The occurrence, site specificity and frequency distribution of Bicotyle vellavoli on Pampus chinensis and Pampus argenteus

THE OCCURRENCE, SITE SPECIFICITY AND FREQUENCY DISTRIBUTION OF BICOTYLE VELLA VOLI ON RAJPUT CH~~E~~rS AND PAMPUS A~GE~~EU~ P. RAMASAMYand

K. RAMALINGAM

Department of Zoology, Life Science Building, University of Madras, Madras 600 02.5, India (Received 20 April 1988;accepted 10 May 1989) Abstract-R,v.iAsAMY P. and RAMALINGAM K. 1989. The occurrence, site specificity and frequency distribution of Bicotyle vellavoli on Patnpus chinensis and Pampus argenteus. International Journal for Parasitology 19: 761-767. The occurrence of Bicotyle vellavoli and copepods at 10 fishing centres along the coast of South India, the site specificity of B. veNavoliand its frequency distribution on Pampus chinensisand P. argenteus were studied. A higher level of prevalence and abundance of 3. vellavoli was recorded on P. ehinensis than on P. argenteus indicating specific differences in host susceptibility. The parasite was significantly less abundant on P. chinensis taken from Madras than on fish from Mandapam, and significantly more abundant on hosts from Madras than those from Pondicherry. The largest ntimbers of B. vellavoli occurred on gill I with decreasing prevalence towards gill IV. The parasite exhibited preference for attachment to the most anterior region of the gills. The differences in B. vellavoli numbers between gills and sectors are not due to area differences. B. vellavoli was overdispersed in both host species populations, and the expected distribution on the basis of the negative binomial was found to be very close to the observed dist~bution on 70-160 and 270-3.50 mm size classes of P. ch~ensis, and on 70-260 mm P. argenteus. INDEX KEY WORDS: BicotyIe vellavoli; Monogenea; Copepoda; Pampus chinensis; Pampus argenteus; site specificity; host specificity; frequency distribution.

INTRODUCT ION

Mahabalipuram, Pondiche~y, Karaikal, Nagapattin~, Point Calimere. Keelakarai, Tiruchendur and Thootur were fixed (within i h of fish capture) in 10% formalin and examined at Madras within a month from the date of collection. The numbers of specimens obtained from each locality are given in Table la. The prevalence (percentage of fish infected = number of individuals of a host species infected with a particular parasite species divided by total number of hosts examined) and abundance or relative density (mean number ofparasites per fish = total number of individuals of a particular parasite species in a sample of hosts divided by total number of individuals (infected and uninfected) of the host species examined = mean number of individuals of a particular parasite species per host examined) of B. veflavoliand copepods for each location were calculated by following Margolis, Esch, Holmes, Kuris & Schad (1982). The non-pammetric Mann-Whitney test (see Zar, 1974) was used as followed by Rohde (1977a) to determine heterogeneity in parasite burden (B. vellavoli) for places where more than 10 hosts were examined. Though the sample size from other localities was small (less than 10 hosts), the parasite burden is given for all the localities (Table 1a.b). A total of 2 13 P. chinensis and 138 P. arzenteus obtained from Madras were used to determine prevalence, abundance and frequency distribution of B. ve~lavolion different size classes of hosts. One-way analysis of variance for unequat samples was carried out following the procedure of Sokal & Rohlf (1981) to determine if significant differences in infection levels were present among different size classes of P. chinensis. The stage of maturity of each parasite was

SPECIES of the genus Bicoryle (Monogenea) occurring on the gills of pomfrets, Pampus chinensis and P. argenteus include four valid species as recognized by

Lebedev (1968) and all are recorded from one or the other species of pomfrets (Goto, 1894; Tripathi, 1956; Unnithan, 1961). The surface topography of B. vellavoliwas described by Ramasamy & Hanna (1986). in spite of the interest shown by various authors in describing the morphology of Bicotyk spp., ecological aspects of the parasites remain neglected. The present report describes the occurrence of B. vellavoli on pomfrets obtained from 10 fishing centres along the coast of South India. Site specificity, prevaience, abundance and frequency dist~bution of B. ve~lavoli on different size classes of hosts were determined for fish landed at Madras. MATERJALS AND METHODS Two hundred and fifty-three specimens of P. chinensis of the size range 70-350 mm (fork length) and 197 snecimens of P. argenteui of the range 70-260 r&n were take~(~~in 1h of captare) from catches of local fishermen at 10 fishing centres along the coast of South India between January 1978 and December 1980. Fish taken from Madras and Mandapam were examined for parasites within an hour of landing. Fish (size composition of the fish in the samples ranged from 7&350 mm) obtained from other centres, namely 761

762

P. RAMASAMY and K. RAMAL~NGAM

determined by the following criteria: Juvenile: Parasites with one-six pairs of clamps and the reproductive system in the initial phase of differentiation. Immature: Each worm possesses more than six pairs of clamps but less than 12 large sucker clamps on one side of the haptor and less than 26 small pincer clamps on the other side; reproductive system fully developed but without eggs.

TABLE 1a-THE

Adult: Each parasite had 13-19 large sucker clamps and 2740 small pincer clamps; eggs present in the uterus. Frequency distribution was tested for goodness-of-fit against negative binomial and Poisson distribution using a corrected Chi-square test (Elliot, 1977). The site preference of B. vellavoli was determined for right- and left-side gills (numbered ILIV from the arch immediately below the

PREVALENCE (PERCENTAGE OF HOSTSINFECTED)ANDABUNDANCE (MEANNUMBEROF PARASITES PERHOST)OF B. veilavoli

ANDTHENUMAEROFHOSTSEXAMINEDATFISHINGCENTRES(LISTEDFROMNORTHTOSOuTH)(DATE,S)OFcOLLEcT,ON)ALONCTHECOASTOF

Sourn

P. chinensis

P. argen feus

Prevalence (%) Abundance Number of hosts examined Prevalence (%) Abundance Number of hosts examined Comparisons

S. chinensis

70.8 4.4

100 1st

75.3 2.3

75 0.7t

100 2t

100 4t

_ -

93.3 7

213 22.5

2 66.6

12 -

4 _

1 _

2 66.6

20

15 41.7

2.7t

0.4t

3

5

0.45

1.3t

~

138

3

_

_

of abundance

Mann-Whitney

* Statistically different. - Hosts were not available. t Comparisons were not carried

Host species

Parasite

AT

10

100

It

3t

3

1

-

0.33

~

48

_

_

U

out due to small sample size.

P.chinensis

~~THEPREVALEN~EANDABUNDANCEOFECTOPARASITICCOPEPODSONTHEHOSTSOFPOMFRETS EXAMINED

33.3

1278* 1876* 141* 1763*

1: vs$ $ vs II IIvs§ $ vs II

S. argenteus

TABLE

INDIA

FISHING CENTRES

(LISTED FROM NORTH TO SOUTH) ALONG THE COAST OF SOUTH

AND

P.argenteus

INDIA

species 1 2 E

P. chinensis

P. argenteus

Caligus stromatei Colobomatus stromatei Lernaeenicus stromatei Caligus sp.

Prevalence Abundance Prevalence Abundance Prevalance Abundance Prevalence Abundance

15.38% 0.27 3.85% 0.04 0 0 0 0

75% 1.25 0 0 0 0 0 0

100% 10.27 0 0 0 0 -

75% 23.25 100% 1.75 100% 8.50 -

0, Parasites absent; -, hosts were not available. Note that numbers of hosts examined at fishing centres are as in Table la.

0 0 0 0 0 0 _ _

0 0 0 0 0 0 0 0

0 0

0 0 0

0 17.64% 1.18 2.17% 0.06

0 0 0 0 0 0 -

0 0 0 0 0 0 -

763

Occurrence, site specificityand frequency distribution of B. vellavoli operculum) and for different regions along the anteriorposterior axis of the giI1.Each gill was divided into four equal regions so that the base Iine of each section had the same length along the ante~or-posterior axis: (i) the anterior region, near the mouth; (ii) the anterior middle; (iii) postetior middle; and (iv) posterior regions (see Rohde, 1977a,b,c, 1979, 1980). The number of parasites on each arch and on each region of the gill was recorded. To determine the differences, if any, in parasite numbers between gills and different regions of a gill, the areas of the gills and sections were determined by following the method of Hughes (1984) and the data were compared with parasite numbers by using the Chi-square test. RESULTS The occurrence of B. vellavoli along the coast of South India The prevalence and abundance of B. ve~~avo~i and

the number of hosts examined at each fishing centre are given in Table 1a. B. veliavoli occurred everywhere but its prevalence and abundance varied from centre to centre. The non-parametric Mann-Whitney test revealed that the parasites were significantly less abundant on P. chinensis taken from Madras than on fish from Mandapam, and significantly more abundant on hosts from Madras than those from Pondicherry. The abundance of parasites on P. argenfeus obtained from Madras and Mandapam was significantly different (see Table la). Higher levels of prevalence and abundance of B. ve~~avol~were recorded on P. chinens~ (prevalence 33-lOO%, abundance 0.7-7 parasites~fish) than on P. argenteus (prevalence 20-66.6%, abundance 0.3-2.7 parasites/ fish).

Site of occurrence, prevalence and abun~n~e of copepo~ along the coast of South India There were three types of copepods, Caligus stromutei, ~oloborna~~s stromatei and ~ernaee~ie~s stromatei, which occurred on P. chinensis. In contrast, the Cakgus sp. alone was encountered on P. argenteus. Caligus sp. occurred mostly in the mouth cavity and a few on the gill filaments. Colobomatus sp. occurred in the nasal fossae whereas Lernaeenicus occurred on the

body surface. The prevalence and abundance copepods are given in Table 1b.

Site preference of B. vellavoli Each specimen of 8. veHavolioccurred between the

adjacent external or internal gill filaments of all gills in both host species and positioned parallel to the axial flow of the ventilation current. However, the greatest number of parasites was recorded on gill I, with progressively fewer towards gill IV (Table 2). The distribution of B. vellavoli along the anterio-posterior axis of the gill is illustrated in Fig. 1A,B. The parasites occurred mainly on the anterior region (i), and to a lesser extent on the posterior region (iv). Relatively few parasites were found on the anterior middle (ii) and posterior middle (iii) positions. The differences in parasite numbers were not due to differences in area of the various gills and gill sections (Table 3).

TABLET-THETOTALNUMBERO~ B.ve~Iavo~~ RE~RDEDONTHE GILLSOF 213 P. C&%W~SAND 138 P.argenteus

Host species

Theprevalence andabundance of B. vellavoli in various host size classes On P. chinensis, the abundance

of B. vellavoli appeared to increase with host-size from 3.04 parasites/fish (70-160 mm size class) to 6.98 parasites/ fish (170-260 mm size class). Thereafter the abundance decreased in the largest size class (2.69 parasites/fish in 270-350 mm size class). The prevalence was similar (71% in 70-160 mm size class; 73% in 170-260 mm size class; 69% in 2’70-350 mm size class) on all size classes of host. On different size classes of P. argenteus, the prevalence of B. vellavoli varied from 16 to 34% and the abundance from 0.3 to 0.7 parasites/fish. The relationship between the host size class and parasite burden was tested by one-way analysis of variance which revealed that the differences among the different size classes of the host P. chinensis were nonsignificant. In both host species, the juveniles and immature worms, in addition to a few adults ones, were observed to occur only on the 70-160 mm size classes of hosts. On the 170-260 and 270-350 mm size classes, juveniles and immature parasites were absent.

of the

P. chinensis W) P. argenteus WI

Gill arch I

II

III

IV

516 (55.84)

186 (20.13)

114 (12.34)

108 (11.68)

(4?!7)

(28?7)

(19%)

(11.:1)

FIG. 1. Diagram illustrating site-specificity of E. vellavoli along the anterio-posterior axis of the host gills (i = anterior region; ii = anterior middle region; iii = posterior middle region; iv = posterior region). The figures represent the total number of parasites recorded from 213 P. chinensis(A) and from 138 P. argenteics (B).

P.

764 TAELE ~-GILL

RAMASAMY and IL RAMALINCAM

AREA MEASUREMENT. EXPECTEDNUMBERCIPPARASITES IN DIFFERENTGILLARCHES AND REGKMOP A cx I

Body weight of a

Totat gill area (mm’)*

Gill area/body weight (mm’ g-‘)

248,713.50 116,563.62

452 777

fish (g) P. chinensis

P. argenteus

5.50 150

Secondary

gill lamellae per mm one side 22 26

Areas of gill arches (mm’) [Expected no. of parasites] Gill arch P. chinensis

P. arge~teus

I

II

111

IV

X2?

33,915.19 [251.94]

32,219.82 1246.771

30,228.37 1224.551

27,027.41 [200.74]

389.48 P < 0.001

16092.38 [17.00]

15129.75 [l&00]

14,537.90 [l&00]

12521.88 [ 14.00]

I I .23 P < 0.025

Areas (mm’) in different regions of gill arch I [Expected no. of parasites] Gill region i (anterior) P. chinensis

P. argenteus

2650.74 [72.22] 3748.16 114.671

ii (anterior

middle)

(posterior

9978.14 [271.85] 5737.99 122.461

111 middle)

14,113.44 [384.51] 4450.94 [17.43]

iv (posterior) 7172.88 [195.42] 2155.19 [8.44]

6945.15 P < 0.001 72.68 P < 0.001

* Measurement of secondary lamellar area is carried out using single lamella dissected out from tip, middle and base ofeach selected filament (every 5th filament) from the II gill arch. Tracings are made on a graph paper using a camera lucida and the number of squares were counted. 7 Expected values were compared with observed values in Table 2. $ Expected values were compared with observed values in Fig. IA, B. Frequency distribution of B. vellavoli The frequency distribution of B. velluvoli was determined for the 70-l 60, 170-260 and 270-350 mm size classes of P. chinensis and for the 70-260 mm size group of P. argenteus. The parasite was grossly overdispersed on the three size classes of P. chinensis but less highly overdispersed on P. argenteus (Figs. Za,b,c, 3). The degree of overdispersion was greatest in the 170-260 mm P. chjne~sis. The estimate of negative binomial distribution was found to correspond closely to the observed frequency distributions of 3. ve~~avoli on the 7&160 and 270-350 mm size ciasses of P. chinensis and on the 70-260 mm size class of P. argenteus (Figs. 2a, c, 3). The Poisson distribution did not fit well. Neither the estimate of negative binomial distribution nor the Poisson distribution fitted the observed frequency distribution of B. vellavoli on the 170-260 mm size class of P. chinensis (Fig.Zb). DISCUSSION The significant differences in prevalence, abundance and frequency distribution of B. ve~~avo~~ on P. ch~~e~sisand P. argenteus might be due to differences in host sus~ptibility to infection or to ecological and behavioural differences which render P. argenteus less liable to infection. 3. vellavoli occurred on both P.

chinensis and P. argenteus at all centres along the coast of South India where the hosts were examined. The prevalence and abundance of B. vellavoli on P. chinensis taken at Madras were significantly different from the figures relating to hosts captured at and Pondicherry. The differences Mandapam observed in the prevalence and abundance of B. vellavok in different localities could have been due to chance because the sample sizes at most sites were so small or due to seasonal effects or to the fact that some samples had been obtained at a restricted time of the year. Therefore, additional studies on the seasonal occurrence of parasites on Pampus spp. at these localities may provide further insights regarding the seasonal dynamics and availability of fish host stocks. Juveniles and immature B. vellavoli were noticed to occur only on the smallest size class of both host species whereas on the larger hosts, only the adult parasites occurred. This suggests that the recruitment of new parasites may occur only in younger hosts and the parasite transmission thus appears to be geared to a time when young fish occur at high density in nursing grounds. Similarly, Arme & Halton (1972) recorded only adult ~i~~idophora ~erlang~ from Gadus merlangus over 200 mm in length.

Occurrence, site specificityand frequency distribution of B. vellavoli

165

0123456

NUMBER FIG. 2. Observed frequency distribution (histogram) (raw data were used) and expected distributions (0-O =

negative binomial, A-A

= Poisson) of E. vellavoli on (a)

7&160 mm size class (mean = 3.04; k = 0.7; N = 93); (b)

OF

PARASITES/HOST

FIG. 3. Observed frequency distribution (histogram) (raw data were used), and expected distributions (0-O = negative binomial, A-A = Poisson) of B. vellavoli on 7(r 260 mm P. argenteus (mean = 0.5; k = 0.28; N = 138).

170-260 mm size class (mean = 6.98; k = 0.432; N = 78); and(c) 270-350 mm size class of P. chinensis (mean = 2.69;k = 0.71; N = 42). k = Value of the negative binomial parameter. N = Number of hosts examined. B. vellavoli exhibited preference for attachment to gill I of Pampus spp. with decreasing preference towards gill IV. Regarding the site of attachment on each gill, there was a marked preference for the anteriormost region, with the posterior position as second choice. These differences in B. vellavoli numbers between gills and regions in an arch are not due to area differences. They may suggest that there is a particular pattern of water flow, a difference in the force and direction of ventilation water currents on the gills of Pampus spp. Preference of monogeneans for certain specific sites on the gills of fish is well known (Rohde, 1977b, 1979, 1980) although the reasons for such microhabitat restriction are obscure. Anne & Halton (1972) and Lebedev (1978) suggested that the force and direction of flow of ventilation currents may determine the microhabitat. On the other hand, Rohde (1977b, 1979, 1980) postulated that the reinforcement of reproductive barriers leads to segregation of related species, and that selection to

increase contact for mating leads to site specificity. Since most monogeneans are sessile (Llewellyn, 1956), active site selection probably occurs during the migratory larval phase. Such activity has been reported in trematode and cestode larvae (Ulmer, 1971) and also in Monogenea (Kearn, 1967, 1971; Tinsley & Earle, 1983). Cone & Burt (1981) have shown that the oncomiracidia of Urocleidus adspectus (Monopisthocotylea; Ancyrocephalinae) invade the full length of the host and the post-oncomiracidia attach at sites such as beneath the scales, at the base of fins, and in nooks in the body surface. Then the postoncomiracidia gradually migrate anteriorly and reach the gills by invading the opercular cavity and the buccal cavity. Similar experimental studies are required to confirm site selection by oncomiracidium of B. ve!lavoli and other gill parasitic polyopisthocotyleans. There are no other species of monogeneans other than B. vellavoli encountered on the gills of Pampus

766

P. RAMASAMYand K. RAMALINGAM

spp. which could have affected the site specificity. However such site segregation and morphoIogi~a1 adaptation to life on different regions of the gills and filaments have been reported in closely related and unrelated monogeneans occurring on the same host (see Rohde, 1977c, 1979; Ramasamy, Ramalingam, Hanna & Halton, 1985). The copepod Culigus sp. occurred only on a few hosts and most of them preferred the mouth cavity. It is, therefore, unlikely that it affected site specificity of the monogenean. Moreover the site specificity of B. velluvoli did not change in the presence of the copepod. The frequency distribution of B. vellavoli showed overdispersion (variance > mean) in all size classes of P. chinensis. The observed frequency distribution correlated with the values predicted by a negative binomial in the 70-160 and 27&350 mm size classes. B. veliavoli was also overdispersed on P. argenteus but the degree of overdispersion was low. The overdispersion of helminth parasites is a common phenomenon (Kennedy, 1975; Anderson, 1978). Crofton (197 1) suggested that overdispersion can minimize the possible deleterious effects of heavy infection by confining the parasites to a few host individuals and therefore the overall effect is low in the population. Anderson (1978) has shown that parasite species with an overdispersed distribution are capable of regulating population growth in a stable manner. The regulation of parasite population growth may be brought about by the following density-dependent mechanisms. (i) The rate of parasite induced host mortality is proportional to the worm burden. The hosts infected with the maximum number of flukes may be dying more rapidly than those with a few flukes. In such a situation, host death also results in the death of parasites representing a major proportion of the population. (ii) Density-dependent egg production (i.e. egg oroduction oer * fluke decreases as the fluke burden increases due to the intraspecific competition prevailing in the heavily infected hosts) and densitydependent death rate of adult or larval flukes as a result of immunological response to the helminth invasion (death rate of parasites increases with the increase in the recruitment of parasites) may determine the growth rate and abundance of the flukes. (iii) In hosts with a few parasites, the densitydependent effects will be less severe and the rate of egg production, recruitment of infective stages and survival of parasites may be greater than in hosts with a large number of parasites. In the latter, the impact of density-dependent mechanisms would be more pronounced. Each of the density-dependent factors acting alone or in combination with other densityindependent environmental factors bring stability to the host-parasite populations. Anderson (1978) suggested that those parasite species which cause little harm or stress to their hosts

are considered to be the successful parasites and the most effective regulators of host population growth. On the other hand, those parasite species which are extremely harmful to their hosts fail to act in a regulatory manner since they cause the death of too many infrapopulations of parasites within individual hosts. Since B. vellavoli is overdispersed, it may be considered to cause little harm or stress to its host Pumpus spp. and probably regulates the host population growth. The differences in host behaviour, variability in the immune responses within the host population, and spatial heterogeneity in the distribution of infective larval stages are some of the causes considered to generate the overdispersed distribution of parasites (Anderson, 1982). The reasons for aggregated distribution of monogeneans is not known. Anderson (1974) reported underdispersed distribution (variance < mean) of a monogenean Diplozoon paradoxurn on the bream Abramis bruma. He is of the opinion that the pre-existing parasite population in the host somehow prevented the recruitment of new infective stages of the parasite and as a result the parasite exhibited an underdispersed distribution. Acknowledgements-The authors are very grateful to Dr R. E. B. Hanna for reviewing the manuscript and Dr W. I. Montgomery for his constructive comments and help in statistical analysis. This work was supported by grants (Indian Council of Aericultural Research Scheme awarded to KR) and a Junior Risearch Fellowship (UGC, New Delhi) for PR. REFERENCES ANDERSON R. M. 1974. An analysis of the influence of host morphometric features on the population dynamics of Diplozoon paradoxum (Nordmann, 1832). Journal of Animal Ecology 43: 873-88 1. ANDERSON R. M. 1978. The regulation of host population growth by parasitic species. Parasitology 76: 119-157. ANDERSON R. M. 1982. Epidemiology. In: Modern Parasitology (Edited by Cox F. E. G.), pp. 204-251. Blackwell Scientific Pubhcations, Oxford. ARME C. & HALTON D. W. 1972. Observations on the occurrence of ~i~~idaphora merlangi (Trematoda: Monogenea) on the gills of whiting, Gadus rner~a~g~~. Journal ofFish Biology 4: 27-32. CONED. K. & BURTM. D. B. 198 I. The invasion route of the gill parasite Urocleides adspectus, Mueller, 1936 (Monogenea: Ancyrocephalinae). Canadian Journal of Zoology 59: 2 166-2 I7 I. CROFTON H. D. 1971. A quantitative approach to parasitism. Parasitology 62: 179-193. ELLIOTJ. M. 1977. Some Methodsfor the Statistical Analysis of Samples of Benthic Invertebrates, No. 25, Freshwater Biological Association, U.K. Titus Wilson & Son Ltd, Kendal. GOTO S. 1894. Studies on the ectoparasitic trematodes of Japan. Journal of College Science (Tokyo) 8: l-273. HUGHESG. M. 1984. Measurement of gill area in fishes: practices and problems. Journal qf the-marine 3~o~ogi~ai Association of the United Kingdom 64: 637655.

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