The amphipod Gammarus fossarum Koch (Crustacea)

as intermediatehostfor some helminth parasites,

with notes on their occurrence in the final host

by

Marion J. van Maren

Institute of Taxonomic Zoology, University of Amsterdam, The Netherlands

&

Dep. de Biologie animale et Zoologie, Universite Claude Bernard - Lyon I, France

Contents Abstract

Abstract 97 Monthly samples of Gammarus fossarum have been taken in

97 the Rhône river determine size Resume system near Lyon, to the

Introduction 98 composition and reproductive activity throughout the year. 98 The Material and methods acanthocephalan parasites of this gammarid species were

Results 100 also regularly collected. Furthermore, the intestinal tracts of

. . . 100 number of I. Intermediate host: Gammarus fossarum a fishes (amongst others Thymallus thymallus),

100 on been for a. Reproductive cycle feeding mainly , have investigated

b. Infestation 100 the of helminth by .... presence parasites.

1. Larval 100 G. the in the stages fossarum reproduces throughout year area

2. laevis 100 near but fluctuations in the rate of females Pomphorhynchus .... Lyon, ovigerous

lOO A infestation 3. Polymorphus minutus appear. peak in the of the gammarids by larvae

4. Metechinorhynchus truttae . . . . 101 of Pomphorhynchus laevis (Acanthocephala) occurred in

5. Infested females 101 ovigerous .... autumn and a second peak, but a lower one, during spring.

membrane, numbers and co- The fish showed infestations 6. Parasite hosts maximal during the same

invasion 101 periods, while during summer the incidence of Pom. laevis

102 both c. Other helminth parasites was low, in the intermediate and in the final host.

II. Final host (see appendix I) 102 From the stomach contents of the fishes it seems that

a. Pomphorhynchus laevis 102 gammarids harbouring the invasive acanthocephalan larva

1. Occurrence in fish 102 are species .... (cystacanth) selectively ingested.

of 2. Stomach contents 102 Reproduction G. fossarum seems not always to be in-

3. Sites occupied by adult worms . . 102 hibited at the presence of acanthocephalan larvae, since several

4. 102 infested female Cysts gammarids were found carrying eggs or

5. Number of parasites 102 juveniles in their brood pouch.

6. mature worms 102 The occurrence of some other helminth is recorded Sexually . . . . parasites

7. Infestation experiment 102 for the region near Lyon.

b. Polymorphus minutus lO2 Résumé 103 c. Other acanthocephalan parasites . . .

d. Other helminth parasites 103 Pendant une année, chaque mois, des prélèvements de Gam-

effectués Discussion 104 marus fossarum ont été dans le bassin du Rhône aux

Life of . . . 104 environs de Lyon, afin de déterminer de la a. cycle Gammarus fossarum la composition

b. Infestation by Acanthocephala 104 et les de de cet .... population cycles reproduction Amphipode.

1. Larval 104 Des spécimens de Gammares infestés des larves d’Acan- stages par 2. Pomphorhynchus laevis 104 thocéphales ont été récoltés également régulièrement. De

tube de diverses 3. Polymorphus minutus 106 plus, le digestif espèces de poissons, qui se

4. Other acanthocephalan parasites . . . 106 nourrissent principalement de Gammares (notamment Thy-

Parasitical castration mallus été examiné déceler la 5. 106 thymallus), a pour présence

6. Parasite membrane, numbers and co- éventuelle de vers parasites.

invasion 107 G. fossarum se reproduit pendant toute l’année dans la

mais des 7. Other helminth parasites .... 107 région lyonnaise, fluctuations dans le pourcentage

Acknowledgements 107 de femelles ovigères apparaissent. L’infestation avec Pompho-

laevis References 107 rhynchus (Acanthocephala) montrait un pic maximum

Appendix I. The occurrence of Acanthocephala in dif- en automne, tandis qu’au printemps un pic, de plus faible

ferent fish species 109 amplitude, était également constaté. Les poissons montraient

Appendix II. Position of the sampling stations . . 110 une infestation maximum pendant ces mêmes saisons; pendant

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de Pom. laevis furent aussi l’été par contre, peu rencontrés, presence of the acanthocephalan Polymorphus

bien dans l’hôte intermédiaire que dans l’hôte définitif. minutus (Goeze, 1782). In agreement with this D’après l’analyse des contenus stomacaux des poissons, the data of who il les Gammares la larve infestante are & Harrison (1965), semble que hébergeant Crompton Pol. minutus in in d’Acanthocephales (cystacanthe) soient sélectivement ingérés. studied a wildfowl reserve

Comme l’infestation de femelles ovigères de G. fossarum Kent. Stark (1965) established sterilization of fut constatée plusieurs fois, la présence de larves d’Acantho- female Gammarus zaddachi Di- semble la du Sexton, 1912, by céphales ne pas toujours empêcher reproduction

Gammare. plocotyle (Cestoda) larvae.

sont Quelques autres espèces de vers parasites signalées Holmes & Bethel (1972) observed changes in la pour région lyonnaise. the behaviour of G. O. Sars, INTRODUCTION 1895, infested by the acanthocephalan Polymor-

Ginetsinskaya (1961) states that freshwater am- phus paradoxus Connell & Corner, 1957. The

phipods (Gammaridae) act as intermediate hosts amphipods harbouring cystacanths are strongly dif- for at least 14 helminth parasite species of 4 positive phototactic and their evasive behaviour is

Cesto- after skim ferent groups (Acanthocephala, Trematoda, markedly altered; disturbance, they

da and Nematoda). along the surface of the water and/or cling to

exists According to Croll (1975) a correlation floating material. Similar behaviour is reported by

in and Stark between the extent of development a host (1965) for Gammarus zaddachi infested

the degree of host specificity. Development of the with Diplocotyle larvae. parasite imposes certain metabolic demands that The influence of the acanthocephalan Pompho-

the host be able The metacercaria laevis must to supply: rhynchus (Miiller, 1776) upon the respira-

in tion of its intermediate Gammarus is stage of Trematoda, occurring e.g. amphipod host, pulex,

described Data Crustacea, undergoes no important development by Rumpus & Kennedy (1974).

in it and and of is characterized by a wide range of hosts; on growth pigmentation infested gam-

the of Acantho- marids Stark and on the other hand, development are provided by (1965) Hindsbo infective takes cephala, from egg to larva, place (1972).

these have Gammarus and in one host and consequently parasites Resistance of species haemocytic

strict for towards minutus studied a rather preference their intermediate reactions Polymorphus are

host. Since acanthocephalans show a relatively wide by Hynes & Nicholas (1958) and Crompton

of final the distribution of these range hosts, (1967).

Gauthier worms is usually determined by the distribution (1923) mentions as

of host. the intermediate intermediate host for Cyathocephalus truncatus,

number For a large of Acanthocephala, para- a cestode causing cyathocephalosis in trout. Baylis

describes larvae sitizing fish or waterfowl, benthic Crustacea like (1931) several of trout parasites

Gammaridae found in G. Bertocchi Francalanci serve as intermediate hosts. pulex. & (1963)

with larval in Most literature on parasites stages mention a serious infestation of trout a fish

in deals with their farm the occurring presence by acanthocephalan Echinorhynchus trut-

the final little attention has been while G. in host and paid tae, many pulex harbouring cystacanth

to the ecology and biology of the amphipod in larvae of this parasite were encountered in the same

host. fish relation to its role as intermediate parasite ponds.

Several of the The has been obtain data authors have given a description present study set up to

within the and the development of acanthocephalan species on occurrence infestation rate of

in Gammaridae or other Amphipoda (Awachie, parasites relation to the life cycle of their gam-

1966b; Nicholas, 1967; Butterworth, 1969; Po- marid host, Gammarus fossarum Koch, in Panzer,

desta & Holmes, 1970; Crompton, 1970). 1836.

LeRoux (1933) referred for the first time to the MATERIAL AND METHODS effect of parasite larvae on the reproduction of

their amphipod host, mentioning sterilization of The present investigations were effectuated during

female Gammarus pulex (Linnaeus, 1758) at the a stay at the Zoological Department of the Univer-

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sity of Lyon. In the Rhone river system, near Lyon, compound microscope with the aid of an eyepiece

Gammarus fossarum is the most common amphi- micrometer (for details on these measurements,

pod species. To establish its size composition and see Dennert et al., 1969).

the intestinal tract of number reproductive cycle during a year, monthly samples Furthermore, a

from G. have been taken of a population of fossarum fishes, feeding mainly on gammarids, were

in the river the river determine the number and of a tributary of Rhone, Ain, studied to species

Dr. H. his work at Gevrieux. Rates of gammarids infested by acan- helminth parasites. Persat, during

laevis thocephalan larvae, mainly Pomphorhynchus on the biology of the grayling Thymallus thymallus

(Miiller, 1776), were also determined from these Linnaeus, 1758 (1976), was so kind as to put a

infestation of G. series of fish for samples. Moreover, rates fos- guts at my disposal analysis on

all sarum harbouring larvae of the acanthocephalan intestinal parasites. Nearly fishes were caught been Polymorphus minutus (Goeze, 1782) have by electric fishing. In most cases, the intestines

in established from samples collected monthly the were opened immediately after killing the fish,

of the river Ain. could be river Albarine, a tributary so that the worms obtained alive.

Part of the sampling of the Amphipoda was The Acanthocephala were left overnight in tap

carried with net. This no water at a of them to out a dip way, though, temperature 5°C, allowing gammarids could be collected in the river Rhone stretch before fixation. The parasites were fixed

the itself, because of depth of this stream. Thanks in 4% formaldehyde or A.F.A. (commercial for- to the kindness of Mr. J.-F. Perrin and of the malin, 10 parts; 95% ethyl alcohol, 70 parts;

in "equipe Rhone" of the Zoological Department glacial acetic acid, 5 parts; distilled water, 15

infested could be taken from the For the of Lyon, gammarids parts). purpose making microscopical

slides the so-called "paniers" (see Perrin, 1976, for a de- (total mountings), worms were, after tailed description of this method, consisting of fixation, clarified in lactic acid and mounted in depositing and lifting limestone-filled waste Euparal.

In data and baskets at regular time intervals in the river). order to get some on the growth

Preferably, the infested amphipods were selected development of the acanthocephalan Pompho- alive, since colour and shape of the parasites are rhynchus laevis in grayling, gammarids harbouring much less visible after fixation. The larvae of that fed gammarids cystacanth parasite were to young

in from fish farm. were preserved 4% formaldehyde. Thymallus (15-20 cm) obtained a

free intestinal After establishing for G. fossarum a linear cor- These fishes were supposed to be of relation between body length and cephalic length parasites, since they had been supplied exclusively

latter has been used in (fig. 1), the determining with fish pellets. The graylings were kept in basins the composition of the population in the river Ain, outside the laboratory, supplied with running water where monthly quantitative samples have been of subterranean origin. During the experiment,

made collected. The measurements were under a that lasted from April till June 1976, temperatures

of the water varied from 14 to 15.5°C. After

feeding the fishes with infested G. fossarum, week-

killed ly some graylings were to establish the

presence and development of the acanthocephalans.

During the experiment the fishes were fed with "SARB" fish pellets, containing neither antibiotics

nor antihelminths.

As far as temperature readings have been made

during the present study, a mercury thermometer

in was used (scale 0.1°C).

Fig. 1. The relation between cephalic length (X-axis) and The position of the sampling stations where body length (Y-axis) in Gammarus fossarum ( N = 139; gammarids and/or fishes have been collected, is correlation = = 0.957; standard error Y 0.025; standard recorded in II, error X = 0.021). appendix

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RESULTS

I. INTERMEDIATE HOST: GAMMARUS FOSSARUM

a. Reproductive cycle

All monthly samples of Gammarus fossarum from

the river Ain contained ovigerous females, al-

their fluctuates though rate throughout the year

(fig. 2). In November no samples could be col-

lected, because of the extreme high level of the

river.

During the months of January and April mini-

in ma were found the mean cephalic length of the

G. fossarum population (fig. 3). The ovigerous

females were distinctly smaller during summer

the of the compared to rest year.

b. Infestation by Acanthocephala

1. Larval stages

first larval The stage of Acanthocephala, the acan-

from the after swallowed thor, emerging egg being

the observed by arthropod host, was never during

small the present study. This is probably due to its

size and the fact that this larva is located in the

The intestine or on the outer surface of the gut.

next larval stages, the acanthella and the infective

larva, the cystacanth, are lying free in the haemo- Fig. 2. Percentage of ovigerous ￿ ￿ (dashed line) in the coel of the host and are much more conspicuous monthly samples of Gammarus fossarum from the river Ain, in size and colour. During the present study both during the period Dec. 1975 - Dec. 1976. Temperatures of the

are also indicated encountered the in water (in °C) (solid line). stages were throughout year

but with Gammarus fossarum, cystacanths a some-

what higher frequency than acanthellae.

The great majority of G. fossarum harbouring

acanthocephalan larvae belonged to the larger size

classes of the population.

2. Pomphorhynchus laevis

Fig. 4 shows the rates of Gammarus fossarum in-

fested by the acanthocephalan Pomphorhynchus

laevis (parasitizing fish) in the monthly samples

from the river Ain. From April till August infesta-

A in tion was low. distinct peak the infestation rate

in and another can be seen September peak, but

much lower, occurs in March. In the river Rhone,

at Pont de Jons (sta. F), the infestation rate of

G. fossarum by Pom. laevis was maximal 2%,

values in never attaining as high as the river Ain. Fig. 3. Mean cephalic length of the specimens of Gammarus

fossarum in the monthly from the river samples Ain, during 3. Polymorphus minutus the Dec. 1975 1976 period - Oct. (bars represent standard Although the sampling station in the river Alba- deviation). The number of specimens examined is indicated rine is situated small as well. (sta. G) on a relatively

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Fig. 4. Percentage of Gammarus fossarum infested by the Fig. 5. Percentage of Gammarus fossarum infested by the acanthocephalan Pomphorhynchus laevis (dashed line) in the acanthocephalan Polymorphus minutus (dashed line) in the monthly samples from the river Ain at Gévrieux, during the monthly samples from the river Albarine at Gévrieux, during period Jan.-Dec. 1976. Temperatures of the water (in °C) the period Dec. 1975 - Dec. 1976. Temperatures of the water

indicated are also indicated (solid line). (in °C) are also (solid line).

have been distance from that in the river Ain, their acantho- thocephalan parasitizing fish, encoun- cephalan faunas show a totally different picture. tered.

Most of the the from the river year gammarids 5. Infested ovigerous females Albarine larvae are infested exclusively by of Not infrequently ovigerous females of Gammarus Polymorphus minutus, a parasite of waterfowl. fossarum were observed harbouring acanthoceph- During January and March peaks in the infestation alan larvae. Cystacanth larvae of Polymorphus rate have been established, while infestation was minutus laevis in or Pomphorhynchus occurred low from till very May September (fig. 5). these females. Precopulae have been collected of An extremely high infestation of Gammarus which both contained acantho- one or partners fossarum by Pol. minutus (48% of the total cephalan larvae. sample!) was observed near the sources of the river

Merloux (sta. H). The population of G. fossarum 6. Parasite membrane, numbers and co-invasion is dense this situated in meadow very at locality, a minutus al- The cystacanths of Polymorphus were with ducks and chickens. The stream is at the found to be surrounded ways by a membrane, sources not more than 0.3 m wide and attains a transparent and brownish in colour. Around the depth of maximal 0.1 m. Not even at 100 m infective larva of Pomphorhynchus laevis, how- downstream from the sources, only 2% of the occurred. ever, no envelope gammarids was found to be infested and somewhat 14 Although gammarids harbouring up to acan- the did contain more downstream sample not any thocephalan larvae have been found during the infested gammarids. present investigations, most commonly 1 to 3

4. larvae encountered Metechinorhynchus truttae were in the amphipods. Besides Pomphorhynchus laevis and Polymorphic Gammarus fossarum harboured normally-devel- minutus, the prevailing parasite species occurring oped larvae of different acanthocephalan species in river and Pom. gammarids from the Rhone system, some (combinations of Pol. minutus laevis, of

larvae Met- Pom. and Gammarus fossarum harbouring of laevis Metechinorhynchus truttae or of echinorhynchus truttae (Schrank, 1788), an acan- Pol. minutus and M. truttae).

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Sites adult c. Other helminth parasites 3. occupied by worms

Never adult Acanthocephala were observed in the At several localities in the Rhone river system stomachs of the fishes that have been investigated. gammarids infested by larval cestodes were col- in and They occurred always the intestine proper, lected. In those cases in which identification was in a few graylings, heavily infested by Pompho- possible Cyathocephalus truncatus (Pallas, 1781) rhynchus laevis, several worms were found attached was found. to the liver, gonads or swim bladder.

4. II. FINAL HOST (SEE APPENDIX I) Cysts

Often the outer surface of the intestinal wall of the laevis a. Pomphorhynchus fishes studied showed cyst-like formations. Upon Occurrence in fish 1. species the closer examination these cysts proved to contain Pomphorhynchus laevis is the most commonly met proboscis and part of the neck of Pomphorhynchus helminth in species grayling, Thymallus thymallus laevis. (Linnaeus, 1758), from the river Ain (sta. A, B

and C) and in barbel, Barbus barbus (Linnaeus, 5. Number of parasites

1758), from the river Albarine (sta. G) (appendix No correlation could be established between the

that in latter fish la & b). It has to be noted the number of Pomphorhynchus laevis occurring in a

Pom. fish species laevis attains a size much larger than particular and the fish's length (age). It must

in and that its colour is than Thymallus deep-orange be noted, though, that only grayling of more

instead smaller of the pink-orange of the worms. 12 cm were available for examination. The number

found in Furthermore, Pom. laevis was trout, of Pom. laevis in the final host is minimal during

Salmo in Noema- than trutta Linnaeus, 1758, loach, summer, but in spring and autumn more 250

in been in cheilus barbatulus (Linnaeus, 1758), roach, Ru- specimens have counted some fishes (ap-

tilus rutilus (Linnaeus, 1758), and in minnow, pendix la).

Phoxinus phoxinus (Linnaeus, 1758), from the 6. river Ain. In burbot, Lota lota (Linnaeus, 1758), Sexually mature worms

mature laevis (gravid from the river Loue in the Jura (sta. E) and in Sexually Pomphorhynchus in females) were in Barbus barbus, but, bullhead, Cottus gobio Linnaeus, 1758, from the present spite of the heavy infestations of Thymallus thy- river Rhone (sta. F) this parasite occurred as well mallus by this parasite, hardly ovigerous worms (appendix Ic). any have been observed in this fish species.

2. Stomach contents 7. Infestation experiment

in 6 shows ob- The presence of Pomporhynchus laevis larvae Fig. adult Pomphorhynchus laevis,

and the stomach contents of their final hosts indicates tained from 2, 4, 5, 7, 10 11 grayling, y 2,

The weeks after had been with recent feeding on gammaridean Amphipoda. they supplied gam-

stomachs of marids larvae of this After 4 grayling, caught during summer, con- harbouring parasite.

tained it weeks all fixed to the intestinal none or hardly any acanthocephalans; worms were wall,

in might be significant that this season the food while after 7 weeks the formation of a capsule

of the fish consisted mainly of insect larvae. around the proboscis and neck of the parasite was

the During the months of October and November observed. The worms found after 10 weeks were

in stomach attached the number of cystacanth larvae the con- solidly to gut wall, forming a cyst-like

of the varied the the the tents fishes from 17 to 48, while structure around upper part of acantho-

food was composed chiefly of Gammarus. cephalan.

Although mainly the cystacanth stage was found, b. Polymorphus minutus also some acanthellae (the earlier, non-infective

Pom. in the larval stage) of laevis were observed Since no birds from the Rhone river system have

of for examination stomachs grayling. been at our disposal on the pres-

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Fig. 6. Adult Pomphorhynchus laevis obtained from grayling, ½ (A), 2 (B), 4 (C), 5 (D), 7 (E), 10 (F) and 11 (G)

weeks after the fishes had been fed with gammarids harbouring larvae of this parasite (19 X).

in the river Loue ence of the parasite Polymorphus minutus, only Burbot (Lota lota), captured

its occurrence in the gammarid host could be (sta. E), was heavily infested by Pseudoechino-

studied. rhynchus clavula (Dujardin, 1845) (appendix Ic).

c. Other acanthocephalan parasites d. Other helminth parasites Many Metechinorhynchus truttae have been col-

lected from in river Furans grayling captured the Cyathocephalus truncatus Pallas, 1781, a cestode,

few laevis in river Furans (sta. D), while only a Pomphorhynchus was collected grayling from the occurred in these fishes. (sta. D) and from the river Ain (sta. B). Both

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larvae and occurred in the laevis adult worms pars pylo- 2. Pomphorhynchus

rica of the intestine, while the former were en- Hine & Kennedy (1974b) established a general

and countered in the stomach as well. absence of a cycle in the incidence intensity

of infestation in gammarids and fishes by Pom-

DISCUSSION phorbynchus laevis in the river Avon (Great

Britain). Infestation of gammarids seems to take a. Life cycle of Gammarus fossarum all in the place year round, only summer parasite The results obtained during the present study con- was slightly less common. Although acanthellae firm the observations of Roux (1970), according in (young larvae of Acanthocephala) are found to which Gammarus fossarum reproduces through- Gammarus fossarum from the river Ain through- out the in the waters near Lyon. He year supposes the distinct minimum in the infestation out year, a that temperature influences the rate of increase or rate of the gammarids can be seen during late decrease in The rate of reproductive activity. ovig- and spring summer (fig. 4). Ginetsinskaya (1961)

females was low in erous very April compared that is assumes the water temperature a major to the rest of the year (fig. 2). Water temperatures determining factor in the life cycle of the parasite, in March in rose from 6.5°C to 14.5°C April. regulating both the period of peak reproduction Although the annual temperature fluctuations seem of the intermediate host and the development of to influence the rate of females, the ovigerous the within it. It concluded in the worm might be

in the Rhone river near temperature range system the present case, that temperature affects mainly Lyon is such that reproduction is possible the whole development of the parasite, as breeding of G. round (5°-17.4°C). year does not to be limited the fossarum appear by Lehman (1967) established that in January the temperatures recorded for the Rhone river system. larger, overwintering females of G. fossarum, In Thymallus thymallus from the river Ain which are already mature, start to breed and that large numbers of Pom. laevis were counted during the first of in February breeding females the new early spring and autumn, while in July and August In with these generation agreement obser- appear. the fish contained relatively few worms (appendix the females from the river Ain vations, ovigerous month la). Moreover, in summer, contrary to the are smaller in and March February compared to larvae of October, only few acanthocephalan were those collected in December and January (fig. 3). in stomachs found the of grayling (the presence of small During summer only females of size were Acanthocephala in the stomach of the fish indicates found to breed. Consequently, the larger ovigerous recent feeding on infested gammarids!). females in April still belong to the old, over- Since the acanthella stage (not yet infective that dies off in late wintering generation, spring. in larva) was rarely found the stomach contents

of the fish, it might be concluded that mainly b. Infestation by Acanthocephala gammarids harbouring the infective larva (cysta-

1. Larval stages canth) are eaten by the final hosts. Bethel &

The larval stages encountered during the present Holmes (1973, 1974), studying Gammarus lacus-

study in Gammarus fossarum were all acanthellae tris infested by the acanthocephalan Polymorphic

discovered that or cystacanths, but never the earliest acanthor larva. paradoxus, a disproportionally large

in number Moreover, agreement with the observations of of infested gammarids, compared to non-

the final host. Hine & Kennedy (1974b), small amphipods were infested specimens, was eaten by

the rarely found to be infested. Spencer (1974), who Furthermore, they found a correlation between

studied the infestation of Gammarus lacustris by behaviour of the amphipods and the infectivity of

the acanthocephalan Polymorphus minutus, men- the parasite larvae. They assume that gammarids

tions that acanthors in the are undoubtedly present the harbouring invasive larva, move, as a result

smaller gammarids, but are not visible because of of their modified behaviour, into a zone of overlap

their small size and location deep in the body of with the feeding niche of the final host, thus in- the host. creasing the probability of parasite transmission.

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Pom. in the river Selective feeding by the fishes on infested Gam- Thymallus by laevis Avon, no

from modified behaviour of the females of this occurred in marus, resulting a gravid parasite gray-

and from the that the of this amphipods harbouring cystacanths ling. They suppose population

in the river is of conspicuousness of the parasite larva (orange worm Avon maintained by eggs

from coloured in the case of Pom. laevis), might be an Pom. laevis originating chub and barbel,

for be the final hosts. explanation the heavy infestations by Pom. which seem to preferred The laevis observed in the fishes from the waters near of Pom. laevis in bullhead Cottus presence ( gobio) Lyon. and loach (Noemacheilus barbatulus) from the

is in Grayling lacks pharyngeal teeth and does not Rhone river system (appendix Ic) agreement

who masticate its food, so that gammarids arrive still with the data presented by Rumpus (1975),

relatively intact in the stomach of the fish. Ac- observed that maturation of this acanthocephalan

cording to Kennedy et al. (1976), Pom. laevis is also possible in these fish species. Since matura-

survive in of the intestinal The tion of the to be in can all parts tract. present parasite seems possible

canal the fish well this fish sites it occupies in the alimentary of trout as (Hine & Kennedy, 1974a),

the of liberation the of Pom. are mainly determined by process species might maintain population

it and activation of the worms. Liberation and activa- laevis in the river Ain, where commonly occurs tion of the take in the cystacanths place pars pylo- next to grayling.

rica of the intestinal tract in grayling. During the

the of present investigations, fixed adult Pom. laevis were Concerning occurrence Pomphorhynchus

in in the laevis in its intermediate and final the fol- always found the intestine proper, never hosts,

fish. has been stomach or pyloric region of the It lowing assumptions are put forward:

— larva observed, though, that the present parasite some- Gammarids harbouring the infective times the often the fish. This penetrates so deep into intestinal wall, (cystacanth) are more eaten by that it and seldom it be result of the of the passes right through not was might a conspicuousness found be attached other in the ab- larva a altered behaviour of the to to organs and/or possible dominal cavity, such as liver, swim bladder or intermediate host.

— the intestinal wall the gonads. Similar observations are mentioned by Cysts on of fishes are

Dorier Petrochenko and Hine (1931), (1971) & provoked by worms having attained already a cer- Kennedy (1974a). tain size. Upon loss of the acanthocephalan from

the the From fig. 6 can be seen that some growth of gut, cyst, containing the neck and proboscis

Pom. laevis took in the of the remains. place grayling during 3 worm, months' period of the infestation experiment. —• Sexually mature worms probably die off after

According to Hine & Kennedy (1974a) the en- some time and are expelled from the intestine. capsulation reaction of the fish host towards Pom. Muzzall & Rabelais (1975) concluded from their laevis is accentuated when the proboscis bulb of observations concerning Acanthocephalus jacksoni the acanthocephalan is well developed. They state Bullock, 1962, that gravid female worms deterio-

in in that this parasite seldom develops a bulb Thy- rate the environment outside the host and that mallus. In studies Pom. laevis showed are released that moment. Nicholas our develop- eggs at &

4 since ment of a bulb already weeks after infestation, Hynes (1958) came to a similar assumption, while in the 11th week formation found of minutus in a cyst-like was they never eggs Polymorphus found the intestinal the the of infested ducks. on wall, containing pro- droppings boscis and neck with bulb of the acanthocephalan. — From the number of cystacanths contained in

Most barbels from the river Albarine, examined the stomach of the fishes examined, and from the during the present study, were infested by Pom. number of worms attached to the gut wall during

mature that maximal laevis (appendix lb). Sexually worms were different seasons, it can be concluded commonly met in this fish species, but in grayling infestation of the final host takes place during

and only on rare occasions. Hine & Kennedy (1974a) autumn spring. During these periods large

in numbers mention that, spite of the heavy infestations of of small Pom. laevis were found in the

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intestines of the from the river Albarine have been fish, indicating recent feeding on Since no birds

for the of infested gammarids. at our disposal examination on presence

its the — Maximum rates of gammarids harbouring acan- Pol. minutus, only occurrence in gammarid

larvae occurred in be studied. thella or cystacanth autumn and host could

spring. It must be assumed that part of the amphi- 4. Other acanthocephalan parasites pods occurring in spring became infested during The grayling from the river Furans (sta. D) har- since the the year before, development of acantho- boured large numbers of the acanthocephalan cephalans is considerably retarded by lower tem- Metechinorhynchus truttae and only a few Pom- peratures. have phorhynchus laevis. However, no gammarids

been examined from this river. Awachie (1966b) 3. Polymorphus minutus Gammarus for mentions pulex as intermediate host The highest infestation rates of Gammarus fos- M. truttae in Great Britain. During the present Albarine with larvae of sarum from the river Poly- investigations Gammarus fossarum from several of morphus minutus, a parasite waterfowl, occurred localities in the Rhone river system were found to while low found in spring, rates were during sum- contain larvae of this parasite. Pol. minutus mer (fig. 5). Hynes (1955) found A specimen of Lota lota (burbot) from the river to be abundant in samples of gammarids ( Gam- Loue indi- (sta. E) harboured over a hundred marus duebeni Liljeborg, 1852 and Gammarus viduals of Pseudoechinorhynchus clavula and only less lacustris)) from Great Britain taken in summer, one Pom. laevis (appendix Ic). Petrochenko common in autumn and rare or even absent during (1971) mentions the amphipods Gammarus pulex winter and spring. Spencer (1974), investigating and Pontoporeia affinis Lindstrom, 1855, as inter- the infestation of Gammarus lacustris with Pol. mediate host for Ps. clavula. Chubb (1967) found minutus in ponds that are ice-covered from No- this parasite in fishes from oligotrophic lakes in vember till April, established peaks in the infesta- the British Isles, where the isopod Asellus meri- tion percentages in April and August. According dianus Racovitza, 1919, seems to be its inter- to infestation rates Ginetsinskaya (1961), may mediate host. vary from one locality to another for the same

parasite species, since annual cycles of the parasites 5. Parasitical castration

related to the of the host's habitat. The effect of are hydrology acanthocephalan larvae on the repro-

In the river the in- duction of the Merloux, near sources, an intermediate host was first men-

festation rate as high as 48% was established for tioned by Leßoux (1933). She states that females

G. fossarum harbouring larvae of Pol. minutus, of Gammarus pulex infested by Polymorphus mi-

while somewhat more downstream no infested nutus do not reproduce. Especially the vitello-

found. These observations in be inhibited the gammarids were are genesis seems to by thepresence of

with who larva. agreement those of Noll (1950), found parasite According to Goodwin (I960) some

more than 60% of G. fossarum to be infested by Crustacea, such as Gammarus, accumulate large

the in small rivulet of carotenoid present worm a downstream quantities of the astaxanthin. At the

duck farm. he established that in- of a Furthermore, moment reproduction a mobilization of this

takes festation of the was localized. to the The gammarids very pigment place eggs. orange- of Pol. in the river The presence minutus Rhone coloured acanthocephalan larva, containing esteri-

system seems to be restricted to those parts of the fied astaxanthin, obtains its carotenoids from the

where of host river, more or less swampy biotopes are haemolymph the amphipod (Barrett & But- available the Vieux Rhone Al- (e.g. near Lyon). terworth, 1968). Hynes & Nicholas (1958) es-

though the river Albarine is a fast running stream tablished that females of Gammarus pulex, G.

in winter and in shows and G. autumn, spring, summer it lacustris duebeni, when infested by Pol.

a totally different picture: the river largely dries minutus, do not reproduce normally.

and consists almost the up exclusively of stagnant During present investigations, several female

little infested pools, very running water being left. gammarids by Acanthocephala have been

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collected carrying eggs or juveniles in their brood 7. Other helminth parasites

pouch. Very few of these females harboured larvae Vik (1958) has found the cestode Cyathocephalus

of Pol. minutus, but ovigerous females with Pom- truncatus in the haemocoel of Gammarus lacustris

phorhynchus laevis were rather commonly found. and G. pulex in Norway. During the present study,

of this According to Crompton (1970), not all developing larvae parasite were observed in G. fos-

their host. but its acanthocephalans castrate Moreover, sarum, occurrence was rare compared to that

who of larvae. Spencer (1974), found many ovigerous fe- the acanthocephalan Awachie (1966a)

males of G. lacustris harbouring Pol. minutus lar- often found adult C. truncatus in trout, but he

established infestation the larval vae, that by parasite, rarely came across stages in Gammarus from

the although decreasing the reproductive potential of same stream. The occurrence of this worm in the the amphipod, not always impaired breeding of the pyloric region of the fish intestine, as es-

females. He mentions two possible explanations: tablished during the present investigations, is in

infestation took place after the females formed agreement with the data by Gauthier (1923).

and host have their egg masses, or parasite come ACKNOWLEDGEMENTS into a state of balance.

I am greatly indebted to the French Government for providing 6. Parasite membrane, numbers and co-invasion me with a which has allowed to grant, me carry out the that I The present investigations show Polymorphus present study. want to express my gratitude also to Prof. A. L. Roux of the of for University Lyon the great hospitality minutus cystacanths are always surrounded by a I experienced during my stay in his laboratory. Furthermore while around the larva of membrane, invasive I owe thanks many to Mr. J.-F. Perrin and Dr. H. Persat for

putting amphipod and fish material Thanks Pomphorhynchus laevis never an envelope was at my disposal.

are also due to Mr. L. A. van der Laan for making the the photo- found. According to Crompton (1964) cap- graphs and to Mr. J. Zaagman for his assistance in preparing

the larva of Pol. con- In sule, surrounding minutus, the I am figures. addition, very grateful to Prof. J. H.

sists of connective tissue and originates from the Stock, to Prof. H. B. N. Hynes, to Drs. F. Pieters and Dr. S.

Pinkster for their constructive criticism the concerning prep- serosa of the host's wall. He assumes that gut aration of the present paper. acanthocephalans that stay associated with the in-

testinal wall of the amphipod host for a longer REFERENCES

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APPENDIX I

The of in different fish For the of occurrence Acanthocephala species. position the sampling stations, see appendix II,

C. = Cyathocephalus; M. = Metechinorhynchus; Pom. = Pomphorhynchus; Ps. = Pseudoechinorhynchus.

Station Date Length of Acanthocephala

fish (cm) (adults) Remarks

number & species

(a) In THYMALLUS THYMALLUS (grayling):

A 28-VII-'75 31 16 Pom. laevis in stomach: 1 cystacanth larva

A 2-VIII-'75 27 7 Pom. laevis stomach content: mainly insects

A 2-VIII-'75 32 — stomach content: mainly insects

A 10-VIII-'75 33 22 Pom. laevis in stomach: 5 cystacanth larvae

B 27-VIII-'75 22 Pom. laevis intestinal 23 cysts on wall

B 27-VIII-'75 24.5 3 Pom. laevis cysts on intestinal wall

B 27-VIII-'75 2 laevis 38 Pom. cysts on intestinal wall

B 27-VIII-'75 33 — cysts on intestinal wall

A 4-X-'75 33 219 Pom. laevis in stomach: 1 cystacanth larva; insects

C 12-X-'75 37.5 157 Pom. laevis

C 280 12-X-'75 43 Pom. laevis cysts on intestinal wall

C 12-X-'75 laevis 36 197 Pom. cysts on intestinal wall

C 12-X-'75 37 185 Pom. laevis cysts on intestinal wall

B 26-X-'75 15 1 Pom. laevis intestine removed

B 26-X-'75 14.3 30 Pom. laevis

B 26-X-'75 13.5 40 laevis Pom. even swim bladder affected

B 26-X-'75 14.5 60 Pom. laevis even liver affected

B 26-X-'75 13 40 Pom. laevis swim bladder also affected

A 26-X-'75 60 Pom. laevis in 2 15 stomach: 5 cystacanth larvae; in intestine: 30 worms/cm !

A 26-X-'75 26.3 46 Pom. laevis in stomach: 21 cystacanth larvae; 2 acanthella larvae

A 26-X-'75 — 28 intestine removed; in stomach: 5 cystacanth larvae; insects

A 26-X-'75 27.8 120 Pom. laevis

A l-XI-'75 27 128 Pom. laevis in stomach: 6 cystacanth larvae

A l-XI-'75 28 55 Pom. laevis in stomach: 32 cystacanth larvae; 2 acanthella larvae; gammarids A l-XI-'75 145 laevis 29 Pom. in stomach: 3 cystacanth larvae; insects

A 8-XI-'75 29 177 Pom. laevis in stomach: 48 cystacanth larvae; 2 acanthella larvae; gammarids A 8-XI-'75 28 74 Pom. laevis in stomach: 30 cystacanth larvae

A 8-XI-'75 27 172 Pom. laevis in stomach: 23 cystacanth larvae

A 8-XI-'75 18.5 11 Pom. laevis

A 8-XI-'75 16.5 20 Pom. laevis in stomach: 1 acanthella larva; insects

A 8-XI-'75 14 34 Pom. laevis in stomach: 2 cystacanth larvae

B l4-III-'76 29.3 160 Pom. laevis

B l4-III-'76 32.2 206 Pom. laevis

B 14-III-'76 30.7 220 Pom. laevis

B 14-III-'76 28 210 Pom. laevis

B l4-III-'76 32 150 Pom. laevis

B 14-III-'76 laevis 33.5 305 Pom. cysts on intestinal wall

B l4-III-'76 27 228 Pom. laevis cysts on intestinal wall

B l4-III-'76 28.7 112 Pom. laevis

B 3-IV- 76 32 190 Pom. laevis

B 3-IV-'76 36 260 Pom. laevis, in stomach: insects

4 M. truttae

B 8-IV-'76 33.5 259 Pom. laevis gonads affected in C. as well; pars pylorica: truncatus (Cestoda) B 8-IV-'76 laevis 31 190 Pom. cysts on intestinal wall

B 8-IV-'76 38 Pom. laevis 29.5 cysts on intestinal wall

B 8-IV-'76 28.7 6 Pom. laevis mature worms (gravid 9 9)

B 8-IV-'76 34 97 Pom. laevis

B 8-IV-'76 27.8 43 Pom. laevis small worms; many cysts on intestinal wall

B 8-IV-'76 laevis 31.5 31 Pom. small worms; many cysts on intestinal wall

B 8-IV-'76 26.8 4 Pom. laevis mature worms

D l4-IV-'76 30 64 M. truttae

D 14-IV-'76 34 3 Pom. laevis, in stomach and pars pylorica: C. truncatus (Cestoda)

121 M. truttae

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Station Date Length of Acanthocephala fish (cm) (adults) Remarks

number & species

D 14-IV- 76 27.5 1 Pom. laeris,, in stomach: C. truncatus (Cestoda)

29 M. truttae

E 27-IV-'76 29.5 —in stomach: mainly insects

E 27-IV-'76 32 1 Pom. laevis

E 27-IV-'76 31 2 Pom. laevis

E 27-IV-'76 31 —in stomach: mainly insects

E 27-IV-'76 31 2 Pom. laevis in stomach: insects

E 27-IV-'76 30.5 1 Pom. laevis in stomach: insects

(b) In BARBUS BARBUS (barbel):

G 14-XII-'75 42.5 Pom. laevis mature worms (gravid 2s) 14-XII-'75 48.5 laevis G Pom. mature worms (gravid 29)

G 14-XII-'75 40.5 laevis intestinal wall Pom. many cysts on

G 14-XII-'75 37 23 Pom. laevis

G 14-XII-'75 35 23 Pom laevis

G 14-XII-'75 42.5 150 Pom. laevis

G 14-111-76 33 8 Pom. laevis 2 intestinal wall mature worms (gravid 2); many cysts on

G 14-111-'76 laevis wall 31 19 Pom. cysts on intestinal

(c) In other fish species (as specified):

Species of fish

B 27-Vlll-'75 Salmo trutta 22 Pom. laevis, cysts of Pom. laevis on intestinal wall

1 M. truttae

B 27-VIII-'75 Salmo trutta 28 Pom. laevis

B 14-XII-'75 Rutilus rutilus Pom. laevis intestinal wall (20 cm) 1 many cysts on

B 8-IV-'76 Phoxinus phoxinus (6 cm) 3 Pom. laevis

B 8-IV-'76 Phoxinus phoxinus (5 cm) 1 Pom. laevis

F 14-IV-'76 Cottus gobio 13 Pom. laevis in stomach: 6 cystacanth larvae

E 27-IV-'76 lota clavula Lota 136 Ps. clavula, also in pars pylorica many Ps.

1 Pom. laevis

B 25-V-'76 Noemacheilus barbatulus 1 Pom. laevis

APPENDIX II

Position of the sampling stations

Station Position Department

A River Ain, E. of Villieu Ain

B River Ain, near Gevrieux, downstream

of the bridge on R.N. 504 Ain

C River Ain, near Chazey-sur-Ain Ain

D River Furans, near Chazey-Bons, N. of

Belley Ain

E River Loue, near Parcey, S. of Dole, E.

of Beaune Jura

F River Rhone, near Pont de Jons, N.E.

of Lyon Ain/Rh6ne

G River Albarine, near Gevrieux, not far

from its confluence with the river Ain Ain

small S.W. of H River Merloux, a stream

Villefranche-sur-Saone Rh6ne

Received: 30 March 1978

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