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Datasheet

Procambarus fallax f. virginalis
(Marmorkrebs)

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Datasheet

Procambarus fallax f. virginalis (Marmorkrebs)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Procambarus fallax f. virginalis
  • Preferred Common Name
  • Marmorkrebs
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Crustacea
  •         Class: Malacostraca
  • Summary of Invasiveness
  • The Marmorkrebs is an enigmatic crayfish species of North American origin. It was first discovered in the German pet trade in the mid-1990s and is the only known decapod crustacean that reproduces by parthenogenesis....

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Pictures

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PictureTitleCaptionCopyright
Procambarus fallax f. virginalis or 'Marmorkrebs': dorsal view - the basic color is highly variable, from tan to dark olive-brown.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': dorsal view - the basic color is highly variable, from tan to dark olive-brown.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': dorsal view - the basic color is highly variable, from tan to dark olive-brown.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': dorsal view - the basic color is highly variable, from tan to dark olive-brown.Christoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': dorsal view close-up of anterior rgion and - the basic colour is highly variable, from tan to dark olive-brown.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': dorsal view close-up of anterior rgion and - the basic colour is highly variable, from tan to dark olive-brown.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': dorsal view close-up of anterior rgion and - the basic colour is highly variable, from tan to dark olive-brown.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': dorsal view close-up of anterior rgion and - the basic colour is highly variable, from tan to dark olive-brown.Christoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view.Christoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.Christoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': ventral view - close-up of posterior region.Christoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': lateral view - the basic colour is highly variable, from tan to dark olive-brown.
TitleAdult
CaptionProcambarus fallax f. virginalis or 'Marmorkrebs': lateral view - the basic colour is highly variable, from tan to dark olive-brown.
CopyrightChristoph Chucholl
Procambarus fallax f. virginalis or 'Marmorkrebs': lateral view - the basic colour is highly variable, from tan to dark olive-brown.
AdultProcambarus fallax f. virginalis or 'Marmorkrebs': lateral view - the basic colour is highly variable, from tan to dark olive-brown.Christoph Chucholl

Identity

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Preferred Scientific Name

  • Procambarus fallax f. virginalis Martin et al., 2010

Preferred Common Name

  • Marmorkrebs

Other Scientific Names

  • Procambarus sp.

International Common Names

  • English: marbled crayfish
  • French: écrevisse marbrée

Local Common Names

  • Madagascar: foza orana; orana vahiny
  • Netherlands: marmerkreeft

Summary of Invasiveness

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The Marmorkrebs is an enigmatic crayfish species of North American origin. It was first discovered in the German pet trade in the mid-1990s and is the only known decapod crustacean that reproduces by parthenogenesis. It has circulated in the European pet trade for several years before the first free-living specimens were captured in Europe and Madagascar in 2003. Marmorkrebs became quickly established in Madagascar and invaded eight of the country's 22 regions, assisted by human-mediated dispersal. Many records from Europe are based on the collection of single specimens; however, recent data prove that established populations exist at least in Germany. Parthenogenesis permits a high reproductive potential and one single Marmorkrebs can create a new population. Marmorkrebs are considered as `perfect invaders´ in Madagascar and there is concern that it may negatively impact rice culture and inland fisheries. Marmorkrebs also threaten native crayfish due to competition and transmission of crayfish plague. 

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Crustacea
  •                 Class: Malacostraca
  •                     Subclass: Eumalacostraca
  •                         Order: Decapoda
  •                             Suborder: Reptantia
  •                                 Unknown: Astacoidea
  •                                     Family: Cambaridae
  •                                         Genus: Procambarus
  •                                             Species: Procambarus fallax f. virginalis

Notes on Taxonomy and Nomenclature

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The Marmorkrebs is a parthenogenetic lineage of the `slough crayfish´ [Procambarus fallax (Hagen, 1870); Martin et al., 2010a]. However, scientists have puzzled for almost a decade about its phylogenetic position and status.

Marmorkrebs have been first discovered in the German pet trade in the mid-1990s, when aquarium enthusiasts reported on an all-female crayfish species that reproduces without males (Lukhaup, 2001). Due to its characteristic and conspicuous colour pattern it became quickly known as `Marmorkrebs´ in German, which translates into English as `marbled crayfish´.

Its general appearance and the presence of an annulus ventralis pointed to a species belonging to Cambaridae. Early attempts to identify the enigmatic crayfish by morphological characters have failed, however, because most identification keys for Cambaridae rely strongly on male characteristics. Subsequent genetic studies confirmed that Marmorkrebs belong to the American genus Procambarus and are most closely related to Procambarus alleni and Procambarus fallax (Scholtz et al., 2003; Braband et al., 2006, Souty-Grosset et al., 2006).

Most recently, Martin et al. (2010a) showed by genetic and morphological comparisons that the Marmorkrebs is the parthenogenetic form of Procambarus fallax, and proposed the tentative scientific name Procambarus fallax f. virginalis. Although `forma´ is not approved by the International Code of Zoological Nomenclature (ICZN, 1999), this name is the first scientific designation of the Marmorkrebs and can be used for the time being.

The taxonomic treatment of parthenogenetic lineages that arise from bisexual species is generally problematic and differs with the applied species concept (cf. Wilkins, 2006). Additional data on the origin and ecology of the Marmorkrebs may warrant a further evaluation of its taxonomic status.  

Description

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The Marmorkrebs is a medium sized crayfish with a distinct, appealing marbled colour pattern and small chelae. The total length can be up to 13 cm, but is more often less than 10 cm. There exist only females.

Morphology

The dorsal portion of the carapace is smooth, while the lateral surface is slightly granulated; an acute cervical spine is present at each side and the cephalic section bears small to medium tubercles laterally (Souty-Grosset et al., 2006; Kawai et al., 2009). One pair of postorbital ridges. The areola is open and approximately four times as long as wide (Kawai et al., 2009).

Rostrum with moderately elevated and slightly thickened margins, tapering to a triangle acumen. Rostral shoulders at the base of the acumen either with a small marginal tubercle (in laboratory specimens and specimens from Madagascar) (Souty-Grosset et al., 2006; Kawai et al., 2009) or a prominent spine (in free-living specimens from Germany) (Martin et al., 2010b; Chucholl and Pfeiffer, 2010). Acumen tip slightly rounded (in laboratory specimens ) or with an acute spine (in free-living specimens from Germany). Median carina absent.

The chelae are relatively small, being two times shorter than the carapace length (Kawai et al., 2009). The palm (propodus) is elongated and the movable finger (dactyl) is only slightly longer than the medial (inner) margin of the palm. Dorsal surface of palm weakly granulated; ventral side with fewer punctuations. Medial (inner) margin of the palm with small tubercles (Kawai et al., 2009).

Ventral side with a symmetrical, bell-shaped annulus ventralis (seminal receptacle) with an s-shaped sinus, located between the bases of the 4th and 5th walking leg pairs (Souty-Grosset et al., 2006; Kawai et al., 2009).

Coloration

The marble pattern, from which the common name Marmorkrebs (German for `marbled crayfish´) is derived, is always present and especially prominent on the lateral parts of the carapace. The basic colour of the carapace is usually dark brown to olive, but can vary from tan to reddish brown or blue. An indistinct median light tan stripe extends from the rostrum to the caudal margin of the carapace. On each side of the carapace and pleon is an oblique dark horizontal stripe, flanked ventrally by a light-coloured area (Kawai et al., 2009; Martin et al., 2010a). The chelipeds are mottled with dark tubercles, while the subsequent walking legs are coloured uniformly (ranging from tan to greenish or blue). The ventral side is dirty white to beige coloured, with dark and white tubercles extending to the median ventral surface of the chelae palms.  

A detailed description of the Marmorkrebs is provided by Kawai et al. (2009).

Distribution

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To this day, Marmorkrebs is only known from aquaria and its introduced range - an indigenous population has never been reported. However, it is reasonable to assume that the Marmorkrebs originates from the indigenous range of P. fallax, which comprises southern Georgia and Florida (USA) (Hobbs, 1989).

The first free-living Marmorkrebs was captured from a gravel pit lake near Karlsruhe in southwestern Germany in late 2003 (Marten et al., 2004). In 2005, anecdotal evidence was presented for a population in a sedimentation pond near the city of Braunschweig (Lower Saxony, Germany); however, this has never been verified. Subsequently, single specimens were captured from small brooks near the city of Neu-Ulm (Bavaria) in 2008 (C Chucholl, University of Ulm, Germany, personal communication, 2011) and in Saxony in 2009 (Martin et al., 2010b). The first informal evidence for an established Marmorkrebs population in Germany was published by newspapers in mid-2010 (Privenau, 2010): local media repeatedly reported on Marmorkrebs coming out of an overpopulated small pond in a village near Halle (Saale, Saxony-Anhalt). Shortly after, another research paper evidenced that Marmorkrebs had formed a stable, reproducing population in a small lake near the city of Freiburg (Baden-Württemberg) (Chucholl and Pfeiffer, 2010). The first Marmorkrebs from this population was captured in 2009, but reported observations date back even further. In North-Rhine Westphalia (western Germany), single Marmorkrebs have been found in the Rivers Ruhr and Rhine (LANUV NRW, 2011) and there exist additional records from southwestern and central Germany which are yet unpublished. Chucholl and Pfeiffer (2010) suggested that the published Marmorkrebs records from Germany represent merely the `tip of the iceberg´.

Free-living Marmorkrebs were also found in the Netherlands (Dordrecht) in 2004 (Soes and van Eekelen, 2006; Souty-Grosset et al., 2006), approximately 30 Marmorkrebs were introduced into a small waterbody in 2003 (Souty-Grosset et al., 2006) and were still present there in 2008 (according to http://www.marmorkrebs.org).

In Italy, a single Marmorkrebs was found living in syntopy with a large Procambarus clarkii population in 2008 (Nonnis Marzano et al., 2009).

Up to date, the Marmorkrebs is most widespread and abundant in Madagascar, where it was probably introduced in 2003 in Ambohimangakely (Jones et al., 2009) and is now present in eight of the country's 22 regions (Heimer, 2010). It is primarily distributed in the central high plains around the capital Antananarivo and is well established in the Ikopa and the Ampasimbe River systems (Jones et al., 2009; Kawai et al., 2009; Heimer, 2010). Large numbers of Marmorkrebs were sold in Moramanga (eastern Madagascar) in 2008 and it might be established in the area by now (Jones et al., 2009).

In Japan, one Marmorkrebs was captured from a river in Sapporo City (Hokkaido) in 2006 (Kawai and Takahata, 2010).

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

Asia

JapanPresentPresent based on regional distribution.
-HokkaidoPresent2006IntroducedKawai and Takahata, 2010One Marmorkrebs was captured from a river in Sapporo City

Africa

MadagascarWidespreadIntroduced Invasive Jones et al., 2009; Kawai et al., 2009; Heimer, 2010

North America

USAPresent only in captivity/cultivation20102004Faulkes, 2010Present in the pet trade
-FloridaPresentMartin et al., 2010aProbable indigenous range
-GeorgiaPresentMartin et al., 2010aProbable indigenous range

Europe

AustriaPresent only in captivity/cultivation2005IntroducedC Chucholl, pers. comm.Present in the pet trade
GermanyPresent, few occurrencesIntroducedC Chucholl, pers. comm.; Martin et al., 2010b; Marten et al., 2004; Chucholl and Pfeiffer, 2010; Privenau, 2010
ItalyPresent, few occurrences2008IntroducedNonnis Marzano et al., 2009Single specimen found living in syntopy with P. clarkii
NetherlandsPresent, few occurrences2008Introduced2003Soes and Eekelen, 2006~30 individuals released from an aquarium in 2003; still present there in 2008
UKAbsent, intercepted onlyIntroducedPeay et al., 2010Marmorkrebs were found illegally in the aquarium trade

History of Introduction and Spread

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Without much doubt, all Marmorkrebs introductions worldwide trace back to its first occurrence in the German pet trade in the mid-1990s. The species has circulated in the European pet trade for several years before the first free-living specimens were captured in Germany and the Netherlands. Probably all records of free-living Marmorkrebs in Europe are the result of pet releases (Soes and van Eekelen, 2006; Souty-Grosset et al., 2006; Chucholl and Pfeiffer, 2010) and there is good evidence that Marmorkrebs have been imported from Europe into other continents through personal contacts between aquarium hobbyists and the international pet trade (Faulkes, 2010).

The situation in Madagascar is different: the reason for the initial introduction remains unclear, although there may be a link to a road building project in 2003/2004, which involved foreign contractors (Jones et al., 2009). The first Marmorkrebs have been discovered in a rice paddy near the capital in 2003. Four years later, Marmorkrebs began to appear in markets, where they were sold as cheap source of protein to impoverished locals (Heimer, 2010). Secondary introductions into rice paddies have probably occurred and the species is sold alive along major transport routes (Jones et al., 2009).

Once established, Marmorkrebs may also spread actively. In Germany, single Marmorkrebs were found in the outflow of a colonized lake (M Pfeiffer, March, Germany, personal communication, 2010) and the species was also observed to migrate over land (Privenau, 2010).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Germany 2003-2010 Aquarium trade (pathway cause) ,
Intentional release (pathway cause)
Yes Chucholl and Pfeiffer (2010); Marten et al. (2004) Release of aquarium species
Italy 2007-2008 Aquarium trade (pathway cause) ,
Intentional release (pathway cause)
Nonnis Marzano et al. (2009)
Madagascar Europe 2003 Yes Jones et al. (2009)
Netherlands 2003 Aquarium trade (pathway cause) ,
Intentional release (pathway cause)
Yes Soes and Eekelen (2006) Release of aquarium specimens, probably from Germany
USA Europe 2004 Aquarium trade (pathway cause) No Faulkes (2010) Present in captivity / aquarium trade

Risk of Introduction

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The major pathway for Marmorkrebs introductions is the deliberate release of aquarium specimens (Soes and van Eekelen, 2006; Souty-Grosset et al., 2006; Chucholl and Pfeiffer, 2010). Its appealing coloration, undemanding nature and exceptional reproduction mode makes the Marmorkrebs attractive to aquarium hobbyists. However, parthenogenesis permits a high reproductive potential and Marmorkrebs can overpopulate an aquarium quickly. Aquarium hobbyists are likely to want to offload excess stock, either to other aquarium hobbyists or to the wild (Souty-Grosset et al., 2006). The fact that Marmorkrebs propagate by parthenogenesis makes the risk of release resulting in a reproducing population considerably greater than for sexually reproducing crayfish species – one single Marmorkrebs is sufficient to create a new population.

The proliferation of Marmorkrebs as aquarium pet increases the propagule pressure and thereby the probability and risk of establishment in the wild. For instance, there is concern that its arrival and spread in the North American pet trade will inevitably also result in releases from captivity there (Faulkes, 2010). Marmorkrebs are available through online pet shops and may be readily shipped across borders (Chucholl, 2010; Peay et al., 2010). Additionally, personal contacts between crayfish enthusiasts may lead to cross-border acquisitions (Faulkes, 2010).

In Madagascar, Marmorkrebs are harvested for human consumption and were sold in markets as cheap source of protein. They are reared in rice paddies and may be given as present to relatives in other regions. Further introductions along the major transport routes are therefore likely (Jones et al., 2009; Kawai et al., 2009; Heimer, 2010).

Currently, Marmorkrebs is a specifically prohibited species in Missouri (USA) (according to http://www.marmorkrebs.org) and its importation or keeping is illegal in some countries, including Sweden (Edsman, 2004) and Great Britain (Peay et al., 2010) in Europe. However, Marmorkrebs was found illegally in the aquarium trade in Great Britain (Peay et al., 2010). 

Habitat

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Introduced Marmorkrebs have been found in both lentic and lotic freshwater habitats (e.g. Marten et al., 2004; Martin et al., 2010b). In Madagascar, Marmorkrebs were reported from a great variety of habitats, including rice paddies, rivers, lakes and swamps (Heimer, 2010), as well as brick pits, drainage ditches and fish ponds (Jones et al., 2009). Established populations in Germany are known from lentic habitats only (Chucholl and Pfeiffer, 2010; Privenau, 2010).

Since an indigenous Marmorkrebs population has never been reported, nothing is known about its natural prime habitat. However, it is reasonable to consider the habitat requirements of its closest relative, Procambarus fallax: P. fallax occurs in streams and rivers but seems to prefer lentic or slow flowing habitats and is typically found in marshes, wet prairies and sloughs with lightweight organic soils (Hendrix and Loftus, 2000; Martin et al., 2010a). This preference is also reflected by the common name of P. fallax of `slough crayfish´. P. fallax also inhabits temporary wetlands, which feature brief dry-downs during which crayfish retreat into refugia or simple burrows (Martin et al., 2010a). It is considered as a tertiary burrowing species, i.e. it lives in open water during most of its life and burrows only under extreme conditions (Dorn and Violin, 2009).

Habitat List

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CategoryHabitatPresenceStatus
Freshwater
Irrigation channels Present, no further details Natural
Lakes Present, no further details
Ponds Present, no further details Harmful (pest or invasive)
Ponds Present, no further details Natural
Rivers / streams Present, no further details
Terrestrial-managed
Ricefields Present, no further details

Biology and Ecology

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Genetics

The Marmorkrebs propagates apomictically and produces genetically uniform clones (Martin et al., 2007). Developmental variation, however, leads to numerous phenotypes, even when reared under identical conditions (Vogt et al., 2008).

Reproductive Biology

The Marmorkrebs is unique in the manner that it is the only known decapod crustacean that reproduces by apomictic parthenogenesis: there exist only females which lay unfertilized eggs that develop into genetically uniform offspring (Scholtz et al., 2003; Martin et al., 2007; Vogt et al., 2008). No males have been found in laboratory or introduced, wild populations (Seitz et al., 2005; Jones et al., 2009).

The available data suggest that the Marmorkrebs is a fast growing species, which exhibits r-selected life history traits like early maturation, an extended breeding period and high fecundity. Parthenogenesis permits a high reproductive potential and since the females do not need to mate in order to reproduce, one single specimen is sufficient to create a new population.

Reproduction and growth of the Marmorkrebs have been studied in the laboratory by Seitz et al. (2005). They found that growth rate was largely temperature dependant and highest at 30°C, while highest survival occurred at 20°C. Marmorkrebs exposed to low water temperatures (8-10°C) mostly survived and some individuals moulted at 10°C.

Females reared at a temperature of 20-25°C started reproduction at an age of 141-255 days (carapace length = 14-22 mm). Fecundity ranged between 45 and 416 pleopodal eggs and increased with the size of the mother. Brooding took between 22 and 42 days and interclutch periods varied between 50 and 85 days.

The fecundity of free-living Marmorkrebs in Madagascar was slightly higher and ranged between approximately 50 and 525 pleopodal eggs (Jones et al., 2009). Three ovigerous Marmorkrebs captured in southwestern Germany carried seven, 160 and 724 pleopodal eggs (Chucholl and Pfeiffer, 2010).

Only limited information is available on the timing of reproduction in free-living Marmorkrebs populations: In Madagascar, ovigerous females have been observed in March, June, July-September and December (Jones et al., 2009). In southwestern Germany, ovigerous females were found from early June to mid-October, at water temperatures between 26 and 15°C (Chucholl and Pfeiffer, 2010; M Pfeiffer and C Chucholl, University of Ulm, Germany, personal communication, 2011). Seitz et al. (2005) reported that Marmorkrebs in the laboratory ceased to reproduce at temperatures of 15°C or below.

Adaptability

Free-living Marmorkrebs captured in Germany seem to have acute spines on the rostrum and postorbital ridges that are usually less pronounced or absent in laboratory specimens (Chucholl and Pfeiffer, 2010; Martin et al., 2010b). However, the question whether this might be a sign of predator- or environment-induced plasticity needs further investigation.

Nutrition

Like most crayfish species, the Marmorkrebs is most likely a polytrophic omnivore. It probably feeds on detritus, algae, plants and invertebrates and may also impact on higher trophic levels (e.g. fish). Vegetable substances dominated the stomach content of ten free-living Marmorkrebs sampled in Madagascar (Kawai et al., 2009). 

Associations

As a crayfish of North American origin, the Marmorkrebs is probably a carrier of Aphanomyces astaci, the causative agent of the crayfish plague (Souty-Grosset et al., 2006). In a preliminary study, Jones et al. (2009) tested six Marmorkrebs from Madagascar as negative; however, the applied preservation method may have led to false negative results and the sample size was limited. Further studies should therefore address the question whether free-living and laboratory Marmorkrebs populations carry the crayfish plague.

Moreover, rickettsiosis and coccidiosis have both been found in Marmorkrebs and Psorospermium sp. is known to infect P. fallax in its indigenous range (Souty-Grosset et al., 2006).

Environmental Requirements

The establishment and rapid expansion of Marmorkrebs in Madagascar leave little doubt that it is a `perfect invader´ in areas with climatic conditions similar to its probable indigenous range (Jones et al., 2009). However, there have been opposing views whether Marmorkrebs are also able to invade cold water environments at higher latitudes or altitudes, e.g. in Central or Northern Europe. While laboratory results and anecdotal observations suggest that Marmorkrebs tolerate low temperatures (8°C) (Seitz et al., 2005) and are able to survive even direct ice cover (Pfeiffer, 2005), other authors argued that their temperature optimum is considerably higher (18-25°C) than the temperatures in many water bodies at temperate zones and that they might not have the potential for wide expansion within Europe (Martin et al., 2010a,b).

Recent records from Germany evidence that Marmorkrebs are able to form stable, reproducing populations in temperate zones; however, so far in lentic habitats only (Chucholl and Pfeiffer, 2010; Privenau, 2010). Based on habitat and temperature preferences of P. fallax and Marmorkrebs, Chucholl and Pfeiffer (2010) suggested that Marmorkrebs are probably able to colonize summer-warm, lentic habitats in most parts of Central Europe.

Feria and Faulkes (2011) developed four species distribution models, using 19 climatic variables, to forecast the distribution of Marmorkrebs in Madagascar, Europe and North America. The model that has been used for the indigenous range of P. fallax and the introduced range of Marmorkrebs suggests that most of Madagascar, almost all of Europe and southeastern and southcentral USA, as well as Mexico and Cuba were suitable habitat for Marmorkrebs.

The species distribution models developed by Feria and Faulkes (2011) suggested also a susceptibility to drought, which has been documented for P. fallax (Dorn and Trexler, 2007). P. fallax is dependent on the presence of surface water, but is able to tolerate brief dry-downs (Martin et al., 2010a).

Overall, Marmorkrebs seem to be tolerant of a wide range of environmental conditions, including low oxygenation and temporary exposure to temperatures < 8°C and > 30°C (Seitz et al., 2005; Souty-Grosset et al., 2006; Feria and Faulkes, 2011; C Chucholl, University of Ulm, Germany, personal communication, 2011).

Climate

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ClimateStatusDescriptionRemark
Af - Tropical rainforest climate Tolerated > 60mm precipitation per month
Am - Tropical monsoon climate Tolerated Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
52 19

Air Temperature

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Parameter Lower limit Upper limit
Absolute minimum temperature (ºC) 8
Mean annual temperature (ºC) 11.1 22.4
Mean maximum temperature of hottest month (ºC) 20 27
Mean minimum temperature of coldest month (ºC) 2 15

Water Tolerances

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ParameterMinimum ValueMaximum ValueTypical ValueStatusLife StageNotes
Water temperature (ºC temperature) 18 25 Optimum <8-30 tolerated, laboratory data (Seitz et al., 2005)

Notes on Natural Enemies

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Marmorkrebs probably fall prey to a wide array of aquatic, semi-aquatic and terrestrial predators, however any specific information is currently lacking.

Means of Movement and Dispersal

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Natural Dispersal

Established Marmorkrebs populations may act as `bridgeheads´ for a further active range expansion. In Germany, single Marmorkrebs were found in the outflow of a colonized lake (M Pfeiffer, March, Germany, personal communication, 2010) and the species was also observed to migrate over land (Privenau, 2010).

Vector Transmission (Biotic)

Marmorkrebs may be prey to a wide array of predators, some of which might also carry single crayfish to new water bodies. For instance, it was shown than waterbird-mediated dispersal is possible for the invasive crayfish Procambarus clarkii (Ferreira et al., 2010). Since a single Marmorkrebs is sufficient to start a new population, this mode of dispersal should be taken into account.

Accidental Introduction

In Europe, Marmorkrebs have become popular as food source for ornamental turtles in recent years (C Chucholl, University of Ulm, Germany, personal communication, 2011). Since ornamental turtles may be kept in open ponds, this use of Marmorkrebs may facilitate accidental introductions.

Intentional Introduction

Marmorkrebs are popular pets and have been introduced into many countries for that reason (Soes and van Eekelen, 2006; Chucholl, 2010; Faulkes, 2010; Peay et al., 2010). They are sold through retail pet shops, various online sources and pet trade shows and may also be acquired through personal contacts between aquarium hobbyists. Its widespread use as pet entails both long-distance (i.e. cross-border and between continents) and local movement and dispersal (Faulkes, 2010). Peay et al. (2010) reported that it was found illegally in the aquarium trade in Great Britain.

Human-mediated transport and intentional introductions contributed to the rapid spread of Marmorkrebs in Madagascar (Jones et al., 2009; Heimer, 2010). Marmorkrebs are harvested for human consumption and have been sold at markets as cheap source of protein (Kawai et al., 2009; Heimer, 2010). They were actively brought into new areas (e.g. from the high plateau to Moramanga in eastern Madagascar) (Jones et al., 2009) and were deliberately introduced into rice fields for that reason. Many farmers apparently promoted the introduction of Marmorkrebs into various water bodies for additional income (Kawai et al., 2009).  As Jones et al. (2009) stated, “transportation by people is likely to result in very patchy distribution with individuals being transferred a long distance and spreading from this new nodes”.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Intentional releaseAquarium discards Yes Souty-Grosset et al., 2006
Internet salesEurope/USA Yes Yes Chucholl, 2010; Faulkes, 2010
Live food or feed tradeMadagascar Yes Jones et al., 2009
Pet tradeEurope/USA Yes Yes Chucholl, 2010; Faulkes, 2010

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aircraft Yes
Bulk freight or cargo Yes
MailC Chucholl, University of Ulm, Germany, personal communication, 2011 Yes Yes
Pets and aquarium speciesC Chucholl, University of Ulm, Germany, personal communication, 2011 Yes

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Economic Impact

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Anecdotal observations from Madagascar suggest a significant impact on fish populations. Local fishermen reported that Marmorkrebs have destroyed fishing in their area (Jones et al., 2009; Heimer, 2010). Inland fisheries in Madagascar rely mostly on introduced fish (e.g. small carp and tilapia) and are an important source of protein and income (Jones et al., 2009; Heimer, 2010). Although the Marmorkrebs may represent a substitute for fish, preliminary data of Jones et al. (2009) suggest that it is of lower economic value and in less demand.

There is also substantial concern that the invasion of Marmorkrebs will negatively impact rice culture in Madagascar (Jones et al., 2009; Kawai et al., 2009; Heimer, 2010). Introduced, non-indigenous crayfish are mostly considered a pest in rice paddies worldwide, because they damage young rice plants as well as irrigation systems and dams (e.g. Anastacio et al., 1995; Souty-Grosset et al., 2006). Preliminary stomach content data stress the ability of Marmorkrebs to feed on plant matter (Kawai et al., 2009) and Heimer (2010) indicated that Marmorkrebs may indeed damage young rice plants. Given the strong dependence of Madagascar’s economy on rice culture, a reduction in rice productivity would involve serious economic damage (Jones et al., 2009).

Environmental Impact

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Impact on Habitats

Marmorkrebs act probably as polytrophic omnivores and were found at very high densities in Madagascar (Jones et al., 2009). Given that, they might have a profound impact on ecosystem functioning and integrity, although specific information is currently lacking.

The related species Procambarus clarkii has had major impacts on native ecosystems and degraded shallow wetlands on the Iberian Peninsular within a few years. In Lake Chozas, the invasion by P. clarkii led to a switch from a clear water state to a turbid one, followed by a severe biodiversity reduction (Rodríguez et al., 2005).

Impact on Biodiversity

Marmorkrebs probably impact fish populations in Madagascar; however, explicit evidence is lacking (Jones et al., 2009; Heimer, 2010).

Marmorkrebs pose a threat to indigenous crayfish species in Madagascar and Europe, due to competition for food and space and crayfish plague transmission (Jones et al., 2009; Kawai et al., 2009; Chucholl and Pfeiffer, 2010).

Jimenez and Faulkes (2011) studied direct aggressive interactions between Marmorkrebs and Procambarus clarkii and concluded that Marmorkrebs have the potential to compete with other crayfish species. Furthermore, Marmorkrebs differ ecologically from indigenous crayfish in Europe and Madagascar in having a fast growth rate, a very high fecundity and an extended breeding period (Seitz et al., 2005; Jones et al., 2009; Chucholl and Pfeiffer, 2010). These life history traits might give an additional competitive advantage to Marmorkrebs.  

The risk of devastating consequences for indigenous crayfish would dramatically increase if Marmorkrebs are infected with crayfish plague: Any contact of Marmorkrebs to susceptible crayfish (i.e. all crayfish native to Europe, Madagascar, Asia, Australia, and South America) would almost certainly result in mass mortalities among the susceptible species (Souty-Grosset et al., 2006; Jones et al., 2009).

Threatened Species

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Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
Astacoides betsileoensisEN (IUCN red list: Endangered) EN (IUCN red list: Endangered)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides caldwelliEN (IUCN red list: Endangered) EN (IUCN red list: Endangered)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides crosnieriDD (IUCN red list: Data deficient) DD (IUCN red list: Data deficient)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides granulimanus (orambato)LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides hobbsiDD (IUCN red list: Data deficient) DD (IUCN red list: Data deficient)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides madagascariensis (Madagascar freshwater crayfish)DD (IUCN red list: Data deficient) DD (IUCN red list: Data deficient)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Astacoides petitiDD (IUCN red list: Data deficient) DD (IUCN red list: Data deficient)MadagascarCompetition - monopolizing resources; Pest and disease transmissionJones et al., 2009
Austropotamobius pallipes (freshwater white-clawed crayfish)EN (IUCN red list: Endangered) EN (IUCN red list: Endangered)GermanyCompetition - monopolizing resources; Pest and disease transmissionChucholl and Pfeiffer, 2010

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Capable of securing and ingesting a wide range of food
  • Highly mobile locally
  • Fast growing
  • Has high reproductive potential
  • Reproduces asexually
Impact outcomes
  • Negatively impacts agriculture
  • Negatively impacts aquaculture/fisheries
  • Threat to/ loss of endangered species
  • Threat to/ loss of native species
Impact mechanisms
  • Herbivory/grazing/browsing
  • Rapid growth
Likelihood of entry/control
  • Highly likely to be transported internationally deliberately
  • Highly likely to be transported internationally illegally
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Uses

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Economic Value

The Marmorkrebs is a popular pet species in Europe and North America (Chucholl, 2010; Faulkes, 2010). In Germany, Marmorkrebs are sold at approximately 5 € per specimen (C Chucholl, University of Ulm, Germany, personal communication, 2011).

In Madagascar, Marmorkrebs are sold in markets for human consumption (Jones et al., 2009, Kawai et al., 2009; Heimer, 2010). However, Heimer (2010) and Jones et al. (2009) concurrently indicate that Marmorkrebs are of low economic value.

Social Benefit

The Marmorkrebs was suggested as laboratory model organism for development, epigenetics and toxicology. Its high number of genetically identical offspring and its undemanding nature are, among other peculiarities, ideal prerequisites for this role (Vogt, 2008; 2010). Recent publications document its increasing use as model organism (e.g. Jirikowski et al., 2010; Rubach et al., 2011).  

Uses List

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Animal feed, fodder, forage

  • Fodder/animal feed

General

  • Botanical garden/zoo
  • Laboratory use
  • Pet/aquarium trade
  • Research model

Human food and beverage

  • Meat/fat/offal/blood/bone (whole, cut, fresh, frozen, canned, cured, processed or smoked)

Diagnosis

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Molecular genetic methods have been used to confirm the identification of introduced Marmorkrebs from Madagascar, Germany and Italy. Please see Jones et al. (2009), Martin et al. (2010b) and Nonnis Marzano et al. (2009) for details.

Detection and Inspection

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Marmorkrebs can be detected by a wide array of methods, including manual search during daytime or night-time (Chucholl and Pfeiffer, 2010), electrofishing (Martin et al., 2010b), crayfish traps (Martin et al., 2010b; C Chucholl, University of Ulm, Germany, personal communication, 2011), throw traps (Dorn et al., 2005) and snorkelling or SCUBA diving (Chucholl and Pfeiffer, 2010). Marmorkrebs may hide under stones, rocks, and driftwood or between macrophytes and vegetation. Juvenile specimens may also be found in leaf litter in shallow water, while larger specimens are generally found in bigger shelters. Jones et al. (2009) used local guides, who were able to locate crayfish within minutes.   

Please refer to the Description section for details on the identification.

Similarities to Other Species/Conditions

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The Marmorkrebs can be distinguished from other crayfish species by morphological and colour characters, as well as its unique reproduction mode. In addition to these classic approaches, DNA barcoding was recently shown to be an effective tool to unambiguously identify introduced Marmorkrebs in Germany (Martin et al., 2010b) and Italy (Nonnis Marzano et al., 2009).

From Parastacidae (crayfish of the southern hemisphere) and Astacidae (European crayfish and genus Pacifastacus), the Marmorkrebs differs in having an annulus ventralis (see Description). This character occurs only in female Cambaridae (Central and North American crayfish) and the east Asian genus Cambaroides.

Marmorkrebs can be distinguished from other North American Cambaridae by its distinct colour pattern (a marble pattern with dark lateral horizontal stripes through the carapace and pleon) and the morphology of its annulus ventralis (see Hobbs, 1989 and Martin et al., 2010a).

Furthermore, the Marmorkrebs exhibits a unique reproduction mode, i.e. there exist only females that propagate by parthenogenesis. This peculiarity of the Marmorkrebs was used to confirm the identification of a captured crayfish as Marmorkrebs in Japan (Kawai and Takahata, 2010) and is presumably the only way to discriminate Marmorkrebs from females of the sexual lineage of P. fallax (with the possible exception of DNA barcoding).

Prevention and Control

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Prevention

SPS measures

Marmorkrebs is a specifically prohibited species in Missouri (USA) and importation or keeping is illegal in some countries, including Sweden (Edsman, 2004) and Great Britain (Peay et al., 2010).

Public awareness

In Europe, many wholesalers and vendors are not aware of the risks associated with Marmorkrebs and there is often no or only poor knowledge about crayfish plague – despite numerous public and trade education efforts.

Since the Marmorkrebs has got a bad reputation because of its tendency to degrade typical aquarium communities quickly, voluntary self-regulation has occurred within the aquarium hobbyists’ community. Marmorkrebs were banned from certain trade shows and some shops do not offer the species any more. However, those initiatives are not the rule and Marmorkrebs are still widespread and readily available through wholesalers and the retail trade (Chucholl, 2010).

In Madagascar, an education campaign has been launched to discourage people from transporting and stocking of Marmorkrebs (Jones et al., 2009; Heimer, 2010).

Eradication

Unfortunately, there is no `magic silver bullet´ to eradicate established non-indigenous crayfish populations (Gherardi et al., 2011). Marmorkrebs do not need to maintain a minimum viable population size, which renders eradication of well-established Marmorkrebs populations even more difficult, or even impossible. However, chemical control at very early stages of invasions or in confined habitats might result in successful eradication (cf. Sandodden and Johnsen, 2010). Action should be taken at the earliest stage possible.

Containment/zoning

In Madagascar, volunteers are checking bush taxi passenger’s baggage to prevent further human-mediated dispersal of Marmorkrebs (Heimer, 2010).

Generally, Marmorkrebs are able to disperse via waterways and over land (Privenau, 2010). Any attempts to contain local populations should take both pathways into account.         

Control

Population control of non-indigenous crayfish is possible, but requires in most cases a combination of different, site-specific control techniques (Gherardi et al., 2011). For instance, a combination of intensive trapping and stocking/ management of indigenous predatory fish has been successfully used to reduce non-indigenous crayfish populations in Switzerland and in the USA (Frutiger and Müller, 2002; Hein et al., 2006).

Physical/mechanical control

P. fallax is known to be susceptible to drought (Dorn and Trexler, 2007). Provided that Marmorkrebs share this susceptibility, draining of habitats for longer periods might reduce confined populations.

Mechanical removal, e.g. by trapping, electrofishing, or by hand, only removes a fraction of the population and requires substantial efforts in order to be effective. Once the control measures have ceased, the population will return to its former level (Gherardi et al., 2011). In Madagascar, rice farmers have began to capture and burn Marmorkrebs in large quantities (Heimer, 2010), but the efficacy of this approach is not known.    

Biological control

Predatory indigenous fish are worth considering as control agents; however, there exist no specific data on Marmorkrebs control. Generally, eels are good candidates to control unwanted crayfish populations and have been shown to be effective in combination with other control methods (e.g. intensive trapping) (Frutiger and Müller, 2002, also see Aquiloni et al., 2010).

Chemical control

The application of biocides (e.g. pyrethroid insecticides) at very early stages of invasions or in confined habitats might result in total eradication (Sandodden and Johnsen, 2010). At a larger scale, the use of biocides is prohibitively expensive and ineffective, because of adverse impacts on non-target organisms (Anastacio et al., 1995) and the tendency of crayfish to escape lethal doses by retreating into burrows or by climbing out of the water.

Gaps in Knowledge/Research Needs

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During the last decade, the Marmorkrebs was primarily known from aquaria and most research was carried out in the laboratory. Its life history and ecology in the wild are understudied topics.

Several important aspects of the biology of free-living Marmorkrebs therefore need immediate attention: First, its life history in the wild should be studied at different latitudes. This knowledge may promote population control and risk assessment. Second, it is unclear whether Marmorkrebs are indeed a carrier of the crayfish plague; more data from its introduced range are needed, since this is a key topic concerning the risk that Marmorkrebs pose to native crayfish outside of the North American continent. Third, there has been merely anecdotal evidence for its economic and ecological impact – although preliminary data, along with the well-documented impacts of its invasive congener P. clarkii, justify eradication and control measures (cf. Jones et al., 2009; Kawai et al., 2009), further studies are necessary to assess its actual impact.

References

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Links to Websites

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WebsiteURLComment
Marmorkrebs.org - Advancing marbled crayfish researchhttp://www.utpa.edu/faculty/zfaulkes/marmorkrebs/

Contributors

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20/04/11 Original text by:

Christoph Chucholl, Fischereiforschungsstelle BW, Argenweg 50/1, D- 88085 Langenargen, & Dept. Experimental Ecology / Bio 3, University of Ulm, Albert-Einstein-Allee 11, D- 89069 Ulm, Germany

Reviewers' names are available on request.

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