Individual voices in a cluttered soundscape: acoustic ecology of the Bocon toadfish, Amphichthys cryptocentrus

  • Erica Staaterman
  • Simon J. Brandl
  • Michelle Hauer
  • Jordan M. Casey
  • Austin J. Gallagher
  • Aaron N. Rice
Article

Abstract

Toadfishes (family Batrachoididae) are a well-studied family of soniferous fishes, yet only a fraction of species within the family have been recorded, and only few detailed descriptions of calls exist. Here, we present the first description of the acoustic ecology of Amphyichtys cryptocentrus, a new-world toadfish species, distributed across the southern Caribbean Sea. We recorded fourteen individuals in a seagrass habitat over six nights in the Bocas del Toro Archipelago. Like other toadfishes, A. cryptocentrus produces compound calls with broadband and tonal components; a typical call contains 1–2 grunts, followed by 1–2 boops (average fundamental frequency = 112 Hz, average source level = 138 dB re:1 μPa RMS). While we observed relatively low between-individual variation in frequency components, our results show that individuals can be readily identified based on their call composition and call rate. This suggests that each toadfish has an individual “voice,” which may transmit selection-linked information to females about body condition, status, or motivation to mate. We also observed that toadfish produced grunts during neighbors’ calls, a previously-described aggressive behavior called “acoustic tagging”, which can intercept a potential rival’s mating advertisement. Our findings suggest that A. cryptocentrus (and its population in Bocas del Toro, in particular) represents a useful system for the study of fish bioacoustics and behavioral ecology, and we demonstrate that acoustic communication represents a major aspect of social behavior in coral reef fishes.

Keywords

Toadfish Batrachoididae Acoustic communication Sound propagation Individual recognition 

Notes

Acknowledgements

We thank the team at the Bocas del Toro research station, the students in the 2016 Three Seas Program, and Matt Ogburn and Denise Breitburg for their support with this project. We also appreciate the thoughtful suggestions from Michael Fine and one anonymous reviewer, which helped improve the analysis and quality of the manuscript. This research was conducted under permit # SE/AP-2-16 and STRI IACUC approval 2016-0101-2019. The Smithsonian MarineGEO Post-doctoral fellowships supported E. Staaterman and S. Brandl, Smithsonian Tropical Research Institute’s visiting research fellowship supported A. Gallagher, and Smithsonian Environmental Research Center’s internship program supported M. Hauer.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in this study were in accordance with the ethical standards of the Smithsonian Tropical Research Institute. This research was conducted under permit # SE/AP-2-16 and STRI IACUC approval 2016–0101-2019.

References

  1. Amorim MCP, Vasconcelos RO (2006) Individuality in the mating call of the male Lusitanian toadfish (Halobatrachus didactylus). Razprave IV Razreda Sazu 47:237–244Google Scholar
  2. Amorim MCP, Vasconcelos RO (2008) Variability in the mating calls of the Lusitanian toadfish Halobatrachus didactylus: cues for potential individual recognition. J Fish Biol 73:1–17.  https://doi.org/10.1111/j.1095-8649.2008.01974.x CrossRefGoogle Scholar
  3. Amorim MCP, Simões JM, Fonseca PJ (2008) Acoustic communication in the Lusitanian toadfish, Halobatrachus didactylus: evidence for an unusual large vocal repertoire. J Mar Biol Assoc UK 88:1069–1073.  https://doi.org/10.1017/S0025315408001677 CrossRefGoogle Scholar
  4. Amorim MCP, Simões JM, Almada VC, Fonseca PJ (2011) Stereotypy and variation of the mating call in the Lusitanian toadfish, Halobatrachus didactylus. Behav Ecol Sociobiol 65:707–716.  https://doi.org/10.1007/s00265-010-1072-3 CrossRefGoogle Scholar
  5. Barimo JF, Fine ML (1998) Relationship of the swim-bladder shape to the directionality pattern of underwater sound in the oyster toadfish. Can J Zool 76:134–143.  https://doi.org/10.1139/z97-160 CrossRefGoogle Scholar
  6. Bass AH, Baker R (1991) Evolution of homologous vocal control traits. Brain Behav Evol 38:240–254.  https://doi.org/10.1159/000114391 CrossRefPubMedGoogle Scholar
  7. Bass AH, Clark CW (2003) The physical acoustics of underwater sound communication. In: Simmons AM, Fay RR, Popper AN (eds) Acoustic communication vol 16. Springer, New York, pp 15–64.  https://doi.org/10.1007/0-387-22762-8_2 CrossRefGoogle Scholar
  8. Bass AH, McKibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog Neurobiol 69:1–26.  https://doi.org/10.1016/S0301-0082(03)00004-2 CrossRefPubMedGoogle Scholar
  9. Bass AH, Rice AN (2010) Vocal-acoustic communication in fishes: neuroethology. In: Breed MD, Moore J (eds) Encyclopedia of animal behavior. Academic Press, Oxford, pp 558–567.  https://doi.org/10.1016/B978-0-08-045337-8.00274-6 CrossRefGoogle Scholar
  10. Bass AH, Marchaterre MA, Baker R (1994) Vocal-acoustic pathways in a teleost fish. J Neurosci 14:4025–4039CrossRefPubMedGoogle Scholar
  11. Bass AH, Gilland EH, Baker R (2008) Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. Science 321:417–421.  https://doi.org/10.1126/science.1157632 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bee MA, Gerhardt C (2001) Neighbour-stranger discrimination by territorial male bullfrogs (Rana catesbeiana): II. Perceptual basis. Anim Behav 62:1141–1150CrossRefGoogle Scholar
  13. Beecher MD (1989) Signalling systems for individual recognition: an information theory approach. Anim Behav 38:248–261.  https://doi.org/10.1016/S0003-3472(89)80087-9 CrossRefGoogle Scholar
  14. Bioacoustics Research Program (2012) Raven Pro 1.4: Interactive Sound Analysis Software. Cornell Lab of Ornithology. Available at: http://www.birds.cornell.edu/brp/raven/RavenOverview.html, Ithaca, NY
  15. Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96:213–232.  https://doi.org/10.1111/j.1439-0310.1994.tb01011.x CrossRefGoogle Scholar
  16. Chagnaud BP, Bass AH (2014) Vocal behavior and vocal central pattern generator organization diverge among toadfishes. Brain Behav Evol 84:51–65.  https://doi.org/10.1159/000362916 CrossRefPubMedGoogle Scholar
  17. Chagnaud BP, Baker R, Bass AH (2011) Vocalization frequency and duration are coded in separate hindbrain nuclei. Nat Commun 2:346.  https://doi.org/10.1038/Ncomms1349 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Collette BB (2002) Order Batrachoidiformes, Batrachoididae, Toadfishes. In: K.E. Carpenter (ed.) The living marine resources of the Western Central Atlantic Vol. 2, Bony fishes. Pt. 1 Acipenseridae to Grammatidae. Food and Agriculture Organization of the United Nations, Rome, pp 1026–1042Google Scholar
  19. Cox TF, Cox MA (2000) Multidimensional Scaling, Second Edition. Chapman & Hall/CRC Press, Boca RatonCrossRefGoogle Scholar
  20. dos Santos ME, Modesto T, Matos RJ, Grober MS, Oliviera RF, Canário A (2000) Sound production by the Lusitanian toadfish, Halobatrachus didactylus. Bioacoustics 10:309–321.  https://doi.org/10.1080/09524622.2000.9753440 CrossRefGoogle Scholar
  21. Edds-Walton PL, Mangiamele LA, Rome LC (2002) Variations of pulse repetiiton rate in boatwhistle sounds from oyster toadfish Opsanus tau around Waquoit Bay, Massachusetts. Bioacoustics 13:153–173.  https://doi.org/10.1080/09524622.2002.9753493 CrossRefGoogle Scholar
  22. Fine ML (1978) Seasonal and geographical variation of the mating call of the oyster toadfish Opsanus tau L. Oecologia 36:45–57.  https://doi.org/10.1007/BF00344570 CrossRefPubMedGoogle Scholar
  23. Fine ML, Lenhardt ML (1983) Shallow-water propagation of the toadfish mating call. Comp Biochem Physiol A 76:225–231.  https://doi.org/10.1016/0300-9629(83)90319-5 CrossRefPubMedGoogle Scholar
  24. Fine ML, Thorson RF (2008) Use of passive acoustics for assessing behavioral interactions in individual toadfish. Trans Am Fish Soc 137:627–637.  https://doi.org/10.1577/T04-134.1 CrossRefGoogle Scholar
  25. Fine ML, Waybright TD (2015) Grunt variation in the oyster toadfish Opsanus tau: effect of size and sex. PeerJ 3:e1330.  https://doi.org/10.7717/peerj.1330 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Fine ML, Malloy KL, King CB, Mitchell SL, Cameron TM (2001) Movement and sound generation by the toadfish swimbladder. J Comp Physiol A 187:371–379.  https://doi.org/10.1007/s003590100209 CrossRefPubMedGoogle Scholar
  27. Fish JF (1972) The effect of sound playback on the toadfish. In: Winn HE, Olla BL (eds) Behavior of Marine Animals, Vol 2. Plenum Press, New York, p 386–434CrossRefGoogle Scholar
  28. Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42:615–635.  https://doi.org/10.1016/s0003-3472(05)80245-3 CrossRefGoogle Scholar
  29. Gower JC, Legendre P (1986) Metric and Euclidean properties of dissimilarity coefficients. J Classif 3:5–48.  https://doi.org/10.1007/bf01896809 CrossRefGoogle Scholar
  30. Granado AA, Gonzalez LW (1988) Aspectos biológicos del sapo bocón, Amphichthys cryptocentrus (Valenciennes, 1837) (Teleostei: Batrachoididae) de las islas Margarita y Cubagua, Venezuela. Investig Pesq 52:215–236Google Scholar
  31. Gray GA, Winn HE (1961) Reproductive ecology and sound production of the toadfish, Opsanus tau. Ecology 42:274–282.  https://doi.org/10.2307/1932079 CrossRefGoogle Scholar
  32. Greenfield DW, Winterbottom R, Collette BB (2008) Review of the toadfish genera (Teleostei: Batrachoididae). Proc Cal. Acad Sci 59:665–710Google Scholar
  33. Hoffman SG, Robertson DR (1983) Foraging and reproduction of two Caribbean reef toadfishes (Batrachoididae). Bull Mar Sci 33:919–927Google Scholar
  34. Mann DA, Ma W-LD, Lobel PS (2002) Sound production by the toadfish Sanopus astrifer. J Acoust Soc Am 112:2202–2203.  https://doi.org/10.1121/1.4778666 CrossRefGoogle Scholar
  35. McKibben JR, Bass AH (1998) Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. J Acoust Soc Am 104:3520–3533.  https://doi.org/10.1121/1.423938 CrossRefPubMedGoogle Scholar
  36. McKibben JR, Bass AH (2001) Effects of temporal envelope modulation on acoustic signal recognition in a vocal fish, the plainfin midshipman. J Acoust Soc Am 109:2934–2943.  https://doi.org/10.1121/1.1373441 CrossRefPubMedGoogle Scholar
  37. Mensinger AF (2014) Disruptive communication: stealth signaling in the toadfish. J Exp Biol 217:344–350.  https://doi.org/10.1242/jeb.090316 CrossRefPubMedGoogle Scholar
  38. Mitchell S, Poland J, Fine ML (2008) Does muscle fatigue limit advertisement calling in the oyster toadfish Opsanus tau? Anim Behav 76:1011–1016.  https://doi.org/10.1016/j.anbehav.2008.03.024 CrossRefGoogle Scholar
  39. Mosharo KK, Lobel PS (2012) Acoustic signals of two toadfishes from Belize: Sanopus astrifer and Batrachoides gilberti (Batrachoididae). Environ Biol Fish 94:623–638.  https://doi.org/10.1007/s10641-011-9969-x CrossRefGoogle Scholar
  40. Myrberg AA, Riggio RJ (1985) Acoustically mediated individual recognition by a coral reef fish (Pomacentrus partitus). Anim Behav 33:411–416.  https://doi.org/10.1016/S0003-3472(85)80065-8 CrossRefGoogle Scholar
  41. Rice AN, Bass AH (2009) Novel vocal repertoire and paired swimbladders of the three-spined toadfish, Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae. J Exp Biol 212:1377–1391.  https://doi.org/10.1242/jeb.028506 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Rice AN, Morano JL, Hodge KB, Muirhead CA (2016) Spatial and temporal patterns of toadfish and black drum chorusing activity in the South Atlantic bight. Environ Biol Fish 99:705–716.  https://doi.org/10.1007/s10641-016-0511-z CrossRefGoogle Scholar
  43. Rome LC (2006) Design and function of superfast muscles: new insights into the physiology of skeletal muscle. Annu Rev Physiol 68:193–221.  https://doi.org/10.1146/annurev.physiol.68.040104.105418 CrossRefPubMedGoogle Scholar
  44. Shaw KL, Herlihy DP (2000) Acoustic preference functions and song variability in the Hawaiian cricket Laupala cerasina. Proc R Soc B 267:577–584.  https://doi.org/10.1098/rspb.2000.1040 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Skoglund CR (1961) Functional analysis of swim-bladder muscles engaged in sound production of the toadfish. J Biophys Biochem Cytol 10:187–200.  https://doi.org/10.1083/jcb.10.4.187 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Staaterman E, Ogburn MB, Altieri AH, Brandl SJ, Whippo R, Seemann J, Goodison M, Duffy JE (2017) Bioacoustic measurements complement visual biodiversity surveys: preliminary evidence from four shallow marine habitats. Mar Ecol Prog Ser 575:207–215.  https://doi.org/10.3354/meps12188 CrossRefGoogle Scholar
  47. Tavolga WN (1958) Underwater sounds produced by two species of toadfish, Opsanus tau and Opsanus beta. Bull Mar Sci Gulf Caribb 8:278–284Google Scholar
  48. Thorson RF, Fine ML (2002a) Acoustic competition in the gulf toadfish Opsanus beta: acoustic tagging. J Acoust Soc Am 111:2302–2307.  https://doi.org/10.1121/1.1466865 CrossRefPubMedGoogle Scholar
  49. Thorson RF, Fine ML (2002b) Crepuscular changes in emission rate and parameters of the boatwhistle advertisement call of the gulf toadfish, Opsanus beta. Environ Biol Fish 63:321–331.  https://doi.org/10.1023/A:1014334425821 CrossRefGoogle Scholar
  50. Urick RJ (1983) Principles of underwater sound, 3rd edition. Peninsula Publishing, Los AltosGoogle Scholar
  51. Vasconcelos RO, Simıes JM, Almada VC, Fonseca PJ, Amorim MCP (2010) Vocal behavior during territorial intrusions in the Lusitanian toadfish: boatwhistles also function as territorial ‘keep-out’ signals. Ethology 116:155–165.  https://doi.org/10.1111/j.1439-0310.2009.01722.x CrossRefGoogle Scholar
  52. Vasconcelos RO, Carriço R, Ramos A, Modesto T, Fonseca PJ, Amorim MCP (2012) Vocal behavior predicts reproductive success in a teleost fish. Behav Ecol 23:375–383.  https://doi.org/10.1093/beheco/arr199 CrossRefGoogle Scholar
  53. Vieira M, Fonseca PJ, Amorim MCP, Teixeira CJC (2015) Call recognition and individual identification of fish vocalizations based on automatic speech recognition: an example with the Lusitanian toadfish. J Acoust Soc Am 138:3941–3950.  https://doi.org/10.1121/1.4936858 CrossRefPubMedGoogle Scholar
  54. Winn HE (1972) Acoustic discrimination by the toadfish with comments on signal systems. In: Winn HE, Olla BL (eds) Behavior of marine animals: current perspectives in research, vol 2: vertebrates. Plenum Press, New York, pp 361–385CrossRefGoogle Scholar
  55. Zeddies DG, Fay RR, Gray MD, Alderks PW, Acob A, Sisneros JA (2012) Local acoustic particle motion guides sound-source localization behavior in the plainfin midshipman fish, Porichthys notatus. J Exp Biol 215:152–160.  https://doi.org/10.1242/jeb.064998 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018
corrected publication April/2018

Authors and Affiliations

  1. 1.Tennenbaum Marine Observatories NetworkSmithsonian Environmental Research CenterEdgewaterUSA
  2. 2.Bureau of Ocean Energy ManagementSterlingUSA
  3. 3.Earth to Ocean Research Group, Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  4. 4.Department of Invertebrate ZoologyNational Museum of Natural History, Smithsonian InstitutionWashingtonUSA
  5. 5.Beneath the Waves, Inc.HerndonUSA
  6. 6.Smithsonian Tropical Research InstituteBocas del ToroPanama
  7. 7.Bioacoustics Research Program, Cornell Laboratory of OrnithologyCornell UniversityIthacaUSA

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