Pup mortality in New Zealand sea lions (Phocarctos hookeri) at Enderby Island, Auckland Islands, 2013-18

Autoři: Sarah A. Michael aff001;  David T. S. Hayman aff003;  Rachael Gray aff001;  Ji Zhang aff003;  Lynn Rogers aff003;  Wendi D. Roe aff002
Působiště autorů: Sydney School of Veterinary Science, The University of Sydney, Camperdown, New South Wales, Australia aff001;  School of Veterinary Science, Massey University, Palmerston North, New Zealand aff002;  Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225461


New Zealand sea lions (Phocarctos hookeri) are an endemic and endangered species. Pup mortality at Enderby Island (50.5°S, 166.28°E) in the New Zealand sub-Antarctic has been well studied, with subsequent investigations yielding more intricate detail of the causes of mortality, as new diagnostic methods become available. Klebsiella pneumoniae was first reported in 2001–02 at this site, causing a pup mortality epizootic and is now known to be present at several colonies. This bacterium is a common mucosal commensal of humans and animals, however the agent found in pups at necropsy is a hypervirulent strain, readily recognised in microbial culture as being hypermucoviscous. Infection causes septicaemia with a common syndrome of subsequent meningitis and polyarthritis. This investigation uses histopathology and microbiology, with new modalities such as matrix assisted laser desorption/ionisation—time of flight mass spectrometry to show that Klebsiella septicaemia could have historically been, and continues to be, the most important cause of pup mortality, but has been previously underrepresented due to the often cryptic presentation and sometimes peracute course of disease. Hypermucoviscous K. pneumoniae should be considered a serious threat to pup survival in the species, causing on average 60.2% of pup deaths annually at Enderby Island between 2013 and 2018, with likely more continuing mortality following pup dispersal and the cessation of the summer monitoring season. Less common causes of death included starvation (14.8%), trauma/asphyxiation (9.9%) and other infections (7%). This study forms the basis for further evaluation of risk factors for pup mortality in the species, with a view to developing active mitigation.

Klíčová slova:

Arthritis – Hookworms – Islands – Meningitis – Necrotic cell death – Sea lions


1. Chilvers BL, Robertson BC, Wilkinson IS, Duignan PJ. Growth and survival of New Zealand sea lions, Phocarctos hookeri: birth to 3 months. Polar Biol. 2007;30(4):459–69. doi: 10.1007/s00300-006-0203-9

2. Childerhouse S, Gales N. Fostering behaviour in New Zealand sea lions Phocarctos hookeri. N Z J Zool. 2001;28(2):189–95. doi: 10.1080/03014223.2001.9518263

3. Childerhouse S, Burns T, Michael S, Godoy D, McNutt L, McCormack C. Final report for CSP Project—New Zealand sea lion Auckland Island monitoring 2017–18. Wellington, New Zealand: Department of Conservation, 2018.

4. Baker A. Unusual mortality of the New Zealand sea lion, Phocarctos hookeri, Auckland Islands, January-February 1998: Report of a workshop held 8–9 June 1998, Wellington, and a contingency plan for future events: Department of Conservation; 1999.

5. Wilkinson IS, Duignan PJ, Castinel A, Grinberg A, Chilvers BL, Robertson BC, editors. Klebsiella pneumoniae epidemics: possible impact on New Zealand sea lion recruitment. Sea lions of the world- conservation and research in the 21st century: 22nd Wakefield Fisheries Symposium; 2006; Alaska, USA.

6. Castinel A, Duignan PJ, Pomroy WE, Lopez-Villalobos N, Gibbs NJ, Chilvers BL, et al. Neonatal mortality in New Zealand sea lions (Phocarctos hookeri) at Sandy Bay, Enderby Island, Auckland Islands from 1998 to 2005. J Wildl Dis. 2007;43(3):461–74. doi: 10.7589/0090-3558-43.3.461 17699084

7. Roe WD, Rogers L, Pinpimai K, Dittmer K, Marshall J, Chilvers BL. Septicaemia and meningitis caused by infection of New Zealand sea lion pups with a hypermucoviscous strain of Klebsiella pneumoniae. Vet Microbiol. 2015;176(3–4):301–8. doi: 10.1016/j.vetmic.2015.01.019 25682024

8. Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev. 2019;32(3):e00001–19. doi: 10.1128/CMR.00001-19 31092506

9. Peirano G, Pitout JD, Laupland KB, Meatherall B, Gregson DB. Population-based surveillance for hypermucoviscosity Klebsiella pneumoniae causing community-acquired bacteremia in Calgary, Alberta. Canadian Journal of Infectious Diseases and Medical Microbiology. 2013;24(3):e61–e4. doi: 10.1155/2013/828741 24421832

10. Chang L, Bastian I, Warner M. Survey of Klebsiella pneumoniae bacteraemia in two South Australian hospitals and detection of hypermucoviscous phenotype and magA/rmpA genotypes in K. pneumoniae isolates. Infection. 2013;41(2):559–63. doi: 10.1007/s15010-012-0374-y 23225226

11. Seguel M, Gottdenker NL, Colegrove K, Johnson S, Struve C, Howerth EW. Hypervirulent Klebsiella pneumoniae in California sea lions (Zalophus californianus): pathologic findings in natural infections. Vet Pathol. 2017;54(5):846–50. doi: 10.1177/0300985817705172 28494709

12. Jang S, Wheeler L, Carey RB, Jensen B, Crandall CM, Schrader KN, et al. Pleuritis and suppurative pneumonia associated with a hypermucoviscosity phenotype of Klebsiella pneumoniae in California sea lions (Zalophus californianus). Vet Microbiol. 2010;141(1–2):174–7. doi: 10.1016/j.vetmic.2009.07.032 19709820

13. Twenhafel NA, Whitehouse CA, Stevens EL, Hottel HE, Foster CD, Gamble S, et al. Multisystemic abscesses in African Green Monkeys (Chlorocebus aethiops) with invasive Klebsiella pneumoniae—identification of the hypermucoviscosity phenotype. Vet Pathol. 2008;45(2):226–31. doi: 10.1354/vp.45-2-226 18424839

14. Michael SA, Chilvers BL, Hunter SA, Duignan P, Roe W. Pathology and epidemiology of stillbirth in New Zealand sea lions (Phocarctos hookeri) from Enderby Island, Auckland Islands, 1998–2012. Vet Pathol. 2016;53(6):1241–7. doi: 10.1177/0300985816638723 27034387

15. Fang C-T, Chuang Y-P, Shun C-T, Chang S-C, Wang J-T. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. J Exp Med. 2004;199(5):697–705. doi: 10.1084/jem.20030857 14993253

16. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15(3):R46. doi: 10.1186/gb-2014-15-3-r46 24580807

17. R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available from: https://www.R-project.org/.

18. Aragon TJ. epitools: Epidemiology Tools. R package version 0.5–10 2017. Available from: https://CRAN.R-project.org/package=epitools.

19. Pinpimai K. Klebsiella pneumoniae in New Zealand sea lions. PhD Thesis: Massey University; 2018.

20. Gonzalez Argandoña A-K. Carriage of pathogens in New Zealand sea lions (Phocarctos hookeri) frozen faecal samples. Masters Thesis: Massey University; 2017.

21. Roberts J, Doonan I. NZ sea lion: demographic assessment of the causes of decline at the Auckland Islands. Demographic model options—correlative assessment. Wellington, New Zealand: Department of Conservation, 2014.

22. Meyer S, Robertson BC, Chilvers BL, Krkošek M. Marine mammal population decline linked to obscured by-catch. PNAS. 2017;114(44):11781–6. doi: 10.1073/pnas.1703165114 29078271

23. Augé AA, Chilvers BL, Moore A, Mathieu R, Robertson BC. Aggregation and dispersion of female New Zealand sea lions at the Sandy Bay breeding colony, Auckland Islands: How unusual is their spatial behaviour? Behaviour. 2009;146(9):1287–311. doi: 10.1163/15683909X427687

24. Lenting B, Gartrell B, Kokosinska A, Duignan P, Michael S, Hunter S, et al. Causes of adult mortality in two populations of New Zealand sea lions (Phocarctos hookeri). Vet Anim Sci. 2019;7:100057. doi: 10.1016/j.vas.2019.100057

25. Pinpimai K, Roe WD, Biggs PJ, Dittmer KE, Michael SA. Draft whole-genome sequences of five Klebsiella pneumoniae isolates from the subantarctic islands of New Zealand. Microbiol Resour Announc. 2018;7(20):e01328–18. doi: 10.1128/MRA.01328-18 30533811

26. Robertson BC, Chilvers BL, Duignan PJ, Wilkinson IS, Gemmell NJ. Dispersal of breeding, adult male Phocarctos hookeri: Implications for disease transmission, population management and species recovery. Biol Conserv. 2006;127(2):227–36. doi: 10.1016/j.biocon.2005.08.011

27. Spraker TR, Lander ME. Causes of mortality in northern fur seals (Callorhinus ursinus), St. Paul Island, Pribilof Islands, Alaska, 1986–2006. J Wildl Dis. 2010;46(2):450–73. doi: 10.7589/0090-3558-46.2.450 20688638

28. Seguel M, Pavés H, Paredes E, Schlatter R. Causes of mortality in South American fur seal pups (Arctocephalus australis gracilis) at Guafo Island, southern Chile (2004–2008). Mar Mamm Sci. 2013;29(1):36–47. doi: 10.1111/j.1748-7692.2011.00534.x

29. Seguel M, Paredes E, Paves H, Molina R, Henriquez F, De Groote F, et al. Pathological findings in South American fur seal pups (Arctocephalus australis gracilis) found dead at Guafo Island, Chile. J Comp Pathol. 2011;145(2–3):308–17. doi: 10.1016/j.jcpa.2011.01.006 21396659

30. Seguel M, Munoz F, Navarrete MJ, Paredes E, Howerth E, Gottdenker N. Hookworm Infection in South American fur seal (Arctocephalus australis) pups: pathology and factors associated with host tissue damage and mortality. Vet Pathol. 2017;54(2):288–97. doi: 10.1177/0300985816677151 28207376

31. Spraker TR, DeLong RL, Lyons ET, Melin SR. Hookworm enteritis with bacteremia in California sea lion pups on San Miguel Island. J Wildl Dis. 2007;43(2):179–88. doi: 10.7589/0090-3558-43.2.179 17495302

32. McIntosh RR, Kennedy CW. Morphology, sex ratio and cause of death in Australian sea lion (Neophoca cinerea) pups. Aust Mammal. 2013;35(1):93–100. doi: 10.1071/am12037

33. Katz H, Morgades D, Castro-Ramos M. Pathological and parasitological findings in South American fur seal pups (Arctocephalus australis) in Uruguay. ISRN Zoology. 2012;2012:1–7. doi: 10.5402/2012/586079

34. Taylor RH. Influence of man on vegetation and wildlife of Enderby and Rose Islands, Auckland Islands. N Z J Bot. 1971;9(2):225–68. doi: 10.1080/0028825X.1971.10429139

35. Childerhouse S, Michael S, Adams L, Burns T, Cockburn S, Hamer D, et al. Final Report: New Zealand sea lion research at the Auckland Islands 2014/15. Wellington, New Zealand: Department of Conservation, 2015.

36. McEwen BJ, Gerdin J. Veterinary forensic pathology: drowning and bodies recovered from water. Vet Pathol. 2016;53(5):1049–56. doi: 10.1177/0300985815625757 26926081

37. Taurisano ND, Butler BP, Stone D, Hariharan H, Fields PJ, Ferguson HW, et al. Streptococcus phocae in marine mammals of northeastern Pacific and Arctic Canada: a retrospective analysis of 85 postmortem investigations J Wildl Dis. 2018;54(1):101–11. doi: 10.7589/2016-09-208 28982020

38. Bartlett G, Smith W, Dominik C, Batac F, Dodd E, Byrne BA, et al. Prevalence, pathology, and risk factors associated with Streptococcus phocae infection in southern sea otters (Enhydra lutris nereis), 2004–10. J Wildl Dis. 2016;52(1):1–9. doi: 10.7589/2015-02-048 26555115

39. González‐Contreras A, Magariños B, Godoy M, Irgang R, Toranzo AE, Avendaño‐Herrera R. Surface properties of Streptococcus phocae strains isolated from diseased Atlantic salmon, Salmo salar L. J Fish Dis. 2011;34(3):203–15. doi: 10.1111/j.1365-2761.2010.01228.x 21306587

40. Lawson PA, Foster G, Falsen E, Davison N, Collins MD. Streptococcus halichoeri sp. nov., isolated from grey seals (Haliochoerus grypus). Int J Syst Evol Microbiol. 2004;54:1753–56. doi: 10.1099/ijs.0.63082-0 15388740

41. Lee K, Kim JY, Jung SC, Lee HS, Her M, Chae C. First Isolation of Streptococcus halichoeri and Streptococcus phocae from a Steller Sea Lion (Eumetopias jubatus) in South Korea. J Wildl Dis. 2016;52(1):183–5. doi: 10.7589/2015-05-112 26555114

42. Moreno B, Bolea R, Morales M, Martín-Burriel I, González C, Badiola J. Isolation and phylogenetic characterization of Streptococcus halichoeri from a European badger (Meles meles) with pyogranulomatous pleuropneumonia. J Comp Pathol. 2015;152(2–3):269–73. doi: 10.1016/j.jcpa.2014.12.012 25678424

43. Foo RM, Chan D. A fishy tale: a man with empyema caused by Streptococcus halichoeri. J Clin Microbiol. 2014;52(2):681–2. doi: 10.1128/JCM.03055-13 24478513

44. Shewmaker P, Whitney A, Humrighouse B. Phenotypic, genotypic, and antimicrobial characteristics of Streptococcus halichoeri isolates from humans, proposal to rename Streptococcus halichoeri as Streptococcus halichoeri subsp. halichoeri, and description of Streptococcus halichoeri subsp. hominis subsp. nov., a bacterium associated with human clinical infections. J Clin Microbiol. 2016;54(3):739–44. doi: 10.1128/JCM.03214-15 26763962

45. Del Giudice P, Plainvert C, Hubiche T, Tazi A, Fribourg A, Poyart C. Infectious cellulitis caused by Streptococcus halichoeri. Acta Derm Venereol. 2018;98(3–4):378–9. doi: 10.2340/00015555-2837 29110017

46. Sturm N, Abalos P, Fernandez A, Rodriguez G, Oviedo P, Arroyo V, et al. Salmonella enterica in pinnipeds, Chile. Emerg Infect Dis. 2011;17(12):2377. doi: 10.3201/eid1712.111103 22172111

47. Gilmartin WG, Vainik PM, Neill VM. Salmonellae in feral pinnipeds off the southern California coast. J Wildl Dis. 1979;15(4):511–4. doi: 10.7589/0090-3558-15.4.511 522219

48. Stoddard R, DeLong R, Byrne B, Jang S, Gulland FM. Prevalence and characterization of Salmonella spp. among marine animals in the Channel Islands, California. Dis Aquat Organ. 2008;81(1):5–11. doi: 10.3354/dao01905 18828559

49. Wirth SE, Ayala-del-Río HL, Cole JA, Kohlerschmidt DJ, Musser KA, Sepúlveda-Torres LdC, et al. Psychrobacter sanguinis sp. nov., recovered from four clinical specimens over a 4-year period. Int J Syst Evol Microbiol. 2012;62(1):49–54. doi: 10.1099/ijs.0.029058–0

50. Bonwitt J, Tran M, Droz A, Gonzalez A, Glover WA. Psychrobacter sanguinis wound infection associated with marine environment exposure, Washington, USA. Emerg Infect Dis. 2018;24(10):1942–4. doi: 10.3201/eid2410.171821 30226173

51. Le Guern R, Wallet F, Vega E, Courcol RJ, Loïez C. Psychrobacter sanguinis: an unusual bacterium for nosocomial meningitis. J Clin Microbiol. 2014;52(9):3475–7. doi: 10.1128/JCM.01197-14 24989605

52. Gerdin JA, McDonough SP, Reisman R, Scarlett J. Circumstances, descriptive characteristics, and pathologic findings in dogs suspected of starving. Vet Pathol. 2016;53(5):1087–94. doi: 10.1177/0300985815575049 25791037

Článek vyšel v časopise


2019 Číslo 11