during warm regimes in the Pacific Ocean , 2021, Regional Studies in Marine Science.

[6]  M. Leftwich,et al.  The role of California sea lion (Zalophus californianus) hindflippers as aquatic control surfaces for maneuverability. , 2021, The Journal of experimental biology.

[7]  F. Trillmich,et al.  Cooperation and opportunism in Galapagos sea lion hunting for shoaling fish , 2021, Ecology and evolution.

[8]  D. Costa,et al.  Influence of hunting strategy on foraging efficiency in Galapagos sea lions , 2021, PeerJ.

[9]  R. Langrock,et al.  Individuality counts: A new comprehensive approach to foraging strategies of a tropical marine predator , 2021, Oecologia.

[10]  Diego Páez-Rosas,et al.  Changes in the Galapagos sea lion diet as a response to El Niño-Southern Oscillation , 2020 .

[11]  M. Moléon,et al.  Hyaenas and lions: how the largest African carnivores interact at carcasses , 2020 .

[12]  J. Krause,et al.  Linking hunting weaponry to attack strategies in sailfish and striped marlin , 2020, Proceedings of the Royal Society B.

[13]  G. E. Machovsky-Capuska,et al.  The Nutritional Ecology of Marine Apex Predators. , 2020, Annual review of marine science.

[14]  D. Vongraven,et al.  Humpback whale (Megaptera novaeangliae) and killer whale (Orcinus orca) feeding aggregations for foraging on herring (Clupea harengus) in Northern Norway , 2017 .

[15]  J. Krause,et al.  Injury-mediated decrease in locomotor performance increases predation risk in schooling fish , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  D. Blumstein,et al.  Social associations between California sea lions influence the use of a novel foraging ground , 2017, Royal Society Open Science.

[17]  J. Krause,et al.  The Evolution of Lateralization in Group Hunting Sailfish , 2017, Current Biology.

[18]  J. Krause,et al.  Correction to ‘Proto-cooperation: group hunting sailfish improve hunting success by alternating attacks on grouping prey’ , 2016, Proceedings of the Royal Society B: Biological Sciences.

[19]  Kristin N. Marshall,et al.  Developing a high taxonomic resolution food web model to assess the functional role of forage fish in the California Current ecosystem , 2016 .

[20]  K. Acevedo‐Whitehouse,et al.  Impact of the 2015 El Niño-Southern Oscillation on the Abundance and Foraging Habits of Guadalupe Fur Seals and California Sea Lions from the San Benito Archipelago, Mexico , 2016, PloS one.

[21]  Pawel Romanczuk,et al.  Proto-cooperation: group hunting sailfish improve hunting success by alternating attacks on grouping prey , 2016, Proceedings of the Royal Society B: Biological Sciences.

[22]  C. Guinet,et al.  Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals. , 2015, The Journal of animal ecology.

[23]  M. Tucker,et al.  Examining predator–prey body size, trophic level and body mass across marine and terrestrial mammals , 2014, Proceedings of the Royal Society B: Biological Sciences.

[24]  A. Moore,et al.  Do yearling New Zealand sea lions (Phocarctos hookeri) learn foraging behavior from their mothers , 2014 .

[25]  J. Krause,et al.  How sailfish use their bills to capture schooling prey , 2014, Proceedings of the Royal Society B: Biological Sciences.

[26]  Y. Tremblay,et al.  Effects of successive predator attacks on prey aggregations , 2014, Theoretical Ecology.

[27]  D. Costa,et al.  Individual Foraging Strategies Reveal Niche Overlap between Endangered Galapagos Pinnipeds , 2013, PloS one.

[28]  Nicholas K Dulvy,et al.  Ecosystem ecology: size-based constraints on the pyramids of life. , 2013, Trends in ecology & evolution.

[29]  A. Gallagher,et al.  White Sharks (Carcharodon carcharias) Scavenging on Whales and Its Potential Role in Further Shaping the Ecology of an Apex Predator , 2013, PloS one.

[30]  Michael D. Scott,et al.  Pelagic predator associations: tuna and dolphins in the eastern tropical Pacific Ocean , 2012 .

[31]  H. Skov,et al.  Wasp-Waist Interactions in the North Sea Ecosystem , 2011, PloS one.

[32]  A. Lowther,et al.  Detecting alternate foraging ecotypes in Australian sea lion (Neophoca cinerea) colonies using stable isotope analysis , 2011 .

[33]  E. Wolkovich,et al.  Scavenging: how carnivores and carrion structure communities. , 2011, Trends in ecology & evolution.

[34]  L. Gygax,et al.  Role of feeding strategies in seabird–minke whale associations , 2011 .

[35]  V. Peddemors,et al.  Broad-scale distribution patterns of sardine and their predators in relation to remotely sensed environmental conditions during the KwaZulu-Natal sardine run , 2010 .

[36]  Pablo Gallo Reynoso Group behavior of common dolphins (Delphinus delphis) during prey capture , 2009 .

[37]  K. Hyrenbach,et al.  Associations between seabirds and subsurface predators around Oahu, Hawaii , 2008 .

[38]  T. Caro,et al.  Interspecific competition and predation in American carnivore families , 2008 .

[39]  B. Würsig,et al.  Dusky Dolphins Influence Prey Accessibility for Seabirds in Admiralty Bay, New Zealand , 2008 .

[40]  D. Costa,et al.  Multiple foraging strategies in a marine apex predator, the Galapagos sea lion Zalophus wollebaeki , 2008 .

[41]  J. J. Bizzarro,et al.  A Review of the Physical and Biological Characteristics of the Bahía Magdalena Lagoon Complex (Baja California Sur, Mexico) , 2008 .

[42]  E. Gese,et al.  Coyotes and recolonizing wolves: social rank mediates risk-conditional behaviour at ungulate carcasses , 2008, Animal Behaviour.

[43]  T. Caro,et al.  To flee or not to flee: predator avoidance by cheetahs at kills , 2007, Behavioral Ecology and Sociobiology.

[44]  K. Hobson,et al.  Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean , 2007 .

[45]  Werner Ulrich,et al.  Consumer-resource body-size relationships in natural food webs. , 2006, Ecology.

[46]  M. Bearzi CALIFORNIA SEA LIONS USE DOLPHINS TO LOCATE FOOD , 2006 .

[47]  S. Buskirk,et al.  Diet, Morphology, and Interspecific Killing in Carnivora , 2006, The American Naturalist.

[48]  D. Costa,et al.  When does physiology limit the foraging behaviour of freely diving mammals , 2004 .

[49]  G. Ponce-Díaz,et al.  Analysis of sportfishing catch rates of striped marlin (Tetrapturus audax) at Cabo San Lucas, Baja California Sur, Mexico, and their relation to sea surface temperature , 2003 .

[50]  Per Berggren,et al.  Mixed species groups in mammals , 2003 .

[51]  Artemio Gallegos-García,et al.  Coastal Upwelling Activity on the Pacific Shelf of the Baja California Peninsula , 2003 .

[52]  F. Galván‐Magaña,et al.  Trophic dynamics and seasonal energetics of striped marlin Tetrapturus audax in the southern Gulf of California, Mexico , 2002 .

[53]  D. Stahler,et al.  Constraints on active-consumption rates in gray wolves, coyotes, and grizzly bears , 2002 .

[54]  Astrid Jarre,et al.  Small pelagics in upwelling systems: patterns of interaction and structural changes in "wasp-waist" ecosystems , 2000 .

[55]  H. Bleckmann,et al.  The ageing of the low-frequency water disturbances caused by swimming goldfish and its possible relevance to prey detection. , 2000, The Journal of experimental biology.

[56]  F. Trillmich,et al.  Fish prey of the sympatric Galápagos fur seals and sea lions: seasonal variation and niche separation , 1999 .

[57]  Michael D. Scott,et al.  DIEL PATTERNS IN AGGREGATIONS OF PELAGIC DOLPHINS AND TUNAS IN THE EASTERN PACIFIC , 1998 .

[58]  D. Heinemann,et al.  OBSERVATIONS OF MULTISPECIES SEABIRD FLOCKS AROUND SOUTH GEORGIA , 1991 .

[59]  G. Polis,et al.  Complex Trophic Interactions in Deserts: An Empirical Critique of Food-Web Theory , 1991, The American Naturalist.

[60]  G. Antonelis,et al.  Diving patterns of California sea lions, Zalophus californianus , 1989 .

[61]  D. Au,et al.  SEABIRD INTERACTIONS WITH DOLPHINS AND TUNA IN THE EASTERN TROPICAL PACIFIC , 1986 .

[62]  David W. Macdonald,et al.  The ecology of carnivore social behaviour , 1983, Nature.

[63]  W. Stockton,et al.  Food falls in the deep sea: occurrence, quality, and significance , 1982 .

[64]  John A. Wiens,et al.  The Ecology of Seabird Feeding Flocks in Alaska , 1981 .

[65]  G. Heckel,et al.  Introduction: Pinnipeds in Latin America , 2021 .

[66]  G. Rivas‐Torres,et al.  Hunting and cooperative foraging behavior of Galapagos sea lion: An attack to large pelagics , 2019, Marine Mammal Science.

[67]  Y. Tremblay,et al.  How to capture fish in a school? Effect of successive predator attacks on seabird feeding success. , 2016, The Journal of animal ecology.

[68]  L. Dill,et al.  Feeding Strategies and Tactics , 2009 .

[69]  A. Baco,et al.  ECOLOGY OF WHALE FALLS AT THE DEEP-SEA FLOOR , 2003 .

[70]  A. Frantzis,et al.  Mixed-species associations of striped dolphins (Stenella coeruleoalba), short-beaked common dolphins (Delphinus delphis), and Risso's dolphins (Grampus griseus) in the Gulf of Corinth (Greece, Mediterranean Sea) , 2002 .

[71]  Eric Clua,et al.  Mixed-species feeding aggregation of dolphins, large tunas and seabirds in the Azores , 2001 .

[72]  C. J. Camphuysen,et al.  Multi-species feeding associations in North Sea seabirds: jointly exploiting a patchy environment , 1999 .

[73]  R. Sluys,et al.  The taxonomic richness of South Africa's marine fauna: a crisis at hand , 1999 .

[74]  A. Bakun Patterns in the ocean: Ocean processes and marine population dynamics , 1996 .

[75]  K. Prior Competition at the carcass : opportunities for social foraging by turkey vultures in southern Ontario , 1991 .