Bythotrephes longimanus
(spiny waterflea)

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.

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).

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.

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.

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).

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).

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.

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).

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. 

09/03/16 Review by:

Donn Branstrator, University of Minnesota Duluth

03/02/15 Original text by:

Adrian Mellage, consultant, Honduras