Invasive Species Compendium

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Xenohaliotis californiensis

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Xenohaliotis californiensis

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Xenohaliotis californiensis
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Proteobacteria
  •     Class: Alphaproteobacteria
  •       Order: Rickettsiales
  •         Family: Anaplasmataceae
  • Summary of Invasiveness
  • Xenohaliotis californiensis (also called WS-RLO) is a bacterium that causes a fatal disease of marine gastropod molluscs of the genus Haliotis (abalones), called withering syndrome (WS).  Disease occur...

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Identity

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Preferred Scientific Name

  • Xenohaliotis californiensis

Other Scientific Names

  • Candidatus Xenohaliotis californiensis

International Common Names

  • English: abalone rickettsia

English acronym

  • WS-RLO

Summary of Invasiveness

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Xenohaliotis californiensis (also called WS-RLO) is a bacterium that causes a fatal disease of marine gastropod molluscs of the genus Haliotis (abalones), called withering syndrome (WS).  Disease occurs in abalones along the eastern Pacific margin of North America in California, USA and Baja California, Mexico; it was first reported in California in 1985 and has been spreading both northwards and southwards.  As infected abalones have been transported to many countries around the world, the geographic range is likely to be broader than originally suspected.  WS is characterized by degeneration of the digestive gland of the host and depletion of glycogen reserves.  Animals cease feeding and catabolize foot muscle protein as an energy source, resulting in atrophy of the pedal muscle, and ultimately death. Some abalone species are endangered or of concern regarding their status, and some are important for fisheries or aquaculture, so the disease can have a significant impact on biodiversity and a significant economic impact. It is on the list of diseases notifiable to the World Organisation for Animal Health (OIE).

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Proteobacteria
  •         Class: Alphaproteobacteria
  •             Order: Rickettsiales
  •                 Family: Anaplasmataceae
  •                     Genus: Xenohaliotis
  •                         Species: Xenohaliotis californiensis

Notes on Taxonomy and Nomenclature

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Xenohaliotis californiensis is a non-motile, Gram-negative intracellular bacterium in the family Anaplasmataceae (originally described as being in the Rickettsiaceae) and is closely related to members of the genera Ehrlichia, Anaplasma and Cowdria (Dumler et al., 2001; Friedman et al., 2000).  Its name is derived from the Latin meaning “a foreign organism in abalone from California”.  The provisional status of Candidatus was created for unculturable and/or poorly characterized organisms (Murray and Schleifer, 1994; Murray and Stackebrandt, 1995) and thus was initially used in this case.  The organism is unable to grow in vitro in artificial media or in fish cell lines and was originally described by using electron microscopy and 16S rRNA sequence analysis (Friedman et al., 2000).  Because it causes a disease in abalone (Haliotis spp.) termed withering syndrome (WS), the organism has also historically been called WS-RLO (rickettsia-like organism).

Distribution

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X. californiensis and the disease that it causes are distributed along the west coast of North America from Baja California, Mexico, to southern Sonoma County, California, and continue to spread along this coast. Infected abalones have been transported to a number of countries around the world, and the species is suspected to have a broad range, particularly where California red abalone (Haliotis rufescens) are cultured or where native species have been exposed to them (OIE, 2012).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Sea Areas

Atlantic, NortheastPresent, few occurrencesIntroducedCrosson et al., 2014Introduced by transport of infected abalones
Pacific, Eastern CentralPresentCrosson et al., 2014
Pacific, NorthwestPresentIntroducedWetchateng et al., 2010; Kiryu et al., 2013Introduced by transport of infected abalones
Pacific, SoutheastPresentCrosson et al., 2014
Pacific, Western CentralPresent, few occurrencesIntroducedWetchateng et al., 2010Introduced by transport of infected abalones

Asia

ChinaPresent, few occurrencesIntroduced2006Wetchateng et al., 2010Introduced by transport of infected abalones
IsraelPresent, few occurrencesIntroducedCrosson et al., 2014Introduced by transport of infected abalones
JapanPresent, few occurrencesIntroduced2010Kiryu et al., 2013Introduced by transport of infected abalones
TaiwanPresent, few occurrencesIntroduced2006Wetchateng et al., 2010Introduced by transport of infected abalones
ThailandPresent, few occurrencesIntroduced2006Wetchateng et al., 2010Introduced by transport of infected abalones

North America

MexicoWidespread2001Caceres-Martinez and Tinoco-Orta, 2001Baja California
USAPresentPresent based on regional distribution.
-CaliforniaWidespread Invasive Crosson et al., 2014First reported in 1985. Present as far north as Sonoma County, including Channel and Farallon Islands

South America

ChilePresent, few occurrencesIntroducedCrosson et al., 2014Introduced by transport of infected abalones

Europe

IcelandPresent, few occurrencesIntroducedCrosson et al., 2014Introduced by transport of infected abalones
IrelandPresent, few occurrencesIntroducedCrosson et al., 2014Introduced by transport of infected abalones
SpainPresent, few occurrencesIntroducedBalseiro et al., 2006; Crosson et al., 2014In Galicia, NW Spain; introduced by transport of infected abalones

History of Introduction and Spread

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Withering syndrome (WS) was first observed in black abalone (Haliotis cracherodii) along the shores of Santa Cruz Island, California, USA, in 1985, shortly after the strong 1982-1983 El Niño-Southern Oscillation (ENSO) event (Crosson et al., 2014).  From 1986 to 1989, WS in black abalone populations was observed at Anacapa Island, followed by losses on Santa Cruz, Santa Rosa, Santa Barbara and San Miguel Islands, California.  In 1988, it was observed in Diablo Canyon, but it was not observed elsewhere along the Californian mainland until its discovery north of Point Conception in 1996.  It spread naturally and via anthropogenic movement of farmed red abalone (Haliotis rufescens) throughout southern California, into the warmer waters of Baja California, Mexico, and northward, from the late 1980s to the present.  It continues to spread in a northward direction and is strongly associated with increasing coastal warming and El Niño events.  WS-RLO is considered to be continuously distributed along the west coast of North America from Baja California to southern Sonoma County, California, including the Channel and Farallon Islands (Crosson et al., 2014).  As infected abalones have been transported to Chile, China, Taiwan, Iceland, Ireland, Israel, Japan, Spain, Thailand, and possibly other countries, the geographic range of the species is suspected to be broad, particularly where H. rufescens are cultured or where native species have been exposed to them (OIE, 2012).

Risk of Introduction

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The geographic distribution of WS-RLO is expanding as abalones are transported worldwide.  Infected abalones have been transported to Chile, China, Taiwan, Iceland, Ireland, Israel, Spain, Thailand (Wetchateng et al., 2010), and most recently Japan (Kiryu et al., 2013).  Several lines of evidence suggest that temperature is extremely important in the ecology of withering syndrome; temperature can modulate both the transmission and development of this disease (Braid et al., 2005; Moore et al., 2000; Vilchis et al., 2005).  Thus, as the Earth’s climate changes and the oceans warm, it is likely that the geographic distribution of WS-RLO will expand into new areas.

Pathogen Characteristics

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Xenohaliotis californiensis is a non-motile, Gram-negative intracellular bacterium that is closely related to members of the genera Ehrlichia, Anaplasma, and Cowdria within the family Anaplasmataceae (originally described as being in the Rickettsiaceae) (Dumler et al., 2001; Friedman et al., 2000).  The organism, which is also referred to as WS-RLO, has not as yet been cultured in artificial media or in fish cell lines, so detailed knowledge of it is limited. 

The disease withering syndrome (WS) was first observed in black abalone (Haliotis cracherodii) along the shores of Santa Cruz Island, California, USA, in 1985 (Crosson et al., 2014).  During the subsequent 10 years, no aetiological agent was identified.  In 1995, Gardner et al. suggested that a Rickettsiales-like prokaryote that infects the mucosal epithelium of the gastrointestinal tract might be the causative agent of WS (Gardner et al., 1995).  In 2000, Friedman et al. identified and named the causative agent of WS based on electron microscopic analysis of infected tissues and phylogenetic analysis of the 16S rRNA sequence of the rickettsia-like organism associated with WS in black abalone from California (Friedman et al., 2000).  In 2012, Friedman and Crosson described a novel WS-RLO variant that was infected with a bacteriophage virus, and phage infection was shown to be responsible for the morphological variation observed in the WS-RLO (Friedman and Crosson, 2012).  Subsequent investigations suggest that the presence of the phage is attenuating WS disease development.  In fact, recent research showed that the presence of phage-infected WS-RLO reduced the host response to infection, WS-RLO infection loads, and associated mortality in infected black abalone (Friedman et al., 2014a).

Hosts/Species Affected

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The WS-RLO agent infects members of the genus Haliotis. Natural infections have been found in black abalones (H. cracherodii), white abalones (H. sorenseni), red abalones (H. rufescens), pink abalones (H. corrugata), green abalones (H. fulgens), the small abalone (H. diversicolor supertexta) (Wetchateng et al., 2010), and the European abalone (H. tuberculata) (Balseiro et al., 2006); flat (H. wallalensis) and Japanese abalones (H. discus hannai) have been infected in the laboratory (OIE, 2012).  Other abalone species have not been tested (OIE, 2012), but are probably susceptible to infection as well.  Susceptibility and mortality vary with species.  For example, H. sorenseni and H. cracherodii are highly susceptible to WS-RLO infection and it is known to cause disease with nearly 100% mortality in these species (Moore et al., 2009; OIE, 2012), while in H. rufescens, only up to 35 % mortality has been observed (Moore et al., 2000).  The magnitude of mortality is not well documented in H. corrugata and H. fulgens.  Clearly, host factors are involved in this differential susceptibility to disease, but the exact nature of these factors remain unknown.

While no definitive vector or intermediate host for WS-RLO has been identified, it has been suggested that some colonial ascidians (commonly called “sea squirts”) may concentrate the bacterium (based on polymerase chain reaction evidence).  Thus, the possibility exists of such species acting as vectors for the bacterium, but further investigation of possible vectors is warranted (OIE, 2012).

Host Animals

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Animal nameContextLife stageSystem
Haliotis corrugataAquatic: All Stages
Haliotis cracherodii (black abalone)Aquatic: All Stages
Haliotis discus
Haliotis discus hannai (Japanese abalone)Aquatic: All Stages
Haliotis diversicolor supertextaAquatic: All Stages
Haliotis fulgens (green abalone)Domesticated host, Wild hostAquatic: All Stages
Haliotis rufescens (red abalone)Aquatic: All Stages
Haliotis sorenseni (white abalone)Aquatic: All Stages
Haliotis tuberculata (European edible abalone)Aquatic: All Stages
Haliotis walallensisAquatic: All Stages

Notes on Natural Enemies

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A bacteriophage virus has been found to infect the bacterium and attenuate development of the disease (Friedman et al., 2014a).

Means of Movement and Dispersal

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WS-RLO has been introduced to a number of countries by the transport of infected abalones (Crosson et al., 2014). As exposure to seawater containing infectious material is sufficient for transmission, with no requirement for direct contact between animals (Balseiro et al., 2006; Braid et al., 2005; Friedman et al., 2002), it is presumably spread locally by water currents.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
HitchhikerTransport of infected abalones Yes Yes Crosson et al., 2014

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stock Yes Crosson et al., 2014
Water Yes

Economic Impact

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The meat (foot muscle) of abalone is used for food, and the shells are used as decorative items and as a source of ‘mother of pearl’ for jewelry, buttons, buckles, and inlay.  Abalone is one of the most highly prized seafood delicacies in many parts of the world, particularly in some parts of Latin America and Asia.  In 2013, the total global production of abalone from legal fisheries and farms was 110,950 metric tonnes (Cook, 2014).  Given that certain species of abalone can sell for about US$30/Kg or more (Cook, 2014), the economic impact from losses due to diseases such as WS can be significant.

Environmental Impact

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Impact on Habitats

Abalones of the genus Haliotis inhabit the nearshore intertidal and shallow subtidal zones.  They are ecologically important in engineering habitat by grazing on micro- and macroalgae, thereby maintaining open areas for the recruitment of conspecifics and other benthic organisms (Crosson et al., 2014). A reduction in their population caused by withering syndrome could therefore have significant ecological effects.

Impact on Biodiversity

Withering syndrome is an important reason for the Critically Endangered status of Haliotis cracherodii (IUCN, 2014), and one of a number of causes of the decline in the populations of H. fulgens and H. corrugata which have led to their being classed as species of concern in the USA (National Marine Fisheries Service, 2009). It is considered to be a potential threat to the Endangered H. sorenseni, but not so far to have been a major factor in the decline of this species in the wild (National Marine Fisheries Service, 2008).

Threatened Species

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Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
Haliotis corrugataNational list(s) National list(s)CaliforniaPathogenicNational Marine Fisheries Service, 2009
Haliotis cracherodii (black abalone)CR (IUCN red list: Critically endangered) CR (IUCN red list: Critically endangered); USA ESA listing as endangered species USA ESA listing as endangered species; CaliforniaPathogenicIUCN, 2014
Haliotis fulgens (green abalone)National list(s) National list(s)CaliforniaPathogenicNational Marine Fisheries Service, 2009
Haliotis sorenseni (white abalone)USA ESA listing as endangered species USA ESA listing as endangered speciesCaliforniaPathogenicNational Marine Fisheries Service, 2008

Risk and Impact Factors

Top of page Impact outcomes
  • Host damage
  • Negatively impacts aquaculture/fisheries
  • Reduced native biodiversity
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally illegally

Gaps in Knowledge/Research Needs

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WS-RLO has remained refractory to in vitro culture.  Thus, there is a critical research need to develop methods to propagate the bacterium in the laboratory.  Another area of continued research should focus on mechanisms of disease resistance in abalone.  In 2012, a bacteriophage virus was discovered infecting WS-RLO, which resulted in morphological changes in the bacterium (Friedman and Crosson, 2012); subsequent studies showed that the presence of phage-infected WS-RLO reduced disease in infected abalone (Friedman et al., 2014a).  Clearly, understanding the mechanisms involved in this phage-induced reduction in pathogenicity could lead to a better understanding of the host-pathogen (and pathogen-phage) relationship and possibly lead to more effective treatment options.

References

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Balseiro P; Aranguren R; Gestal C; Novoa B; Figueras A, 2006. Candidatus Xenohaliotis californiensis and Haplosporidium montforti associated with mortalities of abalone Haliotis tuberculata cultured in Europe. Aquaculture, 258(1/4):63-72. http://www.sciencedirect.com/science/journal/00448486

Braid BA; Moore JD; Robbins TT; Hedrick RP; Tjeerdema RS; Friedman CS, 2005. Health and survival of red abalone, Haliotis rufescens, under varying temperature, food supply, and exposure to the agent of withering syndrome. Journal of Invertebrate Pathology, 89(3):219-231.

Caceres-Martinez J; Tinoco-Orta GD, 2001. Symbionts of cultured red abalone Haliotis rufescens from Baja California, Mexico. Journal of Shellfish Research [4th International Symposium on Abalone Biology, Fisheries, and Culture, University of Capetown, Capetown, South Africa, 6-11 February, 2000.], 20(2):875-881.

Cook PA, 2014. The worldwide abalone industry. Modern Economy, 5:1181-1186.

Crosson LM; Wight N; Vanblaricom GR; Kiryu I; Moore JD; Friedman CS, 2014. Abalone withering syndrome: distribution, impacts, current diagnostic methods and new findings. Diseases of Aquatic Organisms, 108(3):261-270. http://www.int-res.com/abstracts/dao/v108/n3/p261-270/

Dumler JS; Barbet AF; Bekker CP; Dasch GA; Palmer GH; Ray SC; Rikihisa Y; Rurangirwa FR, 2001. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and 'HGE agent' as subjective synonyms of Ehrlichia phagocytophila. International Journal of Systematic and Evolutionary Microbiology, 51(6):2145-2165.

Friedman CS; Andree KB; Beauchamp KA; Moore JD; Robbins TT; Shields JD; Hedrick RP, 2000. 'Candidatus Xenohaliotis californiensis', a newly described pathogen of abalone, Haliotis spp., along the west coast of North America. International Journal of Systematic and Evolutionary Microbiology, 50(2):847-855.

Friedman CS; Biggs W; Shields JD; Hedrick RP, 2002. Transmission of withering syndrome in black abalone, Haliotis cracherodii Leach. Journal of Shellfish Research, 21(2):817-824.

Friedman CS; Crosson LM, 2012. Putative phage hyperparasite in the rickettsial pathogen of abalone, "Candidatus Xenohaliotis californiensis". Microbial Ecology, 64(4):1064-1072. http://rd.springer.com/article/10.1007/s00248-012-0080-4/fulltext.html

Friedman CS; Finley CA, 2003. Evidence for an anthropogenic introduction of "Candidatus Xenohaliotis californiensis", the etiological agent of withering syndrome, into northern California abalone populations via conservation efforts. Canadian Journal of Fisheries and Aquatic Sciences, 60:1424-1431.

Friedman CS; Scott BB; Strenge RE; Vadopalas B; McCormick TB, 2007. Oxytetracycline as a tool to manage and prevent losses of the endangered white abalone, Haliotis sorenseni, caused by withering syndrome. Journal of Shellfish Research, 26(3):877-885. http://www.bioone.org/perlserv/?request=get-abstract&doi=10.2983%2F0730-8000%282007%2926%5B877%3AOAATTM%5D2.0.CO%3B2

Friedman CS; Wight N; Crosson LM; VanBlaricom GR; Lafferty KD, 2014. Reduced disease in black abalone following mass mortality: phage therapy and natural selection. Frontiers in Microbiology, 5(March):78. http://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00078/full

Friedman CS; Wight N; Crosson LM; White SJ; Strenge RM, 2014. Validation of a quantitative PCR assay for detection and quantification of 'Candidatus Xenohaliotis californiensis'. Diseases of Aquatic Organisms, 108(3):251-259. http://www.int-res.com/abstracts/dao/v108/n3/p251-259/

García-Esquivel Z; Cáceres-Martínez J; Montes-Magallón S, 2011. Oxytetracycline water bath treatment of juvenile blue abalone Haliotis fulgens (Philippi 1845) affected by the withering syndrome. Ciencias Marinas, 37(2):191-200.

Gardner GR; Harshbarger JC; Lake JL; Sawyer TK; Price KL; Stephenson MD; Haaker PL; Togstad HA, 1995. Association of prokaryotes with symptomatic appearance of withering syndrome in black abalone Haliotis cracherodii. Journal of Invertebrate Pathology, 66(2):111-120.

González RC; Brokordt K; Lohrmann KB, 2012. Physiological performance of juvenile Haliotis rufescens and Haliotis discus hannai abalone exposed to the withering syndrome agent. Journal of Invertebrate Pathology, 111(1):20-26. http://www.sciencedirect.com/science/article/pii/S0022201112001401

IUCN, 2014. The IUCN Red List of Threatened Species. http://www.iucnredlist.org

Kiryu I; Kurita J; Yuasa K; Nishioka T; Shimahara Y; Kamaishi T; Ototake M; Oseko N; Tange N; Inoue M; Yatabe T; Friedman CS, 2013. First detection of Candidatus Xenohaliotis californiensis, the causative agent of withering syndrome, in Japanese black abalone Haliotis discus discus in Japan. Gyobyo Kenkyu = Fish Pathology, 48(2):35-41. https://www.jstage.jst.go.jp/article/jsfp/48/2/48_35/_article

Kismohandaka G; Friedman CS; Roberts W; Hedrick RP; Crosby MP, 1993. Investigation of physiological parameters of black abalone with withering syndrome. Journal of Shellfish Research, 12:131-132.

Moore JD; Juhasz CI; Robbins TT; Vilchis LI, 2009. Green abalone, Haliotis fulgens infected with the agent of withering syndrome do not express disease signs under a temperature regime permissive for red abalone, Haliotis rufescens. Marine Biology, 156(11):2325-2330. http://springerlink.metapress.com/content/h14550h3531g4877/fulltext.html

Moore JD; Marshman BC; Chun CSY, 2011. Health and survival of red abalone Haliotis rufescens from San Miguel Island, California, USA, in a laboratory simulation of La Niña and El Niño conditions. Journal of Aquatic Animal Health, 23(2):78-84. http://www.informaworld.com/smpp/content~db=all~content=a937258246~frm=titlelink

Moore JD; Robbins TT; Friedman CS, 2000. Withering syndrome in farmed red abalone Haliotis rufescens: thermal induction and association with a gastrointestinal rickettsiales-like prokaryote. Journal of Aquatic Animal Health, 12(1):26-34.

Murray RG; Schleifer KH, 1994. Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. International Journal of Systematic Bacteriology, 44(1):174-176.

Murray RG; Stackebrandt E, 1995. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. International Journal of Systematic Bacteriology, 45(1):186-187.

National Marine Fisheries Service, 2008. White Abalone Recovery Plan (Haliotis sorenseni). Long Beach, California, USA: National Marine Fisheries Service.

National Marine Fisheries Service, 2009. 2009 NMFS West Coast workshop on abalone species of concern, 1 September 2009. Seattle, Washington, USA and Long Beach, California, USA: National Marine Fisheries Service, 25 pp. http://www.nmfs.noaa.gov/pr/pdfs/species/abalone_workshop_soc2009.pdf

National Marine Fisheries Service, 2015. Endangered and Threatened Marine Species. Silver Spring, Maryland, USA: National Marine Fisheries Service. http://www.nmfs.noaa.gov/pr/species/esa/

National Marine Fisheries Service, 2015. Proactive Conservation Program: Species of Concern. Silver Spring, Maryland, USA: National Marine Fisheries Service. http://www.nmfs.noaa.gov/pr/species/concern/

OIE (World Organisation for Animal Health), 2012. Infection with Xenohaliotis californiensis. In: Manual of Diagnostic Tests for Aquatic Animals. Paris, France: World Organisation for Animal Health (OIE), 511-523. [Chapter 2.4.7.] http://www.oie.int/fileadmin/Home/eng/Health_standards/aahm/current/2.4.07_X_CALIF.pdf

Raimondi PT; Wilson CM; Ambrose RF; Engel JM; Minchinton TE, 2002. El Niño and the continued declines of black abalone along the coast of California. Marine Ecology Progress Series, 242:143-152.

Rosenblum ES; Juhasz CI; Friedman CS; Robbins TT; Craigmill A; Tjeerdema RS; Moore JD, 2008. Oxytetracycline as a treatment for abalone withering syndrome, Part II: Efficacy, pharmacokinetics, and long term resistance to re-infection at elevated sea water temperatures. Aquaculture, 277:138-148.

Vilchis LI; Tegner MJ; Moore JD; Friedman CS; Riser KL; Robbins TT; Dayton PK, 2005. Ocean warming effects on growth, reproduction, and survivorship of southern California abalone. Ecological Applications, 15:469-480.

Wetchateng T; Friedman CS; Wight NA; Lee PeiYu; Teng PingHua; Sriurairattana S; Wongprasert K; Withyachumnarnkul B, 2010. Withering syndrome in the abalone Haliotis diversicolor supertexta. Diseases of Aquatic Organisms, 90(1):69-76.

Organizations

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World: OIE (World Organisation for Animal Health), 12, rue de Prony, 75017 Paris, France, http://www.oie.int/

USA: OIE Reference Laboratory for infection with "Candidatus Xenohaliotis californiensis", University of Washington, School of Aquatic & Fishery Sciences, Box 355020, Seattle, WA 98195-5020, http://fish.washington.edu/people/friedman/

Contributors

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27/03/2015 Original text by:

Chris A. Whitehouse, U.S. Army Medical Research Institute of Infectious Diseases, 1425 Porter Street, Fort Detrick, Maryland 21702, USA

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