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Freshwater Reviews (2012) 5, pp. 21-35
© Freshwater Biological Association 2012
DOI: 10.1608/FRJ-5.1.457
21
Article
‘Killer shrimps’, dangerous experiments and misguided
introductions: how freshwater shrimp (Crustacea:
Amphipoda) invasions threaten biological water quality
monitoring in the British Isles
Calum MacNeil1*, Pieter Boets2 and Dirk Platvoet3
1*Department of Environment, Food and Agriculture, Thie Slieau Whallian, Foxdale Road, St. Johns IM4 3AS, Isle of Man.
Email: calum.macneil@gov.im
2 Laboratory of Environmental Toxicology and Aquatic Ecology, Ghent University, J. Plateaustraat 22, B-9000 Ghent, Belgium.
Email: Pieter.Boets@UGent.be
3 Netherlands Centre for Biodiversity/Naturalis Van Steenis building Einsteinweg 2, 2333 CC Leiden, The Netherland.
Email: dirk.platvoet@ncbnaturalis.nl
*Corresponding author
Received 19 October 2011; accepted 31 January 2012; published 1 June 2012
Abstract
In 2010, the ‘killer shrimp’ Dikerogammarus villosus (Crustacea: Amphipoda) invaded the British
Isles. Past research from central Europe has shown this eastern European shrimp invader to be
a ‘voracious omnivore’, highly predatory of a wide range of freshwater macroinvertebrate taxa
and also sh fry. It can become ‘super-abundant’ within invaded sites, greatly dominating native
assemblages in terms of numbers and biomass. Although the vast majority of past research
has focused on the negative impacts of D. villosus invasion on native biodiversity, we consider
the usually overlooked implications for biological water quality monitoring and ecological
assessment. We show how past invasions of other freshwater shrimp in the British Isles, such as
Gammarus pulex and Crangonyx pseudogracilis, have undermined the ability of biotic indices to reliably
reect changes in water quality. Within such invasions, more pollution tolerant invaders can
replace more sensitive natives and invaders can be highly predatory of other macroinvertebrate
taxa which contribute to biotic indices. We predict the impacts of the D. villosus invasion will be
greater than any previous shrimp invasion of the British Isles and indeed potentially of any other
freshwater macroinvertebrate invasion thus far. As it spreads throughout the British Isles, we
predict this species will have drastic deleterious impacts on native macroinvertebrate assemblages,
especially in its preferred rocky/stony habitats. We consider ways forward for future biological
water quality monitoring and ecological assessment within D. villosus invaded watercourses.
Keywords: Biological water quality; ecological assessment; killer shrimp; invader.
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DOI: 10.1608/FRJ-5.1.457
MacNeil, C., Boets, P. & Platvoet, D.
© Freshwater Biological Association 2012
Introduction
“The pump don’t work
’Cause the vandals took the handles”
Bob Dylan ‘Subterranean Homesick Blues’
On 9 September 2010, the ‘killer shrimp’ Dikerogammarus
villosus (Crustacea: Amphipoda) ocially ‘arrived’ in the
British Isles, with its presence confirmed in Grafham Water,
a reservoir in Cambridgeshire, England (MacNeil et al.,
2010a). This eastern European native of the Ponto-Caspian
basin (Black, Azov and Caspian Sea region) is currently
invading many parts of central Europe (e.g. van der Velde
et al., 2000; Muller et al., 2002; Arndt et al., 2009; Messiaen et
al., 2010). It has justiably earned the title of ‘killer shrimp’
because of its predatory tendencies towards a wide range
of macroinvertebrates, including mayies, chironomids,
water hog lice, water eas, damselies, leeches as well as
other amphipod shrimps and even sh larvae (Dick et al.,
2002; MacNeil & Platvoet, 2005; Bollache et al., 2008; Boets
et al., 2010). Indeed, stable-isotope analysis indicates that
this species occupies the same trophic level as predatory
sh (see Marguiller, 1998). However, the success of
D. villosus in newly invaded habitats such as Graam
Water is undoubtedly partially due to its ability to exploit
a diverse food base, not just function as a predator (Dick et
al., 2002; Kley & Maier, 2003; Casellato et al., 2007; Platvoet
et al., 2009), with structural examination of its mouthparts
showing it is neither a specialised carnivore nor herbivore
but is rather unspecialised (Mayer et al., 2008). Indeed,
it has been recently been termed a ‘voracious omnivore’,
which is arguably the most apt description so far (MacNeil
et al., 2011). D. villosus is just the latest of several shrimps
to invade British fresh waters (Gledhill et al., 1993; MacNeil
et al., 1999) but given its history of damaging impacts in
central Europe (van Riel et al., 2006; Panov et al., 2009), we
believe the ecological impacts of this invader will be the
most profound of all the shrimp invaders so far and quite
probably, all of the macroinvertebrate invaders of British
fresh waters so far.
It was unsurprising that the arrival of D. villosus in
Graam sparked a great deal of interest from media and
environmental protection agencies alike (Constable &
Fielding, 2011; Madgwick & Aldridge, 2011). Biologists
from the England and Wales Environment Agency
quickly descended on the reservoir to assess the situation
at ‘ground zero’. What they subsequently found was
alarming, with D. villosus present in huge numbers, with
precopula pairs, juveniles and egg-laden adult females
all evident (MacNeil et al., 2010a). In short, a large
well-established population, with the shrimp occupying
all stony edges of the reservoir, crevices in concrete
structures and under buoys in open water areas. The
various facets of the UK scientic establishment debated
what to do about this arrival and the admiedly remote
possibility of conning it to this single water body. Then,
within weeks, two more populations ‘appeared’, both
in Wales; one in Eglwys Nunydd reservoir Port Talbot
and the other in Cardi Bay. The ‘killer shrimp’ was
obviously in the British Isles to stay and no doubt new sites
will continue to emerge. It joins the increasing ranks of
other damaging invaders in British fresh waters, that it is
probably impossible to eradicate, such as North American
signal craysh, Chinese mien crab and zebra mussel (see
www.nonnativespecies.org for identification guide; Fig. 1).
The success of D. villosus and other freshwater
shrimps as invaders can be linked to their archetypal
invader life history characteristics of rapid growth,
Fig. 1. Dikerogammarus villosus; a new invader of British fresh
waters
DOI: 10.1608/FRJ-5.1.457
23
‘Killer shrimps’, dangerous experiments and misguided introductions
Freshwater Reviews (2012) 5, pp. 21-35
early sexual maturity, a very large reproductive
capacity, wide physico-chemical tolerances and the
ability to exploit a diverse food base (MacNeil et al., 1997,
1999; van der Velde et al., 2000; Dick et al., 2002; Pöckl,
2007, 2009; Tricarico et al., 2010). These characteristics
contribute to them acting as ‘keystone’ species, capable
of impacting on other trophic levels and changing the
structure of the overall macroinvertebrate community
within invaded areas (Savage, 1996; MacNeil et al., 1997;
Dick et al., 2002; MacNeil et al., 2011). Unfortunately, the
success of invasive freshwater shrimps within invaded
sites is also often accompanied by sharp declines in
native biodiversity (Pinkster et al., 1992; Dick et al., 2002;
Kelly et al., 2006; Bollache et al., 2008), as species such as
D. villosus can become ‘super-abundant’, greatly
dominating resident macroinvertebrate assemblages in
terms of relative abundance and biomass (van Riel et
al., 2006; van Riel, 2007). For instance, in some German
rivers, D. villosus now constitutes 90 % of the total
abundance of all benthic macroinvertebrates (Arndt et al.,
2009). Therefore, it is unsurprising that within such sites,
native assemblage structure is often irreversibly changed
through severe competition and predation, with native
species eliminated and replaced (Ricciardi et al., 1998;
Kelly et al., 2002, 2003, 2006; Crawford et al., 2006).
Invasions of freshwater shrimps often also accompany
pollution or environmental degradation (Boets et al., 2011)
or follow major disturbances with more pollution-sensitive
native shrimps being replaced by more tolerant invaders
(den Hartog et al., 1989; Conlan, 1994; MacNeil et al., 2004).
Only months after the Graam Water invasion, the
England and Wales Environment Agency pronounced it
the ‘worst alien invader of England and Wales’ waterways’
and top of the ‘most wanted’ of all invaders in a 2011 list,
which also included Japanese knotweed and mink. Given
the background we have just outlined, it was perhaps to
be expected, that after the arrival of the ‘killer shrimp’, the
immediate focus of the majority of scientic research and
debate focused on the ‘killer’ aspect of the invader and its
potential impacts on native biodiversity (see Madgwick
& Aldridge, 2011). However, we think it is also worth
considering a more indirect eect of this invasion, that
of the serious undermining of established water quality
monitoring programmes in the British Isles and indeed
in many other countries. This is because much of the
biological monitoring of fresh waters tends to rely
on biotic indices generated by macroinvertebrate
assemblages responding to changes in water quality
in predictable ways. However, we will show that this
reliability in ecological assessment can be compromised
by pollution-tolerant invasive shrimps replacing more
sensitive natives and very predatory invaders decimating
native assemblages as a whole. In short, the ability of
the native community to contribute to biotic indices
in a meaningful way to reect changing water quality
will be eectively ‘hamstrung’. There remains debate
about just how serious the impact of D. villosus will be
for British freshwater ecosystems; is it ‘hype’ or ‘horror’
(Madgwick & Aldridge, 2011)? By examining what
happened in respect of biological monitoring during
previous shrimp invasions in the British Isles, we hope
to emphasise just how profound the negative impacts
of invaders such as D. villosus on ecological assessment
and consequently environmental protection could be.
More ‘horror’ than ‘hype’ in this respect, as we will see.
The Water Framework Directive,
good ecological status and shrimp
invaders – why the latter two may
be mutually exclusive
The Water Framework Directive (WFD) (European
Parliament & Council, 2000) is a laudable and visionary
ecological management tool aiming to improve water
quality throughout Europe. In fresh waters, the WFD
requires the maintenance of high ecological status where
it already exists (i.e. near pristine macroinvertebrate
assemblages) and achieving a minimum of good ecological
status in all fresh waters by 2015. Ecological status can be
regarded as shorthand for the structure and functioning
of rivers and lakes – for instance are they pristine and
undisturbed or are they being degraded and suering
from pollution? The implementation requirements of the
WFD have caused development of assessment schemes
24
DOI: 10.1608/FRJ-5.1.457
MacNeil, C., Boets, P. & Platvoet, D.
© Freshwater Biological Association 2012
based on biological elements geared to detect measurable
responses to specic pressures (Solheim & Gulati, 2008).
Assessments of biological river water quality in
the British Isles form a crucial part of the overall WFD
ecological status assessment of rivers. This relies on
assessments of benthic macroinvertebrate assemblages
via the calculation of biotic indices such as the Biological
Monitoring Working Party (BMWP) score and the
Average Score Per Taxon (ASPT) (Biological Monitoring
Working Party, 1978; Armitage et al., 1983; Birk & Hering,
2006; Messiaen et al., 2010). The BMWP system is similar
to many other biotic indices, in that it assigns scores to
macroinvertebrate families based on their perceived
relative sensitivities or tolerances to organic enrichment.
For instance, on a scoring system of 1–10, taxa very
tolerant of poor organic water quality score 1 and taxa
very intolerant of poor water quality score 10, with other
taxa given scores between these extremes depending on
their tolerances. The BMWP is the sum of scores from all
scoring taxa (usually family level) found in the sample
(the ASPT is the average score achieved by all the scoring
taxa and is derived by dividing the BMWP score by
the number of taxa which generated it). The BMWP
is frequently used in tandem with the computer
model RIVPACS (River InVertebrate Prediction and
Classication System – see Wright et al., 2000), which, using
physical, chemical and geographical characteristics of a
water quality monitoring site, can predict what the natural
macroinvertebrate assemblage of that site would be, in
the absence of environmental stress such as pollution. By
comparing predicted values for indices such as the BMWP
with real values obtained during actual sampling, the
level of stress or pollution the resident assemblage has
experienced can be assessed and graded for biological
water quality. The RIVPACS model is based on
macroinvertebrate data from across Britain. In
Northern Ireland a modied version is used with a
reduced taxa list, to take into account the less diverse
macroinvertebrate assemblage, as certain taxa
found in high quality waters in England, Scotland
and Wales have never colonised Irish fresh waters.
High ecological status in WFD terms implies near
pristine macroinvertebrate assemblages (Arbačiauskas et
al., 2008; Arndt et al., 2009) and this obviously must assume
invaders are absent or at the very least, very rare and that
their impacts are inconsequential. We will show that for
many macroinvertebrate assemblages, where invasive
shrimps are present, this is a dangerous assumption.
All shrimps are equal but some
shrimps are more equal than others
– the problem of biotic indices
when a sensitive native is replaced
by a tolerant invader
Invasive shrimps are capable of surviving rigorous
introduction mechanisms, such as being transported
in poor quality ballast water of ships, that allow them to
enter river systems where environmental degradation
has diminished native assemblages (den Hartog et al.,
1989; MacNeil et al., 2004; Boets et al., 2011). They can also
be far more pollution tolerant than the natives they may
be replacing (Dick & Platvoet, 1996; MacNeil et al., 2000).
A major problem that then results, when such invaders
establish themselves within native assemblages, is that the
scoring system of the BMWP and other similar indices do
not distinguish between native and invasive species within
the same family, even when they dier in sensitivity to
organic pollution (Walley & Hawkes, 1996; MacNeil et
al., 2000). The potential for the function and accuracy of
biotic indices to be compromised by a native species being
substituted by an invader requires urgent investigation
(Orendt et al., 2009).
The amphipod crustacean family Gammaridae is
an example of a BMWP scoring family which contains
many native and invasive species with widely diering
physiological tolerances (Walley & Hawkes, 1996; Gaston
& Spicer, 2001). Gammarus spp. have featured in many
invasions because of both accidental and deliberate
introductions linked to shipping, aquaculture, angling
and ‘ecological experiment’ (Hynes, 1950, 1954; MacNeil
et al., 1999a). Gammarus spp. have many traits typical
of successful invaders such as broad environmental
DOI: 10.1608/FRJ-5.1.457
25
‘Killer shrimps’, dangerous experiments and misguided introductions
Freshwater Reviews (2012) 5, pp. 21-35
tolerances, non-selective diet and fast reproduction
(MacNeil et al., 1997, 1999a). In a computer-based
mathematical reappraisal of BMWP allocated scores in
England and Wales, Walley & Hawkes (1996) reassessed
the scores of 85 macroinvertebrate families based on
17 000 standardised kick samples. For the Gammaridae,
they derived a new score of only 4.5 (based on 12 596
samples) as opposed to the allocated score of 6.0 and they
acknowledged that this may reect the more pollution
tolerant North American G. tigrinus invading English
rivers, where the more pollution sensitive English
native G. pulex had been replaced as the representative
amphipod in the BMWP system. This is unsurprising
as G. tigrinus, which was introduced via some unknown
route to the British Isles in the early 20th century
(Sexton, 1939), has been deliberately introduced into
German rivers to improve food resources for native sh,
where native shrimps had been removed by pollution
(Fries & Tesch, 1965). When the BMWP system was
introduced, it was acknowledged that ‘the score system
will probably need to be modied in the light of practical
experience’ (Biological Monitoring Working Party, 1978).
Another example of a well-studied amphipod
species replacement in other British waters, is that of
the replacement of native Gammarus duebeni celticus
by invading Gammarus pulex (Dick, 2008). G. pulex has
featured in both the ‘dangerous ecological experiments’
and ‘misguided introductions’ referenced in the title of
this piece. H.B.N. Hynes, undoubtedly one of the greatest
freshwater ecologists Britain has ever produced, was
the perpetrator of the ‘experiment’ in the Isle of Man (an
island of 500 km2 in the Irish Sea, 26 km from mainland
Britain). Between 1949 and 1956 Hynes introduced
G. pulex from three source locations in the British Isles
(the Crogga River, Isle of Man; the River Terrig, Rhytalog,
Wales; Greasby Brook, near Liverpool) into streams in the
south of the Isle of Man that were either devoid of shrimps
or contained only the native species G. d. celticus. Each site
received either hundreds or thousands of individual G.
pulex, as Hynes aempted to see if and how the invader
could replace the native and if G. pulex was ‘able to colonise
suitable empty streams’ (Hynes, 1950; MacNeil et al., 2009).
Several decades later, Hynes understandably regreed
these ‘experiments’ but pointed out ‘you could do those
sort of things in those days’ (personal communication
to C. MacNeil). Gammarus spp. are also highly regarded
as sh food (MacNeil et al., 1999) and this led to the
‘misguided introduction’ of G. pulex into Northern
Ireland in 1958–59 in order to bolster the riverine food
base in angling waters. Again, this time G. d. celticus was
the native but this time the culprits were not scientists
but shermen who deliberately transplanted tens of
thousands of G. pulex from England into several Northern
Irish rivers (Strange & Glass, 1979; MacNeil et al., 1999).
Gammarus duebeni celticus and G. pulex are ‘lumped’
together as ‘Gammaridae’ in the BMWP index and
assigned the same score (MacNeil et al., 2000). In many
river systems in the Isle of Man and Northern Ireland,
G. pulex has replaced G. d. celticus (Dick, 2008; MacNeil et
al., 2009), through intraguild predation or IGP (predation
between competitors belonging to the same ecological
guild – see Polis et al., 1989), with lower dissolved oxygen
levels and higher levels of organic pollution favouring IGP
of the more sensitive native by the more tolerant invader
(MacNeil et al., 2004). Large dierences in the sensitivity
of these two species to changing water quality could
obviously result in erroneous scores in the BMWP scoring
system, ultimately contributing to false assumptions about
ecological status. This was explicitly tested by MacNeil &
Bria (2009) using an extensive dataset (over 100 sites) from
the Isle of Man and Northern Ireland, with water quality
assessed by the ASPT derivation of the BMWP index
(Armitage et al., 1983). MacNeil & Bria (2009) generated
two ASPT values for each site, one with the Gammaridae
included and one with this group removed. When the
biotic index was calculated for native and invader sites
(Gammarus spp. included), it was evident that the invader
occurred with macroinvertebrate assemblages more
tolerant of organic pollution, while the native occurred with
more sensitive assemblages. When both Gammarus spp.
were excluded from calculation of the indices, it was also
clear that the presence of the invader had falsely elevated
the biotic index score, while the presence of the native had
not. This ‘over-ination’ of scores was most pronounced
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MacNeil, C., Boets, P. & Platvoet, D.
© Freshwater Biological Association 2012
in poorest water quality areas, where G. pulex constituted
the highest scoring BMWP group, whilst co-occurring
with very tolerant taxa such as isopods, chironomids
and oligochaetes. These ndings implied that G. pulex,
at least in the parts of its range where it is considered
as an invader, should be given lower scores relative to
G. d. celticus, in the BMWP and similar indices. It must
also be remembered that the overall freshwater
macroinvertebrate assemblages present in Northern
Ireland and the Isle of Man are much less diverse than
in mainland Britain and this probably accentuates
the impacts of G. pulex on biotic indices. Walley &
Hawkes (1996) thus suggested that the BMWP score
for Gammaridae should be downgraded from 6 to 4
for water quality monitoring purposes, because of the
presence of tolerant invasives. This would mean the
presence of Gammaridae in a sample would indicate
lower estimated biological water quality than before.
Another shrimp invader, the North American
Crangonyx pseudogracilis was probably accidentally
introduced to the British Isles in the 1930s (Hynes, 1955;
Gledhill et al., 1993) and this is found in even lower water
quality areas than G. pulex in the Isle of Man and Northern
Ireland (MacNeil et al., 2000, 2004). For instance, although
G. pulex has replaced G. d. celticus in poorer water quality
areas of rivers, in even more grossly polluted areas, both
native and invader Gammarus spp. are absent and only
C. pseudogracilis is present. Indeed, bioassay transplant
experiments showed that both Gammarus spp. could not
survive in low water quality sites in Northern Irish rivers
where C. pseudogracilis thrived (MacNeil et al., 2000).
Unfortunately, the family Crangonyctidae is grouped
and scored the same as the Gammaridae in the BMWP
and similar biotic scoring systems in Europe (Metclafe,
1989). It is also grouped with Gammarus spp. in WFD
bioassessment methods for the UK (see www.wfduk.org/
bio_assessment/bio_assessment/rivers_invertebrates).
Obviously, this greatly increases the scope for awed
assessments of biological water quality (MacNeil et al., 2000).
Again, the inuence of relatively high scoring invasive
shrimps such as C. pseudogracilis will be disproportionately
high in the sites with poorest water quality, where there is
a sparse and low scoring, highly tolerant assemblage. Such
disparities can only increase as water quality decreases.
Dikerogammarus villosus is another shrimp invader with
wide physico-chemical tolerances (Devin et al., 2003), being
able to survive ship ballast water (Bruijs et al., 2001) and
even several days out of water (Marcus & Grabow, 2008).
However, as we will endeavour to show in the next section,
the ramications for ecological assessment stemming from
the replacement of a more sensitive native shrimp by a
more tolerant D. villosus will be marginal, when compared
to the changes wrought by the ‘killer shrimp’s’ predatory
impact on the whole macroinvertebrate assemblage.
Killer on the loose – the problem of
biotic indices when the invader is
highly predatory of native species
There are obvious implications for river water quality
monitoring when the macroinvertebrate taxa which
contribute to biotic indices are dierentially impacted by
the native species and the more predatory invader which
replaces it. For instance, looking at the replacement of
G. d. celticus by G. pulex in both the Isle of Man and
Northern Ireland, there are very few sites with both
native and invader co-occurring, even though the
majority of rivers contain both species. It seems once
G. pulex has invaded a site, it is dicult for it to coexist with
G. d. celticus on a long-term basis, leading Hynes (1954,
1955) to surmise that the native is invariably eventually
replaced on any land mass invaded by G. pulex. Regardless
of water quality, invasive G. pulex is more predatory than
the native G. d. celticus to a wide range of co-occurring
macroinvertebrates including many BMWP scoring taxa
(MacNeil et al., 1997; Kelly et al., 2002, 2003). For instance,
laboratory experiments have shown that G. pulex is
more predatory of the mayy nymph Baetis rhodani than
G. d. celticus (Kelly et al., 2002) and the Baetidae are a very
commonly occurring BMWP scoring family. Perhaps,
more tellingly, a eld study found that macroinvertebrate
assemblage composition, biomass and diversity diered
markedly between G. pulex and G. d. celticus dominated
areas in contiguous reaches of a Northern Irish river, where
DOI: 10.1608/FRJ-5.1.457
27
‘Killer shrimps’, dangerous experiments and misguided introductions
Freshwater Reviews (2012) 5, pp. 21-35
water chemistry remained constant (see Kelly et al., 2003,
2006). Kelly (2006) ascribed these dierences to increased
competition and predation by the invader relative to the
native. Similar to the ‘killer shrimp’ D. villosus, G. pulex
has also been found in ‘super-abundance’ within invaded
sites, for instance in several sites in the Killymoon River,
Northern Ireland (near the original introduction points
of G. pulex to the country); it constitutes 85 % of all the
macroinvertebrates present in terms of relative abundance,
whereas the native G. d. celticus rarely exceeds 10 % in
physico-chemically similar sites (MacNeil, 1997; MacNeil
et al., 1999). Similarly, in the Isle of Man G. pulex greatly
dominates kick samples taken from some sites for water
quality monitoring purposes and in these areas the
government freshwater biologist has to disregard the
BMWP system and biological monitoring and rather rely
solely on water chemistry results (MacNeil pers. obs.;
Fig. 2). Obviously, all the co-occurring resident
‘non-shrimp’ taxa will experience vast dierences in
magnitude in the levels of competition and predation
between invader and native sites.
The ‘super-abundance’ of D. villosus, as it establishes
itself, dominating the resident macroinvertebrate
assemblage, can simplify assemblage structure and trophic
links (Dick et al., 2002; van Riel et al., 2006). These laer
processes, which have occurred in the River Rhine (van
der Velde et al., 2000), are probably already well under
way in Graam Water (Madgwick & Aldridge, 2011; C.
MacNeil, personal observation). In The Netherlands,
D. villosus has invaded many preferred habitats of the
native shrimp G. duebeni and the previously successful
invader G. tigrinus (Dick & Platvoet, 2008; MacNeil et al.,
2008). Declines in both these Gammarus spp. have been
aributed to severe predation by D. villosus as witnessed
in laboratory mesocosms (Dick & Platvoet, 2000). Declines
in native G. pulex and invasive G. tigrinus populations in
several Flemish canals were also aributed to D. villosus
invasion (Messiaen et al., 2010) and again, predation of
native G. pulex by D. villosus has also been observed in
laboratory mesocosms (MacNeil & Platvoet, 2005). G.
pulex may be under imminent threat of displacement
within many invaded systems in central Europe and, in the
future, the British Isles, as its spatial niche greatly overlaps
with D. villosus (Devin et al., 2003). Laboratory mescosom
experiments suggest that these species replacements
could happen very rapidly as, for instance, one large male
D. villosus can easily eliminate ve individual
Gammarus spp. amphipods within four days,
despite the presence of other ‘food’ such as leaf
lier (MacNeil et al., 2011). In addition, D. villosus
exhibits a signicantly greater type II functional
response to macroinvertebrate prey than these
native and introduced Gammarus spp., indicating
it will be a far more voracious predator with
greater negative impacts on prey populations
(Bollache et al., 2008). This is because
the functional response reects how the
consumption rate of individual consumers
changes with respect to resource density and
a type II response, in a predation context, is
one where the rate of prey consumption by a
predator rises as prey density increases, but
eventually levels o (a ‘plateau’ or asymptote),
at which point the rate of consumption remains
constant regardless of further increases in
Fig. 2. ‘Three-minute’ kick sample from river monitoring site in the River
Colby, Isle of Man. G. pulex is super-abundant and very few other BMWP
scoring families are evident, despite chemical water quality being rated good
to excellent.
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MacNeil, C., Boets, P. & Platvoet, D.
© Freshwater Biological Association 2012
prey density. In other words, D. villosus will keep
eating more prey for longer than these Gammarus spp.
The potential impacts of D. villosus on biotic indices,
water quality monitoring and ecological assessment will
probably be profound (Arndt et al., 2009), but haven’t
been considered for the BMWP and similar indices in
British fresh waters. However, it is an interesting exercise
to apply the British BMWP system to macroinvertebrate
assemblages in central Europe which have experienced
D. villosus invasion. For instance, there have been
dramatic changes in the density of some common
BMWP scoring taxa from routine water quality sites in
several canals in Belgium, coinciding with the arrival
of D. villosus (Fig. 3). It is not unreasonable to expect
similar declines in similar taxa in Britain. Obviously, if
native taxa are eventually eliminated completely by D.
villosus, the reliable functioning of ‘presence/absence’
biotic indices such as the BMWP score will be fatally
undermined within invaded sites. Only time will tell.
Living with the enemy – ways
forward for British water quality
monitoring as D. villosus spreads
Almost inevitably, the British media covering the D.
villosus invasion summoned up post-apocalyptic visions
of devastated rivers and lakes infested with eastern
European invaders scything their way through native
British fauna. However, again, almost inevitably, the
reality may turn out to be somewhat more mundane
and undoubtedly more complex, with a continuum of
impacts ranging from minimal to severe, dependent on
a myriad of factors including the resilience of the native
community and habitat suitability. Despite this, given
a favourable physico-chemical regime and a suitable
substratum (i.e. ‘rocky’ – whether this takes the form of
the ‘natural’ substratum of the boulder/cobble matrix
of a river or lake bed, or the ‘articial’ substratum of
gabions and concrete structures found in many rivers and
reservoirs; see Devin et al., 2003; MacNeil et al., 2008; Boets
et al., 2010), D. villosus has undoubtedly the capacity to
Fig. 3. Changes in the density of some common BMWP scoring taxa from routine water quality sites in several canals in Flanders (Belgium),
coinciding with the arrival of D. villosus (39 samples used to calculate the density of each taxon before invasion and 61 after; data set
covering the period 1991–2005).
DOI: 10.1608/FRJ-5.1.457
29
‘Killer shrimps’, dangerous experiments and misguided introductions
Freshwater Reviews (2012) 5, pp. 21-35
cause the same severe ecological damage to native British
freshwater communities as it has done in many parts
of central Europe (Dick & Platvoet, 2000; van Riel et al.,
2006; Panov et al., 2009). If an invader such as D. villosus
forms up to 90 % by relative abundance/biomass of the
total invertebrate assemblage in a river site (see van Riel,
2006), it is dicult to see how that site could be realistically
used in any meaningful way for biological water quality
monitoring. There are a number of options that may
need to be considered as D. villosus expands its range in
the British Isles. In addition, Constable & Fielding (2011)
rightly point out, that the D. villosus invasion of the UK
will probably eventually impact upon other invertebrate
biotic metrics used for aquatic assessment, not just water
quality. For instance the Lotic Invertebrate Index for Flow
Evaluation (LIFE – Extence et al., 1999), which is used to
assess rivers for ow regime and habitat quality, and the
Community Conservation Index (CCI – Chadd & Extence,
2004), which is used for assessing freshwater sites for
special conservation methods, could both be undermined
by the presence of D. villosus and its impact on the rest of
the resident macroinvertebrate assemblage.
Cardoso & Free (2008) highlighted the increased
debate on how to incorporate invaders such as D. villosus
into ecological assessments owing to their potential to alter
the structure and functioning of aquatic ecosystems. The
UK Technical Advisory Group (UKTAG) on the WFD
recommends accounting for the presence of high impact
invasives when classifying the status of water bodies,
concluding that a water body cannot be classed as high
status if one or more high impact invasives are established
over a signicant area of the water body (www.wfduk.
org/UKCLASSPUB/LibraryPublicDocs/sw_status_
classication). Indeed, based on studies of its impacts in
central Europe, UKTAG have now listed D. villosus as a
high impact ‘red list’ invader for UK fresh waters
(Constable & Fielding, 2011). Unfortunately, many
other approaches to ecological status or water quality
assessment still invariably ignore the presence of invaders,
which can result in the bizarre situation, of a site with
a macroinvertebrate assemblage containing a high
proportion of invaders being classed as having good
ecological condition or good biological water quality
(Arbačiauskas et al., 2008; Cardoso & Free, 2008; MacNeil
& Bria, 2009). It does seem clear that the BMWP score
and related/similar biotic indices need to take into account
the presence of invasives such as amphipods. Orendt et
al. (2009) reviewed the role of invasive species in biological
assessment and after considering the advantages and
disadvantages of inclusion or exclusion of invaders in
assessments of biodiversity and human impact, decided
invasive species should be included. The inclusion of
invasive species has the advantages of allowing analysis of
the functioning of the whole ecosystem and, by recording
the taxonomy of the assemblage as a whole, can act as an
early warning system that the assemblage may be about
to change after the initial arrival of invaders (Orendt et al.,
2009). For instance, where long-term biological datasets
have been established alongside standard chemical
measurements, it should be relatively simple to assess if
the arrival of an invader has had a signicant impact on
the biotic indices, via the use of pre- and post-invader
datasets. Boets et al. (2011), using long-term monitoring
data to investigate changes in species composition in
Ghent harbour, Belgium, found that an improvement
in chemical water quality was reected in an increase
in the biotic index employed (the Multimetric
Macroinvertebrate Index Flanders MMIF – see Gabriels
et al., 2010), as long as alien species were included. If
no aliens were included, no increase in the MMIF was
observed, despite chemical water quality improving
drastically. This may be because the system in question
had almost no taxa (native or alien) due to pollution and
the subsequent arrival and increase in alien taxa actually
reected improving water quality from a very low base.
Gabriels et al. (2005) noted that D. villosus may
outcompete a number of native amphipod species, but
even then, this might not inuence the results of a biotic
index (Belgian Biotic Index or BBI) calculation at family
level, as individuals of surviving Gammaridae may still
be present and the BBI is an example of an index which
does not take abundance into account. Ultimately, given
the possible undermining of biotic indices by D. villosus
and indeed other invasive shrimps outlined here, until
30
DOI: 10.1608/FRJ-5.1.457
MacNeil, C., Boets, P. & Platvoet, D.
© Freshwater Biological Association 2012
there is a major overhaul of established biotic indices, it
may be necessary to rely solely on chemical water quality
and disregard biological water quality assessments in areas
subject to invasion. At the very least, biological water quality
monitoring within invaded fresh waters, should be treated
with a far greater degree of caution than is currently the case.
Despite these problems and realising the need
to somehow integrate the presence of invaders
within established routine monitoring programmes,
Arbačiauskas et al. (2008) proposed a simple method to
assess ‘biocontamination’, a term referring to the mere
presence of an invader, rather than its inherent ecological
impact (see Colaui & MacIsaac, 2004; Ricciardi & Cohen,
2007). This method was designed to utilise routine
water quality monitoring data and thus should require
minimal extra time or eort to that already expended
for WFD purposes. Classes of biocontamination were
dened that corresponded to the ve ecological quality
classes designated for WFD purposes (European
Parliament & Council, 2000), with the impact of invaders
on native macroinvertebrate assemblages assumed to be
proportional to the occurrence and abundance of invaders
within those assemblages. For instance, ‘bad’ ecological
status class is designated when invaders constitute over
50 % of the orders or 50 % of the abundance of the
assemblage (Arbačiauskas et al., 2008) and indeed,
such a situation exists in many European waterways
with abundance contamination exceeding 50 % in the
Nemunas, Oder, Rhine, Main and the Danube
(Arbačiauskas et al., 2008). MacNeil et al. (2010b)
applied the biocontamination index to Isle of Man
fresh waters and found 27 % of river sites exhibited
high or severe biocontamination. Several sites classed
as having very good biological water quality by the
BMWP/RIVPACS system also exhibited moderate to
severe biocontamination, emphasising how this aspect
of assemblage structure is currently being missed, or
rather ignored, in many British monitoring programmes
(MacNeil, 2006; MacNeil & Bria, 2009). This provides
a strong argument that biocontamination should be
regularly assessed alongside established biological
and chemical monitoring programmes to provide an
additional element ‘missing’ in current assessments of the
‘true’ ecological status of rivers. At least then, the ‘context’
of a good or bad score on a biotic index could be judged,
as surely it is a far more legitimate reection of good water
quality to have a high scoring native assemblage than a
similarly high scoring invasive assemblage, where in the
laer situation many natives may have been replaced and/
or eliminated. After all, this laer scenario may become
all too common in D. villosus sites in British fresh waters.
To conclude, we predict that, over time, D. villosus will
have a signicant negative impact on native biodiversity
and thereby biological water quality monitoring and
ultimately ecological assessment of British fresh waters.
Previous shrimp invasions by Gammarus spp. have
had signicant negative impacts on biodiversity and
have probably compromised biological water quality
monitoring in areas of the British Isles such as The Isle
of Man and Northern Ireland. There is every reason
to believe the impacts of D. villosus will be far more
drastic than anything that has gone before. Looking on
the positive side, we are at the very start of an invasion
process, where we know most, if not all, the original
points of introduction of the invader and where we have
numerous established biomonitoring sites, which will give
us a wealth of pre-impact data before (and if!) D. villosus
reaches them. Previous macroinvertebrate taxa lists from
such sites could also function as predictive tools. For
instance, on many BMWP taxa monitoring sheets, the
presence of non-scoring taxa is also recorded, such as
the zebra mussel – Dreissena polymorpha. This particular
Ponto-Caspian invader to Britain is abundant in
Graam Water and various studies from central Europe
have indicated that D. polymorpha may facilitate the
establishment and spread of D. villosus by providing a
suitable substratum, shelter and camouage (MacNeil
et al., 2008; Fig. 4). Obviously having such taxa lists
available for established monitoring sites and with the UK
Environment Agency establishing additional sites to the
national biomonitoring programme in 2011, specically
for D. villosus detection (262 additional sites, with sites
chosen on the basis of either containing suitable habitats
for D. villosus or where there are links to Graam Water
DOI: 10.1608/FRJ-5.1.457
31
‘Killer shrimps’, dangerous experiments and misguided introductions
Freshwater Reviews (2012) 5, pp. 21-35
and Cardi Bay – see www.environment-agency.gov.
uk), will allow the spread of D. villosus to be tracked.
This may then present opportunities for aempts to
‘manage’ or at least slow the spread of the ‘killer shrimp’
via public education and simple biosecurity measures
(Madgwick & Aldridge, 2011). Of course reliable
biological monitoring in badly ‘contaminated’ areas will
probably be a thing of the past, because to paraphrase Bob
Dylan, for tools to work properly, you need all the parts.
Acknowledgements
Thanks to Jaimie Dick for amphipod advice over the years
and funding a trip to Graam Water. Thanks to Nina
Fielding and the biologists at the Environment Agency in
Brampton for specimens and survey information. Thanks
to the Editor and two anonymous reviewers whose
comments greatly improved this manuscript.
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Calum MacNeil has worked on freshwater
community ecology in Scotland, Northern Ireland,
England, The Isle of Man, The Netherlands, Alaska
and New Zealand. His PhD at Queen’s University
Belfast focussed on the impacts of freshwater shrimp
invaders and this interest has stayed with him ever
since. He worked on invasive Gammarus in N. Ireland
and the ‘Killer Shrimp’ Dikerogammarus villous in
the Netherlands. In a series of unsuccessful grant
proposals, to the usual U.K. funding bodies several
years ago, he warned of the imminent arrival of D.
villosus to the U.K. and of the potential impacts of
D. villosus on British fauna, while suggesting some
mitigation measures and some useful ‘pre-emptive’
eld, laboratory and mesocosm experiments in the
U.K. and Central Europe. He hates to say he told
you so.... He is currently the Freshwater biologist and
Environmental Protection Ocer (Water) for The Isle
of Man Government. He is currently following the
invasion and aempted ‘control’ of D. villosus in the
British Isles with a great deal of interest.
Pieter Boets is a PhD student at the department
of Applied Ecology, Laboratory of Toxicology and
Environmental Biology at Ghent University, Belgium.
His research interest is related to the impact and
spread of alien macroinvertebrates in inland waters
in Flanders (Belgium). Based on a combination of
modeling techniques and laboratory experiments
he tries to gain insight into the complex ecology of
invasive species
Dirk Platvoet (PhD, B.Sc.) is researcher at the
Netherlands Centre for Biodiversity/Naturalis in
Leiden. He has studied mainly freshwater amphipods
during the past three decades and recently has
become involved in studies of aquatic invaders of
Western Europe.
Author Prole