Journal of Helminthotogy (1992) 66, 187-192
Abundance/host size relationship in a fish trematode community A. SAAD-FARES. and C. COMBES* Centre de Recherches Marines BP.I23. Jounieh, Liban; * Laboratoire de Biologie Animate, Centre de Biologie el d'Ecologie Tropieale el Mediterraneenne, Universite, 66860 Perpignan, France
ABSTRACT
The abundance of six species of trematodes: Aphanurus stossichi, Bacciger isruelensis, Diphterostomum israelense, Plagioporus idoneus, Lepocreadium album and L. pegorchis, parasitic in the digestive tract of marine teleostei (Sparidae) collected near Jounieh (east Mediterranean), was analysed as a function of the host-size. In two parasite/host systems, infections were observed from the lowest size classes of the sample, with a clear tendency to an increase of abundance in older fish. In four others, parasites appear only above a rather high threshold class, young individuals never being infected. In the last three parasite/host systems, host invasion may occur early or late, but infection decreases above a well defined size class, old fishes rarely or never being infected. A given trematode species, when parasitizing several host species, shows similar abundance/host size relationships, e.g. P. idoneus in Diplodus vulgaris and Oblada melanura. When more than one species of trematode infects a single host species, curves can be markedly distinct; for instance, L. pegorchis was collected from Pagellus erythrinus below 15 cm, whereas D. israelense parasitized the same fish approximately above the same size. There is no evidence that such a replacement of one trematode by another in the course of host growth is a result of interspecific competition. KEY WORDS: abundance, infection dynamics, host-parasite system, competition, host size, Aphanurus slossichi. Bacciger israelensis, Plagioporus idoneus, Lepocreadium album, Lepocreadium pegorchis, Diphterostomum israelense, Trematoda
INTRODUCTION
In parasite/host systems, three types of relationships between parasitism and hostsize can be considered. Firstly, there is the relationship between the number of parasite species and the maximal size of the host: the host species are compared to islands, as in MACARTHUR and WILSON'S biogeographical approach (1967) (e.g., PRICE and CLANCY, 1983; GUEGAN, 1990). Secondly, there is the relationship between the number of parasite species and the size of individuals of a particular host species; this has been very little analysed in parasite/fish systems, although HOLMES (1990) showed that the number of species of helminths was positively correlated with the size of the fish Sebastes nebulosus. Lastly, there is the relationship between a demographic parameter (prevalence, intensity, abundance, etc) of parasitism and the size of individuals of a particular host species: the invasion of a host population by an adult trematode follows a pattern related to age of individual hosts. At birth, every demographic parameter is usually zero; later on, a helminthofauna is acquired, and one may imagine a series of different patterns. For instance, parasitism can increase regularly with time, or there may be a rapid start followed by a plateau due to a regulatory process, or a more tardy acquisition following a phase without parasites, or a decrease or disappearance of parasitism as the host grows older. Patterns of regular increase with age were described long ago in freshwater fish (see DOGIEL, 1964) but such information is very scanty for marine ecosystems. LLEWELLYN (1962) reported data on gill monogeneans from marine fish collected near Plymouth and SCOTT (1975, 1982) analysed intestinal Trematoda
188
A. SAAD-FARES and C. COMBES
from American plaice collected near the Scotian Shelf and the Gulf of St. Lawrence. Due to this incomplete knowledge, it is not currently possible to define either general trends or trends related to particular fish groups, parasite groups or transmission patterns. In the present work, we have analysed the demography of parasitism as a function of the size of individual hosts. The model we studied is represented by the trematodes parasitic in a community of marine fishes collected near the bay of Jounieh (Lebanon). We used abundance as defined by MARGOLIS et al. (1982) to evaluate the demography of parasitism because we think it is the most reliable parameter reflecting the populational aspects of parasite-host relationships. Our aim is to compare the relationships between abundance and host-size in a single trematode species parasitizing different hosts and in various trematode species parasitizing the same host.
MATERIALS AND METHODS Six species of fish, belonging to the family Sparidae, were examined (sample size in parentheses): Diplodus sargus (187), D. vulgaris (130), Lithognathus mormyrus (341), Pagellus erythrinus (191), Boops boops (286), and Oblada melanura (97). All the fish studied were collected in 1983 to 1984 by local fishermen near the bay of Jounieh. The techniques used for fishing did not allow them to go further than 15 km north or south of the port of Jounieh, nor more than 5 km away from the coast (MOUNEIMME, 1978). Each fish was measured (forklength). Lengths were classed into 2 cm length groups. It was then dissected and all the helminths living within the gastrointestinal tract were collected, fixed and prepared for microscopy.
RESULTS Same parasite species/different hosts One of the major characteristics of our survey is to show that the same trematode offers similar infection dynamics when present in different fish species. Three trematodes illustrate this rule (Fig. 1): Plagioporus idoneus which infects both Diplodus vulgaris and Oblada melanura; Diphterostonum israelense in Pagellus erythrinus and Diplodus sargus; and Lepocreadium pegorchis in Pagellus erythrinus and Lithognathus mormyrus. The most representative case is that of P. idoneus. The parasite is present only in fishes exceeding a threshold size class. The histogram of abundances shows a regular increase with size above this class. The only difference between the two parasite species lies in the value of the threshold class: 12 cm in D. vulgaris, 16 cm in O. melanura. In D. israelense, this pattern shows a threshold class in both hosts but a regular increase is shown only in P. erythrinus. An opposite abundance/host-size relationship is seen in L. pegorchis, but, again, is similar in both fish: in P. erythrinus, the graph shows a sharp decrease in abundance from the size class 12-14 cm upwards; beyond this size, the presence of L. pegorchis is exceptional though the number of fish sampled is high. In L. mormyrus, L. pegorchis is abundant in small fish (less than 12 cm) and becomes very
Abundance/host size relationship in a fish trematode community
0.6
189
Ptagioponis idoneus | in Diplodus vulgaris Q in Obfada metanura
0.5 0.4 0.3 0.2 0.1
Diplodus vulgaris Obtada melamjta
i Lepocreadium pegorchis p •• in Pages Pagellus eythrinus erythrinus i Lithognathus Lithth mormyrus ff] in
Diphlerostomum israelense • in Pagellus erythnnus Q in Diplodus sargus
2.0
2.0
1.6
1.6
1.2
1.2
0.8
0.8
0.4
0.4 (see text)
Pagellus erylhrinus Diplodus sargus
Size-classes
55 27 25 13 30 24 12 32 46 42
Pagellus 22
erylhrinus
Lithognathus
mormyrus
Size-classes
30
24 30
: : : : 8 is
s ~i s ; s
FIG. 1. Abundance size-class relationships for the same parasite in two different host species. For both figures sample size is represented on the boxes on top of each size-class.
rare in large fish. However, we must note that a single individual of L. mormyrus, measuring 28 cm, was infected with more than 2000 L. pegorchis; this is an exceptional intensity for which we can provide no explanation. This fish is not taken into account in the figure. Different parasite species/same host We observed two opposite results, depending on the fish species, (a) Similar pattern for the two trematode species (Fig. 2). This was observed in two cases: Aphanurus stossichi and Bacciger israelensis in Boops boops; and Plagioporus idoneus and Lepocreadium album in Oblada melanura. In B. boops, A. stossichi and B. israelensis are present in the smallest fish captured and abundance increases with size. The individual intensities frequently
190
A. SAAD-FARES and C. COMBES
S
PIagioporus idoneus Lepocreadium album in Oblada melanura
2.5 2.0 1.5
Size-classes
1 ;
? f
g § 5
FIG. 2. Abundance size-class relationships for different parasite species showing similar pattern in the same host.
exceed the value of 100 parasites per host, from the 12-14 cm size class upwards. Those of B. israelensis are the highest in our survey, since they can reach 1000 parasites per fish. It should also be noted that the abundance of B. israelensis shows a step (arrow in Fig. 2) at size-class 12-14 cm. In O. melanura, the patterns of P. idoneus and L. album are similar, but to a lesser extent, since the abundance of P. idoneus increases regularly with host size, while L. album shows first an increase (to size-class 20-22) and then a decrease. However, the number of individuals of fish examined is lower in O. melanura than in the other fish (especially in size-class 18-20 and 20-22 cm) and this could weaken the comparison. (b) Dissimilar patterns for the two trematode species (Fig. 1). This is illustrated by the trematodes in Pagellus erythrinus. In this fish, L. pegorchis (see above) is abundant from the smallest fish and decreases sharply from 12-14 cm size-class. On the contrary D. israelense is only present in fishes measuring over 14 cm and a marked increase in abundance is observed in fishes exceeding 20 cm.
DISCUSSION In the majority of the parasite-host systems analysed, there is a positive correlation between the abundance of parasitism and the fish size. In some of them, the parasite is present from the lowest size-class, in others there is a threshold size situated inside the limits of our sample. The correlation between the abundance of the parasites and the host size is clearly negative only in the systems including the trematode L. pegorchis. In a survey on samples from natural populations, it is difficult to determine the causes of the observed variations. However, it is probable that all the parasites studied (though the life cycles are not all known) infect fish through ingestion of an intermediate host carrying the metacercariae. It therefore seems reasonable to assume, as did Scott (1975, 1982), that the changes in parasite abundance are correlated to changes in the fish's diet. The latter can have two origins: either a different
Abundance/host size relationship in a fish trematode community
191
choice of prey as the fish grows, or fish migration to a new biocenosis having a different composition. Hypotheses calling changes in diet into play seem more probable than those based on "stage specificity", which would imply either a change in immune defence processes or a significant variation in the parasite's environment, inside the gut, as the fish grows older. The fact that the same trematode offers similar infection dynamics when present in different fish species seems to favour the hypothesis of infestation by prey which the fish selects on the basis of size. Such an explanation can apply both when the abundance increases with size (as in the case of P. idoneus in D. vulgaris and O. melanura; and D. israelense in P. erythrinus and D. sargus) and when it decreases (as in the case of L. pegorchis in P. erythrinus and L. mormyrus). When two different parasites in the same host show similar patterns, as A. stossichi and B. israelensis in B. boops, this could orient the research towards a comparable or even common mode of transmission. When the infection dynamics are opposite, as in D. israelense and L. pegorchis in P. erythrinus, there is a real "fauna replacement" in the fish, in the course of its life. The gradual disappearance of one of the trematode species could perhaps be due to the infection of the host by the second trematode species implying exclusion by competition. However, the example of B. boops, whose trematodes exhibit the highest abundances registered in our survey, without any sign of mutual exclusion, demonstrates that no competition occurs in that particular case. For most species of parasites studied in this survey, we had samples large enough in number and offering a sufficient range of different sizes, to analyse the relationships with host size. Although a correlation is generally taken to exist between size and age, it is, however, necessary to recall that (i) the correlation between the size of a fish and its real age is approximate, (ii) the correlation is different in different fish species, and (iii) the correlation is contingent upon environmental conditions. Despite this reservation on the precise relationship between age and size, our survey demonstrates that the age structure of fish populations has a marked influence on the distribution of parasite populations. This age/size relationship is probably one of the major factors which contribute to the aggregated character of these distributions.
REFERENCES DOGIEL, V. A. (1964) General Parasitology. Revised and enlarged by Yu. I. Polyanski and E. M. Kheisin. Oliver and Boyd: Edinburgh and London. (English edition). GUEGAN, J. F. (1990) Structure des peuplements parasitaires: Ic modelc Monogenes de Cyprinidae Ouest-Africains. These Doctoral (U.S.T.L. Monlpellier. France), 209 pp. HOLMES, J. C. (1990) Helminth communities in marine fishes. In: Parasile Communities. Patterns and Processes (editor, G. Esch, A. Bush and J. Aho) pp. 101-130 Chapman and Hull: London, New York. LLEWELLYN. J. (1962) The life histories and population dynamics of monogcncan gill parasites of Trachurus trachurus (L.). Journal of the Marine Biological Association of the United Kingdom,
42, 587-600. MACARTHUR, R. H. & WILSON, E. O. (1967) The theory of island biogcography. Princeton University Press, Princeton. New York. MARGOLIS, L..ESCH.G. W., HOLMES. J C , KUR1S. A. M.&SCHAD.G. A. (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology, 68, 131-133. MOUNEIMNE, N. (1978) Poissons des cotes du Liban (Mediterranee Orientale). Biologic et peche. These Doctoral Etat (Uniy. Paris VI), 490 pp. PRICE, P. W. & CLANCY. K. M. (1983) Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitologv, 69, 449-454.
192
A. SAAD-FARES and C. COMBES
SCOTT, J. S. (1975) Incidence of trematode parasites of American plaice (Hippoglossoides platessoides) of the Scotian Shelf and Gulf of St. Lawrence in relation to fish length and food. Journal of the Fisheries Research Board of Canada, 32, 479—483. SCOTT, J. S. (1982) Digenean parasite communities in flatfishes of the Scotian Shelf and southern Gulf of St. Lawrence. Canadian Journal of Zoology, 60, 2804-11. Accepted26th February, 1992.
Abundance/host size relationship in a fish trematode community A. SAAD-FARES. and C. COMBES* Centre de Recherches Marines BP.I23. Jounieh, Liban; * Laboratoire de Biologie Animate, Centre de Biologie el d'Ecologie Tropieale el Mediterraneenne, Universite, 66860 Perpignan, France
ABSTRACT
The abundance of six species of trematodes: Aphanurus stossichi, Bacciger isruelensis, Diphterostomum israelense, Plagioporus idoneus, Lepocreadium album and L. pegorchis, parasitic in the digestive tract of marine teleostei (Sparidae) collected near Jounieh (east Mediterranean), was analysed as a function of the host-size. In two parasite/host systems, infections were observed from the lowest size classes of the sample, with a clear tendency to an increase of abundance in older fish. In four others, parasites appear only above a rather high threshold class, young individuals never being infected. In the last three parasite/host systems, host invasion may occur early or late, but infection decreases above a well defined size class, old fishes rarely or never being infected. A given trematode species, when parasitizing several host species, shows similar abundance/host size relationships, e.g. P. idoneus in Diplodus vulgaris and Oblada melanura. When more than one species of trematode infects a single host species, curves can be markedly distinct; for instance, L. pegorchis was collected from Pagellus erythrinus below 15 cm, whereas D. israelense parasitized the same fish approximately above the same size. There is no evidence that such a replacement of one trematode by another in the course of host growth is a result of interspecific competition. KEY WORDS: abundance, infection dynamics, host-parasite system, competition, host size, Aphanurus slossichi. Bacciger israelensis, Plagioporus idoneus, Lepocreadium album, Lepocreadium pegorchis, Diphterostomum israelense, Trematoda
INTRODUCTION
In parasite/host systems, three types of relationships between parasitism and hostsize can be considered. Firstly, there is the relationship between the number of parasite species and the maximal size of the host: the host species are compared to islands, as in MACARTHUR and WILSON'S biogeographical approach (1967) (e.g., PRICE and CLANCY, 1983; GUEGAN, 1990). Secondly, there is the relationship between the number of parasite species and the size of individuals of a particular host species; this has been very little analysed in parasite/fish systems, although HOLMES (1990) showed that the number of species of helminths was positively correlated with the size of the fish Sebastes nebulosus. Lastly, there is the relationship between a demographic parameter (prevalence, intensity, abundance, etc) of parasitism and the size of individuals of a particular host species: the invasion of a host population by an adult trematode follows a pattern related to age of individual hosts. At birth, every demographic parameter is usually zero; later on, a helminthofauna is acquired, and one may imagine a series of different patterns. For instance, parasitism can increase regularly with time, or there may be a rapid start followed by a plateau due to a regulatory process, or a more tardy acquisition following a phase without parasites, or a decrease or disappearance of parasitism as the host grows older. Patterns of regular increase with age were described long ago in freshwater fish (see DOGIEL, 1964) but such information is very scanty for marine ecosystems. LLEWELLYN (1962) reported data on gill monogeneans from marine fish collected near Plymouth and SCOTT (1975, 1982) analysed intestinal Trematoda
188
A. SAAD-FARES and C. COMBES
from American plaice collected near the Scotian Shelf and the Gulf of St. Lawrence. Due to this incomplete knowledge, it is not currently possible to define either general trends or trends related to particular fish groups, parasite groups or transmission patterns. In the present work, we have analysed the demography of parasitism as a function of the size of individual hosts. The model we studied is represented by the trematodes parasitic in a community of marine fishes collected near the bay of Jounieh (Lebanon). We used abundance as defined by MARGOLIS et al. (1982) to evaluate the demography of parasitism because we think it is the most reliable parameter reflecting the populational aspects of parasite-host relationships. Our aim is to compare the relationships between abundance and host-size in a single trematode species parasitizing different hosts and in various trematode species parasitizing the same host.
MATERIALS AND METHODS Six species of fish, belonging to the family Sparidae, were examined (sample size in parentheses): Diplodus sargus (187), D. vulgaris (130), Lithognathus mormyrus (341), Pagellus erythrinus (191), Boops boops (286), and Oblada melanura (97). All the fish studied were collected in 1983 to 1984 by local fishermen near the bay of Jounieh. The techniques used for fishing did not allow them to go further than 15 km north or south of the port of Jounieh, nor more than 5 km away from the coast (MOUNEIMME, 1978). Each fish was measured (forklength). Lengths were classed into 2 cm length groups. It was then dissected and all the helminths living within the gastrointestinal tract were collected, fixed and prepared for microscopy.
RESULTS Same parasite species/different hosts One of the major characteristics of our survey is to show that the same trematode offers similar infection dynamics when present in different fish species. Three trematodes illustrate this rule (Fig. 1): Plagioporus idoneus which infects both Diplodus vulgaris and Oblada melanura; Diphterostonum israelense in Pagellus erythrinus and Diplodus sargus; and Lepocreadium pegorchis in Pagellus erythrinus and Lithognathus mormyrus. The most representative case is that of P. idoneus. The parasite is present only in fishes exceeding a threshold size class. The histogram of abundances shows a regular increase with size above this class. The only difference between the two parasite species lies in the value of the threshold class: 12 cm in D. vulgaris, 16 cm in O. melanura. In D. israelense, this pattern shows a threshold class in both hosts but a regular increase is shown only in P. erythrinus. An opposite abundance/host-size relationship is seen in L. pegorchis, but, again, is similar in both fish: in P. erythrinus, the graph shows a sharp decrease in abundance from the size class 12-14 cm upwards; beyond this size, the presence of L. pegorchis is exceptional though the number of fish sampled is high. In L. mormyrus, L. pegorchis is abundant in small fish (less than 12 cm) and becomes very
Abundance/host size relationship in a fish trematode community
0.6
189
Ptagioponis idoneus | in Diplodus vulgaris Q in Obfada metanura
0.5 0.4 0.3 0.2 0.1
Diplodus vulgaris Obtada melamjta
i Lepocreadium pegorchis p •• in Pages Pagellus eythrinus erythrinus i Lithognathus Lithth mormyrus ff] in
Diphlerostomum israelense • in Pagellus erythnnus Q in Diplodus sargus
2.0
2.0
1.6
1.6
1.2
1.2
0.8
0.8
0.4
0.4 (see text)
Pagellus erylhrinus Diplodus sargus
Size-classes
55 27 25 13 30 24 12 32 46 42
Pagellus 22
erylhrinus
Lithognathus
mormyrus
Size-classes
30
24 30
: : : : 8 is
s ~i s ; s
FIG. 1. Abundance size-class relationships for the same parasite in two different host species. For both figures sample size is represented on the boxes on top of each size-class.
rare in large fish. However, we must note that a single individual of L. mormyrus, measuring 28 cm, was infected with more than 2000 L. pegorchis; this is an exceptional intensity for which we can provide no explanation. This fish is not taken into account in the figure. Different parasite species/same host We observed two opposite results, depending on the fish species, (a) Similar pattern for the two trematode species (Fig. 2). This was observed in two cases: Aphanurus stossichi and Bacciger israelensis in Boops boops; and Plagioporus idoneus and Lepocreadium album in Oblada melanura. In B. boops, A. stossichi and B. israelensis are present in the smallest fish captured and abundance increases with size. The individual intensities frequently
190
A. SAAD-FARES and C. COMBES
S
PIagioporus idoneus Lepocreadium album in Oblada melanura
2.5 2.0 1.5
Size-classes
1 ;
? f
g § 5
FIG. 2. Abundance size-class relationships for different parasite species showing similar pattern in the same host.
exceed the value of 100 parasites per host, from the 12-14 cm size class upwards. Those of B. israelensis are the highest in our survey, since they can reach 1000 parasites per fish. It should also be noted that the abundance of B. israelensis shows a step (arrow in Fig. 2) at size-class 12-14 cm. In O. melanura, the patterns of P. idoneus and L. album are similar, but to a lesser extent, since the abundance of P. idoneus increases regularly with host size, while L. album shows first an increase (to size-class 20-22) and then a decrease. However, the number of individuals of fish examined is lower in O. melanura than in the other fish (especially in size-class 18-20 and 20-22 cm) and this could weaken the comparison. (b) Dissimilar patterns for the two trematode species (Fig. 1). This is illustrated by the trematodes in Pagellus erythrinus. In this fish, L. pegorchis (see above) is abundant from the smallest fish and decreases sharply from 12-14 cm size-class. On the contrary D. israelense is only present in fishes measuring over 14 cm and a marked increase in abundance is observed in fishes exceeding 20 cm.
DISCUSSION In the majority of the parasite-host systems analysed, there is a positive correlation between the abundance of parasitism and the fish size. In some of them, the parasite is present from the lowest size-class, in others there is a threshold size situated inside the limits of our sample. The correlation between the abundance of the parasites and the host size is clearly negative only in the systems including the trematode L. pegorchis. In a survey on samples from natural populations, it is difficult to determine the causes of the observed variations. However, it is probable that all the parasites studied (though the life cycles are not all known) infect fish through ingestion of an intermediate host carrying the metacercariae. It therefore seems reasonable to assume, as did Scott (1975, 1982), that the changes in parasite abundance are correlated to changes in the fish's diet. The latter can have two origins: either a different
Abundance/host size relationship in a fish trematode community
191
choice of prey as the fish grows, or fish migration to a new biocenosis having a different composition. Hypotheses calling changes in diet into play seem more probable than those based on "stage specificity", which would imply either a change in immune defence processes or a significant variation in the parasite's environment, inside the gut, as the fish grows older. The fact that the same trematode offers similar infection dynamics when present in different fish species seems to favour the hypothesis of infestation by prey which the fish selects on the basis of size. Such an explanation can apply both when the abundance increases with size (as in the case of P. idoneus in D. vulgaris and O. melanura; and D. israelense in P. erythrinus and D. sargus) and when it decreases (as in the case of L. pegorchis in P. erythrinus and L. mormyrus). When two different parasites in the same host show similar patterns, as A. stossichi and B. israelensis in B. boops, this could orient the research towards a comparable or even common mode of transmission. When the infection dynamics are opposite, as in D. israelense and L. pegorchis in P. erythrinus, there is a real "fauna replacement" in the fish, in the course of its life. The gradual disappearance of one of the trematode species could perhaps be due to the infection of the host by the second trematode species implying exclusion by competition. However, the example of B. boops, whose trematodes exhibit the highest abundances registered in our survey, without any sign of mutual exclusion, demonstrates that no competition occurs in that particular case. For most species of parasites studied in this survey, we had samples large enough in number and offering a sufficient range of different sizes, to analyse the relationships with host size. Although a correlation is generally taken to exist between size and age, it is, however, necessary to recall that (i) the correlation between the size of a fish and its real age is approximate, (ii) the correlation is different in different fish species, and (iii) the correlation is contingent upon environmental conditions. Despite this reservation on the precise relationship between age and size, our survey demonstrates that the age structure of fish populations has a marked influence on the distribution of parasite populations. This age/size relationship is probably one of the major factors which contribute to the aggregated character of these distributions.
REFERENCES DOGIEL, V. A. (1964) General Parasitology. Revised and enlarged by Yu. I. Polyanski and E. M. Kheisin. Oliver and Boyd: Edinburgh and London. (English edition). GUEGAN, J. F. (1990) Structure des peuplements parasitaires: Ic modelc Monogenes de Cyprinidae Ouest-Africains. These Doctoral (U.S.T.L. Monlpellier. France), 209 pp. HOLMES, J. C. (1990) Helminth communities in marine fishes. In: Parasile Communities. Patterns and Processes (editor, G. Esch, A. Bush and J. Aho) pp. 101-130 Chapman and Hull: London, New York. LLEWELLYN. J. (1962) The life histories and population dynamics of monogcncan gill parasites of Trachurus trachurus (L.). Journal of the Marine Biological Association of the United Kingdom,
42, 587-600. MACARTHUR, R. H. & WILSON, E. O. (1967) The theory of island biogcography. Princeton University Press, Princeton. New York. MARGOLIS, L..ESCH.G. W., HOLMES. J C , KUR1S. A. M.&SCHAD.G. A. (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology, 68, 131-133. MOUNEIMNE, N. (1978) Poissons des cotes du Liban (Mediterranee Orientale). Biologic et peche. These Doctoral Etat (Uniy. Paris VI), 490 pp. PRICE, P. W. & CLANCY. K. M. (1983) Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitologv, 69, 449-454.
192
A. SAAD-FARES and C. COMBES
SCOTT, J. S. (1975) Incidence of trematode parasites of American plaice (Hippoglossoides platessoides) of the Scotian Shelf and Gulf of St. Lawrence in relation to fish length and food. Journal of the Fisheries Research Board of Canada, 32, 479—483. SCOTT, J. S. (1982) Digenean parasite communities in flatfishes of the Scotian Shelf and southern Gulf of St. Lawrence. Canadian Journal of Zoology, 60, 2804-11. Accepted26th February, 1992.
