HELGOL~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 37, 35-52 (1984)

Zoogeography of marine parasites

K. R o h d e

Department of Zoology, University of N e w England; Armidale, N.S. W., 2351, Australia

ABSTRACT: Latitudinal gradients in species numbers of marine parasites, differences be tween the Atlantic and Indo-Pacific Oceans, latitudinal gradients in frequency and intensity of infection, in host range and specificity, and in fluctuations of infection are discussed, as well as differences between shallow and deep water, parasite endemicity at remote oceanic islands, and importance of temperature for parasite distribution. Examples are given to demonstrate the usefulness of marine parasites as biological tags and as indicators of the geographical origin of hosts.

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

T h e s tudy of t he g e o g r a p h i c a l d i s t r i bu t i on of m a r i n e p a r a s i t e s is in its in fancy .

C o m p r e h e n s i v e t r ea t i ses on m a r i n e z o o g e o g r a p h y i g n o r e p a r a s i t e s c o m p l e t e l y (Ort- mann , 1896; E k m a n , 1935, 1953; Br iggs , 1974), c o m p a r a b l e to t he n e g l e c t of p a r a s i t e s in

ea r ly books on g e n e r a l z o o g e o g r a p h y (e.g. S c h m a r d a , 1853; Hesse , 1924; H e s s e et al.,

2000

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Fig. 1. Numbers of marine fish species at different latitudes. Small dots, interrupted line: Atlantic. Large dots, uninterrupted line: Indo-Pacific. Ordinate: number of fish species. Abscissa: latitude.

(Redrawn after Rohde, 1982)

© Biologische Anstalt Helgoland, Hamburg

36 K. R o h d e

Table 1. Lati tudinal gradients in numbers of m o n o g e n e a n and t rematode genera of commercial mar ine fishes. (Data from Lebedev, 1969)*

Biogeographical zone N u m b e r of species of Number of genera commercia l fish Monogenea Digenea

Arctic approx. 20 15 12 North-boreal 40-- 50 20 50 South-boreal > 50 50 160 Tropical 100-120 95 300 North-ant iboreal 40 - 50 40 80 South-ant iboreal plus Antarct ic approx. 20 3 10

* Parasi tes of tropical fish are much less well known than those of fish from h igher lat i tudes and since 1969, w h e n this tab le was composed, many new genera of Digenea and Monogenea have been descr ibed from tropical oceans

1937, 1951; D a r l i n g t o n , 1957). P o l y a n s k y (1961, R u s s i a n e d i t i o n , 1958) g a v e a b r i e f

d i s c u s s i o n of t h e z o o g e o g r a p h y of p a r a s i t e s of m a r i n e f i s h e s in t h e USSR, a n d D e l y a m u r e

(1968) i n c l u d e d a d e t a i l e d a c c o u n t of z o o g e o g r a p h y i n h i s m o n o g r a p h o n h e l m i n t h s of m a r i n e m a m m a l s . A n u m b e r of m a i n l y R u s s i a n a n d A m e r i c a n p a r a s i t o l o g i s t s h a v e

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

b r i e f r e v i e w o n m a j o r a s p e c t s of m a r i n e p a r a s i t e z o o g e o g r a p h y b e e n p u b l i s h e d (Rohde ,

1982). T h e f o l l o w i n g a c c o u n t a t t e m p t s to g i v e a c o n c i s e b u t u p - t o - d a t e r e v i e w of t h e g e o g r a p h i c a l d i s t r i b u t i o n s h o w n b y m a r i n e p a r a s i t e s . A l so d i s c u s s e d a r e e x a m p l e s to

s h o w t h e u s e of m a r i n e p a r a s i t e s as b i o l o g i c a l t ags .

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Fig. 2. Relative species diversi ty (average n u m b e r of species of gill Monogenea per host species) of teleosts in the Atlantic. Open circle: total n u m b e r of m o n o g e n e a n species/total number of host species examined at each locality. Closed circle: = above, but species occurring in x host species counted x times. Ordinate: mean numbers of m o n o g e n e a n species per host species. Abscissa:

means of annua l sea surface tempera ture ranges in °C (Redrawn after Rohde, 1980b)

Zoogeography of mar ine parasi tes

RESULTS AND DISCUSSION

37

L a t i t u d i n a l g r a d i e n t s i n s p e c i e s d i v e r s i t y

Most groups of animals, whether terrestrial, freshwater or marine, show an increase of species numbers from high to low lati tudes. Mar ine teleosts i l lustrate this phenome- non well (Fig. 1). Among mar ine parasites, l a t i tud ina l gradients in diversi ty with an increase in diversity towards the Equator, greater than that of their hosts, have b e e n shown for genera of Monogenea and Digenea (Table 1) and for species of Monoge ne a (Fig. 2). Al though there are more species of Digenea in warm than in cold waters associated with the much greater n u m b e r of host species, a r e 1 a t i v e 1 y greater number of d i g e n e a n than of host species has not yet b e e n demonstrated.

Maximum species number s of Monogenea per host species also increase towards the Equator, whereas those of Digenea fluctuate great ly but are s imilar at all la t i tudes (Fig. 3).

Reversed diversity gradients are shown by he lmin th parasi tes of p i nn i pe ds and cetaceans which have the greatest species n u m b e r s in the boreal region (Table 2).

Table 2. Helminth species of pinnipeds and cetaceans at different latitudes. (Data from Dogiel, 1964)

Biogeographical Trematodes Cestodes Nematodes Acantho- Total zone cephalans

Arctic 6 7 9 3 25 Boreal 30 24 31 9 94 Tropical 7 2 18 4 31 Antiboreal 0 9 21 8 38 Antarctic 1 7 5 1 14

Delyamure (cited by Dogiel, 1964) assumed that this is due to the reduced popula t ion density of hosts in warm waters, bu t an a l te rnat ive exp lana t ion is that hosts a nd parasi tes have or iginated in cold waters and had more t ime to acquire parasi tes in that envi ron- ment (Rohde, 1982). A greater species r ichness in cold waters has also b e e n demon- strated for piscivorous leeches. According to Epshte in (1970), there are 45 species of Hirudinea be long ing to 24 genera in the arctoboreal region, and only 13 species be longing to 5 genera in the tropical Atlantic. Probably associated with the greater number of species of leeches, which are vectors of blood protozoans, the highest prevalence of haematozoa of mar ine fishes from the Northwest Atlant ic Ocean is found in the cold Labrador area (various authors, see Khan & Newman , 1982). "The overall trend indicates increas ing number s of infected species and higher p reva lence of hemato- zoan infections with increas ing dis tance north of the Equator."

The much greater n u m b e r of studies in nor thern cold- temperate waters expla ins the impressive number s of except ions to the rule of diversi ty increase in warm regions. However, all groups which do not conform to the rule are small r epresen t ing only a minute proportion of mar ine parasites, and the overall t rend appears to be one of increasing diversity towards the Equator and somet imes even of a r e 1 a t i v e 1 y greater increase compared with host groups.

3 8 K. R o h d e

Fig. 3A. M a x i m u m n u m b e r of h e l m i n t h s p e c i e s ( m e a n of 3 f i sh s p e c i e s wi th l a rges t spec i e s n u m b e r s ) at d i f fe ren t l a t i tudes . × T r e m a t o d a in s u r f ace wa te r s , ~ - T r e m a t o d a in d e e p water , O M o n o g e n e a in su r f ace wa te r , • M o n o g e n e a in d e e p water . A d u l t T r e m a t o d a in Atlant ic . F rom r ight to left: (1) G a b o n to M a u r e t a n i a , W e s t Afr ica acc. to F i s ch tha l (1972) (Pomadasys jubelini, Trachinotus glaucus, Galcoides decadactylus); (2) Bel ize acc. to F i sch tha l (1977) (Haemulon flavolineatum, Lutjanus sFnagris, Calamus bajonado); (3) T o r t u g a s F lor ida acc. to M a n t e r (1947) (Haemulon plumieri, H. sciurus, Calamus calamus); (4) T o r t u g a s Florida, d e e p wa t e r acc. to M a n t e r (1934) (Urophycis regius, Merluccius sp., Brotula barbara); (5) Bimini , Bri t ish Wes t Ind ies acc. to S o g a n d a r e s - B e r n a l (1959) (Haemulon sciurus, Holocentrus ascensionis, Haemulon album); (6) Off N e w York Bight , d e e p w a t e r acc. to C a m p b e l l et al. (1980) (Coryphaenoides armatus, Antimora rostrata, Coryphaenoides carapinus); (7) Black Sea acc. to O s m a n o v (1940) (Trachurus trachurus, Onos tricirrata, Crenilabnls pavo); (8) Br i ta in acc, to D a w e s (1947) (Gadus merlangus, Conger conger, Pleuronectesplatessa); (9) C a n a d a W e s t C o a s t acc. to M a r g o l i s & A r t h u r (1979) (Hippoglos- sus hippoglossus, Hippoglossoides platessoides, H. elassodon); (10) G r e e n l a n d acc. to B r i n k m a n n (1975) (Anarhichas minor, A. lupus, A. tatifrons); (11) W h i t e Sea acc. to S h u l m a n & S h u l m a n - A l b o v a (1953) (Anarhichas lupus, Myoxocephalus scorpius, Pleuronectis flesus); (12) Ba ren t s Sea acc. to P o l y a n s k y (1966) (Anarhichas lupus, A. minor, Myoxocephalus scorpius). M o n o g e n e a in Atlant ic . F rom r igh t to left: (1) Brazi l Sao Pau lo S ta te acc. to R ohde (unpubl . ) (Oligoplites saliens, Caranx latus, Scomber japonicus, all g i l l s only); (2) Gul f of M e x i c o acc. to H a r g i s (1954, 1957) (Brevoortia patronus, Scomberomorus maculatus, Mugil cephalus); (3) T o r t u g a s Florida, d e e p w a t e r acc. to M a n t e r (1934) (Helicolenus dactylopterus, Epinephelus niveatus, Pontius longispinus); (4) Mar del Plata, A r g e n t i n a acc. to R o h d e (unpubl . ) (Micropogon [urnieri, S. japonicus, Pn'onotuspunctatus, all g i l l s only); (5) Off N e w York Bight , d e e p w a t e r acc. to C a m p b e l l e t al. (1980) (Antimora rostrata, Atepocephalus agassizi, Coryphaenoides rupestris); (6) Black Sea acc. to O s m a n o v (1940) (Sciaena umbra, Caspialosa pontica, Belone acus)~ (7) Br i ta in acc. to D a w e s (1947) (Trigla lucerna, Merluc- cius merluccius, Gadus merlangus); (8) C a n a d i a n w e s t coas t acc. to M a r g o l i s & Ar thu r (1979) (Hippoglossus hippoglossus, Xiphias gladius, Gadus morhua); (9) N o r w a y acc. to B r i n k m a n n (1952) (G. merlangus, Xyphias gladius, Molva molva); (10) G r e e n l a n d acc. to B r i n k m a n n (1975) (Hippog- lossus hippoglossus, Reinhardtius hippoglossoides); (11) W h i t e Sea acc. to S h u l m a n & S h u l m a n - A l b o v a (1953) (Boreogadus saida, Pleuronectes flesus, Liopsetta glacialis); (12) Ba ren t s Sea acc. to

P o l y a n s k y (1966) (MaHotus villosus, Pollachius virens, Gadus morhua)

Fig. 3B. T r e m a t o d a in Indo-Paci f ic . F r o m r igh t to left: (1) Gu l f of P a n a m a acc. to S o g a n d a r e s - B e r n a l (1959) (Epinephelus analogus, Kyphosus elegans, Seriola mazatiana); (2) G a l a p a g o s a n d coas t E c u a d o r to M e x i c o acc. to M a n t e r (1940) (CheiHchthys annulatus, Paranthias furcifer, Trachinotus rhodopus); (3) H a w a i i acc. to Y a m a g u t i (1970) (Neothunnus macropterus, Parathunnus sibi, Euthyn- nus yaito); (4} N e w Z e a l a n d acc. to M a n t e r (1954b) (Leptocephalus conger, Notothenia mac- rocephala, Helicolenus percoides]; (5) N e w Z e a l a n d acc. to Hewi t t & H i n e (1972) (Conger ver- reauxi, Cyttus australis, Chelidonichthys kumuJ; (6) Sea of J a p a n acc. to Z h u k o v (1960a) (Myoxo- cephalus brandti, Hemitripterus villosus, Sebastodes trivittatus); (7) S u b - A n t a r c t i c to An ta rc t i c acc. to P r u d h o e & Bray (1973) (Champsocephalus gunnari, Notothenia cyanobrancha, Trematomus newnesi); (8) C a n a d i a n e a s t coas t acc. to M a r g o l i s & A r t h u r (1979) (Sebastes alutus, S. pinniger, Syngnathus griseolineatus); (9) E a s t e r n K a m c h a t k a acc. to S t re lkov (1960) (Lepidopsetta bilineata, Limanda aspera, Myoxocephalusjaok). M o n o g e n e a in Indo-Pacif ic . F rom r i gh t to left: (1) Q u e e n s - l a n d a n d P a p u a N e w G u i n e a acc. to R o h d e (unpubl . ) (Epinephelus tauvina, Lethrinus chrysostomus, L. nebulosus, all g i l l s only); (2) N e w S o u t h W a l e s acc. to Rouba l (1981) a n d p e r s o n a l c o m m u n i c a - t ion, R o u b a l e t al. (1983), Rohde , (unpub l . ) (Acanthopagrus australis; Chrysophrys auratus, Euthyn- nus alletteratus]; (3) N e w South W a l e s d e e p w a t e r acc. to R o h d e (unpub l . ) (Hygophum hygomL Myctophum phengodes, Synagrops japonicus); (4) Sou th A u s t r a l i a acc. to R o h d e (unpubl , ) (Acan- thopagrus butcheri, Platycephalus richardsoni a n d Aldrichetta forsteri ); (5) N e w Z e a l a n d acc. to H e w i t t & H i n e (1972) (Trachurus novaezelandiae, Thyrsites atun, Seriolella brama acc. to Rohde et al. 1980); (6) C a n a d i a n e a s t coas t acc. to M a r g o l i s & A r t h u r (1979) (Sebastes alutus, S. caurinus, S. zacentrus); (7) C h u k o t s k P e n i n s u l a acc. to Z h u k o v (1960b) (Eleginus gracilis, Pleuronectes stellatus,

Clupea harengus)

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40 K. Rohde

D i f f e r e n c e s b e t w e e n t h e A t l a n t i c a n d I n d o - P a c i f i c

Most groups of f ree- l iving an imals have greater species r ichness in the Indo-Pacific than in the Atlant ic Ocean (see Fig. 1 for mar ine teleosts). Data for some major parasite groups indicate the same. For example, Parukh in {1975} examined 6500 fish of 200 species b e l o n g i n g to 100 families from various regions and concluded that species number s of nematodes are smal ler in the southern Atlant ic than in the Indo-Pacific. The same was shown for Monogenea by Rohde (1980b }. The b lack bream, Acanthopagrus australls, on the Aus t ra l ian east coast, has n ine species of M o n o g e n e a (Roubal, 1981; and pers. comm.}, and the snapper, Chrysophrys auratus, from the same locality has six (Roubal et al., 1983}. Such large species number s are not k n o w n from Atlantic fish.

The two ocean systems also differ in the species composi t ion of their parasi te faunas as indica ted by numerous endemic species. A consequence of greater diversity, endemic i ty of t rematode and m o n o g e n e a n gene ra is greater in the Indo-Pacific than the Atlant ic (Lebedev, 1969; Tables 3 and 4} and endemic i ty of species is much greater than

Table 3. Endemicity of genera of Digenea in the Atlantic and Indopacific Oceans. (Data from Lebedev, 1969)

No. in Atlantic No. in Indopacific

In 1 region 78 (36 %) 182 (57 %) In 2 regions 136 (64 %) 136 (43 %) Total 214 318

Table 4. Endemicity of genera of Monogenea in the Atlantic and Indo-Pacific Oceans. (Data from Lebedev, 1969)

No. in Atlantic No. in Indopacific

In 1 region 40 (42 %) 114 (67 %) In 2 regions 56 (58 %) 56 (33 %) Total 96 170

that of genera (see review in Rohde, 1982). Thus, according to Manter (1940, 1947, 1955), of 147 shallow water t rematodes at Tortugas, Florida, only 26 species (17.6 %) occurred also in the Pacific, and of the 62 species on the Atlant ic side of Cent ra l America, and the 31 species in the Gulf of Panama, only 5 species occurred in both regions (Sogandares- Bernal, 1959). Nevertheless, according to Sogandares-Bernal , unt i l 1959 the impressive n u m b e r of 41 t rematode species had b e e n found both in the Amer ican Atlant ic and Pacific.

The n u m b e r of he lmin th species common to the cold nor thern Atlantic and Pacific is surpr is ingly high. According to Strelkov (1960), eas tern Kamchatka has 51 know n species of trematodes, cestodes, nematodes and acanthocephalans , and the Barents Sea has 70. Thirty-four species occur in both regions. Of the 57 species recorded from the

Zoogeography of mar ine parasi tes 41

j~.~> ~ 7 0 ~ ~ AMCHATKA

~HITE . . . . . . .

Fig. 4. Number of helminth species in the White and Barents Seas and the northwestern Pacific. Numbers in circles indicate species shared by two regions. (Data from Stetkov, 1960)

White Sea, 26 species are also known from eas tern Kamchatka. The proport ion of helminths shared is s imilar to the propor t ion shared by ad jacen t Pacific seas. Thus, of the

51 species from eastern Kamchatka, 35 are also known from the nor thwes te rn Sea of Japan and 26 also from the South Kuril Islands (Fig. 4) (see also Zhukov, 1960a).

Exchange of species may have occurred dur ing the warm Interglacials . It is of par t icular interest that a compara t ive ly much smal ler number of fish species is

shared by the northern Atlantic and Pacific, and endemic i ty of fish in the nor thern Pacific

is much grea ter than that of their parasi tes (Table 5). Thus, there are no less than 21

Table 5. Distribution of shelf fishes in the Arctic and northern temperate regions. (Data from Ekman, 1953)

Regions Species Genera

In North Pacific including adjacent Polar Sea 550 (76 %) 230 (69 %) In North Atlantic including adjacent Polar 150 {2t %) 51 (15 %) Sea In both regions 25 (3 %) 54 (16 %}

Total 725 335

families of endemic fish in the north Pacific, whe re a s the north Atlant ic has not a s ingle

one (review by Ekman, 1953). One reason for the di f ferences b e t w e e n hosts and parasi tes may be the re la t ively s lower evolu t ion of parasi tes which has not pe rmi t t ed the differen-

tiation in the two regions of as many taxa of parasi tes as of hosts. Another reason may be the possible transfer over wide dis tances of many parasi tes wh ich use in t e rmed ia t e hosts

42 K. Rohde

or have encysted stages and are not strictly host specific. The latter explana t ion can be exc luded for the strictly host-specific and directly deve lop ing Monogenea . According to Zhukov (1960h), of the 22 species of mar ine Gyrodactyl idae know n from the nor thern Pacific and 21 species known from the nor thern Atlantic, 14 species are shared by both regions. The taxonomic review by Ma lmberg (1970) shows that several of Zhukov 's species must be separated into more than one species. Hence, endemic i ty is probably sl ightly greater than assumed by Zhukov. However, Gyrodactyl idae are notoriously difficult and Pacific forms are insuff icient ly known. Nevertheless, the data ava i lab le so far indicate that endemic i ty of m o n o g e n e a n species in the nor thern seas is not signifi- cant ly greater than that of endoparas i tes with indirect development . However, more studies are needed .

L a t i t u d i n a l g r a d i e n t s i n p r e v a l e n c e a n d i n t e n s i t y of i n f e c t i o n , hos t r a n g e a n d spec i f i c i ty , a n d f l u c t u a t i o n s of i n f e c t i o n s

Few studies on the la t i tudinal gradients of infect ion preva lence and in tens i ty have b e e n made. Rohde (1977) examined them for gil l monogeneans . He found a great var iabi l i ty of infect ion in tensi t ies at all lati tudes, but no definite changes with latitude. Prevalence of infection, on the other hand, appears to be greater in warm seas (Fig. 5).

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This is apparen t ly not a result of reduced or absent seasonali ty, as deep water mono- g e n e a n s also have a low preva lence of infect ion (Rohde, unpubl . ; Fig. 5).

Host ranges of Monogenea are very small and s imilar at all la t i tudes (Fig. 6). Trematodes have more restricted host ranges in warm than in cold waters (Manter 1947, 1955; Rohde 1978c). Host specificity indices based on p reva lence (frequency} of infection also show a la t i tudina l gradient for t rematodes (Fig. 7). However, if specificity indices

Fig. 5. Frequencies (prevalence) of infection with gill Monogenea of marine teleosts at different latitudes in the Pacific. Fish species without gill Monogenea not included. • and regression line: surface fish. × deepwater fish off the N.S.W. coast (%). Ordinate: prevalence of infection (%).

Abscissa: means of annual sea surface temperature ranges (°C)

Z o o g e o g r a p h y of m a r i n e p a r a s i t e s 43

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survey by Zhukov (1976)

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Fig. 7. Host specificitiy indices of mar ine Monogenea (circles) and Trematoda (crosses) at different latitudes. Ordinate: Host specificity indices based on densi ty or f requency of infection. Abscissa:

means of annua l sea surface tempera ture ranges in °C (Redrawn after Rohde, 1980c}

b a s e d o n d e n s i t y ( i n t ens i t y ) of i n f e c t i o n a r e u s e d , a l a t i t u d i n a l g r a d i e n t is n o t a p p a r e n t .

T h e r e a s o n is t h a t a l t h o u g h t r e m a t o d e s i n f e c t m o r e h o s t s p e c i e s a n d m a n y of t h e m

f r e q u e n t l y i n c o l d seas , o n l y o n e o r a f e w a r e u s u a l l y h e a v i l y i n f e c t e d . S u f f i c i e n t da t a ,

h o w e v e r , a r e a v a i l a b l e o n l y for t h e W h i t e S e a a n d m o r e s t u d i e s a r e n e e d e d to s u p p o r t

th i s c o n c l u s i o n . O t h e r p a r a s i t e g r o u p s h a v e n o t b e e n a n a l y z e d i n t h i s r e s p e c t .

44 K. Rohde

With regard to f luctuat ions of parasi t ic infections, numerous studies in cold-temper- ate seas have shown that such f luctuat ions are common but not universal (see review in Rohde, 1982). Very few studies in tropical and subtropical waters have been made and conclusions concern ing the exis tence of la t i tudina l gradients cannot at present be

drawn.

D i f f e r e n c e s b e t w e e n s h a l l o w a n d d e e p w a t e r

Rohde (1982) reviewed the ev idence for vertical gradients in parasites of mar ine fish based on the surveys of several authors. He summarized, part ly following Noble (1973), that midwate r fishes examined have far fewer species and numbe r s of parasites than inshore and open ocean surface fishes. There are very few adult helminths. In order of a b u n d a n c e the parasi tes are: larval nematodes, myxozoans, larval cestodes, copepods and larval t rematodes of the family Hemiur idae . The parasi te fauna becomes poorer with depth unt i l the ben thope lag ic zone is reached. Bottom dwel l ing fishes have more species and greater number s of parasi tes than midwater species, because their food probably inc ludes more infected in te rmedia te hosts, and also because they are larger and have a longer life span. However, more s tudies are needed to clarify whether these general iza- t ions hold for all lati tudes. The difference in diversi ty of parasit ic species be tween surface and deep water pelagic fish apparen t ly exists only in regions where the surface waters are warm. It would be of special interest to compare deep sea parasite faunas in tropical and cold- temperate zones on the basis of surveys as large as that by Campbel l et

al. (1980). The f indings of Campbe l l et al. (1980) and my own unpub l i shed data of a survey of

deepwater fish off the New South Wales coast in eastern Austral ia (approximately 900 fish of 30 species) appear i ndeed to indicate that at least some of the genera l trends observed in cold water fish are also found in deep water fish. Thus, max imum species number s per fish species of t rematodes and m o n o g e n e a n s are similar, and prevalence of infect ion with m o n o g e n e a n s is low and roughly s imilar in both groups (Fig. 5). However, my survey is not yet completed and so far ma in ly small pe lagic fish have been examined. Inclusions of larger benth ic fish may well make the data even more similar to those for cold water surface fish. B. Heath is work ing on the endoparas i tes of these fish.

P a r a s i t e e n d e m i c i t y a t r e m o t e o c e a n i c i s l a n d s

Remote oceanic islands, i.e. i s lands 300 miles or more from the neares t continent , were shown to have a low endemic i ty of their fauna in the north and middle Atlantic, a greater endemic i ty in the southern Atlant ic and Pacific, and a very h igh endemic i ty in sub-Antarct ica (Briggs, 1966). Briggs expla ined this by a longer und i s tu rbed evolutio- nary history of the is lands with high endemici ty . Pleis tocene tempera ture reductions apparen t ly were most marked in the nor thern and middle Atlantic, where they wiped out much of the or iginal fauna. Manter (1967) found that endemic i ty of trematodes corres- ponds to that of other animals , and the scanty data for Monogenea appear to follow the same t rend (Rohde, 1982) (Table 6).

Zoogeography of mar ine parasi tes

Table 6. Endemicity of marine fishes and their parasites at oceanic islands according to Rohde (1982)

45

Areas Fishes Endemicity of Trematodes Monogenea

North Atlantic

Azores Madeira Bermuda Cape Verde

South Atlantic St. Helena 27-50 % Tristan da Cunha 23 %

Pacific Galapagos Islands 15-27 % Hawaii 34 % Easter Island 29 % Lord Howe Island 22 % Fiji ? New Caledonia ?

0% ? ? 3% ? ? 5% 2% (1 of 43 species) ? 4% ? ?

? ? ? ?

61% (of 80 species) (6 of 11 species) 74 % (of 92 species) 88 % (128 of 146 species)

? ? ? ?

56 % (of 35 species) ? 45 % (of 33 species) ?

I m p o r t a n c e of t e m p e r a t u r e for p a r a s i t e d i s t r i b u t i o n

Tempera tu re appears to be the major s ingle factor respons ib le for the geograph ica l distribution of mar ine organisms. It affects faunas by increas ing diversi ty in warm seas and by br ing ing about differences in the species composi t ion of faunas. Rohde (1978b)

has shown that t empera tu re is i ndeed the dec is ive factor responsib le for species num-

bers, since habitats which are ident ica l in all o ther character is t ics but tempera ture , support different numbers of parasi te species at different lat i tudes. Such habitats are the gills and the body surface of mar ine fishes. Rohde (1978a, b) exp la ined inc reased

diversi ty in warm env i ronments by an acce le ra ted speed of evolu t ion at h igh t empera - tures, probably due to shorter genera t ion times, faster se lec t ion and possibly faster

mutat ion rates. Rohde (1982) r e v i e w e d the e v i d e n c e for t empera tu re be ing the major factor that

de te rmines species composit ion. Severa l surveys have shown that he lmin th species from

cold seas are also found, but very rarely, in w a r m e r waters, and v ice versa. Thus, Zhukov (1960a) found 87 species of endoparas i t ic he lmin ths in the cold nor thwes te rn Sea of

Japan. Many of these have also b e e n recorded from other cold waters in the At lant ic and

Indo-Pacific, but only two from the warmer southwes tern part and two from the south-

eastern part of North America . The cosmopol i tan t rematode species Derogenes varicus is known from a large

number of fish species in cold and t empera tu re surface waters, but at low lat i tudes it

occurs only in deeper cold water or in regions wi th cold currents (e.g. the Ga lapagos Islands, Manter, 1955). Finally, species from cold d e e p w a t e r at low lat i tudes f requent ly

show distinct affinities wi th surface species from h igher lat i tudes, but not wi th surface

species from the same locality. Thus, according to Mante r (1955), only 5 of 49 t rematode

46 K. Rohde

species from deep water at Tortugas, Florida, were also found in nearby surface water, whereas the most common genera occur also in the nor thern Pacific and Atlantic, in deeper waters at low latitudes, and in the T a s m a n i a n and New Zea land regions.

Effects of hos t m i g r a t i o n o n p a r a s i t e s ( p a r a s i t e s as b i o l o g i c a l tags)

Parasites have repea tedly b e e n used to study fish migrations. Prerequisi tes for the usefulness of parasites for this purpose are that they have a long life span and that infect ion is restricted to cer ta in areas (Margolis, 1965). Parasites which are lost dur ing migra t ion cannot be used. Margolis (1963, 1965) demonst ra ted that two species of endoparas i t ic he lmin ths are excel lent indicators of the geographica l origin of sockeye salmon, Oncorhynchus nerka. The plerocercoid larva of Triaenophorus crassus is restricted to some lakes of wes tern Alaska, and extens ive sampl ing over a period of five years conf i rmed that the parasi te occurs only in downst ream migran t sockeye from these lakes and in adults re tu rn ing to them. The nematode Dacnitis truttae, on the other hand, is found only in some sockeye sa lmon from rivers of the east and west coasts of Kamchatka. Extensive sampl ing failed to f ind it in fish from North America. Both parasi tes have a long life span, as indica ted by the presence of the first species in r e tu rn ing adul t salmon, and by the occurrence of the second species in fish which have spent as much as four years at sea. Sampl ing at sea showed that matur ing and immature sa lmon from wes te rn Alaska are extensively d is t r ibuted to the east and west of their area of origin, with m a x i m u m migra t ions of 1100 to 1200 miles. Matur ing Kamchatkan sa lmon migrate 500 to 700 miles eastward from their area of origin, and immature fish up to 1100 to 1200 miles (Fig. 8). In addition, certain oceanic areas are domina ted by ma tu r ing fish of cer ta in stocks with different p reva lence of Triaenophorus infection as characterist ic for certain streams. Comparisons of inc idence of infect ion in schools from different river systems in wes tern Alaska with that of r e tu rn ing sa lmon showed that there is no or hardly any straying, "even be tween streams whose mouths are only a few miles apart" (Margolis, 1965).

P a r a s i t e s as i n d i c a t o r s of t he g e o g r a p h i c a l o r i g i n of hos t s

Von Iher ing (1891, 1902) was the first to use parasi tes and ec tocommensals to clarify re la t ionships of hosts, as well as places of origin, dispersal of hosts, and anc ien t land connect ions b e t w e e n land masses. The method is therefore cal led the von Ihering method. An impor tant assumpt ion for this method is that an imals have a greater diversity in areas where they have b e e n for a long t ime than in those into which they have recently immigrated. Few mar ine parasi tes have been used in this respect.

M a m a e v et al. (1959) and Margolis (1965) poin ted out that Pacific salmonids have m a n y freshwater parasites specific to them, some with complex life cycles, but no marine endoparasi tes . Only two ectoparasites specific to sa lmonids are marine, a m o n o g e n e a n and a copepod. The authors concluded that sa lmonids must be of freshwater origin, an assumpt ion also supported by other evidence, a l though unt i l recent ly some ichthyolog- ists be l i eved in a mar ine origin of the group (see "Discussion" and "References" in Margolis, 1965).

Another example is the controversy about the geographic origin of the southern

Zoogeography of mar ine parasi tes 47

• Triaenophorus

o Dacnitis

J _.) =~

0

'. , "- o ~,o e, . e •

%00 1 • ,e %

eb

\

~IIIIIIIIIII o o .

• o

~ _ ~ . . ~ o o o ~ " 0 O 0 O ! " " • '.. •

~ - ~ . • • 0

• Triaenophorus o Docnifis o Trioenophorus ond Dacnifis

i ill

\

Fig. 8. Distribution of sockeye salmon infected with Triaenophorus and Dacnitis. Top: maturing fish. Bottom: immature fish (Redrawn after Margolis, 1965)

hake, Merluccius hubbs i (Gadiformes) dis t r ibuted a long the Argen t in i an coast (Fig. 9). It shows the impor tance of accurate and extensive taxonomic studies to avoid wrong conclusions. M. hubbsi had b e e n thought to have evolved from M. merluccius or M. bilinearis in the north Atlantic, but according to Szidat (1961), its parasi tes are s imilar to those of the north Pacific hake M. productus and un l ike those in the Atlantic. The same parasite fauna was found in three other gadiforms from the Argen t in i an coast, i.e. Macruronus magellanicus, Micromesist ius australis and Salilota australis, whereas a fourth, Urophycis brasiliensis, had a typical ly Atlant ic parasi te fauna. Szidat conc luded that the last species immigra ted from the nor thern Atlantic, p r e sumab ly through deep water along the Amer ican east coast, whereas the other four came from the southern Pacific. Kabata (1970) found a parasi t ic copepod on the Pacific coast of C a n a d a which he considered to be conspecific with Szidat 's Neobrachiel la lageniformis k n o w n only from the Argen t in ian coast. This f ind ing apparen t ly supported Szidat 's conclus ion about the origin of M. h ubbsi. However, Ho (1974) observed the same copepod on Atlant ic hake on the coast of Florida, and according to the most recent review of Kabata & Ho (1981), there are three forms of Neobrachiella insidiosa (Heller, 1865), i.e. IV. insidiosa f. insidiosa Kabata, 1979 on Merluccius merluccius; IV. insidiosa f. lageniforrnis Kabata, 1979 on Merluccius hubbs i off Argent ina, o n / ~ . bilinearis off Florida and on Air. australisin New

48 K. R o h d e

,.% MG ~' ~ ~,

z7 Fig. 9. Present dis tr ibut ion of the genus Merluccius (Redrawn after Kabata & Ho, 1981). MA =

lvI. australis; MB = M. bitinearis; MG = M. ga~; MH = M. hubb$i; M M = M. merluccius; MP = M. productus

Z e a l a n d ; a n d IV. insidiosa f. pacif ica K a b a t a , 1979 o n Merluccius productus a n d M. gayi off t h e C a n a d i a n Pac i f i c coas t , C a l i f o r n i a , P e r u a n d C h i l e . T h u s , t h e s p e c i e s o r i g i n a l l y

d e s c r i b e d as Neobrachiel la lageni formis is a f o r m of Neobrachiel la insidiosa r e s t r i c t e d

to A t l a n t i c h a k e . C o n f u s i o n h a d a r i s e n b e c a u s e i t c l o s e l y r e s e m b l e s t h e e a s t e r n Pac i f i c

f o r m i n h a v i n g l a r g e g e n i t a l p r o c e s s e s . T h e Pac i f i c fo rm, h o w e v e r , p o s s e s s e s a p a i r of

p o s t e r i o r p r o c e s s e s w h i c h a r e a b s e n t in y o u n g e r a d u l t f e m a l e s . A b s e n c e of t h e s e

p r o c e s s e s in y o u n g a d u l t s l e d to t h e i r i d e n t i f i c a t i o n as Neobrachiel la lageniformis a n d

t h e f a l s e c o n c l u s i o n s c o n c e r n i n g t h e Pac i f i c o r i g i n of Merluccius hubbsi (Fig. 10).

A C B

Fig. 10. Neobrachiella insidiosa. (A) f. insidiosa (B) f. lageniformis, (C) f. pacifica (Redrawn after Kabata & Ho, 1981)

Zoogeography of mar ine parasi tes 49

Kabata & Ho (1981) re-assessed the ev idence from all copepod parasi tes of M e r l u c -

cius for the origin of the group. "Acutely aware of the pitfalls with which the use of such tags is beset, they bel ieved, nonetheless , that such tags can be used, at least as corroborative evidence, to solve many problems of fish biology, i nc lud ing some pre- sented by the invest igat ions of a phylogene t ic and zoogeographical na ture ." They concluded that the genus M e r l u c c i u s arose in the nor thern Atlant ic and spread south- ward and into the Pacific through the gap b e t w e e n North and South America, and that hi. h u b b s i off Argen t ina immigra ted a long the east coast of South America (Fig. 11}.

&.,"

Fig. 11. Dispersal of the genus Merluccius according to Kabata & Ho (1981). Interrupted lines indicate dispersal of M. hubbsi (Argentina) and M. australis (New Zealand) according to Inada

(1981)

Reimer (1981), examin ing the t rematodes of M e r l u c c i u s , also conc luded that Szidat 's hypothesis is not supported by facts. In summary, pa leonto logica l and other ichthyologi- cal evidence as well as parasi te data now firmly confirm the v iew that hake or ig inated in the northern Atlant ic (references in Kabata & Ho, 1981). However, there is still some doubt on how M. h u b b s i reached the South Amer ican Atlant ic coast. Whereas Kabata & Ho (1981) assume a southward migra t ion a long the South Amer ican east coast, the ichthyologist Inada (1981) suggests migra t ion a long the South Amer ican west coast after crossing the Central Amer ican gap (Fig. 11).

5 0 K. R o h d e

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