THE OCCURRENCE OF ANGUILLICOLA
CRASSUS (KUWAHAR, NIMI, AND HAGAKI,
1974), AN INTRODUCED NEMATODE, IN AN
UNEXPLOITED WESTERN IRISH EEL
POPULATION
M. Morrissey and T.K. McCarthy
ABSTRACT
The presence of Anguillicola crassus , an introduced Asian parasite of eels, into south Connemara is
reported. European eels Anguilla anguilla were found to be infected in the three basins of varying
salinity of Lough Ahalia, but eels sampled in the nearby marine Camus Bay were uninfected.
Variations in infection parameters were analysed. It was concluded that the parasite is a recent
introduction to the river system. The highest prevalence (63.1%) and mean intensity (4.22) of
infection in the lower, most saline, basin of the lough suggest that the parasite was introduced to the
River Screebe system at that location. Potential dispersal mechanisms by which the parasite may have
been introduced to such a relatively isolated location and to such apparently unexploited eel
populations are discussed.
M. Morrissey
(corresponding
author e-mail:
morrissey.
michelle@gmail.com)
and T.K. McCarthy,
Department of
Zoology, National
University of Ireland,
Galway, Ireland.
Received 21 April
2006. Accepted 10
September 2006.
Published 12
February 2007.
BIOLOGY
AND
INTRODUCTION
The swimbladder-inhabiting nematode Anguillicola
crassus (Kuwahar, Nimi, and Hagaki, 1974) is an eelspecific parasite, accidentally introduced into Europe
in the early 1980s through uncontrolled transfer of
live eels from Eastern Asia (Neumann 1985).
Presence of the parasite can induce pathogenic
changes in the swimbladder and reduce the ability
of the eel to withstand additional stressors (Kirk
2003). Anguillicola crassus was first recorded in Ireland
from eels captured in the Waterford Estuary in 1997
(McCarthy et al . 1999). Since then it has become
well established in several commercially exploited
Irish eel fisheries such as those on the Shannon and
Erne river systems (Evans and Matthews 1999;
McCarthy et al . 1999), Lough Corrib, Lough
Neagh and the Nore, Barrow, Suir and Slaney
Rivers (McCarthy et al., in press). As part of a
larger investigation of the population biology of
European eels (Anguilla anguilla L.) in Irish marine
and mixohaline waters, samples from unexploited eel
populations in south Connemara were found to be
infected with A. crassus . In this paper we detail and
analyse the A. crassus infection parameters recorded.
STUDY AREA
European eels Anguilla anguilla were sampled along
a short /2km salinity gradient in Lough Ahalia and
ENVIRONMENT: PROCEEDINGS
OF THE
in Camus Bay, western Ireland (Fig. 1). Lough
Ahalia, a coastal lagoonal lake (Healy 2003), consists
of three basins forming the lower reaches of the
River Screebe catchment. The system flows into
the Atlantic via Camus bay. The upper basin of
Lough Ahalia (surface area /40ha, mean depth
1.7m) is freshwater (0.1˜); the middle basin (surface
area /60ha, mean depth 2.5m) is brackish (12˜),
receiving bi-monthly tidal inputs of saline water
(i.e. on spring tides); the lower basin (surface area
/25ha, mean depth 1.6m) is more influenced by
the tides and receives a twice-daily influx of tidal
water, which leads to near full marine salinities
(25˜). Camus Bay is fully saline (34˜). The site was
chosen because of the relatively steep salinity
gradient over a small distance, but more
importantly, because there is no exploitation of
the eel population.
MATERIALS AND METHODS
Samples of yellow eel were obtained from the four
salinity zones (upper basin, middle basin, lower
basin and Camus Bay) during October 2004, using
unbaited fyke nets. Fyke nets were set at dusk and
lifted the following morning. Eels were transferred
on ice to the lab where they were measured (total
length, to the nearest millimetre), and weighed
(to the nearest gram). An index of condition
was calculated using Fulton’s condition factor
ROYAL IRISH ACADEMY, VOL. 107B, NO. 1, 13 18 (2007).
#
ROYAL IRISH ACADEMY
13
BIOLOGY
Fig. 1
*
AND
ENVIRONMENT
Map of Ireland showing the location of Lough Ahalia and Camus Bay.
K (100W LT3). Sex determination was by
macroscopic examination of the gonads (Beullens
et al . 1997). The swimbladder was removed, and
A. crassus present in the swimbladder lumen were
removed and counted as described by Gollock et al .
(2004) and Molnár et al. (1993). Parasitological
terms (prevalence and mean intensity) are used in
accordance with Bush et al. (1997). Prevalences
were compared by Fishers exact test, and mean
intensities were compared using a Bootstrap 2
sample test (Rózsa et al . 2000). In both cases
differences were considered significant if P B/0.05.
Table 1
*
RESULTS
Descriptive statistics for length and weight and
condition of eels from the four sites are shown in
Table 1. Analysis of variance showed that mean
log-transformed (log (x)) lengths of eels in the four
sites were significantly different (F /4.002, P B/
0.05) and post hoc analysis (LSD) showed that the
differences occurred in eels between Camus Bay
and the lower and upper basins of Lough Ahalia
(P B/0.05). There was a significant difference in
log-transformed weight between the four sites
Summary statistics for eel length, weight and condition from the upper, middle and
lower basins of Lough Ahalia and Camus Bay.
Site
Upper
Middle
Lower
Camus Bay
Total
No. of eels Length (mm)
Min.
Max.
Mean
SD
30
312
694
431.03
109.04
121
300
855
447.76
109.24
65
257
690
418.35
75.51
85
290
755
471.32
100.46
301
257
855
446.4
101.67
Weight (g)
Min.
Max.
Mean
SD
55.2
685
182.34
171.21
53.4
1392
220.37
246.05
43.8
673
145.40
93.11
38.8
896
214.25
163.44
38.8
1392
198.66
193.08
Condition
Min.
Max.
Mean
SD
0.136
0.221
0.1845
0.0196
0.129
0.365
0.1957
0.0386
0.139
0.56
0.1821
0.0384
0.132
0.221
0.1753
0.0187
0.129
0.456
0.1859
0.0334
14
THE
OCCURRENCE OF
(ANOVA; F /3.296, P B/0.05), and the LSD test
showed the lower basin of Lough Ahalia was
significantly different to the middle basin and
Camus Bay (P/ 0.05). There was a significant
difference in square-root-transformed condition
between the four sites (ANOVA; F/4.021, P B/
0.05), and the LSD test showed that the differences
occurred in eels from Camus Bay and those
from the lower and upper basins of Lough Ahalia
(P B/0.05).
Details of the infection levels of A. crassus
recorded in eels in the four sampling sites expressed
as prevalence (% infected), mean intensity (mean
number per infected host) and maximum burden
are given in Table 2. Anguillicola crassus was not
found in eels examined from Camus Bay.
Prevalence and mean intensities were highest in
the lower basin of Lough Ahalia and decreased from
lower to middle to upper basins of Lough Ahalia.
There was a significant difference in both
prevalence (P B/0.05) and mean intensity (P B/
0.05) between the middle and lower basin.
Sex was determined for all eels (n /301). An
overall predominance of females (88%) was
observed (n /265). There was no significant
difference in sex ratios between the 4 sites (x2 /
7.63, d.f. /3, P /0.054). Table 2 also displays
mean intensity of infection, prevalence and
maximum burden of A. crassus in male and female
eels for the total sample and from the middle basin
and the lower basin, where levels of infection were
highest. Overall, levels of infection were higher in
males than females. Levels of infection were
compared between males and females in the
middle and lower basins. In the middle basin
there was a significant difference in prevalence
(P B/0.05), with males having a higher prevalence
than females but not a greater mean intensity (P/
Table 2
*
ANGUILLICOLA
CRASSUS
0.7475). In the lower basin there was no significant
difference between the sexes with regard to
prevalence (P/0.304) or mean intensity (P/
0.3215).
Variation in infection intensity between length
classes is shown in Fig. 2. Spearman rank order
correlations showed a highly significant negative
correlation between length of eel and number of A.
crassus present in the middle basin (rs / /0.252,
P B/0.05) and no correlation in the lower basin (rs /
0.070, P/0.578). Though not systematically
investigated during the present study, damage to
the swimbladder wall was frequently observed in eels
infected with A. crassus . There was no significant
correlation between Fulton’s condition factor (K) of
eels and their parasite burdens in either the middle
basin (rs / /0.018, P /0.845) or lower basin (rs /
0.201, P /0.108). Because smaller eels in the middle
basin tended to have more parasites, both male and
females in the smallest length class ( B/400mm) from
this basin were compared to investigate whether
there was a relationship between sex and intensity of
infection. A significant difference was found
between males (n /15) and females (n /32)
B/400mm, with males having a higher intensity of
infection than females in the same size range (x2 /
10.885 df /4, P B/0.05).
The variance-to-mean ratio (/s2 =x) of parasite
abundance was calculated to provide an index of the
degree of dispersion of A. crassus among individual
host eels. A ratio of /1 indicates overdispersion, a
ratio equal to 1 indicates random distribution in the
parasite, and a ratio of B/1 indicates underdispersion
(Anderson and Gordon 1982). The variance-tomean ratios were both /1, indicating overdispersion
(middle basin s2 =x /2.28 and lower basin s2 =x /
5.63). The abundance of A. crassus in eels displayed a
negative binomial distribution in both the middle
Anguillicola crassus maximum burden, % prevalence and mean intensity for total
sample of eels (in bold) and male and females separately, sampled from the upper,
middle and lower basins of Lough Ahalia and Camus Bay.
Site
Upper
Female
Male
Middle
Female
Male
Lower
Female
Male
Camus Bay
Female
Male
No. of eels
Infected eels
Max. burden
Prevalence (%)
Mean intensity
30
24
6
121
106
15
65
54
11
85
81
4
2
2
0
36
25
11
41
36
5
0
0
0
1
1
0
7
7
5
17
16
17
0
0
0
6.7
6.7
0
29.8
23.58
77.33
63.1
66.66
45.45
0
0
0
1.5
1.5
0
1.75
1.8
1.64
4.22
3.83
7.0
0
0
0
15
BIOLOGY
AND
ENVIRONMENT
Mean number of parasite ± 95%CI
4.5
Middle Basin
4
Lower Basin
3.5
3
2.5
2
1.5
1
0.5
0
200-299
Fig. 2
*
300-399
400-499 500-599 600-699
Length class (mm)
DISCUSSION
Anguillicola crassus , accidentally introduced from Asia
in the 1980s, has been progressively expanding its
range in the eel-inhabited inland waters of Europe.
Its dissemination has been linked to the extensive
commercial transport of live eels and re-stocking of
eel fisheries with infected fish, as well as natural
movements of infected eels (Kennedy and Fitch
1990; Wickströem et al. 1998; Kirk 2003). Its arrival
in Ireland in the 1990s and its subsequent
colonisation of major eel fisheries has been
documented by McCarthy et al . (in press). The
discovery that eels in the relatively isolated lower
River Screebe area are now infected suggests that the
species is progressively extending its range in Ireland
and that a better understanding of its dispersal
routes and mechanisms is needed. The parasite is
recognised as being pathogenic in the European eel,
with adverse effects on affected swimbladders and on
various other aspects of eel physiology having been
recorded (Kirk 2003). Despite the damage caused by
A. crassus to swimbladders of eels noted in the
(a) 100
Observed
Expected
75
50
25
(b) 100
Observed
Expected
n = 65
75
50
25
0
0
0
16
present study, infected eels generally appeared to be
in good condition. Thus, in the present study, no
correlation was observed between Fulton’s
condition factor (K) and parasite burden in Lough
Ahalia. However, such eels are likely to have their
capacity to migrate to the Sargasso spawning area
adversely affected by their A. crassus infections. As
demonstrated in experimental studies on Dutch
silver eels, A. crassus can reduce the swimming
speeds and increase the metabolic cost of silver eel
migration (EELREP 2005).
The observations made on the infection levels
of A. crassus in Lough Ahalia eels (Table 2) suggest
that they were initially introduced to the mixohaline
lower basin and that, as indicated by the
progressively lower infection parameters in the
middle and upper basins, the parasite has been
gradually spreading towards the freshwater areas
upstream. A car parking area adjacent to Screebe
Bridge, where Lough Ahalia discharge connects to
Camus Bay, may have enabled someone transporting
live eels to exchange water in their transport tanks.
This practice was commonly undertaken by
commercial eel dealers in the past. Alternatively,
even though no authorisations have been granted by
the fishery owner or licenses issued for that area by
the Western Regional Fishery Board for over eight
% frequency
% frequency
n = 121
*
800-899
Variation of Anguillicola crassus intensity with eel length class in middle and lower basin.
(k/0.465) and lower basin (k/0.556) (Fig. 3a
and 3b).
Fig. 3
700-799
2
4
6
8
10 12
Number of A. crassus
14
16
0
2
4
6
8
10 12
Number of A. crassus
14
16
Percentage frequency of Anguillicola crassus in eels from (a) the middle and (b) the lower basin of Lough Ahalia.
THE
OCCURRENCE OF
years, it is known that some illegal fishing for eels
occasionally occurs in the area. It is possible that
transport of eel catches between river basins by such
fishermen resulted in the spread of A. crassus to the
Screebe system. Dispersal by natural mechanisms
from River Corrib basin, where A. crassus is well
established, seems less likely. A cormorant colony
located on an island in the upper basin of Lough
Ahalia might have a role in extending the
distribution of A. crassus through fish regurgitation,
involving infected eels or paratenic hosts, as has been
shown in Polish studies (Wlasow et al. 1998).
However, observations on flight direction adopted
by foraging birds suggest that they do not regularly
forage in the Corrib system. Likewise, though
theoretically possible, it is unlikely that the initial
colonisation of the Screebe River system resulted
from natural movements of infected eels or paratenic
hosts. The need to consider such possibilities is
suggested by recent observations on the variety of
migratory strategies adopted by eel species in which
local movements between waters of differing
salinities can occur throughout the yellow eel
foraging phase of the eel life cycle (Harrod et al.
2005). Eels from Camus Bay examined in this study
(Table 2) were found not to be infected with A.
crassus , suggesting that colonisation of the Lough
Ahalia eel populations did not occur through eels
migrating into the system from the marine
environment. The spread of A. crassus within the
system may have been facilitated by the natural
movement of eels between the Lough Ahalia basins
(Harrod et al. 2005).
Parasite infections typically vary among size
classes of their fish hosts, and differences in
transmission rates often reflect ontogenic trophic
niche shifts. Various studies have shown that larger
eels tend to have higher numbers of A. crassus than
smaller eels (Audenaert et al . 2003; Schabuss et al.
2005). However, in the Lough Ahalia middle basin
samples, A. crassus abundance was negatively
correlated with eel size. This may reflect unusual
features of the habitat and the trophic ecology of its
eels. Piscivory is typical of eels greater than 50cm in
length in many freshwater habitats. However,
limited observations on stomach contents of the
eels captured in the marine and mixohaline habitats
sampled in Camus Bay and Lough Ahalia suggests
that larger prey items are more likely to be crabs,
such as the euryhaline Carcinus maenas . Larger eels
typically do not feed directly on copepods, such as
those bearing infective A. crassus larvae, but can be
infected by preying on fish fry containing numerous
recently ingested copepods (Kirk 2003).
Unlike most European habitats colonised by
A. crassus , the Screebe system is characterised by
having relatively species-poor fish assemblages. In
this respect it is typical of smaller western Irish
ANGUILLICOLA
CRASSUS
rivers and lakes, where cyprinids and other nonindigenous coarse fish are generally absent. Results
of stable isotope analyses of eels from the three
basins of Lough Ahalia suggested that the trophic
niche occupied by eels in the middle basin was
narrower than either of the other basins (Harrod
et al. 2005). This may be due to limited fish prey,
although it may also reflect food web changes
associated with the presence of salmon-rearing
cages in that lake basin.
Interestingly males had more parasites than
females of the same size class in the middle basin.
However, whether this resulted from differences in
trophic ecology, inter-habitat movements or other
factors is unclear. Several of the euryhaline species
present in the lower basin and in nearby Camus
Bay, are listed among the more than 37 species
recorded as paratenic hosts for A. crassus (Höglund
and Thomas 1992; Szekely 1994; Kirk 2003). The
higher prevalence of A. crassus in the lower basin of
Lough Ahalia may be due to ingestion of infected
paratenic hosts by eels.
The absence of A. crassus in the eels sampled in
Camus Bay may be explained by research that has
shown that the parasite prefers lower salinities
(Kennedy and Fitch 1990). However, adult
nematodes can survive within eels in the marine
environment by osmoconforming with the blood
plasma of the eel (Kirk et al . 2002), so their absence
from Camus Bay may not be entirely due to salinity.
A further explanation may be the lack of available
intermediate hosts, which is a known factor to
limiting the spread of A. crassus (Kirk et al. 2000).
Concerns have been expressed about the
negative impact A. crassus may have on the
capacity of eels to undertake their oceanic
spawning migrations. It has been suggested that
A. crassus parasitism may be contributing to the
dramatic decline that has occurred in European eel
stocks in recent decades (Køie 1991). Therefore,
more systematic analyses of dispersal and pathogenic
effects are needed. As indicated by Kirk 2003,
relatively little is known about A. crassus in coastal
and brackish water habitats, with the exception of
studies on exploited Baltic eel populations and
some other local studies on estuarine habitats.
McCarthy et al. (in press) reviewed available
information on parasites of Irish eels and
highlighted the need for parasitological research
on eels in marine and mixohaline waters. The
results of the present study, while providing new
information on this species in Ireland and
contributing to knowledge of eel ecology in
mixohaline waters, also suggest that further
investigations on A. crassus transmission in such
habitats are needed.
17
BIOLOGY
AND
ACKNOWLEDGEMENTS
This study was funded as part of the HEA-PTRLI
Cycle 3 project Population Biology of Eels in
Marine and Mixohaline Waters. We would like to
thank Dr Chris Harrod for help with fieldwork and
the Screebe Fishery for allowing us to sample the
eel populations of Lough Ahalia.
REFERENCES
Anderson, R.M. and Gordon, D.M. 1982 Processes
influencing the distribution of parasite numbers
within host populations with special emphasis on
parasite-induced host mortalities. Parasitology 85,
373 98.
Audenaert, V., Huyse, T., Goemans, G., Belpaire, C. and
Volckaert, F.A.M. 2003 Spatio-temporal dynamics
of the parasitic nematode Anguillicola crassus in
Flanders, Belgium. Diseases of Aquatic Organisms
56, 223 33.
Beullens, K., Eding, E.H., Gilson, P., Ollevier, F.,
Komen, J. and Richter, C.J.J. 1997 Gonadal
differentiation, intersexuality and sex ratios of
European eel (Anguilla anguilla ) maintained in
captivity. Aquaculture 153, 135 50.
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W.
1997 Parasitology meets ecology on its own terms:
Margolis et al . revisited. Journal of Parasitology 83,
575 83.
EELREP 2005 Final report: estimation of the
reproduction capacity of European eel. pp. 272.
(EU-project EELREP (Q5RS-2001-01836)).
Evans, D.W. and Matthews, M.A. 1999 Anguillicola
crassus
(nematoda,
Dracunculoidea);
first
documented record of this swimbladder parasite in
eels in Ireland. Journal of Fish Biology 55, 665 8.
Gollock, M.J., Kennedy, C.R., Quabius, S.E. and
Brown, A.J. 2004 The effect of parasitism of
European eels with the nematode, Anguillicola
crassus , on the impact of netting and arial
exposure. Aquaculture 233, 45 54.
Harrod, C., Grey, J., McCarthy, T.K. and Morrissey, M.
2005 Stable isotope analyses provide new insights
into ecological plasticity in a mixohaline population
of European eel. Oecologia 144, 673 83.
Healy, B. 2003 Coastal lagoons. In M.L. Otte (ed.),
Wetlands of Ireland. Distribution, ecology and economic
value , 51 78. Dublin. University College Dublin.
Höglund, J. and Thomas, K. 1992 The black goby Gobius
niger as a potential paratenic host for the parasitic
nematode Anguillicola crassus in a thermal effluent of
the Baltic. Diseases of aquatic organisms 13, 175 80.
Kennedy, C.R. and Fitch, D.J. 1990 Colonization,
larval survival and epidemology of the nematode
18
ENVIRONMENT
Anguillacola crassus, parasitic in the eel, Anguilla
anguilla , in Britain. Journal of Fish Biology 36,
117 31.
Kirk, R.S. 2003 The impact of Anguillicola crassus on
European eels. Fisheries Management and Ecology 10,
385 94.
Kirk, R.S., Lewis, J. W. and Kennedy, C.R. 2000
Survival and transmission of Anguillicola crassus
Kuwahara, Niimi and Itagaki, 1974 (Nematoda) in
seawater eels. Parasitology 120, 289 95.
Kirk, R.S., Morritt, D., Lewis, J.W. and Kennedy, C.R.
2002 The osmotic relationship of the swimbladder
nematode Anguillicola crassus with seawater eels.
Parasitology 124, 339 47.
Køie, M. 1991 Swimbladder nematodes (Anguillicola
spp.) and gill monogeneans (Pseudodactylogyrus
spp.) parasitic on the European eel (Anguilla
anguilla ). Journal du Conseil International pour
l’Exploration de la Mer 47, 391 8.
McCarthy, T.K., Creed, K., Naughton, O., Cullen, P.
and Copley, L. in press The metazoan parasites of
eels (Anguilla anguilla ) in Ireland: zoogeographical,
ecological and fishery management perspectives.
In J. Casselman and D. Cairns (eds), American
Fisheries Society Symposium series.
McCarthy, T.K., Cullen, P. and O’Connor, W. 1999
The biology and management of River Shannon eel
populations. Fisheries Bulletin (Dublin) 17.
Molnár, K., Baska, F., Csaba, G., Glávatis, R. and
Székely, C. 1993 Pathological and histopathological studies of the swimbladder of eels
Anguilla anguilla infected by Anguillicola crassus
(Nematoda:Dranunculoidea). Diseases of Aquatic
Organisms 15, 41 50.
Neumann, W. 1985 Schwimmblasenparasit Anguillicola
bei Aalen. Fischer Teichwirt 11, 322.
Rózsa, L., Reiczigel, J. and Majoros, G. 2000
Quantifying parasites in samples of hosts. Journal of
Parasitology 86, 228 32.
Schabuss, M., Kennedy, C.R., Konecny, R., Grillitsch,
B., Reckendorfer, W., Schiemer, F. and Herzig, A.
2005 Dynamics and predicted decline of Anguillicola
crassus infection in European eels, Anguilla anguilla ,
in Neusiedler See, Austria. Journal of Helminthology
79, 159 67.
Szekely, C.S. 1994 Paratenic hosts for the parasitic
nematode Anguillicola crassus in Lake Balaton,
Hungary. Diseases of Aquatic Organisms 18, 11 20.
Wickströem, H., Clevestam, P. and Höglund, J. 1998
The spreading of Anguillicola crassus in freshwater
lakes in Sweden. Bulletin Francais de la Pêche et de la
Pisciculture 349, 215 21.
Wlasow, T., Gomulka, P., Martyniak, A., Boron, S.,
Hliwa, P., Terelecki, J. and Szymanska, U. 1998
Anguillicola crassus larvae in cormorant’s prey fish in
Vistula Lagoon, Poland. Bulletin Francais de la Pêche et
de la Pisciculture 349, 223 7.