distribution, prevalence and intensity of anguillicola crassus (nematoda) infection in anguilla...

Journal of Fish Biology (2014)

doi:10.1111/jfb.12344, available online at wileyonlinelibrary.com

Distribution, prevalence and intensity of Anguillicolacrassus (Nematoda) infection in Anguilla anguilla in the

Republic of Ireland

G. Becerra-Jurado*†, R. Cruikshanks*, C. O’Leary*, F. Kelly*,R. Poole‡ and P. Gargan*

*Inland Fisheries Ireland, Research Section, Swords Business Campus, Swords, Co. Dublin,Ireland and ‡Marine Institute, Furnace, Newport, Co. Mayo, Ireland

(Received 13 August 2013, Accepted 14 January 2014)

This study is the first comprehensive documentation of the geographical range of Anguillicola crassusin its host, the European eel Anguilla anguilla, in the Republic of Ireland. The prevalence and intensityof infections across 234 sites and 93 river basins in Ireland comprising rivers, lakes and transitionalwaters (estuaries) were analysed. While only 32% of the river basins were affected by this nematode,they correspond to 74% of the total wetted area. Significant differences in infection levels among waterbody types were found with lakes and transitional waters yielding the highest values, which can beattributed to the proportions of juvenile (total length, LT < 300 mm) A. anguilla caught. There were nosignificant differences in infection levels between water body types for adult A. anguilla or betweensexes for any water body type. Prevalence was significantly lower in juvenile compared with adultA. anguilla captured in rivers and a positive correlation between infection levels and host size-classeswas found. Future efforts should focus on monitoring the spread of A. crassus infections and assessingthe swimbladder health of A. anguilla in Ireland.

© 2014 The Fisheries Society of the British Isles

Key words: eel parasites; European eel; infestation; pathology; swimbladder.

INTRODUCTION

Many studies have focused on the infection of Anguillicola crassus in the European eelAnguilla anguilla (L. 1758) (Naismith & Knights, 1993; Lefebvre et al., 2002; Nortonet al., 2005; Neto et al., 2010). In the Republic of Ireland, infections of A. crassus havebeen reported previously in a limited number of river basins and it was only in 1997that it was first recorded in Waterford Estuary (McCarthy et al., 1999). The parasitewas subsequently recorded in the Erne (Evans & Matthews, 1999; Evans et al., 2001),Shannon, Barrow, Nore, Suir and Slaney river basins (McCarthy et al., 1999), as wellas in Lough Ahalia and Camus Bay in the west of Ireland (Morrissey & McCarthy,2007). The most geographically extensive study in Ireland presented only presence orabsence information on a limited number of sites (McCarthy et al., 2009).

This swimbladder parasite may hinder the stock recovery of A. anguilla (Van Banning& Haenen, 1990; Molnár et al., 1993), a fish species classified as critically endangered

†Author to whom correspondence should be addressed. Tel.: +353 1 8842611 email: [email protected]

1

© 2014 The Fisheries Society of the British Isles

2 G . B E C E R R A- J U R A D O E T A L.

in the IUCN Red List of Threatened Species (Freyhof & Kottelat, 2010). The needfor the adoption of a national approach focusing on the geographical range of infec-tions became apparent in 2008 with the commencement of the National Eel MonitoringProgramme in Ireland. The National Eel Monitoring Programme is a three-year cycleprogramme that was created in response to the EC regulation (E.U., 2007) establishingmeasures for the recovery of A. anguilla. This regulation required Ireland to establisha management plan with the aim of reducing A. anguilla mortality and ensuring anincrease in the number of A. anguilla escaping to spawn. One of the monitoring objec-tives was to determine the extent of A. crassus infections in the country, including themost important river basins and water body types for A. anguilla.

In the European context, efforts are being made to collate A. crassus infection data aspartofaEuropeanEelQualityDatabase (Belpaireetal., 2011).Thisdatabasewascreatedas an initiative within the Joint EIFAC/ICES Working Group on Eels whereby a numberof European countries agreed to provide data on A. crassus infections. Data collectionis in progress with studies either focussing on the monitoring of the parasite in a limitednumber of sites (e.g. one water body over 21 years; Bernies et al., 2011) or on its geo-graphical range (e.g. 11 sites; Popielarczyk et al., 2012). As far as is known, no extensivestudy on A. crassus has been undertaken at a national scale. This study provides an inter-national reference for future studies on the geographical range and infection levels of A.crassus and represents a baseline dataset against which any changes can be compared.

MATERIALS AND METHODS

S T U DY A R E ASampling of A. anguilla populations for the presence of A. crassus was undertaken at 234 sites

in 93 river basins with a wide geological range. Transboundary river basins shared with North-ern Ireland were included. The river basins represent 88⋅6% of the total wetted area in Ireland(McGinnity et al., 2003). Sampling took place in lakes, rivers and transitional waters (estuaries).All river basins known to contribute considerably to A. anguilla production were sampled.

S A M P L I N G A N D L A B O R AT O RY W O R KA total of 3408 A. anguilla individuals were collected during the 3 year period 2008–2010

under the National Eel Monitoring Programme and the Water Framework Directive (E.U.,2000) Fish Monitoring Programme. Sampling took place from June to October annually. Lakesand rivers were typically sampled first, during June to September, followed by transitionalwaters in October. Lakes and transitional waters were sampled using chains of either three orfive Dutch fyke nets (knot to knot mesh size ranging from 18 mm for the leader net to 11 mmfor the cod end) set at multiple locations. Nets were normally set overnight and net locationswere randomly selected.

Rivers were surveyed by electrofishing. Three fishing runs were conducted in a containedstretch of channel. In channels <0⋅8 m in depth, bankside equipment was used, consisting of ananode with combined landing net, a control box, a portable generator and a cathode. Fishing wascarried out in an upstream direction. In channels >0⋅8 m in depth, fishing was carried out usingboats with either standard or high-voltage equipment. In channels 0⋅8–1⋅5 m in depth, fishingwas carried out using flat-bottomed boats and standard boat fishing gear heading in a downstreamdirection. A typical boat-based electrofishing unit consisted of a generator, control box andcathode, with two anodes and two landing nets. In channels>1⋅5 m in depth, high-voltage equip-ment was used. This system required the use of larger boats and consisted of a high-poweredgenerator, control box and cathode. The number of anodes and landing nets used varied. Wherepossible, all habitat types (i.e. riffle, glide and pool) were sampled.

© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, doi:10.1111/jfb.12344

A N G U I L L I C O L A C R A S S U S R A N G E I N I R E L A N D 3

An overdose of chlorobutanol was used to kill A. anguilla. The number of A. anguilla indi-viduals collected per site was subject to availability. Total length (LT) was recorded on freshspecimens and fish were frozen (−20∘ C) for later dissection when the swimbladder was removedand all A. crassus present in the swimbladder lumen (pre-adult and adult forms, regardless ofsex) were counted macroscopically. Examination of swimbladder walls for the presence of theparasite was not conducted. Sex determination of A. anguilla was carried out by macroscopicobservation of gonads (Beullens et al., 1997). Anguilla anguilla with LT < 300 mm were classi-fied as juveniles as they were generally shown to have undifferentiated or intersexual gonads.

DATA A NA LY S I S

The full dataset was used to determine the geographical distribution of A. crassus infection inIreland but to allow representative comparisons, a sample size >5 (mean= 28⋅2, range= 6–110)A. anguilla was used to map the site prevalence and mean intensity of A. crassus, as well as tocompare differences in infection in the Irish A. anguilla population.

Datasets were tested for normality (Kolmogorov–Smirnov K–S test; P> 0⋅05) and homo-geneity of variances (Levene test; P> 0⋅05) (Field, 2005). Differences in prevalence (Pearson 𝜒2

test) and intensity of A. crassus in the A. anguilla population among water body types, betweenjuvenile and adult (male and female) A. anguilla, as well as between sexes (Kruskal–Wallisand Mann–Whitney U-tests) were tested. Correlations between prevalence and mean intensityof A. crassus, and LT classes were also investigated. Due to data constraints (i.e. the selectivenature of fyke nets), these correlations were carried out for fish captured in all water body types(pooled data) and for fish captured in rivers only. In addition, differences in infection levelsbetween juvenile and adult (male and female) A. anguilla were only conducted for fish capturedin rivers. Bonferroni adjustment was carried out on Pearson 𝜒2 and Mann–Whitney U-tests tokeep the significance level (Field, 2005). All statistical analyses were carried out using PASWStatistics 18 (www.spss.com.hk/statistics).

RESULTS

G E O G R A P H I C A L D I S T R I B U T I O N O F A . C R A S S U S I N F E C T I O N

The presence or absence of A. crassus at 234 sites in the 93 river basins studied isshown in Fig. 1. A total of 93 sites (40% of those surveyed) in 30 river basins (32% ofthose surveyed) contained infected A. anguilla. These river basins corresponded to 74%of the wetted area in Ireland and include the largest river basins: Erne, Moy, Corrib,Shannon, Boyne, Barrow, Nore, Suir and Blackwater. In contrast, the south-westernareas of Ireland, as well as a large number of mostly small coastal river basins dis-tributed throughout Ireland, were parasite-free.

P R E VA L E N C E A N D I N T E N S I T Y

Most infected sites had prevalences >50% (median= 51⋅5%), ranging from 2⋅0 to100% (Fig. 2 and Appendix). The highest prevalences were found on Urlaur Lough,Co. Mayo (100%, n= 6), Tacumshin Lake, Co. Wexford (85⋅7%, n= 7), CorglassLough, Co. Cavan (83⋅3%, n= 6), Lower Lough Corrib, Co. Galway (83⋅3%, n= 6)and the River Barrow (Pass Bridge), Co. Kildare (83⋅3%, n= 6). Most infected siteshad mean intensity values of >3 (median= 3⋅72), ranging from 1 to 24⋅50 (Fig. 3).The highest mean intensities were generally located in western sites, although someeastern and south-eastern sites also had high mean intensity values. The highest meanintensity values were found on Camus Bay, Co. Galway (mean= 24⋅50, n= 8), UrlaurLough, Co. Mayo (mean= 16⋅33, n= 6), Lough Cullin, Co. Mayo (mean= 13⋅92,



N

100

Blackwater

Suir

Nore

Barrow

Boyne

ShannonCorrib

Moy

Erne

50250km

Fig. 1. Presence or absence of Anguillicola crassus at individual sites per water body type ( , lakes presence; ,lakes absence; , rivers presence; , rivers absence; , transitional waters presence; , transitional watersabsence) in river basins ( ) in Ireland. Areas not sampled ( ) are shown.



N

100

2

5

4

1

3

50250km

Rosslare port

Fig. 2. Prevalence (%) of Anguillicola crassus at individual sites ( , 0; , <20⋅0; , 20⋅0–39⋅9; , 40⋅0–59⋅9;

, 60⋅0–79⋅9; ,>79⋅9) in river basins ( ), as well as location of Rosslare Port, Ireland, where 1=UrlaurLough, 2=Tacumshin Lake, 3=Corglass Lough, 4=Lower Lough Corrib and 5=River Barrow (PassBridge). Only sites with a sample size> 5 Anguilla anguilla are shown. Locations of 1997–1999 ( ) and2003–2004 ( ) A. crassus records (Evans & Matthews, 1999; McCarthy et al., 1999; Evans et al., 2001;Morrissey & McCarthy, 2007; McCarthy et al., 2009), and the most likely entry point of the parasite intoIreland (Rosslare Port) are included.



n= 99), Lower Shannon Estuary, Co. Clare (mean= 11⋅00, n= 6) and Lough Gill(mean= 9⋅30, n= 32).

Water body typesThe per cent of juvenile A. anguilla caught was 0⋅4% for lakes, 70⋅3% for rivers

and 8⋅8% for transitional waters. These percentages differed significantly among waterbody types (Pearson 𝜒2, d.f. = 2, P< 0⋅001). Specifically, differences in the per centof juvenile A. anguilla caught were detected between all water body types (rivers v.lakes: Pearson 𝜒2, d.f. = 1, P< 0⋅05, rivers v. transitional waters: Pearson 𝜒2, d.f. = 1,P< 0⋅05, lakes v. transitional waters: Pearson 𝜒2, d.f. = 1, P< 0⋅05).

The per cent of infected sites for the three water body types was between 38 and 46%(Table I). There was a significant difference in prevalence among the A. anguilla popu-lation of the three water body types (Pearson 𝜒2, d.f. = 2, P< 0⋅001). Anguilla anguillacaptured in rivers had a lower prevalence rate compared with those captured in lakesand transitional waters (rivers v. lakes: Pearson 𝜒2, d.f. = 1, P< 0⋅05, rivers v. transi-tional waters: Pearson 𝜒2, d.f. = 1, P< 0⋅05), but there was no difference in prevalencebetween A. anguilla captured in lakes and those captured in transitional waters (lakesv. transitional waters: Pearson 𝜒2, d.f. = 1, P> 0⋅017). When juvenile A. anguilla wereremoved from the analysis, there was no significant difference in prevalence amongthe A. anguilla population of the water body types (Pearson 𝜒2, d.f. = 2, P > 0⋅05).

Differences in infection intensities of A. crassus in the A. anguilla population amongwater body types were significant (Kruskal–Wallis, d.f. = 2, P< 0⋅001). Differencesin infection intensities between A. anguilla captured in rivers and those capturedin lakes, as well as between A. anguilla captured in rivers and those captured intransitional waters, were significant (rivers v. lakes: Mann–Whitney U-test, d.f. = 1,P< 0⋅05, rivers v. transitional waters: Mann–Whitney U-test, d.f. = 1, P< 0⋅05), butthere was no difference in infection intensity between A. anguilla captured in lakesand those captured in transitional waters (lakes v. transitional waters: Mann–WhitneyU-test, d.f. = 1, P> 0⋅05). As in the case of prevalence, no statistical differences wereobtained when juvenile A. anguilla were removed from the analysis (Kruskal–Wallis,d.f. = 2, P >0⋅05).

LT and sexSignificant positive correlations were obtained between prevalence and host

size-classes (all water body types: correlation, d.f. = 10, r = 0⋅91, P< 0⋅001, rivers:correlation, d.f. = 14, r = 0⋅85, P< 0⋅001), as well as between mean intensity and hostsize-classes (all water body types: correlation, d.f. = 10, r = 0⋅69, P< 0⋅05, rivers:correlation, d.f. = 14, r = 0⋅72, P< 0⋅01) for both A. anguilla captured in all waterbody types and for A. anguilla captured in rivers only (Table II). Differences betweenjuvenile and adult (male and female) A. anguilla were significant in terms of prevalence(rivers: Pearson 𝜒2, d.f. = 1, P< 0⋅001) and, although not significant, approachedsignificance in terms of intensity (rivers: Mann–Whitney U-test, d.f. = 1, P> 0⋅05).

No differences were found in A. crassus infection between male and female A.anguilla captured in any water body type both in terms of prevalence (lakes: Pearson𝜒2, d.f. = 1, P > 0⋅017, rivers: Pearson 𝜒2, d.f. = 1, P > 0⋅017, transitional waters:Pearson 𝜒2, d.f. = 1, P > 0⋅017) and intensity (lakes: Mann–Whitney U-test, d.f. = 1,P > 0⋅017, rivers: Mann–Whitney U-test, d.f. = 1, P > 0⋅017, transitional waters:Mann–Whitney U-test, d.f. = 1, P > 0⋅017).



100

2

4

1

3

5

Rosslare port

50250km

N

Fig. 3. Mean intensity of Anguillicola crassus at individual sites ( , 0; , 1⋅00–1⋅99; , 2⋅00–2⋅99; ,

3⋅00–4⋅99; , 5⋅00–6⋅99; , >6⋅99) in river basins ( ), as well as location of Rosslare Port in Ireland,where 1=Camus Bay, 2=Urlaur Lough, 3=Lough Cullin, 4=Lower Shannon Estuary and 5=LoughGill. Only sites with a sample size> 5 Anguilla anguilla are shown. Locations of 1997–1999 ( ) and2003–2004 ( ) A. crassus records (Evans & Matthews, 1999; McCarthy et al., 1999; Evans et al., 2001;Morrissey & McCarthy, 2007; McCarthy et al., 2009), and the most likely entry point of the parasite intoIreland (Rosslare Port) are included.



Tab

leI.

Num

ber

and

per

cent

ofin

fect

edsi

tes

and

Ang

uill

aan

guil

la,p

reva

lenc

ean

din

tens

itype

rw

ater

body

type

.Onl

ysi

tes

with

sam

ple

size

>5

are

incl

uded

Inte

nsity

Inte

nsity

(juv

enile

A.

angu

illa

not

incl

uded

)W

ater

body

type

Num

ber

of site

sIn

fect

edsi

tes

(%)

Num

ber

ofA

.ang

uill

aan

dnu

mbe

rof

infe

cted

indi

vidu

als

from

infe

cted

site

sPr

eval

ence

(%)

Prev

alen

ce(%

)(j

uven

ileA

.an

guil

lano

tin

clud

ed)

Ran

geM

ean±

s.d.

Med

ian

Ran

geM

ean±

s.d.

Med

ian

Lak

e59

27(4

6)10

25(5

95)

58⋅0

58⋅1

1–

626⋅

02±

7⋅91

31

–62

6⋅00

±7⋅

913

Riv

er51

21(4

1)41

9(1

08)

25⋅8

51⋅0

1–

203⋅

22±

3⋅04

21

–20

4⋅07

±3⋅

833

Tra

nsiti

onal

Wat

er29

11(3

8)22

7(1

15)

50⋅7

52⋅0

1–

455⋅

33±

6⋅41

31

–45

5⋅50

±6⋅

693

Juve

nile

A.a

ngui

lla,

indi

vidu

als

tota

llen

gth,

LT<

300

mm

.



Tab

leII

.Pr

eval

ence

and

mea

nin

tens

ityof

Ang

uill

icol

acr

assu

sin

Ang

uill

aan

guil

lafr

omal

lwat

erbo

dyty

pes

(poo

led

data

)an

dri

vers

only

per

tota

lle

ngth

(LT)

clas

s

All

wat

erbo

dyty

pes

(poo

led

data

)R

iver

son

ly

LT

clas

s(m

m)

Mea

nL

T(m

m)

Prev

alen

ce(%

)M

ean

inte

nsity

±s.

d.L

Tcl

ass

(mm

)M

ean

LT

(mm

)Pr

eval

ence

(%)

Mea

nin

tens

ity±

s.d.

<20

015

77⋅

11⋅

60±

0⋅84

<17

514

24⋅

41⋅

80±

0⋅84

200

–24

922

616

⋅22⋅

27±

1⋅49

175

–19

918

712

⋅11⋅

40±

0⋅89

250

–29

927

629

⋅82⋅

81±

2⋅04

200

–22

421

311

⋅11⋅

50±

0⋅58

300

–34

932

642

⋅45⋅

00±

4⋅33

225

–24

923

918

⋅92⋅

33±

1⋅51

350

–39

937

450

⋅85⋅

10±

5⋅75

250

–27

426

121

⋅63⋅

00±

1⋅87

400

–44

942

254

⋅34⋅

77±

5⋅98

275

–29

928

725

⋅62⋅

33±

1⋅21

450

–49

947

255

⋅85⋅

72±

6⋅39

300

–32

431

218

⋅91⋅

78±

0⋅67

500

–54

952

356

⋅06⋅

72±

9⋅49

325

–34

933

529

⋅33⋅

00±

1⋅79

550

–59

957

160

⋅46⋅

41±

9⋅10

350

–37

436

241

⋅73⋅

00±

2⋅31

600

–64

962

067

⋅410

⋅87±

14⋅7

737

5–

399

386

33⋅3

4⋅50

±4⋅

5165

0–

699

672

52⋅4

13⋅0

9±

15⋅8

140

0–

424

412

20⋅0

8⋅00

±n.

a.>

699

731

83⋅3

3⋅50

±1⋅

2742

5–

449

440

16⋅7

5⋅00

±n.

a.45

0–

474

460

63⋅6

3⋅57

±2⋅

7047

5–

499

491

58⋅3

6⋅29

±4⋅

7550

0–

524

512

55⋅6

3⋅00

±3⋅

46>

524

568

70⋅0

6⋅00

±6⋅

43



DISCUSSION

The large geographical area covered in this study allows the first comprehensivedocumentation of the range of A. crassus in Ireland. Results showed that 32% of thesurveyed river basins in Ireland are infected with the parasite, corresponding to 74% ofits total wetted area. A total of 219 mainly small coastal river basins were not sampledduring the study and a number of sites were excluded from analyses where sampleswere≤ 5. While few infection details have been published from Northern Ireland todate, it is likely that the parasite is now widely distributed in the area, as the parasitewas first recorded in Lough Neagh in 2003 (McCarthy et al., 2009).

This study showed that A. crassus is present in the largest river basins, which gener-ally correspond to the river basins where A. anguilla was commercially exploited suchas the Shannon, Erne, Corrib and Moy river basins, and also that most south-westernareas showed no infection. The distribution pattern of infections coincides with thestops taken by lorries in their commercial activities with local fishermen, during whichregular uncontrolled water changes took place in the past (McCarthy et al., 2009), apractice also highlighted as being the most likely cause of A. crassus infections inEast Anglia in the U.K. (Kennedy & Fitch, 1990). Several sites in close proximity toRosslare Port, an area of earlier interest (McCarthy et al., 1999, 2009), showed highprevalence. The distribution found, along with the locations of early records of the par-asite in Ireland, indicates that the introduction of A. crassus occurred in a short periodof time at multiple locations such as Lough Derg, Lough Ree and Lough Bofin (Shan-non river basin), Lough Erne (Erne river basin) and Lough Corrib (Corrib river basin),with probable reinfections taking place subsequently.

Various factors may have facilitated the spread of A. crassus starting in the late 1990s.First, the spread across river basins and in some cases between distant locations withinriver basins was probably facilitated by the water exchanges undertaken by commer-cial dealers. In addition, the transport of A. anguilla as a result of illegal fishing mayhave further contributed to its spread. Studies also show that, when a river basin hasbeen infected, the containment of its spread may be difficult as A. crassus can rapidlydisperse via natural movements of infected A. anguilla and, to some degree, via theuse of a wide range of paratenic hosts, piscivorous birds such as cormorants, as wellas recreational boating (Kirk, 2003). Lastly, the spread of A. crassus is also assisted bythe ability of the parasite to survive short periods as a free-living parasite in a range ofhabitat types, with water salinity having a negative effect on egg hatching and larvalsurvival (Kennedy & Fitch, 1990; Kirk et al., 2000) and temperature limiting the spreadand infection levels in boreal regions (Höglund & Andersson, 1993; Knopf et al., 1998;Sjöberg et al., 2009). Information on the distribution of A. crassus infections is scarcein most cases and studies are normally limited to one water body type.

All three water body types studied were infected. It is striking that the geologyof the lake and river sites infected generally corresponds to the calcareous areas ofIreland such as the central area, and some parts in the west and north-west (Holland &Sanders, 2009). The general characteristics of the infected sites suggest that the spreadof infection occurrences has been greatly facilitated by the high population densityof A. anguilla present at these productive calcareous areas (DCENR, 2008) and thehigh degree of existent surface water connectivity. In contrast, sparsely populated andrelatively isolated non-calcareous areas such as the south-west and some parts in theeast, characterized by high slopes and the potential presence of barriers do not appear



to have been infected, as natural movements of A. anguilla individuals from infectedareas to these locations are greatly limited and A. crassus eggs are likely to be washeddownstream with the flow. Future studies focusing on various environmental factorssuch as proportion of river basin comprising calcareous geology, as well as surfacewater connectivity, would be necessary to analyse their role in the occurrence of theparasite in A. anguilla across its geographical distribution.

Lakes, but also transitional waters, were highlighted as yielding the highest infec-tion values compared to rivers. Similar results were found in a study by Taraschewskiet al. (1987) who showed that A. crassus had the highest prevalence and mean inten-sity values in the Ruhr Lake, compared to a number of river and transitional watersites. A further study would be required to establish the effect of A. anguilla feedinghabits and general productivity of the various water body types on A. crassus infectionlevels.

The differences in infection levels found between juvenile (i.e. LT < 300 mm) andadult (male and female) A. anguilla had a clear effect on these results. Not only didthe results show that the proportion of juvenile A. anguilla caught was statisticallydifferent among water body types, but also that no statistical differences in infectionlevels were found among water body types when juvenile A. anguilla were removedfrom the analyses. In addition, significant positive correlations were obtained betweenprevalence and mean intensity, and host size-classes. These findings agree with otherstudies showing that larger A. anguilla have a longer exposure time to the parasite, alarger swimbladder (i.e. higher harbouring capacity) and potentially different feedinghabits compared with smaller A. anguilla (Lefebvre et al., 2002; Neto et al., 2010).Further analyses would be required to study the effect of these factors on the infectionlevels of A. crassus in the A. anguilla population in Ireland, including an examinationof swimbladder walls for encapsulated A. crassus.

There were no differences between A. anguilla captured in lakes and transitionalwaters (both sampled using fyke netting and analyses including juvenile A. anguilla)in terms of prevalence and intensity. This indicated that, despite the potential differ-ences in water salinity, differences in infection levels between A. anguilla present inthese two water body types did not occur within the selectivity range of fyke netting(cod end knot to knot mesh size= 11 mm), i.e. generally A. anguilla with LT > 250 mm(Bevacqua et al., 2009). In this regard, the higher densities of A. anguilla normallypresent in transitional waters compared to other water body types located some dis-tance from the tidal limit (Naismith & Knights, 1993; Laffaille et al., 2003; Domingoset al., 2006; Imbert et al., 2008) may have offset the effect of salinity on infection lev-els. Nevertheless, the wide range of existing salinity conditions in the transitional watersites of this study may have influenced the results. Future studies should consider thegeographical scale and the salinity gradient at which the study is conducted, as somestudies have suggested that a smaller geographic scale may be necessary to detect theeffect of salinity on A. crassus infections (Lefebvre et al., 2002; Norton et al., 2005;Morrissey & McCarthy, 2007).

Despite the closure of the commercial fishery of A. anguilla in Ireland under theNational Eel Management Plan in 2009, this study has shown that the distributionof A. crassus in the country is widespread. As health status constitutes a key aspectin the conservation of A. anguilla, future efforts should focus on monitoring thespread of A. crassus infections and assessing the swimbladder health of A. anguilla inIreland.



This study was carried out under the National Eel Monitoring Programme and the WaterFramework Directive (2000/60/EC) Fish Monitoring Programme, funded by the Departmentof Communications, Energy and Natural Resources of Ireland. We would like to thank all thestaff involved in this study, including the Water Framework Directive Team, for assisting duringfieldwork and contributing with samples. We would also like to thank two anonymous refereesfor their valuable comments on a draft of this manuscript.

References

Belpaire, C., Geeraerts, C., Evans, D., Eleonora, C. & Poole, R. (2011). The European eel qualitydatabase: towards a pan-European monitoring of eel quality. Environmental Monitoringand Assessment 183, 273–284.

Bernies, D., Brinker, A. & Daugschies, A. (2011). An invasion record for the swimblad-der nematode Anguillicoloides crassus in European eel Anguilla anguilla in a deepcold-monomictic lake, from invasion to steady state. Journal of Fish Biology 79,726–746.

Beullens, K., Eding, E. H., Gilson, P., Ollevier, F., Komen, J. & Richter, C. J. J. (1997). Gonadaldifferentiation, intersexuality and sex ratios of European eel (Anguilla anguilla L.) main-tained in captivity. Aquaculture 153, 135–150.

Bevacqua, D., De Leo, G. A., Gatto, M. & Melià, P. (2009). Size selectivity of fyke nets forEuropean eel Anguilla anguilla. Journal of Fish Biology 74, 2178–2186.

DCENR (2008). National Report for Ireland on Eel Stock Recovery Plan, Including River BasinDistrict Eel Management Plans. Dublin: Department of Communications, Energy andNatural Resources.

Domingos, I., Costa, J. L. & Costa, M. J. (2006). Factors determining length distribution andabundance of the European eel, Anguilla anguilla, in the River Mondego (Portugal).Freshwater Biology 51, 2265–2281.

Evans, D. W. & Matthews, M. A. (1999). Anguillicola crassus (Nematoda: Dracunculoidea);first documented record of this swim bladder parasite of eels in Ireland. Journal of FishBiology 55, 665–668.

Evans, D. W., Matthews, M. A. & McClintock, C. A. (2001). The spread of the eel swimbladdernematode Anguillicola crassus through the Erne system, Ireland. Journal of Fish Biology59, 1416–1420.

Field, A. (2005). Discovering Statistics Using SPSS, 2nd edn. London: Sage.Höglund, J. & Andersson, J. (1993). Prevalence and abundance of Anguillicola crassus in the

European eel (Anguilla anguilla) at a thermal discharge site on the Sweden coast. Journalof Applied Ichthyology 9, 115–122.

Holland, C. H. & Sanders, I. S. (2009). The Geology of Ireland. Edinburgh: Dunedin AcademicPress.

Imbert, H., de Lavergne, S., Gayou, F., Rigaud, C. & Lambert, P. (2008). Evaluation of rela-tive distance as new descriptor of yellow European eel spatial distribution. Ecology ofFreshwater Fish 17, 520–527.

Kennedy, C. R. & Fitch, D. J. (1990). Colonization, larval survival and epidemiology of thenematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain. Journalof Fish Biology 36, 117–131.

Kirk, R. S. (2003). The impact of Anguillicola crassus on European eels. Fisheries Managementand Ecology 10, 385–394.

Kirk, R. S., Kennedy, C. R. & Lewis, J. W. (2000). Effect of salinity on hatching, survivaland infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Diseases ofAquatic Organisms 40, 211–218.

Knopf, K., Würtz, J., Sures, B. & Taraschewski, H. (1998). Impact of low water temperature onthe development of Anguillicola crassus in the final host Anguilla anguilla. Diseases ofAquatic Organisms 33, 143–149.

Laffaille, P., Feunteun, E., Baisez, A., Robinet, T., Acou, A., Legault, A. & Lek, S. (2003).Spatial organisation of European eel (Anguilla anguilla L.) in a small catchment. Ecologyof Freshwater Fish 12, 254–264.



Lefebvre, F., Contournet, P., Priour, F., Soulas, O. & Crivelli, A. J. (2002). Spatial and temporalvariation in Anguillicola crassus counts: results of a 4 year survey of eels in Mediter-ranean lagoons. Diseases of Aquatic Organisms 50, 181–188.

McCarthy, T. K., Cullen, P. & O’Connor, W. (1999). The biology and management of RiverShannon eel populations. Fisheries Bulletin (Dublin) 17, 9–20.

McCarthy, T. K., Creed, K., Naughton, O., Cullen, P. & Copley, L. (2009). The Metazoan para-sites of eels in Ireland: zoogeographical, ecological and fishery management perspectives.In Eels at the Edge (Casselman, J. & Cairns, D., eds), pp.175–187. American FisheriesSociety Symposium 58.

McGinnity, P., Gargan, P., Roche W., Mills, P. & McGarrigle, M. (2003). Quantification of thefreshwater salmon habitat asset in Ireland using data interpreted in a GIS platform. IrishFreshwater Fisheries Ecology and Management Series No.3. Dublin: Central FisheriesBoard.

Molnár, K., Baska, F., Csaba, G. Y., Glávits, R. & Székely, C. S. (1993). Pathological andhistopathological studies of the swimbladder of eels (Anguilla anguilla) infected withAnguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15,41–50.

Morrissey, M. & McCarthy, T. K. (2007). The occurrence of Anguillicola crassus (Kuwahar,Nimi, and Hagaki, 1974), an introduced nematode, in an unexploited western Irish eelpopulation. Biology and Environment: Proceedings of the Royal Irish Academy 107B,13–18.

Naismith, I. A. & Knights, B. (1993). The distribution, density and growth of the Europeaneel, Anguilla anguilla, in the freshwater catchment of the River Thames. Journal of FishBiology 42, 217–226.

Neto, A. F., Costa, J. L., Costa, M. J. & Domingos, I. (2010). Epidemiology and pathologyof Anguillicoloides crassus in European eel Anguilla anguilla from the Tagus estuary(Portugal). Diseases of Aquatic Organisms 88, 225–233.

Norton, J., Rollinson, D. & Lewis, J. W. (2005). Epidemiology of Anguillicola crassus in theEuropean eel (Anguilla anguilla) from two rivers in southern England. Parasitology 130,679–686.

Popielarczyk, R., Robak, S. & Siwicki, K. A. (2012). Infection of European eel, Anguillaanguilla (L.), with the nematode Anguillicoloides crassus (Kuwahara, Niimi et Itagaki,1974) in Polish waters. Polish Journal of Veterinary Sciences 15, 253–257.

Sjöberg, N. B., Petersson, E., Wickström, H. & Hansson, S. (2009). Effects of the swimbladderparasite Anguillicola crassus on the migration of European silver eels Anguilla anguillain the Baltic sea. Journal of Fish Biology 74, 2158–2170.

Taraschewski, H., Moravec, F., Lamah, T. & Anders, K. (1987). Distribution and morphol-ogy of two helminthes recently introduced into European eel populations: Anguillicolacrassus (Nematoda, Dracunculoidea) and Paratenuisentis ambiguous (Acanthocephala,Tenuisentidae). Diseases of Aquatic Organisms 3, 167–176.

Van Banning, P. & Haenen, O. L. M. (1990). Effect of swimbladder nematode Anguillicola cras-sus in wild and farmed eel, Anguilla anguilla. In Pathology in Marine Science (Perkins,F. O. & Chen, T. C., eds), pp. 317–330. New York, NY: Academic Press.

Electronic Reference

E.U. (2000). Directive 2000/60/EC of the European Parliament and of the Council of 23 October2000 establishing a framework for Community action in the field of water policy. OfficialJournal of the European Communities L 327, 1–72. Available at http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2000:327:0001:0072:EN:PDF (last accessed 24June 2013).

E.U. (2007). Council Regulation (EC) No. 1100/2007 of 18 September 2007 establishing mea-sures for the recovery of the stock of European eel. Official Journal of the EuropeanUnion L 248, 17–23. Available at http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2007:248:0017:0023:EN:PDF (last accessed 24 June 2013).

Freyhof, J. & Kottelat, M. (2010). Anguilla anguilla. IUCN Red List of Threatened Species.Version 2012.2. Available at www.iucnredlist.org (last accessed 24 June 2013).



APPENDIX

Appendix: Presence or absence, prevalence and intensity levels per site of Anguillicola crassusin Anguilla anguilla in Ireland. Only sites with sample size> 5 are included

River basindistrict

Riverbasin Site name

Prevalence(%) Intensity

Numberof A.

anguilla

Neagh-Bann Blackwater Blackwater River 50 3⋅00 6Dee White River 0 0⋅00 6

Castletown Castletown transitionalwaters

0 0⋅00 18

Eastern Boyne Blackwater (Kells) River 25 3⋅67 12Boyne (railway viaduct)

River0 0⋅00 6

Boyne transitionalwaters

40 5⋅60 25

Liffey Liffey (Lucan) River 75 8⋅83 9Ryewater River 0 0⋅00 17Dodder River 0 0⋅00 27

Dargle Dargle River 0 0⋅00 35Nanny Nanny River 0 0⋅00 21Coastal Rogerstown transitional

waters0 0⋅00 10

Coastal Broadmeadowtransitional waters

0 0⋅00 6

Tolka Tolka transitional waters 0 0⋅00 9Lough Dan 0 0⋅00 9Avoca transitional waters 0 0⋅00 20

South Eastern Coastal North Slob Channeltransitional waters

67 6⋅63 12

Coastal Tacumshin transitionalwaters

86 3⋅83 7

Lady’s Islandtransitional waters

0 0⋅00 30

Coastal Lower Slaneytransitional waters

54 4⋅86 13

Slaney Douglas (Ballon) River 29 1⋅50 7Slaney River 0 0⋅00 7

Owenavorragh Owenavorragh River 41 N/A 29Banoge 2 1⋅67 48

Barrow Barrow (Pass Bridge)River

83 2⋅20 6

Gowran River 0 0⋅00 24Waterford transitional

waters60 4⋅20 99

Nore Nore River 53 2⋅81 30Kings River 71 3⋅00 7Suir River 31 2⋅63 26



Appendix: Continued

River basindistrict



Numberof A.

anguilla

Duncormick Duncormick River 0 0⋅00 28Bridgetown transitional

waters0 0⋅00 7

Colligan Colligan River 0 0⋅00 8South Western Blackwater Blackwater River 27 2⋅83 22

Awbeg (Buttevant) River 0 0⋅00 7Upper Blackwater

transitional waters32 8⋅22 28

Coastal Kilkeran Loughtransitional waters

0 0⋅00 12

Glashaboy Glashaboy River 0 0⋅00 16Glashaboy transitional

waters0 0⋅00 15

Lee River 0 0⋅00 29Upper Lee transitional

waters0 0⋅00 8

Bandon Upper Bandontransitional waters

0 0⋅00 6

Argideen Argideen River 0 0⋅00 32Coastal Lough Glenbeg 0 0⋅00 20Blackwater

(Kenmare)Lough Brin 0 0⋅00 23

Carragh Lough Carragh 0 0⋅00 21Lough Acoose 0 0⋅00 21

Laune Lough Leane 0 0⋅00 11Owenreagh River 0 0⋅00 18

Maine Maine River 0 0⋅00 55Shannon Shannon Lough Meelagh 77 5⋅12 23

Lough Urlaur 100 16⋅33 6Lough Cavetown 33 5⋅50 8Lough O’Flynn 14 4⋅00 7Lough Upper Ree 57 6⋅18 49Lough Lower Ree 56 3⋅35 61Lough Upper Derg 62 4⋅72 103Lough Upper Derg 52 4⋅15 66Lough Lower Derg 55 3⋅56 47Lough Lower Derg 46 3⋅42 71Shannon (Battlebridge)

River50 2⋅50 8

Suck (Ballyforan) River 67 4⋅25 6Bow River 0 0⋅00 10Limmerick Docks


Shannon EstuaryNorth

Lower Shannontransitional waters

17 11⋅00 6



Appendix: Continued

River basindistrict



Numberof A.

anguilla

Shannon EstuarySouth

Lough Gur 0 0⋅00 7Maigue River 12 1⋅60 42Owvane River 7 1⋅00 30

Coastal Broadford River 44 1⋅75 9Fergus Lough Buny 0 0⋅00 14

Lough Muckanagh 0 0⋅00 11Lough Callaun 0 0⋅00 8Lough Inchicronan 0 0⋅00 10Lough Dromore 0 0⋅00 6Moyree River 0 0⋅00 12Fergus (Clonroad) River 10 1⋅00 31Fergus transitional

waters33 5⋅00 9

Anagh Glendine River 8 1⋅00 13Owencashla Lough Cam 0 0⋅00 6Tyshe Tyshe (Ardfert) River 0 0⋅00 49

Tyshe River 0 0⋅00 49Feale Feale River 0 0⋅00 6

Smearlagh River 0 0⋅00 7Feale transitional waters 0 0⋅00 21Cashen transitional

waters0 0⋅00 21

Creegh Creegh River 0 0⋅00 8Inagh Lough Lickeen 0 0⋅00 10

Western Corrib Lough Carra 75 3⋅22 12Lough Mask 75 2⋅17 8Lough Maumwee 67 6⋅25 6Lough Upper Corrib 50 2⋅90 103Lough Upper Corrib 41 6⋅33 12Lough Lower Corrib 83 8⋅40 6Lough Lettercraffroe 0 0⋅00 7

Kilcolgan Lough Rea 8 2⋅00 13Coastal Lough Ardderry 27 3⋅00 11

Lough Shindilla 33 1⋅30 18Camus transitional

waters25 24⋅50 8

Lough an Aibhinntransitional waters

38 2⋅17 16

Moy Lough Cullin 77 13⋅90 99Lough Conn 52 7⋅90 110Castlebar River 2 2⋅00 51Deel (Crossmolina)

River55 2⋅50 11



Appendix: Continued

River basindistrict



Numberof A.

anguilla

Garvogue Lough Gill 72 9⋅30 32Bridge Lough


Kinvarra Owendalulleegh River 0 0⋅00 10Coastal Lough Aughrusbeg 0 0⋅00 18Dawros Lough Kylemore 0 0⋅00 14

Lough Glencullin 0 0⋅00 33Newport Lough Beltra 0 0⋅00 22Srahmore Lough Feeagh 0 0⋅00 6Glenamoy Glenamoy River 0 0⋅00 27

Sruwaddacontransitional waters

0 0⋅00 31

Ballinglen Ballinglen River 0 0⋅00 28Easky Lough Easky 0 0⋅00 10Dunneill Dunneill River 0 0⋅00 35Ballysadare Lough Templehouse 0 0⋅00 6

Ballysadare River 0 0⋅00 8Druncliff Lough Glencar 0 0⋅00 8Owenmore Lough Carrowmore 0 0⋅00 6

North Western Erne Lough Corglass 83 2⋅60 6Lough Upper Erne 67 3⋅77 90Lough Derrybrick 50 6⋅20 12Lough Lower Macnean 71 4⋅50 17Lough Upper Macnean 76 3⋅00 21Erne (Belturbet) River 69 5⋅50 16Lough Melvin 0 0⋅00 50

Coastal Durnesh transitionalwaters

0 0⋅00 6

Owentocker Owentocker River 0 0⋅00 7Coastal Lough Kiltooris 0 0⋅00 11Gwebarra Lough Barra 0 0⋅00 6

Gwebarra transitionalwaters

0 0⋅00 6

Coastal Lough Dungloe 0 0⋅00 12Gwedore Lough Anure 0 0⋅00 18

Lough Glen 0 0⋅00 10Leannan Lough Fern 0 0⋅00 11Coastal Lough Sessiagh 0 0⋅00 10Clonmany Ballyhallan (Clonmany)

River0 0⋅00 13

Coastal Inch Lough transitionalwaters

0 0⋅00 32

N/A, not applicable as no information was available.


distribution, prevalence and intensity of anguillicola crassus (nematoda) infection in anguilla...

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