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In addition to decreased performance, dolphin mothers swimming in echelon were required to increase effort compared to periods of solitary swimming. For a given speed, mothers swimming in echelon significantly increased tailbeat frequency with the result that distance covered per stroke significantly decreased by 13% compared to solitary swimming (Fig. 4). Interestingly, the proportion of decreased distance per stroke in ‘infant carrying’ dolphin mothers is strikingly similar to the 17% decrease in distance per leap measured empirically for marmosets ( Callithrix jacchus) carrying weights equivalent to their newborn twin offspring (Schradin & Anzenberger 2001). Furthermore, although female wallabies carrying a load (approximating the mass of a fully developed offspring) did not alter stride frequency, they increased the time the foot applied force on the ground, which likely increased the stored elastic strain energy to levels necessary to transport the additional load (Baudinette & Biewener 1998). Regardless of habitat (aquatic vs. arboreal) or forces to overcome (hydrodynamic drag vs. gravity) in these systems maternal effort must change to support an increased load. The increase in maternal effort for dolphin mothers swimming in echelon compared to periods of solitary swimming may be associated with changes in water flow patterns and drag. The presence of the calf may disrupt the boundary flow around the mother causing it to separate, which would increase turbulent flow. In addition, the entrained calf could increase the surface area of the mother, which effectively increases the drag of the swimmer (Webb 1975). More power is required to overcome increased turbulent flow and drag (Webb 1975). As a greater proportion of maternal power output is utilized to accommodate increased turbulent flow and drag, there is less energy available to propel the animal forward. As a result, locomotor performance decreases because power output per stroke is limited by mechanical constraints (Fish & Hui 1991) and total work is limited by the animal’s metabolic scope (Weibel et al. 1987). These relationships may explain the observed decrease in swim speed and distance covered per stroke for mothers swimming in echelon position. Although Weihs (2006) suggested that the gain in forward forces by the following body (calf) is larger than the added cost to the leading body (mother), a more detailed theoretical examination of the drag and flow patterns for the leading body in echelon position is warranted to validate the hypotheses for the proposed decreased maternal performance observed in the present study. Given that infant carrying mothers must forage and evade predators, one of many constraints on newborn offspring mass may be its impact on maternal locomotor performance. As a result, newborn dolphins and marmosets represent a similar proportion of maternal mass, 15% (mass data from a mother–calf pair in this study) and 17% (Tardif, Harrison & Simek 1993), respectively. Ultimately as an infant ages and increases in size, maternal costs associated with infant carrying theoretically increase in aquatic (Weihs 2004, 2006) and arboreal (Schradin & Anzenberger 2001) environments. Optimal theory predicts that maternal carrying costs should not outweigh the sum of the costs of independent locomotion © 2007 The Author. Journal compilation © 2007 British Ecological Society, Functional Ecology, 22, 284–288 Infant carrying in dolphins 287 by the mother and her offspring (Kramer 1998). Therefore, the transition to offspring locomotor independence may represent a parent–offspring conflict (Trivers 1974) as energy expenditure to carry an infant may limit the mother’s available energy to invest in future offspring (Kramer 1998). As cetacean and primate offspring increase in size, there is an increase in the active prevention and/or avoidance of infant carrying by mothers in both groups (Altmann 1980; Taber & Thomas 1982; Mann & Smuts 1999), such that with age there is a decrease in the time cetacean infants swim in echelon (Taber & Thomas 1982; Mann & Smuts 1999; Noren & Edwards 2007) and primate infants are carried (Altmann & Samuels 1992; Salvage et al. 1996; Pontzer & Wrangham 2006). Examination of human infant carrying behaviour also suggests that by a certain mass and age, mothers encourage their infants to walk independently (Kramer 1998). In summary, this study provides the first empirical evidence of the maternal consequences of ‘infant carrying’ in an aquatic environment. Although infant carrying provides a solution for mothers that must manoeuvre within their environment while accompanied by their underdeveloped offspring, this behaviour is associated with maternal costs regardless of environment, as evident in arboreal (Schradin & Anzenberger 2001) and aquatic (present study) regimes. The decreased locomotor performance and increased locomotor effort associated with infant carrying undoubtedly impacts maternal energy budgets, foraging efficiency and predator evasion. Given the prevalence of infant carrying behaviour across diverse taxa and habitats and the consequences of this behaviour, it is surprising that the energetics of infant carrying have largely been ignored. Future investigations are warranted, particularly in a volant environment, which remains unexplored. Acknowledgments I thank Dolphin Quest, particularly J. Sweeney and R. Stone, for providing the experimental facilities and animals and for funding portions of data collection and analyses. I also thank Southwest Fisheries Science Center (SWFSC), particularly S. Reilly and E. Edwards, for funding portions of data collection. In addition, I thank the staff at Dolphin Quest Hawaii (particularly G. Biedenbach and C. Buczyna), T. Williams of the University of California Santa Cruz for the use of her Peak Motus system, and J. Redfern of SWFSC for assistance with data management. References Altmann, J. (1980) Baboon Mothers and Infants. Harvard University Press, Cambridge. Altmann, J. & Samuels, A. (1992) Costs of maternal care: infant-carrying baboons. Behavioural Ecology and Sociobiology, 29, 391–398. Au, D. & Perryman, W. (1982) Movement and speed of dolphin schools responding to an approaching ship. Fishery Bulletin, 80, 371–379. Baudinette, R.V. & Biewener, A.A. (1998) Young wallabies get a free ride. Nature, 395, 653–654. Carrier, D.R. (1996) Ontogenetic limits on locomotor performance. Physiological Zoology, 69, 467–488. Doran, D.M. (1992) The ontogeny of chimpanzee and pygmy chimpanzee locomotor behavior: a case study of paedomorphism and its behavorial correlates. Journal of Human Evolution, 23, 139–158. Fish, F.E. (1993) Power output and propulsive efficiency of swimming bottlenose dolphins ( Tursiops truncatus). Journal of Experimental Biology, 185, 179–193. Fish, F.E. & Hui, C.A. (1991) Dolphin swimming – a review. Mammal Review, 21, 181–195.
288 S. R. Noren Kelly, H.R. (1959) A two body problem in the echelon swimming of porpoise. Naval Ordinance Test Station Technical Note 40606–1. Kooyman, G.L. & Ponganis, P.J. (1998) The physiological basis for diving at depth: birds and mammals. Annual Review of Physiology 60, 19–32. Kramer, P.A. (1998) The costs of human locomotion: maternal investment in child transport. American Journal of Physical Anthropology, 107, 71–85. Lang, T.G. (1966) Hydrodynamic analysis of cetacean performance. Whales, Dolphins, and Porpoises (ed. K.S. Norris), pp. 410–432. University of California Press, Berkeley. Mann, J. & Smuts, B. (1999) Behavioral development in wild bottlenose dolphin newborns ( Tursiops sp.). Behavior, 136, 529–566. McBride, A.F. & Kritzler, H. (1951) Observations on pregnancy, parturition, and post-natal behavior in the bottlenose dolphin. Journal of Mammology, 32, 251–266. Noren, S.R. & Edwards, E.F. (2007) Physiological and behavioral development in dolphin calves: implications for calf separation and mortality due to tuna purse-seine sets. Marine Mammal Science, 23(1), 15–29. Noren, S.R., Biedenbach, G. & Edwards, E.F. (2006) The ontogeny of swim performance and mechanics in bottlenose dolphins ( Tursiops truncatus). Journal of Experimental Biology, 209(23), 4724–4731. Noren, S.R., Biedenbach, G., Redfern, J.V. & Edwards, E.F. (2008) Hitching a ride: the formation locomotion strategy of dolphin calves. Functional Ecology. doi: 10.1111/j.1365-2435.2007.01353.x. Norris, K.S. & Prescott, J.H. (1961) Observations on Pacific cetaceans of Californian and Mexican waters. University of California Publications in Zoology, 63, 291–402. Pontzer, H. & Wrangham, R.W. (2006) Ontogeny of ranging in wild chimpanzees. International Journal of Primatology, 27(1), 295–309. Rohr, J.R. & Fish, F.E. (2004) Strouhal numbers and optimization of swimming by odontocete cetaceans. Journal of Experimental Biology, 207, 1633–1642. Ross, C. (2001) Park or ride? Evolution of infant carrying in primates. International Journal of Primatology, 22(5), 749–771. Salvage, A., Snowden, P.T., Giraldo, L.H. & Soto, L.H. (1996) Parental care patterns and vigilance in wild cotton-top tamarins (Saguinus oedipus). Adaptive Radiation of Neotropical Primates (eds N.A. Norconk, A.L. Rosenberg & P.A. Garber), pp. 187–199. Plenum Press, New York. Schradin, C. & Anzenberger, G. (2001) Costs of infant carrying in common marmosets, Callithrix jacchus: an experimental analysis. Animal Behavior, 62, 289–295. Skrovan, R.C., Williams, T.M., Berry, P.S. & Moore, P.W. (1999) The diving physiology of bottlenose dolphins (Tursiops truncatus) II. Biomechanics and changes in buoyancy at depth. Journal of Experimental Biology, 202, 2749– 2761. Taber, S. & Thomas, P. (1982) Calf development and mother–calf spatial relationships in southern right whales. Animal Behaviour, 30, 1072–1083. Tardif, S.D., Harrison, M.L. & Simek, M.A. (1993) Communal infant care in marmosets and tamarins: relation to energetics, ecology, and social organization. Marmosets and Tamarins: Systematics, Behavior, and Ecology (ed. A.B. Rylands), pp. 200–219. Oxford Press, Oxford. Tavolga, M.C. & Essapian, F.S. (1957) The behavior of the bottle-nosed dolphin (Tursiops truncatus): mating, pregnancy, parturition and mother– infant behavior. Zoologica, 42, 11–31. Trivers, R. (1974) Parent-offspring conflict. American Zoologist, 14, 249–264. Webb, P.W. (1975) Hydrodynamics and energetics of fish propulsion. Bulletin of the Fisheries Research Board of Canada, 190, 1–159. Weibel, E.R., Taylor, C.R., Hoppeler, H. & Karas, R.H. (1987) Adaptive variation in the mammalian respiratory system in relation to energetic demand: I. Introduction to problem and strategy. Respiration Physiology, 69, 1–6. Weihs, D. (2004) The hydrodynamics of dolphin drafting. Journal of Biology, 3(8), 1–23 (http://jbiol.com/content/3/2/8). Weihs, D. (2006) Aerodynamic interactions between adjacent slender bodies. American Institute of Aeronautics and Astronautics Journal, 44, 481–484. Wells, J.P. & Turnquist, J.E. (2001) Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II postural and locomotor behavior and habitat use in a free-ranging colony. American Journal of Physical Anthropology, 115, 80– 94. Williams, J.M., Hsien-Yang, L. & Pusey, A.E. (2002) Costs and benefits of grouping for female chimpanzees at Gombe. Behavioural Diversity in Chimpanzees and Bonobos (ed. C. Boesch), pp. 192–203. Cambridge University Press, Cambridge. Wrangham, R.W. (2000) Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. Primate Males, Causes and Consequences of Variation in Group Composition (ed. P.M. Kaeppler), pp. 248–258. Cambridge University Press, Cambridge. Received 12 June 2007; accepted 27 September 2007 Handling Editor: Francisco Bozinovic © 2007 The Author. Journal compilation © 2007 British Ecological Society, Functional Ecology, 22, 284–288
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ECOLOGY, BEHAVIOR & CONSERVATION OF
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ABOUT BELIZE Research Site: The pro
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Ecology, Behavior & Conservation of
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2012 Field Course Policy & Liabilit
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FIELD JOURNALS You are required to
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OUR INVESTIGATION Figure 2. G. crut
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OUR INVESTIGATION Introduction The
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OUR INVESTIGATION Introduction We f
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OUR RESEARCH FINDINGS Introduction
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area on the north part of the islan
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Introduction Our Investigation Befo
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Introduction Sea stars have long be
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Introduction Lunar reproductive rhy
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2010 VT: Scholar, BANNER, Safe Zone
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presentation to Horn Point Environm
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LaCommare, Katherine S. November 20
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172 NOTES Caribbean Journal of Scie
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174 FIG. 1. Drowned Cayes study are
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176 severe event occurred in 1998 (
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Coral Reefs (1997) 16, Suppl.: S23
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Bradbury RH, Seymour RM, Antonelli
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Social Interactions in Captive Fema
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Captive Female Manatee Social Behav
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Community Structure, Population Con
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422 THE AMERICAN NATURALIST the pla
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424 THE AMERICAN NATURALIST sarily
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Environmental Conservation 29 (2):
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194 C.M. Duarte well as more recent
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202 C.M. Duarte detecting losses of
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204 C.M. Duarte Coles, R. & Fortes,
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206 C.M. Duarte Ramos-Esplá, A., M
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$1.2 million (Moore et al. 2009a).
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and positively related to knowledge
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student’s ability to learn facts
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Conservation and Behaviour Richard
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animals may adopt microhabitat choi
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decision rules they use in response
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(Halodule wrightii and Syringodium
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Diurnal and Nocturnal Scans Four of
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in 2006. Although this difference i
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manatus in Costa Rica. Biological C
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574 D. J. Semeyn et al. and natural
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580 D. J. Semeyn et al. Fig. 4 Kern
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582 D. J. Semeyn et al. biologists
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Intraspecific and geographic variat
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III. RESULTS Manatees in Florida an
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Genetica (2011) 139:833-842 DOI 10.
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Genetica (2011) 139:833-842 835 dur
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Genetica (2011) 139:833-842 837 Tab
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Genetica (2011) 139:833-842 839 Man
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Genetica (2011) 139:833-842 841 edu
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Fish Sci (2011) 77:795-798 DOI 10.1
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Fish Sci (2011) 77:795-798 797 was
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Low genetic variation and evidence
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Reduced Belize manatee dispersal an
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and respond to human encounters by
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tourist vessels are present, and th
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that approach behaviour may be habi
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to structure almost completely the
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MARINE MAMMAL SCIENCE, 27(3): 606-6
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Journal of Zoology The lesser of tw
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E. M. Arraut et al. & Sparks, 1989)
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E. M. Arraut et al. Frequent cloud
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E. M. Arraut et al. rising-water we
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E. M. Arraut et al. (Link, 1795) an
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The Journal of Experimental Biology
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Fig. 1. Rescue locations of manatee
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The present study is the first to c
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Bearhop, S., Waldron, S., Votier, S
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Table 1. Results from the GLM relat
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28
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Figure 1. Map of the Drowned Cayes
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Figure 3. Histogram of number of ma
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a. b. c. Power Power Power 100 80 6
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