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Interspecific territoriality despite vocal divergence in two sympatric Laterallus crakes

  • Emiliano A. DepinoEmail author
  • Juan I. Areta
Original Article

Abstract

Territoriality is a widespread behavioral phenomenon that functions for partitioning space and defending resources. Birds tend to defend territories against homospecific individuals through long-distance acoustic signals, but some species also exhibit interspecific territoriality. Two main hypotheses could explain interspecific territoriality mediated by long-distance acoustic signals: (1) misidentification of heterospecifics as homospecifics (misdirected aggression), or (2) recognition of heterospecifics as threats (purposeful aggression). The sympatric Red-and-white crake (Laterallus leucopyrrhus) and the Rufous-sided crake (L. melanophaius) are reciprocally territorial, but the mechanism underlying this interspecific territoriality is not known. We assessed the similarity of territorial long-distance acoustic signals (duet trills) between these crakes in comparison to more closely related species: Red-and-white vs. Rufous-faced crake (L. xenopterus) and Rufous-sided vs. White-throated crake (L. albigularis). Duet trills are two-parted, beginning with soft initial notes audible at close range and followed by a loud-trilled portion audible at long range. We ran univariate comparisons (Kruskal–Wallis), assessed overlap in multivariate acoustic space (PCA), and calculated vocal similarities (cluster analysis; Euclidean distances). The loud-trilled portions of the interspecifically territorial Red-and-white and Rufous-sided crakes occupied completely non-overlapping acoustic spaces, and were not grouped together by vocal similarity. Their territorial signals were more similar to those of their closest relatives, than between them. Soft initial notes of duet trills were in general very different between species, and their general structure matched the phylogenetic relationships. We found no evidence for strong character convergence and partial phylogenetic conservatism in signal explained overall similarities in vocalizations among species. The highly divergent vocalizations of Red-and-white and Rufous-sided crakes in conjunction with their interspecific territorial responses suggest that recognition of heterospecifics as threats, and not misidentification of heterospecifics as homospecifics, mediates their vocal responses. Our study adds evidence showing that interspecific territoriality represents purposeful heterospecific aggression and is not the product of misdirected homospecific aggression.

Keywords

Interspecific territoriality Interspecific interactions Acoustic signal Signal perception Competition Playback Crakes Rallidae 

Zusammenfassung

Interspezifische Territorialität trotz gesanglicher Divergenz bei zwei sympatrisch vorkommenden Rallenarten

Territorialität ist ein weitverbreitetes Verhaltensphänomen, das dazu dient, Räume aufzuteilen und Ressourcen zu verteidigen. Vögel neigen dazu, Reviere gegen Artgenossen mit Hilfe weitreichender akustischer Signale zu verteidigen, doch einige Arten zeigen auch interspezifische Territorialität. Zwei Haupthypothesen könnten die durch weitreichende akustische Signale vermittelte interspezifische Territorialität erklären: (1) die Fehlerkennung von Nicht-Artgenossen als Artgenossen (fehlgeleitete Aggression) oder (2) die Erkennung von Nicht-Artgenossen als Bedrohung (zielgerichtete Aggression). Zwei sympatrisch vorkommende Rallenarten, Weißbrustralle (Laterallus leucopyrrhus) und Rothalsralle (L. melanophaius), sind wechselseitig territorial, doch der dieser interspezifischen Territorialität zugrundeliegende Mechanismus ist unbekannt. Wir haben die Ähnlichkeit der zur Revierverteidigung eingesetzten weitreichenden akustischen Signale (Duett-Triller) zwischen diesen beiden Rallenarten abgeschätzt und die Signale zudem mit denen jeweils näher verwandter Arten verglichen–die der Weißbrustralle mit denen der nah verwandten Rotgesichtralle (L. xenopterus) und die der Rothalsralle mit denen der nah verwandten Weißkehlralle (L. albigularis). Die Duett-Triller sind zweiteilig und beginnen mit leisen Anfangstönen, die nur auf kurze Entfernung hörbar sind, gefolgt von einem lauten Trillerteil, der auch auf längere Entfernung hörbar ist. Wir haben univariate Vergleiche durchgeführt (Kruskal–Wallis), die Überlappung im multivariaten akustischen Raum abgeschätzt (PCA) und Gesangsähnlichkeiten berechnet (Clusteranalyse; euklidischer Abstand). Die lauten Trilleranteile der interspezifisch territorialen Weißbrust- und Rothalsrallen überlappten im akustischen Raum gar nicht und konnten nicht anhand von Gesangsähnlichkeiten zusammengefasst werden. Die territorialen Signale dieser beiden Rallenarten wiesen geringere Ähnlichkeit miteinander auf als mit den Signalen der jeweils nächsten Artverwandten. Die leisen Anfangstöne der Duett-Triller unterschieden sich allgemein sehr zwischen den untersuchten Arten, und ihre generelle Struktur stand im Einklang mit den stammesgeschichtlichen Beziehungen. Wir fanden keine Belege für eine starke Merkmalskonvergenz, und ein teilweiser stammesgeschichtlicher Konservatismus im Signal erklärte die allgemeinen Ähnlichkeiten zwischen den Lautäußerungen der verschiedenen Arten. Die höchst divergenten Lautäußerungen der Weißbrust- und Rothalsrallen deuten in Verbindung mit ihren interspezifischen Revierantworten darauf hin, dass die Erkennung von Nicht-Artgenossen als Bedrohung (und nicht deren Fehlerkennung als Artgenossen) die Gesangsantworten herbeiführt. Unsere Studie liefert weitere Belege dafür, dass interspezifische Territorialität zielgerichtete Aggression gegenüber Nicht-Artgenossen repräsentiert und nicht das Ergebnis fehlgeleiteter Aggression gegenüber Artgenossen ist.

Notes

Acknowledgements

We thank Fabricio Gorleri, and all the rangers of the Reserva Natural Punta Lara and Aguara-Ñú 2016 for their companionship and help in the field. We specially thank Juan Pablo Carricart, Myriam Velazquez, Elisa Bonaccorso and Patricia Escalante Pliego for their help with study permits and field trip logistical requirements in Argentina, Paraguay, and Ecuador, respectively. F. Burgos, E. Jordan, F. Gorleri, I. Holzmann, J. Amaya, J. Benítez Saldivar, and M. Juhant provided helpful comments on the manuscript. Our research was funded by the Consejo Nacional de Investigaciones Científicas y Técnicas, the Neotropical Bird Club (Conservation Award), and the Association of Field Ornithologists (Bergstrom Memorial Research Award). None had any input into the contents of the manuscript, nor required their approval of the manuscript before submission or publication. All the study permits needed for the development of our field studies were granted by the pertinent governmental institutions of Argentina, Paraguay, and Ecuador. Sound Archive:  https://doi.org/10.7479/v1cx-nr21.

Supplementary material

10336_2019_1735_MOESM1_ESM.pdf (47 kb)
Table S1 Supporting information of the sound recordings used of the four Laterallus species studied. (PDF 46 kb)
10336_2019_1735_MOESM2_ESM.docx (12 kb)
Supplementary material 2 (DOCX 12 kb)
10336_2019_1735_MOESM3_ESM.docx (12 kb)
Supplementary material 3 (DOCX 11 kb)
10336_2019_1735_MOESM4_ESM.tiff (10.5 mb)
Fig. S1 Illustration of spectrogram-based acoustic variables measured on loud-trilled portions of duet trills vocalizations of Laterallus crakes showed on main trill view (center), detailed view of individual notes of trills (left), and spectrogram slice view (right). (TIFF 10779 kb)
10336_2019_1735_MOESM5_ESM.xlsx (13 kb)
Supplementary material 5 (XLSX 12 kb)

References

  1. Areta JI, Depino EA (2012) Red-and-white Crake (Laterallus leucopyrrhus). Neotropical Birds Online. http://neotropical.birds.cornell.edu/portal/species/overview?p_p_spp=135636 Accessed 10 March 2016.
  2. Budka M, Osiejuk TS (2013) Neighbour–stranger call discrimination in a nocturnal rail species, the Corncrake Crex crex. J Ornithol 154:685–694CrossRefGoogle Scholar
  3. Catchpole CK (1978) Interspecific territorialism and competition in Acrocephalus warblers as revealed by playback experiments in areas of sympathy and allopatry. Anim Behav 26:1072–1080CrossRefGoogle Scholar
  4. Catchpole CK, Leisler B (1988) Interspecific territoriality in Acrocephalus: a reply to Murray’s critical review. Ornis Scand 19:314–316CrossRefGoogle Scholar
  5. Catchpole CK, Slater PB (2008) Bird song: biological themes and variations. Cambridge University, CambridgeCrossRefGoogle Scholar
  6. Charif RA, Waack AM, Strickman LM (2010) Raven Pro 1.4 User’s Manual. Cornell Lab of Ornithology, New YorkGoogle Scholar
  7. Clapperton BK (1987) Individual recognition by voice in the pukeko, Porphyrio porphyrio melanotus (Aves: Rallidae). New Zeal J Zool 14:11–18CrossRefGoogle Scholar
  8. Cody ML (1969) Convergent characteristics in sympatric species: a possible relation to interspecific competition and aggression. Condor 71:223–239CrossRefGoogle Scholar
  9. Cody ML (1973) Character convergence. Annu Rev Ecol Syst 4:189–211CrossRefGoogle Scholar
  10. Depino EA, Areta JI (2017) Ecological segregation and vocal interactions in two sympatric Laterallus crakes. J Ornithol 158:431–441CrossRefGoogle Scholar
  11. Dhondt AA (2012) Interspecific competition in birds. Oxford University, OxfordGoogle Scholar
  12. Dooling R (2004) Audition: can birds hear everything they sing? In: Marler P, Slabbekoorn H (eds) Nature’s music: the science of Journal of Ornithology birdsong. Elsevier Academic Press, CaliforniaGoogle Scholar
  13. Emlen ST (1972) An experimental analysis of the parameters of bird song eliciting species recognition. Behav 41(1–2):130–171CrossRefGoogle Scholar
  14. Forrest TG (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654CrossRefGoogle Scholar
  15. Freeman BG (2015) Strong asymmetric interspecific aggression between two sympatric New Guinean robins. Ibis 158:75–81CrossRefGoogle Scholar
  16. Garcia RJC, Gibb GC, Trewick SA (2014) Deep global evolutionary radiation in birds: diversification and trait evolution in the cosmopolitan bird family Rallidae. Mol Phylogenet Evol 81:96–108CrossRefGoogle Scholar
  17. Goodale E, Kotagama SW (2005) Testing the roles of species in mixed-species bird flocks of a Sri Lankan rain forest. J Trop Ecol 21:669–676CrossRefGoogle Scholar
  18. Goodale E, Kotagama SW (2006) Alarm Calling in Sri Lankan mixed-species bird flocks. Auk 122:108CrossRefGoogle Scholar
  19. Gorton RE (1977) Territorial interactions in sympatric song sparrow and Bewick’s wren populations. Auk 94:701–708CrossRefGoogle Scholar
  20. Green DM, Swets JA (1966) Signal detection theory and psychophysics. Wiley, New YorkGoogle Scholar
  21. Grether GF (2011) The neuroecology of competitor recognition. Integr Comp Biol 51:807–818PubMedCrossRefPubMedCentralGoogle Scholar
  22. Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol rev Camb Phil Soc 84:617–635CrossRefGoogle Scholar
  23. Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N, Okamoto K, Peiman KS (2013) The evolutionary consequences of interspecific aggression. Ann N Y Acad Sci 1289:48–68PubMedCrossRefPubMedCentralGoogle Scholar
  24. Hair JF, Black WC, Babin BJ, Anderson RE, Tatham RL (2006) Multivariate Data Analysis. Pearson Education, New DelhiGoogle Scholar
  25. Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol electron 4:9Google Scholar
  26. Hick KG, Doucet SM, Mennill DJ (2015) Interspecific vocal discrimination in Neotropical wrens: responses to congeneric signals in sympatry and allopatry. Anim Behav 109:113–121CrossRefGoogle Scholar
  27. Kaiser HF (1974) An index of factorial simplicity. Psychometrika 39:31–36CrossRefGoogle Scholar
  28. Lambrechts MM, Dhondt AA (1995) Individual Voice Discrimination in Birds. In: Power DM (ed) Current Ornithology, vol 12. Springer, Boston, pp 115–139CrossRefGoogle Scholar
  29. Lengagne T, Jouventin P, Aubin T (1999) Finding one’s mate in a king penguin colony: efficiency of acoustic communication. Behaviour 136:833–846CrossRefGoogle Scholar
  30. Livezey BC (1998) A phylogenetic analysis of the Gruiformes (Aves) based on morphological characters, with an emphasis on the Rails (Rallidae). Philos Trans R Soc Lond Ser B 353:2077–2151CrossRefGoogle Scholar
  31. Lovell SF, Lein MR (2004) Neighbor-stranger discrimination by song in a suboscine bird, the alder flycatcher, Empidonax alnorum. Behav Ecol 15:799–804CrossRefGoogle Scholar
  32. Luther DA, Wiley RH (2009) Production and perception of communicatory signals in a noisy environment. Biol Lett 5:183–187PubMedPubMedCentralCrossRefGoogle Scholar
  33. Magrath RD, Pitcher BJ, Gardner JL (2007) A mutual understanding? Interspecific responses by birds to each other’s aerial alarm calls. Behav Ecol 18:944–951CrossRefGoogle Scholar
  34. Maher CR, Lott DF (1995) Definitions of territoriality used in the study of variation in vertebrate spacing systems. Anim Behav 49:1581–1597CrossRefGoogle Scholar
  35. Martin PR, Dobbs RC (2014) Asymmetric response to heterospecific songs in two sympatric Wrens (Troglodytidae) in Argentina: house Wren (Troglodytes aedon) and Mountain Wren (T. Solstitialis). Ornitol Neotrop 25:407–419Google Scholar
  36. Martin PR, Fotheringham JR, Ratcliffe L, Robertson RJ (1996) Response of American redstarts (suborder Passeri) and least flycatchers (suborder Tyranni) to heterospecific playback: the role of song in aggressive interactions and interference competition. Behav Ecol Sociobiol 39:227–235CrossRefGoogle Scholar
  37. Mathevon N, Aubin T (2001) Sound-based species-specific recognition in the Blackcap Sylvia atricapilla shows high tolerance to signal modifications. Behav 138:511–524CrossRefGoogle Scholar
  38. Matyjasiak P (2004) Birds associate species-specific acoustic and visual cues: recognition of heterospecific rivals by male Blackcaps. Behav Ecol 16:467–471CrossRefGoogle Scholar
  39. Mikami OK, Kawata M (2004) Does interspecific territoriality reflect the intensity of ecological interactions? A theoretical model for interspecific territoriality. Evol Ecol Res 6:765–775Google Scholar
  40. Murray BG (1971) The ecological consequences of interspecific territorial behavior in birds. Ecol 52:414–423CrossRefGoogle Scholar
  41. Murray BG (1981) The origins of adaptive interspecific territorialism. Biol Rev 56:1–22CrossRefGoogle Scholar
  42. Murray BG (1988) Interspecific territoriality in Acrocephalus: a critical review. Ornis Scand 19:309–313CrossRefGoogle Scholar
  43. Orians GH, Willson MF (1964) Interspecific territories of birds. Ecology 45:736–745CrossRefGoogle Scholar
  44. Peiman KS, Robinson BW (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158PubMedCrossRefPubMedCentralGoogle Scholar
  45. Policht R, Hart V, Goncharov D, Surový P, Hanzal V, Červený J, Burda H (2019) Vocal recognition of a nest-predator in black grouse. Peer J 7:1–12CrossRefGoogle Scholar
  46. Prescott DRC (1987) Territorial responses to song playback in allopatric and sympatric populations of Alder (Empidonax alnorum) and Willow (E. traillii) flycatchers. Wil Bull 99:611–619Google Scholar
  47. Reed TM (1982) Interspecific territoriality in the chaffinch and great tit on islands and the mainland of Scotland: playback and removal experiments. Anim Behav 30:171–181CrossRefGoogle Scholar
  48. Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11CrossRefGoogle Scholar
  49. Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, PrincetonCrossRefGoogle Scholar
  50. Ryan M (2019) A taste for the beautiful: the evolution of attraction. Princeton University Press, PrincetonGoogle Scholar
  51. Slabbekoorn H (2004) Singing in the wild: the ecology of birdsong. In: Marler P, Slabbekoorn H (eds) Nature’s music: the science of birdsong. Elsevier Academic Press, CaliforniaGoogle Scholar
  52. Sosa-López JR, Martínez Gómez JE, Mennill DJ (2015) Divergence in mating signals correlates with genetic distance and behavioural responses to playback. J Evol Biol 29:306–318PubMedCrossRefPubMedCentralGoogle Scholar
  53. Sosa-López JR, Mennill DJ, Renton K (2017) Sexual differentiation and seasonal variation in response to conspecific and heterospecific acoustic signals. Ethol 123:460–466CrossRefGoogle Scholar
  54. Stiles FG, Levey DJK (1988) The Gray-breasted Crake (Laterallus exilis) in Costa Rica: vocalizations, distribution, and interactions with White-throated Crakes (L. albigularis). Condor 90:607–612CrossRefGoogle Scholar
  55. Stoddard PK, Beecher MD, Horning CL, Campbell SE (1991) Recognition of individual neighbors by song in the song sparrow, a species with song repertoires. Behav Ecol Sociobiol 29:211–215CrossRefGoogle Scholar
  56. Storer RW (1981) The rufous-faced crake (Laterallus xenopterus) and its Paraguayan congeners. Wilson Bull 93:137–144Google Scholar
  57. Taylor B, van Perlo B (1998) Rails: a guide to the rails, crakes, gallinules and coots of the world. Helm, LondonGoogle Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.Laboratorio de Ecología, Comportamiento y Sonidos Naturales (ECOSON)Instituto de Bio y Geociencias del Noroeste Argentino (IBIGEO-CONICET)SaltaArgentina

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