Metazoan parasite community of a European eel (Anguilla anguilla) population from an estuary in Portugal

Bull. Eur. Ass. Fish Pathol., 28(1) 2008, 35

Metazoan parasite community of a Europeaneel (Anguilla anguilla) population from an

estuary in PortugalM. Hermida1,2 , A. Saraiva1,2* and C. Cruz1,2

1Departamento de Zoologia e Antropologia, Faculdade de Ciências, Universidade do Porto, PraçaGomes Teixeira, 4099-002 Porto, Portugal; 2CIIMAR Centro Interdisciplinar de Investigação Marinha

e Ambiental, Rua dos Bragas, 289, 4050-123 Porto, Portugal.

AbstractOver an 11-month period, the gills, digestive tract, and swimbladder of eels from the Ria deAveiro were examined for the presence of parasites. Fifteen metazoan parasite species werefound: one myxosporean (Myxidium giardi), one monogenean (Pseudodactylogyrus anguillae), fivedigeneans (Deropristis inflata, Lecithochirium rufoviride, Helicometra fasciata, Podocotyle spp., andLecithochirium sp. metacercariae), two cestodes (Proteocephalus sp. and Bothriocephalus claviceps),two nematodes (Anguillicola crassus and Contracaecum sp. larvae), two acantocephalans(Acanthocephalus clavula and Pomphorhynchus laevis), and two crustaceans (Ergasilus gibbus andGnathiidae gen. sp.). The parasite species D. inflata, L. rufoviride, Lecithochirium sp. metacercariae,H. fasciata, Proteocephalus sp., Contracaecum sp. larvae, P. laevis, and Gnathiidae gen. sp. are recordedin Portugal for the first time in this host. Although the eels from Ria de Aveiro presented a veryrich parasite community, several species occur very rarely. The low diversity observed in theintestinal infracommunity of the Ria de Aveiro eels reflects the high proportion of eels that werenot parasitized or harboured only one helminth species.

* Corresponding author’s E-mail: [email protected]

IntroductionThe European eel, Anguilla anguilla L., is aneconomically important fish whosegeographical distribution includes allEuropean waters and the Mediterraneanbasin. The EU production of the European eelwas estimated in 10 thousand tones per year.Most of this production occurs in freshwaterbut small quantities are also produced inmarine and brackish waters (Cross, 2003). Riade Aveiro is the most important brackishwater lagoon in the Portuguese coast whereseveral fish species, including the Europeaneel, are extensively produced.

Several studies on the parasite communitiesof the European eel have been conducted inPortugal (Carvalho-Varela et al., 1984; Saraiva& Chubb, 1989; Saraiva & Eiras, 1996; Saraivaet al., 2005), but none was done in brackish orsaltwater environments and only onecomprehensively analysed eel parasitecommunities (Saraiva et al., 2005).

The main aim of this work is to study abrackish water eel parasite community fromPortugal and, since the Portuguese coast is atransitional area between the Mediterraneanand the Northeast Atlantic, to compare thiscommunity with those observed in otherEuropean coasts.


Materials and methodsDuring an eleven-month period, 134 live eels(total length: 36.1 ± 6.3, weight: 85.1 ± 54.6 g)from the Ria de Aveiro, estuarine bay of theRiver Vouga, were acquired from localfishermen. The eels were transported live tothe laboratory where they were killed,dissected, and the gills, digestive tract andswimbladder examined for the presence ofmetazoan parasites. The prevalence, intensity,mean intensity, and mean abundance weredetermined according to Bush et al. (1997).

The characterization of the parasitecommunity structure was done at component

community and intestinal helminthinfracommunity levels (Bush et al., 1997),using the total number of parasite species(species richness), the Simpson’s reciprocalindex (1/D), the Shannon-Wiener index (H’)and its Evenness (Pielou’s index) (E), theBerger-Parker Dominance index (d), the meannumber of parasites and species per eel andthe Brillouin’s index (HB). All these indiceswere adopted in order to facilitatecomparisons with results from other authorsand calculated in accordance with Magurran(1989) and Krebs (1999). Component specieswere defined as species presentingprevalences of 10% or greater (Kennedy, 1993).

Table 1. Infected organ, total number of parasites (TN), prevalence (P), mean intensity (I) ± standard deviation(SD), (minimum – maximum ), and mean abundance (A) ± standard deviation (SD) of eel parasites from Riade Aveiro. * Number of cysts.

N = 134 121 (90.3%)

Number of observed eels Number of infected eels (%) Parasite species

Infected organ TN P (%) I ± SD (min‐max) A ± SD

Myxidium giardi Gills 2189* 38.8 42.1* ± 91.94

(1-552) 16.34 (± 60.84)

Pseudodactylogyrus anguillae Gills 255 31.3 6.1 ± 7.49

(1-45) 1.90 ± 5.05

Deropristis inflata Stomach and intestine 2075 47.0 32.9 ± 94.99

(1-732) 15.49 ± 67.17

Lecithochirium rufoviride Stomach 46 7.5 4.6 ± 6.39

(1-23) 0.34 ± 2.12

Lecithochirium sp. metacercariae Gills 8 0.8 8.0 0.06

Podocotyle sp. Intestine 254 9.7 19.5 ± 27.01

(1-106) 1.90 ± 10.21

Helicometra fasciata Intestine 50 3.7 10.0 ± 17.02

(1-44) 0.37 ± 3.79

Proteocephalus sp. Intestine 10 5.2 1.4 ± 0.49

(1-2) 0.07 ± 0.34

Bothriocephalus claviceps Intestine 5 2.2 1.7 ± 0.94

(1-3) 0.04 ± 4.97

Anguillicola crassus Swim bladder 228 32.8 5.2 (± 5.84)

(1-24) 1.70 ± 4.14

Contracaecum sp. larvae Intestinal wall 417 13.4 23.2 ± 71.00

(1-311) 3.11 ± 27.20

Acanthocephalus clavula Intestine 2 1.5 1.0 0.01 Pomphorhynchus laevis Intestine 1 0.8 1.0 0.01

Ergasilus gibbus Gills 76 9.7 5.9 ± 6.36

(1-25) 0.57 ± 2.63

Gnathiidae gen. sp. Gills 9 3.7 1.8 ± 1.17

(1-4) 0.07 ± 0.41


ResultsComposition of the parasite communityA total of 121 eels (90.3%) were infected withone to six parasite species. Fifteen metazoanparasite species were detected in the studiedeels: one myxosporean (Myxidium giardi), onemonogenean (Pseudodactylogyrus anguillae),five digeneans (Deropristis inflata ,Lecithochirium rufoviride, Helicometra fasciata,Podocotyle spp., and Lecithochirium sp.metacercariae), two cestodes (Proteocephalussp. and Bothriocephalus claviceps), two

nematodes (Anguillicola crassus andContracaecum sp. larvae), two acantho-cephalans (Acanthocephalus clavula andPomphorhynchus laevis), and two crustaceans(Ergasilus gibbus and Gnathiidae gen. sp.). Theinfection levels observed are presented inTable 1.

Only five parasite species occurred in eels allyear round (M. giardi, D. inflata, L. rufoviride,A. crassus, and Contracaecum sp.) Two gillparasites, P. anguillae and E. gibbus, were not

Table 2. Component community structure of the Aveiro eel population and other European brackish watereel populations (D. i. = Deropristis inflata, P. a. = Pseudodactylogyrus anguillae, B. c. = Bothriocephalus claviceps,E. s. = Ergasilus sieboldi; *values calculated from data given by the authors; ‡ helminth parasites only).

Portugal Spain France Italy Present study

Outeiral et al., 2001/2002 Maíllo et al., 2005

Ternengo et al., 2005

Kennedy et al., 1997‡

Ave

iro

Aro

usa

Ferr

ol

Enca

nyis

sada

Tanc

ada

Can

al V

ell

Urb

ino

Bura

no

Fogl

iano

Mon

aci

Cap

rola

ce

Species richness 14 19 17 5 3 5 5 8 4 4 3 Number of component species

4 4 2 3 3 3 3 3 4 3 2

Simpson’s Index 2.53 3.55* 1.73* 1.18* 1.63* 4.07* 1.20* 3.70* 3.72* 2.63* 1.97* Shannon-Wiener Index 2.01 1.77* 1.15* 0.50 1.02 2.14 0.56* 1.31 1.34 1.05 0.86

Pielou’s Evenness 0.53 0.44* 0.29* 0.21 0.64 0.92 0.24* 0.63 0.97 0.76 0.78 Berger-Parker Dominance 0.60 0.43* 0.72* 0.92 0.77 0.31 0.91* 0.54 0.34 0.40 0.67

Dominant Species D. i. D. i. D. i. P. a. P. a. P. a. D. i. D. i. D. i. D. i. D. i.

Denmark Poland Germany

Køie, 1988 Seyda, 1973‡

Orecka‐Grabda & Wierzbicka1994

Reimer, 1987

Ulf

Sun

d

Rin

gk. F

jord

Isef

jord

w.K

atte

gat

Szcz

ecin

Fir

th

Riv

er O

dra

mou

th

area

Wis

mar

er B

ucht

Gre

ifsw

alde

n Bo

dden

Lass

an

Species richness 13 8 13 7 8 6 10 6 12 Number of component species 9 5 7 5 3 4 2 3 2

Simpson’s Index 3.89* 3.50* 3.09* 2.70* 2.78* 3.95* 1.61* 1.75* 1.59* Shannon-Wiener Index 2.26* 2.18* 2.04* 1.87* 1.92* 2.24* 1.31* 1.37* 1.26*

Pielou’s Evenness 0.61* 0.73* 0.55* 0.67* 0.64* 0.87* 0.40* 0.53* 0.35* Berger-Parker Dominance

0.33* 0.43* 0.47* 0.56* 0.55* 0.40* 0.78* 0.75* 0.78*

Dominant Species P. a. P.a. D. i. D. i. B. c. E. s. D. i. D. i. D. i.


detected in the summer, and Podocotyle sp.,H. fasciata, and Proteocephalus sp. occurred inonly two seasons. The remainder five speciesoccurred just in one season with very lowprevalence values.

Component community structureData on the eel metazoan (excludingMyxosporea) parasite community structureobserved in the present study as well as thosereported from previous studies in brackish ormarine European waters are presented inTable 2.

In the present study the species richness andthe number of component species of the eelparasite community were high. The Shannon-Wiener index was also relatively high, whilethe Simpson’s index and Pielou’s evennesswere lower when compared to other brackishwater communities. The trematode D. inflatawas the dominant species with a Berger-Parker dominance index of 0.60.

Infracommunity structureData on the eel intestinal helminthinfracommunity are presented in table 3. Mosteels (84%) were uninfected or harboured onlyone intestinal parasite species. A maximum

of 3 intestinal helminth species per eel wasfound. Although the mean number ofparasites per eel was high the mean numberof helminth species per eel and the Brillouin’sindex (all eels and infected eels only) werelow.

DiscussionEight out of the fifteen parasite speciesobserved were detected for the first time ineels from Portugal (D. inflata, L. rufoviride,Lecithochirium sp. metacercariae, H. fasciata,Proteocephalus sp., Contracaecum sp. larvae,P. laevis and Gnathiidae gen. sp.) probablybecause this is the first study in brackishenvironments in this country. All theseparasites have been observed in eels frombrackish or saltwater environments (Seyda,1973; Vaes, 1978; Reimer, 1987; Køie, 1988;Pilcher & Moore, 1993; Orecka-Grabda &Wierzbicka, 1994; Reimer et al., 1994;Wierzbicka & Orecka-Grabda, 1994; Dezfulliet al., 1997; Kennedy et al., 1997; Outeiral etal., 2001, 2002; Maíllo et al., 2005; Ternengo etal., 2005) and all but P. laevis were previouslyfound in eels from the neighbour Galicia,Spain. (Outeiral et al., 2001, 2002). Six of theparasite species detected are eel specialists

Ria de Aveiro, Portugal 2004/2005

Number of eels 134 Mean number of helminths (± sd)

18.25 (± 67.61)

Mean number of helminth species (± sd) and max.

0,79 (± 0,75) 3

Brillouin’s Index Mean (± sd) and max.

0,054 (± 0,145) 0,795

Brillouin’s Index (infected eels only) Mean (± sd)

0.089 (±0.179)

Proportion of eels with 0 or 1 sp of helminth 0.84

Table 3. Intestinal helminth infracommunity of eels from Ria de Aveiro.


(M. giardi, P. anguillae, D. inflata, B. claviceps,A. crassus, and E. gibbus) and these species arethe most prevalent.

Although the number of parasite speciesobserved in the present study was lower thanthat reported by Outeiral et al. (2001, 2002) inGalicia, the number of component species,diversity, and evenness detected weregenerally higher. The Pielou’s evenness valuesdetected by several authors were usuallyhigher than those observed in the Ria deAveiro which indicate more stablecommunities. It is interesting to observe thatwhile freshwater parasite communities wereusually dominated by a nematode species(Saraiva et al., 2005) the studies in brackishor saltwater environments indicate that thedominant species was usually the specialistdigenetic D. inflata.

Although most of the parasite speciesdetected in the present study were observedin the intestine this organ was never infectedwith more than three species. The lowdiversity observed in the intestinalinfracommunity of the Ria de Aveiro eelsreflects the high proportion of eels that werenot parasitized or harboured only onehelminth species.

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Metazoan parasite community of a European eel (Anguilla anguilla) population from an estuary in Portugal