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Abundance of the New Zealand subantarctic southern right whale population estimated from photo-identification and genotype mark-recapture

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Abstract

The abundance of New Zealand subantarctic southern right whales (Eubalaena australis) was estimated for the first time using mark-recapture methods based on photo-identification and microsatellite genotyping (13 loci). Individual identification photographs of 383 whales and microsatellite genotypes of 235 whales were collected during annual austral winter field surveys from 1995 to 1998. Given the 4-year survey period and lack of geographic and demographic closure, we estimated super-population abundance using the POPAN Jolly-Seber model implemented in the software programme MARK. Models with constant survivorship but time-varying capture probability and probability of entry into the population were the most suitable due to the survey design. This provided estimates of abundance in 1998 of 908 non-calf whales (95% C.L. = 755, 1,123) for the photo-identification and 910 non-calf whales (95% C.L. = 641, 1,354) for the microsatellite genotype data sets. The current estimate of 900 whales may represent less than 5% of the pre-whaling abundance in New Zealand waters.

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References

  • Aasen E, Medrano J (1990) Amplification of the ZFX and ZFY genes for sex identification in humans, cattle, sheep and goats. Nat Biotechnol 8:1279–1281

    Article  CAS  Google Scholar 

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest

    Google Scholar 

  • Arnason A, Schwartz MK (1999) Using POPAN-5 to analyse banding data. Bird Study 46(Suppl):S157–S168

    Article  Google Scholar 

  • Arnason A, Schwarz C (1996) A general methodology for the analysis of capture–recapture experiments in open populations. Biometrics 52:860–873

    Article  Google Scholar 

  • Baker CS, Slade RW, Bannister JL, Abernethy R, Weinrich M, Lien J, Urban J, Corkeron P, Calambokidis J, Vasquez O, Palumbi S (1994) Hierarchical structure of mitochondrial DNA gene flow among humpback whales, Megaptera novaeangliae, world-wide. Mol Ecol 3:313–327

    Article  CAS  Google Scholar 

  • Baker CS, Medrano-Gonzalez L, Calambokidis J, Perry A, Pichler F, Rosenbaum H, Straley J, Urban-Ramirez J, Yamaguchi M, von Ziegesar O (1998) Population structure of nuclear and mitochondrial DNA variation among humpback whales in the North Pacific. Mol Ecol 7:695–707

    Article  CAS  Google Scholar 

  • Bannister JL (2008) Population trend in right whales off southern Australia 1993–2007. Unpublished report (SC/60/BRG14) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Bérubé M, Jørgensen H, McEwing R, Palsbøll P (2000) Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale Megaptera novaeangliae. Mol Ecol 9:2181–2183

    Article  Google Scholar 

  • Best P (1993) Increase rates in severely depleted stocks of baleen whales. ICES J Mar Sci 50:169–186

    Article  Google Scholar 

  • Best P (1994) Seasonality of reproduction and the length of gestation in southern right whales Eubalaena australis. J Zool (Lond) 232:175–189

    Article  Google Scholar 

  • Best P, Reeb D, Rew M, Palsbøll P, Schaeff C, Brandao A (2005) Biopsying southern right whales: their reactions and effects on reproduction. J Wildl Manage 69:1171–1180

    Article  Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetic studies. Mol Ecol 13:3261–3273

    Article  CAS  Google Scholar 

  • Botsetein D, White R, Skolnick M, Davis R (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Gen 32:314–331

    Google Scholar 

  • Brandão A, Best P, Butterworth D (2010) Estimates of demographic parameters for southern right whales off South Africa from survey data 1979 to 2006. Unpublished report (SC/62/BRG30) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Burnell SR (2008) Estimates of demographic parameters of southern right whales off Australia. Unpublished report (SC/60/BRG12) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference, 2nd edn. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Method Res 33:261–304

    Article  Google Scholar 

  • Carroll EL, Patenaude NJ, Alexander AM, Steel D, Harcourt R, Childerhouse S, Smith S, Bannister JL, Constantine R, Baker CS (2011) Population structure and individual movement of southern right whales around New Zealand and Australia. Mar Ecol Prog Ser 432:257–268

    Article  CAS  Google Scholar 

  • Cawthorn M (1978) New Zealand progress report on cetacean research June 1976 to May 1977. Rep Int Whal Comm 28:109–113

    Google Scholar 

  • Cawthorn M (1989) New Zealand progress report on cetacean research January 1987 to April 1988. Rep Int Whal Comm 39:185–187

    Google Scholar 

  • Cawthorn M (1993) New Zealand progress report on cetacean research, April 1991 to April 1992. Rep Int Whal Comm 43:286–288

    Google Scholar 

  • Childerhouse S, Double M, Gales N (2010) Satellite tracking of southern right whales (Eubalaena australis) at the Auckland Islands, New Zealand. Unpublished report (SC/62/BRG19) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Choquet R, Lebreton J-D, Gimenez O, Reboulet A-M, Pradel R (2009) U-CARE: utilities for performing goodness of fit tests and manipulationg CApture–REcapture data. Ecography 32:1071–1074

    Article  Google Scholar 

  • Constantine R, Garrigue C, Steel D, Jackson JA, Burns D, Clapham P, Hauser N, Mattila D, Oremus M, Poole M, Robbins J, Thompson K, Baker CS (2010) Abundance of humpback whales in Oceania based on fluke photo-identification and DNA profiling. Unpublished report (SC/62/SH18) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Cooch E, White BN (2010) Program MARK: a gentle introduction. Available from http://www.phidot.org/software/mark/docs/book/

  • Cooke J, Rowntree V, Payne R (2001) Estimates of demographic parameters for southern right whales (Eubalaena australis) observed off Peninsula Valdes, Argentina. J Cetacean Res Manage Special Issue 2:125–132

    Google Scholar 

  • Cooke J, Rowntree V, Payne R (2003) Analysis of inter-annual variation in reproductive success of South Atlantic right whales (Eubalaena australis) from photo-identification of calving females observed off Peninsula Valdés. Unpublished report (SC/55/O23) presented to the Scientific Committee of the International Whaling Commission, Cambridge, UK

  • Dawbin W (1986) Right whales caught in waters around south eastern Australia and New Zealand during the nineteenth and early twentieth centuries. Rep Int Whal Comm Special Issue 10:261–268

    Google Scholar 

  • Donoghue M (1995) New Zealand progress report on cetacean research, April 1993 to March 1994. Rep Int Whal Comm 45:247–250

    Google Scholar 

  • Dreher B, Winterstein S, Luckacs P, Etter D, Rosa G, Lopez V, Libants S, Fileck K (2007) Noninvasive estimation of black bear abundance incorporating genotyping errors and harvested bear. J Wildl Manage 71:2684–2693

    Article  Google Scholar 

  • Fewster R, Patenaude NJ (2009) Cubic splines for estimating the distribution of residence time using individual resighting data. Environ Ecol Stat 3:393–415

    Google Scholar 

  • Frasier TR, Rastogi T, Brown MW, Hamilton P, Kraus SD, White BN (2006) Characterization of tetranucleotide microsatellite loci and development and validation of multiplex reactions for the study of right whale species (genus Eubalaena). Mol Ecol Notes 6:1025–1029

    Article  CAS  Google Scholar 

  • Garrigue C, Dodemont R, Steel D, Baker CS (2004) Organismal and ‘gametic’ capture-recapture using microsatellite genotyping confirm low abundance and reproductive autonomy of humpback whales on the wintering ground of New Caledonia. Mar Ecol Prog Ser 274:251–262

    Article  Google Scholar 

  • Gaskin DE (1964) Return of the southern right whale (Eubalaena australis Desm.) to New Zealand waters, 1963. Tuatara 12:115–118

    Google Scholar 

  • Gilson A, Syvanen M, Levine K, Banks J (1998) Deer gender determination by polymerase chain reaction: validation study and application to tissues, bloodstains, and hair forensic samples from California. Calif Fish Game 84:159–169

    Google Scholar 

  • Groch K, Palazzo J, Flores P, Ardler F, Fabian M (2005) Recent rapid increase in the right whale (Eubalaena australis) population off southern Brazil. Lat Am J Aquat Mamm 4:41–47

    Article  Google Scholar 

  • Hammond PS (1986) Estimating the size of naturally marked whale populations using capture-recapture techniques. Rep Int Whal Comm Special Issue 8:253–282

    Google Scholar 

  • Hurvich C, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307

    Article  Google Scholar 

  • IWC (2001) Report of the workshop on the comprehensive assessment of right whales: a worldwide comparison. J Cetacean Res Manage Special Issue 2:1–60

    Google Scholar 

  • Jackson JA, Carroll EL, Smith T, Patenaude NJ, Baker CS (2009) Appendix 3: Taking stock: the historical demography of the New Zealand right whale (the Tohora) ZBD2005-05 progress report #5 to the NZ Ministry of Fisheries, June 2009, pp 188

  • Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 9:801–888

    Google Scholar 

  • Kemper C, Cochran D, Warneke R, Pirzl R, Watson M, Gales R, Gibbs S (2008) Southern right whale (Eubalaena australis) mortalities and human interactions in Australia, 1950–2006. J Cetacean Res Manage 10:1–8

    Google Scholar 

  • Kraus SD, Moore MJ, Price CA, Crone M, Watkins W, Winn H, Prescott JH (1986) The use of photographs to identify individual North Atlantic right whales (Eubalaena glacialis). Rep Int Whal Comm Special Issue 10:145–151

    Google Scholar 

  • Kraus SD, Hamilton P, Kenney R, Knowlton AR, Slay CK (2001) Reproductive parameters of the North Atlantic right whale. J Cetacean Res Manage Special Issue 2:231–236

    Google Scholar 

  • Lambersten R (1987) A biopsy system for large whales and its use for cytogenetics. J Mamm 68:443–445

    Article  Google Scholar 

  • Leaper R, Cooke J, Trathan P, Reid K, Rowntree V, Payne R (2006) Global climate drives southern right whale (Eubalaena australis) population dynamics. Biol Lett 2:289–292

    Article  Google Scholar 

  • Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  • McKelvey KS, Schwartz MK (2005) DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework. Mol Ecol Notes 5:716–718

    Article  CAS  Google Scholar 

  • Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecol Appl 10:283–294

    Article  Google Scholar 

  • Oremus M, Poole M, Steel D, Baker CS (2007) Isolation and interchange among insular spinner dolphin communities in the South Pacific revealed by individual identification and genetic diversity. Mar Ecol Prog Ser 336:275–289

    Article  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  Google Scholar 

  • Palsbøll P, Allen J, Bérubé M, Clapham P, Fedderson T, Hammond PS, Hudson R, Jørgensen H, Katona S, Larsen AH, Larsen F, Lien J, Mattila D, Sigurjonsson J, Sears R, Smith T, Sponer R, Stevick PT, Øien N (1997a) Genetic tagging of humpback whales. Nature 388:767–769

    Article  Google Scholar 

  • Palsbøll P, Bérubé M, Larsen AH, Jørgensen H (1997b) Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol 6:893–895

    Article  Google Scholar 

  • Patenaude NJ (2002) Demographic and genetic status of right whales at the Auckland Islands, New Zealand. PhD thesis, Auckland

  • Patenaude NJ (2003) Sightings of southern right whales around ‘mainland’ New Zealand. Science for Conservation New Zealand Department of Conservation, vol 225, pp 1–37

  • Patenaude NJ, Baker CS (2001) Population status and habitat use of southern right whales in the sub-Antarctic Auckland Islands of New Zealand. J Cetacean Res Manage Special Issue 2:111–116

    Google Scholar 

  • Patenaude NJ, Baker CS, Gales N (1998) Observations of southern right whales on New Zealand’s subantarctic wintering grounds. Mar Mamm Sci 14:350–355

    Article  Google Scholar 

  • Patenaude NJ, Todd B, Stewart R (2001) A note on movement of southern right whales between the sub-Antarctic Auckland and Campbell Islands, New Zealand. J Cetacean Res Manage Special Issue 2:121–123

    Google Scholar 

  • Patenaude NJ, Portway V, Schaeff C, Bannister JL, Best P, Payne R, Rowntree V, Rivarola M, Baker CS (2007) Mitochondrial DNA diversity and population structure among southern right whales (Eubalaena australis). J Hered 98:147–157

    Article  CAS  Google Scholar 

  • Payne R, Brazier O, Dorsey E, Perkins J, Rowntree V, Titus A (1983) External features in southern right whales (Eubalaena australis) and their use in identifying individuals. In: Payne R (ed) Communication and behaviour of whales. Westview Press, Boulder, pp 371–445

    Google Scholar 

  • Peakall R, Smouse P (2005) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildl Monogr 107:1–97

    Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859

    Article  CAS  Google Scholar 

  • Pradel R, Hine J, Lebreton J-D, Nichols JD (1997) Capture-recapture survival models taking account of transients. Biometrics 53:60–72

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sherrin R (1886) Handbook of the fishes of New Zealand. Wilsons & Horton, Auckland

    Google Scholar 

  • Statistics New Zealand (1841–1853) Blue book of statistics. 1841–1853. Australian Joint Copying Project Colonial Office (CO213) Pro reel 1502–1504

  • Stewart S, Todd B (2001) A note on observations of southern right whales at Campbell Island, New Zealand. J Cetacean Res Manage Special Issue 2:117–120

    Google Scholar 

  • Taberlet P, Luikart G (1999) Non-invasive genetic sampling and individual identification. Biol J Linn Soc 68:41–55

    Article  Google Scholar 

  • Taberlet P, Camarra JJ, Griffin S, Uhrés E, Hanotte O, Waits LP, Dubois-Paganon C, Burke T, Bouvet J (1997) Noninvasive genetic tracking of the endangered Pyrenean brown bear population. Mol Ecol 6:869–876

    Article  CAS  Google Scholar 

  • Tormosov D, Mikhaliev Y, Best P, Zemsky V, Sekiguchi M, Brownell R (1998) Soviet catches of Southern right whales Eubalaena australis 1951–1971: biological data and conservation implications. Biol Conserv 86:185–197

    Article  Google Scholar 

  • Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156

    Article  CAS  Google Scholar 

  • van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol 8:1762–1765

    Google Scholar 

  • Wade P, Kennedy A, LeDuc RG, Barlow J, Carretta J, Shelden K, Perryman W, Pitman R, Robertson K, Rone B, Salinas JC, Zerbini AN, Brownell R, Clapham P (2010) The world’s smallest whale population? Biol Lett. doi:10.1098/rsbl.2010.0477

    Article  Google Scholar 

  • Waits JP, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199

    Article  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    Article  CAS  Google Scholar 

  • Waldick RC, Brown MW, White BN (1999) Characterization and isolation of microsatellite loci from the endangered North Atlantic right whale. Mol Ecol 8:1763–1765

    Article  CAS  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Suppl):120–138

    Article  Google Scholar 

  • Whitehead H, Christal J, Tyack P (2000) Studying cetacean social structure in space and time: innovative techniques. In: Mann J, Connor R, Tyack P, Whitehead H (eds) Cetacean societies. University of Chicago press, Chicago, pp 65–87

    Google Scholar 

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Acknowledgments

Samples were collected under NZ Department of Conservation (DOC) Marine Mammal Research permit and University of Auckland Animal Ethics Committee approved protocol (to C. S. Baker) in the Auckland Islands. The 1995–1998 Auckland Islands field trips were funded by Whale and Dolphin Conservation Society, the U.S. Department of State (Program for Cooperative US/NZ Antarctic Research), the Auckland University Research Council and the NZ Marsden Fund. Logistic support was given by the Southland DOC Conservancy University of Auckland and the Australian Antarctic Division. We thank the Captain and crew of the ‘Evohe’ for their help and support in the field. Laboratory work was funded by the NZ Marsden Fund, DOC, the Heseltine Trust and an OMV NZ Ltd. Scholarship to EC. EC was supported by a Tertiary Education Commission Top Achiever Scholarship. Thanks to Rochelle Constantine, Jennifer Jackson and two anonymous reviewers who provided helpful comments on an earlier version of the manuscript.

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Carroll, E.L., Patenaude, N.J., Childerhouse, S.J. et al. Abundance of the New Zealand subantarctic southern right whale population estimated from photo-identification and genotype mark-recapture. Mar Biol 158, 2565–2575 (2011). https://doi.org/10.1007/s00227-011-1757-9

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