Gammarus tigrinus

Invasion History

First Non-native North American Tidal Record: 1956
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1956

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General Invasion History:

Gammarus tigrinus is native to the East coast of North America from the southern Gulf of St. Lawrence to Florida. It is typically found in brackish habitats, at salinities of 0-25 PSU (Bousfield 1973). Gulf Coast (Florida to Louisiana) populations, referred to as G. cf. tigrinus are probably conspecific, but have small morphological differences from Atlantic specimens (LeCroy 2000). This euryhaline amphipod has successfully invaded fresh and brackish waters outside its historical native range, in the Great Lakes-St. Lawrence system, the upper Mississippi River, and fresh and brackish waters of Europe and South America (Pinkster 1975; Jazdzewski et al. 2004; Grigorovich 2005; Kelly et al. 2006a; Kelly et al. 2006b; Martin and Diaz 2007; Grigorovich 2008; Ba et al. 2010; Kotta et al. 2013). Gammarus tigrinus has been included in a key as a potential invader in California (Chapman 2007) and its potential worldwide range has been predicted with distribution modelling (Ba et al. 2010).

North American Invasion History:

Invasion History on the West Coast:

Gammarus tigrinus was reported in a survey of ship hull fouling in Vancouver Harbor, British Columbia (2007-2009, Sylvester et al. 2011). However, no details on the identification were given. These specimens could be the similar G. daiberi, which is established in San Francisco Bay.

Invasion History on the East Coast:

As described above, G. tigrinus is native from the East Coast of Florida to the Gulf of St. Lawrence. Gulf coast populations are native and either conspecific or closely related (LeCroy 2000). Several lineages occur on the East Coast, with major genetic breaks at Cape Hatteras and Cape Cod, and extending to Labrador and the northern shore of the Gulf of St. Lawrence. Bousfield (1958) collected G. tigrinus in the lower St. Lawrence from Montreal to brackish portions of the estuary. These populations were later found to be genetically divergent from presumably native populations in the southern Gulf (New Brunswick, Caraquet River estuary, and Mirimichi Estuary, lineage N1), and most closely related to populations in the Hudson River, and to recently discovered, introduced populations in the Great Lakes (lineage N3). They were presumably introduced from the Hudson estuary by dispersal through canals by hull fouling or ballast water (Kelly et al. 2006a; Kelly et al.2006b).

Gammarus tigrinus was discovered in Superior Bay, Lake Superior in 2001 and later found to be widespread through the Great Lakes (Grigorovich et al. 2005). These populations, like those in the estuary, are most closely related to those in the Hudson River, suggesting the Erie or Lake Champlain Canals as a possible vector, although shipping transport along the coast, and then up the St. Lawrence River, is also possible (Kelly et al. 2006a; 2006b). The date of the Great Lakes invasion is not known, due to confusion with the native G. fasciatus (Grigorovich et al. 2006).

Invasion History Elsewhere in the World:

In 2004, G. tigrinus was found at one location on the upper Mississippi at River Mile (RM) 99, and at two sites on the Ohio, at RMs 3 and 92, all near the Ohio-Mississippi confluence. In 2005, it was found at RM 840 and in 2006 at RM 768 (Grigorevich et al. 2008). Gammarus tigrinus made up 0.1-2.5 % of the amphipods collected during these surveys. Transport from the Great Lakes on barge fouling with Zebra Mussels, or on trailered boats is possible. However, the location of first capture is suggestive of transport up the lower Mississippi (Grigorovich et al. 2008).

In Europe, G. tigrinus was first found and described by Sexton in 1939, from brine seeps at Salwarpe, England in 1931. It was later (1953) found in brackish tidal waters in Frodsham Marsh, near the Manchester Ship Canal, Cheshire (Hynes 1955, as G. fasciatus). It was established in the freshwater Lough Neagh, Northern Ireland before 1955 (Hynes 1955; Bousfield 1958). Individuals from English brine seeps were introduced to the river Werra, Germany, polluted by salt-mining in 1957, as fish forage, and spread through the River Weser and Ems estuaries into the western Baltic. It reached the western Baltic, and the Schlei estuary, Germany, through the Kiel Canal (Jazdzewski 1980; Kelly et al. 2005b). Gammarus tigrinus has spread eastward through the Baltic, reaching the Odra River estuary and the Szczecin Lagoon, Poland in 1991 (Gruzka 1999), the Vistula Lagoon, Poland in 2000 (Jazdzewski et al. 2005), the Gulf of Riga, Latvia in 2003 (Kotta 2005), and the Gulf of Finland and the Neva River Estuary, Russia in 2003-2004 (Pienimäki et al. 2004; Berezina et al. 2007). Another deliberate stocking, of G. tigrinus from Lough Neagh, Northern Ireland, was made in 1964, in the freshwater lake Ijsselmeer, in the Netherlands, for fish forage, leading to dispersal through the Rhine Delta (Pinkster 1975), and eventual dispersal, by canals, east to the German Wadden Sea in 2009 (Buschbaum et al. 2012) and west to Belgium and France in 1995 (Kerckhof et al. 2007), reaching as far west as the Loire Valley by 2005 (Piscart et al. 2007).

The history of the invasion and genetic analysis indicate that there were multiple invasions of Europe by G. tigrinus. Specimens from Salwarpe, England, other locations in England, and sites in Germany and the Baltic belonged to a lineage (N1), originating from Maine to the Gulf of St. Lawrence (Kelly et al. 200b). The G. tigrinus found in Lough Neagh, Northern Ireland, and introduced to the Netherlands, belonged to another lineage (N4a), found in Chesapeake and Delaware Bays. The two lineages have spread widely throughout European waters, and seem to differ in salinity tolerance, with N1 favored in brackish waters and N4 favored in fresh waters (Kelly et al. 2006b). Gammarus tigrinus appears to have colonized Europe through multiple ballast water introductions, and spread through canals, fish-forage stockings (Pinkster 1975; Kelly et al. 2006b), and probably spread locally with vectors such as aquatic plants, trailered boats, and river transport. Gammarus tigrinus has also been collected at several sites in the Orinoco Delta, Venezuela, possibly by ballast water of oil tankers (Martin and Diaz 2007; Ba et al. 2010).

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Description

Gammarus tigrinus has a short rostrum. Its eye is large, kidney-shaped, and black. Antennae 2 is slightly longer than antenna 1. Antenna 1 has a prominent accessory flagellum with four or more segments. The basal segments of the flagellum have alternate posterior setae about twice the width of the segment. Segments 1, 2, and 3 of the peduncle, have respectively 1-2, 2-4, and 2 posterior marginal groups of setae. In the male, the distal segments (4-5) of the peduncle of Antenna 2 have many clusters of setae on the posterior margin.

Gnathopod 2 is larger than gnathopod 1. The palms of the gnathopods are oblique and the dactyls are slender. Coxal plates 1-4 bear moderately stiff setae on the anterior-ventral and posterior-ventral edge, but the ventral edge lacks setae. The hind margins of the abdominal side plates end in a slightly produced, acute angle. The urosome segments have paired clusters of lateral spines. The two rami of Uropod 3 are roughly equal in length. The telson consists of two rami, each of which bear two lateral bundles of spines. Males are 8-12 mm in size and females are 6-8 mm. This description is based on Bousfield 1958 and Bousfield 1973.

LeCroy (2000) refers to Gulf coast populations (Florida to Louisiana) as Gammarus cf. tigrinus, differing slightly from Atlantic populations in eye shape, fewer curly setae on antenna 2 and pereiopods 5-7, and a preference for lower salinities. ‘It seems more likely that the Gulf coast specimens merely represent a slightly different form of G. tigrinus’ (LeCroy 2000).

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Taxonomy

Ecology

General:

Gammarus tigrinus has separate sexes, brooded young, and development is direct (Bousfield 1973). The sexes are distinguishable at 6 mm, and females can begin bearing eggs at this size. Males reach slightly larger maximum sizes than females (15 mm vs. 13 mm). The mean numbers of eggs carried by females increase with body size, from 10.8 at 6-7 mm to 78.4 at 12-13 mm (Hynes 1955). Females bear eggs from March-April through October (Hynes 1955; Bousfield 1973). In the northern edge of its range, there may be one brood per year, but in warmer waters, multiple broods and generations are possible per year (Bousfield 1973).

Gammarus tigrinus tolerates a wide temperature range, from near freezing to above 31°C (Bousfield 1973; Wijnhoven et al. 2003; Lenz 2011). It has extensively colonized nontidal waters in Europe, the Great Lakes, and the upper Mississippi River (Bousfield 1958; Grigorovich et al. 2008). This amphipod is most abundant at salinities from 1-25 PSU, but can tolerate salinities up to 35 PSU (Dorgelo 1975). However, different genetic lineages appear to vary in their salinity tolerance and preference, and ability to invade fresh or brackish water (LeCroy 2000; Kelly et al. 2006b). Gammarus tigrinus is attracted to sheltered habitats, including debris, algae, submerged and emergent vascular plant, hydroids (Cordylophora caspia), pilings, pebbles, and freshwater seeps and pools on rocky shores (Hynes 1955; Bousfield 1973; Grigorovich 2995; Kotta et al. 2011). Gammarus sp. are omnivores, feeding on algae, aquatic plants, and invertebrates, including juvenile amphipods of their own and other species (Janes et al. 2015). Gammarid amphipods, including G. tigrinus, are a major food source for fishes (Janes et al. 2015).

Food:

Amphipods, invertebrates, algae, vascular plants

Consumers:

Amphipods, Shrimp (Palaemon spp.), fishes

Trophic Status:

Omnivore

Omni

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Habitats

General Habitat	Nontidal Freshwater	None
General Habitat	Fresh (nontidal) Marsh	None
General Habitat	Grass Bed	None
General Habitat	Coarse Woody Debris	None
General Habitat	Tidal Fresh Marsh	None
General Habitat	Salt-brackish marsh	None
General Habitat	Oyster Reef	None
General Habitat	Marinas & Docks	None
General Habitat	Rocky	None
General Habitat	Canals	None
Tidal Range	Subtidal	None
Tidal Range	Low Intertidal	None
Vertical Habitat	Epibenthic	None

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Tolerances and Life History Parameters

Minimum Temperature (ºC)	0	Based on geographical range
Maximum Temperature (ºC)	31	Experimental, Wijnhoven et al. 2003; Lenz 2011
Minimum Salinity (‰)	0	Experimental, field (Bousfield 1958; Bousfield 1973; Dorgelo 1975, Santagata et al., unpublished)
Maximum Salinity (‰)	34	Experimental, field (Bousfield 1958; Bousfield 1973; Dorgelo 1975, Santagata et al., unpublished; Piscart et al. 2011)
Minimum Reproductive Temperature	10	Pinkster 1975 (experimental)
Minimum Reproductive Salinity	0.6	Pinkster 1975 (experimental, no reproduction at 0.3 PSU)
Maximum Reproductive Salinity	32	Pinkster 1975 (experimental, highest tested)
Maximum Length (mm)	14	Adults (Bousfield 1973)
Broad Temperature Range	None	Cold temperate-Tropical
Broad Salinity Range	None	Nontidal-Euhaline

General Impacts

Impacts of introduced Gammarus tigrinus have not been studied in the St. Lawrence River estuary, or in the Great Lakes and upper Mississippi, where it would be competing primarily with native amphipods G. fasciatus, G. pseudolimnaeus, and the introduced Echinogammarus ischnus. Predation on the smaller native Crangonyx pseudogracilis is likely (Grigorovich et al. 2005; Grigorovich et al. 2008). Impacts of G. tigrinus have been better studied in Europe, where it has competed with, and preyed on, some fresh and brackish-water amphipod species (Pinkster 1975; Pinkster et al. 1992; Kotta et al. 2011; Janes et al. 2015). Economic impacts are few, but some deliberate introductions of G. tigrinus have been made in order to provide gamefish food in salt-contaminated bodies of water in Europe (Jazdzewski 1980).

Ecological Impacts

Competition- The invasion of Gammarus tigrinus has resulted in the complete or partial displacement of some native brackish water and freshwater amphipods in northern Europe. Among the species affected are the brackish G. duebeni, G. zaddachi, G. salinus, and G. oceanicus (Pinkster et al. 1975; Pinkster et al. 1992; Janes et al. 2015; Dobrzycka-Krahel et al. 2016), and some populations of the freshwater Gammarus pulex (Pinkster et al. 1993).

Predation- Gammarid amphipods are omnivorous, and their prey can include juveniles of their own species and their potential competitors. Gammarus tigrinus is both predator, prey, and competitor in many European amphipod communities, resulting in complex interactions. In Koiguste Bay, Gulf of Riga, Latvia, the combined effect of high fecundity and predation on juvenile amphipods favors G. tigrinus over G. duebeni (Janes et al. 2015). However, in freshwater Lough Neagh, Northern Ireland, G. tigrinus is preyed on by G. pulex and G. duebeni, which does restrict its habitat in the lake (Dick 1996). Gammarus tigrinus is an effective predator on the smaller introduced North American freshwater amphipod Crangonyx pseudogracilis, leading to the latter's disappearance from much of its invaded range (Dick 1996; Pinkster et al. 1992).

Trophic Cascade- The high abundance, high fecundity, and intermediate trophic position of G. tigrinus has led to complicated trophic interactions. At a site in the Gulf of Finland, replacement of G. duebeni and G. zaddachi by the more carnivorous G. tigrinus has led to increased algal biomass (Packalén et al. 2008). In the Gulf of Riga, dense populations of G. tigrinus have attracted schools of a fish (Threespine Stickleback; Gasterosteus aculeatus), and the increased predation has reduced the abundance of the native G. salinus, increasing the dominance of the more fecund G. tigrinus (Kotta et al. 2010).

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Regional Impacts

B-IX	None		Ecological Impact	Competition
Gammarus tigrinus is replacing and out-reproducing native Gammarus dueben, Gammarus zaddachi in the Gulf of Finland (Packalén et al. 2008)
B-IX	None		Ecological Impact	Trophic Cascade
Gammarus tigrinus is replacing more herbivorous native Gammarus duebeni and G. zaddachi, probably leading to decreased herbivory, increased algal biomass (Packalén et al. 2008)
B-VIII	None		Ecological Impact	Trophic Cascade
Experiments suggest that Gammarus tigrinus has had indirect effects on the native amphipod G. salinus in Baltic waters, by developing large populations in pebble habitats, which attract the predatory fish Gasterosteus aculeatus (Three-Spined Stickleback). The introduced amphipod has a higher reproductive rate, which compensates for increased predation, but the native species decreases in abundance, because of the intensified predation (Kotta et al. 2010).
B-VIII	None		Ecological Impact	Competition
Experiments suggest that Gammarus tigrinus competes with the native amphipod G. salinus in pebble habitats in Baltic waters, under predation by predatory fish Gasterosteus aculeatus (Three-spined Stickleback). The introduced amphipod has a higher reproductive rate, which compensates for increased predation, but the native species decreases in abundance, because of the intensified predation (Kotta et al. 2010). The two amphipod species tended to avoid one another, but the presence of G. tigrinus had a greater effect on habitat choice by G. salinus. However, this effect was weak and variable (Kotta et al. 2011). Gammarus tigrinus have greater fecundity than native G. duebeni in Koiguste Bay, Gulf of Riga. The combination of high fecundity and predation on juvenile amphipods favors G. tigrinus (Janes et al. 2015). Gammarus tigrinus displaced the native amphipods (G. salinus, G. oceanicus G. zaddachi) from shallow waters dominated by vascular plants, moving them to deeper areas vegetated with seaweeds (Reisalu et al. 2016).
B-VII	None		Ecological Impact	Competition
Gammarus tigrinus has a strong competitive impact in the Vistula Lagoon, replacing natives and other invaders (Jazdzewski et al. 2005; Grabowski et al. 2006; Zaiko et al. 2011). By 2008-2010, G. tigrinus was dominant at most stations in the Vistula lagoon, and the native species G. zaddachi and G. duebeni were extinct (Dobrzycka-Krahel et al. 2016). Impacts in the Gulf of Gdansk were classified as 'moderate', and those in the Curonian Lagoon as 'low' (Zaiko et al. 2011).
B-VIII	None		Ecological Impact	Predation
Adults of both Gammarus tigrinus and the native G. duebeni both prey on juvenile amphipods of both species. However, G. tigrinus has greater fecundity than G. duebeni in Koiguste Bay, Gulf of Riga. The combination of high fecundity and predation on juvenile amphipods favors G. tigrinus (Janes et al. 2015).
NEA-II	None		Ecological Impact	Competition
Since its discovery in the Netherlands in 1964, Gammarus tigrinus rapidly spread and largely replaced the native G. duebeni, G. pulex, and G. zaddachi in fresh and brackish coastal waters of the Netherlands (Pinkster 1975; Pinkster et al. 1992).

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