HELGOLKNDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 37, 5-33 (1984)

Ecology of marine parasites

K. Rohde

Department of Zoology, University of N e w England; Armidale, N.S. IV., Australia

ABSTRACT: Important ecological aspects of marine parasites are discussed. Whereas effects of parasites on host individuals sometimes leading to death are known from many groups of parasites, effects on host populations have been studied much less. Mass mortalities have been observed mainly among hosts occurring in abnormally dense populations or after introduction of parasites by man. As a result of large-scale human activities, it becomes more and more difficult to observe effects of parasites on host populations under "natural" conditions. Particular emphasis is laid on ecological characteristics of parasites, such as host range and specificity, microhabitats, mac- rohabitats, food, life span, aggregated distribution, numbers and kinds of parasites, pathogenicity and mechanisms of reproduction and infection and on how such characteristics are affected by environment and hosts. It is stressed that host specificity indices which take frequency and/or intensity of infection into account, are a better measure of restriction of parasites to certain hosts than "host range" which simply is the number of host species found to be infected.

I N T R O D U C T I O N

T h e s c i e n c e of e c o l o g y is c o n c e r n e d w i t h i n t e r a c t i o n s of o r g a n i s m s a n d t h e i r b io t i c and ab io t i c e n v i r o n m e n t . T h e e n v i r o n m e n t of p a r a s i t e s d i f fers f rom tha t of f r e e - l i v i n g

o r g a n i s m s in h a v i n g two c o m p o n e n t s . O n e , t he m i c r o e n v i r o n m e n t , is t he hos t i tself ; t h e other, the m a c r o e n v i r o n m e n t , is t he e n v i r o n m e n t of t h e hos t (Fig. 1). T h e m a c r o e n v i r o n -

m e n t affects p a r a s i t e s e i t h e r i n d i r e c t l y t h r o u g h the host , or it a f fects t h e m di rec t ly , for

i n s t ance by p r o v i d i n g a su i t ab l e s a l in i ty to ec topa ra s i t e s . D i r e c t e f fec t s of p a r a s i t e s on

the m a c r o e n v i r o n m e n t a r e n e g l i g i b l e , a c o n s e q u e n c e of t h e s m a l l s i ze of p a r a s i t e s a n d the ba r r i e r b e t w e e n e n d o p a r a s i t e s a n d m a c r o e n v i r o n m e n t r e p r e s e n t e d by t h e host . O n

the o the r hand , p a r a s i t e s a n d hos t s a f fec t e a c h o t h e r in m a n y ways . S u c h in t e rac t ions , as

w e l l as t h e ef fec ts of t h e m a c r o e n v i r o n m e n t on pa ras i t e s , w i l l b e d i s c u s s e d in t h e

fo l lowing , w i t h s p e c i a l e m p h a s i s on cha rac t e r i s t i c s of p a r a s i t e s a n d h o w t h e y a re affected.

E F F E C T S O F P A R A S I T E S O N H O S T S

Paras i tes m a y af fec t i n d i v i d u a l hos ts in a n u m b e r of ways , b y m e c h a n i c a l ac t ion , w i t h d r a w a l or s u p p l y of subs tances , t r ans fe r of m i c r o - o r g a n i s m s , p o s s i b l y tox ic effects ,

and effects on the hos t ' s i m m u n e r e s p o n s e s (Fig. 1). T h e s tudy of s u c h e f fec t s is t he t a sk

of p a t h o l o g y a n d no t of e c o l o g y s e n s u str icto. H e n c e , o n l y a f e w e x a m p l e s wi l l be b r i e f ly m e n t i o n e d . A c a n t h o c e p h a l a m a y p e r f o r a t e t h e i n t e s t i n e of f ish ( m e c h a n i c a l ac t ion) ,

ce s todes m a y use u p nu t r i en t s in t h e i n t e s t i n e of f ish ( w i t h d r a w a l of subs tances ) , l e e c h e s m a y t r ansmi t p r o t o z o a n b l o o d p a r a s i t e s to f ishes , a n d v a r i o u s h e l m i n t h s a f fec t t h e i r hos t s

poss ib ly by tox ic e x c r e t i o n s or sec re t ions , a l t h o u g h e v i d e n c e is a m b i g u o u s . F ina l ly ,

© Biologische Anstalt Helgoland, Hamburg

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Ecology of mar ine parasites 7

"masking" of t rypanosomes induces changes in the host 's recogni t ion of parasi tes a nd consequent ly its i m m u n e response. Mar ine examples of supply of subs tances and changes in the host 's i m m u n e responses by parasi tes are not known. Direct observat ions in aquar ia and sometimes in na ture indica te that parasi tes may kill host ind iv idua l s and circumstant ia l evidence from natura l infections provides further ev idence for fatal effects of parasites.

However, not all effects are negat ive. For example, Lincicome has shown that protozoan and helminth parasites may supply compounds lacking in a deficient diet and thus may be of benefi t to the host (Rohde, 1982) and Berland (1980} sugges ted that ascaridoid nematodes in the stomach of fishes, mar ine birds, seals and whales may mechanical ly loosen and b reak up large food particles, permi t t ing the digest ive fluids to seep into the core quickly. This could be impor tant because food is often inges ted whole or in large chunks. Berland (1961) provided c i rcumstant ia l ev idence that char, Salmo alpinus, is lured to the mouth of the s luggish G r e e n l a n d shark by copepods, Ommatokoita elongata, which live a t tached to the shark 's eyes. Finally, an imals l iv ing in the parasite 's macroenv i ronment may harm it (e.g. c leaner fish} or be of benef i t to it {e.g. as sources of food}.

Effects of parasites on host popula t ions in the sea are much less known. Only few cases of large-scale mortali t ies unde r apparen t ly normal condit ions have b e e n recorded. For example, 500-600 dead mul le t per km of shoreline, caused by infect ion with the myxozoan Myxobolus exiguus were observed in parts of the Black and Azov Seas (Petrushevsky & Shulman, 1961). Dogiel & Bychowsky (1934) and D u b i n i n a (1949) reported mass mortal i t ies of fish due to larval t rematodes in brackish es tuar ine envi ron- ments (Aral Sea, Volga delta}.

Rohde (1982) reviewed the ev idence for mar ine mass mortal i t ies clue to parasites. He concluded that parasi te number s unde r na tura l condi t ions are usua l ly far be low that which a host ind iv idua l and popula t ion could carry, as ev idenced by the heavy parasi te loads occasionally observed, and "corresponding to the low infect ion rates of hosts with most parasites, observations of mass mortal i t ies unde r na tura l condit ions are rare. Even in cases where condit ions seem to be normal, the effects of h u m a n activities, such as overfishing or removal of predators, cannot be ruled out".

Nevertheless, the fact that mass mortali t ies due to parasi tes have b e e n observed so rarely under natura l conditions, does not necessar i ly m e a n that mass mortali t ies are rare. It could also mean that fish w e a k e n e d by disease are soon ea ten by predators. Experi- ments under carefully controlled condit ions s imula t ing the na tura l env i ronment , and extended observations in na ture are necessary to improve our knowledge of this important aspect of mar ine parasitology. Unfortunately, inc reas ing h u m a n activities make observation of diseases in the sea unde r "na tura l" condit ions more and more difficult.

On the other hand, observat ions of mass mortal i t ies unde r abnormal , crowded conditions, are not rare. Oyster beds have b e e n devasta ted repea tedly by parasites, al though other factors beside parasites may have b e e n contr ibutory factors (discussion in Rohde, 1982}, and fish kept in tanks or aquar ia are often ki l led by parasites, par t icular ly by Protozoa and Monogenea. Directly t raceable to h u m a n activities is the long- term destruction of s turgeon fisheries in the Aral Sea by the m o n o g e n e a n Nitzschia sturionis, which is well documen ted {e.g. Lutta, 1941a~ Petrushevsky & Shulman, 1961}. Dogiel &

8 K. Rohde

Lutta (1937) reported that spiny sturgeon, Acipenser nudiventris, were dying in large numbers , due to the large (up to 2 cm long) g i l l -dwel l ing monogenean . In saltwater areas infect ion was 100 %, in areas with slightly reduced sal ini ty almost 100 %. Max- imum intens i ty of infect ion was 600. Worms did not only cover the gills, but also had spread to the lips and into the mouth. Some worms had even crept into the gut, where they r ema ined active for some time. Fish with many worms had a reduced fat content, and there was a genera l emacia t ion of the body, as welt as j aundice with yellowish- green colourat ion of the organs ad jacen t to the gall bladder , and wr ink l ing of the liver. No other parasi tes were present, nor was there any s ign of bacter ia l disease. Nitzschia sturionis was not found dur ing a previous examinat ion in 1930, and local f ishermen had not seen the parasi te previously. It was apparent ly in t roduced into the Aral Sea from the Caspian Sea. In 1933, 350 000 larvae and in 1934, 7 mi l l ion larvae of Caspian stellate s turgeon were in t roduced into the Aral Sea. In addition, 90 spawners were introduced in 1934 wi thout previous inspect ion for fish disease, and Nitzschia was k n o w n to occur in the Casp ian Sea (Dogiel & Lutta, 1937). According to Osmanov (1963) mortali t ies due to the parasi te in the Aral Sea occurred in 1936, and sturgeon fisheries had no commercial s ignif icance for the next 20 years.

Lutta (1941b) made a deta i led study of the effects of Nitzschia sturionison Acipenser nudiventris. Its opisthaptor causes a mechanica l irritation of the gill tissue. This and supposed act ion by toxic subs tances secreted by the worm, leads to an in f lammat ion of the gills. "Histological examina t ion revealed the following effects: mechanica l destruc- t ion of the gill t issuel hyperplas ia of the epi thel ium of the pr imary gill layers and to a lesser degree hyper t rophy of the connect ive tissue~ atrophy of the gil l capillaries~ and atrophy of the secondary gill layers. Morphological changes were so marked that gas exchange was apparen t ly par t ia l ly or completely impossible, l ead ing to acute disease

and mass mortali ty."

EFFECTS OF MACRO- AND MICROENVIRONMENT ON CHARACTERISTICS OF PARASITES

Main ecological characteristics of mar ine parasites (and any other parasites) are shown in Figure 2. That both macro- and microenvi ronment jointly or separately deter-

Macrohabitat Microhabitat of endoparasite Food of endoparasite

Pathogenicity of endoparasite Reproductive mechanisms of

endotmrasite

Environment

_ _ ~ Host

Host range Microhabitat of ectoparasite Intensity and prevalence of infection Food of ectoparasite Life span Aggregated distribution Species diversity Pathogenicity of endoparasite Reproductive mechanisms of ectoparasite Infection mechanism

Parasite

Fig, 2, Diagram showing the factors that determine ecological characteristics of parasites

Ecology of mar ine parasi tes 9

mine some of the characters, wil l be i l lustrated by two examples (Fig. 2). The mi-

crohabitat of monogeneans on the gills of mar ine fish is charac te r ized by cer ta in physical parameters of the macroenvi ronment (e,g. s t rength and direct ion of wa te r currents), but

also by characterist ics of the host (e.g. gil l arch or f i lament for at tachment) . Mi- crohabi ta ts of nematode larvae in the mesen te ry of fishes, on the other hand, are ent i re ly

de t e r mi ned by characteristics of the host. Finally, the macrohab i ta t of a parasi te , be ing

the total of habitats occupied by the host species infec ted wi th a par t icular parasi te , is en t i re ly determined by factors in the macroenvi ronment , some affect ing the host, others

affect ing free-l iving stages of the parasi te , etc. Examples will be taken from various groups of mar ine he lmin ths and parasi t ic

protozoans. The relative impor tance of var ious groups of parasi tes of mar ine fishes, wh ich have

b e e n studied best, is i l lustrated by Tables 1 and 2. M a n y s tudies h a v e shown that d igenet ic t rematodes have the greates t species diversity, fo l lowed by m o n o g e n e a n s and

copepods.

HOST RANGE AND H O S T SPECIFICITY

Rohde (1982) d i s t inguished host r ange and host specif ic i ty of parasi tes. Host range is the number of host species infected by a cer ta in paras i te species i r respect ive of how

heavily and f requent ly the var ious host species are infected, whe reas host specif ici ty

takes intensi ty and/or p r eva l ence (frequency) of infect ion into account. For accurate quant i ta t ive descript ions of host specificity, Rohde (1980a) d e v e l o p e d specif ici ty indices.

One index is based on densi ty of infect ion (total number of parasi te ind iv iduals found in

a host popu la t ion /number of host ind iv iduals examined) .

Table 1. Numbers of known parasites from mullets (after various authors, from Paperna & Over- street, 1981)

Parasites Eastern Northern Black Sea Mississippi Additional Mediterranean Red Sea reports from

southeastern US

Blood Protozoa 0 1 0 2 0 Gill Protozoa 1 2 3 4 2 Microspora 0 1 0 0 0 Myxozoa 2 4 2 3 0 Monogenea 6 5 2 3 6 Digenea - adults 6 7 7 11 5 Metacercariae 12 2 2 6 3 Cestoda - larvae 2 0 1 3 0 Nematoda 4 0 1 3 4 Acanthocephala 2 1 1 1 0 Copepoda 4 4 1 6 11 Branchiura 0 0 0 1 4 Isopoda 0 2 0 1 1 Hirudinea 0 0 0 1 1

Total 39 29 20 45 37

10 K. R o h d e

Table 2. Host ranges of parasi tes of fish in the Barents Sea. Host records from other seas are considered, records of accidental hosts in which paras i tes do not mature are not [data from

Polyansky, 1966)

Parasite group Number Percentage of species of species In 1 host In > 1 In 1 Primarily In Undeter-

species species of family in 1 several mined 1 genus family families

Protozoa 25 21,7 4.3 17,4 21,7 8.7 26.2 Monogenea 21 52.4 9.5 33.3 4.8 0 0 Digenea 37 2.8 11.1 25,0 16.7 44.4 2.8 Cestoda 19 12,5 6.2 18,7 25.0 31.4 6,2 Nematoda 12 9.1 0 36.3 g. 1 36.4 9.1 Acanthocepha la 3 0 0 0 0 100.0 0 Hi rudinea 3 33.3 33.3 33,3 0 0 0 Copepoda 15 6,7 20.0 27,0 33,2 6.7 6.7 Isopoda 1 0 0 0 100.0 0 0

Total 136 17.2 9.2 24.9 17.9 23.9 6.9

Xi]

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(S i = h o s t s p e c i f i c i t y of i th p a r a s i t e s p e c i e s ; Xij - n u m b e r of p a r a s i t e i n d i v i d u a l s of i th

s p e c i e s i n j t h h o s t s p e c i e s ; nj = n u m b e r of h o s t i n d i v i d u a l s of j t h s p e c i e s e x a m i n e d ; hij = v

r a n k of h o s t s p e c i e s j b a s e d o n d e n s i t y of i n f e c t i o n AiJ, s p e c i e s w i t h g r e a t e s t d e n s i t y h a s r a n k 1). nj

A s p e c i f i c i t y i n d e x of a l l p a r a s i t e s p e c i e s of a c o m m u n i t y c a n b e d e f i n e d S i as S c ( d e n s i t y ) -

r tp

(np = n u m b e r of p a r a s i t e s p e c i e s i n t h e c o m m u n i t y ) . T h e s p e c i f i d t y i n d e x b a s e d o n

f r e q u e n c y ( p r e v a l e n c e ) of i n f e c t i o n u s e s t h e s a m e f o r m u l a b u t t h e p a r a m e t e r s i n t h e

f o r m u l a a r e c h a n g e d as fo l lows : Xij = n u m b e r of h o s t i n d i v i d u a l s of j t h s p e c i e s i n f e c t e d

w i t h p a r a s i t e s p e c i e s i, nj -~ n u m b e r of h o s t i n d i v i d u a l s of t h e j t h s p e c i e s e x a m i n e d , hij =

r a n k of h o s t s p e c i e s b a s e d o n f r e q u e n c y of ' i n fec t ion . It is p o s s i b l e to t a k e b o t h i n t e n s i t y a n d f r e q u e n c y of i n f e c t i o n i n t o c o n s i d e r a t i o n , for

i n s t a n c e b y u s i n g Si ( dens i t y ) + Si ( f r equency} d i v i d e d b y a f ac to r of two, V a l u e s for b o t h i n d i c e s v a r y b e t w e e n 0 a n d I. T h e c l o s e r to I , t h e h i g h e r t h e d e g r e e

of h o s t spec i f i c i ty . A n e x a m p l e is g i v e n i n T a b l e 3. Lecithaster gibbosus i n f e c t s 12 of 31

h o s t s p e c i e s i n t h e W h i t e Sea . H o w e v e r , s e v e r a l h o s t s p e c i e s a r e m o r e f r e q u e n t l y

i n f e c t e d t h a n o t h e r s a n d S i ( f r e q u e n c y ) is t h e r e f o r e 0.54. M o s t p a r a s i t e i n d i v i d u a l s a r e

f o u n d i n o n e h o s t s p e c i e s , a n d Si ( d e n s i t y ) is t h e r e f o r e 0.99 i n d i c a t i n g t h a t o n e f i sh

s p e c i e s s e r v e s a s a m o r e e f f e c t i v e h o s t t h a n a l l t h e o t h e r s c o m b i n e d .

A m o n g p a r a s i t e s of m a r i n e f ish, M o n o g e n e a h a v e t h e m o s t r e s t r i c t e d h o s t r a n g e s

a n d t h e g r e a t e s t d e g r e e of h o s t spec i f i c i ty . For i n s t a n c e , a c c o r d i n g to t h e d a t a i n R o h d e

Tab

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95

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84

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64

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15

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83

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83

143

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98

0.84

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41

83

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99

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12 K. Rohde

(1978, 1979), of 435 species of mar ine Monogenea 78 % were restricted to one host species, 89 % to one genus, 96 % to one family, a nd 98 % to one order. However, all groups of parasi tes show host specificity of vary ing degrees. Sometimes, hosts be long to one taxon or to closely re la ted taxa; in other words, parasi tes have a so-called phy- logenet ic host specificity. In other cases, ecological factors de te rmine specificity and it is often reduced w h e n ecological barriers are removed, for ins tance in aquaria.

Factors responsible for host specificity are little unders tood {see review by Rohde, 1982). In some cases, morphological adaptat ions of a parasi te facilitate its a t tachment to a par t icular host in a lock and key pattern; in other cases cer ta in physicochemical factors may induce ha tch ing in one host species but not in another. Such factors may determine host as wel l as site specificity {see discussion of microhabitats) . Often, differential mortal i ty leads to host restriction. Thus, if m o n o g e n e a n s of the species Entobdella soleae are exper imenta l ly transferred to wrong hosts, worms become de tached after 24-30 h, a l though they survive on glass for 2 -6 days (Kearn, 1967, 1970). Se rum factors were shown to be responsible for host specificity of the cestode Acanthobothrium quadripar- titum. In vitro, it survives for more than 24 h in fish serum from its na tura l host, the ray Raja naevus, but 80 % of the worms are ki l led in serum from the "wrong" host, Raja radiata, with in 2 h (McVicar & Fletcher, 1970). Presence of another parasi te species may be a prerequis i te for infect ion of a host. Thus, larvae of the bird schistosome Austrobilharzia terrigalensis occur only in snai ls of the species Velacumanthus australis on the New South Wales coast of Australia, which are also infected with other tre-

matodes {Walker, 1979}. Ecological factors de t e rmin ing host specificity may be the feeding habits of the

host{s). Thus, final hosts of the t rematode Paucivitellosus fragilis on the coast of eastern Austra l ia are several un re l a t ed fish species, al l of which are grazers {Pearson, 1968}. The infect ive cercaria is a t tached to a subs t ra tum and inges ted by feeding fish. Non-graz ing fish have no chance of becoming infected a l though they are probably sui table hosts if artificially infected.

MICROHABITATS

There are no species of parasi tes that infect all t issues and organs of the host 's body equally, i,e. all species show preferences for certain microhabitats of vary ing degrees. Examples are represen ted in Figures 3 and 4 and in Tables 4 and 5. O n Prionotus punctatus, a teleost fish from the cold- temperate coast of Argent ina, only three species of gill and skin parasites were found. An isopod was recovered only once from the fins and no s ta tements other than that it is an ectoparasi te are possible about its microhabitats. Cysts of u n k n o w n nature are restricted to the gill f i laments which they appear to infect more or less at random. The copepod Blias prionoti also occurs only on the gill f i laments bu t prefers the first three long i tud ina l quarters and the tips of the f i laments (Fig. 3).

O n Scomberjaponlcus in the warm waters off Sao Paulo State, Brazil, 10 species of parasi tes were found, on the gills and in the mouth cavity (Fig. 4; Table 5). Three species of d idymozoid t rematodes show the greatest site specificity. Two hundred and sixteen ind iv idua ls (always encapsu la ted in pairs) were found only in a small site unde r the gill operculum. Two hund red and forty-four ind iv idua l s of a different species of the same genus (Nemathobothrium sp. III) occurred in the dorsal roof of the mouth cavity, and 36

E c o l o g y of m a r i n e p a r a s i t e s 13

Table 4. Prionotus punctatus, Mar del Plata, Argent ina. Distr ibution of ectoparasi tes on 32 fish

Gill Gill Gill no. Longitudinal Exter- Inter- fila- arch quarter no. nal nal ment fila- fila-

1 2 3 4 1 2 3 4 ment ment

Fins

Blias prionotl 85 0 18 27 26 14 21 35 22 6 25 59 0 (Copepoda) Cysts 22 0 3 7 10 2 4 9 9 0 12 11 0 Isopod 0 0 0 0 0 0 0 0 0 0 0 0 1

i n d i v i d u a l s i n t h e a n t e r i o r a n d p o s t e r i o r e n d s of t h e a r c h e s of a l l fou r gi l ls . A t h i r d

s p e c i e s ( N e m a t h o b o t h r i u m sp. II) w a s r e s t r i c t e d to t h e g i l l f i l a m e n t s , a n d p a r t i c u l a r l y to

t h e i n t e r n a l f i l a m e n t s of t h e f i rs t g i l l a n d t h e e x t e r n a l f i l a m e n t s of t h e t h i r d gi l l . Al l o t h e r

s p e c i e s o n S c o m b e r japon icus , for w h i c h s u f f i c i e n t d a t a a r e a v a i l a b l e , s h o w s i m i l a r

m i c r o h a b i t a t p r e f e r e n c e s . E x a m p l e s for m i c r o h a b i t a t s p e c i f i c i t y of e n d o p a r a s i t e s a n d

p a r a s i t e s of i n v e r t e b r a t e s w e r e g i v e n b y R o h d e (1982).

M i c r o h a b i t a t s f r e q u e n t l y a re n o t s ta t ic , t h a t is, t h e y c h a n g e w i t h t h e a g e of t h e

5 c m

P

1 o Cysts

'I " " ) ~ ~ ) 2cm

Fig. 3. Prionotus punctatus, Mar del Plata, Argent ina. Distr ibution of ectoparasi tes on 32 fish

14 K. Rohde

I 5 cm

2cm I t

2

",.

• Nemathobothrium sp. I J Grubea sp,

. . I I • Caligus productus o . ,, I I , single pairs x Caligus pelamydis

0 " ', I I , juv. • Clavellisa scombri © ,, ,, III [] Cysts , Kuhnia sp. I n . " II

Fig. 4a. Scomber ]aponicus, $5o Paulo State, Brazil. Distribution of didymozoids and ectoparasites on 98 fish. Body surface examined in 50 fish and Nemathobothrium sp, III. recorded in 70 fish

paras i tes and /or wi th the age of the host. For example , l a rvae and young females and males of the copepod Caligus diaphanus l ive on the gil l f i laments of the gunard, Trigla lucema, at He lgo land , whereas adults infect the inner wal l of the opercular cavity (Rohde, 1980b). In some cases seasonal microhabi ta t changes have b e e n demons t ra ted or

changes due to the effect of other parasites. Thus, sites of the acan thocepha lan

Ecology of mar ine parasi tes 15

D

122 ~ . . . .

5 cm ,I

2cm I l

2

Fig. 4b. Scomberjaponicus, Distribution of several parasites, For symbols see Fig. 4a

Echinorhynchus gadi in Melanogrammus aeglefinus undergo seasonal changes (Scott, 1981), and the same parasi te is more restricted to the posterior in tes t ine w h e n the nematode Hysterothylacium clavatum is also present. Conversely, H. clavatum is more restricted to the anter ior in tes t ine in the presence of E. gadi (Shotter, 1976).

Very little is known about the reasons for site preferences (see review by Rohde, 1982). In some cases, morphological characteristics de te rmine at least partly, whe ther a parasite can live in a certain microhabi ta t or not (Figs 5-8). For example, of three species of ectoparasitic he lmin ths on the gills of Seriolella brama in New Zealand, Syncoelium filiferum is always at tached to the spines of the gill rakers and arches by me a ns of a stalked muscular ventral sucker which is not capable of a t taching to gil l f i laments or smooth surfaces. The m o n o g e n e a n Neogrubea seriolellae has posterior c lamps which consist of two valves sui table for g rasp ing gi l l f i laments bu t not sp ines or smooth surfaces. A second monogenean , Eurysorchis australis is a lways a t tached to the gil l arches by means of modif ied clamps which do not act as g rasp ing organs bu t as flat suckers for a t tachment to the smooth surface of the arches (Rohde et al., 1980). The

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E c o l o g y of m a r i n e pa ra s i t e s 17

go

t e - -

yo -__~/ iFr

Fig. 5. Syncoelium filiferum, go = gonopore, ov = ovaries, te = testes, yo = yolk glands

Fig. 6. Ventral sucker of Syncoelium [ililerum grasping spines of gill arch

s t ruc ture of t h e a c e t a b u l u m in Syncoel ium d o e s no t on ly d e t e r m i n e t h e m i c r o h a b i t a t of the paras i te , bu t a lso its hos t r a n g e . A l a r g e v a r i e t y of f ish s p e c i e s w e r e f o u n d to b e

infec ted , bu t o n l y t h o s e w i t h s p i n e s on the g i l l a r c h e s or rakers .

In o the r cases , p h y s i c o - c h e m i c a l hos t s t imul i w e r e s h o w n to b e at l ea s t pa r t l y r e spons ib l e for s i te spec i f ic i ty . Thus , e x - s h e a t h m e n t a n d d e v e l o p m e n t of c e r t a i n n e m a t o d e s pec i e s w e r e s h o w n to r e q u i r e hos t s t imul i . A l t h o u g h t h e s t imu l i t h e m s e l v e s

m a y not be v e r y spec i f ic , t h e y m a y ac t on l a r v a e of d i f f e r en t s p e c i e s u n d e r d i f f e r en t

condi t ions of r e d o x p o t e n t i a l a n d p H a n d thus d e t e r m i n e t he i r m i c r o h a b i t a t s (and hosts)

18 K. R o h d e

(Rogers , 1957; S o m m e r v i l l e , 1957). H o w e v e r , a l l n e m a t o d e s s t u d i e d so fa r a r e n o n -

m a r i n e .

W i t h r e g a r d to t h e b i o l o g i c a l f u n c t i o n of m i c r o h a b i t a t r e s t r i c t i o n , R o h d e (1976a, b,

1977) s u g g e s t e d t h a t e n h a n c e m e n t of t h e c h a n c e s to m a t e m a y b e a n i m p o r t a n t f ac to r

r e s p o n s i b l e for s u c h r e s t r i c t i o n . E v i d e n c e is t h a t s e x u a l l y m a t u r e a n d s e s s i l e s p e c i e s as

w e l l as s p e c i e s o c c u r r i n g i n l o w d e n s i t i e s o f t e n h a v e t h e m o s t c l e a r l y r e s t r i c t e d mi -

c r o h a b i t a t s .

Fig. 7. Eurysorchis australis from the gill arches of Seriolella brama (after Rohde et al., 1980). bs = buccal sucker, c = caecum, ci = cirrus, cl ---- clamps ov = ovary, pad = clamp pad,

p h ~ pharynx, ut = uterus, vd = vas deferens, vit = vi tel lar ia

M A C R O H A B I T A T S

T h e m a c r o h a b i t a t of a p a r a s i t e c o n s i s t s of t h o s e n i c h e c o m p o n e n t s w h i c h a l so

r e p r e s e n t t h e h a b i t a t of i ts hos t ( s ) (Rohde , 1982). For e x a m p l e , a c c o r d i n g to C a n n o n

(1977a, b), a m o n g n e m a t o d e l a r v a e of m a r i n e f i sh i n s o u t h e a s t e r n Q u e e n s l a n d , Anisak i s

o c c u r s o n l y i n o p e n w a t e r f ish , Contracaecum ( p r o b a b l y Hysterothylacium) o n l y in

Ecology of mar ine paras i tes 19

inshore shal low wate r fish, and two others, Phocanema (= Pseudoterranova) and Thyn-

nascaris (= Hysterothylacium) have in t e rmed ia t e distr ibutions. Russian authors have ex tens ive ly s tudied the factors wh ich affect the dis t r ibut ion of

mar ine ,pa ras i t e s in different macrohabi ta ts . A r e v i e w of this work was g iven by

Polyansky (1961). The impor tance of chemica l factors and par t icular ly sal ini ty was shown for parasi tes and espec ia l ly ectoparas i tes in the Aral Sea. Some groups l ike

Myxozoa and Ci l iophora were absent in the sa l ine part, and M o n o g e n e a and Trema toda were bet ter r ep resen ted in the f reshwater part. Tempera tu r e affects, for instance, the

t rematode Derogenes varicus, which occurs in numerous fish species in cold surface

Fig. 8. Neogrubea seriolellae from the gill filaments of Seriolella brama (after Rohde et al., 1980). e = egg, lh = large hamutus, te = testes, v 1 = 1st valve of clamp, v~ = 2nd valve of clamp. For

further abbreviations see Figure 7

waters. At low lati tudes, it occurs only in deepe r cold waters or in areas wi th cold currents.

Ectoparasites somet imes must be able to wi ths tand ex t reme condi t ions in the

environment of their hosts, and somet imes rapid changes in those conditions. Thus, the louse Antarctophthirus ogmorhini on the Wedde l seal, Leptonychotes weddelli, in

Antarctica is exposed to ex t remely low tempera tu res and rapid pressure changes dur ing

diving of the hosts. It could be shown that the paras i te survives cool ing to - 2 0 °C for 36 h, and diving to 600 m for 45 min (Murray, 1976).

20 K. Rohde

PREVALENCE AND INTENSITY OF INFECTION IN HOSTS OF DIFFERENT AGE AND SEX, AND IN DIFFERENT SEASONS

In all host species which have b e e n wel l examined , infect ions wi th parasi tes change with age. Some spec ies are most common in juven i l e hosts, others in hosts of midd le or

old age. Scott (1969) found that the t rematode Hemiuros Ievlnseni in 581 Argentina sllus from the nor thwes te rn Atlant ic had a h igh intensi ty and p r e v a l e n c e in young fish, both

pa ramete r s dec reas ing with age. Lecithophyllum botryophoram, another t rematode, on

the other hand, had a h ighe r intensi ty and p reva l ence of infect ion in larger fish. A third species, Derogenes various, was in termedia te . Apparen t reasons for the differences were

migra t ion of the fish wi th a cor responding change of diet. Young a rgen t ines feed heavi ly

on p lanktonic copepods in shal low water and become infec ted with Hemiurus, whereas

matur ing fish move into deepe r water and eat a h ighe r proport ion of near-bot tom

organisms which are second in t e rmed ia t e hosts of Le¢ithophyllum. In long- l ived parasites, h igher infect ion may s imply be due to a chance accumula-

t ion of paras i tes over time. Larger hosts, furthermore, eat more and come into contact wi th la rger vo lumes of wa te r which increases the chances of infect ion with endo- and

ectoparasi tes , and they also represen t a la rger var ie ty of la rger microhabitats . Immune

react ions which e l imina te some parasites, as wel l as age res is tance which may be due to th icker body layers p r even t ing entry of parasites, counteract this to a certain degree .

However , a l toge ther an increase of parasi te infect ions wi th age is more common than a decrease . A w e l l - d o c u m e n t e d e x a m p l e is r ep resen ted in F igure 9.

Differences of infect ion b e t w e e n the two sexes of a host species are less common. 6 0 " 4

! I I

1 9 5 0 - 1 9 5 1 ~ / / -- 30

1961-1952

2 5 c" 0 ~a E 2 0 0 .;-

E 0 a)

I 0

5

0 2 3 4 5 6 7

Years

Fig. 9. Increase of mean level of infection of Clupea harengus pallasi with larval Anisakis in 1950-51 and 1951-52. Ordinate: geometric means of nematodes per fish. Abscissa: age of fish in

years (redrawn after Bishop & Margolis, 1955)

Ecology of mar ine parasi tes 21

Male walleye pollock, Theragra chalcogramma, in British Columbia , Canada , were more heavily infected with the third stage larvae of Anisakis s implex and plerocercoids of Nybelinia surmenicola than females of s imilar lengths, a l though preva lence of infection did not differ significantly. The other two he lmin th species examined, larval anisakids, infected both sexes equa l ly (Arthur et al., •982). According to Wil l iams (1965), the monogenean Calicotyle kroyeri was never found in gravid female rays, Raja radiata, al though non-grav id females may be infected. Male snails, Hydrobia ulvae, in Britain were much more commonly infected with larval t rematodes than females, the ratio of infected males to infected females sometimes reaching 16 : 1 (Rothschild, 1938). Reasons for the differences may be of different kinds: different feed ing habits of males and females (shown for some fish species), sexual differences in the composi t ion of the skin (shown for freshwater trout), and possibly hormonal and t issue differences (snails?) (see review in Rohde, 1982).

Seasonal f luctuations are k n o w n for m a n y parasi te species of fish in cold- temperate seas. According to M611er (1974, 1975) most endoparas i tes of f lounder, Pla tich thys flesus, and all of Gadus morhua in the Bay of Kiel showed seasonal fluctuations. Ectoparasites may show more distinct fluctuations. However, even in cold- temperate seas f luctuat ions are by no means universal , and very few studies in warm waters have b e e n made. An example is the study of larval t rematodes of two snai l species on the Great Barrier Reef by Rohde & Sand land (1973) and Rohde (1981). Over two years, no seasonal f luctuat ions occurred in any of the trematodes.

Reasons for seasonal differences may be differences in feed ing habits du r ing the cold and warm months, changes in the composi t ion of the skin of fishes (shown for freshwater trout), and seasonal i ty of the infective stages of parasi tes (shown for m a n y helminth species).

Table 6. Food of some marine helminths

Parasite Food Source

Monogenea Polyopisthocotylea

Monogeuea Monopisthocotylea

Didymozoida (Trematoda)

Aporocotyle simplex (Trematoda)

Cestoda

Nematoda

Hysterothylacium bidentatum (Nematoda)

Salvelinema walkeri (Nematoda)

Acanthocephala

Hirudinea

Larval Gnathiidae (Isopoda)

Copepoda

Blood, also low molecular organic compounds from water

Mucus, epithelial cells, sometimes blood

Blood and/or tissue fluid

Blood

Gut contents, tissue liquid

Gut contents, host tissue, or blood

Fluid contents of stomach

Blood

Contents of intestine, tissue liquid

Blood, some also prey

Blood

Blood, tissue, mucus

Various authors Halton (1978)

Various authors

Yamaguti (1970)

Thulin (1980)

Various authors

Various authors

Geller (1957)

Margolis (1967)

Various authors

Various authors

Various authors

Kabata (1970)

22 K. Rohde

FOOD

Some examples of food resources used by mar ine parasi tes are g iven in Table 6. Of par t icular interest is that species of ectoparasites may supp l emen t host nutr ients by compounds from the macroenvi ronment . Hal ton (1978) showed that Dididophora mer- langi can absorb L-a lan ine and L-leucine from the water through its tegument , a l though it feeds l ike all other polyopis thocotylean m o n o g e n e a n s also (and probably mainly} on the host 's blood. The food may differ with the sex or age of the parasite. For example, the copepod Lepeophtheirus salmonis feeds on the blood of its host, the Atlant ic sa lmon Salmo salar, but adul t females do this to a greater extent than males and postchal imus larvae (Brandal et al., 1976).

LIFE SPAN

This aspect has b e e n s tudied much less thoroughly than in parasi tes of man and domest ic animals . It is k n o w n that h u m a n schistosomes may live for many years, whereas other h u m a n parasi tes are short- l ived and infect ions are lost after short periods.

Seasonal i ty of infect ion with many species of Monogenea indicates that the adults l ive less than one year (e.g. Gastrocotyle trachuri, according to Llewellyn, 1962, 1964). T ime unt i l matura t ion depends on tempera ture (Benedenia seriolae: 18 days at 21.8-26 °C, 45 days at 17-18 °C) and may be slow (Diclidophora denticulata: 180 days) (Table 7).

Table 7. Survival and maturation times of oncomiracidia of some marine Monogenea

Species Survival time Time until maturation Source (days)

Benedeniaseriolae l day 18 (21.8-26°C) Hoshina (1968) 45 (17 -18°c)

Entobdella soleae

E. hippoglossl

Neobenedenia melleni

Diclldophora dentlculata

Diclldophora merlangi

Gastrocotyle trachuri

1 day

> 1 day

6 h (loss of cilia) -

1 day 180

12-15 h

_ 9 h

30h

> 1 day

(13 °C, end of active swimming)

(18 °C, end of active swimming)

(18 °C, death)

Keam (1967)

Kearn (1974a)

Jahn & Kuhn (1932)

Frankland (1955)

MacDonald (1975)

Llewellyn (1964)

Examples of some mar ine hemiur id t rematodes are g iven in Table 8. They show that even b e t w e e n species of one family there may be great differences in maturat ion t ime

and life span. The acan thocepha lan Echinorhynchus lageniformis lives for about one year in the final host, the starry f lounder Platlchthy$ stellatu$, since older fish lose the parasi tes (Olson & Pratt, 1971). Among the leeches, the species Johanssonia arctica lives

Ecology of mar ine paras i tes 23

Table 8. Survival and maturation time of some hemiurid trematodes of marine fishes

Parasite Life span Time until Source maturation

Hemiurus communis 8 months (average) - Meskal (1967) 15 months (maximum)

H. communis? Several years - Balozet & Sicart (1960)

Lecithophyllum botryophorum 8-10 months - Scott (1969)

Lecithaster sp. 3-9 months - Boyce (1967)

Tubulovesicula lindbergi -> 31 months 2-4 months Margolis & Boyce (1969)

Lecithastergibbosus 2-9 months 1-2 weeks Margolis & Boyce (1969)

Table 9. Survival times of a marine metacercaria and some marine cercariae

Parasite Survival time Source

Bucephalus haimeanus (metacercaria)

Paucivitellosus [ragilis (furcocystocerceus cercaria)

3 species of cystophorous cercariae

--> 10 months Matthews (1973)

3-4 days Pearson (1968)

2-5 days (Iocomotory activity)

2, 4-5, 20-25 days (medium life span)

6-7, 10-14, 35--40 days (maximum life span)

Timofeeva (1978)

21/2 years at - 1 to 2 °C (Khan, 1982), but others l ive less than one year. Thus, j uven i l e

Calllobde1Ia carotlnensls at tach t hemse lves to fish in win te r and die after cocoon

deposi t ion by May (Sawyer & Hammond , 1973). In Hemibde l la soleae, matur i ty is

reached in about 23 days after infection, and full size in about 37 days (Llewellyn, 1965}. Larval s tages have vast ly var iab le life spans {Table 9). A m o n g t rematode larvae,

unencysted forms l ike mirac id ia or cercar iae l ive only for hours (cercariae probably for

> 1 day). Furcocystocercous and cystophorous cercar iae, wh ich are somewha t pro tec ted from the environment , may survive for several or many days, and in me tace rca r i ae wi th

their effective cyst-wall, survival t ime may ex tend to many months. Some terrestr ial and freshwater forms may e v e n l ive for many years. In oncomirac id ia of Monogenea , which

are very small (< 1 mm long} and fragile, dea th occurs usual ly wi th in 1 day (Table 7).

AGGREGATED DISTRIBUTION

Most parasite species are not r andomly or uni formly dis t r ibuted in host populat ions , they show an agg rega t ed (overdispersed, contagious) distr ibution; that is, some indi-

viduals of a host popula t ion are more heav i ly in fec ted than expec t ed in a r andom distribution, and others are infected very lit t le or not at all. Severa l theoret ical distr ibu-

24 K. R o h d e

Table 10. Observed frequency distribution of Stephanostomum baccatum metacercariae in juvenile plaice from Firemore Bay, with negat ive binomial fitted to data (after MacKenzie & Liversidge,

1975). X 2 = 11.386, P > 0.05

Number Observed number Fitted negative of parasites of plaice binomial distribution

0 136 1- 5 164 6- 10 50

11- 15 35 16-- 20 12 21- 25 16 26- 30 3 31- 35 6 36- 40 1 41- 45 2 46- 50 1 51- 55 1 56- 60 2 61- 65 1 66- 70 1 71- 75 0 76- 80 0 81- 85 0 8 6 - 90 0 91- 95 0 96-100 1

101-145 0 146-150 1

125.9 154.9 60.1 33.2 20.2 12.8 8.4 4.6

11 13.0

t ions h a v e b e e n u s e d to d e s c r i b e a g g r e g a t i o n in pa ras i t e s , t h e m o s t c o m m o n one b e i n g

the n e g a t i v e b i n o m i a l . T a b l e 10 con t a in s d a t a on f r e q u e n c y d i s t r i bu t ion of a l a rva l t r e m a t o d e s p e c i e s in p l a i ce . T h e d a t a c a n b e f i t t ed a lmos t pe r f ec t l y to a n e g a t i v e

b i n o m i a l (other e x a m p l e s in Rohde , 1982). Cro f ton (1971) e v e n u s e d a g g r e g a t e d dis-

t r i b u t i o n as a c h a r a c t e r i s t i c of pa ra s i t i sm. H o w e v e r , as p o i n t e d ou t by R o h d e (1982), such

d i s t r i bu t ions a r e a l so c o m m o n a m o n g f r e e - l i v i n g a n i m a l s a n d plants . Cro f ton (1971) h a s d i s c u s s e d the c o n d i t i o n s w h i c h l e a d to n o n - r a n d o m n e s s a n d

a g g r e g a t i o n in p a r a s i t e d i s t r ibu t ion . T h e s e c o n d i t i o n s are : (1) A ser ies of exposu re s , e a c h

w i t h a d i f f e ren t c h a n c e of i n f ec t i ons (e.g. n u m b e r s of c e r c a r i a e s h e d by sna i l s vary); (2)

t he i n f e c t i v e s t a g e s a r e no t r a n d o m l y d i s t r i b u t e d (e.g. c e r c a r i a e c l u s t e r e d c lose to snails) ; (3) a n i n f e c t i o n e n h a n c e s t h e p r o b a b i l i t y of f u r t he r i n f e c t i o n (e.g. d e c r e a s e of hos t ' s

r e s i s t a n c e d u e to h e a v y h e l m i n t h in fec t ion) ; (4) an i n f e c t i o n d e c r e a s e s t he p robab i l i t y of fu r the r i n f e c t i o n (e.g. i m m u n i t y ) ; (5) v a r i a t i o n s in hos t i n d i v i d u a l s m a k e the c h a n c e s of

i n f e c t i o n u n e q u a l (e.g. d i f f e r en t i n d i v i d u a l s w i t h d i f f e r en t food p re fe rences ) ; (6) t he

c h a n c e s of i n f e c t i o n of i n d i v i d u a l s c h a n g e w i t h t i m e (e.g. a g e res is tance) . O t h e r c o n d i t i o n s w h i c h c o n t r i b u t e to a g g r e g a t i o n are: (7) a s i n g l e p a r a s i t e ind i -

v i d u a l m a y m u l t i p l y on or in t h e hos t (e.g. g y r o d a c t y l i d m o n o g e n e a n s ) ; (8) hos t i n d i v i d u - als p r e f e r i n f e c t e d i n t e r m e d i a t e or t r anspor t hos ts to u n i n f e c t e d o n e s (e.g. i n f e c t i o n l e ads

Ecology of m a r i n e pa ras i t e s 25

to behav iour changes of i n t e rmed ia t e hosts which expose t hem to p r e d a t i o n by f inal hosts). Several of these factors wi l l u sua l ly be jo in t ly r e spons ib l e for a g g r e g a t e d distr ibut ions of paras i tes .

Some authors have m a d e sugges t ions conce rn ing the b io log ica l funct ion of a g g r e g a - tion of paras i tes . Accord ing to M a y (1977) it m a y b r ing about s t ab i l i za t ion of the host- paras i te associat ion, and accord ing to K e n n e d y (1975) b e c a u s e of a g g r e g a t i o n only few heavi ly infec ted ind iv idua l s of a host popu l a t i on usua l ly die. Dea th of these hosts m a y ensure comple t ion of the life cyc le of a pa ra s i t e which d e p e n d s on b e i n g e a t e n by the next host, but the host popu la t i on as a w h o l e is not g rea t ly affected. K e n n e d y (1976) also sugges ted that pa ras i t es in a g g r e g a t e d popu la t ions m a y have g rea te r chances of contact- ing ma t ing par tners .

However , no empi r i ca l ev idence in suppor t of any of the sugges t ions is ava i l ab le .

NUMBERS AND KINDS OF SPECIES

Concern ing the effects of eco log ica l factors on the n u m b e r of pa ras i t e s in m a r i n e fish, Polyansky & Bychowsky (1963) s u m m a r i z e d the resul ts of ex tens ive s tudies by Russian workers as follows: number s of pa ras i t e s a re i nc reased by (1) a g rea t va r ie ty of food (and consequen t ly of poss ib le i n t e r m e d i a t e hosts); (2) a long life span; (3) a l a rge a rea over which a fish mig ra t e s and consequen t ly an inc rease in contacts wi th o ther f inal hosts (exchange of pa ras i t e s wi th d i rec t deve lopmen t ) and i n t e r m e d i a t e hosts; (4) school formation; (5) a l a rge body size.

The At lant ic cod, Gadus morhua, is a l a rge fish occurr ing in dense popu la t ions ; it migra tes over long dis tances , has a long life (15 years) and a r ich var ie ty of food (in the Barents Sea more than 200 spec ies of fish, ben thos and plankton) , and consequen t ly a rich paras i te fauna, Dollfus (1953) c o m p i l e d da ta on its pa ras i t e s and r eco rded 71 species.

Type of die t and habi t s de t e rmine which k inds of pa ras i t e s are present . For example , the paras i te fauna of mul le t in the Black Sea (Reshetnikova, 1955) and the e a s t e rn Med i t e r r anean (Paperna, 1975) changes th roughou t the life of the fish, c o r r e spond ing to changes in hab i ta t and f eed ing pre fe rences . F ish sma l l e r t han 30 m m in coas ta l and es tuar ine waters have many d idymozo id t rematodes , ces todes and la rva l nema todes , acquired dur ing p l ank ton ic f eed ing in the open water . They are r e p l a c e d b y t r e m a t o d e s and acan thocepha lans acqu i r ed by ben th ic f e ed ing and ec toparas i t es from o lder fish with whom young fish now share the same habi ta ts . Fish re tu rn ing for s p a w n i n g to the open sea acqui re d e e p w a t e r t rematodes .

According to Po lyansky & Bychowsky (1963), g e n e r a l l y fry of mar ine fish b e c o m e infected first wi th paras i tes which use i n t e r m e d i a t e hosts, b e c a u s e schools of d i f ferent ly aged marine fish do not usua l ly mix and e x c h a n g e ec toparas i t es wi th d i rec t l ife cycles. Freshwater fish of di f ferent ages , on the o ther hand, mix f ree ly and acqu i re pa ras i t e s by contact first.

PATHOGENICITY

Marine paras i tes show a w ide r a n g e in the i r d e g r e e of pa thogen ic i ty . Var ious authors have repor ted that l a rvae of p s e u d o p h y l l i d e a n ces todes have l i t t le effect, and the same is true of many Monogenea . Accord ing to Kearn (1963), the sk in m o n o g e n e a n

26 K. Rohde

Entobdella soleae on Solea solea moves around f requent ly and the skin regenera tes fast. Thus, little damage is done. On the other hand, Neobenedenia melleni on several fish species can severely harm its hosts, by destroying their eyes, etc., and lead to death. However, fish may acquire p e r m a n e n t or partial i m m u n i t y after repeated exposures (e.g. Nigrelli , 1937). In t rematode larvae, t issue react ions may depend on the species, the site of infect ion and on whether the larvae are dead or al ive (see review in Rohde, 1982).

Effects may be aggravated when other parasites are present. Thus, Noble (1963) found a posit ive associat ion be tween the ciliate Trichodina and the m o n o g e n e a n Gyrodactylus on Gillichthys mirabilis, i.e. in tens i ty of infect ion with one species was greater w h e n the other was present. Al though no direct ev idence was provided, the author sugges ted that the ciliate feeds on host tissue da ma ge d by the m o n o g e n e a n (see also McVicar & MacKenzie, 1977).

Effects may also depend on env i ronmenta l conditions. Paperna & Overstreet (1981) reported that adul t t rematodes p robab ly cause little damage to mul le t in their natural habitats, but effects may be very severe when fish are t rapped in little water with many snails. Water qual i ty was shown to affect pa thogenic i ty of Monogenea . Thus, Skinner (1982) s tudied infect ions of the fish Gerres cinereus, Lutjanus griseus and Strongylura timucu with the m o n o g e n e a n s Neodiplectanum wenningeri, Ancyrocephalus sp. and Ancyrocephalus parvus, respectively, and the associated gill pathology. Fish were from two habi ta ts in South Biscayne Bay, Florida, one heavi ly pol luted with h igh amounts of ammonia , trace metals, and pesticides, and the other not polluted. Only fish from the pol lu ted habi ta t were heavi ly infected and showed marked pathological effects. Neodi- plectanum wenningeri, in l ight infections, caused mechanica l damage by deflect ing gill lamellae. In heavy infections, the lamel lae were covered with the monogeneans , and there was increase in mucus product ion and c lubb ing of f i laments where parasites were attached. Similarly, heavy infect ion with the two species of Ancyrocephalus caused pathological changes at the site of at tachment . Localized host react ion to the parasites ' hooks inc luded epi thel ia l hyperplas ia and heavy mucus production, and the respiratory ep i the l ium was lost in some instances. Often the side of the f i lament opposite the worm a t tachment was also affected. "In addit ion, the l amel lae were deflected and adhered to each other, and in severe cases, c lubb ing of f i laments was almost always present as was obl i terat ion of normal f i lament structure." The affected f i laments appeared white in fish preparat ions and the gills were congested with mucus. "'Few fish from the non-pol lu ted habi ta t had above-normal mucus, whereas all the fish from the pol lu ted habi ta t had increased mucus product ion and moderate to severe pathological effects" (Skinner, 1982).

MECHANISMS OF REPRODUCTION

Compared with free- l iving relatives, parasi tes usual ly have a much increased reproduct ive potent ia l (see review in Rohde, 1982). This is clearest in endoparasi tes with indirect life cycles. An excess of offspring is necessary to compensa te for the hazards involved in the life cycle, par t icular ly in f inding the hosts. In addi t ion to large numbers of eggs, pa r thenogene t i c and/or asexual reproduct ion increases the n u m b e r of offspring even further, and hermaphrodi t i sm enhances the chances to find mat ing partners in low- densi ty popula t ions (review in Rohde, 1982). Seasonal i ty in egg production of many mar ine parasi tes indicates that temperature, ei ther directly or indirect ly via the host, has

Ecology of mar ine parasi tes 27

an important effect on reproduction, and somet imes eggs are seasonal ly r e l eased from the host. Thus, according to Lester (1980), most d idymozoid t rematodes of the species

Neometad idymozoon hel ic is in the dermis of the buccal cavi ty and the gil l arches of flathead, Plaiycephalus [uscus, in Moreton Bay, Queens land , d i sappear b e t w e e n Sep-

tember and May, l eav ing beh ind depress ions in the mucosa. Apparent ly , the capsule wall breaks down and re leases the worms conta in ing numerous eggs. It is known that

immune responses affect egg product ion in var ious parasites, but no studies of mar ine

parasites have been made in this regard.

M E C H A N I S M S OF INFECTION

Infection of hosts by parasi tes may be by contact transfer, inocula t ion by a vector,

ingest ion of transport (paratenic) or in te rmedia te hosts, by eggs, spores or cysts, or by

free l iving larvae. Examples for each are shown in Table 11. Contact transfer has been shown for small m o n o g e n e a n s of the family Gyrodacty-

lidae, which are common on f reshwater and mar ine fish. Leeches inocula te t rypano-

Table 11. Some examples of infection mechanisms used by marine parasites

Means of infection Group of parasites Source

Contact transfer

Inoculation

Ingestion of transport hosts

Ingestion of intermediate hosts

Ingestion of eggs

Ingestion of cysts

Spores

Free larvae or juveniles

Gyrodactylidae (Monogenea)

Blood Protozoa of fish

Anisakidae (Nematoda)

Pricea, Gotocotyla (Monogenea)

Loba tostoma (Aspidogastrea)

Trypanorhyncha (Cestoda)

Lobatostoma (Aspidogastrea) (by snail)

Many Trematoda (metacercariae)

Myxozoa

Many Monogenea

Many Trematoda (miracidia)

Leeches

Bychowsky (1957)

Khan (1976, 1977a, b, 1978, 1980); Burreson (1979, 1982)

Several authors

Bychowsky & Nagibina (1967); Popova & Gitchenok (1978)

Rohde (1973)

Several authors

Rohde (1973)

Many authors

Several authors

Many authors

Many authors

Llewellyn (1965)

somes, piroplasms and probably h a e m o g r e g a r i n e s into mar ine fishes, and larval

nematodes of various genera b e l o n g i n g to the Anisak idae are accumula ted through a

food chain consist ing of small inver tebrates , la rge inver tebrates , small and large fish, many of them serving as transport hosts in wh ich no d e v e l o p m e n t of the parasi tes occurs.

Final hosts (marine mammals , fish and birds) become infected by ea t ing transport hosts

close to the top of the food chain.

In termediate hosts differ from transport hosts in that parasi tes deve lop in them. In

28 K. Rohde

several cases, infect ion of a final host was shown to occur by inges t ing in termedia te hosts. Thus, the aspidogastr id Lobatostoma manteri develops to (almost) full size in snails, bu t matur i ty is reached only after inges t ion of snai ls harbour ing the parasi te by fish, Trachinotus blochi. Elasmobranchs become infected by ea t ing in termedia te hosts con ta in ing the larvae of t rypanorhynchs. Of par t icular interest is the f inding that among the Monogenea , most of which have a direct life cycle, species of some genera (Pricea, Gotocotyla) apparen t ly use smaller fish as " ' intermediate" hosts. Only juveni les are found on the gills of such fish, and matura t ion occurs only on the gills of large predatory fish. Infection of the latter appears to be by inges t ion of the " in termedia te" hosts. An example of inges t ion of eggs l ead ing to infect ion is the aspidogastr id Lobatostoma ment ioned above. Snails ingest eggs con ta in ing infective larvae which hatch in their digest ive tract. Trematode metacercar iae are examples of cysts l ead ing to infection w h e n swallowed. Spores are the infective stages of Myxozoa, protozoan parasites common in m a n y mar ine fish species.

Finally, free larvae or juven i les of m a n y parasi tes are responsible for infect ing the hosts. The leech Calliobdella carolinensis, for instance, dies after cocoon deposi t ion in May. Juven i les hatch and attach themselves to the fish host the following winter (Sawyer & Hammond, 1973). Miracidia of numerous t rematode species hatch, swim freely and infect snail hosts. Several deta i led studies have b e e n made on infection mechanisms of mar ine Monogenea invo lv ing free oncomiracidia .

In a s imple case, the acanthocotyl id Acanthocotyle lobianchi on the ray Raja montagui, the non-c i l i a ted oncomiracidia hatch w h e n the host settles on the eggs, i nduced by a specific subs tance (urea) in the mucus of the ray (Kearn & MacDonald, 1976) (Table 12). Where f ree -swimming larvae are involved, some " ingenious" infection mechan i sms have evolved. This is necessary since oncomiracidia swim slowly compared with their fish host. Kearn (1967) measured the sw imming speed of larval Entobdella soleae as 5 mm/sec, and M a g n a n (1930) found that the average cruis ing speed (lasting

Table 12. Hatching rhythms and stimuli in some Monogenea

Parasite Host Endogenous Hatching Source hatching stimulus

Entobdella soleae Solea solea Early morning Non-specific

E. hippoglossi Hippoglossus Early night hippoglossus

Acanthocotyle Raja spp. None lobianchi

Dictyocotyle coeliaca Raja naevus None

Didodophora Merlangius Morning merlangi {Scotland) merlangus

D. merlangi {England) Merlangius Late night merlangus

urea

None

Specific urea

None

None

None

Kearn (1973, 1974b, 1975b); Kearn & MacDonald {1976)

Keam (1974a)

Keam & MacDonald {1976}

Kearn ( 1975a}

MacDonald (1975)

MacDonald (1975)

E c o l o g y of m a r i n e p a r a s i t e s 29

s e v e r a l hours) of s o m e m a r i n e f i sh s p e c i e s w a s 3.2 b o d y l e n g t h s / s e c . O v e r s h o r t p e r i o d s ,

f i sh m a y r e a c h m u c h g r e a t e r s p e e d s (e.g. B a i n b r i d g e , 1960). To o v e r c o m e t h i s d i s c r e -

p a n c y , e n d o g e n o u s h a t c h i n g r h y t h m s of s o m e s p e c i e s a r e c o r r e l a t e d w i t h t h e h o s t ' s

b e h a v i o u r a n d e n h a n c e t h e c h a n c e s of i n f e c t i o n ( T a b l e 12). H o s t - s p e c i f i c h a t c h i n g

factors p r o d u c e d b y t h e h o s t i n d u c e h a t c h i n g of s o m e s p e c i e s , a n d s o m e t i m e s b o t h

e n d o g e n o u s r h y t h m s a n d h o s t i n d u c e d h a t c h i n g o c c u r t o g e t h e r .

T h e r e m a y e v e n b e d i f f e r e n c e s in t h e b e h a v i o u r p a t t e r n of d i f f e r e n t p o p u l a t i o n s of

o n e s p e c i e s of M o n o g e n e a , a p p a r e n t l y a n a d a p t a t i o n to d i f f e r e n c e s i n b e h a v i o u r p a t -

t e r n s of d i f f e r e n t h o s t p o p u l a t i o n s . T h u s , a c c o r d i n g to M a c D o n a l d (1975), o n e p o p u l a t i o n

of Diclidophora merlangi h a t c h e d m a i n l y d u r i n g t h e f i rs t 4 - 6 h of t h e i l l u m i n a t i o n

pe r i od , a n o t h e r h a t c h e d m a i n l y d u r i n g t h e 2 h p e r i o d b e f o r e l igh t . T h e h o s t is t h e

w h i t i n g , Merlangius merlangus, w h i c h u n d e r g o e s v e r t i c a l m i g r a t i o n s u n d e r e x p e r i m e n -

t a l c o n d i t i o n s i n r e l a t i o n to l igh t . It is p o s s i b l e t h a t d i f f e r e n t s t o c k s of f i sh s h o w d i f f e r e n t

b e h a v i o u r p a t t e r n s a n d t h u s e x p o s e t h e m s e l v e s to i n f e c t i o n a t d i f f e r e n t t i m e s of t h e

l i g h t - d a r k cycle . H o w e v e r , s u c h d i f f e r e n c e s b e t w e e n h o s t p o p u l a t i o n s h a v e n o t y e t b e e n

d e m o n s t r a t e d , b u t d i f f e r e n c e s i n p a r a s i t e b e h a v i o u r m a y g i v e a c l u e c o n c e r n i n g t h e

h o s t ' s b e h a v i o u r a n d i n i t i a t e i t s s tudy .

Acknowledgment. I wish to thank B. Heath, U.N.E., for useful comments.

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