Humpback whale song occurrence reflects ecosystem variability in feeding and migratory habitat of the northeast Pacific
Autoři:
John P. Ryan aff001; Danelle E. Cline aff001; John E. Joseph aff002; Tetyana Margolina aff002; Jarrod A. Santora aff003; Raphael M. Kudela aff004; Francisco P. Chavez aff001; J. Timothy Pennington aff001; Christopher Wahl aff001; Reiko Michisaki aff001; Kelly Benoit-Bird aff001; Karin A. Forney aff005; Alison K. Stimpert aff007; Andrew DeVogelaere aff008; Nancy Black aff009; Mark Fischer aff010
Působiště autorů:
Monterey Bay Aquarium Research Institute, Moss Landing, California, United States of America
aff001; Department of Oceanography, Naval Postgraduate School, Monterey, California, United States of America
aff002; Department of Applied Mathematics, University of California Santa Cruz, Santa Cruz, California, United States of America
aff003; Ocean Sciences Department, University of California Santa Cruz, Santa Cruz, California, United States of America
aff004; Marine Mammal & Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Moss Landing, California, United States of America
aff005; Moss Landing Marine Laboratories, San Jose State University, Moss Landing, California, United States of America
aff006; Bioacoustics/Vertebrate Ecology, San Jose State University, Moss Landing Marine Laboratories, Moss Landing, California, United States of America
aff007; Monterey Bay National Marine Sanctuary, National Ocean Service, National Oceanic and Atmospheric Administration, Monterey, California, United States of America
aff008; Monterey Bay Whale Watch, Monterey, California, United States of America
aff009; Aguasonic Acoustics, Santa Clara, California, United States of America
aff010
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222456
Souhrn
This study examines the occurrence of humpback whale (Megaptera novaeangliae) song in the northeast Pacific from three years of continuous recordings off central California (36.713°N, 122.186°W). Song is prevalent in this feeding and migratory habitat, spanning nine months of the year (September–May), peaking in winter (November–January), and reaching a maximum of 86% temporal coverage (during November 2017). From the rise of song in fall through the end of peak occurrence in winter, song length increases significantly from month to month. The seasonal peak in song coincides with the seasonal trough in day length and sighting-based evidence of whales leaving Monterey Bay, consistent with seasonal migration. During the seasonal song peak, diel variation shows maximum occurrence at night (69% of the time), decreasing during dawn and dusk (52%), and further decreasing with increasing solar elevation during the day, reaching a minimum near solar noon (30%). Song occurrence increased 44% and 55% between successive years. Sighting data within the acoustic detection range of the hydrophone indicate that variation in local population density was an unlikely cause of this large interannual variation. Hydrographic data and modeling of acoustic transmission indicate that changes in neither habitat occupancy nor acoustic transmission were probable causes. Conversely, the positive interannual trend in song paralleled major ecosystem variations, including similarly large positive trends in wind-driven upwelling, primary productivity, and krill abundance. Further, the lowest song occurrence during the first year coincided with anomalously warm ocean temperatures and an extremely toxic harmful algal bloom that affected whales and other marine mammals in the region. These major ecosystem variations may have influenced the health and behavior of humpback whales during the study period.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Physical sciences – Psychology – Animals – Social sciences – Vertebrates – Amniotes – Mammals – Zoology – Physics – Behavior – Earth sciences – Ecology and environmental sciences – Ecology – Ecosystems – Animal behavior – Marine biology – Marine and aquatic sciences – Habitats – Seasons – Bioacoustics – Acoustics – Foraging – Animal sexual behavior – Marine mammals – Whales – Humpback whales – Animal migration – Seasonal variations
Zdroje
1. Payne RS, McVay S. Songs of Humpback Whales. Science. 1971; 173 (3997): 585–597. doi: 10.1126/science.173.3997.585 17833100
2. Cholewiak DM, Sousa‐Lima RS, Cerchio S. Humpback whale song hierarchical structure: Historical context and discussion of current classification issues. Mar Mamm Sci. 2013; 29:E312–E332.
3. Frankel AS, Clark CW, Herman LM, Gabriele CM. Spatial distribution, habitat utilization, and social interactions of humpback whales, Megaptera novaeangliae, off Hawai’i, determined using acoustic and visual techniques. Can J Zool. 1995; 73, 1134–1146.
4. Smith JN, Goldizen AW, Dunlop RA, Noad MJ. Songs of male humpback whales, Megaptera novaeangliae, are involved in intersexual interactions. Animal Behav. 2008; 76(2): 467–477. doi: 10.1016/j.anbehav.2008.02.013
5. Cholewiak DM, Cerchio S, Jacobsen JK, Urbán- R. J, Clark CW. Songbird dynamics under the sea: acoustic interactions between humpback whales suggest song mediates male interactions. R Soc Open Sci. 2018; doi: 10.1098/rsos.171298 29515847
6. Norris TF, McDonald M, Barlow J. Acoustic detections of singing humpback whales (Megaptera novaeangliae) in the eastern North Pacific during their northbound migration. J Acoust Soc Am. 1999; 106:506–514. doi: 10.1121/1.427071 10420640
7. Mercado E III. The Sonar Model for Humpback Whale Song Revised. Front Psychol. 2018; 9:1156. doi: 10.3389/fpsyg.2018.01156 30061851
8. Noad MJ, Cato DH, Bryden MM, Jenner M, Jenner KCS. Cultural revolution in whale songs. Nature. 2000; 408:537. doi: 10.1038/35046199 11117730
9. Garland EC, Goldizen AW, Rekdahl ML, Constantine R, Garrigue C, Hauser ND, et al. Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale. Curr Biol. 2011; 21(8):687–691. doi: 10.1016/j.cub.2011.03.019 21497089
10. Fournet MEH, Gabriele CM, Culp DC, Mellinger DK, Sharpe F, Klinck H. Some things never change: multi-decadal stability in humpback whale calling repertoire on Southeast Alaskan foraging grounds. Sci Rep. 2018; 8(1): 13186 doi: 10.1038/s41598-018-31527-x 30262835
11. Mattila DK, Guinee LN, Mayo CA. Humpback whale songs on a North Atlantic feeding ground. J Mammal. 1987; 68(4): 880–883.
12. McSweeney DJ, Chu KC, Dolphin WF, Guinee, LN. North Pacific humpback whale songs: a comparison of southeast Alaskan feeding ground songs with Hawaiian wintering ground songs. Mar Mamm Sci. 1989; 5(2):139–148. doi: 10.1111/j.1748-7692.1989.tb00328.x
13. Charif RA, Clapham PJ, Clark CW. Acoustic detections of singing humpback whales in deep waters off the British Isles. Mar Mamm Sci. 2001; 17(4): 751–768. doi: 10.1111/j.1748-7692.2001.tb01297.x
14. Clark CW, Clapham PJ. Acoustic monitoring on a humpback whale (Megaptera novaeangliae) feeding ground shows continual singing into late spring. Proc R Soc Lond B. 2004; 271:1051–1057. doi: 10.1098/rspb.2004.2699 15293859
15. Vu ET, Risch D, Clark CW, Gaylord S, Hatch LT, Thompson MA, et al. Humpback whale song occurs extensively on feeding grounds in the western North Atlantic Ocean. Aquat Biol. 2012; 14:175–183. doi: 10.3354/ab00390
16. Stimpert AK, Peavey LE, Friedlaender AS, Nowacek DP. Humpback whale song and foraging behavior on an Antarctic feeding ground. PLoS ONE. 2012; 7(12): e51214. doi: 10.1371/journal.pone.0051214 23284666
17. Español-Jiménez S, van der Schaar M. First record of humpback whale songs in Southern Chile: Analysis of seasonal and diel variation. Mar Mamm Sci. 2018; 34(3):718–733. doi: 10.1111/mms.12477
18. Kowarski K, Evers C, Moors‐Murphy H, Martin B, Denes SL. Singing through winter nights: Seasonal and diel occurrence of humpback whale (Megaptera novaeangliae) calls in and around the Gully MPA, offshore eastern Canada. Mar Mamm Sci. 2018; 34: 169–189. doi: 10.1111/mms.12447
19. Magnúsdóttir EE, Lim R. Subarctic singers: Humpback whale (Megaptera novaeangliae) song structure and progression from an Icelandic feeding ground during winter. PLoS ONE. 2019; 14(1): e0210057. doi: 10.1371/journal.pone.0210057 30673737
20. Clapham PJ, Mattila DK. Humpback whale songs as indicators of migration routes. Mar Mamm Sci. 1990; 6: 155–160. doi: 10.1111/j.1748-7692.1990.tb00238.x
21. Dawbin WH, Gill PC. Humpback whale survey along the west coast of Australia: a comparison of visual and acoustic observations. Mem Qld Mus. 1991; 30: 255–257.
22. Bettridge S, Baker CS, Barlow J, Clapham PJ, Ford M, Gouveia D, et al. Status review of the humpback whale (Megaptera novaeangliae) under the endangered species act. NOAA -TM-NMFS-SWFSC-540. 2015. U. S. Department of Commerce.
23. Baker CS, Palumbi SR, Lambertsen RH, Weinrich MT, Calambokidis J, O’Brien SJ. Influence of seasonal migration on the distribution of mitochondrial DNA haplotypes in humpback whales. Nature. 1990; 344:238–240. doi: 10.1038/344238a0 1969116
24. Baker CS, Slade RW, Bannister JL, Abernethy RB, Weinrich MT, Lien J, et al. Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, world-wide. Mol Ecol. 1994; 3:313–327. 7921358
25. Baker CS, Steel D, Calambokidis J, Falcone E, González-Peral U, Barlow J, et al. Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales. Mar Ecol Prog Ser. 2013; 494:291–306. doi: 10.3354/meps10508
26. Steiger GH, Calambodikis J, Sears R, Balcomb KC, Cubbage JC. Movement of humpback whales between California and Costa Rica. Mar Mamm Sci. 1991; 7:306–310. doi: 10.1111/j.1748-7692.1991.tb00105.x
27. Calambokidis J, Steiger GH, Evenson JR, Flynn KR, Balcomb KC, Claridge DE, et al. Interchange and isolation of humpback whales off California and other feeding grounds in the North Pacific. Mar Mamm Sci. 1996; 12:215–226. doi: 10.1111/j.1748-7692.1996.tb00572.x
28. Calambokidis J, Steiger GH, Rasmussen K, Urbán J, Balcomb KC, Ladrón de Guevara P, et al. Migratory destinations of humpback whales that feed off California, Oregon and Washington. Mar Ecol Prog Ser. 2000; 192:295–304. doi: 10.3354/meps192295
29. Urbán J, Jaramillo A, Aguayo A, Ladrón de Guevara P, Salinas M, Alvarez C, et al. Migratory destinations of humpback whales wintering in the Mexican Pacific. J Cetacean Res Manag. 2000; 2: 101–110.
30. Calambokidis J, Barlow J. Abundance of blue and humpback whales in the eastern North Pacific estimated by capture‐recapture and line‐transect methods. Mar Mamm Sci. 2004; 20: 63–85. doi: 10.1111/j.1748-7692.2004.tb01141.x
31. Online: https://sanctuarysimon.org/1970/02/historic-whaling-in-moss-landing/.
32. Ryther JH. Photosynthesis and Fish Production in the Sea. Science. 1969; 166 (3901): 72–76. doi: 10.1126/science.166.3901.72 5817762
33. Huyer A. Coastal upwelling in the California Current System. Prog Oceanogr. 1983; 12:259–284. doi: 10.1016/0079-6611(83)90010-1
34. Barber RT, Smith RL. Coastal upwelling ecosystems. In: Longhurst AR, editor. Analysis of Marine Ecosystems. Academic; 1981. pp. 31–68.
35. Carr ME, Kearns EJ. Production regimes in four Eastern Boundary Current systems. Deep Sea Res Part II Top Stud Oceanogr. 2003; 50:3199–3221. doi: 10.1016/j.dsr2.2003.07.015
36. Chavez FP, Messié M. A comparison of Eastern Boundary Upwelling Ecosystems. Prog Oceanogr. 2009; 83: 80–96. doi: 10.1016/j.pocean.2009.07.032
37. Santora JA, Sydeman WJ, Schroeder ID, Wells BK, Field JC. Mesoscale structure and oceanographic determinants of krill hotspots in the California Current: Implications for trophic transfer and conservation. Prog Oceanogr. 2011; 91:397–409. doi: 10.1016/j.pocean.2011.04.002
38. Santora JA, Field JC, Schroeder, Sakuma KM, Wells BK, Sydeman WJ. Spatial ecology of krill, micronekton and top predators in the central California Current: Implications for defining ecologically important areas. Prog Oceanogr. 2012; 106:154–174. doi: 10.1016/j.pocean.2012.08.005
39. Santora JA, Zeno R, Dorman JG, Sydeman WJ. Submarine canyons represent an essential habitat network for krill hotspots in a Large Marine Ecosystem. Sci Rep. 2018; 8(1). doi: 10.1038/s41598-018-25742-9 29765085
40. Calambokidis J, Steiger GH, Curtice C, Harrison J, Ferguson MC, Becker EA, et al. Biologically important areas for selected cetaceans within U.S. waters ‐ West Coast region. Aquat Mamm. 2015; 41(1): 39–53. doi: 10.1578/AM.41.1.2015.39
41. Becker EA, Forney KA, Fiedler PC, Barlow, Chivers SJ, Edwards CA, et al. Moving Towards Dynamic Ocean Management: How Well Do Modeled Ocean Products Predict Species Distributions? Remote Sens. 2016; 8:149. doi: 10.3390/rs8020149
42. Becker EA, Forney KA, Redfern JV, Barlow J, Jacox MG, Roberts JJ, et al. Predicting cetacean abundance and distribution in a changing climate. Divers Distrib. 2019; 25: 626–643. doi: 10.1111/ddi.12867
43. Ryan J, Cline D, Dawe C, McGill P, Zhang Y, Joseph J, et al. New passive acoustic monitoring in Monterey Bay National Marine Sanctuary. OCEANS MTS/IEEE, Monterey, CA. 2016; pp. 1–8. doi: 10.1109/OCEANS.2016.7761363
44. Online: cetus.ucsd.edu/technologies_Software.html.
45. Online: http://www.cs.wisc.edu/condor.
46. Online: naif.jpl.nasa.gov/naif/.
47. Collins MD. A split-step Padé solution for the parabolic equation method. J Acoust Soc Am. 1993; 93:1736–1742. doi: 10.1121/1.406739
48. Au WWL, Pack AA, Lammers MO, Herman LM, Deakos MH, Andrews K. Acoustic properties of humpback whale songs. J Acoust Soc Am. 2006; 120(2):1103–1110. doi: 10.1121/1.2211547 16938996
49. Online: https://podaac.jpl.nasa.gov/Integrated_Multi-Mission_Ocean_AltimeterData.
50. Auad G, Roemmich D, Gilson J. The California Current System in relation to the Northeast Pacific Ocean circulation. Prog Oceanogr. 2011; 91:576–592.
51. Schwing FB, O’Farrell M, Steger JM, Baltz K. Coastal upwelling indices west coast of North America 1946–95. NOAA-TM-NMFS-SWFSC-231. 1996. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service.
52. Online: https://coastwatch.pfeg.noaa.gov/erddap.
53. Rudnick DL, Zaba KD, Todd RE, Davis RE. A climatology of the California Current System from a network of underwater gliders. Prog Oceanogr. 2017; 154:64–106. doi: 10.1016/j.pocean.2017.03.002
54. Pennington JT, Chavez FP. Seasonal fluctuations of temperature, salinity, nitrate, chlorophyll and primary production at station H3/M1 over 1989–1996 in Monterey Bay, California. Deep Sea Res Part II Top Stud Oceanogr. 2000; 47(5–6):947–973. doi: 10.1016/S0967-0645(99)00132-0
55. Scholin CA, Gulland F, Doucette GJ, Benson S, Busman M, Chavez FP, et al. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature. 2000; 403, 80–84. doi: 10.1038/47481 10638756
56. Trainer VL, Bates SS, Lundholm N, Thessen AE, Adams NG, Cochlan WP, et al. Pseudo‐nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae. 2012; 14, 271–300.
57. Kudela R, Pitcher G, Probyn T, Figueiras F, Moita T, Trainer V. Harmful algal blooms in coastal upwelling systems. Oceanography. 2005; 18, 184–197.
58. Van Dolah FM (2005) Effects of harmful algal blooms. In: Reynolds J, Perrin W, Reeves R, Montgomery S, Ragen T, editors. Marine mammal research: conservation beyond crisis. Johns Hopkins University Press; 2005. pp. 85–101.
59. Fire SE, Wang Z, Leighfield TA, Morton SL, McFee WE, McLellan WA, et al. Domoic acid exposure in pygmy and dwarf sperm whales (Kogia spp.) from southeastern and mid-Atlantic U.S. waters. Harmful Algae. 2009; 8(5):658–664. doi: 10.1016/j.hal.2008.12.002
60. Fire SE, Wang Z, Berman M, Langlois GW, Morton SL, Sekula-Wood E, et al. Trophic transfer of the harmful algal toxin domoic acid as a cause of death in a minke whale (Balaenoptera acutorostrata) stranding in southern California. Aquat Mamm. 2010; 36(4):342–350. doi: 10.1578/AM.36.4.2010.342
61. McCabe RM, Hickey BM, Kudela RM, Lefebvre KA, Adams NG, Bill BD, et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett. 2016; 43, 10,366–10,376, doi: 10.1002/2016GL070023 27917011
62. Lane JQ, Roddam CM, Langlois GW, Kudela RM. Application of Solid Phase Adsorption Toxin Tracking (SPATT) for field detection of the hydrophilic phycotoxins domoic acid and saxitoxin in coastal California. Limnol Oceanogr Methods. 2010; 8, 645–660.
63. Online: http://sccoos.org.
64. Sakuma KM, Field JC, Mantua NJ, Ralston S, Marinovic BB, Carrion CN. Anomalous epipelagic micronekton assemblage patterns in the neritic waters of the California Current in spring 2015 during a period of extreme ocean conditions. CalCOFI Rep. 2016; 57: 163−183.
65. Ralston S, Field JC, Sakuma KM. Long-term variation in a central California pelagic forage assemblage. J Mar Syst. 2015; 146: 26−37.
66. Santora JA, Hazen EL, Schroeder ID, Bograd SJ, Sakuma KM, Field JC. Impacts of ocean climate variability on biodiversity of pelagic forage species in an upwelling ecosystem. Mar Ecol Prog Ser. 2017; 580:205–220. doi: 10.3354/meps12278
67. Szoboszlai AI, Thayer JA, Wood SA, Sydeman WJ, Koehn LE. Forage species in predator diets: synthesis of data from the California Current. Ecol Inform. 2015; 29:45–56.
68. Santora JA, Schroeder ID, Field JC, Wells BK, Sydeman WJ. Spatio-temporal dynamics of ocean conditions and forage taxa reveals regional structuring of seabird−prey relationships. Ecol Appl. 2014; 24: 1730−1747. 29210234
69. Fleming AH, Clark CT, Calambokidis J, Barlow J. Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current. Glob Change Biol. 2016; 22: 1214–1224. doi: 10.1111/gcb.13171 26599719
70. Online: https://www.integratedecosystemassessment.noaa.gov/regions/california-current/cc-indicator-status-trends.
71. Thompson AR, Schroeder ID, Bograd SJ, Hazen EL, Jacox MG, Leising A, et al. (2018) State of the California Current, 2017–18. CalCOFI Rep. 2018; 59. California Cooperative Oceanic Fisheries Investigations. University of California, San Diego.
72. Wright A, Walsh L. Mind the gap: Why neurological plasticity may explain seasonal interruption in humpback whale song. J Mar Biol Assoc U.K. 2010; 90(8):1489–1491. doi: 10.1017/S0025315410000913
73. Cates KA, Atkinson S, Gabriele CM, Pack AA, Straley JM, Yin S. Testosterone trends within and across seasons in male humpback whales (Megaptera novaeangliae) from Hawaii and Alaska. Gen Comp Endocrinol. 2019; 279:164–173. doi: 10.1016/j.ygcen.2019.03.013 30904390
74. Au WW, Mobley J, Burgess WC, Lammers MO, Nachtigall PE. Seasonal and diurnal trends of chorusing humpback whales wintering in waters off western Maui. Mar Mamm Sci. 2000; 16: 530–544. doi: 10.1111/j.1748-7692.2000.tb00949.x
75. Helweg DA, Herman LM. Diurnal patterns of behaviour and group membership of humpback whales (Megaptera novaeangliae) wintering in Hawaiian waters. Ethology. 1994; 98: 298–311. doi: 10.1111/j.1439-0310.1994.tb01078.x
76. Gentemann CL, Fewings MR, García-Reyes M. Satellite sea surface temperatures along the west coast of the United States during the 2014–2016 northeast Pacific marine heat wave. Geophys Res Lett. 2017; 44:312–319. doi: 10.1002/2016GL071039
77. Benson SR, Croll DA, Marinovic BB, Chavez FP, Harvey JT. Changes in the cetacean assemblage of a coastal upwelling ecosystem during El Niño 1997–98 and La Niña 1999. Prog Oceanogr. 2002; 54:279–291. doi: 10.1016/S0079-6611(02)00054-X.
78. Chavez FP, Pennington JT, Castro CG, Ryan JP, Michisaki RP, Schlining B, et al. Biological and chemical consequences of the 1997–98 El Niño in central California waters. Prog Oceanogr. 2002; 54:205–232.
79. Ryan JP, Kudela RM, Birch JM, Blum M, Bowers HA, Chavez FP, et al. Causality of an extreme harmful algal bloom in Monterey Bay, California, during the 2014–2016 northeast Pacific warm anomaly. Geophys Res Lett. 2017; 44: 5571–5579. doi: 10.1002/2017GL072637
80. Calambokidis J, Barlow J, Flynn K, Dobson E, Steiger GH. Update on abundance, trends, and migrations of humpback whales along the US West Coast. 2017. International Whaling Commission Paper SC/A17/NP/13. 17 pp.
81. Chamberlin TC. The method of multiple working hypotheses. Science. 1890; reprinted 1965; 148(3671): 754–759. doi: 10.1126/science.148.3671.754 17748786
82. Gedamke J, Harrison J, Hatch L, Angliss R, Barlow J, Berchok C, et al. NOAA Ocean Noise Strategy Roadmap. NOAA. 2016; 138pp. Online: https://cetsound.noaa.gov/road-map.
83. Office of National Marine Sanctuaries. Monterey Bay National Marine Sanctuary Condition Report partial update: a new assessment of the state of Sanctuary resources. 2015. U.S. Department of Commerce, NOAA, Office of National Marine Sanctuaries, Silver Spring, MD. 133 pp.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania