Sea star wasting disease demography and etiology in the brooding sea star Leptasterias spp.


Autoři: Noah Jaffe aff001;  Renate Eberl aff001;  Jamie Bucholz aff001;  C. Sarah Cohen aff001
Působiště autorů: Estuary and Ocean Science Center, Biology Department, San Francisco State University, San Francisco, California, United States of America aff001;  Santa Rosa Junior College, Santa Rosa, California, United States of America aff002;  University of Wisconsin-River Falls, River Falls, Wisconsin, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225248

Souhrn

Sea star wasting disease (SSWD) describes a suite of disease signs believed to have led to catastrophic die-offs in many asteroid species, beginning in 2013. While most studies have focused on large, easily visible sea stars with widely-dispersing larvae, less information is available on the effect of this disease outbreak on smaller sea star species, such as the six-armed sea star Leptasterias spp. Unlike many larger sea stars, Leptasterias brood non-feeding young instead of broadcast-spawning planktonic larvae. Limited dispersal and thus limited gene flow may make these sea stars more vulnerable to local selective pressures, such as disease outbreaks. Here, we examined Leptasterias populations at sites along the California coast and documented abundance changes coincident with recent Pacific coast SSWD in 2014. Detection of Leptasterias in central California declined, and Leptasterias were not detected at multiple sites clustered around the San Francisco Bay outflow in the most recent surveys. Additionally, we categorized disease signs in Leptasterias in the field and laboratory, which mirrored those seen in larger sea stars in both settings. Finally, we found that magnesium chloride (MgCl2) slowed the progression of physical deterioration related to SSWD when applied to sea stars in the laboratory, suggesting that MgCl2 may prolong the survival of diseased individuals.

Klíčová slova:

California – Cryptic speciation – Epidemiology – Invertebrates – Magnesium chloride – Population density – Salinity – Starfish


Zdroje

1. Bucci C, Francoeur M, McGreal J, Smolowitz R, Zazueta-Novoa V, Wessel GM, et al. Sea Star Wasting Disease in Asterias forbesi along the Atlantic Coast of North America. PLoS ONE. 2017; 12(12): e0188523. doi: 10.1371/journal.pone.0188523 29228006

2. Eisenlord ME, Groner ML, Yoshioka RM, Elliott J, Maynard J, Fradkin S, et al. Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Philos Trans R Soc Lond B. 2016; 371(1689): 20150212.

3. Menge BA, Cerny-Chipman EB, Johnson A, Sullivan J, Gravem S, Chan F. Sea star wasting disease in the keystone predator Pisaster ochraceus in Oregon: insights into differential population impacts, recovery, predation rate, and temperature effects from long-term research. PLoS One. 2016; 11(5): e0153994. doi: 10.1371/journal.pone.0153994 27144391

4. Montecino-Latorre D, Eisenlord ME, Turner M, Yoshioka R, Harvell CD, Pattengill-Semmens CV, et al. Devastating transboundary impacts of sea star wasting disease on subtidal asteroids. PLoS One. 2016; 11(10): e0163190. doi: 10.1371/journal.pone.0163190 27783620

5. Harvell CD, Montecino-Latorre D, Caldwell JM, Burt JM, Bosley K, Keller A, et al. Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Sci. Adv. 2019; 5 (1): eaau7042. doi: 10.1126/sciadv.aau7042 30729157

6. Hewson I, Button JB, Gudenkauf BM, Miner B, Newton AL, Gaydos JK, et al. Densovirus associated with sea-star wasting disease and mass mortality. Proc Natl Acad Sci. 2014; 111(48): 17278–83. doi: 10.1073/pnas.1416625111 25404293

7. Miner CM, Burnaford JL, Ambrose RF, Antrim L, Bohlmann H, Blanchette CA,et al. Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery. PLoS One. 2018; 13(3): e0192870. doi: 10.1371/journal.pone.0192870 29558484

8. Groner ML, Maynard J, Breyta R, Carnegie RB, Dobson A, Friedman CS, et al. Managing marine disease emergencies in an era of rapid change. Philos Trans R Soc Lond B. 2016; 371(1689): 20150364.

9. Maynard J, Hooidonk R van, Harvell CD, Eakin CM, Liu G, Willis BL, et al. Improving marine disease surveillance through sea temperature monitoring, outlooks and projections. Philos Trans R Soc Lond B. 2016; 371(1689): 20150208.

10. Bates AE, Hilton BJ, Harley CDG. Effects of temperature, season and locality on wasting disease in the keystone predatory sea star Pisaster ochraceus. Dis Aquat Org. 2009; 86(3): 245–51. doi: 10.3354/dao02125 20066959

11. Kohl WT, McClure TI, Miner BG. Decreased temperature facilitates short-term sea star wasting disease survival in the keystone intertidal sea star Pisaster ochraceus. PLoS ONE. 2016; 11(4): 1–9.

12. Hewson I, Bistolas KSI, Cardé QME, Button JB, Foster PJ, Flanzenbaum JM, et al. Investigating the complex association between viral ecology, environment, and Northeast Pacific sea star wasting. Front Mar Sci. 2018; 5(77).

13. Braun C, Fisher R, D’Avignon M, Jaffe N, Park S, Langhans M, et al. Leptasterias spp. and sea star wasting disease: a temperature and salinity challenge experiment. Proceedings of the 100th meeting of the Western Society of Naturalists; 2016 Nov 10–13; Monterey, CA.

14. Fuess LE, Eisenlord ME, Closek CJ, Tracy AM, Mauntz R, Gignoux-Wolfsohn S, et al. Up in arms: immune and nervous system response to sea star wasting disease. PLoS ONE. 2015; 10(7): e0133053. doi: 10.1371/journal.pone.0133053 26176852

15. Gudenkauf BM, Hewson I. Metatranscriptomic analysis of Pycnopodia helianthoides (Asteroidea) affected by sea star wasting disease. PLoS ONE. 2015; 10(5): 1–10.

16. Wares JP, Schiebelhut LM. What doesn’t kill them makes them stronger: an association between elongation factor 1-alpha overdominance in the sea star Pisaster ochraceus and “sea star wasting disease.” PeerJ. 2016; 4: e1876. doi: 10.7717/peerj.1876 27069810

17. Paine RT. Food web complexity and species diversity. Am Nat. 1966; 100(910): 65–75.

18. Paine RT. The Pisaster-Tegula Interaction: Prey patches, predator food preference, and intertidal community structure. Ecology. 1969; 50(6): 950–61.

19. Menge BA. Effect of wave action and competition on brooding and reproductive effort in seastar, Leptasterias hexactis. Ecology. 1974; 55(1): 84–93.

20. Menge BA. Community regulation—under what conditions are bottom-up factors important on rocky shores. Ecology. 1992; 73, 755–765.

21. Gravem SA, Morgan SG. Prey state alters trait-mediated indirect interactions in rocky tide pools. Funct Ecol. 2015; 30(9): 1574–82.

22. Morgan SG, Gravem SA, Lipus AC, Grabiel M, Miner BG. Trait-mediated indirect interactions among residents of rocky shore tidepools. Mar Ecol Prog Ser. 2016; 552: 31–46.

23. Hemond EM, and Vollmer SV. Genetic Diversity and Connectivity in the Threatened Staghorn Coral (Acropora cervicornis) in Florida. PLoS ONE. 2010; 5, e8652. doi: 10.1371/journal.pone.0008652 20111583

24. Chia F. Brooding Behavior of a 6-Rayed Starfish Leptasterias hexactis. Biol Bull. 1966; 130: 304–315.

25. George S. The Leptasterias (Echinodermata, Asteroidea) species complex—variation. Mar Ecol Prog Ser. 1994; 109(1): 95–8.

26. Bingham BL, Giles K, Jaeckle WB. Variability in broods of the seastar Leptasterias aequalis. Can J Zool. 2004; 82(3): 457–63.

27. Menge BA. Brood or broadcast—adaptive significance of different reproductive strategies in 2 intertidal sea stars Leptasterias hexactis and Pisaster ochraceus. Mar Biol. 1975; 31(1): 87–100.

28. Strathmann RR. What controls the type of larval development? Summary statement for the evolution session. Bull Mar Sci. 1986; 39(2): 616–622.

29. Sherman CDH, Hunt A, Ayre DJ. Is life history a barrier to dispersal? Contrasting patterns of genetic differentiation along an oceanographically complex coast. Biol J Linn Soc Lond. 2008; 95: 106–116.

30. Vollmer SV, Palumbi SR. Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: implications for the recovery of endangered reefs. J Hered. 2007; 98: 40–50. doi: 10.1093/jhered/esl057 17158464

31. Groner ML, Burge CA, Couch C, Kim CJS, Siegmund GF, Singhal S, et al. Host demography influences the prevalence and severity of eelgrass wasting disease. Dis Aquat Org. 2014; 108, 165–175. doi: 10.3354/dao02709 24553421

32. Jurgens LJ, Rogers-Bennett L, Raimondi PT, Schiebelhut LM, Dawson MN, Grosberg RK, et al. Patterns of mass mortality among rocky shore invertebrates across 100 km of northeastern pacific coastline. PLoS ONE. 2015; 10(6): e0126280. doi: 10.1371/journal.pone.0126280 26039349

33. Gravem SA, Morgan SG. Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators. Ecology. 2017; 98: 1006–1015. doi: 10.1002/ecy.1672 27935647

34. Lafferty KD, Harvell CD, Conrad JM, Friedman CS, Kent ML, Kuris AM, et al. Infectious diseases affect marine fisheries and aquaculture economics. Ann Rev Mar Sci. 2015; 7: 471–496. doi: 10.1146/annurev-marine-010814-015646 25251276

35. Miner M, Gaddam R, Douglass M. Sea Star Wasting Syndrome [Internet]. Santa Cruz (CA): Multi-Agency Rocky Intertidal Network [updated 2018 Nov 13]. Available from: https://www.eeb.ucsc.edu/pacificrockyintertidal/data-products/sea-star-wasting/Pearse JS, Hines AH. Long-term population dynamics of sea urchins in a central California kelp forest: rare recruitment and rapid decline. Mar Ecol Prog Ser. 1987; 39(3): 275–83.

36. Pearse JS, Hines AH. Long-term population dynamics of sea urchins in a central California kelp forest: rare recruitment and rapid decline. Mar Ecol Prog Ser. 1987; 39(3): 275–83.

37. Sagarin RD, Barry JP, Gilman SE, Baxter CH. Climate-related change in an intertidal community over short and long time scales. Ecol Monogr. 1999; 69(4): 465–90.

38. Bates CR, Scott G, Tobin M, Thompson R. Weighing the costs and benefits of reduced sampling resolution in biomonitoring studies: Perspectives from the temperate rocky intertidal. Biol Conserv. 2007; 137(4): 617–25.

39. Schoch GC, Menge BA, Allison G, Kavanaugh M, Thompson SA, Wood SA. Fifteen degrees of separation: Latitudinal gradients of rocky intertidal biota along the California Current. Limnol Oceanogr. 2006; 51(6): 2564–85.

40. Blanchette CA, Miner CM, Raimondi PT, Lohse D, Heady KEK, Broitman BR. Biogeographical patterns of rocky intertidal communities along the Pacific coast of North America. J Biogeogr. 2008; 35(9): 1593–607.

41. Moritsch MM, Raimondi PT. Reduction and recovery of keystone predation pressure after disease-related mass mortality. Ecol Evol. 2018; 8(8): 3952–64. doi: 10.1002/ece3.3953 29721271

42. Murray SN, Ambrose R, Dethier MN. Monitoring rocky shores. Oakland: University of California Press; 2006. pp. 240.

43. Pearse J, Salzman J. What is LiMPETS? [Internet]. Santa Cruz (CA): Longterm Monitoring and Experiential Training for Students [updated 2019]. Available from: http://limpets.org/what-is-limpets/

44. Goddard J, Pearse J. Long-term faunal changes in California nudibranchs: climate change and local ocean health. California Sea Grant College Program Final Report. 2011.

45. Goddard JHR, Schaefer MC, Hoover C, Valdés Á. Regional extinction of a conspicuous dorid nudibranch (Mollusca: Gastropoda) in California. Mar Biol. 2013; 160: 1497–1510.

46. Goddard JHR, Treneman N, Pence WE, Mason DE, Dobry PM, Green B, et al. Nudibranch range shifts associated with the 2014 warm anomaly in the Northeast Pacific. Bull South Calif Acad Sci. 2016; 115: 15–40.

47. Kuta KG, and Richardson LL. Abundance and distribution of black band disease on coral reefs in the northern Florida keys. Coral Reefs. 1996; 15: 219–223.

48. Richardson LL, Goldberg WM, Carlton RG, Halas JC. Coral disease outbreak in the Florida Keys: Plague Type II. Rev Biol Trop. 1998; 46, 187–198.

49. Burge CA, Friedman CS, Getchell R, House M, Lafferty KD, Mydlarz LD, et al. Complementary approaches to diagnosing marine diseases: a union of the modern and the classic. Philos Trans R Soc Lond B Biol Sci. 2016; 371: 20150207. doi: 10.1098/rstb.2015.0207 26880839

50. Kahle D, Wickham H. ggmap: Spatial Visualization with ggplot2. The R Journal. 5(1): 144–161. Available from: http://journal.r-project.org/archive/2013-1/kahle-wickham.pdf

51. Bingham BL, Burr J, Head HW. Causes and consequences of arm damage in the sea star Leptasterias hexactis. Can J Zool. 2000; 78(4): 596–605.

52. Strathmann MF. Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. Washington: University of Washington Press; 1987.

53. Statistix Analytical Software. Version 10 [software]. [cited 2016 July] Available from: https://www.statistix.com/.

54. Marchesiello P, McWilliams JC, and Shchepetkin A. Equilibrium structure and dynamics of the California current system. J Phys Oceanogr. 2003; 33: 753–783.

55. Kelly RP, Palumbi SR. Genetic structure among 50 species of the Northeastern Pacific rocky intertidal community. PLoS ONE. 2010; 5(1): e8594. doi: 10.1371/journal.pone.0008594 20062807

56. Anderson RM, May RM. The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos Trans R Soc Lond B Biol Sci. 1986; 314: 533–570. doi: 10.1098/rstb.1986.0072 2880354

57. Lafferty KD, Porter JW, Ford SE. Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst. 2004; 35: 31–54.

58. Núñez-Pons L, Work TM, Angulo-Preckler C, Moles J, Avila C. Exploring the pathology of an epidermal disease affecting a circum-Antarctic sea star. Sci Rep. 2018; 8: 11353. doi: 10.1038/s41598-018-29684-0 30054527

59. Lafferty KD, and Holt RD. How should environmental stress affect the population dynamics of disease? Ecol Lett. 2003; 6: 654–664.

60. Munroe DM, Powell EN, Ford SE, Hofmann EE, and Klinck JM. Outcomes of asymmetric selection pressure and larval dispersal on evolution of disease resistance: a metapopulation modeling study with oysters. Mar Ecol Prog Ser. 2015; 531: 221–239.

61. Melroy LM, Smith RJ, Cohen CS. Phylogeography of direct-developing sea stars in the genus Leptasterias in relation to San Francisco Bay outflow in central California. Mar Biol. 2017; 164: 152.Melroy LM. Temporal and spatial variation in population structure and distribution of a direct-developing cryptic species complex, Leptasterias. M.Sc. Thesis, San Francisco State University. 2016.

62. Melroy LM. Temporal and spatial variation in population structure and distribution of a direct-developing cryptic species complex, Leptasterias. M.Sc. Thesis, San Francisco State University. 2016.

63. Schiebelhut LM, Puritz JB, Dawson MN. Decimation by sea star wasting disease and rapid genetic change in a keystone species, Pisaster ochraceus. Proc Natl Acad Sci. 2018: 201800285.

64. Uthicke S, Schaffelke B, Byrne M. (2009). A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr. 2009; 79: 3–24.

65. Crowe TP, Thompson RC, Bray S, Hawkins SJ. Impacts of anthropogenic stress on rocky intertidal communities. J Aquat Ecosyst Stress Recovery. 2000; 7(4): 273–97.

66. Noble RT, Griffith JF, Blackwood AD, Fuhrman JA, Gregory JB, Hernandez X, et al. Multitiered approach using quantitative PCR to track sources of fecal pollution affecting Santa Monica Bay, California. Appl Environ Microbiol. 2006; 72(2): 1604–12. doi: 10.1128/AEM.72.2.1604-1612.2006 16461716

67. Puritz JB, Toonen RJ. Coastal pollution limits pelagic larval dispersal. Nat Commun. 2011; 2: 1238.

68. Conomos TJ, Smith RE, Gartner JW. Environmental setting of San Francisco Bay. Hydrobiologia. 1985; 129(1): 1–12.

69. Stickle WB, Denoux GJ. Effects of in situ tidal salinity fluctuations on osmotic and ionic composition of body fluid in Southeastern Alaska rocky intertidal fauna. Mar Biol. 1976; 37(2): 125–35.

70. Shirley TC, Stickle WB. Responses of Leptasterias hexactis (Echinodermata: Asteroidea) to low salinity. Mar Biol. 1982; 69(2): 147–54.

71. Agüera A, Schellekens T, Jansen JM, Smaal AC. Effects of osmotic stress on predation behaviour of Asterias rubens L. J. Sea Res. 2015; 99: 9–16.

72. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, et al. The impacts of climate change in coastal marine systems. Ecol Lett. 2006; 9(4): 228.

73. Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world’s marine ecosystems. Science. 2010; 328(5985): 1523–8. doi: 10.1126/science.1189930 20558709

74. Harvell CD, Aronson R, Baron N, Connell J, Dobson A, Ellner S, et al. The rising tide of ocean diseases: unsolved problems and research priorities. Front Ecol Environ. 2004; 2(7): 375–82.

75. Burge CA, Eakin CM, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, et al. Climate change influences on marine infectious diseases: implications for management and society. Ann Rev Mar Sci. 2014; 6(1): 249–77.

76. Lawrence JM. The effect of temperature-salinity combinations on the functional well-being of adult Lytechinus variegatus (Lamarck) (Echinodermata, Echinoidea). J Exp Mar Bio Ecol. 1975; 18(3): 271–5.

77. Held MBE, Harley CDG. Responses to low salinity by the sea star Pisaster ochraceus from high- and low-salinity populations. Invertebr Biol. 2009; 128(4): 381–90.

78. Niesen TM. Population and reproductive biology of the six-rayed sea star Leptasterias hexactis on the protected outer coast. Dissertation, The University of Oregon. 1973.

79. Menge BA. Competition for food between two intertidal starfish species and its effect on body size and feeding. Ecology. 1972; 53(4): 635–44.

80. Gravem SA, Morgan SG. Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators. Ecology. 2016; 98(4): 1006–15.

81. Gravem SA, Morgan SG. Trait-mediated indirect effects in a natural tidepool system. Mar Biol. 2019; 166 (2), 23.

82. Soulé ME, Bolger DT, Alberts AC, Wrights J, Sorice M, Hill S. Reconstructed Dynamics of Rapid Extinctions of Chaparral-Requiring Birds in Urban Habitat Islands. Conservation Biology. 1988; 2(1): 75–92.

83. Courchamp F, Langlais M, Sugihara G. Cats protecting birds: modelling the mesopredator release effect. Journal of Animal Ecology. 1999; 68(2): 282–92.

84. Dulvy NK, Freckleton RP, Polunin NVC. Coral reef cascades and the indirect effects of predator removal by exploitation. Ecology Letters. 2004; 7(5): 410–6.

85. Ritchie EG, Johnson CN. Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters. 2009; 12(9): 982–98. doi: 10.1111/j.1461-0248.2009.01347.x 19614756

86. Meldrum DR, Ayala A, Chaudry IH. Energetics of lymphocyte “burnout” in late sepsis: adjuvant treatment with ATP-MgCl2 improves energetics and decreases lethality. J Surg Res. 1994; 56: 537–542. doi: 10.1006/jsre.1994.1086 8015308

87. Robinson DA, Griffith RW, Shechtman D, Evans RB, Conzemius MG. In vitro antibacterial properties of magnesium metal against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Acta Biomater. 2010; 6(5): 1869–77. doi: 10.1016/j.actbio.2009.10.007 19818422

88. Alarcón PO, Sossa K, Contreras D, Urrutia H, Nocker A. Antimicrobial properties of magnesium chloride at low pH in the presence of anionic bases. Magnes Res. 2014; 27(2): 57–68. doi: 10.1684/mrh.2014.0362 25252874

89. Butt D, O’Connor SJ, Kuchel R, O’Connor WA, Raftos DA. Effects of the muscle relaxant, magnesium chloride, on the Sydney rock oyster (Saccostrea glomerata). Aquac. 2008; 275: 342–346.

90. Söderhäll K, Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol. 1998; 10(1): 23–8. doi: 10.1016/s0952-7915(98)80026-5 9523106

91. Söderhäll K. Special issue: Invertebrate immunity. Dev Comp Immunol. 1999; 23: 263–266. doi: 10.1016/s0145-305x(99)00009-9

92. Nappi AJ, Christensen BM. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem Mol Biol. 2005; 35(5): 443–59. doi: 10.1016/j.ibmb.2005.01.014 15804578

93. Sorrentino RP, Carton Y, Govind S. Cellular immune response to parasite infection in the drosophila lymph gland is developmentally regulated. Dev Biol. 2002; 243(1): 65–80. doi: 10.1006/dbio.2001.0542 11846478

94. Santos R, Haesaerts D, Jangoux M, Flammang P. The tube feet of sea urchins and sea stars contain functionally different mutable collagenous tissues. J Exp Biol. 2005; 208(12): 2277–88.


Článek vyšel v časopise

PLOS One


2019 Číslo 11