Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-16T21:46:05.473Z Has data issue: false hasContentIssue false
  • English
  • Français

Behavioural reactions of wintering humpback whales (Megaptera novaeangliae) to biopsy sampling in the western South Atlantic

Published online by Cambridge University Press:  12 February 2010

Mauricio Cantor ,
Taiana Cachuba ,
Luena Fernandes  and
Márcia H. Engel
Mauricio Cantor*
Affiliation:
Instituto Baleia Jubarte, Rua Barão do Rio Branco, 26, CEP 45900-000, Caravelas, BA, Brazil
Taiana Cachuba
Affiliation:
Instituto Baleia Jubarte, Rua Barão do Rio Branco, 26, CEP 45900-000, Caravelas, BA, Brazil
Luena Fernandes
Affiliation:
Instituto Baleia Jubarte, Rua Barão do Rio Branco, 26, CEP 45900-000, Caravelas, BA, Brazil
Márcia H. Engel
Affiliation:
Instituto Baleia Jubarte, Rua Barão do Rio Branco, 26, CEP 45900-000, Caravelas, BA, Brazil
*
Correspondence should be addressed to: M. Cantor, Instituto Baleia Jubarte, Rua Barão do Rio Branco, 26, CEP 45900-000, Caravelas, BA, Brazil email: m.cantor@ymail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Molecular analysis has become a powerful tool in cetacean ecology since it supports efficient conservation policies. Remote biopsy sampling is the most efficient method to obtain epithelial material for analysis purposes; however, as an intrusive technique it presents inherent costs, evidenced by behavioural reactions. Clarifying which factors influence these responses is essential to assess its impact and prevent possible long-term effects. For eleven winters, samples from humpback whales were collected in the Abrolhos Bank, the main breeding ground of this species in the western South Atlantic. We analysed the influence of several characteristics of the shot, vessels, groups and behaviour on the frequency and intensity of the whales' response. The majority of biopsied whales did not show any detectable response. Among those that responded, a low-level category of reaction was most frequent. The use of larger boats resulted in less intense responses. Responses were influenced by group size and behavioural state: large groups, which were involved in aggressive mating behaviour, reacted less frequently than smaller groups. Females with calves showed less intense reactions than non-lactating females. The behaviour of the animals prior to and during the boat approach also affected their response: resting whales responded more intensely than whales involved in social or travel activities. Comparison with previous studies confirmed that reactions vary in intensity according to location: whales biopsied in feeding grounds responded with more intensity than those in breeding grounds, which in turn responded more intensely than whales in migration. This study reinforces existing evidence that biopsy sampling is unlikely to have long-term effects and can thus continue to be used as one of the main tools to access information which is vital for conservation.

Keywords

biopsybehavioural responsesshort-term effecthumpback whaleMegaptera novaeangliaebreeding ground
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 90 , Special Issue 8: Marine Mammals , December 2010 , pp. 1701 - 1711
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Altmann, J. (1974) Observational study of behavior: sampling methods. Behaviour 49, 227–265.CrossRefGoogle ScholarPubMed
Andriolo, A., Martins, C.C.A., Engel, M.H., Pizzorno, J.L., Mas-Rosa, S., Freitas, A., Morete, M.E. and Kinas, P.G. (2006) The first aerial survey to estimate abundance of humpback whale (Megaptera novaeangliae) in the breeding ground off Brazil. Journal of Cetacean Research and Management 8, 307–311.Google Scholar
Amos, B. and Hoelzel, A.R. (1990) DNA fingerprinting cetacean biopsy samples for individual identification. Report of the International Whaling Commission Special Issue 12, 79–85.Google Scholar
Au, W.W.L. and Green, M. (2000) Acoustic interactions between humpback whales and whale-watching boats. Marine Environmental Research 49, 469–481.CrossRefGoogle ScholarPubMed
Baker, C.S., Palumbi, S.R., Lambertsen, R.H., Weinrich, M.T., Calambokidis, J. and O'Brien, S.J. (1990) Influence of seasonal migration on geographic distribution of mitochondrial DNA haplotypes in humpback whales (Megaptera novaeangliae). Nature (London) 344, 238–240.CrossRefGoogle Scholar
Baker, C.S., Perry, A., Bannister, J.L., Weinrich, M.T., Abernethy, R.B., Calambokidis, J., Lien, J., Lambertsen, R.H., Ramirez, J.U., Vasquez, O., Clapham, P.J., Alling, A., O'brien, S.J. and Palumbi, S.R. (1993) Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proceedings of the National Academy of Sciences of the United States of America 90, 8239–8243.Google Scholar
Baker, C.S., Slade, R.W., Bannister, J.L., Abernethy, R.B., Weinrich, M.T., Lien, J., Urban-, R.J., Corkeron, P., Calambokidis, J., Vasquez, O. and Palumbi, S.R. (1994) Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, world-wide. Molecular Ecology 3, 313–327.CrossRefGoogle ScholarPubMed
Baraff, L. and Weinrich, M.T. (1993) Separation of humpback whale mothers and calves on a feeding ground in early autumn (Megaptera novaeangliae). Marine Mammal Science 9, 431–434.CrossRefGoogle Scholar
Barrett-Lennard, L.G., Smith, T.G. and Ellis, G.M. (1996) A cetacean biopsy system using lightweight pneumatic darts and its effect on the behavior of killer whales. Marine Mammal Science 12, 14–27.CrossRefGoogle Scholar
Bearzi, G. (2000) First report of a common dolphin (Delphinus delphis) death following penetration of a biopsy dart. Journal of Cetacean Research and Management 2, 217–221.Google Scholar
Bejder, L., Saumel, A., Whitehead, H., Gales, N., Mann, J., Connor, R., Heithaus, M., Watson-Capps, J., Flaherty, C. and Krützen, M. (2006) Decline in relative abundance of bottlenose dolphins exposed to long-term disturbance. Conservation Biology 20, 1791–1798.CrossRefGoogle ScholarPubMed
Bérubé, M. and Palsbøll, P. (1996) Identification of sex in cetaceans by multiplexing using ZFX and ZFY specific primers. Molecular Ecology 5, 283–287.CrossRefGoogle ScholarPubMed
Best, P.B., Reeb, D., Rew, M.B., Palsbøll, P.J., Schaeff, C. and Brandão, A. (2005) Biopsying southern right whales: their reactions and effects on reproduction. Journal of Wildlife Management 69, 1171–1180.CrossRefGoogle Scholar
Bilgmann, K., Griffiths, O.J., Allen, S.J. and Möller, L.M. (2007) A biopsy pole system for bow-riding dolphins: sampling success, behavioral responses and test for sampling bias. Marine Mammal Science 23, 218–225.CrossRefGoogle Scholar
Borobia, M., Gearing, P.J., Simard, Y., Gearing, J.N. and Beland, P. (1995) Blubber fatty acids of finback and humpback whales from the Gulf of St. Lawrence. (Balaenoptera physalus, Megaptera novaeangliae). Marine Biology (Berlin) 122, 341–353.Google Scholar
Brown, M.W., Kraus, S.D. and Gaskin, D.E. (1991) Reaction of North Atlantic right whales (Eubalaena glacialis) to skin biopsy sampling for genetic and pollutant analysis. Report of the International Whaling Commission (Genetic Ecology of Whales and Dolphins) Special Issue 13, 81–89.Google Scholar
Brown, M.R. and Corkeron, P.J. (1995) Pod characteristics of migrating humpback whales (Megaptera novaeangliae) off the east Australian coast. Behavior 132, 163–179.Google Scholar
Brown, M.R., Corkeron, P.J., Hale, P.T., Schultz, K.W. and Bryden, M.M. (1994) Behavioral responses of east Australian humpback whales (Megaptera novaeangliae) to biopsy sampling. Marine Mammal Science 10, 391–400.Google Scholar
Cerchio, S. (2003) Paternity, polygyny and alternative mating tactics in humpback whales (Megaptera novaeangliae). PhD thesis. University of Michigan, Ann Arbor, USA.Google Scholar
Cerchio, S., Jacobsen, J.K., Cholewiak, D.M., Falcone, E.A. and Merriwether, D.A. (2005) Paternity in humpback whales, Megaptera novaeangliae: assessing polygyny and skew in male reproductive success. Animal Behavior 70, 267–277.Google Scholar
Chittleborough, R.G. (1965) Dynamics of two populations of the humpback whale, Megaptera novaeangliae (Borowski). Australian Journal of Marine and Freshwater Research 16, 33–128.CrossRefGoogle Scholar
Clapham, P.J. (2000) The humpback whale: seasonal feeding and breeding in baleen whale. In Mann, J., Connor, R.C., Tyack, P.L. and Whitehead, H. (organizers) Cetacean societies—field studies of dolphins and whales. Chicago: The University of Chicago Press, pp. 173–196.Google Scholar
Clapham, P.J. and Mattila, D.K. (1993) Reactions of humpback whales to skin biopsy sampling on a West Indies breeding ground (Megaptera novaeangliae). Marine Mammal Science 9, 382–391.Google Scholar
Clapham, P.J. and Palsbøll, P.J. (1997) Molecular analysis of paternity shows promiscuous mating in female humpback whales (Megaptera novaeangliae, Borowski). Proceedings of the Royal Society of London, Series B Biological Sciences 264, 95–98.CrossRefGoogle ScholarPubMed
Clapham, P.J., Palsbøll, P.J., Mattila, D.K. and Vasquez, O. (1992) Composition and dynamics of humpback whale competitive groups in the West Indies (Megaptera novaeangliae). Behavior 122, 182–194.CrossRefGoogle Scholar
Clapham, P.J., Palsbøll, P.J. and Mattila, D.K. (1993) High energy behaviors in humpback whales as a source of sloughed skin for molecular analysis. Marine Mammal Science 9, 214–220.Google Scholar
Cunha, H.A. and Sole-Cava, A.M. (2007) Molecular sexing of tucuxi dolphins (Sotalia guianensis and Sotalia fluviatilis) using samples from biopsy darting and decomposed carcasses. Genetics and Molecular Biology 30, 1186–1188.CrossRefGoogle Scholar
Cypriano-Souza, A.L. (2008) Caracterização genética da população de baleias jubarte, Megaptera novaeangliae, da Área de Reprodução do Oceano Atlântico Sul Ocidental baseada em microssatélites nucleares. MSc thesis. Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil.Google Scholar
Engel, M. (1996) Comportamento reprodutivo da baleia jubarte (Megaptera novaeangliae) em Abrolhos. Etologia 14, 275–284.Google Scholar
Engel, M.H., Fagundes, N.J.R., Rosenbaum, H.C., Leslie, M.S., Ott, P.H., Schmitt, R., Secchi, E., Dalla Rosa, L. and Bonattelo, S.L. (2008) Mitochondrial DNA diversity of the Southwestern Atlantic humpback whale (Megaptera novaeangliae) breeding area off Brazil, and the potential connections to Antarctic feeding areas. Conservation Genetics 9, 1253–1262.CrossRefGoogle Scholar
Fossi, M.C., Marsili, L., Neri, G., Casini, S., Bearzi, G., Politi, E., Zanardelli, M. and Panigada, S. (2000) Skin biopsy of Mediterranean cetaceans for the investigation of interspecies susceptibility to xenobiotic contaminants. Marine Environmental Research 50, 517–521.Google Scholar
Freitas, A.C., Kinas, P.G., Martins, C.C.A. and Engel, M.H. (2004) Abundance of humpback whales on the Abrolhos Bank wintering ground, Brazil. Journal of Cetacean Research and Management 3, 225–230.Google Scholar
Gauthier, J. and Sears, R. (1999) Behavioral response of four species of balaenopterid whales to biopsy sampling. Marine Mammal Science 15, 85–101.CrossRefGoogle Scholar
Gendron, D., Aguiniga, S. and Carriquiry, J.D. (2001) 8∧15n And 8∧13c in skin biopsy samples: a note on their applicability for examining the relative trophic level in three rorqual species. Journal of Cetacean Research and Management 3, 41–44.Google Scholar
Gill, J.A., Norris, K. and Sutherland, W.J. (2001) Why behavioral responses may not reflect the population consequences of human disturbance. Biological Conservation 97, 265–268.CrossRefGoogle Scholar
Gorgone, A., Haase, P.A., Griffith, E.S. and Hohn, A.A. (2008) Modeling response of target and nontarget dolphins to biopsy darting. Journal of Wildlife Management 72, 926–932.CrossRefGoogle Scholar
Green, M.L., Herzing, D.L. and Baldwin, J.D. (2007) Noninvasive methodology for the sampling and extraction of DNA from free-ranging Atlantic spotted dolphins (Stenella frontalis). Molecular Ecology Notes 7, 1287–1292.Google Scholar
Hain, J.H.W., Karter, G.R., Kraus, S.D., Mayo, C.A. and Winn, H.E. (1982) Feeding behavior of humpback whale (Megaptera novaeangliae) in the western North Atlantic. Fishery Bulletin 80, 259–268.Google Scholar
Harlin, A.D., Würsig, B., Baker, C.S. and Markowitz, T.M. (1999) Skin swabbing for genetic analysis: application to dusky dolphins (Lagenorhynchus obscurus). Marine Mammal Science 15, 409–425.CrossRefGoogle Scholar
Herman, E.Y.K., Herman, L.M., Pack, A.A., Marshall, G., Shepard, C.M. and Bakhtiari, M. (2008) When whales collide: Crittercam offers insight into the competitive behavior of humpback whales on their Hawaiian wintering grounds. Marine Technology Society Journal 41, 35–43.Google Scholar
Hoelzel, A.R. (1991) Report of the workshop on the genetic analysis of cetacean populations. Report of the International Whaling Commission (Genetic Ecology of Whales and Dolphins) Special Issue 13, 3–22.Google Scholar
Hoelzel, A.R. and Amos, W. (1988) DNA fingerprinting and ‘scientific’ whaling. Nature (London) 333, 305.CrossRefGoogle ScholarPubMed
Hooker, S.K., Baird, R.W., Al-Omari, S.A., Gowans, S. and Whitehead, H. (2001) Behavioral reactions of northern bottlenose whales (Hyperoodon Ampullatus) to biopsy darting and tag attachment procedures. Fishery Bulletin 99, 303–308.Google Scholar
International Whaling Commission (IWC) (1991) Report of the ad-hoc working group on the effect of biopsy sampling on individual cetaceans. Report of International Whaling Commission Special Issue 13, 23–27.Google Scholar
Jackson, J.A., Patenaude, N.J., Carroll, E.L. and Baker, C.S. (2008) How few whales were there after whaling? Inference from contemporary mtDNA diversity. Molecular Ecology 17, 236–251.Google Scholar
Jahoda, M., Airoldi, S., Azzellino, A., Biassoni, N., Borsani, J.F., Cianfanelli, L., Lauriano, G., Sciara, G.N.D., Panigada, S., Vallini, C. and Zanardelli, M. (1996) Behavioral reactions to biopsy-darting on Mediterranean fin whales. European Research on Cetaceans 10, 43–47.Google Scholar
Jahoda, M., Lafortuna, C.L., Biassoni, N., Almirante, C., Azzellino, A., Panigada, S., Zanardell, I.M. and di Sciara, G.N. (2003) Mediterranean fin whale's (Balaenoptera physalus) response to small vessels and biopsy sampling assessed through passive tracking and timing of respiration. Marine Mammal Science 19, 96–110.Google Scholar
Jefferson, T.A. and Hung, S.K. (2008) Effects of biopsy sampling on Indo-Pacific humpback dolphins (Souza chinensis) in a polluted coastal environment. Aquatic Mammals 34, 310–316.Google Scholar
Krützen, M., Barré, L.M., Möller, L.M., Heithaus, M.R., Simms, C. and Sherwin, W.B. (2002) A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Marine Mammal Science 18, 863–878.CrossRefGoogle Scholar
Lambertsen, R.H. (1987) A biopsy system for large whales and its use for cytogenetics. Journal of Mammalogy 68, 443–445.Google Scholar
Landis, J.R. and Koch, G.G. (1977) The measurement of observer agreement for categorical data. Biometrics 33, 159–174.CrossRefGoogle ScholarPubMed
Mansour, A.A.H., Mckay, D.W., Lien, J., Orr, J.C., Banoub, J.H., Oien, N. and Stenson, G. (2002) Determination of pregnancy status from blubber samples in minke whales (Balaenoptera acutorostrata). Marine Mammal Science 18, 112–120.Google Scholar
Martins, C.C.A., Morete, M.E., Engel, M.H., Freitas, A., Secchi, E.R. and Kinas, P.G. (2001) Aspects of habitat use patterns of humpback whales in the Abrolhos Bank, Brazil, breeding ground. Memoirs of the Queensland Museum 47, 563–570.Google Scholar
Medrano, L., Salinas, M., Salas, I., Ladron De Guevara, P., Aguayo, A., Jacobsen, J. and Baker, C.S. (1994) Sex identification of humpback whales, Megaptera novaeangliae, on the wintering grounds of the Mexican Pacific Ocean. Canadian Journal of Zoology 72, 1771–1774.Google Scholar
Mesnick, S.L., Clapham, P. and Dizon, A.E. (1999) A note on the collection of associated behavioral data with biopsy samples during cetacean assessment cruises. Journal of Cetacean Research and Management 1, 205–211.Google Scholar
Metcalfe, C., Koenig, B., Metcalfe, T., Paterson, G. and Sears, R. (2004) Intra- and inter-species differences in persistent organic contaminants in the blubber of blue whales and humpback whales from the Gulf of St Lawrence, Canada. Marine Environmental Research 57, 245–260.CrossRefGoogle Scholar
Morete, M.E., Freitas, A., Engel, M.H., Pace, R.M. III and Clapham, P.J. (2003) A novel behavior observed in humpback whales on wintering grounds at Abrolhos Bank (Brazil). Marine Mammal Science 19, 694–707.CrossRefGoogle Scholar
Morete, M.E., Bisi, T.L. and Rosso, S. (2007) Mother and calf humpback whale responses to vessels around the Abrolhos Archipelago, Bahia, Brazil. Journal of Cetacean Research and Management 9, 241–248.Google Scholar
Morete, M.E., Bisi, T.L., Pace, R.M. III and Rosso, S. (2008) Fluctuating abundance of humpback whales (Megaptera novaeangliae) in a calving ground off coastal Brazil. Journal of the Marine Biological Association of the United Kingdom 88, 1229–1235.Google Scholar
Pack, A.A., Salden, D.R., Ferrari, M.J., Glockner-Ferrari, D.A., Herman, L.M., Stubbs, H.A. and Straley, J.M. (1998) Male humpback whale dies in competitive group (Megaptera novaeangliae). Marine Mammal Science 14, 861–873.Google Scholar
Palsbøll, P.J., Vader, A., Bakke, I. and El-Gewely, M.R. (1992) Determination of gender in cetaceans by polymerase chain reaction. Canadian Journal of Zoology 70, 2166–2170.CrossRefGoogle Scholar
Palsbøll, P.J., Allen, J., Bérubé, M., Clapham, P.J., Feddeersen, T.P., Hammond, P.S., Hudson, R.R., Jogensen, H., Katona, S., Larsen, A.H., Larsen, F., Lien, J., Mattila, D.K., Sigurjonsson, J., Sears, R., Smith, T., Sponer, R., Stevick, P. and Oien, A.N. (1997) Genetic tagging of humpback whales (Megaptera novaeangliae). Nature (London) 388, 767–769.Google Scholar
Parsons, K.M., Durban, J.W. and Claridge, D.E. (2003) Comparing two alternative methods for genetic sampling of small cetaceans. Marine Mammal Science 19, 224–231.CrossRefGoogle Scholar
Pizzorno, J.L.A., Brito, L.J., Dorneles, P.R., Azevedo, A.F. and Do, N.Gurgel, I.M.G. (1998) Review of strandings and additional information on humpback whales, Megaptera novaeangliae, in Rio de Janeiro, southeastern Brazilian coast (1981–1997). Report of International Whaling Commission 48, 443–446.Google Scholar
Richardson, W.J., Fraker, M.A., Würsig, B. and Wells, R.S. (1985) Behavior of bowhead whales Balaena mysticetus summering in the Beaufort Sea: reactions to industrial activities. Biological Conservation 32, 195–230.Google Scholar
Rosenbaum, H.C., Best, P.B., Findlay, K.P., Engel, M.H., Pomilla, C., Razafindrakoto, Y., Morete, M.E., Vely, M., Freitas, A.C., Baker, C.S., Jenner, C., Jenner, M-N and Bannister, J. (2000) Mitochondrial DNA variation among humpback whales from the wintering grounds in the South Atlantic and Southwestern Indian Oceans. Report of Scientific Committee of International Whaling Commission, SC/52/IA11 (unpublished).Google Scholar
Ross, D. (1976) Mechanics of underwater noise. New York: Pergamon Press.Google Scholar
Simões, D.G., Macedo, R.H.F. and Engel, M.H. (2005) Turismo de observação de cetáceos como ferramenta no estudo do comportamento de baleias jubarte (Megaptera novaeangliae). Revista de Etologia 1, 3–14.Google Scholar
Sousa-Lima, R.S. and Clark, C.W. (2008) Modeling the effect of boat traffic on the fluctuation of humpback whale singing activity in the Abrolhos National Marine Park, Brazil. Canadian Acoustics 36, 174–181.Google Scholar
Tyack, P. and Whitehead, H. (1983) Male competition in large groups of wintering humpback whales. Behavior 83, 132–154.Google Scholar
Watkins, W.A. (1981) Reactions of three species of whales Balaenoptera physalus, Megaptera novaeangliae, and Balaenoptera edeni, to implanted radio tags. Deep-Sea Research 28A, 589–599.Google Scholar
Watkins, W.A. (1986) Whale reactions to human activities in Cape Cod waters. Marine Mammal Science 2, 251–262.Google Scholar
Weinrich, M.T. and Kuhlberg, A.E. (1991) Short-term association patterns of humpback whale (Megaptera novaeangliae) groups on their feeding grounds in the southern Gulf of Maine. Canadian Journal of Zoology 69, 3005–3011.Google Scholar
Weinrich, M.T., Lambertsen, R.H., Baker, C.S., Schilling, M.R. and Belt, C.R. (1991) Behavioral responses of humpback whales (Megaptera novaeangliae) in the Southern Gulf of Maine to biopsy sampling. Report of the International Whaling Commission (Genetic Ecology of Whales and Dolphins) Special Issue 13, 91–97.Google Scholar
Weinrich, M.T., Lambertsen, R.H., Belt, C.R., Schilling, M.R., Iken, H.J. and Syrjala, S.E. (1992) Behavioral reactions of humpback whales, Megaptera novaeangliae, to biopsy procedures. Fishery Bulletin 90, 588–598.Google Scholar
Weller, D.W., Cockcroft, V.G., Würsig, B., Lynn, S.K. and Fertl, D. (1997) Behavioral responses of bottlenose dolphins to remote biopsy sampling and observations to surgical biopsy wound healing. Aquatic Mammals 23, 49–58.Google Scholar
Whitehead, H. (1983) Structure and stability of humpback whale groups off Newfoundland. Canadian Journal of Zoology 61, 1391–1397.Google Scholar
Whitehead, H., Gordon, J., Mathews, E.A. and Richard, K.R. (1990) Obtaining skin samples from living sperm whales. Marine Mammal Science 6, 316–326.Google Scholar
Zar, J.H. (1999) Biostatistical analysis, 4th edition. Upper Saddle River, NJ: Prentice-Hall.Google Scholar
Zerbini, A.N., Andriolo, A., da Rocha, J.M., Simões-Lopes, P.C., Siciliano, S., Pizzorno, J.L.A., Waite, J.M., DeMaster, D.P. and Van Blaricom, G.R. (2004) Winter distribution and abundance of humpback whales, Megaptera novaeangliae, off Northeastern Brazil. Journal of Cetacean Research and Management 6, 101–107.Google Scholar