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Enlargement of the host range of Polylabris tubicirrus (Monogenea, Polyopisthocotylea) under fish-farming conditions
Aquacu~ture, 47 (1985) 267-270
267
Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands
Short Communication ENLARGEMENT OF THE HOST RANGE OF POLYLABRIS TUBICIRRUS (MONOGENEA, POLYOPISTHOCOTYLEA) UNDER FISH-FARMING CONDITIONS
P. SILAN’, P. CABRAL2 and C. MAILLARD’
1Laboratoire de Parasitologic Comparde (UA CNRS 698), Universitk des Sciences et Techniques du Languedoc, Place E, Bataillon, 34060 Montpellier Ckdex (France) 2Laboratoire d ‘Ichthyo~og~e et de Pa~ito~ogie G&&ale, Wniversitk des Sciences et Techniques du La~uedo~, Place E. Bataillon, 34060 Montpe~lier Ckdex (France) (Accepted
28 March 1985)
ABSTRACT Silan, P., Cabral, P, and Maillard, C., 1985. Enlargement of the host range of Polylabris tubicirrus (Monogenea, Polyopisthocotylea) under fish-farming conditions. Aqua”
culture, 47 : 267-270. In the Medi~~anean Sea, Poty~abr~ tubicirrus (Monogenea, Poly~p~thocotylea) is found only on breams of the genus Diplodus: D. sargus, D. annuls, D. vulgaris. The discovery of this parasite on farmed gilt head sea breams (Sparus au&a) raises the problem of the enlargement of the host range of a parasite under artificial conditions of confinement, and of the potential danger this type of transfer can involve.
INTRODUCI’ION
In the Western Mediterranean Sea, the gilt head sea breams, Sparus auratu, harbor two gill monogeneans. One, Furnestinia echeneis (Wagener, 1857) belongs to the Monopisthocotylea, and one, Microcotyle chrysophrii Van Beneden and Hesse, 1863, to the Polyopisthocotylea. To date the only epizootic linked to a member of the Monogenea was due to Furnestiniu echeneis, which caused considerable damage to cultivated Sparus ff~~ta in the gulf of Elat (Red Sea} (Papema et al., 1977; Papema and Baudin Laurencin, 1979). In 1982 heavy mo~~ities were reported in Corsican raceways (France), and the gilt head sea breams which were examined revealed the presence of a third species of Monogenea never yet found on this fish. RESULTS AND DISCUSSION
On the gills of fingerlings weighing about 50 g, a parasite was identified as ~o~y~~r~ t~~ici~us (Paperna and Kohn, 1964) Mamaev and Parukhin, 1976. 0044-8486/85/$03.30
Q 1985 Elsevier Science Publishers B.V.
268
on which several taxonomic studies have This polyopisthocotylean, been carried out (Paperna and Kohn, 1964; Euzet and Cauwet, 1967; Mamaev and Parukhin, 1976), has never been observed on wild Sparus ~~~~~~(Noisy, 1978; L. Euzet, personal communication, 1985). Polylubris t~bic~rr~s has previously been noted only on Sparidae of the genus Diplod~s: D. surgus, D. unn~~r~s and D. u~lgaris (Euzet and Cauwet, 1967). This species, associated or not with Atriaster heterodus, constitutes 90% of the microcotylidean populations on Diplodus sargus, with mean intensities’ ranging from 3.4 (P. tubicirrus in the presence of A. heterodus) to 3.8 (R tubicirrus alone) (Noisy, 1978). In the same geographical area, Microcotyle chrysophrii is found parasitizing Spurus aurutu with a prevalence’ and an autumnal mean intensity of 85% and 10.6 respectively (Noisy, 1978). M. chrysophrii is also present on the three wild Diplodus spp. Up to now, out of five species of Microcotylidae belonging to the genera Microcotyle Van Beneden and Hess@, 1863, Polylabris Euzet and Cauwet, 1967, Atriuster Mamaev and Parukhin, 1969 and Atrispinum Euzet and Maillard, 1973, it was the only one to be found indifferently parasitizing either Spurus uurutu or the three Diplodus species mentioned above. Since cultivated gilt head sea breams were found to be infested by dozens of Polylabris tubicirrus, it can be stated that: (1) under special conditions of aquaculture (race-way), this species has enlarged its host range; (2) the observed intensities are higher than those noted for M~crocutyle ch~sophri~ in a natural environment; and (3) this monogenean is more numerous than on its usual host, i.e. breams of the genus D~plodus. The transfer of Pulylubris tubici~us to a new host raises the problem of its specificity, as defined by Euzet and Combes (1980), towards Sparidae. These authors refer to specificity as the intersection of the following three sets: the “required scope” for the parasite, “ethological filter” and “biocenosis limits”. Breams of the genus Diplodus and gilt head sea breams belong to nearly the same biocenosis in a natural environment, and thus either the ethological filter prevents Polylubris tubicirrus from reaching Sparus uurutu, or this parasite requires a more restricted scope than does Microco ty le chrysophrii. In the race-ways concerned, the intervention of an ethological filter and required scope would signify: - behavioural variations which increase host accessibility, or 1 Mean intensity: Total number of individuals of a particular parasite species in a sample of a host species/Number of infected individuals of the host species in the sample (= mean number of individuals of a particular parasite species per infected host in a sample) (Margolis et al., 1982). ’ Prevalence: Number of individuals of a host species infected with a particular parasite species/Number of hosts examined (Margolis et al., 1982).
269
- a modification of biotic agents (such as parasite attraction, host immunity reactions) or abiotic ones (physicochemical conditions) leading to the fish becoming the definitive host. These two mechanisms may be involved either individually or synergically. It seems unlikely that confinement would be the only cause of this infection; in other words a transgression of the ethological barrier cannot be the only factor responsible. As far as abiotic agents are concerned, it was shown that Polyhbris tubicirrus remained on Sparus auratu and reproduced during summer (temperature above 25°C) as well as in winter marine water (lo-15%) of the fish farm. Thus, transfer of the monogenean to S. auratu does not only happen under special thermic conditions. Among biotic agents, the lowering of the host resistance due to stress is certainly important in this type of transfer. One must remember that if a parasite infests an uncommon host, the latter often reacts more violently. Thus this form of parasitism is sometimes more pathogenic. The signific~t increase of parasite populations recorded during sampling was related to the close confinement caused by hydraulic supply problems: the water had to be recycIed and the inflow into the reservoirs reduced. The gilt head sea breams involved came from a continental French hatchery. The problem of the origin of the parasite has therefore to be solved. As the fish were never caged and had not been in contact with breams of the genus Diplodus before going to Corsica, it is almost certain that first infestations occurred on this island. In this Corsican fish-farm, a sea-water pumping system, with drain-pipes under the beach, prevents the penetration of monogeneans. On the other hand, breams of the genus Diplodus caught in their natural environment and kept next to gilt head sea breams are an obvious cause of parasite transfer whether or not fish of the two genera were in direct contact. In fact, the eggs of Polylubris tubicirrus have a hooked filament by which they can become attached accidentally to a net used also in adjacent reservoirs and so be introduced involuntarily. In order to prevent such transfer from occurring, simple prophylactic measures must be taken: the presence of various species of Teleostei in the same reservoir, especially if they belong to the same family, should be avoided, as should any manipulation which might introduce the parasite. These observations emphasize the importance of parasite transfer to a species which is not a natural host in wild populations; this phenomenon is particularly important if the host specificity is of the “stenoxene” or “euryxene” type (Euzet and Combes, 1980). Thus it is essential that any introduction of hosts must be strictly controlled. New methods of intensive production, such as the introduction of species from temperate zones into subtropical waters in order to hasten their growth, will increase the risks of epizootics. A recent example of this danger is the transfer and proliferation of ~pibde~iu melleni McCallum, 1927, a tropical monogenean with low specificity (Jahn and Kuhn, 1932) on sea bass, Dicentmrchus labmx, which are reared in cages on the French island of Martinique in the West Indies.
270 ACKNOWLEDGEMENT
This research received financial support from the “Institut Franqais de Recherche pour 1’Exploitation de la Mer” (Contract 82/2718).
REFERENCES Euzet, L. and Cauwet, A., 1967. Polylubris diplodi n.g. n.sp. (Monogenea, Microcotylidae), parasite de Tbl6ostbns du genre Diplodus Sparidae. Bull. Mus. Nat. Hist. Nat., Paris, 2 ser., 39: 213-220. Euzet, L. and Combes, C., 1980. Les problsmes de l’esp&ce chez les animaux parasites. In: Les Problames de l’Esp8ce dans le Ri?gne Animal. M&m. Sot. Zool. France, 2: 239-285. Jahn, T.L. and Kuhn, L.R., 1932. The life history of ~p~bdel~a ~el~eni MacCallum, 1927, a monogenetic trematode parasitic on marine fishes. Biol. Bull. (Woods Hole, Mass.), 62: 89-112. Mamaev, Yu.L. and Parukhin, A.M., 1976. The genus Polylabris Euzet et Cauwet, 1967 and some closely related species of microcotylids (Monogenoidea, Microcotylidae). Parazitologiya, 10: 245-254 (in Russian). Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M. and Schad, G.A., 1982. The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists). J. Parasitol., 68 (1): 131-133. Noisy, D., 1978. Recherches sur le microhabitat branchial des Microcotylidae (Monogenea) ectoparaaites de Sparidae (Teleostei). These 3me Cycle, Univ. Sci. Tech. Languedot (Montpellier), 132 pp. Paperna, I. and Baudin-Laurencin, F., 1979. Parasitic infections of sea bass, Dicentrarchus labrax, and gilt head sea bream, Sparus aurafu, in marieulture facilities in France. Aquaculture, 16: 173-175. Paperna, I. and Kahn, A., 1964. Report on monogenetic trematodes collected from East Mediterranean. Rev. Bras. Biol., 24: 249-258. Paperna, I., Colorni, A., Gordin, H. and Kissll, G.H., 1977. Diseases of Sparus aurato in marine culture at Elat. Aquaculture, 10: 195-213.
267
Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands
Short Communication ENLARGEMENT OF THE HOST RANGE OF POLYLABRIS TUBICIRRUS (MONOGENEA, POLYOPISTHOCOTYLEA) UNDER FISH-FARMING CONDITIONS
P. SILAN’, P. CABRAL2 and C. MAILLARD’
1Laboratoire de Parasitologic Comparde (UA CNRS 698), Universitk des Sciences et Techniques du Languedoc, Place E, Bataillon, 34060 Montpellier Ckdex (France) 2Laboratoire d ‘Ichthyo~og~e et de Pa~ito~ogie G&&ale, Wniversitk des Sciences et Techniques du La~uedo~, Place E. Bataillon, 34060 Montpe~lier Ckdex (France) (Accepted
28 March 1985)
ABSTRACT Silan, P., Cabral, P, and Maillard, C., 1985. Enlargement of the host range of Polylabris tubicirrus (Monogenea, Polyopisthocotylea) under fish-farming conditions. Aqua”
culture, 47 : 267-270. In the Medi~~anean Sea, Poty~abr~ tubicirrus (Monogenea, Poly~p~thocotylea) is found only on breams of the genus Diplodus: D. sargus, D. annuls, D. vulgaris. The discovery of this parasite on farmed gilt head sea breams (Sparus au&a) raises the problem of the enlargement of the host range of a parasite under artificial conditions of confinement, and of the potential danger this type of transfer can involve.
INTRODUCI’ION
In the Western Mediterranean Sea, the gilt head sea breams, Sparus auratu, harbor two gill monogeneans. One, Furnestinia echeneis (Wagener, 1857) belongs to the Monopisthocotylea, and one, Microcotyle chrysophrii Van Beneden and Hesse, 1863, to the Polyopisthocotylea. To date the only epizootic linked to a member of the Monogenea was due to Furnestiniu echeneis, which caused considerable damage to cultivated Sparus ff~~ta in the gulf of Elat (Red Sea} (Papema et al., 1977; Papema and Baudin Laurencin, 1979). In 1982 heavy mo~~ities were reported in Corsican raceways (France), and the gilt head sea breams which were examined revealed the presence of a third species of Monogenea never yet found on this fish. RESULTS AND DISCUSSION
On the gills of fingerlings weighing about 50 g, a parasite was identified as ~o~y~~r~ t~~ici~us (Paperna and Kohn, 1964) Mamaev and Parukhin, 1976. 0044-8486/85/$03.30
Q 1985 Elsevier Science Publishers B.V.
268
on which several taxonomic studies have This polyopisthocotylean, been carried out (Paperna and Kohn, 1964; Euzet and Cauwet, 1967; Mamaev and Parukhin, 1976), has never been observed on wild Sparus ~~~~~~(Noisy, 1978; L. Euzet, personal communication, 1985). Polylubris t~bic~rr~s has previously been noted only on Sparidae of the genus Diplod~s: D. surgus, D. unn~~r~s and D. u~lgaris (Euzet and Cauwet, 1967). This species, associated or not with Atriaster heterodus, constitutes 90% of the microcotylidean populations on Diplodus sargus, with mean intensities’ ranging from 3.4 (P. tubicirrus in the presence of A. heterodus) to 3.8 (R tubicirrus alone) (Noisy, 1978). In the same geographical area, Microcotyle chrysophrii is found parasitizing Spurus aurutu with a prevalence’ and an autumnal mean intensity of 85% and 10.6 respectively (Noisy, 1978). M. chrysophrii is also present on the three wild Diplodus spp. Up to now, out of five species of Microcotylidae belonging to the genera Microcotyle Van Beneden and Hess@, 1863, Polylabris Euzet and Cauwet, 1967, Atriuster Mamaev and Parukhin, 1969 and Atrispinum Euzet and Maillard, 1973, it was the only one to be found indifferently parasitizing either Spurus uurutu or the three Diplodus species mentioned above. Since cultivated gilt head sea breams were found to be infested by dozens of Polylabris tubicirrus, it can be stated that: (1) under special conditions of aquaculture (race-way), this species has enlarged its host range; (2) the observed intensities are higher than those noted for M~crocutyle ch~sophri~ in a natural environment; and (3) this monogenean is more numerous than on its usual host, i.e. breams of the genus D~plodus. The transfer of Pulylubris tubici~us to a new host raises the problem of its specificity, as defined by Euzet and Combes (1980), towards Sparidae. These authors refer to specificity as the intersection of the following three sets: the “required scope” for the parasite, “ethological filter” and “biocenosis limits”. Breams of the genus Diplodus and gilt head sea breams belong to nearly the same biocenosis in a natural environment, and thus either the ethological filter prevents Polylubris tubicirrus from reaching Sparus uurutu, or this parasite requires a more restricted scope than does Microco ty le chrysophrii. In the race-ways concerned, the intervention of an ethological filter and required scope would signify: - behavioural variations which increase host accessibility, or 1 Mean intensity: Total number of individuals of a particular parasite species in a sample of a host species/Number of infected individuals of the host species in the sample (= mean number of individuals of a particular parasite species per infected host in a sample) (Margolis et al., 1982). ’ Prevalence: Number of individuals of a host species infected with a particular parasite species/Number of hosts examined (Margolis et al., 1982).
269
- a modification of biotic agents (such as parasite attraction, host immunity reactions) or abiotic ones (physicochemical conditions) leading to the fish becoming the definitive host. These two mechanisms may be involved either individually or synergically. It seems unlikely that confinement would be the only cause of this infection; in other words a transgression of the ethological barrier cannot be the only factor responsible. As far as abiotic agents are concerned, it was shown that Polyhbris tubicirrus remained on Sparus auratu and reproduced during summer (temperature above 25°C) as well as in winter marine water (lo-15%) of the fish farm. Thus, transfer of the monogenean to S. auratu does not only happen under special thermic conditions. Among biotic agents, the lowering of the host resistance due to stress is certainly important in this type of transfer. One must remember that if a parasite infests an uncommon host, the latter often reacts more violently. Thus this form of parasitism is sometimes more pathogenic. The signific~t increase of parasite populations recorded during sampling was related to the close confinement caused by hydraulic supply problems: the water had to be recycIed and the inflow into the reservoirs reduced. The gilt head sea breams involved came from a continental French hatchery. The problem of the origin of the parasite has therefore to be solved. As the fish were never caged and had not been in contact with breams of the genus Diplodus before going to Corsica, it is almost certain that first infestations occurred on this island. In this Corsican fish-farm, a sea-water pumping system, with drain-pipes under the beach, prevents the penetration of monogeneans. On the other hand, breams of the genus Diplodus caught in their natural environment and kept next to gilt head sea breams are an obvious cause of parasite transfer whether or not fish of the two genera were in direct contact. In fact, the eggs of Polylubris tubicirrus have a hooked filament by which they can become attached accidentally to a net used also in adjacent reservoirs and so be introduced involuntarily. In order to prevent such transfer from occurring, simple prophylactic measures must be taken: the presence of various species of Teleostei in the same reservoir, especially if they belong to the same family, should be avoided, as should any manipulation which might introduce the parasite. These observations emphasize the importance of parasite transfer to a species which is not a natural host in wild populations; this phenomenon is particularly important if the host specificity is of the “stenoxene” or “euryxene” type (Euzet and Combes, 1980). Thus it is essential that any introduction of hosts must be strictly controlled. New methods of intensive production, such as the introduction of species from temperate zones into subtropical waters in order to hasten their growth, will increase the risks of epizootics. A recent example of this danger is the transfer and proliferation of ~pibde~iu melleni McCallum, 1927, a tropical monogenean with low specificity (Jahn and Kuhn, 1932) on sea bass, Dicentmrchus labmx, which are reared in cages on the French island of Martinique in the West Indies.
270 ACKNOWLEDGEMENT
This research received financial support from the “Institut Franqais de Recherche pour 1’Exploitation de la Mer” (Contract 82/2718).
REFERENCES Euzet, L. and Cauwet, A., 1967. Polylubris diplodi n.g. n.sp. (Monogenea, Microcotylidae), parasite de Tbl6ostbns du genre Diplodus Sparidae. Bull. Mus. Nat. Hist. Nat., Paris, 2 ser., 39: 213-220. Euzet, L. and Combes, C., 1980. Les problsmes de l’esp&ce chez les animaux parasites. In: Les Problames de l’Esp8ce dans le Ri?gne Animal. M&m. Sot. Zool. France, 2: 239-285. Jahn, T.L. and Kuhn, L.R., 1932. The life history of ~p~bdel~a ~el~eni MacCallum, 1927, a monogenetic trematode parasitic on marine fishes. Biol. Bull. (Woods Hole, Mass.), 62: 89-112. Mamaev, Yu.L. and Parukhin, A.M., 1976. The genus Polylabris Euzet et Cauwet, 1967 and some closely related species of microcotylids (Monogenoidea, Microcotylidae). Parazitologiya, 10: 245-254 (in Russian). Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M. and Schad, G.A., 1982. The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists). J. Parasitol., 68 (1): 131-133. Noisy, D., 1978. Recherches sur le microhabitat branchial des Microcotylidae (Monogenea) ectoparaaites de Sparidae (Teleostei). These 3me Cycle, Univ. Sci. Tech. Languedot (Montpellier), 132 pp. Paperna, I. and Baudin-Laurencin, F., 1979. Parasitic infections of sea bass, Dicentrarchus labrax, and gilt head sea bream, Sparus aurafu, in marieulture facilities in France. Aquaculture, 16: 173-175. Paperna, I. and Kahn, A., 1964. Report on monogenetic trematodes collected from East Mediterranean. Rev. Bras. Biol., 24: 249-258. Paperna, I., Colorni, A., Gordin, H. and Kissll, G.H., 1977. Diseases of Sparus aurato in marine culture at Elat. Aquaculture, 10: 195-213.