Evaluation of parameters of health in Australian fur seal (Arctocephalus pusillus doriferus) pups during early and mid-lactation

Jessalyn J. Taylor; Rebecca R. McIntosh; Isabelle Charrier; Rachael B. Gray

doi:10.1071/ZO24041

RESEARCH ARTICLE (Open Access)

Next Contents Vol 73(4)

Evaluation of parameters of health in Australian fur seal (Arctocephalus pusillus doriferus) pups during early and mid-lactation

Jessalyn J. Taylor

^A ^* , Rebecca R. McIntosh

^B , Isabelle Charrier ^C and Rachael B. Gray ^A

+ Author Affiliations

- Author Affiliations

^A Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Camperdown, NSW 2050, Australia.

^B Conservation Department, Phillip Island Nature Parks, Cowes, Vic 3922, Australia.

^C Université Paris-Saclay, Institut des Neurosciences Paris-Saclay, CNRS, Saclay 91400, France.

^* Correspondence to: jessalyn.taylor@sydney.edu.au

Handling Editor: Brad Law

Australian Journal of Zoology 73, ZO24041 https://doi.org/10.1071/ZO24041

Submitted: 12 December 2024 Accepted: 13 June 2025 Published: 7 July 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Seal Rocks, Victoria, is the largest Australian fur seal (Arctocephalus pusillus doriferus) breeding colony, but has one of the highest rates of decline in live pup abundance for the species. Establishing the current health status in the population is important as a point of comparison for future monitoring. This study aimed to develop haematological reference intervals and assess body condition in pups at Seal Rocks in early and mid-lactation. Pups from the 2021 and 2022 breeding seasons were sampled at 3–6 weeks of age (early lactation, n = 180) and 5–6 months of age (mid-lactation, n = 172). Haematological and morphometric parameters differed significantly (P < 0.05) between early and mid-lactation, but body condition did not. The differences in health parameters between early and mid-lactation relate to normal growth and ontogeny but highlight the increased vulnerability of pups in early lactation. These results provide an important reference point for future evaluations of health parameters in Australian fur seal pups.

Keywords: Australian fur seal, body condition, conservation management, haematology, marine conservation, pinniped, reference intervals, wildlife monitoring.

References

Aguirre AA, Balazs GH, Spraker TR, Gross TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without Fibropapillomas. Physiological Zoology 68(5), 831-854.
| Crossref | Google Scholar |

Arnould JPY, Hindell MA (2001) Dive behaviour, foraging locations, and maternal-attendance patterns of Australian fur seals (Arctocephalus pusillus doriferus). Canadian Journal of Zoology 79(1), 35-48.
| Crossref | Google Scholar |

Arnould JPY, Hindell MA (2002) Milk consumption, body composition and pre-weaning growth rates of Australian fur seal (Arctocephalus pusillus doriferus) pups. Journal of Zoology 256(3), 351-359.
| Crossref | Google Scholar |

Atkinson S, Arnould JPY, Mashburn KL (2011) Plasma cortisol and thyroid hormone concentrations in pre-weaning Australian fur seal pups. General and Comparative Endocrinology 172(2), 277-281.
| Crossref | Google Scholar | PubMed |

Back JJ, Hoskins AJ, Kirkwood R, Arnould JPY (2018) Behavioral responses of Australian fur seals to boat approaches at a breeding colony. Nature Conservation 31, 35-52.
| Crossref | Google Scholar |

Bossart GD (2010) Marine mammals as sentinel species for oceans and human health. Veterinary Pathology 48(3), 676-690.
| Crossref | Google Scholar | PubMed |

Bradshaw CJA, Davis LS, Lalas C, Harcourt RG (2000) Geographic and temporal variation in the condition of pups of the New Zealand fur seal (Arctocephalus forsteri): evidence for density dependence and differences in the marine environment. Journal of Zoology 252(1), 41-51.
| Crossref | Google Scholar |

Bradshaw CJA, Harcourt RG, Davis LS (2003) Male-Biased sex ratios in New Zealand fur seal pups relative to environmental variation. Behavioral Ecology and Sociobiology 53(5), 297-307.
| Crossref | Google Scholar |

Brandimarti ME, Gray R, Silva FRO, Herbert CA (2021) Kangaroos at maximum capacity: health assessment of free-ranging eastern grey kangaroos on a coastal headland. Journal of Mammalogy 102(3), 837-851.
| Crossref | Google Scholar | PubMed |

Brock PM, Hall AJ, Goodman SJ, Cruz M, Acevedo-Whitehouse K (2012) Applying the tools of ecological immunology to conservation: a test case in the Galapagos sea lion. Animal Conservation 16(1), 19-31.
| Crossref | Google Scholar |

Brock PM, Hall AJ, Goodman SJ, Cruz M, Acevedo-Whitehouse K (2013) Immune activity, body condition and human-associated environmental impacts in a wild marine mammal. PLoS ONE 8(6), e67132.
| Crossref | Google Scholar | PubMed |

Cavagnolo RZ, Vedros NA (1979) Serum and colostrum immunoglobulin levels in the northern fur seal Callorhinus ursinus. Developmental & Comparative Immunology 3, 139-146.
| Crossref | Google Scholar | PubMed |

Costa DP, Trillmich F, Croxall JP (1988) Intraspecific allometry of neonatal size in the Antarctic fur seal (Arctocephalus galapagoensis). Behavioral Ecology and Sociobiology 22, 361-364.
| Crossref | Google Scholar |

Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Functional Ecology 22(5), 760-772.
| Crossref | Google Scholar |

Day MJ (2007) Immune system development in the dog and cat. Journal of Comparative Pathology 137, S10-S15.
| Crossref | Google Scholar | PubMed |

Desforges J-PW, Sonne C, Levin M, Siebert U, De Guise S, Dietz R (2016) Immunotoxic effects of environmental pollutants in marine mammals. Environment International 86, 126-139.
| Crossref | Google Scholar | PubMed |

Erdsack N, Dehnhardt G, Hanke W (2013) Coping with heat: function of the natal coat of cape fur seal (Arctocephalus pusillus pusillus) pups in maintaining core body temperature. PLoS ONE 8(8), e72081.
| Crossref | Google Scholar | PubMed |

Finnegan D (2022) ‘Package ‘referenceIntervals’, Vol. 2023.’ (CRAN) Available at https://cran.r-project.org/web/packages/referenceIntervals/index.html

Friedrichs KR, Harr KE, Freeman KP, Szladovits B, Walton RM, Barnhart KF, Blanco-Chavez J (2012) ASVCP reference interval guidelines: determination of de novo reference intervals in veterinary species and other related topics. Veterinary Clinical Pathology 41(4), 441-453.
| Crossref | Google Scholar | PubMed |

Fulham M, Power M, Gray R (2020) Diversity and distribution of Escherichia coli in three species of free-ranging Australian pinniped pups. Frontiers in Marine Science 7, 571171.
| Crossref | Google Scholar |

Fulham M, McDougall F, Power M, McIntosh RR, Gray R (2022) Carriage of antibiotic resistant bacteria in endangered and declining Australian pinniped pups. PLoS ONE 17(1), e0258978.
| Crossref | Google Scholar | PubMed |

Gardner BR, Stenos J, Hufschmid J, Arnould JPY, McIntosh RR, Tadepalli M, Tolpinrud A, Marenda M, Lynch M, Stent A (2022) An old pathogen in a new environment–implications of Coxiella burnetii in Australian fur seals (Arctocephalus pusillus doriferus). Frontiers in Marine Science 9, 809075.
| Crossref | Google Scholar |

Geeson JJ, Hindell MA, Hobday AJ, Speakman CN, Arnould JPY (2023) Long-term decline in body condition of female Australian fur seals: potential causes and implications. Frontiers in Marine Science 10, 1231337.
| Crossref | Google Scholar |

Gerlinsky CD, Haulena M, Trites AW, Rosen DAS (2018) Reference ranges and age-related and diving exercise effects on hematology and serum chemistry of female Steller sea lions (Eumetopias jubatus). Journal of Zoo and Wildlife Medicine 49(1), 18-29.
| Crossref | Google Scholar | PubMed |

Gibbens J, Parry LJ, Arnould JPY (2010) Influences on fecundity in Australian fur seals (Arctocephalus pusillus doriferus). Journal of Mammalogy 91(2), 510-518.
| Crossref | Google Scholar |

Greig DJ, Gulland FMD, Rios CA, Hall AJ (2010) Hematology and serum chemistry in stranded and wild-caught harbor seals in central California: reference intervals, predictors of survival, and parameters affecting blood variables. Journal of Wildlife Diseases 46(4), 1172-1184.
| Crossref | Google Scholar | PubMed |

Halvorsen S, Bechensteen AG (2002) Physiology of erythropoietin during mammalian development. Acta Paediatrica 91(438), 17-26.
| Crossref | Google Scholar |

Harrison XA, Donaldson L, Correa-Cano ME, Evans J, Fisher DN, Goodwin CED, Robinson BS, Hodgson DJ, Inger R (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6, e4794.
| Crossref | Google Scholar | PubMed |

Horn PS, Pesce AJ (2003) Reference intervals: an update. Clinica Chimica Acta 334(1–2), 5-23.
| Crossref | Google Scholar |

IPCC (2023) Summary for policymakers. In ‘Climate change 2023: synthesis report. Contribution of working groups I, II and III to the sixth assessment report of the Intergovernmental Panel on Climate Change’. (Eds H Lee, J Romero) pp. 1–34. (IPCC: Geneva, Switzerland)

Jacob EA (2016) Hematological differences in newborn and aging: a review study. Hematology & Transfusion International Journal 3(3), 178-190.
| Crossref | Google Scholar |

Keogh MJ, Maniscalco JM, Atkinson S (2010) Steller sea lion (Eumetopias jubatus) pups undergo a decrease in circulating white blood cells and the ability of T cells to proliferate during early postnatal development. Veterinary Immunology and Immunopathology 137(3–4), 298-304.
| Crossref | Google Scholar | PubMed |

Kliska K, McIntosh RR, Jonsen I, Hume F, Dann P, Kirkwood R, Harcourt R (2022) Environmental correlates of temporal variation in the prey species of Australian fur seals inferred from scat analysis. Royal Society of Open Science 9(10), 211723.
| Crossref | Google Scholar |

Kohyama K, Kiyota M, Inoshima Y (2021) Longitudinal study of northern fur seal (Callorhinus ursinus) hematology. Journal of Veterinary Medical Science 83(7), 1128-1137.
| Crossref | Google Scholar | PubMed |

Lander ME, Harvey JT, Gulland FMD (2003) Hematology and serum chemistry comparisons between free-ranging and rehabilitated harbor seal (Phoca vitulina richardsi) pups. Journal of Wildlife Diseases 39(3), 600-609.
| Crossref | Google Scholar | PubMed |

Le Bœuf BJ, Condit R, Reiter J (1989) Parental investment and the secondary sex ratio in northern elephant seals. Behavioral Ecology and Sociobiology 25, 109-117.
| Crossref | Google Scholar |

Lea M-A, Guinet C, Cherel Y, Duhamel G, Dubroca L, Pruvost P, Hindell M (2006) Impacts of climatic anomalies on provisioning strategies of a Southern Ocean predator. Marine Ecology Progress Series 310, 77-94.
| Crossref | Google Scholar |

Lenth RV (2024) ‘Emmeans: estimated marginal means, aka least-squares means.’ (CRAN) Available at https://cran.r-project.org/web/packages/emmeans/index.html

Lindsay SA, Fulham M, Caraguel CGB, Gray R (2023) Mitigating disease risk in an endangered pinniped: early hookworm elimination optimizes the growth and health of Australian sea lion pups. Frontiers in Veterinary Science 10, 1161185.
| Crossref | Google Scholar | PubMed |

Marcus AD, Higgins DP, Gray R (2015) Health assessment of free-ranging endangered Australian sea lion (Neophoca cinerea) pups: effect of haematophagous parasites on haematological parameters. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 184, 132-143.
| Crossref | Google Scholar |

Martin M, Gridley T, Elwen SH, Charrier I (2022) Assessment of the impact of anthropogenic airborne noise on the behaviour of Cape fur seals during the breeding season in Namibia. Journal of Experimental Marine Biology and Ecology 550, 151721.
| Crossref | Google Scholar |

Martin M, Gridley T, Elwen S, Charrier I (2023) Inter-site variability in the Cape fur seal’s behavioural response to boat noise exposure. Marine Pollution Bulletin 196, 115589.
| Crossref | Google Scholar | PubMed |

McCartney J (2022) Interpretation of hematologic data in nonclinical studies. In ‘Schalm’s veterinary hematology.’ 7th edn. (Eds MB Brooks, KE Harr, DM Seelig, KJ Wardrop, DJ Weiss) pp. 93–99. (Wiley-Blackwell: Hoboken)

McCourt MR, Rizzi TE (2022) Hematology of dogs. In ‘Schalm’s veterinary hematology’. 7th edn. (Eds MB Brooks, KE Harr, DM Seelig, KJ Wardrop, DJ Weiss) pp. 971–982. (Wiley-Blackwell: Hoboken)

McIntosh RR, Kirkwood R, Sutherland DR, Dann P (2015) Drivers and annual estimates of marine wildlife entanglement rates: a long-term case study with Australian fur seals. Marine Pollution Bulletin 101(2), 716-725.
| Crossref | Google Scholar | PubMed |

McIntosh RR, Kirkman SP, Thalmann S, Sutherland DR, Mitchell A, Arnould JPY, Salton M, Slip DJ, Dann P, Kirkwood R (2018) Understanding meta-population trends of the Australian fur seal, with insights for adaptive monitoring. PLoS ONE 13(9), e0200253.
| Crossref | Google Scholar | PubMed |

McIntosh RR, Sorrell KJ, Thalmann S, Mitchell A, Gray R, Schinagl H, Arnould JPY, Dann P, Kirkwood R (2022) Sustained reduction in numbers of Australian fur seal pups: implications for future population monitoring. PLoS ONE 17(3), e0265610.
| Crossref | Google Scholar | PubMed |

McLean LJ, George S, Ierodiaconou D, Kirkwood RJ, Arnould JPY (2018) Impact of rising sea levels on Australian fur seals. PeerJ 6, e5786.
| Crossref | Google Scholar | PubMed |

McMichael L, Edson D, McLaughlin A, Mayer D, Kopp S, Meers J, Field H (2015) Haematology and plasma biochemistry of wild black flying-foxes, (Pteropus alecto) in Queensland, Australia. PLoS ONE 10(5), e0125741.
| Crossref | Google Scholar |

Meza Cerda M-I, Gray R, Thomson PC, Butcher L, Simpson K, Cameron A, Marcus AD, Higgins DP (2022) Developing immune profiles of endangered Australian sea lion (Neophoca cinerea) pups within the context of endemic hookworm (Uncinaria sanguinis) infection. Frontiers in Veterinary Science 9, 824584.
| Crossref | Google Scholar | PubMed |

Ono KA, Boness DJ (1996) Sexual dimorphism in sea lion pups: differential maternal investment, or sex-specific differences in energy allocation? Behavioral Ecology and Sociobiology 38, 31-41.
| Google Scholar |

Pulvirenti J, Reina RD, Chiaradia A (2023) Exploring subcolony differences in foraging and reproductive success: the influence of environmental conditions on a central place foraging seabird. Royal Society Open Science 10(6), 220362.
| Crossref | Google Scholar |

Rea LD, Castellini MA, Fadely BS, Loughlin TR (1998) Health status of young Alaska Steller sea lion pups (Eumetopias jubatus) as indicated by blood chemistry and hematology. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 120(4), 617-623.
| Crossref | Google Scholar |

R Core Team (2023) ‘R: A Language and Environment for Statistical Computing’. (R Foundation for Statistical Computing: Vienna, Austria). Available at https://www.R-project.org/

Reif JS, Bachand A, Aguirre AA, Borjesson DL, Kashinsky L, Braun R, Antonelis G (2006) Morphometry, hematology, and serum chemistry in the Hawaiian monk seal (Monachus Schauinslandi). Marine Mammal Science 20(4), 851-860.
| Crossref | Google Scholar |

Reinhold S-L, Goldsworthy SD, Arnould JPY, Gillanders BM, Connell SD, McIntosh RR (2022) Tracing seal predation back to the source colony of their penguin prey: a trace element and stable isotope analysis. Frontiers in Marine Science 9, 813106.
| Crossref | Google Scholar |

Roletto J (1993) Hematology and serum chemistry values for clinically healthy and sick pinnipeds. Journal of Zoo and Wildlife Medicine 24(2), 145-157.
| Google Scholar |

Ross PS, De Swart RL, Visser IKG, Vedder LJ, Murk W, Bowen WD, Osterhaus ADME (1994) Relative immunocompetence of the newborn harbour seal, Phoca vitulina. Veterinary Immunology and Immunopathology 42(3–4), 331-348.
| Crossref | Google Scholar | PubMed |

Souza CD, Eren MV (2022) Monocytes and macrophages and their disorders. In ‘Schalm’s veterinary hematology.’ 7th edn. (Eds MB Brooks, KE Harr, DM Seelig, KJ Wardrop, DJ Weiss) pp. 386–394. (Wiley-Blackwell: Hoboken)

Speakman CN, Hoskins AJ, Hindell MA, Costa DP, Hartog JR, Hobday AJ, Arnould JPY (2020) Environmental influences on foraging effort, success and efficiency in female Australian fur seals. Scientific Reports 10(1), 17710.
| Crossref | Google Scholar | PubMed |

Spence-Bailey LM, Verrier D, Arnould JPY (2007) The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups. Journal of Comparative Physiology B 177(4), 483-494.
| Crossref | Google Scholar |

Taylor S, Terkildsen M, Stevenson G, de Araujo J, Yu C, Yates A, McIntosh RR, Gray R (2021) Per and polyfluoroalkyl substances (PFAS) at high concentrations in neonatal Australian pinnipeds. Science of the Total Environment 786, 147446.
| Crossref | Google Scholar | PubMed |

Taylor JJ, McIntosh RR, Gray RB, Charrier I (2024) Behavioural response of Australian fur seals (Arctocephalus pusillus doriferus) to vessel noise during peak and off-peak human visitation. Marine Pollution Bulletin 208, 116947.
| Crossref | Google Scholar |

Tripovich JS, Hall-Aspland S, Charrier I, Arnould JP (2012) The behavioural response of Australian fur seals to motor boat noise. PLoS ONE 7(5), e37228.
| Crossref | Google Scholar | PubMed |

Trumble SJ, Castellini MA (2002) Blood chemistry, hematology, and morphology of wild harbor seal pups in Alaska. The Journal of Wildlife Management 66(4), 1197-1207.
| Crossref | Google Scholar |

Wall D, Thalmann S, Wotherspoon S, Lea M-A (2023) Is regional variability in environmental conditions driving differences in the early body condition of endemic Australian fur seal pups? Wildlife Research 50(12), 993-1007.
| Crossref | Google Scholar |

Warneke RM, Shaughnessy PD (1985) Arctocephalus pusillus, the South African and Australian fur seal: taxonomy, evolution, biogeography, and life history. In ‘Studies of sea mammals in south latitudes’. (Eds JK Ling, MM Bryden) (South Australian Museum: Adelaide)

Young KM, Layne EA (2022) Eosinophils and their disorders. In ‘Schalm’s veterinary hematology.’ 7th edn. (Eds MB Brooks, KE Harr, DM Seelig, KJ Wardrop, DJ Weiss) pp. 363–372. (Wiley-Blackwell: Hoboken)