Ž .
All parasites found only helminths in our case were collected and cleaned in 9‰ ClNa solution, then extended and fixed in Berland’s fluid, preserved in 70 alcohol,
´
Ž .
processed by standard methods see Alvarez et al., 1994, 1995a,b for examination by light microscopy or scanning electron microscopy.
Parasite ecology terms such as prevalence, intensity, mean intensity and mean Ž
. Ž
. abundance are used in accordance with Margolis et al. 1982 and Bush et al. 1997 .
Three measures of diversity were used as follows. Ž .
l Species richness S was estimated directly as the number of species observed in Ž
. the sample Magurran, 1988 .
Ž
X
. Ž
X
. l The Shannon–Wiener diversity index H
and the evenness index of Pielou J Ž
. were calculated using base-two logarithms Pielou, 1966, 1975; Magurran, 1988 .
Ž .
l Dominance was evaluated by the Berger–Parker index Magurran, 1988 . Parasite community composition was compared between size classes using two
Ž .
equations: The qualitative Jaccard similarity index Magurran, 1988 and the quantitative Ž
. Ž .
percentage overlap similarity index PS Brower et al., 1990 .
Ž Aggregation of each parasite species was quantified with the dispersion index D.I.;
. Ž
. Anderson and Gordon, 1982 . Significance of the values was checked by Ping’s 1995
test.
3. Results
A total of nine species of helminths were detected, namely five cestodes, three Ž
. nematodes and one acanthocephalan Tables 1 and 2 . Trematodes, either digenean or
monogenean, were not detected. No protozoans were detected either.
Table 1 Parasite species detected in 74 undulate rays captured between February, 1992 and December, 1993 in the Rıa
´
of Muros. Values for prevalence, intensity and aggregation indices
U U
U
Ž .
Species Site
Prevalence I SD range
A D.I.
Cestodes Ž
. O. uncinatum
Spiral valve 97.3
12.69.6 1–35 12.3
7.64 Ž
. P. lactuca
Spiral valve 49.3
32.7 1–12 1.4
3.89 Ž
. E. beauchampi
Spiral valve 32
2.93.4 1–15 0.9
5.93 Ž
. A. benedeni
Spiral valve 62.6
1226.1 1–166 7.5
101.15 Ž
. Grillotia sp.
Spiral valve 57.3
7.67.7 1–37 4.4
11 Nematodes
Ž .
Schulmanela Spiral valve
12 1.91.2 1–4
0.22 2.34
Ž .
Piscicapillaria sp. Ž
. Pseudanisakis
Spiral valve 8
3.33.4 1–9 0.26
4.8 rotundata
Ž . Cystidicolidae sp.
Spiral valve 1.3
1 1 0.01
1 gen. larvae
Acanthocephalans Ž
. Acan. propinquus
Spiral valve, stomach 4
21 1–3 0.05
23
U
I s mean intensity, As mean abundance, SDsstandard deviation, D.I.sdispersion index.
Table 2 Classification of the helminth species detected in the undulate ray from the Rıa of Muros in accordance with
´
host–parasite relationships
U U
Species G,S,A
Percentage of total Percentage of
AU, AL examined rays
infected rays where the species
where the species is dominant
is dominant Cestodes
O. uncinatum S
70.6 72.6
Au P. lactuca
S 4
8.1 Au
E. beauchampi S
1.3 4.2
Au A. benedeni
S 14.6
23.4 Au
Grillotia sp. S
10.6 18.6
Au Nematodes
Ž .
Schulmanela Piscicapillaria sp. S
Au Pseudanisakis rotundata
S Au
Cystidicolidae gen. sp. larvae A
Au Acanthocephalans
Acan. propinquus A
Au
U
G s generalist, Ssspecialist, A saccidental, AUsautogenic, AL sallogenic.
Except for the taxa Cystidicolidae gen. sp. and Acanthocephaloides propinquus Ž
. Dujardin, 1845 Meyer, 1932, both of which can be considered accidental in undulate
ray, all the parasites detected were specific for elasmobranches, and all were detected in Ž
. the adult form in the gastrointestinal tract generally the spiral valve .
The overall prevalence of infection was very high, with at least one parasite being detected in all except one of the 75 host individuals.
The number of individual parasites per host ranged from 0 to 191, with 70 of hosts showing between 1 and 30 parasites. Mean intensity of infection was 27 28 parasites
per host, with mean abundance practically the same. Cestodes were the dominant group. Over 98 of individuals examined showed at
least one of the five cestode species. 3.1. DiÕersity and eÕenness
Ž
X
. Ž
. The value obtained for the Shannon–Wiener index
H was 2 Table 3 . This is
Ž . high, bearing in mind the relatively low observed species richness
9 , and the Ž
X
. intermediate value of Pielou evenness J s 0.631 , attributable to the low frequency of
non-cestode helminths. The difference in yearly values for observed species richness is Ž
probably due to number of rays examined in each year 30 versus 45 specimens, .
respectively . The frequency distribution of H
X
in individual hosts is shown in Fig. 1a. More than 65 of host individuals showed H
X
values between 0.4 and 1.8. The frequency
X
Ž .
distribution of J Fig. 1b was skewed to the right, with over 60 of host individuals
showing J
X
values between 0.4 and 0.9. In more than 70 of the fish examined, the
Table 3 Diversity statistics for the helminth community of the undulate ray in the Rıa of Muros. H
X
sShannon–Weaver
´
diversity index, J
X
s Pielou evenness index, Ssspecies richness, N s total number of individual parasites.
i
1992 1993
1992–1993
X
H 1.771
2.043 2.0
X
J 0.685
0.694 0.631
S 6
9 9
N 558
1478 2036
1
dominant helminth was Onchobothrium uncinatum Rudolphi, 1819. This species was Ž
. present in 73 97 of the 75 fish examined, and accounted for 45 of all parasite
Ž individuals detected. Three species
Acanthobothrium benedeni Loemberg, 1889, Gril-
¨
Ž .
. lotia sp. and Phyllobothrium lactuca Rudolphi, 1819 Mosgovoy, 1950 showed a
prevalence of about 49 or more, but were dominant in less than 20 of host Ž
. individuals, and only in large individuals Table 2 .
3.2. Aggregation Ž
. The values of the dispersion index D.I., Table 1 suggest an aggregated distribution
Ž .
V A for all taxa except Cystidicolidae sp. larvae, for which the distribution was
Ž
X
. Fig. 1. Histograms showing the frequency distributions of Shannon–Wiener diversity
H and Pielou
Ž
X
. evenness J
indexes in individual hosts. The upper limit of each class is shown.
Fig. 2. Histograms showing the frequency distributions of the number of parasite species per individual host Ž
. infracommunity species richness .
Ž .
random V s A . Considering the species with aggregated distribution, D.I. was highest for A. benedeni and Grillotia sp., and lowest for P. lactuca Beneden, 1850, Schul-
Ž .
manela Piscicapillaria sp. and Acan. propinquus. 3.3. Infracommunity patterns
The number of parasite species per host ranged from zero to six, and was two to four Ž
. in 65 of the fish examined Fig. 2 . The most frequent number of parasites per host
Ž .
was three 28 of host individuals . Considering cestodes only, we detected a total of 16 different species combinations
Ž .
Ž Fig. 3 . Individual hosts contained between one cestode species
in all cases O. .
Ž .
uncinatum; 7.5 of the total and five cestode species 13 of the total . The frequency Ž
. distribution of the number of cestode species per host Fig. 4 was roughly bell-shaped,
though slightly skewed to the right, the class with highest frequency being three species Ž
. 32 of hosts . This curve is therefore similar to that obtained considering all parasite
Fig. 3. Histogram showing the frequency distribution of cestode species combinations in individual hosts Ž
. Os O. uncinatum, P s P. lactuca, A s A. benedeni, G sGrillotia sp., E s E. beauchampi .
Fig. 4. Histograms showing the frequency distributions of the number of cestode species per individual host.
Ž .
species Fig. 2 . O.uncinatum was present in all cestode-infected individuals. O.
Ž .
uncinatum and A. benedeni were found together with or without other species in 60 Ž
. of cestode-infected individuals Fig. 3 .
3.4. Seasonal Õariations When the data were grouped by month, the prevalence, intensity and abundance of
Ž the major taxa O. uncinatum; P. lactuca; A. benedeni; Echeneibothrium beauchampi
. Euzet, 1959; Grillotia sp. showed no consistent patterns of seasonal variation. When
the data were grouped seasonally, however, clear patterns were observed for several Ž
. species
Fig. 5 , with both prevalence and mean abundance peaking in spring or summer. In general, Shannon–Wiener diversity and Pielou evenness showed similar
Ž .
time courses to those of prevalence and mean abundance Fig. 6a,b .
Ž .
Ž .
Fig. 5. Seasonal variation in the prevalence a–b and mean abundance c–d of infection by the major parasites of undulate ray in the Rıa of Muros. Wi s winter, Spsspring, Su ssummer, Au sautumn.
´
Ž
X
. Ž
X
. Fig. 6. Monthly and seasonal variation in Shannon–Wiener diversity H
and Pielou evenness J indexes in
undulate rays from the Rıa of Muros. Wi s winter, Spsspring, Su ssummer, Au sautumn.
´
3.5. Variation among size classes The host specimens were grouped into six size classes, for analysis of the helminth
communities present in each. 3.5.1. Class A length - 23 cm, 17 hosts
Ž .
The five cestode species were detected Table 1 . The number of parasite species per host ranged from one to four and the most frequent value for observed infracommunity
Ž . Ž
. species-richness
S was one speciesrhost 47 of host individuals . The overall
i
Ž .
all-species intensity of infection ranged from 2 to 38 parasitesrhost, with a mean Ž
. overall intensity and mean overall abundance of 11.06 9.66 parasitesrhost.
3.5.2. Class B length 23–28 cm, 15 hosts The same five species as in Class A were detected. S was also similar to that of
i
Ž .
Ž Class A zero to four , but the most frequent value was three species per host 33 of
. host individuals , and 60 of hosts contained three to four species. One specimen of this
group was free of parasites. The overall intensity of infection ranged from 0 to 47 parasitesrhost, with a mean overall intensity of 20.71 10.92 parasitesrhost and a
mean overall abundance of 19.33 11.8 parasitesrhost.
3.5.3. Class C length 28–33 cm, 17 hosts The five cestode species and Acan. propinquus were detected in this class. The
Ž .
number of parasite species per host was also higher two to five , and the most frequent Ž
. value for S was four species per host 35 of host individuals . The overall intensity of
i
Ž infection ranged from 5 to 48 parasitesrhost, with a mean overall intensity and mean
. overall abundance of 27.23 12.46 parasitesrhost.
3.5.4. Class D length 33–38 cm, six hosts Six parasite species were detected, including the cestodes and, for the first time, a
Ž .
nematode the capillariinaean Schulmanela sp. . The most frequent values for S were
i
Ž .
again three and four species per host range one to six . The overall intensity of infection was slightly higher than in the preceding class: range was 12–49 parasitesrhost, while
Ž .
mean overall intensity and also mean overall abundance
was 33.50 15.75 parasitesrhost.
3.5.5. Class E length 38–43 cm, eight hosts Seven parasite species were detected, those present in the preceding class, plus P.
rotundata. Infracommunity species richness ranged from two to six, with 50 of host individuals containing five or six species. The overall intensity of infection ranged from
Ž
X
. Ž
X
. Fig. 7. Mean infracommunity Shannon–Wiener diversity
H and Pielou evenness
J in undulate rays
grouped into size classes.
Table 4 Similarity between the helminth communities of the different size classes
Ž .
Jaccard index qualitative J A
B C
D E
F A
1 0.83
0.83 0.71
0.55 B
83.7 0.83
0.83 0.71
0.55 C
81.5 90.9
0.71 0.62
0.66 D
59.5 73.2
73.2 0.75
0.66 E
59.2 74.9
69.1 85.8
0.77 F
32 45
39.3 59
69.1 Ž
. Percentage overlap quantitative PS
Ž .
11–49 parasitesrhost. Mean overall intensity and mean overall abundance
was 30.50 12.88 parasitesrhost.
3.5.6. Class F length 43 cm, 12 hosts All nine parasite species were detected. S ranged from two to seven. The overall
i
Ž intensity of infection ranged from 5 to 191 parasitesrhost. Mean overall intensity and
. mean overall abundance was 54.0 56.1 parasitesrhost.
These findings show that overall species richness, observed infracommunity species richness, and number of individual parasites per host all increase with increasing host
size. The five cestode species were present in all size classes, with the elasmobranch- Ž
. specific nematodes being detected only in the larger classes D–F . In smaller fish, the
dominant parasite was O. uncinatum, which gradually gave way to A. benedeni, and to a lesser extent Grillotia sp., with increasing host size.
Infracommunity H
X
and J
X
values likewise increased with host size. Mean infracom- munity H
X
ranged from 0.464 in Class A to 1.686 in Class D, with the values observed Ž
. in the subsequent classes E and F being similar to that observed in Class D, or rather a
Ž .
X
bit lower, but always higher than Class C Fig. 7a . Mean infracommunity J showed a Ž
. similar pattern Fig. 7b .
Ž .
Values of the Jaccard similarity index Table 4
were relatively high for all between-class comparisons, except those for A-versus-F and B-versus-F, which were
Ž .
lower reflecting the presence of the three non-cestode species in F . Values of
Ž .
percentage overlap which takes into account differences in intensity were not so high, reflecting the marked differences in A. benedeni and Grillotia sp. intensity between
Ž . classes A–C and the largest size class F .
4. Discussion
