1. Soundscapes of the forest Implications for evolution and applications for conservation Dr. Hans Slabbekoorn Institute of Biology, Leiden University The Netherlands

2. Soundscapes of the forest Implications for evolution Applications for conservation Soundscapes Function of bird song Environmental selection Habitat degradation Urbanisation Song and speciation

3. All habitats have their own specific soundscape

4. The soundscape is build up by abiotic sound sources…

5. … and biotic sound sources depending on the local animal community

6. A soundscape can be simple with one or few species acoustically active at the same time…

7. … or complex with many species more or less overlapping in time, frequency, and space

8. Sonogram: graphic representation of the sound energy distribution (Slabbekoorn JASA 2004)

9. The acoustic equivalent of the rainforest is found in the underwater soundscape of coral reefs

10. And we have the urban jungle… What are the consequences? Stress, disturbance, deterrence Masking of relevant sounds

11. Most birds have elaborate ways to communicate acoustically!

12. Territorial defense: experiment with great tits Birdsong Other sound (Krebs, Ashcroft & Webber: Nature 1978)

13. Mate attraction: experiment with pied flycatcher (Eriksson & Wallin: Behav.Ecol.&Sociobiol. 1986) Flycatcher song Without sound

14. Birdsong plays a role in Territorial defense and Mate attraction

15. Songs vary between populations of the same species and between species Can song variation between populations play a role in speciation? Geographic separation needed? Or by ecological divergence?

16. Ecological speciation in birds Morphological Divergence Song Divergence Reproductive Isolation Divergent Selection (Slabbekoorn & Smith: Phil.Trans.Roy.Soc. 2002)

17. Foto: Robert Hughes Fox sparrow Tijd (sec) Frequentie (kHz) 8.0 6.0 4.0 2.0 0 0 0.5 1.0 1.5 2.0

18. 1. High frequency attenuation 2. Reverberations Sound transmission Frequency Amplitude Time

19. Frequency (kHz) Time (sec) 0 2.0 4.0 6.0 8 6 4 2 8 6 4 2 8 6 4 2 A B C Sonograms of ‘closed’ habitat bird species (Slabbekoorn Nature’s Music 2004)

20. Frequency (kHz) 0 2.0 4.0 6.0 8 6 4 2 8 6 4 2 8 6 4 2 A B C Sonograms of ‘open’ habitat bird species Time (sec) (Slabbekoorn Nature’s Music 2004)

21. Also within species: Habitat-dependent divergence in trill rate in the rufous-collared sparrow Time (seconds) Frequency (kHz) (Handford 2004)

22. Ambient noise

23. (Slabbekoorn & Smith: Evolution 2002) Case 1: little greenbuls of Africa ( Andropadus virens )

24. *** p < 0.001 * p < 0.05 Rainforest Ecotone (Smith et al. : Science 1997) Despite gene flow, there is divergence in morphology and song Minimum freq Maximum freq Delivery rate Herz Herz #/sec *** *** *** N = 72 57 N = 72 57 N = 72 57 Song (Slabbekoorn & Smith: Evolution 2002) Body weight Wing length Bill depth grams mm mm *** *** * N = 45 60 N = 45 61 N = 44 61 Morphology

25. Frequency (kHz) Time (sec) 8 6 4 2 8 6 4 2 Habitat-dependent differences in the maximum frequency of song type III II I III I II III 0 2.0 4.0 6.0 Acoustic divergence may be driven by habitat-dependent masking NOISE

26. Ecology versus Isolation: do glacial rainforest refugia play a role in divergence and speciation?

27. Ecology versus Isolation: do glacial rainforest refugia play a role in divergence and speciation?

28. (Kirschel et al.: Evolution 2011) Ecology versus Isolation:

29. (Kirschel et al.: Evolution 2011) Ecology versus Isolation: do glacial rainforest refugia play a role in divergence and speciation? Habitat differences in maximum frequency of song type III are consistent! What about response levels? Do little greenbuls recognize birds from their own habitat?

30. Approach distance (m) (Kirschel et al.: Evolution 2011) Cameroon Uganda No discrimination in the ecotone between own population versus nearby other habitat or far-away own habitat

31. Approach distance (m) Cameroon Uganda (Kirschel et al.: Evolution 2011)

32. Approach distance (m) Cameroon Uganda (Kirschel et al.: Evolution 2011) Significantly decreased response strength in the rainforest to nearby other habitat but not to far-away own habitat

33. Case 2: grey-breasted wood-wrens of South America ( Henicorhina leucophrys )

34. leucophrys hilaris Temperate Elfin forest Tropical Lowlands Two subspecies at different but adjacent elevations in the Andes

35. Song divergence: high notes again... leucophrys hilaris

36. Consistent across Ecuador (and Colombia)

37. Divergent environmental selection? hilaris : El Limo, 1000 m leucophrys : Yanaycu, 2100 m “ WET” & Cold “ DRY” & Warm

38. leucophrys Time(s) hilaris (Dingle et al.: JEB 2009; Evolution 2011) Presence of high notes strongly associated with high levels of high-frequency ambient noise What about response levels? Do wood-wrens recognize birds from their own habitat? Divergent environmental selection?

39. Recognition and discrimination tested through playback experiments 2 subspecies leucophrys hilaris Andes Peru Columbia Pacific ocean 2 playback songs: In adjacent populations: far-away own nearby other far-away own nearby other (Dingle et al.: JEB 2009; Evolution 2011)

40. Activity time(s) Activity time (s) Playback: results Significantly decreased response strength at high-elevation to nearby other habitat but not to far-away own habitat (Dingle et al.: JEB 2009; Evolution 2011) 99 124 92 98 27 167 100 202

41. Little summary: Spectral divergence possibly related to noise profile Maintenance of divergence in song despite contact zone Spectral divergence very likely related to noise profile Discrimination of songs from other at high elevation Discrimination of songs from other habitat in rainforest Divergence in song and morphology despite gene flow

42. Habitat degradation

43. Habitat degradation can be related to very specific changes in the noise profile Habitat-specific noise profiles, related to succession and degradation, have potential value for monitoring changes in animal communities and assessing forest health

44. ANOVA, F = 232.48, P = 0.004, with habitat and song type as fixed factors and sites as random factor nested within habitat (Smith et al.: Mol. Ecol. 2008) Song changes with habitat degradation?

45. ANOVA, F = 232.48, P = 0.004, with habitat and song type as fixed factors and sites as random factor nested within habitat (Smith et al.: Mol. Ecol. 2008) Song changes with habitat degradation? Variation in environmental selection pressures among forest locations, related to succession or degradation, have the potential to affect evolutionary processes of differentiation

46. (speculation Slabbekoorn: Bogota 2011) Habitat-degradation in the Andes: moving up the mountain? Anthropogenic impact, through forest degradation, global warming, or urbanization, has the potential to undermine the balance in evolutionary processes and the coexistence of (sub)species URBAN NOISE

47. Does traffic noise affect urban bird song? Can we learn from cities about the forest? Roads, highways, and cities yield a noise profile opposite of what is found in many forests

48. Time (seconds) Frequency (kHz) 10.0 8.0 6.0 4.0 2.0 0 0.5 1.0 1.5 Leiden - quiet territory

49. Time (seconds) Frequency (kHz) 10.0 8.0 6.0 4.0 2.0 0 0.5 1.0 1.5 Leiden - noisy territory

50. 2750 3000 3250 3500 3750 4000 40 45 50 55 60 65 (Slabbekoorn & Peet: Nature 2003) Minimum Frequency (Hz) Pearson’s r = 0.377, n = 32 & p < 0.05 Noise level in dB(A) Loud low-frequency noise correlated to singing at higher frequencies in Leiden great tits

51. Amsterdam Berlin London Paris Prague Does traffic noise also lead to habitat differences at the population level?

52. Ten cities and ten forest sites

53. Liesbos 01 Time (seconds) Frequency (kHz) 10.0 8.0 6.0 4.0 2.0 0 0.5 1.0 1.5 We recorded 252 forest individuals (17-39 per site with 24-52 different song types ).

54. Prague 20 Time (seconds) Frequency (kHz) 10.0 8.0 6.0 4.0 2.0 0 0.5 1.0 1.5 We recorded 213 forest individuals (16-27 per site with 24-35 different song types ).

55. Frequency (kHz) Paired t-test: n=10, t=7.86, p < 0.001 Forest Urban Ten city-forest pairs across Europe are consistently different in frequency use (Slabbekoorn & den Boer-Visser: Current Biology 2006) Urban noise affects frequency use in urban birds in a way that reduces masking Urban and forest noise can have the same impact on song divergence among populations of the same species

56. Soundscapes of the forest Implications for evolution Applications for conservation Soundscapes Ambient noise affects song evolution Song important to ecological speciation Ecological gradients important to current and future biodiversity: listen to the forest!

57. Soundscapes of the forest THANK YOU Tom Smith Caroline Dingle Wouter Halfwerk Lina Caro Paula Caycedo Rosales

59. (Verzijden et al. JEB 2010) Urban noise provides opportunity for experimentation: Highway versus Riverside

60. Urban noise provides opportunity for experimentation: Highway versus Riverside A4

61. 2400 2600 2800 3000 3200 highway riverside riverside + noise playback riverside 1 day after noise playback Minimum Frequency (Hz) a a b b (mean+/- s.e.), letters indicate significant differences. Chiffchaffs sing higher along highway like great tits (Verzijden et al. JEB 2010)

62. 2400 2600 2800 3000 3200 highway riverside riverside + noise playback riverside 1 day after noise playback Frequency (Hz) a a b b (mean+/- s.e.), letters indicate significant differences. Chiffchaffs sing higher along highway and immediately shift upwards with noise playback at quiet riverside (Verzijden et al. JEB 2010)

63. H (Halfwerk et al. unpublished) Distinct acoustic barrier despite plasticity related to song learning Genetic leakage associated with heterospecific song copying? H H H H H H L L L L

64. &quot;Soundscapes of the forest: implications for evolution and applications for conservation&quot; Environments are full of biotic and abiotic sounds which yield an acoustic landscape, or so-called soundscape, that varies in time and space. Soundscapes of the forest are different from those from the desert or urban areas. There is also significant variation among different types of forest, which has relevance for two aspects that will be addressed: implications for evolution and applications for conservation. First, many animals use sounds as acoustic signals that play a crucial role in survival and reproduction. The habitat- and community-specific soundscapes strongly determine the ecological space available for specific animal species and their acoustic signals. Therefore, we can learn a lot about evolution in the forest by listening in the forest. Second, fragmentation and degradation of forest typically affect the distribution and character of biotic and abiotic sound sources. Such often human-induced changes in natural soundscapes may have secondary consequences for the remaining animal community and alter local selection pressures. Consequently, an acoustic trace of damage may make sound recording and analyses a unique tool for habitat quality assessment and maybe an attractive method to monitor and broadcast conservation efforts.