Hemigrapsus takanoi (brush-clawed shore crab)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Habitat List
- Biology and Ecology
- Latitude/Altitude Ranges
- Water Tolerances
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Impact Summary
- Environmental Impact
- Risk and Impact Factors
- Detection and Inspection
- 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
- Hemigrapsus takanoi Asakura & Watanabe, 2005
Preferred Common Name
- brush-clawed shore crab
Other Scientific Names
- Hemigrapsus tanakoi Asakura & Watanabe, 2005 (misspelling)
International Common Names
- English: japanese crab; pencil crab
- French: crabe à pinceaux; crabe japonaise
Local Common Names
- Netherlands: penseelkrab; penseelkrabbetje
Summary of InvasivenessTop of page
Hemigrapsus takanoi is a small crab native to the rocky coasts of northwest Pacific regions (Asakura and Watanabe, 2005). H. takanoi belongs to the family Grapsoidea, which, along with the Portunoidea and Majiodia, have a high number of invasive species. It was first recorded in Europe in 1994. It was recorded in France as H. penicillatus, a sibling related species of H. takanoi, so previous records of H. penicillatus in Europe have now been identified as records of H. takanoi (Asakura et al., 2008). Possible vectors of introduction in Europe include accidental transport in hull fouling, ballast water and oyster shipments. It is considered invasive because it outcompetes the native European green crab Carcinus maenas in Europe in rocky shore habitats, particularly where it occurs in high densities. H. takanoi is now well established in Europe and is present along approximately 1,000 km of coastline, from Spain to the Wadden Sea from The Netherlands to Denmark to Lower Saxony in Germany to Sweden, and is common at many sites within this area (Gittenberger et al., 2010).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Crustacea
- Class: Malacostraca
- Subclass: Eumalacostraca
- Order: Decapoda
- Suborder: Pleocyemata
- Family: Varunidae
- Genus: Hemigrapsus
- Species: Hemigrapsus takanoi
Notes on Taxonomy and NomenclatureTop of page
Hemigrapsus takanoi is a small crab of the family Varunidae (formerly classified as Grapsidae). Recently, Asakura and Watanabe (2005) described Hemigrapsus takanoi as a sibling species of the most common Japanese intertidal grapsid crab, Hemigrapsus penicillatus De Haan (1835). Previously, the name Hemigrapsus penicillatus was used to cover animals that are now known to represent two distinct species.
In 1997 two forms were described in populations of H. penicillatus (Takano et al., 1997) and recognized as sibling species, with clear differentiating characteristics between the two (Akiwa, 2002; Mingkid et al., 2006a). The validity of this distinction was questioned by Sakai (2007) and rebutted by Asakura et al. (2008). The international scientific community seems largely to retain them as new species (Ng et al., 2008).
DescriptionTop of page
H. takanoi is a small crab: the cephalothorax regularly reaches 2.5 cm in its greatest dimension, with larger specimens hardly exceeding 3 cm; it has three spines. The general form of the shell is approximately square, slightly wider than long (ratio length/width is between 1.10 and 1.20). Dorsally, the colour still appears quite dark, greyish, greenish or brown; the walking legs, fairly broad and flattened, are usually marked with darker bands, more or less distinct in different individuals. The outer edge of the clamp of the male has a dense tuft of yellow bristles (known as setae) on their chelae (Asakura and Watanabe, 2005).
DistributionTop of page
H. takanoi has only recently been distinguished from Hemigrapsus penicillatus; the true extent of its native geographical distribution is therefore not yet precisely known. The distribution of this species in Japan is so far confirmed as Honshu, Shikoku, and Kyushu. This species has also been found in Ishikari Bay, Hokkaido (Takano et al., 1999). H. penicillatus has previously been recorded in the north of Sakhalin island (Russia), in the south of Hong Kong, China, the Korea Peninsula, Okinawa island (south Japan) and Taiwan (Sakai, 1976). Its distribution in these areas remains largely unconfirmed, although recent studies have confirmed the species presence in Korean waters (Lee et al., 2013). In addition, there is a record of H. penicillatus from Hawaii by Edmondson (1959), but the supporting material is apparently lost, so its identification cannot be confirmed (Asakura and Watanabe, 2005).
When the first species of Hemigrapsus spp. was introduced to European coasts ca. 1995, Hemigrapsus takanoi (Asakura and Watanabe, 2005) had not yet been described, so the crab was named Hemigrapsus penicillatus De Haan (1835) (Noël et al., 1997). In subsequent years, this name was used many times for European records (Türkay, 2012). However, previous records of H. penicillatus in Europe were actually of H. takanoi (Asakura et al., 2008) and the genetic sequence H. takanoi collected in Japan showed a high degree of homology with that reported for specimens collected in Europe (Yamasaki et al., 2011).
Its non-native distribution is in the North Sea, Wadden Sea and Northeast Atlantic, where it is now established (Dauvin et al., 2009; Gollasch et al., 2009; Gittenberger et al., 2010; Landschoff et al., 2013). It was first documented in France in 1993 and is now present in Spain, Netherlands, Belgium and Germany (Noël et al., 1997 and references therein). The first confirmed occurance in Sweden was in 2016, of a male with a 15 mm carapace width at 58.248352°N 11.439560°E (Artportalen, 2016; University of Gothenburg, 2016).
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.Last updated: 17 Dec 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||Native||H. penicillatus, is present but H. takanoi is unconfirmed.|
|Japan||Present||Present based on regional distribution.|
|France||Present||Introduced||1993||Invasive||First record in Europe|
|Russia||Present||Present based on regional distribution.|
|-Russian Far East||Present||Native||H. penicillatus is present but H. takanoi is unconfirmed. Sakhalin island|
|Sweden||Present, Few occurrences||Introduced||Single male, 15 mm wide carapace, 58.248352°N 11.439560°E. Only known occurrance as of August 2016|
|-Hawaii||Absent, Unconfirmed presence record(s)||Recorded as H. penicillatus but presence of H. takanoi is unconfirmed.|
|Atlantic - Northeast||Present||Introduced||Invasive||Ranges from Northeast Spain to Germany|
|Pacific - Northwest||Present, Widespread||Native||Northern Japan, some regions of Russia’s Pacific coast, Korea, China, Hong Kong and Taiwan|
History of Introduction and SpreadTop of page
H. takanoi Asakura and Watanabe (2005) was initially identified as H. penicillatus de Haan (1835) and was reported form a non-native area for the first time in La Rochelle, on the Atlantic coast of France, in 1994. It is thought to have arrived in 1993 (Noël et al., 1997) and in the same year six juveniles were detected on the hull fouling of a Japanese vessel in Bremerhaven (Germany). The ship was known to have passed the French coast so it is likely that this vessel could have been a potential vector for introduction into the French coast (Gollasch, 1999).
By 1997, its range in Europe extended around the Bay of Biscay, from Fromentine in France to Laredo in Spain, and it had become locally abundant, covering a coastline of 700 kilometres (Noël, et al., 1997). By 1999 it had reached Le Havre on the English Channel (Dauvin et al., 2009), where it formed abundant populations of juveniles. It reached the Eastern Scheldt (Netherlands) in 1999 (Breton et al., 2002) and Oosterschelde tidal bay and the Westerschelde estuary (The Netherlands) in the year 2000, but probably arrived earlier in 1999, and could be found throughout the Dutch delta (D’udekem D’acoz and Faasse, 2002; Wolff, 2005). It was also reported on the Belgian coast in the Westerschelde near Baalhoek in 2003 (Dumoulin, 2004) and, by 2005, it had reached the French Opal Coast at the entrance to the North Sea (Dauvin et al., 2009).
By the end of 2007, the population of the Bay of Biscay had spread to Brittany, reaching Lorient harbour (Noël and Gruet, 2008). In the English Channel and the North Sea, H. takanoi is present in Bay of Seine (Saint-Vaast-la-Hougue, Normandy, and Le Havre), and from the Opal Coast (Dauvin and Delhay, 2011) through to the Belgian coast in Zeeschelde estuary (Soors et al., 2010) to the tidal zone near Norddeich along the German coast in Bremerhaven (Lower Saxony) (Obert et al., 2007). Recently, it has been reported in Sweden (NORSAS, 2012). The species has not yet reached the British coast (Dauvin et al., 2009).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|France||Japan||1993||Hitchhiker (pathway cause)||Yes||Noël et al. (1997)||Ballast water/hull fouling|
|Germany||Netherlands||2007||Yes||Obert et al. (2007)|
|Netherlands||France||1999-2000||Yes||Breton et al. (2002); D'udekem and D'acoz Faasse (2002); Wolff (2005)|
|Spain||France||1997||Yes||Noël et al. (1997)|
HabitatTop of page
The species predominantly inhabits intertidal areas of mudflats, estuaries and lagoons with sufficient shelter opportunities, typically among rocks and boulders, but can also be found in soft sediment and occasionally in subtidal regions (Asakura and Watanabe, 2005). H. takanoi is found in mid to low intertidal areas, occasionally sub-tidal (to 20 m), among rocks, cobbles and soft sediment (Brockerhoff and McLay, 2011).
It is generally found in more wave-sheltered areas than H. penicillatus, although the two species often occur sympatrically (Asakura and Watanabe, 2005). Mingkid et al. (2006a) examined the geographical distribution patterns of the two species along the coast of Tokyo Bay and found that H. takanoi was predominant in the inner part of the bay, whereas H. penicillatus was collected mainly along the middle to outer coasts of the bay.
In its introduced area (France), it is found in sheltered areas of the mid-littoral (Noël et al., 1997; Dauvin et al., 2009) and has a preference for low hydrodynamic muddy habitats (Dauvin, 2009). H. takanoi occupies the same habitat as H. sanguineus, but the latter occurrs in large numbers on the rocky shore of the open sea, while H. takanoi is abundant in sheltered harbours (Dauvin et al., 2009). Additionally, H. takanoi thrives in the new habitat provided by the expanding oyster reefs of Crassostrea gigas (Pacific oyster) in the Dutch delta waters (Brink van den et al., 2012a).
Habitat ListTop of page
|Littoral||Coastal areas||Principal habitat||Natural|
|Littoral||Intertidal zone||Principal habitat||Natural|
|Littoral||Salt marshes||Secondary/tolerated habitat||Natural|
|Marine||Benthic zone||Secondary/tolerated habitat||Natural|
Biology and EcologyTop of page
H. takanoi can be distinguished from its the sibling species H. penicillatus by genetics, according to work by Yamasaki et al. (2011). The genetic sequence of H. takanoi specimens collected in Japan showed a high degree of homology with the genetic sequence reported for specimens collected in Europe. Hybridization between H. takanoi and its sibling species H. penicillatus in its native range has not been recorded.
Although there is limited information about the life history of H. takanoi, and although larval phases have not yet been described (Yamasaki et al., 2011), the similarities between the species and the more commonly documented H. penicillatus suggest that their life histories are probably similar. Assuming this, H. takanoi females became ovigerous at 1 year old and the minimum body size of ovigerous individuals is about 6.4 mm CW. The breeding season is from spring to autumn. The incubation period shows little variation at a given water temperature, but shortens with rising temperature (Fukui, 1988).
Mean number of broods is between 5 to 6 per year and the number of eggs per brood is 56,000; the number is related to the female carapace width. H. penicillatus has approximately three times as many eggs per body size as H. sanguineus (Fukui, 1988). The size of the eggs is about 0.2814 mm (Akiwa, 2002). Once hatched, larvae are planktonic for up to one month before becoming juvenile crabs (EOEEA, 2012). Growth and maturation are rapid (Pillay and Ono, 1978), and crabs reach maturity after several months (Brink van den et al., 2012b).
High salinities are required for successful larval development of H. takanoi. In an experiment with water temperature of about 24ºC, the development of H. takanoi larvae, from hatching to the first juvenile stage, occurred only in high salinities (from 25 to 35 per mil). At very low salinities only a few larvae metamorphosed to the second zoeal stage and no larvae developed further than the megalopa stage (Mingkid et al., 2006b).
The duration of brood and larval development is highly dependent on water temperature.
Physiology and Phenology
The larvae are planktonic for up to one month. During this period, before the larvae develop into juvenile crabs, they may be transported considerable distances by currents. Larvae may also be transported in ships’ ballast water before being released into harbours or bays (Mingkid et al., 2006a). The estimated growth rate of immature crabs is similar between males and females. After maturity, however, the estimated growth rate is apparently lower in females than in males (Fukui, 1988).
H. takanoi expends increased metabolic effort to tolerate abrupt reductions in salinity compared to changes towards increasingly brackish water or seawater (Shinji et al., 2009).
As with H. penicillatus, H. takanoi would be expected to show territorial behaviour among individuals with the same size of caparace (Kurihara and Okamoto, 1987).
Population Size and Density
In France it is found reaching high densities of up to 50-60 individuals/m2 (Dauvin et al., 2009). It has reached almost 80 m−2 on the Dutch coast (Brink van den, 2012a).
In the northeast Atlantic H. takanoi (formerly presumed to be H. penicillatus) occupies the same habitat as the native crab Carcinus maenas and the exotic crab H. sanguineus (Breton et al., 2002). H. sanguineus occurrs in large numbers on the rocky shore of the open sea, while H. takanoi is abundant in sheltered harbours (Dauvin et al., 2009). In its non-native range it is associated with mussels or oysters, such as the Japanese oyster Crassostrea gigas (Dumoulin, 2004).
In its native range H. takanoi can be commonly found in bays and estuaries, including areas where salinities and temperatures fluctuate highly (7-35 per mil and 12.5-20ºC, respectively) (Mingkid et al., 2006a). The adults of H. takanoi have a wide tolerance range of water salinity, thereby enhancing its ability to colonize coastal habitats with high fluctuations in salinity (Shinji et al., 2009).
ClimateTop of page
|C - Temperate/Mesothermal climate||Preferred||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
|D - Continental/Microthermal climate||Preferred||Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Water TolerancesTop of page
|Parameter||Minimum Value||Maximum Value||Typical Value||Status||Life Stage||Notes|
|Salinity (part per thousand)||7||35||Optimum|
|Water temperature (ºC temperature)||12.5||20||Optimum|
Natural enemiesTop of page
Notes on Natural EnemiesTop of page
Potential predators would include some bottom-feeding fishes; birds and other crabs have also been recorded as preying upon grapsid crabs occasionally (Fukui, 1988). In its non-native range birds such as herons and sea-gulls are predators of H. takanoi (Noel et al., 1997).
Parasites of two brachyurans of the varunid genus Hemigrapsus are known from their native habitats, but, except for an undescribed larval nematode, none have been found in those examined from non-native locations. These parasites include the metacercariae of eight species of Microphallid trematode, the rhizocephalan barnacles Polyascus polygenea, Sacculina nigra and Sacculina senta, and the obligate gut-inhabiting mesomycetozoan Enteromyces callianassae (potential parasite) (McDermott, 2011).
Means of Movement and DispersalTop of page
Natural Dispersal (Non-Biotic)
Natural dispersal following initial introductions occurs when pelagic larvae are dispersed by currents. Dauvin and Dufossé (2011) proposed that the spread of Hemigrapsus sp. may be predicted by taking account of the current direction along the French coast of the English channel.
Vector Transmission (Biotic)
No spread on live animal vectors that are not transported commercially is recorded.
H. takanoi has been introduced to European waters in its larval form; hull fouling communities (Gollasch, 1999) and ballast water (Gollasch et al., 2009) are the principal vectors. Landschoff et al. (2013) describe the rapid spread of this species in the Wadden Sea and emphasise that it is the crabs ability to cling to surfaces and hide in narrow crevices that allows it to travel widely on ship trunks, in anchor boxes, on ropes, or inside ballast water systems. Invasion in the Wadden Sea is also likely to have been made possible by the increased use of hard coastal defences, changing the habitat from a predominately soft environment to one suitable for rocky shore species (Landschoff et al., 2013).
It has been suggested that professional oyster transportation could be responsible for the introduction of H. takanoi along some parts of the French coast (Dauvin and Delhay, 2011; Noel, 2011) and The Netherlands (Nijland, 2000; Faasse et al., 2002).
There are no recorded cases of intentional introduction of H. takanoi.
Pathway CausesTop of page
Pathway VectorsTop of page
Impact SummaryTop of page
Environmental ImpactTop of page
Impact on Biodiverisity
H. takanoi outcompetes the native European green crab Carcinus maenas in Europe, particularly in rocky shore habitats, where it occurs in high densities (Noel et al, 1997; Gollasch, 1999; Dauvin et al. 2009). H. takanoi completely dominated the intertidal hard substrate environments, on which juvenile C. maenas depend, by expelling C. maenas from their shelters. On soft sediment substrate, where H. takanoi densities are low, the native and exotic shore crab species are presently more or less equally abundant (Brink van den et al., 2012a). Both species may compete for food, as stomach content analysis has shown that the optimal-sized prey for Carcinus spp. is similar to that of H. takanoi in the latter’s native range (Wataru et al., 2011).
Its recent invasion and establishment in the coastal and delta waters in the Netherlands is thought to impact especially upon newly settled shellfish, such as mussel and oyster splat through predation (Brink van den, 2013).
Risk and Impact FactorsTop of page
- Proved invasive outside its native range
- Abundant in its native range
- Highly adaptable to different environments
- Tolerant of shade
- Capable of securing and ingesting a wide range of food
- Highly mobile locally
- Fast growing
- Has high reproductive potential
- Altered trophic level
- Ecosystem change/ habitat alteration
- Increases vulnerability to invasions
- Modification of natural benthic communities
- Modification of nutrient regime
- Modification of successional patterns
- Monoculture formation
- Negatively impacts aquaculture/fisheries
- Reduced native biodiversity
- Threat to/ loss of native species
- Competition - monopolizing resources
- Competition - shading
- Interaction with other invasive species
- Rapid growth
- 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
Detection and InspectionTop of page
In order to distinguish the sibling species H. penicillatus and H. takanoi without specific taxonomic knowledge, barcode analysis using the 16S rRNA gene and the cytochrome c oxidase subunit 1 gene of the mitochondrial (mt) DNA, identified by Yamasaki et al. (2011), could be used. They found that polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis is highly effective for the distinction of these two species. More detail about the sequence can be found in NCBI (2012).These molecular techniques can also be used to help detect the presence of H. takanoi larvae in ballast water.
Similarities to Other Species/ConditionsTop of page
H. takanoi has a sibling species, H. penicillatus; both species are very similar in morphology. The key character separating both species is the difference in the pigmentation patterns on the ventral face of the abdominal somites: H. penicillatus has dark spots on that surface, which are lacking in H. takanoi, and males of H. penicillatus have a smaller ratio of the diameter of the patch of setae on the chela than H. takanoi (Takano et al., 1997; Asakura and Watanabe, 2005; Mingkid et al., 2006a). By these criteria, 99% of the individuals are clearly separated into the two species (Mingkid et al., 2006a).
Another species similar to H. takanoi is H. sanguineus, which has also established invasive populations in Europe. Breton et al. (2002) and D’udekem d’Acoz (2006) provided descriptions and figures to differentiate both species.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
The management of H. takanoi requires appropriate treatment/exchange of ballast water; removal of hull fouling may limit or prevent its introduction. In the Wadden Sea, a change from using hard structures for sea defences to soft defences could limit further spread of this species (Landschoff et al., 2013).
Early Warning Systems
H. takanoi is included as a species still exotic to Australia by the Australian Emergency Marine Pest Plan (EMPPlan).
On the West Coast of the USA, this species has been identified as a potential invader and ID cards have prepared by the Massachusetts office of Coastal Zone Management to increase public awareness (EOEEA, 2012).
Monitoring and Surveillance (incl. Remote Sensing)
Its high colonization potential suggests that H. takanoi could continue its invasion in European waters. Therefore, a European surveillance network might be necessary to monitor its progression in the north-eastern Atlantic Ocean.
Gaps in Knowledge/Research NeedsTop of page
Research is needed on the environmental impact of H. takanoi. In addition, a management plan to control this species must be developed. Due to the recognition of H. takanoi as a sibling species of H. penicillatus since 2005, it is also necessary to revise the current distribution of the species in its non-native and native range. H. takanoi has the adaptive capabilities to inhabit European coasts, although the detailed physiological and ecological reasons have not been fully studied (Asakura et al., 2008).
ReferencesTop of page
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Dauvin JC; Rius AT; Ruellet T, 2009. Recent expansion of two invasive crabs species Hemigrapsus sanguineus (de Haan, 1835) and H. takanoi Asakura and Watanabe 2005 along the Opal Coast, France. Aquatic Invasions, 4(3):451-465. http://www.aquaticinvasions.ru/2009/AI_2009_4_3_Dauvin_etal.pdf
d'Udekem d'Acoz C, 2006. First record of the Asian shore crab Hemigrapsus sanguineus (De Haan, 1835) in Belgium (Crustacea, Brachyura, Grapsoidea). De Strandvlo, 26(3):74-82.
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Dumoulin E, 2004. Quick range extension of pencil-crab Hemigrapsus penicillatus (de Haan, 1835) along the coasts of the Southern Bight of the North Sea, status of its intrusion in the Westerschelde, and considerations on its ecology and behaviour. De Strandvlo, 24(1):5-35.
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Faasse M; Nijland R; D'Udekem D'Acoz C; Duivenvoorde JM, 2002. Opmars van de penseelkrab Hemigrapsus penicillatus De Haan, 1935 in Nederland. Het Zeepaard, 63(2):41-44.
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Gittenberger A; Rensing M; Stegenga H; Hoeksema BW, 2010. Native and non-native species of hard substrata in the Dutch Wadden Sea. Nederlandse Faunistische Mededelingen, 33:21-75.
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31/01/13 Original text by:
Manuel A Duenas, Consultant, Spain
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