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Parasite community study of the undulate ray
Raja undulata in the Rıa of Muros
´
ž
Galicia, northwest Spain
/
M.L. Sanmartın
´
), M.F. Alvarez, D. Peris, R. Iglesias, J. Leiro
Laboratorio de Parasitologıa, Instituto de In´ Õestigacion y Analisis Alimentarios, Facultad de Farmacia,´ ´
UniÕersidad de Santiago de Compostela, AÕda. de Vigo srn, 15706, Santiago de Compostela, Spain
Accepted 11 October 1999
Abstract
Ž .
The parasites present in 75 undulate rays Raja undulata Lacepede, 1802 captured in the Rıa` ´
Ž .
of Muros, a coastal embayment rıa in northwest Spain were studied. A total of five species of´
Ž
cestodes Onchobothrium uncinatum, Phyllobothrium lactuca, Echeneibothrium beauchampi,
. Ž w
Acanthobothrium benedeni and Grillotia sp. , three species of nematodes Schulmanela
Piscica-x .
pillaria sp., Pseudanisakis rotundata and Cystidicolidae gen. sp. and one acanthocephalan
ŽAcanthocephaloides propinquus were detected. All species were elasmobranch-specific except.
Cystidicolidae sp. and Acan. propinquus, which can both be considered accidental in this host.
Ž
Species diversity peaked over the period April–September Shannon–Wiener diversitys1.9–
.
2.2; Pielou evennesss0.8–0.9 . The dominant species were cestodes, notably O. uncinatum
Žpresent in 73 of the 75 hosts, and accounting for 45% of all parasites detected , followed by A..
benedeni, P. lactuca and Grillotia sp., all of which were present in more than 30% of the host individuals. All species detected were autogenous, and all individuals except those of Cystidicoli-dae gen. sp. were adults.
The five species of cestodes were present in hosts of all sizes, though single-host species richness, single-host species diversity and overall intensity of infection increased with increasing
Ž .
host size. Nematodes appeared in larger individuals body length)33 cm . Larval Cystidicolidae
Ž .
gen. sp. appeared only in the largest size class )43 cm , probably because only rays of this size are capable of ingesting relatively large demersal fish, the usual intermediate hosts in this area. Analysis of the species compositions of single-host parasite communities, considering cestodes only, suggests that negative interspecific interactions do not occur, despite the typically large size
)Corresponding author. Tel.:q34-981-563100, ext. 14893; fax:q34-981-593316.
Ž .
E-mail address: [email protected] M.L. Sanmartın .´
0044-8486r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
and abundance of the parasites, and their spatial concentration in the spiral valve.q2000 Elsevier Science B.V. All rights reserved.
Keywords: Raja undulata; Northwest Spain; Spiral valve; Helminth parasites; Seasonal trends;
Infracommuni-ties
1. Introduction
Ž .
The undulate ray Raja undulata Lacepede, 1802 Chondrichthyes: Rajidae is a
`
bottom-dwelling elasmobranch that occurs on continental shelves to depths of up to 200Ž .
m, most frequently on soft sandy bottoms Stehmann and Burkel, 1989 . It is distributed
¨
Ž .
along the eastern edge of the Atlantic, from Mauritania West Africa in the south to southern Ireland and southwest England in the north, and is also present along the western Mediterranean coast of North Africa. It is a carnivore, feeding on a wide variety of benthic vertebrates and invertebrates. It reproduces between March and September,
Ž
by laying 90=50 mm egg capsules. These hatch about 91 days later about 116 days
. Ž .
after copulation Pinto de la Rosa, 1998 . The high urea concentrations in tissues and Ž body fluids of elasmobranches gives rise to a highly specialized parasite fauna
Wil-. liams, 1964; Williams et al., 1970; Cislo and Caira, 1993 .
In European waters Raja species are not generally targeted by commercial fisheries ŽAnonymous, 1995 . In Spain, however, and particularly in the Galicia region, ray is. widely consumed, and is an important target for the coastal fishing fleet. For example, in
Ž .
the Rıa of Arousa one of the most productive coastal fishing areas in Spain , rays are
´
Ž .
the third most important fish by capture volume 80 tons in 1996 , and the fourth most
Ž . Ž .
important economically about US$175,000 in the same year Iglesias Prol, 1998 . They have also been studied by local fish farms as possible future cultivable species.
There have been few previous complete studies of the parasites of rays. In the present study, we determined the helminth parasites of R. undulata from the Rıa of Muros
´
ŽGalicia, Northwest Spain , and investigated possible relationships with environmental. factors.2. Material and methods
A total of 75 specimens of undulate ray, captured between February 1992 and
Ž X X X X
December 1993 on the Misela Bank in the Rıa of Muros 42
´
846.5 –42848 N; 9854 –9857 .W were examined. All the fish were caught by trawling or in funnel traps, then transferred to the laboratory in aerated seawater, and maintained alive until dissection Ž0–4 days . They were killed by an overdose of anesthetic MS222 Sigma . Immediately. Ž .
Ž .
after death, the fish were measured total body length to the last 0.5 cm and weighed to the last 0.1 g. A body-surface mucus sample was obtained by scraping in search for protozoa. The viscera and gills were then removed and examined with a
stereomicro-Ž .
scope. Spiral intestine was examined as described by Williams 1964 and Williams et Ž .
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 .
lSpecies richness S was estimated directly as the number of species observed in
Ž .
the sample Magurran, 1988 .
Ž X
. Ž X
.
lThe 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 .
lDominance 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 12.6"9.6 1–35 12.3 7.64
Ž .
P. lactuca Spiral valve 49.3 3"2.7 1–12 1.4 3.89
Ž .
E. beauchampi Spiral valve 32 2.9"3.4 1–15 0.9 5.93
Ž .
A. benedeni Spiral valve 62.6 12"26.1 1–166 7.5 101.15
Ž .
Grillotia sp. Spiral valve 57.3 7.6"7.7 1–37 4.4 11
Nematodes
Ž .
Schulmanela Spiral valve 12 1.9"1.2 1–4 0.22 2.34
ŽPiscicapillaria sp..
Ž .
Pseudanisakis Spiral valve 8 3.3"3.4 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 2"1 1–3 0.05 23 U
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 0 0 Au
Pseudanisakis rotundata S 0 0 Au
Cystidicolidae gen. sp. larvae A 0 0 Au
Acanthocephalans
Acan. propinquus A 0 0 Au
U
Gsgeneralist, Ssspecialist, Asaccidental, AUsautogenic, ALsallogenic.
Except for the taxa Cystidicolidae gen. sp. and Acanthocephaloides propinquus ŽDujardin, 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 s0.631 , 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 HX in individual hosts is shown in Fig. 1a. More than 65% of host individuals showed HX values between 0.4 and 1.8. The frequency
X
Ž .
Table 3
Diversity statistics for the helminth community of the undulate ray in the Rıa of Muros. HX
sShannon–Weaver
´
diversity index, JX
sPielou evenness index, Ssspecies richness, Nistotal number of individual parasites.
1992 1993 1992–1993
X
H 1.771 2.043 2.0
X
J 0.685 0.694 0.631
S 6 9 9
N1 558 1478 2036
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 ŽV)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.
Fig. 2. Histograms showing the frequency distributions of the number of parasite species per individual host
Žinfracommunity species richness ..
Ž .
random VsA . 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 ŽFig. 3 . Individual hosts contained between one cestode species. Žin 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 Ž32% 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
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. SeasonalÕariations
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 .
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. Wis´ winter, Spsspring, Sussummer, Ausautumn.
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 Si was one speciesrhost 47% of host individuals . The overall Žall-species intensity of infection ranged from 2 to 38 parasites. rhost, 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 ofi
Ž . Ž
.
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 ofi
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 werei
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.
Table 4
Similarity between the helminth communities of the different size classes
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 overalli 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 HX and JX values likewise increased with host size. Mean infracom-munity HX 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
Similar results have been obtained in other studies of elasmobranches. We are not aware of acanthocephalans reported previously in elasmobranches. After a study of more
Ž . Ž .
Ž .
in elasmobranch body fluids and tissues. Cislo and Caira 1993 likewise suggest that acanthocephalans are absent from elasmobranches for this reason. In the present study, we found a few immature individuals of the acanthocephalan Acan. propinquus.
Ž
However, these individuals were in poor condition not alive at the moment of .
dissection, body much softer and fragile than specimens found in other hosts ; further-more, in our study area this species is the dominant adult helminth in a number of demersal fish species that are probably important prey items for the undulate ray Žnotably Gobius niger, G. auratus and G. cobitis; personal unpublished findings . Acan.. propinquus is also present in other species possibly preyed upon by the undulate ray.
These findings suggest that the presence of Acan. propinquus in undulate ray, as detected in the present study, was probably accidental.
Ž .
The diet of rays varies with both species and size. Daan et al. 1993 , in a study of four species of the genus Raja, observed that smaller individuals feed almost entirely on
Ž
invertebrates -80 cm for R. claÕata, -70 cm for R. montagui, -25 cm for R.
. radiata, -15 cm for R. naeÕus; the authors do not specify the length measured . We
are not aware of any previous studies of the diet of R. undulata, but it is worth noting
Ž .
that in the present study all helminths detected in the smaller size classes A, B and C were cestodes, except for a few individuals of Acan. propinquus in Class C.
These size classes include fish from 17 to 33 cm in total body length. From Daen et al.’s paper, one would expect rays of this size to feed principally on invertebrates. However, small demersal fish are taken too, such as G. niger, since even very small gobies have been found to harbour plerocercoids of the same Grillotia sp. found here as
Ž .
an adult our own unpublished data , and also two types of plerocercoids of the Scolex
pleuronectis group, whose scolex morphology remembers those of Acanthobothrium
spp. and Onchobothrium spp. The latter were also found in small specimens of Ciliata
mustela.
Capillariinaean nematodes were not detected until Class D, P. rotundata not until Class E and Cystidicolidae gen. sp. not until Class F. These results reflect cumulatively increasing predation of the intermediate hosts of these parasites. We have found larval Cystidicolidae encysted in the body cavity of benthic fishes from the Galician rias ŽGobius spp., Syngnathus acus, Trigla lucerna, C. mustela, Symphodus spp., personal
. Ž
unpublished results , but only in the largest individuals for example, black gobies )13
. Ž
cm that would not, for their size, be feasible prey for rays smaller than class F i.e., .
body length )43 cm . This suggests that Cystidicolidae larvae may be no more than Ž
accidental in the undulate ray, since the adult form of Cristitectus congeri the only . cystidicolid species identified to date in the Galician rias; Quinteiro et al., 1989, 1992 is specific for the conger eel. This view is supported by the low prevalence of Cystidicoli-dae larvae in our R. undulata sample.
Apart from the Cystidicolidae larvae and Acan. propinquus, all the parasites detected are specific for elasmobranches. This is again attributable to the high urea concentrations in elasmobranches, which is nevertheless essential for successful maturation of other
Ž .
species Hamilton and Byram, 1974; McVicar, 1977 . Furthermore, many species of elasmobranch cestodes are specific to a single host species. In some cases, antibody-complement systems impeding the establishment of certain cestodes have been
demon-Ž .
The relatively large number of individual parasites detected in undulate rays in the present study, together with the typically large size of most of the parasite species
Ž .
present especially O. uncinatum and P. lactuca and their almost exclusive location in the spiral valve, means that individuals are spatially concentrated, raising the possibility of interactions between species.
Ž
Considering only cestodes the group with highest prevalence; all species had .
prevalences of at least 32% , we detected 16 different species combinations. The Ž
majority of these combinations comprised two or three species five combinations in .
each case, totalling 18.7% and 32.0% of individuals, respectively . The two-species combinations, and some of the three- and four-species combinations, had similar and very low prevalences. However, the majority of the three-species combinations, several of the four-species combinations and the five-species combination had relatively high prevalences. This implies an absence of negative interspecific interactions, and raises the possibility that there may in some cases be positive interactions.
All the parasites detected in the present study are autogenous, reflecting the fact that
Ž .
the undulate ray is a predator at the top of the food chain ‘‘superpredators’’ , with the result that it typically acts as definitive host. This finding is in accordance with Zander
Ž .
and Kesting 1996 , who suggest that autogenous species are typically frequent in Ž
non-contaminated environments. Furthermore, almost all the species detected certainly .
the cestodes, and possibly P. rotundata have a planktonic first intermediate host ŽDollfus, 1976; Zander and Kesting, op. cit. , though the second intermediate host is in.
Ž .
almost all cases benthic crustaceans, molluscs or fish .
It is necessary to compare our results with those obtained in the other Galician rias Žsome relatively eutrophic , with the aim of more accurately assessing the extent to. which predictions of this type are met in superpredators like R. undulata.
Acknowledgements
We would like to thank Dr. Cesar Sanchez, Professor of Biological Statistics of the
´
´
University of Santiago de Compostela, for his advice on statistical tests.This work was financially supported by grant XUGA 23702B97.
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