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On the Sperm Whale (Physeter Macrocephalus) Ecology, Sociality and Behavior Off Ischia Island (Italy): Patterns of Sound Production and Acoustically Measured Growth

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On the Sperm Whale (Physeter Macrocephalus) Ecology, Sociality and Behavior Off Ischia Island (Italy): Patterns of Sound Production and Acoustically Measured Growth DEPARTMENT OF ENVIRONMENTAL BIOLOGY “CHARLES DARWIN” SAPIENZA UNIVERSITY OF ROME PHD IN ENVIRONMENTAL AND EVOLUTIONARY BIOLOGY ANIMAL BIOLOGY CURRICULUM XXVIII CYCLE On the sperm whale (Physeter macrocephalus) ecology, sociality and behavior off Ischia Island (Italy): patterns of sound production and acoustically measured growth by Daniela Silvia Pace Tutor: Prof. Giandomenico Ardizzone, Sapienza University of Rome, Italy External Reviewer: Prof. Gianni Pavan, University of Pavia, Italy Rome, November 2016 Table of contents _____________________________________________________________________________________________________ List of Figures List of Tables Goals and thesis outline Chapter 1 – Sperm whale biology 1.1 General anatomy ……………………………………………………………………………………………………………... 1 1.2 Abundance, distribution and movements ………………………………………………………………………….. 2 1.3 Reproduction and social structure ……………………………………………………………………………………. 5 1.4 Feeding and main prey …………………………………………………………………………………………………….. 7 1.5 Diving behavior …………………………………………………….…………………………………………………………. 8 1.6 Threats and conservation ………………………………………………………………………………………………… 9 Chapter 2 – Sperm whale acoustics 2.1 The spermaceti organ …………………………………………………………………………………………….……… 12 2.2 Click structure ………………………………………………………………………………………………………………. 14 2.3 Type of sounds ……………………………………………………………………………………………………………… 16 2.3.1 Usual clicks ………………………………………………………………………….…….………………..…… 16 2.3.2 Creaks …………………………………………………..……………………………………………………..…. 17 2.3.3 Codas …………………………………………….……………………………………………………………..… 19 2.3.4 Slow clicks and gunshots ……………………………………………………………………………..….. 20 2.3.5 Tonal sounds and other vocalizations ...……………...…………………………………………..… 22 2.4 Click development …………………………………………………………………………………………..………….…. 24 2.5 Ears and hearing …………………………………………………………………………………………………………… 24 Chapter 3 – Setting the scene: what do we know about sperm whales off Ischia Island? 3.1 Study area ……………………………………………………………………………………………………………….……. 26 3.2 Surveys and data collection ………………………………………………..……………………………………….…. 29 3.3 Distribution and encounter rate ………………………………………………………………………………….…. 31 3.3.1. Methods ………………………………………………………………………………...…………………….… 31 3.3.2. Results …………………………………………………………………………………………...………...….… 32 3.3.3. Discussion ……………………………………………………………………………………………………… 38 3.4 Habitat suitability ……………………………………………………..……….………………………………………….. 39 3.4.1. Methods ……………………………………………………………………………………………………..….. 40 3.4.2. Results …………………………………………………………………………………………………………… 41 3.4.3. Discussion ……………………………………………………………………………………………………… 45 - ii - 3.5 Photoidentification and group composition ………………………………………………………………..….. 48 3.5.1. Methods ……………………………………………………………………………………………………..….. 48 3.5.2. Results …………………………………………………………………………………………………..………. 50 3.5.3. Discussion ……………………………………………………………………………………………………… 53 3.6 Dives and surface periods .…………………………………………………………………………………….……….. 56 3.6.1. Methods ……………………………………………………………………………………………………...…. 56 3.6.2. Results …………………………………………………………………………………………………………… 58 3.6.3. Discussion ……………………………………………………………………………………………………… 62 Chapter 4 – Patterns of sound production 4.1 Data collection …………………………………………………………..………………………………………..………… 65 4.2 Acoustic repertoire and habitat use …………….…………………………………………………………………. 66 4.2.1 Methods ……………………..…………………………………….……………………………………….……. 66 4.2.2 Results …………………………………………….……………………………………………………..………. 70 4.2.3 Discussion ……………………………………………………………………………………………….….….. 72 4.3 Social vocalizations: codas ………………………….……………………………………..…………….…………….. 77 4.3.1 Methods ………………………..………………………………………………………………………..………. 77 4.3.2 Results ……………………………………….………………………………………………………..…………. 79 4.3.3 Discussion ……………………………………………………………………………………………….……... 83 4.4 Unusual vocalizations: trumpets …………………………………………………………………………................ 88 4.4.1 Methods ………………………..…………………………………………………………………….….………. 89 4.4.2 Results ……………………………………….………………………………………………………………..…. 89 4.4.3 Discussion …………………………………………………………………………………………….………... 94 Chapter 5 – Acoustically derived growth rate 5.1 Introduction …………………………………………………………………………………………………………………. 95 5.2 Methods ………………………………………………………………………..………………..…………………..………… 99 5.3 Results ………………………………………………………………………………………………………….…………….. 103 5.4 Discussion …………………………………………………………………………………………………….…………….. 109 Chapter 6 – Conclusions and future directions Acknowledgments References - iii - List of figures ____________________________________________________________________________________ Figure 1. Global distribution of the sperm whale. The red dashed lines indicate the range of females and immature males. Figure 2(1). (A) Left lateral view (dorsal pointing up) of the reconstructed sperm whale head; dense connective tissue (case, rein of case) and maxillonasolabialis muscle semi-transparent. (B) Sagittal view of the reconstructed sperm whale head (dorsal pointing up, tip of nose facing left). The green line represents the proposed acute-angled main acoustic pathway throughout the bent acoustic horn and their (preceding) reverberation within the spermaceti organ. On its presumed path, the sound waves travel through the connecting acoustic window (CAW) into the junk and are released via the terminal acoustic window (TAW) into the water (bent horn acoustic hypothesis). Figure 2(2). Position and structure of the monkey lips in the sperm whale nasal complex (both figures from Huggenberger et al., 2014). Figure 3. Evolutionary tree of sperm whales, showing the relationships of extinct and living species, and when reduction of the spermaceti organ took place. Figure 4. On-axis and off-axis clicks according to the bent-horn model of sound production. Figure 5. Spectrogram and waveform of a usual click sequence produced at depth in the Mediterranean Sea. Figure 6. Spectrogram and waveform of a creak sequence produced at depth in the Mediterranean Sea. Figure 7. Spectrogram and waveform of a coda-creak sequence produced at surface in the Mediterranean Sea. Figure 8. Spectrogram and waveform of a fast click (or chirrup) sequence produced at surface in the Mediterranean Sea. Figure 9. Spectrogram and waveform of a coda sequence produced at surface in the Mediterranean. Figure 10. Spectrogram and waveform of a slow click sequence produced at depth in the Mediterranean Sea. Figure 11. Spectrogram and waveform of a squeal produced at surface in the Mediterranean Sea. Figure 12. Spectrogram and waveform of a trumpet produced near the surface in the Mediterranean Sea. The armonic structure and the modulation frequency of the sub-units are well represented. Figure 13. The study area is located in the central Tyrrhenian Sea (Mediterranean Sea, Italy) and includes the Pontine Archipelago in the Gulf of Gaeta (white circle) and the Campanian Arcipelago in Gulf of Naples (red cirlce). Figure 14. The submarine canyon of Cuma (modified from Pennetta et al., 1998; de Alteriis and Toscano, 2003). Figure 15. The marine region around Ischia and Capri Islands (source: D’Argenio et al., 2004). Figure 16. Map of Regno di Nettuno MPA. Zones A-D fall under the protection of the MPA with varying levels of restrictions. Figure 17. The research vessel Jean Gab (© Oceanomare Delphis Onlus). Figure 18. Routes effort (2002-2015). Figure 19. Sperm whale encounter rate in the study area (2002-2015). - iv - Figure 20. Overall and yearly encounters and tracking lines during 2004-2015 period. Different encounter types (see section 3.5) are represented as following: indicates social units (SU) of females and immatures; indicates clusters (CL) of whales comprising immature males (‘bachelor groups’) or individuals of unknown sex/age class (possibly males); indicates solitary whales. Figure 21. Mean values of depth (m), slope (%) and distance from coast (km) of the encounters over the study period (2002-2015). Figure 22. Survey effort during 2007-2015 period. Figure 23. Mean AUC (red line) for assessing the predictive accuracy of suitable habitat on a scale of 0 to 1 in (a) all sperm whale encounters, (b) solitary individuals (SI), (c) clusters (CL), and (d) social units (SU). Figure 24. Jackknife tests of variable contributions for informing the model training gain for predicting suitable habitat for (a) all encounters, (b) solitary individuals (SI), (c) clusters (CL), and (d) social units (SU). Models were run with each variable in isolation (blue bars) and with each variable excluded (green bars). The red bars indicate the model run with all variables included. Figure 25. Suitability habitat map for (a) all sperm whale encounters, (b) solitary individuals (SI), (c) clusters (CL) and (d) social units (SU). Figure 26. Discovery curve by cumulative number of identifications. Figure 27. Genital area of a male sperm whale from underwater video (from Pace et al., 2014; ©Oceanomare Delphis Onlus). Figure 28. Boxplots of the dive cycle duration in different encounter types during 2009-2015 surveys. Figure 29. Boxplots of the diving phase duration in different encounter types during 2009-2015 surveys. Figure 30. Boxplots of the surfacing phase duration in different encounter types in 2009-2015 surveys. Figure 31. Boxplots of blow rate in different encounter types during 2009-2015 surveys. Figure 32. Scatterplots of the relationship between dive cycle variables in different encounter types during 2009-2015 surveys. Figure 33. Spectrogram of a sperm whale usual click (UC) sequence followed by a phase of transition clicks (TR) continunuing in a creak (CR) sequence. Figure 34. Spectrogram of a sperm whale usual click (UC)-transition click
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