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Comparative physiology of vocal musculature in two odontocetes, the bottlenose dolphin (Tursiops truncatus) and the harbor porpoise (Phocoena phocoena)

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Abstract

The mechanism by which odontocetes produce sound is unique among mammals. To gain insight into the physiological properties that support sound production in toothed whales, we examined myoglobin content ([Mb]), non-bicarbonate buffering capacity (β), fiber-type profiles, and myosin heavy chain expression of vocal musculature in two odontocetes: the bottlenose dolphin (Tursiops truncatus; n = 4) and the harbor porpoise (Phocoena phocoena; n = 5). Both species use the same anatomical structures to produce sound, but differ markedly in their vocal repertoires. Tursiops produce both broadband clicks and tonal whistles, while Phocoena only produce higher frequency clicks. Specific muscles examined in this study included: (1) the nasal musculature around the phonic lips on the right (RNM) and left (LNM) sides of the head, (2) the palatopharyngeal sphincter (PPS), which surrounds the larynx and aids in pressurizing cranial air spaces, and (3) the genioglossus complex (GGC), a group of muscles positioned ventrally within the head. Overall, vocal muscles had significantly lower [Mb] and β than locomotor muscles from the same species. The PPS was predominately composed of small diameter slow-twitch fibers. Fiber-type and myosin heavy chain analyses revealed that the GGC was comprised largely of fast-twitch fibers (Tursiops: 88.6%, Phocoena: 79.7%) and had the highest β of all vocal muscles. Notably, there was a significant difference in [Mb] between the RNM and LNM in Tursiops, but not Phocoena. Our results reveal shared physiological characteristics of individual vocal muscles across species that enhance our understanding of key functional roles, as well as species-specific differences which appear to reflect differences in vocal capacities.

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References

  • Amundin M, Andersen SH (1983) Bony nares air pressure and nasal plug muscle activity during click production in the harbour porpoise, Phocoena phocoena, and the bottlenosed dolphin, Tursiops truncatus. J Exp Biol 105:275–282

    Google Scholar 

  • Au WWL, Kastelein RA, Benoit-Bird KJ et al (2006) Acoustic radiation from the head of echolocating harbor porpoises (Phocoena phocoena). J Exp Biol 209:2726–2733. doi:10.1242/jeb.02306

    Article  PubMed  Google Scholar 

  • Blessing MH (1972) Studies on the concentration of myoglobin in the sea-cow and porpoise. Comp Biochem Physiol Part A 41:475–480. doi:10.1016/0300-9629(72)90005-9

    Article  CAS  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Sound production. Princ. Anim. Commun. Sinauer Associates, Inc., Sunderland, pp 75–112

    Google Scholar 

  • Burns JM, Castellini MA (1996) Physiological and behavioral determinants of the aerobic dive limit in Weddell seal (Leptonychotes weddellii) Pups. J Comp Physiol B 166:473–483. doi:10.1007/BF02338290

    Article  Google Scholar 

  • Cartwright R, Newton C, West KM et al (2016) Tracking the development of muscular myoglobin stores in mysticete calves. PLoS One 11:1–18. doi:10.1371/journal.pone.0145893

    Article  Google Scholar 

  • Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J Comp Physiol B 143:191–198

    CAS  Google Scholar 

  • Castellini MA, Kooyman GL, Ponganis PJ (1992) Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J Exp Biol 165:181–194

    CAS  PubMed  Google Scholar 

  • Cobb MA, Schutt WA, Petrie JL, Hermanson JW (1994) Neonatal development of the diaphragm of the horse, Equus caballus. Anat Rec 238:311–316

    Article  CAS  PubMed  Google Scholar 

  • Cotten PB, Piscitelli MA, McLellan WA et al (2008) The gross morphology and histochemistry of respiratory muscles in bottlenose dolphins, Tursiops truncatus. J Morphol 269:1520–1538. doi:10.1002/jmor.10668

    Article  PubMed  PubMed Central  Google Scholar 

  • Cranford TW, Amundin M, Norris KS (1996) Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J Morphol 228:223–285. doi:10.1002/(SICI)1097-4687(199606)228:3<223::AID-JMOR1>3.0.CO;2-3

    Article  CAS  PubMed  Google Scholar 

  • Cranford TW, Elsberry WR, Van Bonn WG et al (2011) Observation and analysis of sonar signal generation in the bottlenose dolphin (Tursiops truncatus): evidence for two sonar sources. J Exp Mar Bio Ecol 407:81–96. doi:10.1016/j.jembe.2011.07.010

    Article  Google Scholar 

  • Dearolf JL (2002) Morphology and development of the diaphragm of bottlenose dolphins (Tursiops trunatus). Cornell University, Ithaca

    Google Scholar 

  • Dearolf JL (2003) Diaphragm muscle development in bottlenose dolphins (Tursiops truncatus). J Morphol 256:79–88. doi:10.1002/jmor.10077

    Article  CAS  PubMed  Google Scholar 

  • Dearolf JL, McLellan WA, Dillaman RM et al (2000) Precocial development of axial locomotor muscle in bottlenose dolphins (Tursiops truncatus). J Morphol 244:203–215. doi:10.1002/(SICI)1097-4687(200006)244:3<203::AID-JMOR5>3.0.CO;2-V

    Article  CAS  PubMed  Google Scholar 

  • Dolar MLL, Suarez P, Ponganis PJ, Kooyman GL (1999) Myoglobin in pelagic small cetaceans. J Exp Biol 202:227–236

    CAS  PubMed  Google Scholar 

  • Dormer KJ (1979) Mechanism of sound production and air recycling in delphinids: cineradiographic evidence. J Acoust Soc Am 65:229–239. doi:10.1121/1.382240

    Article  Google Scholar 

  • Elemans CPH, Mead AF, Rome LC, Goller F (2008) Superfast vocal muscles control song production in songbirds. PLoS One 3:6–11. doi:10.1371/journal.pone.0002581

    Article  Google Scholar 

  • Elemans CPH, Mead AF, Jakobsen L, Ratcliffe JM (2011) Superfast muscles set maximum call rate in echolocating bats. Science 333:1885–1888. doi:10.1126/science.1207309

    Article  CAS  PubMed  Google Scholar 

  • Gillooly JF, Ophir AG (2010) The energetic basis of acoustic communication. Proc R Soc B 277:1325–1331. doi:10.1098/rspb.2009.2134

    Article  PubMed  PubMed Central  Google Scholar 

  • Green RF, Ridgway SH, Evans WE (1980) Functional and descriptive anatomy of the bottlenosed dolphin nasolaryngeal system with special reference to the musculature associated with sound production. Anim. Sonar Syst. Springer US, pp 199–228

  • Harrison LK, Davis RW (1998) Heterogeneity of myoglobin in cetacean swimming muscles. In: The world marine mammal science conference, Monaco, 20–24 January 1998, p 60

  • Hermanson J, Evans H (1993) The muscular system. Miller’s Anat. Dog. W.B. Saunders, Philadelphia, pp 258–384

    Google Scholar 

  • Hermanson JW, Hurley KJ (1990) Architectural and histochemical analysis of the biceps brachii muscle of the horse. Acta Anat (Basel) 137:146–156. doi:10.1017/CBO9781107415324.004

    Article  CAS  Google Scholar 

  • Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395:5–20. doi:10.3354/meps08353

    Article  Google Scholar 

  • Holt MM, Noren DP, Dunkin RC, Williams TM (2015) Vocal performance affects metabolic rate in dolphins: implications for animals communicating in noisy environments. J Exp Biol 2:1–8. doi:10.1242/jeb.122424

    Google Scholar 

  • Houser DS, Finneran J, Carder D et al (2004) Structural and functional imaging of bottlenose dolphin (Tursiops truncatus) cranial anatomy. J Exp Biol 207:3657–3665. doi:10.1242/jeb.01207

    Article  PubMed  Google Scholar 

  • Hückstädt LA, Tift MS, Riet-Sapriza F et al (2016) Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lion (Otaria byronia). J Exp Biol 219:2320–2330. doi:10.1242/jeb.138677

    Article  PubMed  Google Scholar 

  • Huggenberger S, Rauschmann MA, Oelschläger HHA (2008) Functional morphology of the hyolaryngeal complex of the harbor porpoise (Phocoena phocoena): implications for its role in sound production and respiration. Anat Rec 291:1262–1270. doi:10.1002/ar.20745

    Article  Google Scholar 

  • Huggenberger S, Rauschmann MA, Vogl TJ, Oelschläger HHA (2009) Functional morphology of the nasal complex in the harbor porpoise (Phocoena phocoena L.). Anat Rec 292:902–920. doi:10.1002/ar.20854

    Article  Google Scholar 

  • Kanatous SB, Dimichele LV, Cowan DF, Davis RW (1999) High aerobic capacities in the skeletal muscles of pinnipeds: adaptations to diving hypoxia. J Appl Physiol 86:1247–1256

    Article  CAS  PubMed  Google Scholar 

  • Kielhorn CE, Dillaman RM, Kinsey ST et al (2013) Locomotor muscle profile of a deep (Kogia breviceps) versus shallow (Tursiops truncatus) diving cetacean. J Morphol 274:663–675. doi:10.1002/jmor.20124

    Article  CAS  PubMed  Google Scholar 

  • Kooyman GL (1989) Diverse divers. Springer, New York

    Book  Google Scholar 

  • Kuhn M, Weston S, Wing J, Forester J (2013) The contrast package

  • LaFramboise WA, Daood MJ, Guthrie RD et al (1991) Emergence of the mature myosin phenotype in the rat diaphragm muscle. Dev Biol 144:1–15

    Article  CAS  PubMed  Google Scholar 

  • Lammers MO, Castellote M (2009) The beluga whale produces two pulses to form its sonar signal. Biol Lett 5:297–301. doi:10.1098/rsbl.2008.0782

    Article  PubMed  PubMed Central  Google Scholar 

  • Lawrence B, Schevill WE (1956) The functional anatomy of the delphinid nose. Bull Mus Comp Zool 114:103–182

  • Lawrence B, Schevill WE (1965) Gular musculature in delphinids. Bull Mus Comp Zool Harvard Univ 133:1–65

    Google Scholar 

  • Liste F, Palacio J, Ribes V et al (2006) Anatomic and computed tomographic atlas of the head of the newborn bottlenose dolphin (Tursiops truncatus). Vet Radiol Ultrasound 47:453–460. doi:10.1111/j.1740-8261.2006.00167.x

    Article  PubMed  Google Scholar 

  • Liu Y, Jia S, Hou Y (2009) Effects of ovariectomy on rat genioglossal muscle contractile properties and fiber-type distribution. Angle Orthod 79:509–514. doi:10.2319/031608-149.1

    Article  PubMed  Google Scholar 

  • Madsen PT, Wisniewska DM, Beedholm K (2010) Single source sound production and dynamic beam formation in echolocating harbour porpoises (Phocoena phocoena). J Exp Biol 213:3105–3110. doi:10.1242/jeb.044420

    Article  CAS  PubMed  Google Scholar 

  • Madsen PT, Lammers M, Wisniewska D, Beedholm K (2013) Nasal sound production in echolocating delphinids (Tursiops truncatus and Pseudorca crassidens) is dynamic, but unilateral: clicking on the right side and whistling on the left side. J Exp Biol 216:4091–4102. doi:10.1242/jeb.091306

    Article  PubMed  Google Scholar 

  • Marsh RL, Taigen TL (1987) Properties enhancing aerobic capacity of calling muscles in gray tree frogs Hyla versicolor. Am J Physiol 252:R786–R793

    Article  CAS  PubMed  Google Scholar 

  • Mead JG (1975) Anatomy of the external nasal passages and facial complex in the Delphinidae (Mammalia: Cetacea). Smithson Contrib to Zool 1–72. doi:10.5479/si.00810282.207

  • Melcón ML, Cummins AJ, Kerosky SM et al (2012) Blue whales respond to anthropogenic noise. PLoS One 7:1–6. doi:10.1371/journal.pone.0032681

    Article  Google Scholar 

  • Mu L, Sanders I (2002) Muscle fiber-type distribution pattern in the human cricopharyngeus muscle. Dysphagia 17:87–96. doi:10.1007/s00455-001-0108-2

    Article  PubMed  Google Scholar 

  • Noren SR (2004) Buffering capacity of the locomotor muscle in cetaceans: correlates with postpartum development, dive duration, and swim performance. Mar Mammal Sci 20:808–822. doi:10.1111/j.1748-7692.2004.tb01194.x

    Article  Google Scholar 

  • Noren SR, Williams TM (2000) Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp Biochem Physiol A 126:181–191. doi:10.1016/S1095-6433(00)00182-3

    Article  CAS  Google Scholar 

  • Noren SR, Williams TM, Pabst DA et al (2001) The development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence. J Comp Physiol B 171:127–134. doi:10.1007/s003600000161

  • Noren SR, Lacave G, Wells RS, Williams TM (2002) The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity. J Zool Lond 258:105–113. doi:10.1017/S0952836902001243

    Article  Google Scholar 

  • Noren DP, Holt MM, Dunkin RC, Williams TM (2013) The metabolic cost of communicative sound production in bottlenose dolphins (Tursiops truncatus). J Exp Biol 216:1624–1629. doi:10.1242/jeb.083212

    Article  PubMed  Google Scholar 

  • Noren SR, Noren DP, Gaydos JK (2014) Living in the fast lane: rapid development of the locomotor muscle in immature harbor porpoises (Phocoena phocoena). J Comp Physiol B 184:1065–1076. doi:10.1007/s00360-014-0854-8

    Article  PubMed  Google Scholar 

  • Ophir AG, Schrader SB, Gillooly JF (2010) Energetic cost of calling: general constraints and species-specific differences. J Evol Biol 23:1564–1569. doi:10.1111/j.1420-9101.2010.02005.x

    Article  CAS  PubMed  Google Scholar 

  • Pattengale PK, Holloszy JO (1967) Augmentation by a program of skeletal muscle myoglobin of treadmill running. Am J Physiol 213:783–785

    CAS  PubMed  Google Scholar 

  • Petrof BJ, Kelly AM, Rubinstein NA, Pack AI (1992) Effect of hypothyroidism on myosin heavy chain expression in rat pharyngeal dilator muscles. J Appl Physiol 73:179–187

    Article  CAS  PubMed  Google Scholar 

  • Piscitelli MA, McLellan WA, Rommel SA et al (2010) Lung size and thoracic morphology in shallow- and deep-diving cetaceans. J Morphol 271:654–673. doi:10.1002/jmor.10823

    PubMed  Google Scholar 

  • Ponganis PJ (2011) Diving mammals. Compr Physiol 1:517–535. doi:10.1002/cphy.c091003

    Google Scholar 

  • Ponganis PJ, Pierce RW (1978) Muscle metabolic profiles and fiber-type composition in some marine mammals. Comp Biochem Physiol 59:7–10

    Google Scholar 

  • Ponganis PJ, Costello ML, Starke LN et al (1997) Structural and biochemical characteristics of locomotory muscles of emperor penguins, Aptenodytes forsteri. Respir Physiol 109:73–80

    Article  CAS  PubMed  Google Scholar 

  • Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145

    CAS  PubMed  Google Scholar 

  • Richmond JP, Burns JM, Rea LD (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 176:535–545. doi:10.1007/s00360-006-0076-9

    Article  PubMed  Google Scholar 

  • Ridgway SH, Carder DA, Green RF et al (1980) Electromyographic and pressure events in the nasolaryngeal system of dolphins during sound production. In: Busnel R, Fish JF (eds) Anim. Sonar Syst. Plenum Press, New York, pp 239–250

    Chapter  Google Scholar 

  • Ridgway SH, Carder DA, Kamolnick T et al (2001) Hearing and whistling in the deep sea: depth influences whistle spectra but does not attenuate hearing by white whales (Delphinapterus leucas) (Odontoceti, Cetacea). J Exp Biol 204:3829–3841

    CAS  PubMed  Google Scholar 

  • Ridgway S, Samuelson Dibble D, Van Alstyne K, Price D (2015) On doing two things at once: dolphin brain and nose coordinate sonar clicks, buzzes and emotional squeals with social sounds during fish capture. J Exp Biol 218:3987–3995. doi:10.1242/jeb.130559

    Article  PubMed  Google Scholar 

  • Rome LC (2006) Design and function of superfast muscles: new insights into the physiology of skeletal muscle. Ann Rev Physiol 68:193–221. doi:10.1146/annurev.physiol.68.040104.105418

    Article  CAS  Google Scholar 

  • Rome LC, Syme DA, Hollingworth S et al (1996) The whistle and the rattle: the design of sound producing muscles. Proc Natl Acad Sci USA 93:8095–8100. doi:10.1073/pnas.93.15.8095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saigusa H, Niimi S, Yamashita K et al (2001) Morphological and histochemical studies of the genioglossus muscle. Ann Otol Rhinol Laryngol 110:779–784

    Article  CAS  PubMed  Google Scholar 

  • Sassoon DA, Gray GE, Kelley DB (1987) Androgen regulation of muscle fiber type in the sexually dimorphic larynx of Xenopus laevis. J Neurosci 7:3198–3206

    CAS  PubMed  Google Scholar 

  • Schiaffino S, Gorza L, Ausoni S, Bottinelli R, Reggiani C, Larson L, Edstrom L, Gundersen K, Lomo T (1990) Muscle fiber types expressing different myosin heavy chain isoforms. Their functional properties and adaptive capacity. In: Schiaffino S, Gorza L, Ausoni S (eds) The dynamic state of muscle fibers: proceedings of the international symposium. Walter de Gruyter, Berlin, pp 329–341

  • Schrøder HD, Reske-Nielsen E (1983) Fiber types in the striated urethral and anal sphincters. Acta Neuropathol 60:278–282

    Article  PubMed  Google Scholar 

  • Shero MR, Andrews RD, Lestyk KC, Burns JM (2012) Development of the aerobic dive limit and muscular efficiency in northern fur seals (Callorhinus ursinus). J Comp Physiol B 182:425–436. doi:10.1007/s00360-011-0619-6

    Article  CAS  PubMed  Google Scholar 

  • Smith KK (1989) Histological demonstration of muscle spindles in the tongue of the rat. Arch Oral Biol 34:529–534. doi:10.1016/0003-9969(89)90091-5

    Article  CAS  PubMed  Google Scholar 

  • Sutlive TG, McClung JR, Goldberg SJ (1999) Whole-muscle and motor-unit contractile properties of the styloglossus muscle in rat. J Neurophysiol 82:584–592

    Article  CAS  PubMed  Google Scholar 

  • Sutlive TG, Shall MS, McClung JR, Goldberg SJ (2000) Contractile properties of the tongue’s genioglossus muscle and motor units in the rat. Muscle Nerve 23:416–425

  • Turner DL, Butler PJ (1988) The aerobic capacity of locomotory muscles in the tufted duck, Aythya fuligula. J Exp Biol 135:445–460

    CAS  PubMed  Google Scholar 

  • Tyack PL, Miller EH (2002) Vocal anatomy, acoustic communication and echolocation. In: Hoelzel AR (ed) Mar. Mammal Biol. an Evol. Approach, 1st edn. Blackwell Science Ltd, Malden, pp 142–184

    Google Scholar 

  • Velten BP, Dillaman RM, Kinsey ST et al (2013) Novel locomotor muscle design in extreme deep-diving whales. J Exp Biol 216:1862–1871. doi:10.1242/jeb.081323

    Article  CAS  PubMed  Google Scholar 

  • Villegas-Amtmann S, Costa DP (2010) Oxygen stores plasticity linked to foraging behaviour and pregnancy in a diving predator, the Galapagos sea lion. Funct Ecol 24:785–795. doi:10.1111/j.1365-2435.2009.01685.x

    Article  Google Scholar 

  • Villegas-Amtmann S, Atkinson S, Paras-Garcia A, Costa DP (2012) Seasonal variation in blood and muscle oxygen stores attributed to diving behavior, environmental temperature and pregnancy in a marine predator, the California sea lion. Comp Biochem Physiol A 162:413–420. doi:10.1016/j.cbpa.2012.04.019

    Article  CAS  Google Scholar 

  • Weilgart LS (2007) The impacts of anthropogenic ocean noise on cetaceans and implications for management. Can J Zool 85:1091–1116. doi:10.1139/Z07-101

    Article  Google Scholar 

  • Weise MJ, Costa DP (2007) Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. J Exp Biol 210:278–289. doi:10.1242/jeb.02643

    Article  PubMed  Google Scholar 

  • Werth AJ (2007) Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat Rec 290:546–568. doi:10.1002/ar.20538

    Article  Google Scholar 

  • Williams TM (1999) The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Philos Trans R Soc Lond B 354:193–201

    Article  Google Scholar 

  • Williams TM, Friedl WA, Haun JE (1993) The physiology of bottlenose dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentration during exercise. J Exp Biol 179:31–46

    CAS  PubMed  Google Scholar 

  • Williams CT, Sheriff MJ, Schmutz JA et al (2011a) Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator. J Comp Physiol B 181:1101–1109. doi:10.1007/s00360-011-0593-z

    Article  PubMed  Google Scholar 

  • Williams TM, Noren SR, Glenn M (2011b) Extreme physiological adaptations as predictors of climate-change sensitivity in the narwhal, Monodon monoceros. Mar Mammal Sci 27:334–349. doi:10.1111/j.1748-7692.2010.00408.x

    Article  Google Scholar 

  • Yeates LC, Williams TM, Fink TL (2007) Diving and foraging energetics of the smallest marine mammal, the sea otter (Enhydra lutris). J Exp Biol 210:1960–1970. doi:10.1242/jeb.02767

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Joy Reidenberg, Ted Cranford, Bill McLellan, Ann Pabst, Mario Muscedere, Sarah McHugh, Megan Murphy, and Adrienne White, as well as the Long Marine Lab Marine Mammal Stranding Network, the Marine Mammal Center, the UNCW Stranding Network, and the Southwest Fisheries Science Center. This research was conducted under NMFS Scientific Research Permit #19590 to TMW, and NOAA Parts Authorization 110314 to RCD.

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Correspondence to Nicole M. Thometz.

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This research was supported by the Office of Naval Research (N000141410460 to TMW and RCD; and N0001416IP00023, N0001415IP00039, and N0001414IP20045 to DPN and MMH).

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Communicated by G. Heldmaier.

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Thometz, N.M., Dearolf, J.L., Dunkin, R.C. et al. Comparative physiology of vocal musculature in two odontocetes, the bottlenose dolphin (Tursiops truncatus) and the harbor porpoise (Phocoena phocoena). J Comp Physiol B 188, 177–193 (2018). https://doi.org/10.1007/s00360-017-1106-5

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