Bythotrephes longimanus
(spiny waterflea)

Identity

Preferred Scientific Name

• Bythotrephes longimanus Leydig, 1860

Preferred Common Name

• spiny waterflea

Other Scientific Names

• Bythotrephes cederstroemii Schodler, 1877

International Common Names

• English: Eurasian spiny waterflea; longspined waterflea

Local Common Names

• Germany: Cederström-Blattfußkrebs
• Poland: iglik

Summary of Invasiveness

B. longimanus, commonly referred to as the spiny waterflea, is an invasive crustacean zooplankton in the Great Lakes region of North America and areas of Europe. Its native range encompasses large areas of northern and central Europe and Asia. It is a carnivorous member of the zooplankton community, feeding primarily on smaller cladocerans such as Daphnia and Bosmina. Invasions by B. longimanus have resulted in marked declines in the diversity and abundance of native crustacean zooplankton, with long-lasting effects. Some negative effects on the abundance of zooplankton may be the result of predator avoidance, whereby prey inhabit deeper, colder parts of a lake to minimize risk of being eaten by B. longimanus and in doing so experience reduced growth and reproduction. Because of its rapid population growth, energetic demands, and dietary preferences, B. longimanus is believed to compete with zooplanktivorous fish for food.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Crustacea
•                 Class: Branchiopoda
•                     Order: Cladocera
•                         Suborder: Onychopoda
•                             Family: Cercopagidae
•                                 Genus: Bythotrephes
•                                     Species: Bythotrephes longimanus

Notes on Taxonomy and Nomenclature

The species of Bythotrephes that invaded North America was originally identified as Bythotrephes cederstroemi, but genetic analyses have concluded that the taxon is conspecific to B. longimanus (Berg et al., 2002; Therriault et al., 2002). Nonetheless, there is substantial polymorphism within the species and two morphological forms are widely recognized called the ‘longimanus’ form and the ‘cederstroemi’ form. Specimens of B. longimanus in North America resemble the cederstroemi form. They tend to have a longer caudal process (tail spine) that bears a distinctive, mid-length kink (Therriault et al., 2002). Both forms of B. longimanus are widely distributed throughout Asia and Europe and are known to co-occur in the same water bodies.

Description

B. longimanus typically reaches a length of 10-15 mm at maturity (Branstrator, 2005). The species is characterized by its long caudal process (tail spine), which comprises about two-thirds of its total length, and a dorsal brood (egg) pouch which expands and becomes round as embryos grow.

The tail spine bears one to four pairs of lateral barbs, also called articular spines. The number of barb pairs indicates developmental instar. During instar advancement, the tail spine grows from the basal end and adds a pair of lateral barbs, but does not shed exoskeleton. Females born through parthenogenesis mature at instar II or III. Males mature at instar II and do not advance to instar III. Females born through sexual reproduction may eventually have four pairs of lateral barbs (Yurista, 1992). The tail spine of an individual born from a resting egg of the cederstroemi form does not bear a distinctive kink. This has been used as a marker to document the fraction of individuals in a population of the cederstroemi form born from resting eggs (Brown and Branstrator, 2011).

The head of B. longimanus contains a large black compound eye and a pair of multi-cusped, sickle-shaped mandibles (Martin and Cash-Clark, 1995). Several experiments indicate that B. longimanus uses vision to detect prey (Muirhead and Sprules, 2003; Pangle and Peacor, 2009; Jokela et al., 2013). A pair of large second antennae, positioned directly behind the eye, is used in swimming. Four pairs of forward-positioned thoracic legs are used to catch prey (Martin and Cash-Clark, 1995; Branstrator et al., 2005). The body and tail spine can occasionally appear blue, green, or red (Branstrator, 2005). Average body size of each instar can range widely on a seasonal basis within a lake (Burkhardt, 1994; Pothoven et al., 2003), and between lakes (Bilkovic and Lehman, 1997), driven by water temperature, nutrition, and fish predation pressure. 

Distribution

B. longimanus is distributed widely throughout the Holarctic region. Its native range encompasses the Baltic nations, Scandinavia, Germany, Switzerland, Poland, Austria, Italy, the British Isles, the Caucasus region, Turkey, Ukraine, Russia and China. It has been introduced to the North American Great Lakes region, and all populations there are non-indigenous, deriving from invasions occurring over the last few decades. B. longimanus has also recently expanded its range into Belgium and the Netherlands (Thierrault et al., 2002).

Distribution Table

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.

History of Introduction and Spread

The origin of B. longimanus in the Laurentian Great Lakes of North America has been attributed to the ballast water of cargo ships containing dormant gametogenetic eggs (Sprules et al., 1990; Lehman, 1987). These eggs can survive extended exposure to saltwater (Branstrator et al., 2013). Sprules et al. (1990) suggested that cargo ships carrying them may have originated from the Baltic Sea. Berg et al. (2002) used genetic data to propose that cargo ships in the Gulf of Finland and at the harbour in St. Petersburg may have taken on ballast water originating from inland freshwater lakes (such as Lake Ladoga) with a direct connection to the harbours, thus taking up B. longimanus specimens with them. 

B. longimanus was sampled in Lake Ontario as early as 1982 (Johannsson et al., 1991), with detections in Lake Huron in 1984 and Lake Erie in 1985 (Bur et al., 1986). The species subsequently spread in the Great Lakes system to all five lakes. Since the 1980s, the species has become widespread in inland lakes in Ontario and in many states of the United States surrounding the Great Lakes. B. longimanus has also spread beyond its native range in Europe into lakes in Belgium and The Netherlands.

Introductions

Risk of Introduction

The introduction of B. longimanus in North America has been attributed to international trade, with cargo ships that sail from Baltic ports carrying viable dormant B. longimanus eggs in their ballast water (Sprules et al., 1990). The spread of the species in North American systems is thought to have arisen from contaminated boating and angling equipment, to which the species attaches (Weisz and Yan, 2010; Kerfoot et al., 2011). The risk of introduction therefore lies in the use of brackish waters as ballast and the spread of the species through recreational activities.

MacIsaac et al. (2004) conducted a modelling study to attempt to predict the spread of B. longimanus in inland lakes in Ontario, Canada. They based their model on ‘human-mediated vector flows’ between already invaded and uninvaded water bodies and validated their predictions with already existing invasion records (back-casting). The authors found that the specific invaded lakes had high activity flow and they were able to pinpoint so-called invasion hubs which served as the source for further invasions. MacIsaac et al. (2004) concluded that the spread of the species will continue in central Ontario and that human activity can be used to predict the vulnerability of certain systems. Ultimately they recommended focussing on management of human-related vectors to reduce spread.

Habitat

B. longimanus can be found in all types of lentic water bodies (Grigorovich et al., 1998). Although it exhibits a high level of tolerance to changing and different habitats, it thrives in large, deep, temperate lakes, where it mostly inhabits the deeper, central areas of the water body and is seldom found at the shallower fringe (Grigorovich et al., 1998). It is usually found in mesotrophic and oligotrophic environments, probably due to its reliance on sight for predation and the reduced predation pressure from fish compared to eutrophic lakes (MacIsaac et al., 2000; Therriault et al., 2002; Branstrator et al., 2006; Jokela et al., 2013). It is known to thrive in reservoirs (Brown et al., 2012). Vertical and horizontal distribution patterns are discussed in more detail in the Activity Patterns section.

Habitat List

Biology and Ecology

Reproductive Biology

B. longimanus can reproduce both asexually (parthenogenesis) and sexually (gametogenesis). Asexual reproduction occurs during spring, summer, and autumn; sexual reproduction is usually confined to autumn (Straile and Hälbich, 2000; Branstrator, 2005; Brown and Branstrator, 2011). The generation time is short, ranging from 7 to 15 days, and is strongly temperature-dependent (Lehman and Branstrator, 1995; Kim and Yan, 2010). Several asexual generations of offspring are produced during one season (Brown et al., 2012; Miehls et al., 2012). The formation of the dorsal egg pouch marks the beginning of the parthenogenetic cycle. As embryos develop they are nourished by nutrient solution in the pouch and hatch as free-swimming juveniles (Alwes and Scholtz, 2014). Due to rapid growth and maturation, and parthenogenetic offspring production by predominantly female populations, B. longimanus numbers can increase rapidly (Yan et al., 2001; Brown et al., 2012).

The parthenogenetic cycle is interrupted in the autumn by a period of sexual reproduction (Branstrator, 2005). The sexual reproduction period serves to produce gametogenetic eggs, also known as diapausing or resting eggs; these dormant eggs serve as B. longimanus’ overwintering strategy (Herzig, 1985; Yurista, 1992; Yurista, 1997). During the gastrula stage the sexually fertilized diapausing eggs develop in the female’s brood pouch; once they are released they settle down to the sediment and remain dormant until the right environmental conditions prompt them to hatch (Yurista, 1997; Jarnagin et al., 2000; Brown and Branstrator, 2011).

The sex of individuals is assigned non-genetically and influenced by environmental stress factors. When females sense a shift in environmental conditions in the autumn (temperature drop/food scarcity), they produce more male offspring which can then facilitate the production of gametogenetic resting eggs (Cáceres and Lehman, 2010; Brown and Branstrator, 2011). This explains the shift from asexual to sexual reproduction during the end of the growing season.

Physiology and Phenology

The tail spine, which makes up most of B. longimanus’ body, protects it from predation by small <100 mm) gape-limited fish (Barnhisel, 1991a,b; Barnhisel and Harvey, 1995). The species also exhibits patterns of diel vertical migration to deeper waters as well as the ability to produce resting eggs in order to survive the pressures of predation (Ketelaars et al., 1995; Grigorovich et al., 1998; Cáceres and Lehman, 2010). The resting eggs can pass viably through the digestive systems of fish and waterfowl (Jarnagin et al., 2000; Charalambidou et al., 2003). Diel vertical migration to deeper waters reduces exposure to predatory fish (Young and Yan, 2008).

B. longimanus exhibits a lot of morphological variability in physical traits such as tail spine length and structure (Martin and Cash-Clark, 1995; Grigorovich et al., 1998; Therriault et al., 2002). Morphological differences are thought to be evidence of adaptability to different conditions in a waterbody (Grigorovich et al., 1998). Predation pressures have been identified as a selection process, resulting in an increase in tail spine length in populations under high predation pressures (Ketelaars et al., 1995; Grigorovich et al., 1998). Miehls et al. (2012) suggested that fish may directly act as natural selection agents, in that their selective consumption of smaller sized specimens may result in a shift in the average tail spine length in a B. longimanus population. Straile and Hälbich (2000) observed that females in populations under growing stress from gape-limited fish tended to shift egg/offspring production from many small eggs to a few large eggs producing larger offspring.

Longevity

Kim and Yan (2013) reported a maximum lifespan for B. longimanus individuals of less than 22 days for low prey density environments. The median observed lifespan was 12 days (Kim and Yan, 2013). B. longimanus resting eggs may survive dormancy for up to 17 months but most eggs appear to hatch after one winter (Andrew and Herzig, 1984; Herzig, 1985; Brown and Branstrator, 2011).

Activity Patterns

B. longimanus exhibits diel vertical migration (DVM) patterns, remaining in the deeper parts of lakes during daytime hours and migrating to upper sections at night (Ketelaars et al., 1995; Young and Yan, 2008; Brown et al., 2012). The DVM patterns exhibited by B. longimanus populations mirrored the observed migration trends and population densities, with depth, of Daphnia, the prey of B. longimanus (Ketelaars et al., 1995). Ketelaars et al. (1995) concluded that the trend supports the hypothesis that B. longimanus’ migration is related to its active pursuit of prey. Daytime migrations in clear, natural lakes are generally only into the metalimnion (Lehman and Cáceres, 1993; Young and Yan, 2008). Avoidance of the hypolimnion may reflect the need for light to feed (Jokela et al., 2013) and the avoidance of coldwater fish predators (Young and Yan, 2008). In reservoirs, daytime migrations to the bottom are common and may be temperature and food driven (Brown et al., 2012).

The horizontal distribution of B. longimanus is highly influenced by climatic conditions such as storminess and prevailing wind direction that control the mixing cycle and near surface currents in large basins (Grigorovich et al., 1998; Ketelaars et al., 1995).

Nutrition

B. longimanus is a predatory zooplankton (Therriault et al., 2002) that feeds primarily on small-bodied cladoceran species, such as Daphniidae and Bosminidae ranging in size from 300 to 700 µm, but larger daphnids are not immune from attack and consumption (Vanderploeg et al., 1993; Schulz and Yurista, 1999; Pichloivá-Ptácníková and Vanderploeg, 2011). B. longimanus offspring begin to feed immediately after hatching and are cannibalistic, making it difficult to culture and raise specimens in the laboratory without isolation of each individual in its own vessel (Kim and Yan, 2010). B. longimanus catches its prey using its large front thoracic legs, secures it with all four pairs of legs, and shreds it with the mandibles during consumption (Branstrator, 2005).

Predation rates and prey selectivity have been estimated by numerous researchers using a variety of approaches including experimental enclosures, bioenergetics models, and nutrient mass balance budgets (Vanderploeg et al., 1993; Burkhardt and Lehman, 1994; Lehman and Branstrator, 1995; Yurista and Schulz, 1995; Schulz and Yurista, 1999; Pangle and Peacor, 2009; Yurista et al., 2010; Jokela et al., 2013). Predation rates as a function of food density were studied experimentally by Kim and Yan (2013) who reported that B. longimanus consumes between 9-22 prey per day from a mixed species assemblage. 

Associations

Grigorovich et al. (1998) and Hessen et al. (2011) reported that B. longimanus populations are correlated with populations of Leptodora kindtii, the giant waterflea. Studies have shown low frequency of their co-occurrence among lakes, and inverse population dynamics in lakes where both species are present. In lakes with invasive B. longimanus, L. kindti densities decline (Branstrator and Lehman, 1991; Weisz and Yan, 2011).

Climate

Latitude/Altitude Ranges

Water Tolerances

Natural enemies

Notes on Natural Enemies

B. longimanus is consumed by several fish species in Eurasia and North America including rainbow smelt (Osmerus mordax), lake herring (Coregonus artedii)), lake whitefish (Coregonus clupeaformis), yellow perch (Perca flavescens), white perch (Morone americana), white bass (Morone chrysops), walleye (Sander vitreus), alewife (Alosa pseudoharengus), bloater chub (Coregonus hoyi), emerald shiner (Notropis antherinoides), spottail shiner (Notropis hudsonius), deepwater sculpin (Myoxocephalus thompsoni) and chinook salmon (Oncorhynchus tshawytscha), as well as the crustacean, Mysis relicta, in inland lakes in Ontario (Craig, 1978; Evans, 1988; Bur and Klarer, 1991; Hartman et al., 1992; Mills et al., 1992; Nordin et al., 2008; Isaac et al., 2012; Jacobs et al., 2013).

B. longimanus is predated on by juvenile and adult fish. The long tail spine of B. longimanus makes it a challenging prey for small <100 mm) fish to consume (Barnhisel, 1991a,b; Barnhisel and Harvey, 1995; Compton and Kerfoot, 2004; Jarnagin et al., 2004).  Selective predation can result in natural selection of long-tailed B. longimanus specimens (Miehls et al., 2012).

Means of Movement and Dispersal

Once introduced, the spread of B. longimanus within and among water bodies is believed to be partly the result of human-assisted dispersal due to its attachment onto recreational equipment such as fishing gear, anchors, boat lines, bait buckets, bilge water, and boat live wells (Lui et al., 2010; MN-DNR, 2015; USGS NAS, 2015). Free-swimming organisms do not survive out of water for long, but their resting eggs can survive under some conditions and remain viable until introduced into a new habitat (Brown, 2008; Lui et al., 2010; Branstrator et al., 2013; MN-DNR, 2015). Resting eggs in fish and migratory birds that have consumed B. longimanus are also thought to contribute to the species’ spread (Grigorovich et al., 1998).

Impact Summary

Environmental Impact

The main ecological impact of B. longimanus is its direct influence on the abundance and make-up of the zooplankton community through the consumptive effects of predation (Yan and Pawson, 1997; Boudreau and Yan, 2003). Potential prey such as Daphnia that migrate to deeper strata in a lake to avoid B. longimanus may also suffer reduced growth and reproductive rates if the water there is cold (Pangle et al., 2007). Reduced abundance and diversity of zooplankton caused by B. longimanus may affect energy flow to higher trophic levels (Foster and Sprules, 2009) and the health of fish that eat zooplankton. Fish health may also suffer as a result of injury from handling and consuming the tail spine of B. longimanus (Compton and Kerfoot, 2004).

The introduction of B. longimanus in Lake Michigan, USA, resulted in changes in population size of the native predatory cladoceran Leptodora kindtii, as well as the former’s most common prey, Daphnia (Lehman and Cáceres, 1993). L. kindti densities declined in areas of high B. longimanus abundance (Lehman and Cáceres, 1993). There were observed shifts in Daphnia assemblages, with reduced abundances of specific taxa in areas with high B. longimanus densities. Where formerly three abundant species of Daphnia existed, only Daphnia galeata mendotae was observed in large numbers after the introduction of B. longimanus (Lehman, 1991; Lehman and Cáceres, 1993).

Similar observations were made by Barbiero and Tuchman (2004) in Lakes Huron and Erie. The authors observed a reduction in the abundance of zooplankton species on which B. longimanus fed, such as Eubosmina coregoni, Holopedium gibberum, Daphnia retrocurva, Daphnia pulicaria, and Leptodora kindtii, with the complete disappearance of the copepod species Mesocyclops edax. Based on the wide range of affected zooplankton, Barbiero and Tuchman (2004) hypothesized that prey susceptibility was not only a function of suitable size but also of morphology, their vertical distribution in the basin, and defence adaptations against predation.  

Yan et al. (2002) observed a marked reduction in cladoceran taxa in the zooplankton fraction of an invaded Canadian shield lake (Harp Lake) in the presence of B. longimanus, when compared to uninvaded lakes in the same area. Similar results were observed in a later study by Boudreau and Yan (2003) for a larger set of lakes. Yan et al. (2002) suggested that the impact observed in Canadian shield lakes in Ontario could be the onset of a broad zooplankton biodiversity reduction in all lakes affected by B. longimanus invasion, with direct impacts on cladoceran (including Daphnia) abundance.

Social Impact

B. longimanus can ruin fishing gear when they are attached to fishing lines and accidentally reeled in (Brown, 2008; USGS NAS, 2015). Spiny waterfleas collect in ‘jelly-lake masses’ on fishing gear (Lui et al., 2010).

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Capable of securing and ingesting a wide range of food
• Benefits from human association (i.e. it is a human commensal)
• Fast growing
• Has high reproductive potential
• Gregarious
• Reproduces asexually

• Reduced native biodiversity
• Threat to/ loss of native species

• Competition - monopolizing resources
• Pest and disease transmission
• Fouling
• Rapid growth
• Produces spines, thorns or burrs

• Highly likely to be transported internationally accidentally
• Difficult to identify/detect as a commodity contaminant

Detection and Inspection

B. longimanus specimens can be collected from the zooplankton fraction via netting techniques. Barbiero and Tuchman (2004) collected specimens with a vertical net tow at specified depths. Straile and Hälbich (2010) utilized a standardized Clarke-Bumpus sampler (335 µm mesh size) for collection. Similarly, Miehls et al. (2012) used a zooplankton net with a 1 m diameter opening and a mesh size of 363 µm.

Similarities to Other Species/Conditions

The invasive fishhook waterflea (Cercopagis pengoi) is similar to B. longimanus (Lui et al., 2010; USGS NAS, 2015). C. pengoi can be distinguished from B. longimanus by the differences in their tail spines and egg pouches. C. pengoi’s tail spine comprises about 80% of its total length, proportionally longer than that of B. longimanus (Lui et al., 2010), and the brood pouch of C. pengoi is elongated and pointed, as opposed to the rounded brood pouch of B. longimanus (Lui et al., 2010). B. longimanus is larger than C. pengoi and does not have a hook at the end of its tail (USGS NAS, 2015).

Prevention and Control

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.

To avoid the spread of B. longimanus that have attached to fishing gear, the USGS recommends pressure-washing fishing equipment at pressures greater than 250 psi, or to wash equipment with hot water at temperatures above 50°C for at least 10 minutes (USGS NAS, 2015). Studies by Beyer et al. (2011) and Branstrator et al. (2013) provide experimental results on the efficacy of alternative methods to kill B. longimanus. Because the resting eggs do not survive exposure to dry air for 6 hours or longer (Branstrator et al., 2013), drying is commonly prescribed as a method to decontaminate equipment. 

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Links to Websites

Contributors

09/03/16 Review by:

Donn Branstrator, University of Minnesota Duluth

03/02/15 Original text by:

Adrian Mellage, consultant, Honduras

Distribution Maps