Skip to main content
Log in

Variation in the emission rate of sounds in a captive group of false killer whales Pseudorca crassidens during feedings: possible food anticipatory vocal activity?

  • Biology
  • Published:
Chinese Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

This study examines whether a group of captive false killer whales (Pseudorca crassidens ) showed variations in the vocal rate around feeding times. The high level of motivation to express appetitive behaviors in captive animals may lead them to respond with changes of the behavioral activities during the time prior to food deliveries which are referred to as food anticipatory activity. False killer whales at Qingdao Polar Ocean World (Qingdao, China) showed significant variations of the rates of both the total sounds and sound classes (whistles, clicks, and burst pulses) around feedings. Precisely, from the Transition interval that recorded the lowest vocalization rate (3.40 s/m/d), the whales increased their acoustic emissions upon trainers’ arrival (13.08 s/m/d). The high rate was maintained or intensified throughout the food delivery (25.12 s/m/d), and then reduced immediately after the animals were fed (9.91 s/m/d). These changes in the false killer whales sound production rates around feeding times supports the hypothesis of the presence of a food anticipatory vocal activity. Although sound rates may not give detailed information regarding referential aspects of the animal communication it might still shed light about the arousal levels of the individuals during different social or environmental conditions. Further experiments should be performed to assess if variations of the time of feeding routines may affect the vocal activity of cetaceans in captivity as well as their welfare.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Acevedo-Gutièrrez A, Stienessen S C. 2004. Bottlenose dolphins (Tursiops truncatus) increase number of whistles when feeding. Aquatic Mammals, 30 (3): 357–362, http://dx.doi.org/10.1578/AM.30.3.2004.357.

    Article  Google Scholar 

  • Akiyama J, Ohta M. 2007. Increased number of whistles of bottlenose dolphins, Tursiops truncatus, arising from interaction with people. J. Vet. Med. Sci., 69 (2): 165–170.

    Article  Google Scholar 

  • Albeck D S, McKittrick C R, Blanchard D C, Blanchard R J, Nikulina J, McEwen B S, Sakai R R. 1997. Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain. The Journal of Neuroscience, 17 (12): 4895–4903.

    Google Scholar 

  • Amsel A. 1958. The role of frustrative nonreward in noncontinuous reward situations. Psychol. Bull., 55 (2): 102–199.

    Article  Google Scholar 

  • Amstrong S. 1980. A chronometric approach to the study of feeding behavior. Neurosci. Biobehav. Rev., 4 (1): 27–53.

    Article  Google Scholar 

  • Andrews M W, Rosenblum L A. 1991. Attachment in monkey infants raised in variable-and low-demand environments. Child Dev., 62 (4): 686–693.

    Article  Google Scholar 

  • Andrews M W, Rosenblum L A. 1993. Assessment of attachment in differentially reared infant monkeys (Macaca radiata): response to separation and a novel environment. J. Comp. Psychol., 107 (1): 84–90.

    Article  Google Scholar 

  • Au W W L, Pawloski J L, Nachtigall P E, Blonz M, Gisner R C. 1995. Echolocation signals and transmission beam pattern of a false killer whale (Pseudorca crassidens). J. Acoust. Soc. Am., 98 (1): 51–59.

    Article  Google Scholar 

  • Azzaydi M, Madrid J A, Zamora S, Sánchez-Vázquez F J, Martı́nez F J. 1998. Effect of three feeding strategies (automatic, ad libitum demand-feeding and time-restricted demand-feeding) on feeding rhythms and growth in European sea bass (Dicentrarchus labrax L.). Aquaculture, 163 (3-4): 285–296, http://dx.doi.org/10.1016/S0044-8486 (98)00238-5.

    Article  Google Scholar 

  • Baird R W, Gorgone A M, McSweeney D J, Webster D L, Salden D R, Deakos M H, Ligon A D, Schorr G S, Barlow J, Mahaffy S D. 2008. False killer whales (Pseudorca crassidens) around the main Hawaiian Islands: long-term site fidelity, inter-island movements, and association patterns. Marine Mammal Science, 24 (3): 591–612.

    Article  Google Scholar 

  • Baird R W, Schorr G S, Webster D L, McSweeney D J, Hanson M B, Andrews R D. 2010. Movements and habitat use of satellite-tagged false killer whales around the main Hawaiian Islands. Endangered Species Research, 10: 107–121.

    Article  Google Scholar 

  • Baldwin R F. 1992). Behavior of Carnivores in Outdoor Exhibits at the National Zoological Park). George Mason University, Fairfax, Virginia). 154p.

    Google Scholar 

  • Barrett-Lennard L G, Ford J K B, Heise K A. 1996. The mixed blessing of echolocation: differences in sonar use by fisheating and mammal-eating killer whales. Anim. Behav., 51 (3): 553–565.

    Article  Google Scholar 

  • Bassett L, Buchanan-Smith H M. 2007. Effects of predictability on the welfare of captive animals. Appl. Anim. Behav. Sci., 102 (3-4): 223–245.

    Article  Google Scholar 

  • Bayart F, Hayashi K T, Faull K F, Barchas J D, Levine S. 1990. Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 104 (1): 98–107.

    Article  Google Scholar 

  • Bazúa-Durán C, Au W W L. 2002. Whistles of Hawaiian spinner dolphins. J. Acoustic. Soc. Am., 112(5): 3 064–3 072, http://dx.doi.org/doi.10.112/1.1508785.

    Article  Google Scholar 

  • Bloomsmith M A, Lambeth S P. 1995. Effects of predictable versus unpredictable feeding schedules on chimpanzee behavior. Appl. Anim. Behav. Sci., 44 (1): 65–74.

    Article  Google Scholar 

  • Boinski S, Gross T S, Davis J K. 1999. Terrestrial predator alarm vocalizations are a valid monitor of stress in captive brown capuchins (Cebus apella). Zoo Biology, 18 (4): 295–312.

    Article  Google Scholar 

  • Brando S. 2010. Advances in husbandry training in marine mammal care programs. Int. J. Comp. Psychol., 23 (4): 777–791.

    Google Scholar 

  • Brickman J J. 2003. Factors Influencing Whistle Usage of the Pacific White-sided Dolphin, Lagenorhynchus obliquidens, at the John G. Shedd Aquarium). Western Illinois University, Quad Cities, Moline). 135p.

    Google Scholar 

  • Brown D H, Caldwell D K, Caldwell M C. 1966. Observations on the behavior of wild and captive false killer whales, with notes on associated behavior of other genera of captive delphinids. Contributions in Science, 95: 1–32.

    Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J. 2000. Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behavioral Neuroscience, 114 (2): 320–327, http://dx.doi.org/10.1037/0735-7044.114.2.320.

    Article  Google Scholar 

  • Burgdorf J, Panksepp J. 2001. Tickling induces reward in adolescent rats. Physiology and Behavior, 72 (1-2): 167–173.

    Article  Google Scholar 

  • Burman O H P, Ilyat A, Jones G, Mendl M. 2007. Ultrasonic vocalizations as indicators of welfare for laboratory rats (Rattus norvegicus). Appl. Anim. Behav. Sci., 104 (1-2): 116–129, http://dx.doi.org/10.1016/j.applanim.2006.04.028.

    Article  Google Scholar 

  • Busnel R G, Dziedzic A. 1966. Acoustic signals of the Pilot whale, Globicephala melaena, and of the porpoise Delphinus delphis and Phocoena phocoena). In: Norris K S ed. Whales, Dolphins and Porpoises. Univ. California Press, Berkley, USA). p.607–648.

    Google Scholar 

  • Busnel R G, Dziedzic A. 1968. Caracteristiques physiques des signaux acoustiques de Pseudorca crassidens owen (cetacea odontocete). Mammalia, 32 (1): 1–5.

    Article  Google Scholar 

  • Caine N G, Addington R L, Windfelder T L. 1995. Factors affecting the rates of food calls given by red-bellied tamarins. Anim. Behav., 50 (1): 53–60.

    Article  Google Scholar 

  • Caldwell D K, Prescott J H, Caldwell M C. 1966. Production of pulsed sounds by the pigmy sperm whale, Kogia breviceps. Bulletin Southern California Academy of Science, 65: 245–248.

    Google Scholar 

  • Caldwell M C, Caldwell D K. 1968. Vocalization of naïve captive dolphins in small groups. Science, 159 (3819): 1121–1123, http://dx.doi.org/10.1126/science.159.3819.1121.

    Article  Google Scholar 

  • Carlstead K. 1986. Predictability of feeding: its effect on agonistic behaviour and growth in grower pigs. Appl. Anim. Behav. Sci., 16 (1): 25–38.

    Article  Google Scholar 

  • Carlstead K. 1998. Determining the causes of stereotypic behaviors in zoo carnivores: towards developing appropriate enrichment strategies). In: Shepherdson D J, Mellen J D, Hutchins M eds. Second Nature: Environmental Enrichment for Captive Animals). Smithsonian Institution Press, Washington DC, USA). p.172–183.

    Google Scholar 

  • Castellote M, Fossa F. 2006. Measuring acoustic activity as a method to evaluate welfare in captive beluga whales (Delphinapterus leucas). Aquatic Mammals, 32 (3): 325–333, http://dx.doi.org/10.1578/AM.32.3.2006.325.

    Article  Google Scholar 

  • Champoux M, Suomi S J. 1994. Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment. Primates, 35 (2): 191–202.

    Article  Google Scholar 

  • Cheney D L, Seyfarth R M. 1982. How vervet monkeys perceive their grunts: field playback experiments. Animal Behaviour, 30 (3): 739–751.

    Article  Google Scholar 

  • Clay Z, Smith C L, Blumstein D T. 2012. Food-associated vocalizations in mammals and birds: what do these calls really mean? Anim. Behav., 83 (2): 323–330, http://dx.doi. org/10.106/j.anbehav.2011.12.008.

    Article  Google Scholar 

  • Clay Z, Zuberbü hler K. 2009. Food-associated calling sequences in bonobos. Animal Behaviour, 77 (6): 1387–1396, http://dx.doi.org/10.1016/j.anbehav.2009.02.016.

    Article  Google Scholar 

  • Connor R C, Smolker R A. 1996. ‘Pop’ goes the dolphin: a vocalization male bottlenose dolphins produce during consortships. Behaviour, 133 (9): 643–662.

    Article  Google Scholar 

  • Crowell D, Comuzzie D K. 1993. Baboon vocalizations as measures of psychological well-being. Laboratory Primate Newsletter, 32: 5–6.

    Google Scholar 

  • Dawkins M S. 1998. Evolution and animal welfare. Q. Rev. Biol., 73 (3): 305–328.

    Article  Google Scholar 

  • Dawson S M, Thorpe C W. 1990. A quantitative analysis of the sounds of Hector’s dolphin. Ethology, 86 (2): 131–145.

    Article  Google Scholar 

  • de Waal F B M. 1993. Reconciliation among primates: a review of empirical evidence and unresolved issue). In: Mason W A, Mendoza S P eds. Primate Social Conflict, State University of New York Press, Albany). p.111–143.

    Google Scholar 

  • de Waal F B M, Hoekstra J A. 1980. Contexts and predictability of aggression in chimpanzees. Anim. Behav., 28 (3): 929–937.

    Article  Google Scholar 

  • de Waal F B M, Tyack P L. 2003). Animal Social Complexity: Intelligence, Culture, and Individualized Societies). Harvard University Press, Cambridge, MA, US). p.342–362.

    Book  Google Scholar 

  • Désautés C, Bidanel J P, Mormède P. 1997. Genetic study of behavioral and pituitary-adrenocortical reactivity in response to an environmental challenge in pigs. Physiology & Behavior, 62 (2): 337–345.

    Article  Google Scholar 

  • Di Bitetti M S. 2005. Food-associated calls and audience effects in tufted capuchin monkeys, Cebus apella nigritus. Anim. Behav., 69 (4): 911–919.

    Article  Google Scholar 

  • Díaz López B. 2011. Whistle characteristics in free-ranging bottlenose dolphins (Tursiops truncatus) in the Mediterranean Sea: influence of behaviour. M ammalian Biology -Zeitschrift für Säugetierkunde, 76 (2): 180–189.

    Article  Google Scholar 

  • Dittus W P G. 1984. Toque macaque food calls: semantic communication concerning food distribution in the environment. Anim. Behav., 32 (2): 470–477.

    Article  Google Scholar 

  • dos Santos M E, Almada V C. 2004. A case for passive sonar: foraging by bottlenose dolphins in a turbid estuary). In: Thomas J, Moss C, Vater M eds. Advances in the Study of Echolocation: Comparison between Bats and Dolphins). University of Chicago Press, Chicago). p.400–403.

    Google Scholar 

  • dos Santos M E, Louro S, Couchinho M, Brito C. 2005. Whistles of bottlenose dolphins (Tursiops truncatus) in the Sado estuary, Portugal: characteristics, production rates, and long-term contour stability. Aquatic Mammals, 31 (4): 453–462, http://dx.doi.org/10.1578/AM.31.4.2005.453.

    Article  Google Scholar 

  • Dreher J J, Evans W E. 1964. Cetacean communication). In: Tavolga W N ed. Marine Bio-Acoustics). Pergamon, Oxford. p.373–393.

    Google Scholar 

  • Dreher J J. 1966). Cetacean communication: small group experiment). In: Norris K S ed. Whales, Dolphins, and Porpoise. University of California, Berkeley). p.529–541.

    Google Scholar 

  • Düpjan S, Schön P C, Puppe B, Tuchscherer A, Manteuffel G. 2008. Differential vocal responses to physical and mental stressors in domestic pigs (Sus scrofa). Appl. Anim. Behav. Sci., 114 (1-2): 105–115, http://dx.doi.org/10.1016/ j.applanim.2007.12.005.

    Article  Google Scholar 

  • Esch H C, Sayigh L S, Blum J E, Wells R S. 2009. Whistles as potential indicators of stress in bottlenose dolphins (Tursiops truncatus). Journal of Mammalogy, 90 (3): 638–650, http://dx.doi.org/10.1644/08-MAMM-A-069R.1.

    Article  Google Scholar 

  • Fish M P, Mowbray W H. 1962. Production of underwater sound by the white whale or beluga, Delphinapterus leucas (Pallus). Journal of Marine Research, 20: 149–162.

    Google Scholar 

  • Friedman E M, Boinski S, Coe C L. 1995. Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques. American Journal of Primatology, 35 (2): 143–155.

    Article  Google Scholar 

  • Frohoff T G. 2004. Stress in Dolphins). In: Bekoff M ed. Encyclopedia of Animal Behavior). Greenwood Press, Westport, CT). p.1 158–1 164.

    Google Scholar 

  • Galhardo L, Appleby M C, Waran N K, Dos Santos M E. 1996. Spontaneous activities of captive performing bottlenose dolphins (Tursiops truncatus). Animal Welfare, 5 (4): 373–389.

    Google Scholar 

  • Galhardo L, Vital J, Oliveira R F. 2011. The role of predictability in the stress response of a cichlid fish. Physiology & Behavior, 102 (3-4): 367–372, http://dx.doi.org 10.1016/j. physbeh.2010.11.035.

    Article  Google Scholar 

  • Gilbert-Norton L B, Leaver L A, Shivik J A. 2009. The effect of randomly altering the time and location of feeding on the behaviour of captive coyotes (Canis latrans). Appl. Anim. Behav. Sci., 120 (3-4): 179–185, http://dx.doi. org/10.1016/j.applanim.2009.06.007.

    Article  Google Scholar 

  • Goldstein L E, Rasmusson A M, Bunney B S, Roth R H. 1996. Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. The Journal of Neuroscience, 16 (15): 4787–4798.

    Google Scholar 

  • Gottlieb D H, Coleman K, McCowan B. 2013. The effects of predictability in daily husbandry routines on captive Rhesus macaques (Macaca mulatta). Appl. Anim. Behav. Sci., 143 (2-4): 117–127, http://dx.doi.org/10.1016/j. applanim.2012.10.010.

    Article  Google Scholar 

  • Grandin T. 1998. The feasibility of using vocalization scoring as an indicator of poor welfare during cattle slaughter. Appl. Anim. Behav. Sci., 56 (2-4): 121–128, http://dx.doi. org/10.1016/S0168-1591(97)00102-0.

    Article  Google Scholar 

  • Hansen S W, Jeppesen L L. 2006. Temperament, stereotypies and anticipatory behaviour as measures of welfare in mink. Applied Animal Behaviour Science, 99 (1-2): 172–182, http://dx.doi.org/10.1016/j.applanim.2005.10.005.

    Article  Google Scholar 

  • Hawkins E R, Gartside D F. 2009a. Patterns of whistles emitted by wild Indo-Pacific bottlenose dolphins (Tursiops aduncus) during a Provisioning Program. Aquat. Mamm., 35 (2): 171–186.

    Article  Google Scholar 

  • Hawkins E R, Gartside D F. 2009b. Interactive behaviours of bottlenose dolphins (Tursiops aduncus) during encounters with vessels. Aquat. Mamm., 35 (2): 259–268.

    Article  Google Scholar 

  • Hawkins E R, Gartside D F. 2010. Whistle emissions of Indo-Pacific bottlenose dolphins (Tursiops aduncus) differ with group composition and surface behaviors. J. Acoustic Soc. Am., 127 (4): 2652–2663.

    Article  Google Scholar 

  • Hennessy J W, King M G, McClure T A, Levine S. 1977. Uncertainty, as defined by the contingency between environmental events, and the adrenocortical response of the rat to electric shock. J. Comp. Physiol. Psychol., 91 (6): 1447–1460.

    Article  Google Scholar 

  • Herzing D L. 1996. Vocalizations and associated underwater behavior of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat Mamm., 22 (2): 61–79.

    Google Scholar 

  • Herzing D L. 2000. Acoustics and social behavior of wild dolphins: implications for a sound society). In: Au W W L, Fay R R, Popper A N eds. Hearing by Whales and Dolphins). Springer, New York. p.225–272.

    Chapter  Google Scholar 

  • Higa J J, Staddon J E R. 1997. Dynamic models of rapid temporal control in animals). In: Bradshaw C M, Szabadi E eds. Time and Behaviour: Psychological and Neurobehavioural Analyses. Elsevier, Amsterdam, The Netherlands. p.1–40.

    Chapter  Google Scholar 

  • Howell S M, Matevia M, Fritz J, Nash L, Maki S. 1993. Prefeeding agonism and seasonality in captive groups of chimpanzees (Pan troglodytes). Animal Welfare, 2 (2): 153–163.

    Google Scholar 

  • Hughes B O, Duncan I J H. 1988. The notion of ethological ‘need’, models of motivation and animal welfare. Anim. Behav., 36 (6): 1696–1707.

    Article  Google Scholar 

  • Janik V M, Todt D, Dehnhardt G. 1994. Signature whistle variations in a bottlenosed dolphin, Tursiops truncatus. Behavioral Ecology and Sociobiology, 35 (4): 243–248.

    Article  Google Scholar 

  • Jenny S, Schmid H. 2002. Effect of feeding boxes on the behavior of stereotyping Amur tigers (Panthera tigris altaica) in the Zurich Zoo, Zurich, Switzerland. Zool Biol., 21 (6): 573–584.

    Article  Google Scholar 

  • Jensen A L M, Delfour F, Carter T. 2013. Anticipatory behavior in captive bottlenose dolphins (Tursiops truncatus): a preliminary study. Zoo Biology, 32 (4): 436–444.

    Article  Google Scholar 

  • Johanneson T, Ladewig J. 2000. The effect of irregular feeding times on the behaviour and growth of dairy calves. Appl. Anim. Behav. Sci., 69 (2): 103–111.

    Article  Google Scholar 

  • Johnson C M. 1993. Animal communication by way of coordinated cognitive systems). In: Bateson P P G, Klopfer P H, Thompson N S eds. Perspectives in Ethology). Plenum Press, New York). p.187–205.

    Google Scholar 

  • Jones M, Pillay N. 2004. Foraging in captive hamadryas baboons: implications for enrichment. Appl. Anim. Behav. Sci., 88 (1-2): 101–110, http://dx.doi.org/10.1016/j. applanim.2004.03.002.

    Article  Google Scholar 

  • Kamminga C, van Velden J G. 1987. Investigations on cetacean sonar VIII: sonar signals of Pseudorca crassidens in comparison with Tursiops truncatus. Aquatic Mammals, 13 (2): 43–49.

    Google Scholar 

  • Kaznadzei V V, Krechi S A, Khakhalkina E N. 1976. Types of dolphin communication signals and their organization. Soviet Physical Acoustics, 22 (6): 484–488.

    Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J. 1998. Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology, 112 (1): 65–73.

    Article  Google Scholar 

  • Krishnamurthy R. 1994. Vocalizations of captive François’ langurs linked to stereotypy and possible stress. Folia Primatologica, 63 (2): 91–95.

    Article  Google Scholar 

  • Lammers M O, Au W W L, Herzing D L. 2003. The broadband social acoustic signaling behavior of spinner and spotted dolphins. J. Acoust. Soc. Am., 114 (3): 1629–1639.

    Article  Google Scholar 

  • Laudenslager M L, Boccia M L, Berger C L, Gennaro-Ruggles M M, McFerran B, Reite M L. 1995. Total cortisol, free cortisol, and growth hormone associated with brief social separation experiences in young macaques. Developmental Psychobiology, 28 (4): 199–211.

    Article  Google Scholar 

  • Madsen P T, Kerr I, Payne R. 2004. Echolocation clicks of two free-ranging, oceanic delphinids with different food preferences: false killer whales Pseudorca crassidens and Risso’s dolphins Grampus griseus. J. Exp. Biol., 207: 1 811–1 823, http://dx.doi.org/10.1242/jeb.00966.

    Article  Google Scholar 

  • Mallapur A, Chellam R. 2002. Environmental Influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in southern India. Zoo Biology, 21 (6): 585–595, http://dx.doi.org/10.1002/zoo.10063.

    Article  Google Scholar 

  • Mann J, Kemps C. 2003. The effects of provisioning on maternal care in wild bottlenose dolphins, Shark Bay, Australia. Books Online, 5: 304–320.

    Google Scholar 

  • Manser M B, Seyfarth R M, Cheney D L. 2002. Suricate alarm calls signal predator class and urgency. Trend in Cognitive Sciences, 6 (2): 55–57.

    Article  Google Scholar 

  • Manteuffel G, Puppe B, Schön P C. 2004. Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science, 88 (1-2): 163–182.

    Article  Google Scholar 

  • Marino L, Connor R C, Fordyce R E, Herman L M, Hof P R, Lefebvre L, Lusseau D, McCowan B, Nimchinsky E A, Pack A A, Rendell L, Reidenberg J S, Reiss D, Uhen M D, van der Gucht E, Whitehead H. 2007. Cetaceans Have Complex Brains for Complex Cognition. Essay. PLoS Biology, 5 (5): e139.

    Article  Google Scholar 

  • Marino L. 2004. Dolphin cognition. Curr. Biol., 14 (21): R910–R911.

    Article  Google Scholar 

  • Mason G J. 1991. Stereotypies: a critical review. Anim. Behav., 41 (6): 1015–1037.

    Article  Google Scholar 

  • McCowan B, Rommeck I. 2006. Bioacoustic monitoring of aggression in group-housed rhesus macaques. Journal of Applied Animal Welfare Sciences, 9 (4): 261–268.

    Article  Google Scholar 

  • Melcón M L, Failla M, Iñíguez M A. 2012. Echolocation behavior of Franciscana dolphins (Pontoporia blainvillei) in the wild. J. Acoustic. Soc. Am., 131 (6): EL448, http:// dx.doi.org/10.1121/1.4710837.

    Article  Google Scholar 

  • Mercado E III, Uyeyama R K, Pack A A, Herman L M. 1999. Memory for action events in the bottlenosed dolphin. Anim. Cogn., 2 (1): 17–25.

    Article  Google Scholar 

  • Mistlberger R E. 1994. Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev., 18 (2): 171–195.

    Article  Google Scholar 

  • Mitani J C, Nishida T. 1993. Contexts and social correlates of long-distance calling by male chimpanzees. Anim. Behav., 45: 735–746.

    Article  Google Scholar 

  • Mistlberger R E. 2009. Food-anticipatory circadian rhythms: concepts and methods. European Journal of Neuroscience, 30 (9): 1718–1729, http://dx.doi.org/10.1111/j.1460-9568.2009.06965.x.

    Article  Google Scholar 

  • Mistlberger R E. 2011. Neurobiology of food anticipatory circadian rhythms. Physiology & Behavior, 104 (4): 535–545.

    Article  Google Scholar 

  • Monticelli P F, Tokumaru R S, Ades C. 2004. Isolation induced changes in Guinea Pig Cavia porcellus pup distress whistles. An. Acad. Bras. Ciênc., 76 (2): 368–372.

    Article  Google Scholar 

  • Morisaka T, Shinohara M, Nakahara F, Alamatsu T. 2005. Effects of ambient noise on the whistles of indo-pacific bottlenose dolphin populations. Journal of Mammalogy, 86 (3): 541–546.

    Article  Google Scholar 

  • Mulligan B E, Baker S C, Murphy M R. 1994. Vocalizations as indicators of emotional stress and psychological wellbeing in animals. Animal Welfare Information Center Newsletter, 5 (3): 1–3.

    Google Scholar 

  • Murray S O, Mercado E, Roitblat H L. 1998a. Characterizing the graded structure of false killer whale (Pseudorca crassidens) vocalizations. J. Acoust. Soc. Am., 104 (3): 1679–1688.

    Article  Google Scholar 

  • Murray S O, Mercado E, Roitblat H L. 1998b. The neural network classification of false killer whale (Pseudorca crassidens) vocalizations. J. Acoust. Soc. Am., 104 (6): 3626–3633.

    Article  Google Scholar 

  • Nachtigall P E, Supin A Y. 2008. A false killer whale adjusts its hearing when it echolocates. J Exp. Biol., 211 (11): 1714–1718, http://dx.doi.org/10.1242/jeb.013862.

    Article  Google Scholar 

  • Nemiroff L, Whitehead H. 2009. Structural characteristics of pulsed calls of long-finned pilot whales, Globicephala melas. Bioacoustics, 19 (1-2): 67–92.

    Article  Google Scholar 

  • Neuringer A J. 1969. Animals respond for food in the presence of free food. Science, 166 (3903): 399–401.

    Article  Google Scholar 

  • Norris K S, Dohl T P. 1980. Behavior of the Hawaiian spinner dolphins, Stenella longirostris. Fish. Bull., 77: 821–849.

    Google Scholar 

  • Norris K S, Würsig B, Wells R S, Würsig M. 1994. The Hawaiian Spinner Dolphin. University of California Press, Berkeley, CA. 436p.

    Google Scholar 

  • Nowacek D P. 2005. Acoustic ecology of foraging bottlenose dolphins (Tursiops truncatus), habitat-species use of three sound types. Marine Mammal Science, 21 (4): 587–602, http://dx.doi.org/10.1111/j.1748-7692.2005.tb01253.x.

    Article  Google Scholar 

  • Odell D K, McClune K M. 1999. False killer whale, Pseudorca crassidens (Owen, 1846)). In: Ridgway S H, Harrison R eds. Handbook of Marine Mammals). Academic Press, Orlando, FL). p. 213–243.

    Google Scholar 

  • Overstrom N A. 1983. Association between burst-pulse sounds and aggressive behavior in captive Atlantic bottlenosed dolphins (Tursiops truncatus). Zoo Biology, 2 (2): 93–103.

    Article  Google Scholar 

  • Owings D H, Virginia R A. 1978. Alarm calls of California ground squirrels (Spermophilus beecheyi). Zeitschrift für Tierpsychologie, 46 (1): 58–70.

    Article  Google Scholar 

  • Panksepp J, Burgdorf J. 2000. 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behavioural Brain Research, 115 (1): 25–38.

    Article  Google Scholar 

  • Polizzi di Sorrentino E, Schino G, Visalberghi E, Aureli F. 2010. What time is it? Coping with expected feeding time in capuchin monkeys. Animal Behavior, 80 (1): 117–123, http://dx.doi.org/10.1016/j.anbehav.2010.04.008.

    Article  Google Scholar 

  • Puente A E, Dewsbury D A. 1976. Courtship and copulatory behavior of bottlenose dolphins (Tursiops truncatus). Cetology, 21: 1–9.

    Google Scholar 

  • Ralston J V, Herman L M. 1989. Dolphin auditory perception). In: Doolin J R, Hulse S H eds. Complex Acoustic Perception: The Comparative Psychology of Complex Acoustic Perception). Hillsdale, NJ: Lawrence Erlbaum Associates). p.295–338.

    Google Scholar 

  • Reebs S G, Lague M. 2000. Daily food-anticipatory activity in golden shiners. A test of endogenous timing mechanisms. Physiol. Behav., 70 (1-2): 35–43.

    Google Scholar 

  • Rehn N, Filatova O A, Durban J W, Foote A D. 2011. Crosscultural and cross-ecotype production of a killer whale ‘excitement’ call suggests universality. Naturwissenschaften, 98 (1): 1–6.

    Article  Google Scholar 

  • Rehn N, Teichert S, Thomsen F. 2007. Structural and temporal emission patterns of variable pulsed calls in free-ranging killer whales (Orcinus orca). Behaviour, 144 (3): 307–329.

    Article  Google Scholar 

  • Rendall D, Cheney D L, Seyfarth R M. 2000. Proximate factors mediating ‘contact’ calls in adult female baboons (Papio cynocephalus ursinus) and their infants. Journal of Comparative Psychology, 114 (1): 36–46.

    Article  Google Scholar 

  • Rendell L E, Matthews J N, Gill A, Gordon J C D, MacDonald D W. 1999. Quantitative analysis of tonal calls from five odontocete species, examining interspecific and intraspecific variation. J. Zool., 249 (4): 403–410.

    Article  Google Scholar 

  • Reneerkens J, Piersma T, Ramenofsky M. 2002. An experimental test of the relationship between temporal variability of feeding opportunities and baseline levels of corticosterone in a shorebird. J. Exp. Zool., 293 (1): 81–88.

    Article  Google Scholar 

  • Reynolds V, Luscombe G P. 1969). Social behavior of chimpanzees in an open environment. In: Proceedings of the 1st Aeromedical Research Laboratory, Aerospace Medical Division. United States Air Force. 657p.

    Google Scholar 

  • Richelle M. 1980. Time in Animal Behavior. Pergamon Press, Oxford, UK. 273p.

    Google Scholar 

  • Ridgway S H, Moore P W, Carder D A, Romano T A. 2014. Forward shift of feeding buzz components of dolphins and belugas during associative learning reveals a likely connection to reward expectation, pleasure and brain dopamine activation. The Journal of Experimental Biology, 217 (16): 2910–2919, http://dx.doi.org/10.1242/ jeb.100511.

    Article  Google Scholar 

  • Roberts W A. 1998. Principles of Animal Cognition. McGraw-Hill, Boston. 480p.

    Google Scholar 

  • Rosenblum L A, Paully G S. 1984. The effects of varying environmental demands on maternal and infant behavior. Child Dev., 55 (1): 305–314.

    Article  Google Scholar 

  • Ruiz-Miranda C R, Wells S A, Golden R, Seidensticker J. 1998. Vocalizations and other behavioral responses of male cheetahs (Acinonyx jubatus) during experimental separation and reunion trials. Zoo Biology, 17 (1): 1–16.

    Article  Google Scholar 

  • Sánchez J A, López-Olmeda J F, Blanco-Vives B, Sánchez-Vázquez F J. 2009. Effects of feeding schedule on locomotor activity rhythms and stress response in sea bream. Physiology & Behavior, 98 (1-2): 125–129.

    Article  Google Scholar 

  • Sayigh L S, Quick N, Hastie G, Tyack P. 2013. Repeated call types in short-finned pilot whales, Globicephala macrorhynchus. Mar. Mamm. Sci., 29 (2): 312–324.

    Article  Google Scholar 

  • Scarpaci C, Bigger S W, Corkeron P J, Nugegoda D. 2000. Bottlenose dolphins, Tursiops truncatus, increase whistling in the presence of “swim-with-dolphin” operations. J. Cetacean Res. Manage., 2 (3): 183–186.

    Google Scholar 

  • Schapiro S J, Bloomsmith M A. 1994. Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys. American Journal of Primatology, 32 (3): 159–170.

    Article  Google Scholar 

  • Scheer M. 2013. Short note: call vocalizations recorded among short-finned pilot whales (Globicephala macrorhynchus) off Tenerife, Canary Islands. Aquatic Mammals, 39 (3): 306–313, http://dx.doi.org/10.1578/AM.39.3.2013.306.

    Article  Google Scholar 

  • Schön P C, Puppe B, Manteuffel G. 2004. Automated recording of stress vocalisations as a tool to document impaired welfare in pigs. Animal Welfare, 13 (2): 105–110.

    Google Scholar 

  • Schwartzkopf-Genswein K S, Stookey J M, Welford R. 1997. Behavior of cattle during hot-iron and freeze branding and the effects on subsequent handling ease. Journal of Animal Science, 75 (8): 2064–2072.

    Article  Google Scholar 

  • Sekiguchi Y, Kohshima S. 2003. Resting behaviors of captive bottlenose dolphins (Tursiops truncatus). Physiology and Behavior, 79 (4-5): 643–653, http://dx.doi.org/10.1016/S0031-9384(03)00119-7.

    Article  Google Scholar 

  • Seligman M E, Meyer B. 1970. Chronic fear and ulcers in rats as a function of the unpredictability of safety. J. Comp. Physiol. Psychol., 73 (2): 202–207, http://dx.doi.org/10. 1037/h0030219.

    Article  Google Scholar 

  • Seligman M E. 1968. Chronic fear produced by unpredictable electric shock. J. Comp. Physiol. Psychol., 66 (2): 402–411, http://dx.doi.org/10.1037/h0026355.

    Article  Google Scholar 

  • Seyfarth R M, Cheney D L. 2003a. Meaning and emotion in animal vocalizations). Annals of the New York Academy of Sciences, 1000: 32–55.

    Article  Google Scholar 

  • Seyfarth R M, Cheney D L. 2003b. Signalers and receivers in animal communication). Annual Review of Psychology, 54: 145–173.

    Article  Google Scholar 

  • Shepherdson D J, Carlstead K, Mellen J D, Seidensticker J. 1993. The influence of food presentation on the behavior of small cats in confined environments. Zoo Biology, 12 (2): 203–216.

    Article  Google Scholar 

  • Sikes R S, Gannon N W L. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92 (1): 235–253.

    Article  Google Scholar 

  • Sjare B L, Smith T G. 1986. The relationship between behavioral activity and underwater vocalizations of the white whale, Delphinapterus leucas. Can. J. Zool., 64 (12): 2824–2831.

    Article  Google Scholar 

  • Slocombe K E, Zuberbühler K. 2006. Food-associated calls in chimpanzees: responses to food types or food preferences? Animal Behavior, 72 (5): 989–999, http://dx.doi.org/10. 1016/j.anbehav.2006.01.030.

    Article  Google Scholar 

  • Slooten E. 1994. Behavior of hector’s dolphin: classifying behavior by sequence analysis. Journal of Mammology, 75 (4): 956–964.

    Article  Google Scholar 

  • Smolker R A, Mann J, Smuts B B. 1993. Use of signature whistles during separations and reunions by wild bottlenose dolphin mothers and infants. Behav. Ecol. Sociobiol., 33 (6): 393–402.

    Article  Google Scholar 

  • Spruijt B M, van den Bos R, Pijlman F T A. 2001. A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Appl. Anim. Behav. Sci., 7 (2): 145–171.

    Article  Google Scholar 

  • Stacey P J, Leatherwood S, Baird R W. 1994. Pseudorca crassidens. Mammalian Species, 456: 1–6.

    Article  Google Scholar 

  • Stewart B S, Clapham P J, Powell J A, Reeves R R. 2002). National Audubon Society). Guide to Marine Mammals of the World. Knopf, New York). 528p.

    Google Scholar 

  • Supin A Y, Nachtigall P E, Au W W L, Breese M. 2004. The interaction of outgoing echolocation pulses and echoes in the false killer whale’s auditory system: evoked-potential study. J. Acoust. Soc. Am., 115 (6): 3218–3225.

    Article  Google Scholar 

  • Supin A Y, Nachtigall P E, Au W W L, Breese M. 2005. Invariance of evoked-potential echo-responses to target strength and distance in an echolocating false killer whale: evoked potential study. J. Acoust. Soc. Am., 117 (6): 3928–3935.

    Article  Google Scholar 

  • Supin A Y, Nachtigall P E, Pawloski J L, Au W W L. 2003. Evoked potential recording during echolocation in a false killer whale Pseudorca crassidens (L). J. Acoust. Soc. Am., 113 (5): 2408–2411.

    Article  Google Scholar 

  • Tanchez E K. 2003). Factors Affecting the Diel Underwater Sound Production of Captive Belugas (Delphinapterus leucas) at the John G. Shedd Aquarium). Western Illinois University, Quad Cities, Moline). 40p.

    Google Scholar 

  • Tavolga W N. 1983. Theoretical principles for the study of communication in cetaceans. Mammalia, 47 (1): 3–26.

    Article  Google Scholar 

  • Taylor A A, Weary D M. 2000. Vocal responses of piglets to castration: Identifying procedural sources of pain. Applied Animal Behaviour Science, 70 (1): 17–26.

    Article  Google Scholar 

  • Therrien S C, Thomas J A, Therrien R E, Stacey R. 2012. Time of day and social change affect underwater sound production by bottlenose dolphins (Tursiops truncatus) at the Brookfield Zoo. Aquatic Mammals, 38 (1): 65–75, http://dx.doi.org/10.1578/AM.38.1.2012.65.

    Article  Google Scholar 

  • Thomas J, Stoermer M, Bowers C, Anderson L, Garver A. 1988. Detection abilities and signal characteristics of echolocating false killer whales (Pseudorca crassidens). In: Nachtigall P E, Moore P W B eds. Animal Sonar. Springer, US, 156: 323–328.

    Article  Google Scholar 

  • Tyack P. 1986. Whistle repertoires of two bottlenosed dolphins, Tursiops truncatus: mimicry of signature whistles? Behavioral Ecology and Sociobiology, 18 (4): 251–257.

    Article  Google Scholar 

  • Ulyan M J, Burrows A E, Buzzell C A, Raghanti M A, Marcinkiewicz J L, Phillips K A. 2006. The effects of predictable and unpredictable feeding schedules on the behavior and physiology of captive brown capuchins (Cebus apella). Applied Animal Behaviour Science, 101 (1-2): 154–160, http://dx.doi.org/10.1016/j.applanim.2006.01.010.

    Article  Google Scholar 

  • van Rooijen J. 1991. Predictability and boredom. Appl. Anim. Behav. Sci., 31 (3-4): 283–287.

    Article  Google Scholar 

  • Vinke C M, van den Bos R, Spruijt B M. 2004. Anticipatory activity and stereotypical behaviour in American mink (Mustela vison) in three housing systems differing in the amount of enrichments. Appl. Anim. Behav. Sci., 89 (1-2): 145–161, http://dx.doi.org/10.1016/j.applanim.2004.06.002.

    Article  Google Scholar 

  • von Borell E, Ladewig J. 1992. Relationship between behaviour and adrenocortical response pattern in domestic pigs. Applied Animal Behaviour Science, 34 (3): 195–206.

    Article  Google Scholar 

  • Waitt C, Buchanan-Smith H M. 2001. What time is feeding?: how delays and anticipation of feeding schedules affect stump-tailed macaque behavior. Appl. Anim. Behav. Sci., 75 (1): 75–85.

    Article  Google Scholar 

  • Waitt C, Buchanan-Smith H M. 2006. Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior. American Journal of Primatology, 68 (11): 1054–1067, http://dx.doi.org/10. 1002/ajp.20303.

    Article  Google Scholar 

  • Wallace R J. 1979. Novelty and partibility as determinants of hoarding in the albino rat. Animal Learning & Behavior, 7 (4): 549–554.

    Article  Google Scholar 

  • Wang Z T, Fang L, Shi W J, Wang K X, Wang D. 2013. Whistle characteristics of free-ranging Indo-Pacific humpback dolphins (Sousa chinensis) in Sanniang Bay, China. J. Amer. Acoust. Soc., 133 (4): 2479–2489.

    Article  Google Scholar 

  • Warris P D, Brown S N, Adams S J M. 1994. Relationships between subjective and objective assessments of stress at slaughter and meat quality in pigs. Meat Science, 38 (2): 329–430.

    Article  Google Scholar 

  • Wasserman F E, Cruikshank W W. 1983. The relationship between time of feeding and aggression in a group of captive hamadryas baboons. Primates, 24 (3): 432–435.

    Article  Google Scholar 

  • Weary D M, Braithwaite L A, Fraser D. 1998. Vocal response to pain in piglets. Applied Animal Behaviour Science, 56 (2-4): 161–172.

    Article  Google Scholar 

  • Weary D M, Fraser D. 1995. Calling by domestic piglets: reliable signals of need? Anim. Behav., 50 (4): 1047–1055.

    Article  Google Scholar 

  • Weary D M, Ross S, Fraser D. 1997. Vocalizations by isolated piglets: a reliable indicator of piglet need directed towards the sow. Applied Animal Behaviour Science, 53 (4): 249–257.

    Article  Google Scholar 

  • Weilgart L S, Whitehead H. 1990. Vocalizations of the North Atlantic pilot whales (Globicephala melas) as related to behavioral contexts. Behav. Ecol. Sociobiol., 26: 399–402.

    Article  Google Scholar 

  • Weir C R, Frantzis A, Alexiadou P, Goold J C. 2007. The burstpulse nature of ‘squeal’ sounds emitted by sperm whales (Physeter macrocephalus). Journal of the Marine Biological Association of the United Kingdom, 87 (1): 39–46.

    Article  Google Scholar 

  • Weller S H, Bennett C L. 2001. Twenty-four hour activity budgets and patterns of behavior in captive ocelots (Leopardus pardalis). Appl. Anim. Behav. Sci., 71 (1): 67–79.

    Article  Google Scholar 

  • White R G, Deshazer J A, Tressler C J, Borcher G M, Davey S, Waninge A, Parkhurst A M, Milanuk M J, Clemens E T. 1993. Vocalization and physiological response of pigs during castration with or without a local anesthetic. Journal of Animal Science, 73 (2): 381–386.

    Article  Google Scholar 

  • Wilson W L, Wilson C C. 1968). Aggressive interactions of captive chimpanzees living in a semi-free-ranging environment). Technical Report No. ARL-TR-68-9. Aeromedical Research Laboratory, Mew Mexico). p.1–10.

    Google Scholar 

  • Zar J H. 1996). Biostatistical Analysis). 3 rd edn. Prentice Hall, Englewood Cliffs, NJ). 960p.

    Google Scholar 

  • Zimmerman P H, Koene P, van Hooff J A R. 2000. Thwarting of behaviour in different contexts and the gakel-call in the laying hen. Applied Animal Behaviour Science, 69 (4): 255–264.

    Article  Google Scholar 

  • Zimmerman P H, Koene P. 1998. The effect of frustrative nonreward on vocalisations and behaviour in the laying hen, Gallus gallus domesticus. Behavioural Processes, 44 (1): 73–79.

    Article  Google Scholar 

  • Zimmerman P H, Lundberg A, Keeling L J, Koene P. 2003. The effect of an audience on the gakel-call and other frustration behaviours in the laying hen (Gallus gallus domesticus). Animal Welfare, 12 (3): 315–326.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sara Platto.

Additional information

Supported by grants from the Institute of Hydrobiology, Chinese Academy of Sciences

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Platto, S., Wang, D. & Wang, K. Variation in the emission rate of sounds in a captive group of false killer whales Pseudorca crassidens during feedings: possible food anticipatory vocal activity?. Chin. J. Ocean. Limnol. 34, 1218–1237 (2016). https://doi.org/10.1007/s00343-016-5074-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-016-5074-5

Keywords

Navigation