Abstract
Age composition is an important population parameter for understanding and managing endangered species. There are very few studies involving cetaceans in estimating the age of individuals in the wild. In this study, we rigorously quantified the body color pattern of 37 stranded Indo-Pacific humpback dolphins (Sousa chinensis) of the Pearl River Estuary (PRE), which showed a significant, albeit with variability between individuals, correlation with age for both the males (between age 1 and 35, r2 = 0.84) and females (between age 1 and 25, r2 = 0.85). The population-averaged correlation (r2 = 0.85) was then applied to a large volume of photo-identification data (2011–2015) to estimate the age composition of the population occurring in the greater deltaic region, which further suggested a spatial difference in age composition and, therefore, a complex demographic process of the humpback dolphin across the region. In particular, the age composition of humpback dolphins in the east PRE (Lingding Bay) is severely aged. Finally, a population viability analysis with the consideration of observed age structure and the simulated age-specific fecundity suggested that 95.75% of the Lingding Bay humpback dolphins are projected to be lost after three generations. Given the sophisticated anthropogenic landscape in the PRE, we suggest that management units of the humpback dolphins should be clearly defined and the regional-specific conservation measures are much needed.
Similar content being viewed by others
Change history
05 August 2020
The author would like to correct the formula in the publication of the original article.
References
Barros NB, Jefferson TA, Parsons ECM (2004) Feeding habits of Indo-Pacific Humpback Dolphins (Sousa chinensis) stranded in Hong Kong. Aquat Mamm 30:179–188. https://doi.org/10.1578/am.30.1.2004.179
Beissinger SR, Westphal MI (1998) On the use of demographic models of population viability in endangered species management. J Wildl Manag 62:821–841. https://doi.org/10.2307/3802534
Berkeley SA, Chapman C, Sogard SM (2004) Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes Melanops. Ecology 85:1258–1264. https://doi.org/10.2307/3450168
Brown AM, Bejder L, Parra GJ, Cagnazzi D, Hunt T, Smith JL, Allen SJ (2016) Sexual dimorphism and geographic variation in dorsal fin features of Australian Humpback Dolphins, Sousa sahulensis. Adv Mar Biol 73:273–314. https://doi.org/10.1016/bs.amb.2015.08.002
Cañadas A, Aguilar de Soto N, Aissi M et al (2017) The challenge of habitat modelling for threatened low density species using heterogeneous data: the case of Cuvier’s beaked whales in the Mediterranean. Ecol Indic 85:128–136. https://doi.org/10.1016/j.ecolind.2017.10.021
Chan SC, Karczmarski L (2017) Indo-Pacific humpback dolphins (Sousa chinensis) in Hong Kong: modelling demographic parameters with mark-recapture techniques. PLoS ONE 12:e0174029. https://doi.org/10.1371/journal.pone.0174029
Chang WL, Karczmarski L, Huang SL, Gailey G, Chou LS (2016) Reproductive parameters of the Taiwanese humpback dolphin (Sousa chinensis taiwanensis). Reg Stud Mar Sci 8:459–465. https://doi.org/10.1016/j.rsma.2016.08.001
Chen T, Hung SK, Qiu Y, Jia X, Jefferson TA (2010) Distribution, abundance, and individual movements of Indo-Pacific humpback dolphins (Sousa chinensis) in the Pearl River Estuary, China. Mammalia 74:117–125. https://doi.org/10.1515/mamm.2010.024
Chen B, Jefferson TA, Lin Wang HG, Zhang H, Zhou Y, Xu X, Yang G (2018) Geographic variation in pigmentation patterns of Indo-Pacific humpback dolphins (Sousa chinensis) in Chinese waters. J Mammal 99:915–922. https://doi.org/10.1093/jmammal/gyy068/5053874
Chittleborough R (1959) Determination of Age in the Humpback Whale, Megaptera nodosa (Bonnaterre). Mar Freshw Res 10:125–143. https://doi.org/10.1071/MF9590125
Cipro CVZ, Bustamante P, Taniguchi S, Montone RC (2012) Persistent organic pollutants and stable isotopes in pinnipeds from King George Island, Antarctica. Mar Pollut Bull 64:2650–2655. https://doi.org/10.1016/j.marpolbul.2012.10.012
Cosens SE, Blouw A (2003) Size and age-class segregation of bowhead whales summering in Northern Foxe Basin: a photogrammetric analysis. Mar Mammal Sci 19:284–296. https://doi.org/10.1111/j.1748-7692.2003.tb01109.x
Evans K, Hindell MA (2004) The age structure and growth of female sperm whales (Physeter macrocephalus) in southern Australian waters. J Zool 263:237–250. https://doi.org/10.1017/s0952836904005096
Fan X, Cui B, Zhang Z (2012) Spatial variations of river water quality in Pearl River Delta, China. Front Earth Sci 6:291–296. https://doi.org/10.1007/s11707-012-0295-1
Geraci JR, Lounsbury VJ, Yates N (2006) Marine mammals ashore: a field guide for strandings, 2nd edn. National Aquarium in Baltimore
Gerson HB, Hickie JP (1985) Head scarring on male narwhals (Monodon monoceros): evidence for aggressive tusk use. Can J Zool 63:2083–2087. https://doi.org/10.1139/z85-306
Gowans S, Würsig B, Karczmarski L (2008) The social structure and strategies of delphinids: predictions based on an ecological framework. In: David WS (ed) Advances in marine biology. Academic Press, New york, pp 195–294. https://doi.org/10.1016/S0065-2881(07)53003-8
Gui D, Yu R, Karczmarski L, Ding Y, Zhang H, Sun Y, Zhang M, Wu Y (2017) Spatio-temporal trends of heavy metals in Indo-Pacific humpback dolphins (Sousa chinensis) from the western Pearl River Estuary, China. Environ Sci Technol 51:1848–1858. https://doi.org/10.1021/acs.est.6b05566
Gui D, Zhang L, Zhan F, Liu W, Yu X, Chen L, Wu Y (2018) Levels and trends of polycyclic aromatic hydrocarbons in the Indo-Pacific humpback dolphins from the Pearl River Estuary (2012–2017). Mar Pollut Bull 131:693–700. https://doi.org/10.1016/j.marpolbul.2018.04.058
Hartman KL, Wittich A, Cai JJ, van der Meulen FH, Azevedo JMN (2016) Estimating the age of Risso’s dolphins (Grampus griseus) based on skin appearance. J Mammal 97:490–502. https://doi.org/10.1093/jmammal/gyv193
Hernando B, Ibarrola-Villava M, Fernandez LP, Peña-Chilet M, Llorca-Cardeñosa M, Oltra SS, Alonso S, Boyano MD, Martinez-Cadenas C, Ribas G (2016) Sex-specific genetic effects associated with pigmentation, sensitivity to sunlight, and melanoma in a population of Spanish origin. Biol Sex Differ. https://doi.org/10.1186/s13293-016-0070-1
Hilborn R, Waiters CJ (1992) Quantitative fisheries stock assessment: choice, dynamics and uncertainty. Rev Fish Biol Fish 2:177–186. https://doi.org/10.1007/BF00042883
Huang SL, Karczmarski L (2014) Indo-Pacific humpback dolphins: a demographic perspective of a threatened species. Primates and cetaceans: field research and conservation of complex mammalian societies, primatology monographs. Springer, Tokyo, pp 249–272. https://doi.org/10.1007/978-4-431-54523-1_13
Huang SL, Karczmarski L, Chen J, Zhou R, Lin W, Zhang H, Li H, Wu Y (2012) Demography and population trends of the largest population of Indo-Pacific humpback dolphins. Biol Conserv 147:234–242. https://doi.org/10.1016/j.biocon.2012.01.004
Huang SL, Chang WL, Karczmarski L (2014) Population trends and vulnerability of humpback dolphins Sousa chinensis off the west coast of Taiwan. Endanger Species Res 26:147–159. https://doi.org/10.3354/esr00619
Jefferson TA (2000) Population biology of the Indo-Pacific hump-backed dolphin in Hong Kong waters. Wildl Monogr 144:1–65. https://doi.org/10.2307/3830809
Jefferson TA, Leatherwood S (1997) Distribution and abundance of Indo-Pacific hump-backed dolphins (Sousa chinensis Osbeck, 1765) in Hong Kong waters. Asian marine biology. Hong Kong University Press, Hong Kong, pp 93–110
Jefferson TA, Rosenbaum HC (2014) Taxonomic revision of the humpback dolphins (Sousa spp.), and description of a new species from Australia. Mar Mammal Sci 30:1494–1541. https://doi.org/10.1111/mms.12152
Jefferson TA, Hung SK, Robertson KM, Archer FI (2012) Life history of the Indo-Pacific humpback dolphin in the Pearl River Estuary, southern China. Mar Mammal Sci 28:84–104. https://doi.org/10.1111/j.1748-7692.2010.00462.x
Jennings S, Reynolds JD, Mills SC (1998) Life history correlates of responses to fisheries exploitation. Proc R Soc Lond B 265:333–339. https://doi.org/10.1098/rspb.1998.0300
Karczmarski L (1999) Group dynamics of humpback dolphins (Sousa chinensis) in the Algoa Bay region, South Africa. J Zool 249:283–293. https://doi.org/10.1111/j.1469-7998.1999.tb00765.x
Karczmarski L, Huang SL, Or CKM et al (2015) Humpback dolphins in Hong Kong and the Pearl River Delta: status, threats and conservation challenges. Adv Mar Biol 73:27–64. https://doi.org/10.1016/bs.amb.2015.09.003
Karczmarski L, Huang SL, Chan SCY (2017) Threshold of long-term survival of a coastal delphinid in anthropogenically degraded environment: Indo-Pacific humpback dolphins in Pearl River Delta. Sci Rep 7:42900. https://doi.org/10.1038/srep42900
Kasuya T (1985) Effect of exploitation on reproductive parameters of the spotted and striped dolphins off the Pacific coast of Japan. Sci Rep Whales Res Inst 36:107–138
Li M, Wang X, Xu Y, Chen T (2017) Preliminary investigation on characteristics of Indo-Pacific humpback dolphins (Sousa chinensis) in waters between Shangchuan Island and Hailing Island. South China Fish Sci 13:1–7. https://doi.org/10.3969/j.issn.2095-0780.2017.05.001
Lin W, Karczmarski L, Li J, Chan SCY, Guo L, Wu Y (2019) Differential population dynamics of a coastal porpoise correspond to the fishing effort in a large estuarine system. Aquat Conserv Mar Freshw Ecosyst 29:223–234. https://doi.org/10.1002/aqc.2998
Lin W, Karczmarski L, Guo L, Zhou R, Mo Y, Yiu SKF, Ning X, Wai T-C, Wu Y (2020) Did a decline in prey lead to diet shift in the largest population of Indo-Pacific humpback dolphins? (Under review)
Lindstrom MJ, Bates DM (1990) Nonlinear mixed-effects models for repeated measures data. Biometrics 46:673–687. https://doi.org/10.2307/2532087
Liu X, Zhong K, Sun C, Li X (2016) The correlation between land use and water quality in the typical urbanized region of China: a case study in the river net area of Pearl River. In: International workshop on earth observation & remote sensing applications. IEEE. https://doi.org/10.1109/EORSA.2016.7552840
Miller PS (2016) A population viability analysis for the Chinese white dolphin (Sousa chinensis) in the Pearl River Estuary: final report. IUCN/SSC Conservation Breeding Specialist Group, Apple Valley
Myrick TE, Berven BA, Haywood FF (1983) Determination of concentrations of selected radionuclides in surface soil in the U.S. Health Phys 45:631–642. https://doi.org/10.1097/00004032-198309000-00006
Natale CA, Duperret EK, Zhang J (2016) Sex steroids regulate skin pigmentation through nonclassical membrane-bound receptors. Elife. https://doi.org/10.7554/eLife.15104.001
Ohsumi S (1965) Reproduction of the sperm whale in the North-West Pacific. Sci Rep Whales Res Inst 19:1–35
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara RB, Simpson G, Solymos P, Henry M, Stevens H (2012). The community ecology package: package “vegan”. https://cran.r-project.org. Accessed 4 Nov 2019
Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485. https://doi.org/10.1038/nature09210
Perrin WF, Myrick AC (1980) Age determination of toothed whales and sirenians. In: Proceedings of the international conference on determining age of Odeontocete Cetaceans (and Sirenians) La Jolla, California. Sept 5–19, 1978
Perrin WF, Coe JM, Zweifeli JR (1976) Growth and reproduction of spotted porpoise, Stenella attenuata, in the offshore Eastern Tropical Pacific. Fish Bull 74:229–269
Ramos RMA, Di Beneditto APM, Lima NRW (2000) Relationship between dental morphology, sex, body length and age in Pontoporia blainvillei and Sotalia fluviatilis (Cetacea) in Northern Rio De Janeiro, Brazil. Rev Bras Biol 60:283–290. https://doi.org/10.1590/S0034-71082000000200012
Roulin A, Saino N, Romano M, Rubolini D, Teplitsky C, Ambrosini R, Caprioli M, Canova L, Wakamatsu K (2013) Sexual dimorphism in melanin pigmentation, feather coloration and its heritability in the barn swallow (Hirundo rustica). PLoS ONE 8:e58024. https://doi.org/10.1371/journal.pone.0058024
Sarkar R, Bansal S (2017) Skin pigmentation in relation to gender: truth and myth. Pigment Int 4:1
Walton MJ, Silva MA, Magalhães SM, Prieto R, Santos RS (2007) Using blubber biopsies to provide ecological information about bottlenose dolphins (Tursiops truncatus) around the Azores. J Mar Biol Assoc UK 87:223–230. https://doi.org/10.1017/s0025315407054537
Wang JY, Hung SK, Yang SC, Jefferson TA, Secchi ER (2008) Population differences in the pigmentation of Indo-Pacific humpback dolphins, Sousa chinensis, in Chinese waters. Mammalia 72:302–308. https://doi.org/10.1515/mamm.2008.030
Wang XY, Miao X, Wu FX, Yan CX, Liu WH, Zhu Q (2012) Investigation on the distribution of Sousa chinensis in the coastal waters between Xiamen and the Pearl River Estuary. J Oceanogr Taiwan Strait 31:225–230. https://doi.org/10.3969/J.ISSN.1000-8160.2012.02.011
World Bank (2015) East Asia's changing urban landscape measuring a decade of spatial growth. World Bank, Washington, DC. https://www.worldbank.org/content/dam/Worldbank/Publications/Urban%20Development/EAP_Urban_Expansion_full_report_web.pdf
Ye H, Chen C, Sun Z, Tang S, Song X, Yang C, Tian L, Liu F (2014) Estimation of the primary productivity in Pearl River Estuary using MODIS data. Estuaries Coasts 38:506–518. https://doi.org/10.1007/s12237-014-9830-5
Yin K, Lin Z, Ke Z (2004) Temporal and spatial distribution of dissolved oxygen in the Pearl River Estuary and adjacent coastal waters. Cont Shelf Res 24:1935–1948. https://doi.org/10.1016/j.csr.2004.06.017
You Z, Wang L, Feng Z, Yang Y (2013) Spatio-temporal pattern and variation characteristics of population distribution at the county level in the Pearl River Delta. Trop Geogr 33:156–163. https://doi.org/10.13284/j.cnki.rddl.002319
Yuan R, Zhu J (2015) The effects of dredging on tidal range and saltwater intrusion in the Pearl River Estuary. J Coast Res 316:1357–1362. https://doi.org/10.2112/jcoastres-d-14-00224.1
Zhang Y, Li X, Ma Y, Bao Y (2014) Analyzing shoreline change of Pear River Estuary base on remote sensing. Hydrogr Surv Charting 34:52–55. https://doi.org/10.3969/j.issn.1671-3044.2014.03.014
Zhang X, Yu RQ, Lin W, Gui D, Sun X, Yu X, Guo L, Cheng Y, Ren H, Wu Y (2019) Stable isotope analyses reveal anthropogenically driven spatial and trophic changes to Indo-Pacific humpback dolphins in the Pearl River Estuary, China. Sci Total Environ 651:1029–1037. https://doi.org/10.1016/j.scitotenv.2018.09.256
Zhou X, Cai L (2010) Coastal and marine environmental issues in the Pearl River Delta region, China. Int J Environ Stud 67:137–145. https://doi.org/10.1080/00207231003683549
Acknowledgements
This study was supported by the Natural Science Foundation of China (no. 41576128), the Provincial Natural Science Foundation of Guangdong (2017A030308005) in China, the Ocean Park Conservation Foundation of Hong Kong (AW04.1617, MM01.1718), the Biodiversity Investigation, Observation and Assessment Program (2019-2023) of Ministry of Ecology and Environment of China (no. 9-38-27-1), and the Natural Science Foundation of Guangdong Province (2018A030313870). Photographic data of free-ranging dolphins was collected in collaboration with University of Hong Kong and Cetacea Research Institute-Hong Kong, and partially supported with Research Grants Council (RGC) of Hong Kong grant HKU17100015 and Marine Ecology Enhancement Fund (MEEF) grant MEEF2017015 and MEEF2017015A awarded to Dr Leszek Karczmarski. We thank Dr L. Karczmarski and Dr. Stephen C.Y. Chan of Cetacea Research Institute for their various help throughout this research project. We thank the teams of Chinese White Dolphin National Nature Reserve of Guangdong Pearl River Estuary and Chinese White Dolphin Nature Reserve of Guangdong Jiangmen for sample collection.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Editor: U. Siebert.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by undisclosed experts.
Rights and permissions
About this article
Cite this article
Guo, L., Lin, W., Zeng, C. et al. Investigating the age composition of Indo-Pacific humpback dolphins in the Pearl River Estuary based on their pigmentation pattern. Mar Biol 167, 50 (2020). https://doi.org/10.1007/s00227-020-3650-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-020-3650-x