Aggressive thresholds in Dendropsophus ebraccatus: habituation and sensitization to different call types

Abstract

Males in many chorusing anuran species use aggressive calls during defense of calling spaces from other males. The minimal intensity of another male’s vocalizations that elicits an aggressive call response has been termed the aggressive threshold. Previous studies of aggressive thresholds have shown that they are plastic: males habituated (increased their aggressive thresholds) in response to repeated presentation of stimuli above initial threshold levels. Habituation likely contributes to the stable chorus structure of these species, in which aggressive calling is rare compared to advertisement calls. I have observed high levels of aggressive calling in the treefrog Dendropsophus ebraccatus, suggesting that males of this species do not habituate. In this study, I investigated the plasticity of aggressive thresholds in D. ebraccatus. I measured the aggressive thresholds of males before and after suprathreshold stimulation by both advertisement and aggressive calls. I found that the different call types had different effects: males habituated to advertisement calls but lowered their aggressive thresholds in response to aggressive calls. I consider the latter response to be an example of sensitization, a behavior that has been documented infrequently in vocalizing anurans. Sensitization is a plausible mechanism responsible for the high levels of aggressive calling observed in this species. Given the high costs of aggressive calling, however, it is unclear why a mechanism that increases aggressive call output would be maintained.

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References

  1. Allan DM (1973) Some relationships of vocalization to behavior in the Pacific treefrog, Hyla regilla. Herpetologica 29:366–371

    Google Scholar 

  2. Backwell PRY (1988) Functional partitioning in the two-part call of the leaf folding frog Afrixalus brachycnemis. Herpetologica 44:1–7

    Google Scholar 

  3. Bee MA (2001) Habituation and sensitization in bullfrogs (Rana catesbiana): testing the dual-process theory of habituation. J Comp Psychol 115:307–316

    Article  CAS  PubMed  Google Scholar 

  4. Bosch J, Marquez R (2001) Call timing in male–male acoustical interactions and female choice in the midwife toad Alytes obstetricans. Copeia 1:169–177

    Article  Google Scholar 

  5. Brenowitz EA (1989) Neighbor call amplitude influences aggressive behavior and intermale spacing in choruses of the Pacific Treefrog (Hyla regilla). Ethology 83:69–79

    Google Scholar 

  6. Brenowitz EA, Rose GJ (1994) Behavioural plasticity mediates aggression in choruses of the Pacific treefrog. Anim Behav 47:633–641

    Article  Google Scholar 

  7. Brenowitz EA, Rose GJ (1999) Female choice and plasticity of male calling behaviour in the Pacific treefrog. Anim Behav 57:1337–1342

    Article  PubMed  Google Scholar 

  8. Brenowitz EA, Wilczynski W, Zakon HH (1984) Acoustic communication in spring peepers. J Comp Physiol A 155:585–592

    Article  Google Scholar 

  9. Brzoska J (1982) Vocal response of male European water frogs (Rana esculenta complex) to mating and territorial calls. Behav Processes 7:37–47

    Article  Google Scholar 

  10. Brzoska J, Schneider H, Nevo E (1982) Territorial behavior and vocal response in male Hyla arborea savignyi (Amphibia: Anura). Isr J Zool 31:27–37

    Google Scholar 

  11. Bucher TL, Ryan MJ, Bartholomew GA (1982) Oxygen consumption during resting, calling, and nest building in the frog Physalaemus pustulosus. Physiol Zool 55:10–22

    Google Scholar 

  12. Burmeister S, Wilczynski W, Ryan MJ (1999) Temporal call changes and prior experience affect graded signalling in the cricket frog. Anim Behav 57:611–618

    Article  PubMed  Google Scholar 

  13. Gerhardt HC, Diekamp B, Ptacek M (1989) Inter-male spacing in choruses of the spring peeper, Pseudacris (Hyla) crucifer. Anim Behav 38:1012–1024

    Article  Google Scholar 

  14. Grafe TU (1995) Graded aggressive calls in the African painted reed frog Hyperolius marmoratus (Hyperoliidae). Ethology 101:67–81

    Article  Google Scholar 

  15. Grafe TU (1996) The function of call alternation in the African reed frog (Hyperolius marmoratus): precise call timing prevents auditory masking. Behav Ecol Sociobiol 38:149–158

    Article  Google Scholar 

  16. Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450

    Article  CAS  PubMed  Google Scholar 

  17. Lopez PT, Narins PM, Lewis ER, Moore SW (1988) Acoustically induced call modification in the white-lipped frog, Leptodactylus albilabris. Anim Behav 36:1295–1308

    Article  Google Scholar 

  18. Marshall VT (2003) Social aspects of communication in gray treefrogs: intraspecific and interspecific interactions. Unpublished PhD dissertation. Columbia, MO: University of Missouri

  19. Marshall VT, Humfeld SC, Bee MA (2003) Plasticity of aggressive signalling and its evolution in male spring peepers, Pseudacris crucifer. Anim Behav 65:1223–1234

    Article  Google Scholar 

  20. Martínez-Rivera C, Gerhardt H (2008) Advertisement-call modification, male competition, and female preference in the bird-voiced treefrog Hyla avivoca. Behav Ecol Sociobiol 63:195–208

    Article  PubMed  Google Scholar 

  21. Megela AL, Capranica RR (1983) A neural and behavioral study of auditory habituation in the bullfrog, Rana catesbeiana. J Comp Physiol A 151:423–434

    Article  Google Scholar 

  22. Oldham RS, Gerhardt HC (1975) Behavioral isolating mechanisms of treefrogs Hyla cinerea and Hyla gratiosa. Copeia 2:223–231

    Article  Google Scholar 

  23. Owen PC, Perrill SA (1998) Habituation in the green frog, Rana clamitans. Behav Ecol Sociobiol 44:209–213

    Article  Google Scholar 

  24. Peeke HVS (1982) Stimulus- and motivation-specific sensitization and redirection of aggression in the three-spined stickleback (Gasterosteus aculeatus). J Comp Physiol Psychol 96:816–822

    Article  Google Scholar 

  25. Petrinovich L, Patterson TL (1981) Field studies of habituation: IV. Sensitization as a function of the distribution and novelty of song playback to white-crowned sparrows. J Comp Physiol Psychol 95:805–812

    Article  Google Scholar 

  26. Rand AS, Ryan MJ (1981) The adaptive significance of a complex vocal repertoire in a neotropical frog. Z Tierpsychol 57:209–214

    Google Scholar 

  27. Robertson JGM (1984) Acoustic spacing by breeding males of Uperolia rugosa (Anura: Leptodactylidae). Z Tierpsychol 64:283–297

    Google Scholar 

  28. Rose GJ, Brenowitz EA (1991) Aggressive thresholds of male pacific treefrogs for advertisement calls vary with amplitude of neighbors’ calls. Ethology 89:244–252

    Article  Google Scholar 

  29. Rose GJ, Brenowitz EA (1997) Plasticity of aggressive thresholds in Hyla regilla discrete accommodation to encounter calls. Anim Behav 53:353–361

    Article  Google Scholar 

  30. Rosen M, Lemon RE (1974) Vocal behavior of spring peepers, Hyla crucifer. Copeia 1974:940–950

    Article  Google Scholar 

  31. Ryan MJ (1988) Energy, calling, and selection. Am Zool 28:885–898

    Google Scholar 

  32. Schwartz J, Buchanan B, Gerhardt HC (2002) Acoustic interactions among male gray treefrogs, Hyla versicolor, in a chorus setting. Behav Ecol Sociobiol 53:9–19

    Article  Google Scholar 

  33. Schwartz JJ (1986) Male calling behavior and female choice in the Neotropical treefrog Hyla microcephala. Ethology 73:116–127

    Google Scholar 

  34. Schwartz JJ (1987) The function of call alternation in anuran amphibians: a test of three hypotheses. Evolution 41:461–471

    Article  Google Scholar 

  35. Schwartz JJ (1991) Why stop calling? A study of unison bout singing in a Neotropical treefrog. Anim Behav 42:565–577

    Article  Google Scholar 

  36. Schwartz JJ, Wells KD (1983) An experimental study of acoustic interference between two species of Neotropical treefrogs. Anim Behav 31:181–190

    Article  Google Scholar 

  37. Schwartz JJ, Wells KD (1984) Interspecific acoustic interactions of the Neotropical treefrog Hyla ebraccata. Behav Ecol Sociobiol 14:211–224

    Article  Google Scholar 

  38. Schwartz JJ, Wells KD (1985) Intraspecific and interspecific vocal behavior of the Neotropical treefrog Hyla microcephala. Copeia 1985:27–38

    Article  Google Scholar 

  39. Stewart MM, Rand AS (1992) Diel variation in the use of aggressive calls by the frog Eleutherodactylus coqui. Herpetologica 48:49–56

    Google Scholar 

  40. Taigen TL, Wells KD (1985) Energetics of vocalization by an anuran amphibian (Hyla versicolor). J Comp Physiol B 155:163–170

    Article  Google Scholar 

  41. Telford SR (1985) Mechanisms and evolution of inter-male spacing in the painted reedfrog (Hyperolius marmoratus). Anim Behav 33:1353–1361

    Article  Google Scholar 

  42. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43

    Article  CAS  PubMed  Google Scholar 

  43. Thompson RF, Groves PM, Teyler TJ, Roemer RA (1973) A dual-process theory of habituation: theory and behavior. In: Peeke HVS, Herz MJ (eds) Habituation I: behavioral studies. Academic, New York, pp 239–271

    Google Scholar 

  44. Wagner WE (1989a) Fighting, assessment, and frequency alteration in Blanchard’s cricket frog. Behav Ecol Sociobiol 25:429–436

    Article  Google Scholar 

  45. Wagner WE (1989b) Graded aggressive signals in Blanchard’s cricket frog: vocal responses to opponent proximity and size. Anim Behav 38:1025–1038

    Article  Google Scholar 

  46. Wagner WE (1992) Deceptive or honest signaling of fighting ability—a test of alternative hypotheses for the function of changes in call dominant frequency by male cricket frogs. Anim Behav 44:449–462

    Article  Google Scholar 

  47. Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693

    Article  Google Scholar 

  48. Wells KD (1988) The effect of social interactions on anuran vocal behavior. In: Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 433–454

    Google Scholar 

  49. Wells KD (1989) Vocal communication in a Neotropical treefrog, Hyla ebraccata—responses of males to graded aggressive calls. Copeia 1989:461–466

    Article  Google Scholar 

  50. Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago

    Google Scholar 

  51. Wells KD, Bard KM (1987) Vocal communication in a Neotropical treefrog, Hyla ebraccata—responses of females to advertisement and aggressive calls. Behaviour 101:199–210

    Article  Google Scholar 

  52. Wells KD, Greer BJ (1981) Vocal responses to conspecific calls in a Neotropical hylid frog, Hyla ebraccata. Copeia 1981:615–624

    Article  Google Scholar 

  53. Wells KD, Schwartz JJ (1984a) Vocal communication in a Neotropical treefrog, Hyla ebraccata—advertisement calls. Anim Behav 32:405–420

    Article  Google Scholar 

  54. Wells KD, Schwartz JJ (1984b) Vocal communication in a Neotropical treefrog, Hyla ebraccata—aggressive calls. Behaviour 91:128–145

    Article  Google Scholar 

  55. Wells KD, Taigen TL (1986) The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor). Behav Ecol Sociobiol 19:9–18

    Article  Google Scholar 

  56. Wells KD, Taigen TL (1989) Calling energetics of a Neotropical treefrog, Hyla microcephala. Behav Ecol Sociobiol 25:13–22

    Article  Google Scholar 

  57. Whitney CL, Krebs JR (1975) Mate selection in Pacific tree frogs. Nature 255:325–326

    Article  Google Scholar 

  58. Wiewandt TA (1969) Vocalization, aggressive behavior, and territoriality in the bullfrog, Rana catesbeiana. Copeia 1969:276–285

    Article  Google Scholar 

  59. Wilczynski W, Brenowitz EA (1988) Acoustic cues mediate inter-male spacing in a neotropical frog. Anim Behav 36:1054–1063

    Article  Google Scholar 

  60. Wilczynski W, McClelland BE, Rand AS (1993) Acoustic, auditory, and morphological divergence in 3 species of neotropical frog. J Comp Physiol A 172:425–438

    Article  CAS  PubMed  Google Scholar 

  61. Wollerman L (1998) Stabilizing and directional preferences of female Hyla ebraccata for calls differing in static properties. Anim Behav 55:1619–1630

    Article  PubMed  Google Scholar 

  62. Wollerman L (1999) Acoustic interference limits call detection in a Neotropical frog Hyla ebraccata. Anim Behav 57:529–536

    Article  PubMed  Google Scholar 

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Acknowledgements

I would like to thank Flávia Barbosa and Carl Gerhardt for their support and helpful comments on the experimental design and, along with Dave Geary, the manuscript. Two anonymous reviewers provided additional helpful commentary on the manuscript, which greatly clarified the text. John Christy served as the sponsor of this project at the Smithsonian Tropical Research Institute. I thank the staff of S.T.R.I. for assistance with logistics and permits and the government of the Republic of Panama for providing permission to carry out this project. Kathryn Kettenbach assisted with analysis of recordings. Financial support was provided by a Smithsonian Institution 10-week predoctoral fellowship and a Graduate Assistance in Areas of National Need fellowship from the University of Missouri. The experimental protocol was approved by the Institutional Animal Care and Use Committees of the University of Texas (IACUC protocol no. 06051202) and the Smithsonian Tropical Research Institute (IACUC protocol no. 2006-08-07-07-06).

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Correspondence to Michael S. Reichert.

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Communicated by J. Christensen-Dalsgaard

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Reichert, M.S. Aggressive thresholds in Dendropsophus ebraccatus: habituation and sensitization to different call types. Behav Ecol Sociobiol 64, 529–539 (2010). https://doi.org/10.1007/s00265-009-0868-5

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Keywords

  • Aggressive
  • Threshold
  • Frog
  • Habituation
  • Sensitization
  • Communication