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      Sexually produced ossiani morph (on the right) and parthenogenetically
produced pengoi morph (on the left) produced morphs of Cercopagis pengoi
(Photo: Dr. Igor Grigorovich, University of Windsor, Canada) - Click for full size   Sexual female Cecopagis pengoi with a resting egg: anterior region (on the left) and complete body with caudal process (on the right) (Photo: Dr. Igor Grigorovich, University of Windsor, Canada) - Click for full size   Male Cercopagis pengoi: anterior region (on left) and complete body with caudal process (on right) (Photo: Dr. Igor Grigorovich, University of Windsor, Canada) - Click for full size
    Taxonomic name: Cercopagis pengoi (Ostroumov, 1891)
    Synonyms: Cercopagis (Apagis) ossiani (Mordukhai-Boltovskoi 1968)
    Common names: cercopag (Russian), fishhook waterflea (English), Kaspischer Wasserfloh (German), petovesikirppu (Finnish), röövtoiduline vesikirp (Estonian), rovvattenloppa (Swedish), tserkopag (Russian)
    Organism type: crustacean
    Cercopagis pengoi is a water flea native to the Ponto-Aralo-Caspian basin in South Eastern Europe, at the meeting point of the Middle East, Europe and Asia. It has spread from its native range and become invasive in some waterways of Eastern Europe and in the Baltic Sea. It has been introduced to the Great Lakes of North America, quickly becoming established and is now increasing its range and abundance. Cercopagis pengoi is a voracious predator and may compete with other planktivores. Through this competition, C. pengoi has the potential to affect the abundance and condition of zooplanktivorous fish and fish larvae. It also interferes with fisheries by clogging nets and fishing gear.
    Description
    The most pronounced parts of the body are the head, the second pair of antenna, four pairs of thoracic legs (thoracopodsI-IV), abdomen, caudal process, and a brood pouch in females. The head is essentially composed of a large single eye, where the amount of black pigment makes less than one half of the diameter of the eye. The second antenna is a large appendage containing of two branches - the endopod and exopod. The first pair of thoracic legs (thoracopods I) are 3-4 times longer than the second ones. Abdomen length is equal to the length of the rest of the body, and spines are large, equal to 2-3 diameters of caudal process (Mordukhai-Boltovskoi & Rivier, 1987; Rivier 1998). Parthenogenic females of the first generation of C. pengoi that hatch from resting eggs are morphologically distinct from parthenogenic females of following generations. They have a short straight caudal spine unlike the characteristically looped caudal spine of parthenogenically-produced individuals (Simm & Ojaveer 1999). C. pengoi possesses a high degree of regional variability in morphology. Largest adult parthenogenic females are found in the Baltic Sea (mean body length 2.0 mm), while those in the Caspian Sea and in Lake Ontario are smaller (1.7 and 1.4 mm, respectively). Caudal process is largest in the instar III parthenogenic females from the Baltic Sea (mean length 9.6 mm), medium in Lake Ontario (8.6 mm), and shortest in females from the Caspian Sea (7.5 mm). However, relative to body length, the length of caudal process is largest in populations from Lake Ontario (mean 5.9 mm), medium in the Baltic (4.9 mm), and smallest in the Caspian populations (4.3 mm) (Grigorovich et al. 2000).
    Similar Species
    Bythotrephes longimanus

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    Occurs in:
    estuarine habitats, lakes, marine habitats, water courses, wetlands
    Habitat description
    Cercopagis pengoi is a euryhaline and eurythermic, having a wide tolerance to salinity temperatures. It occurs in both brackish, up to 17%, and fresh waters, as well as temperatures of 3 – 38 ºC (c.f. Gorokhova et al. 2000). However, highest population densities are found at summer temperatures (16 – 26 ºC) and at salinities of up to 10% (Mordukhai-Boltovskoi & Rivier, 1987; Rivier, 1998). Although some specimens may be found at temperatures of 10 °C it generally requires temperatures of 15 °C or higher to establish a significant population. It also resides above the thermocline in stratified waters in warmer, more active waters (Pollumae & Valjataga, 2004). Both in the Caspian Sea (Rivier, 1998) and Lake Ontario (Ojaveer et al. 2001) C. pengoi abundance increases with distance from shore, suggesting that this is a typical pelagic species, which live in the open sea, away from the littoral zone.
    General impacts
    Cercopagis pengoi preys on native zooplankton, may compete with native zooplanktivores, fouls fishing nets and other equipment, and may cause an array of other ecological impacts to aquatic systems. C. pengoi affects resident zooplankton communities by selective predation in Lake Ontario (Benoit et al. 2002); Gulf of Riga (Ojaveer et al. 1999, 2004); Gulf of Finland (Uitto et al. 1999; Lehtiniemi & Gorokhova 2008). Its invasion and populations in the Baltic Sea correlate to significant declines in small, cladoceran prey species Bosmina coregoni maritime, Evadne nordmanni, and Pleopsis polyphemoides (Kotta et al. 2006). A similar decrease in the abundance of copepods, including key species Eurytemora affinis, in the Gulf of Finland is believed to be caused by C. pengoi as well (Lehtiniemi & Gorokhova 2008). It is also a potential competitor with young stages of planktivorous fish for herbivorous zooplankton (Vanderploeg et al. 2002). Such changes in ecology may result in increased competition among zooplanktivores, decreased grazing pressure on phytoplankton, enhanced algal blooms, and major changes to higher trophic levels.

    Additionally, this large cladoceran tends to attach to fishing gears, clogs nets and trawls, causing problems and ultimate economic losses for fishermen. Reports of their fouling and costly impacts have come from the Gulf of Finland, the Neva Estuary, the Archipelago Sea, the Northern Bothnian Sea, and on the coasts of Lithuania (Birnbaum 2006 and references therein). Its effects on the food-web and energy transfer in lower trophic levels are likely to cause problems with fish stocks (E. Gorokhova pers. comm., in Birnbaum 2006; Ojaveer et al. 2001). Anecdotal evidence suggests that it can cause allergic reactions in fisherman who clean remains from nets (Leppäkoski & Olenin 2000; ICES 2002).

    Uses
    In the Baltic and in the Great Lakes, zooplanktivorous fish and mysids are reported to prey on C. pengoi, implying that it has become a new food source. Its importance increases in larger fish (Antsulevich and Välipakka 2000; Gorokhova et al. 2004; Ojaveer et al. 2004; Bushnoe et al. 2003) and in actively migrating mysids (Gorokhova and Lehtiniemi 2007).
    Notes
    The paucity of ecological studies on C. pengoi is in part due to the difficulties in handling and culturing Cercopagis as this hampers experimental studies.
    Geographical range
    Native range: Southern Europe - Ponto-Aralo-Caspian basin, i.e. Caspian, Black and Azov seas and small coastal lakes in this area (Mordukhai-Boltovskoi and Rivier 1987; Rivier 1998). Known introduced range: waterways and reservoirs in the Eastern Europe, Baltic Sea, Laurentian Great Lakes, Finger Lakes (North America) (Leppäkoski and Olenin 2000; Therriault et al. 2002; Vanderploeg et al. 2002).
    Introduction pathways to new locations
    Natural dispersal: One expansion route for Ponto-Caspian species to the Mediterranean is the through the Bosporus (Istanbul Strait )(Cristescu et al., 2001 in Guher, 2004).
    Ship ballast water:


    Local dispersal methods
    Boat: On fishing lines.
    Management information
    There is currently no known method of eradication or control for Cercopagis pengoi. Prevention of establishment and spread are the only means of management. Most probably, all trans-oceanic introductions of C. pengoi have resulted from the dumping of ship ballast water containing adults or eggs in new locations. Strengthening and improving existing ballast water regulations and promoting awareness of C. pengoi would therefore help in preventing the spread (Birnbaum, 2006). Prompted by the explosive increase of ship-borne exotic species in the Great Lakes, the USA implemented a regulation that requires inbound vessels to exchange freshwater/estuarine ballast with highly saline oceanic water in May 1993 (Ricciardi and MacIssac 2002). In theory, this procedure should have greatly reduce the risk of invasion as freshwater organisms would be purged or killed by seawater and would be replaced by marine organisms that would not survive if released into the freshwaters. However, the recent invasion of C. pengoi causes concern as it was apparently introduced after implementation of ballast water regulations, which raises concern that either these measures are not effective against gametogenic eggs of Cercopagis or control over the water exchange is not effective.

    A few measures are recommended to prevent further local spread of C. pengoi and other species with similar ecology. Bait or bait water should not be released into water body or transport from one water body to another. Good containment measures should be followed to control both the spread of adults and resting eggs, which are capable of surviving desiccation and freezing for periods of several years. Rinsing boat and equipment with hot water (>40°C), high-pressure water spray, or drying boat and equipment for at least 5 days before re-entering water body will help to control the spread of adult C. pengoi. Thoroughly draining and cleaning motor; bilge, transom and live wells; bait buckets; and fishing apparatus and gear will help to control the spread of adult C. pengoi and resting eggs (Crosier and Molloy, Undated).

    Nutrition
    Cercopagis pengoi is a generalist feeder which preys on various species of cladocerans, copepods, rotifers, i.e., both micro- and mesozooplankton (Mordukhai-Boltovskoi 1968; Laxson et al. 2003; Gorokhova et al. 2005; Lehtiniemi and Linden 2006; Pichlova-Ptacnikova and Vanderploeg 2009). It is able to capture and handle prey about its own body size to those seventeen times smaller. Cercopagids capture their prey with the thoracopods I, retain it by thoracopods II-IV, crush its cuticle by mandibles, and suck the prey body contents (Mordukhai-Boltovskoi 1968; Mordukhai-Boltovskoi and Rivier 1987).
    Reproduction
    As many other cladocerans, Cercopagis pengoi is a cyclic parthenogen. It reproduces parthenogenically during the summer and gametogenically later in the year. The parthenogenically-produced young develop in a fluid-filled dorsal brood pouch that ruptures to release the young. In late summer and autumn, parthenogenic females produce eggs that develop into males and gametogenic females, which copulate. Gametogenic reproduction results in resting eggs, which are released when the brood pouch ruptures, and overwinter in the sediment. After a refractory period, development proceeds and neonates hatch in spring-summer, depending on local temperatures, to re-found the population (Mordukhai-Boltovskoi and Rivier 1987; Rivier 1998). Sexual females are reproductive only at instars II and III, producing 1-4 resting eggs, while parthenogenic females produce between 1 and 24 embryos; average clutch size decreases gradually from instar I to instar III and from early to late stage of embryonic development (Grigorovich et al. 2000). The embryonic development time of parthenogenic Cercopagis in the Baltic Sea is 3.2 d and generation time is 14.7 d, which implies that during summer season there could be 5-7 generations, depending on temperature (Svensson and Gorokhova 2007).
    Lifecycle stages
    Female, both parthenogenic and gametogenic, and male Cercopagis pengoi possess 3 life-history stages or instars, which differ by number of spines, or barbs, on the caudal process. At each molt, the animal sheds its exoskeleton to the base of the caudal process. A new pair of proximal barbs and the growth of an intercalary segment are inserted between the existing tail spine and the body. The newborn parthenogenic females (instar I) have one pair of barbs on the caudal process, compact oval embryos in the brood pouch without a pointed apex. The second stage (instar II) has two pairs of barbs and the mature stage (instar III) of the parthenogenic female has a large brood pouch with a pointed apex housing embryos. In males at this stage paired penes behind the last thoracic legs and a toothed hook on the first pair of legs are developed (Mordukhai-Boltovskoi & Rivier, 1987; Rivier 1998). Parthenogenic females of the first generation of C. pengoi proceed through 3 moult yielding 4 pairs of proximal barbs on the caudal process unlike the females of following generations that undergo 2 molts to reach adulthood (Simm & Ojaveer 1999).
    This species has been nominated as among 100 of the "World's Worst" invaders
    Reviewed by: Elena Gorokhova, Professor, Dept. of Applied Environmental Science, Stockholm University, Sweden
    Compiled by: Profile revision: National Biological Information Infrastructure (NBII) & IUCN/SSC Invasive Species Specialist Group (ISSG)
    Last Modified: Monday, 6 September 2010


ISSG Landcare Research NBII IUCN University of Auckland