- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Plant Type
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Biology and Ecology
- Water Tolerances
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Impact Summary
- Economic Impact
- Environmental Impact
- Risk and Impact Factors
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Pseudochattonella verruculosa (Y. Hara et Chihara) Tanabe-Hosoi, Honda, Fukuya, Inagaki & Sako, 2007
Other Scientific Names
- Chattonella verruculosa Y. Hara et Chihara in Hara, Doi et Chihara, 1994
- Verrucophora verruculosa (Y. Hara et Chihara) Eikrem 2007
Local Common Names
- Japan: "burr-shaped" Chattonella
Summary of InvasivenessTop of page
Over recent decades P. verruculosa has not only increased in abundance in coastal waters of Japan, but has been found in tidal estuaries and lagoons on the eastern coast of the United States, and off the coasts of Germany and New Zealand. Its sibling species Pseudochattonella farcimen, although of uncertain geographic origin, has bloomed recurrently in Scandinavian waters since identification in 1998. The species are therefore showing invasive traits in disjunct geographical regions with apparent potential to spread more widely in temperate inshore waters.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Plantae
- Phylum: Heterokontophyta
- Class: Dictyochophyceae
- Order: Florenciellales
- Genus: Pseudochattonella
- Species: Pseudochattonella verruculosa
Notes on Taxonomy and NomenclatureTop of page
The name Chattonella verruculosa, along with three other Chattonella species, was first published as a nomen nudum in the book “Red tide organisms in Japan” (Fukuyo et al., 1990). The four species were subsequently validly published in Hara et al. (1994). In 2007 Chattonella verruculosa was independently renamed as Pseudochattonella verruculosa by Hosoi-Tanabe et al. (2007) and as Verrucophora verruculosa by Edvardsen et al. (2007). The first of these names, Pseudochattonella verruculosa, has priority.
DescriptionTop of page
Cells 12-45 µm in diameter, nearly globose. Two unequal flagellae emerge from the anterior end of the cell, the longer directed anteriorly and undulating during swimming, the shorter trailing. No osmiophilic particles present in the cytoplasm beneath the cell surface. Several warts of large mucocysts, containing bullet-shaped inclusions in the outer half, distributed randomly around the cell periphery and these eject in response to slight changes in environmental conditions; verrucose protrusions of mucocyst heads visible by light microscopy. Discoid chloroplasts numerous, situated mainly in the ectoplasm; chloroplasts pale-yellow to yellow-brown, relatively small, 2-3 µm long and 1-2.5 µm wide, each with a single embedded pyrenoid. Pyrenoid matrix invaded by a single tubular intrusion originating in the periplastidal space. Spherical nucleus central in the cell. Comparatively large mitochondria located in the endoplasm; smaller ones in the ectoplasm. Contractile vacuoles and eyespots absent (Hara et al., 1994; Hallegraeff and Hara, 2003; Hosoi-Tanabe et al., 2007).
Plant TypeTop of page Aquatic
DistributionTop of page
Type locality: Harima-nada, Tokushima, Japan.
Distribution TableTop of page
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/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Atlantic, Northeast||Localised||2000||Introduced||Riisberg and Edvardsen, 2008|
|Atlantic, Northwest||Localised||2008||Introduced||Marshall et al., 2005; Marshall et al., 2005|
|Atlantic, Western Central||Localised||2003||Introduced||Hayes and Lewitus, 2003|
|Pacific, Northwest||Present||Native||Hosoi-Tanabe et al., 2007|
|Pacific, Southwest||Present||2003||Introduced||Bowers et al., 2006|
|Japan||Present||Native||Hosoi-Tanabe et al., 2007|
|-Kyushu||Present||Native||Hara et al., 1994|
|USA||Present||Present based on regional distribution.|
|-South Carolina||Present||Introduced||Hayes and Lewitus, 2003||Brackish lagoons|
|-Virginia||Present||Introduced||Marshall, 2003; Marshall et al., 2005; Chesapeake Bay Program, 2007; Marshall et al., 2009||Noted as rare in Chesapeake Bay and also its tidal tributaries|
|Germany||Localised||2000||Introduced||Riisberg and Edvardsen, 2008|
|New Zealand||Present||Introduced||Bowers et al., 2006; Riisberg and Edvardsen, 2008|
History of Introduction and SpreadTop of page
In the coastal waters of Japan, the abundance of Pseudochattonella verruculosa appears to have increased over recent decades. P. verruculosa, along with Heterocapsa circularisquama (Dinophyceae), have been said to have caused ‘novel red tides’ in the coastal waters of western Japan because they have only been identified there since the late 1980s (Yamaguchi et al., 1997). Since that time they have replaced red tide species such as Chattonella antiqua, Chattonella marina and Heterosigma akashiwo) and, leading up to 1997, became the predominant causative organism of harmful red tides (Yamaguchi et al., 1997).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Atlantic, Northeast||Pacific, Northwest||2000||Hitchhiker (pathway cause)||Riisberg and Edvardsen (2008)|
|Atlantic, Northwest||Pacific, Northwest||1996||Hitchhiker (pathway cause)||Marshall et al. (2005)|
|Atlantic, Western Central||Pacific, Northwest||2002||Hitchhiker (pathway cause)||Hayes and Lewitus (2003)|
|Pacific, Southwest||Pacific, Northwest||2003||Hitchhiker (pathway cause)||Riisberg and Edvardsen (2008)|
Risk of IntroductionTop of page
The increasing distribution and abundance of Pseudochattonella species in cool temperate waters over the past decade suggests that this species has been introduced to new regions, and could therefore be introduced elsewhere. Ships’ ballast water has been suggested as a possible vector.
HabitatTop of page
In the Seto Inland Sea of Japan, P. verruculosa is one of the species found in red tide blooms that occur frequently from spring to autumn (Hara et al., 1994). In the eastern USA, P. verruculosa has been found in Chesapeake Bay and its tidal tributaries, and in brackish lagoons in South Carolina (Hayes and Lewitus, 2003; Marshall et al., 2005a,b).
Habitat ListTop of page
|Lagoons||Present, no further details||Harmful (pest or invasive)|
|Inshore marine||Present, no further details||Harmful (pest or invasive)|
Biology and EcologyTop of page
Nuclear 18S and plastid 16S sequence data supported the movement of “Chattonella” verruculosa from the Raphidophycae to the Dictyophyceae (Bowers et al., 2006). Cultures from Japan and New Zealand shared 99% sequence similarity in the 18S region and 100% with respect to the plastid 16S locus (Bowers et al., 2006).
ClimateTop of page
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
Water TolerancesTop of page
|Parameter||Minimum Value||Maximum Value||Typical Value||Status||Life Stage||Notes|
|Salinity (part per thousand)||25||Optimum||15-35 tolerated|
|Water temperature (ºC temperature)||15||Optimum||12-22 tolerated|
Notes on Natural EnemiesTop of page
Means of Movement and DispersalTop of page
Pathway VectorsTop of page
Impact SummaryTop of page
Economic ImpactTop of page
Red tides in the Japan Inland Sea have significant impact on the fishing industry. Species of the genus Chattonella (but encompassing P. verruculosa) are major causative organisms and, in 1987, an estimated 2.4 billion yen was lost by the aquaculture industry in the Inland Sea due to red tides caused by Chattonella antiqua (Murayama-Kayano et al., 1998). Blooms of P. verruculosa have been associated with the mortality of fish, including yellowtail, amberjack, and red and black sea bream, in early summer and winter (Yamamoto and Tanaka, 1990; Baba et al., 1995; Yamaguchi et al., 1997). In Chesapeake Bay the presence of Pseudochattonella has not been associated with annual toxic events (Marshall et al., 2005a).
Environmental ImpactTop of page
As discussed above, P. verruculosa is known to have caused mortalities in wild fish populations.
Risk and Impact FactorsTop of page Invasiveness
- Abundant in its native range
- Fast growing
- Has high reproductive potential
- Reproduces asexually
- Damaged ecosystem services
- Negatively impacts livelihoods
- Negatively impacts aquaculture/fisheries
- Threat to/ loss of native species
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
Similarities to Other Species/ConditionsTop of page
The two species of Pseudochattonella share with species of Chattonella the presence of two unequal flagella inserted in a shallow depression near the anterior end of the cell (Hara, 1990; Hara et al., 1994; Hallegraeff and Hara 1995; 2003; Hosoi-Tanabe et al., 2007) and the absence of a contractile vacuole and eyespot (Hara et al., 1994; Hosoi-Tanabe et al., 2007). However, Pseudochattonella species differ to Chattonella species in having: mucocysts with bullet-shaped inclusions and verrucose protrusions; an absence of osmiophilic particles in the peripheral cytoplasm; generally smaller cell size (12-45 µm compared to =30 µm); longitudinal axes of the chloroplasts not oriented to the centre of the cell; and an unclear boundary between the endoplasm and ectoplasm (Hara, 1990; Hara et al., 1994; Hallegraeff and Hara, 1995; 2003; Hosoi-Tanabe et al., 2007).
Prevention and ControlTop of page
Gaps in Knowledge/Research NeedsTop of page
Knowledge on the origin and distribution of both Pseudochattonella species remains uncertain, as are complete details on their life history and environmental requirements, and the mechanism of ichthyotoxicity.
ReferencesTop of page
Akizuki Y; Kitakado I; Sasaki M, 1981. Globular type of flagellates occurring at the early stage of Hornellia blooms. Report of previous conjecture and researches of red tides in 1979. Seto Inland Sea Block.
Aure J; Danielssen DS; Skogen M; Svendsen E; Soiland H; Pettersson L, 2001. Environmental conditions during the Chattonella bloom in the North Sea and Skagerrak in May 1998. In: Harmful Algal Blooms 2000 [ed. by Hallegraeff GM, Bolch CJS, Blackburn SI, Lewis R] Paris, : Intergovernmental Oceanographic Commission of UNESCO, 82-85.
Bowers HA; Tomas C; Tengs T; Kempton JW; Lewitus AJ; Oldach DW, 2006. Raphidophyceae [Chadefaud ex Silva] systematic and rapid identification: sequence analysis and real-time PCR assays. Journal of Phycology, 42:1333-1348.
CICCM, 2009. Cawthron Institute Culture Collection of Micro-algae (CICCM) - Catalogue of strains: May 2009. Website edition. http://www.cawthron.org.nz/aquatic-biotechnologies/downloads/cat-web-may-2009.pdf
Edvardsen B; Eikrem W; Shalchian-Tabrizi K; Riisberg I; Johnson G; Naustvall L; Throndsen J, 2007. Verrucophora farcimen gen. et sp. nov. (Dictyochophyceae, Heterokonta) - a bloom-forming ichthyotoxic flagellate from the Skagerrak, Norway. Journal of Phycology, 43:1054-1070.
Hallegraeff GM; Hara Y, 2003. Taxonomy of harmful marine raphidophytes. Second edition. In: Manual on Harmful Marine Microalgae [ed. by Hallegraeff GM, Anderson DM, Cembella A] Paris, : UNESCO, 511-522.
Hara Y, 1990. Chattonella verruculosa Y. Hara et Chihara. In: Red Tide Organisms in Japan - An Illustrated Taxonomic Guide [ed. by Fukuyo Y, Takano H, Chihara M, Matsuoka K] Tokyo, : Uchida Rokakuho, 342-343.
Hosoi-Tanabe S; Honda D; Fukaya S; Otake I; Inagaki Y; Sako Y, 2007. Proposal of Pseudochattonella verruculosa gen. nov., comb. nov. (Dictyochophyceae) for a former raphidophycean alga Chattonella verruculosa, based on 18S rDNA phylogeny and ultrastructural characteristics. Phycological Research, 55:185-192.
Marshall HG; Egerton TA; Burchardt L; Cerbin S; Kokocinski MJ, 2005. Long term monitoring results of harmful algal populations in Chesapeake Bay and its major tributaries in Virginia, USA. Oceanological and Hydrological Studies, 34(Suppl. 3):35-41.
Marshall HG; Lane MF; Nesius KK; Burchardt L, 2009. Assessment and significance of phytoplankton species composition within Chesapeake Bay and Virginia tributaries through long-term monitoring program. Environmental Monitoring and Assessment, 150:143-155.
Murayama-Kayano E; Yoshimatsu S; Kayano T; Nishio T; Ueda H; Nagamune T, 1998. Application of the random amplified polymorphic DNA (RAPD) technique to distinguishing species of the red tide phytoplankton Chattonella (Raphydophyceae). Journal of Fermentation and Bioengineering, 85:343-345.
Naustvoll L-J, 2006. NOBANIS Invasive Alien Species Fact Sheet on Chattonella aff. Verruculosa. Online Database of the North European and Baltic Network on Invasive Alien Species (NOBANIS). http://www.nobanis.org
Riisberg I, 2008. Genetic characterization of the marine ichthyotoxic flagellate Pseudochattonella farcimen (Heterokonta) and phylogenetic relationships among heterokonts. Oslo, Norway: University of Oslo. http://www.duo.uio.no/sok/work.html?WORKID=81197
Riisberg I; Edvardsen B, 2008. Genetic variation in bloom-forming ichthyotoxic Pseudochattonella species (Dictyochophyceae, Heterokonta) using nuclear, mitochondrial and plastid DNA sequence data. European Journal of Phycology, 43:413-422.
Yamaguchi M; Itakura S; Nagasaki K; Matsuyama Y; Uchida T; Imai I, 1997. Effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). Journal of Plankton Research, 19:1167-1174.
ContributorsTop of page
02/08/09 Original text by:
John Lewis, ES Link Services Pty Ltd Queensberry Place, North Melbourne, Vic. 3051, Australia
Distribution MapsTop of page
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