Hemimysis anomala G.O. Sars, 1907 expands its invasive range to Northern Ireland

The invasive crustacean Hemimysis anomala was first discovered in the Republic of Ireland in April 2008. By 2009 it had extended its range to lakes throughout the navigated River Shannon waterway, occasionally occurring in large swarms in shallow waters and in lower densities at deep sites. In this study, a standardised stratified fish survey of Upper Lough Erne in 2013 found H. anomala in the stomach contents of four perch (Perca fluviatilis). These fish were captured at sites located at the northern and southern extremes of the lake, suggesting that invasive H. anomala are distributed throughout this waterbody. This catchment is directly linked to the River Shannon through the Shannon– Erne canal and our data indicates that, as previously predicted, the distribution of H. anomala now includes Northern Irish freshwaters.


Introduction
Non native invasive species are one of the greatest threats to biodiversity worldwide (Scalera and Zaghi 2004;Caffrey et al. 2008) and are of particular concern on islands (O' Neill and Stokes 2004;Stokes et al. 2006).Invasive species may often outcompete or consume native species (Dick et al. 2013) resulting in the domination and sometimes bioengineering of the environment (Jones et al. 1994;Holsman et al. 2010).
The numbers of freshwater invasive species in Ireland have increased dramatically during the last 30 years (Kelly et al. 2014), including the recent discovery of the Asian clam Corbicula fluminea (O.F. Müller, 1774) in 2009 (Sweeney 2009).The rates of inoculations are accelerating, primarily due to increased travel and trade (Caffrey et al. 2008;Maguire et al. 2011).
Hemimysis anomala G.O. Sars, 1907, a crustacean originating in the Ponto-Caspian region, has spread across continental Europe (Ketelaars et al. 1999;Ricciardi et al. 2012;Penk and Minchin 2014), arriving in Great Britain in 2006 (Holdich et al. 2006).It has also been found in the North American Great Lakes (Ricciardi et al. 2012).It was first described in the Republic of Ireland from a single lake, Lough Derg, on the River Shannon system in 2008 (Minchin and Holmes 2008), and subsequently lakes Ree and Key in the same system (Gallagher et al. 2010;Minchin and Boelens 2010) (Figure 1).
This study describes the most up-to-date range for H. anomala on the island of Ireland and its first occurrence in Northern Ireland.

Materials and methods
Upper Lough Erne was surveyed for fish during three consecutive nights from the 15 th to the 18 th October 2013 using 19 benthic and 2 pelagic mono-filament, multi-mesh (CEN 2005) gill nets (12 panel, 5-55mm mesh).The netting effort was supplemented with four benthic braided gill nets (62.5mm mesh).Netting locations were selected randomly in pre-determined depth strata (0-3m, 6-12m, 12-20m).A handheld GPS was used to record the precise location of each study site.Nets were returned to the shore for processing.Once removed from nets, fish were identified to species and measured (fork length ± 1 mm).In all fish a longitudinal ventral incision from the vent to a line level with the pectoral fin was made and stomach contents were removed and examined under a dissection microscope (20 magnification) and individual prey items were recorded.

Results and discussion
In total 751 fish specimens of four species and one hybrid were captured in the gill net survey (Table 1).Multiple individuals (circa 20 per fish) of H. anomala were recovered from the preserved stomach contents of four perch (Perca fluviatilis Linnaeus, 1758).These perch were all captured in monofilament benthic gill nets set at depths ranging from 8-16 m at three different sites in Upper Lough Erne (Table 2; Figure 2).One site was at the southern, upstream section of the lake, near to where the Woodford River is linked to the Shannon-Erne Waterway.The two other sites were at the northern end of the lake where the River Erne leaves Upper Lough Erne   (1999).This is a first record for H. anomala in Northern Ireland.The presence of this species at the two extreme ends of Upper Lough Erne indicates that H. anomala is now established throughout this lake.Given the riverine character and low turnover time of 0.04 years (NIEA 2009) of Upper Lough Erne (U.L.E.), it is probable that the species is also present in Lower Lough Erne.Its mode of transmission to U.L.E. is likely to have been anthropogenically assisted through the discharge of bilge/domestic water from water craft or discharge of water from anglers' bait boxes (Minchin and Boelens 2010).The path of spread of Hemimysis has followed that of the zebra mussel (Dreissena polymorpha (Pallas, 1771)) (Rosell et al. 1998).
H. anomala is a lipid rich organism providing perch with similar nutritional value as to that provided by juvenile fish (Borcherding et al. 2007).Borcherding et al. (2007) also found that in the River Rhine H. anomala contributes from 20 to 100% of the diet of 0+ perch.Growth rates of juvenile perch also accelerated in the presence of H. anomala.
In the Netherlands, an invasion by H. anomala caused a decline in phytoplankton and zooplankton biomass (Ketelaars et al. 1999).Two months after the discovery, a sharp reduction in anomopod densities, compared to the three previous years, was observed.The invertebrate predators Bythotrephes longimanus (Leydig, 1860) and Leptodora kindti (Focke, 1844) soon vanished as did the anomopod Chydorus sphaericus (Muller, 1785).However, copepod densities remained unaffected.Ketelaars et al. (1999) also found that densities of Daphnia spp., Bosmina spp., Ostracods, and Rotifera declined significantly in the period directly after initial detection of H. anomala.Uncertainties regarding the top down effects of H. anomala on zooplankton exist when algal production is low and therefore limits zooplankton production (Ketelaars et al. 1999).
The introduction of this species to the River Erne catchment is worrying as this species is known to be a voracious predator capable of consuming zooplankton prey at three times the rate of its closest native ecological equivalent Mysis salemaai (Audzijoynte and Vanola 2005), formerly Mysis relicta Lovén, 1862 (Dick et al. 2013).Lough Erne has also experienced an ecological shift (Rosell 2012) since the introduction of Dreissena polymorpha in the period between 1996 and 1998 (Rosell et al. 1998).The presence of H. anomala may in the short-term aid the population expansion and growth of some fishes (Borcherding et al. 2007), however in the long term it may adversely affect zooplankton composition that is crucial for the success of 0+ fish, including the endangered pollan (Coregonus pollan Thompson, 1835) (Harrod et al. 2002).The co-occurrence of these two high impact invaders (Maguire and Grey 2006;Gallardo and Aldridge 2013) is likely to compound the current changes in ecological state that this water body is already experiencing (Rosell 2014).
Attention must now be concentrated on monitoring this species and inhibiting its expansion into other catchments.The migrational habits of this species make it difficult to sample and monitor using conventional methods of netting and trapping.A novel technique gleaned from this study could be to use stomach content analysis of established predatory fish such as the perch, coupled with night time sampling as per Minchin and Boelens (2010) to provide accurate results of the early spread of this invasive species.

Figure 1 .
Figure 1.Map detailing previous range of Hemimysis anomala in Ireland.

Figure 2 .
Figure 2. Map of Upper Lough Erne detailing sampling sites.

Table 1 .
Species and sample size encountered in Upper Lough Erne gill net survey.

Table 2 .
Positive sample site locations.