Latitudinal differences in host-specificity of marine Monogenea and digenea

Marine Biology 47, 125-134 (1978) MARINE BIOLOGY �9 by Springer-Verlag 1978

Latitudinal Differences in Host-Specificity of Marine Monogenea and Digenea

K. Rohde

Department of Zoology, The University of New England; Armidale, New South Wales, Australia

Abstract

Data from 15 surveys of marine trematodes (average of 91 trematode species and more than 80 fish species per survey) and from 12 surveys of marine Monogenea (average of 52 Monogenea species and more than 49 fish species per survey) show that the degree of host specificity of marine digenetic trematodes increases from cold to warm seas; Monogenea do not show such a trend, and the trend is probably reversed in the Pacific Ocean. The difference between the two groups is explained in terms of r- andK- strategy. Monogenea tend to follow a K- strategy (great com- plexity of adult, few offspring), which results in a high degree of host- and site- specificity to facilitate mating in low-density populations. Only one or a few related host species can be infected, and as more related host species are present in the warm Pacific, host-specificity there is reduced. Digenea tend to follow an r- strategy (simple structure of adult, many offspring), part of which is to in- fect many ecologically suitable hosts. Host-specificity in cold-temperate seas is reduced because of the less patchy and ecologically less restricted distribution of hosts.

I ntroduction

Host-specificity, the restriction of parasites to certain host species, is universal, although its degree differs among different parasite species and groups of parasites. Of the platyhel- minths parasitizing marine fishes, for instance, Monogenea are extremely host- specific, most species occurring on a single species or at most a single genus or family only (Bychowsky, 1961; Rohde, 1977a, his Table 6 and further references therein). Digenetic trematodes, on the other hand, often have a wider host spectrum. Thus, according to the data

less diverse fauna. Rohde (1977a) compared data from 5 surveys of marine Mono- genea and pointed out that host-specificity appears to be more extreme in cold- temperate seas. On the basis of a much more extensive material, it will be shown in the following that marine Di- genea show a gradient of decreasing host specificity from warm to cold seas, but that such a gradient does not exist in marine Monogenea.

MaterialandMethods

In the surveys at Lizard and Heron Is- given by Polyanski (1966), of the 34 spe- lands, Great Barrier Reef, fish were ex- cies of Digenea recorded from fishes in the Barents Sea, 21 are known from several host species belonging to more than one family.

Manter (1947, 1955), on the basis of very limited data, was apparently the first to draw attention to differences in the degree of host-specificity of Digenea from different seas. He sug- gested that Digenea in warm seas with a rich fish and parasite fauna are more specific than those in cold seas with a

amined not more than a few hours after catching (for details see Rohde, 1977a). Most fishes from these localities were identified by Dr. G. Allen, Western Aus- tralian Museum, Perth, and Dr. D. Hoese, Australian Museum, Sydney. Most sea- surface temperatures are from Ekman (1953), those for Lizard and Heron Is- lands and for Queensland from Brandon (1973), those for Hawaii from Banner (1974), and those for Japan, South India and the Bay of Bengal from Ministerstvo

0025-3162/78/0047/01 25/S02.00

126 K. Rohde: Host-Specificity in Marine Monogenea and Digenea

Oboroni SSSR Vojenno-morskoi flot (I 974) . Table I. Survey localities with latitudes and annual sea-

The taxonomy of fishes is based on surface temperature ranges

Jordan (1963); fish genera not listed by South India, Trivandrum 8ON 28o-29oc this author were allocated to families using Golvan (1965) , Norman (1966) and Bay of Bengal between

Madras and Calcutta 13-22~ 27o-29Oc BShlke and Chaplin (1968). The localities at which the surveys were made, to- Lizard Island, Great

Barrier Reef 15OS 23~ gether with latitudes and annual ranges in sea-surface temperatures, are listed Tortugas, Florida 25ON 22 ~ 29Oc in Table I �9 Heron Island, Great

The data for Digenea in New Zealand Barrier Reef 23es 20o-28oc

are from Manter's (1954) species descrip- Queensland, between Green tions, not from his discussion, or his Island and Brisbane 17-27Os 19~176

review published in 1 955. Hawaii, Canoehe Bay, Oahu 20ON 20 ~ 27~

Only those data from the literature Guif of Panama and Bimini, are considered which are the result of Galapagos Islands and coast comprehensive surveys. Data based on the of Ecuador to Mexico 4os-3ooN 16o-29Oc

examination of large numbers of indi- Gulf of Mexico 3OON 12o-29oc

viduals of only one or a few species are Japan (most surveys in not included, as such data provide lit- warm waters) 30-45ON

tle or no information about host-speci- New Zealand 40-45es ficity and also tend to give a distorted Black Sea 45ON

picture because of some abnormal host Woods Hole, Massachusetts 41ON 3o-19Oc records ("temporary hosts" of Malmberg, 1970, pp 156 and 160, usually found when British Isles (many data

from colder waters) 50-60ON conditions are unfavourable; examples in

Kulatchkova, 1 97 5) . South Kuril Islands 45ON Yamaguti's (1952, 1953b) survey of

Barents Sea 7OON trematodes in Celebes is not considered, because the author states that the great- White Sea 65ON er part of his collection suffered se- East Kamtchatka 55ON vere damage during transport and could Chukotsk Peninsula, not be studied. His data show that 54 Sehring Sea 63-64~ <2o-(2-8)~

species of trematodes (93%) occur on a single host species and 4 species (7%) on 2 host species, thus supporting the hypothesis that there is an increased Shulman and Shulman-Albova (1953) degree of host-specificity in Digenea list one species of Monogenea in the from warm seas. White Sea as occurring on fish species

The following surveys of Monogenea belonging to two orders (Gyrodactylus ar- are not considered, because only a small cuatus on Gasterosteidae, G. arcuatus elegi- proportion of all monogeneans was col- ni on Gadidae). According to Malmberg lected from the fish examined, or be- (1970), the latter subspecies is a syn- cause part of the material was lost, as onym of G. eligini Bychowsky and his opin- stated by the authors or evidenced by ion, based on a careful morphological the data: Meserve (1938), Galapagos Is- analysis, is accepted for calculating lands; Linton (1940), Woods Hole, Massa- the degree of host-specificity in Ta- chusetts; Yamaguti (1953a), Celebes; bles 4 and 5. Following Malmberg, G. Koratha (1955a, b), Gulf of Mexico. All gr~nlandicus pacificus from Enophrys diceraus, these surveys show a host-specificity of G. harengi from Clupea harangue, and G. ha- 100% or close to 1OO% and therefore sup- rengi from Ammodytes hexapterus recorded by port the hypothesis that there is no Zhukov (1960b) in the Behring Strait, change of host-specificity of Monogenea are considered to be separate species. with latitude. The surveys by Tripathi (1957) in the Bay of Bengal, Unnithan (1957-1971) in South India and Young Resul~ (1967a-1970) in Queensland are comprehensive and therefore included, although The data from the surveys are presented

5~176 (Honshu-Kyushu)

Ii~176 (Cook Strait)

(3-6)O-ca. 2OoC

there may be a strong bias towards certain groups of Monogenea and fishes. For this reason, these surveys should not, or only with caution, be taken into consideration when examining the ques- tion of whether there are slight changes in host-specificity of Monogenea at low latitudes.

in Tables 2-5. Table 2 shows that there is an increase in the proportion of species of Digenea occurring on a single host species, from 20-35% in cold seas to 56-83% in temperate and warm seas. Correspondingly, the proportion of Di- genea species occurring in more than 5 fish species decreases from ]8-36% in

9e-17oc (SE entrance of

English Channel)

-io-(8-13)ec

lo-(9-10)oc

~Barents Sea

<Oo-looc

Table 2. Host-specificity (preference for a certain number of host species) of adult trematodes of marine fishes in different seas

Locality No. of fish No. of trematode species in: Total Data from: species/specimens examined

i fish 2 fish 3 fish 4 fish 5 fish >5 fish species species species species species species

Tortugas, Florida 237/2039 105 43 14 7 25~ a (55.6%) (22.8%) (7.4%) (3.7%)

Hawaii >[44b/ca. 2000 235 54 16 6 20~ (>1933) (74.8%) (17.2%) (5.1%) (1.9%)

Gulf of Panama and 208/484 60 15 2 7 Bimini, West Indies (69.0%) (17.2%) (2.3%) (8.0%) i0-26ON

Galapagos Islands nearly 51 19 7 1 and coast of Ecuador [00/532 (62.2%) (23.2%) (8.6%) (1.2%) to Mexico 4os-30~

Japan 30-45ON ?/Many 169 32 16 5

(73.8%) (14.O%) (7.0%) (2.2%)

New Zealand 58/239 55 8 O O 40-45~ (83.3%) (12.1%)

Black Sea 34/439 30 3 1 1 45~ (83.3%] (8.3%) (2.8%) (2.8%)

Woods Hole, Massachu- ~94b/Many 37 7 5 4 setts 42~ (53.6%) (10.1%) (7.2%) (5.8%)

British Isles ?/Many 28 7 7 5

50-60~ (47.5%) (11.9%) (11.9%) (8.5%)

South Kuril Islands 55/664 12 9 3 5

45~ (27.3%) (20.5%) (6.8%) (11.4%)

Barents Sea 46/1OO3 12 5 6 i

70~ (35.3%) (14.7%) (17.6%) (2.9%)

White Sea 31/1376 7 4 i 3

5 ~ (30.4%) (17.4%) (4.3%) (13.O%)

East Kamtchatka 34/385 5 2 7 O

55~ (20.0%) (8.0%) (28.O%)

aIncluding deepwater species.

buninfected species of fish not listed, but possibly absent.

8 ii (4.2%) (5.8%)

O 3 1%)

2 1 (2.3%) 1.1%)

3 1 (3.7%) i .2%)

189 Manter (1947)

314 Yamaguti (1970)

87 Sogandares-Bernal (1959)

82 Manter (1940)

4 3 229 Manter (1947; data (1.7%) (1.3%) from Yamaguti, many

papers)

1 2 66 Manter (1954) (1.5%) (3.O%)

O i 36 Osmanov (1940) (2.8%}

1 15 69 Linton (1940) (1.4%) (21.7%)

4 8 59 Manter (1947; data (6.8%) (13.6%) from Nicoll, 1914;

and Dawes, 1946)

O 15 44 Zhukov (196Oa) (34.1%)

4 6 34 Polyanski (1966) (11.8%) (17.6%)

3 5 23 Shulman and shulman- (13.O%) (21.7%) Albova (1953)

2 9 25 Strelkov (1960) (8.0%) (36.0%)

Table 3. Host-specificity (preference for a certain number of supraspecific host taxa) of adult trematodes of marine fishes in different seas

Locality No. of trematode species in: Total Data from: I order >i order I family >I family 1 genus >i genus of fish of fish of fish of fish of fish of fish

Tortugas, Florida a 162 27 151 38 141 48 189 Manter (1947) (86%) (14%) (80%) (20%) (75%) (25%)

Hawaii 308 6 269 18 268 46 314 Yamaguti (1970) (98%) (2%) (94%) (6%) (85%) (15%)

Gulf of Panama and 82 5 72 15 68 19 87 Sogandares-Bernal Bimini, West Indies (94%) (6%) (83%) (17%) (78%) (22%) (1959)

Galapagos Islands and 76 6 69 13 58 24 82 Manter (1940) coast of Ecuador to Mexico (93%) (7%) (84%) (16%) (71%) (29%)

New Zealand 56 10 55 11 55 11 66 Manter (1984) (85%) (15%) (83%) (17%) (83%] (17%)

Woods Hole, Massachu- 42 27 38 31 37 32 69 Linton (1940) setts (61%) (39%) (55%) (45%) (54%) (46%)

South Kuril Islands 22 22 15 29 13 31 44 Zhukov (196Oa) (50%) (50%) (34%) (66%) (30%) (70%)

Barents Sea b 17 17 13 21 5 29 34 Polyanski (1966) (50%) (50%) (38%) (62%) (15%) (85%)

East Kamtchatka 9 16 7 18 5 20 25 Strelkov (1960) (36%) (64%) (28%) (72%) (20%) (80%)

Total 772 136 716 194 650 260 910 (85%) (15%) (79%) (21%) (71%) (29%)

aDeepwater species included.

bRecords from other seas included.


Table 4. Host-specificity (preference for a certain number of host species) of Monogenea of marine

fishes in different seas

Locality No. of fish No. of Monogenea species on: Total Data from: species/spec- I fish 2 fish 3 fish >3 fish

imens examined species species species species

South India >37a/~few 57(1OO%) O 0 O 57 8ON hundred

Bay of Bengal >39a/1533 32(91%) 2(6%) i(3%) O 35

13-22ON

Lizard Island 54/169 39(71%) 10(18%) 2(4%) 4(7%) 55

15Os

Heron Island 74/381 80(82%) 16(16%) i(1%) i(1%) 98 23os

Queensland >51a/>180 53(83%) 8(12%) 3(5%) 0 64

17-27os

Hawaii >122a/2097 103(71%) 21(14%) 11(7.5%) Ii(7.5%) 146

2OON

Gulf of Mexico >45a/3335 67(89%) 7(9.5%) i(1.5%) 0 75

3OON

Black Sea 34/439 b 5(83%) i(17%) O O 6 45ON

Barents Sea 46/1OO3 18(86%) 3(14%) 0 O 21

7OON

White Sea 31/1376 8(80%) 2(20%) O O 10

65ON

Chukotsk Peninsula 25/240 20(83%) 3(13%) e O i(4%) d 24

63-64ON

Unnithan (1957-1971)

Tripathi (1957)

Rohde (1977a)

Rohde (1977a)

Young (1967a-1970)

Yamaguti (1968)

Hargis (1957)

Osmanov (1940)

Polyanski (1966)

Shulman and Shulman- Albova (1953)

Zhukov (196Ob)

auninfected host species not listed by the author and therefore not included.

bFreshwater species not included.

CBecause of high degree of host-specificity in the genus Gyrodactylus, possibly several species.

dAccording to Malmberg (1970), probably several species.

Table 5. Host-specificity (preference for a certain number of supraspecific host taxa) of Monogenea of marine

fishes in different seas

Locality No. of Monogenea species on: Total Data from: 1 order >i order 1 family >i family i genus >i genus of fish of fish of fish of fish of fish of fish

South India 57(100%) 0 57(1OO%) O 57(1OO%) O 57 Unnithan (1957-1971)

Bay of Bengal 35(1OO%) O 35(100%) O 31(88.6%) 4(11.4%) 35 Tripathi (1957)

Lizard Island 55(100%) O 55(1OO%) 0 48(87%) 7(13%) 85 Rohde (1977a)

Heron Island 98(100%) O 97(99%) 9(1%) a 95(97%) 3(3%) 98 Rohde (1977a)

Queensland 64(1OO%) O 62(96.9%) 2(3.1%) 61(95.3%) 3(4.7%) 64 Young (1967a-1970)

Hawaii 141(97%) 5(3%) 135(92%) 11(8%) 117(80%) 29(20%) 146 Yamaguti (1968)

Gulf of Mexico 75(100%) O 75(1OO%) O 75(1OO%) O 78 Hargis (1957)

Black Sea 6(1OO%) O 6(1OO%) O 6(100%) O 6 Osmanov (1940)

Barents Sea 21(1OO%) O 21(1OO%) 0 18~86%) 3(14%) 21 Polyanski (1966)

White Sea 10(1OO%) O 10(1OO%) O 8(80%) 2(20%) io Shulman and Shulman- Albova (1953)

Chukotsk Peninsula 23(96%) i(4%) b 21(88%) 3(12%) h 21(88%) 3(12%) b 24 Zhukov (196Ob)

Total 585(99.0%) 6(1.O%) 574(97.1%) 17(2.9%) 537(90.9%) 54(9.1%) 591

a On the closely related Scombridae and Thunnidae (often included in one family).

bprobably more host-specific, see footnotes c and d to Table 4.

K. Rohde: Host-Specificity in Marine Monogenea and Digenea 129

cold seas to I-6% in warm and temperate seas. Woods Hole and the British Isles are intermediate locations, with corre- sponding intermediate host specificities. The same trend with regard to higher taxonomic categories of the hosts is shown in Table 3.

Tables 4 and 5 show that Monogenea do not have an increased host specificity at low latitudes. The percentages of species recorded from a single host species

o\~ 100

50

. . . . . . . . . . . . . o_ . . . . . . . o

o ~ - ~ - ~ - X - X ~ ~ ~ x

Fig. 1. Hos%-specificity of marine Monogenea and

range from 71 to 100%, with the two low- trematodes at different latitudes. Ordinate: per- est values in warm Pacific waters. Corre- centages of species of Monogenea (circles) and sponding to the slightly smaller number marine trematodes (crosses) parasitizing one and

two host species. Abscissa: approximate means of of species on a single host in warm Pa- cific waters, there appears to be a larg- annual sea-surface temperature ranges at various er number of species found on more than localities. Localities of Monogenea from left to three hosts, right: Chukotsk Peninsula, White Sea, Barents

Sea, Black Sea, Gulf of Mexico, Hawaii, Queens- Fig. I illustrates the differences be- land, Heron Islandr Lizard Island, Bay of Bengal,

tween the two groups, using combined South India; localities of trematodes from left data for species parasitizing one and two hosts.

The papers by Brinkmann (1952, 1975) and Fischthal (1977) were received after the paper had been accepted for publica- tion and their data are not included in Fig. I and Tables I-6.

Brinkmann (1952) examined 460 specimens of 31 marine fish species in Nor- way [58~ (5 ~ to 14~ to (IO-I0~ mean temperature ca. 7.5oc]. Of the 30 species of Monogenea found, 27 (90%) occurred on I host species, 2 (7%) on 2 host species and I (3%) on 4 host species; 29 species of Monogenea were found on I genus, and I on 2 genera belonging to different orders.

Brinkmann (1975) examined more than 1OO specimens of 20 marine fish species

to right: East Kamtchatka, White Sea, Barents Sea, South Kuril Islands, British Isles, Woods Hole, Black Sea, New Zealand, Japan, Galapagos, Panama-Bimini, Hawaii, Florida. Regression lines are eye fits, ignoring the trematode data for the Black Sea and New Zealand (see "Discussion"). Regressions calculated from all data are -- Mono- genea: slope = -O.18, intersect 99.2, SD = 4.9; trematodes: slope = 2.2, intersect 40.6, SD = 13.5. The difference between both regressions is highly significant at the O.1% level

Di~ussion

Reality of Gradients in Host-Specificity

Most surveys of digenetic trematodes are comprehensive and permit reliable con-

from near Godhavn in Greenland (ca. 69ON; clusions. The survey in New Zealand is <I ~ to <5oc, mean temperature ca. 2~ the least comprehensive and it may be ex- Of the 24 trematode species found, 11 pected that further studies will reveal (46%) occurred on I host species, 5 (21%) a lesser degree of host-specificity than on 2, 5 (21%) on 3, I (4%) on 4, I <4%) on 5, shown in Table 2. The data would then and I (4%) on >5 host species. Nineteen (79%) trematode species were limited to I genus, 19 (79%) to I family, and 19 (79%) to I order of fish.

Fischthal (1977) examined 200 specimens of 36 marine fish species at Belize, Caribbean Sea (17o-18ON; ca. 22 ~ to 29~ Of the 78 trematode species found, 50 (64%) occurred on I host species, 19 (24%) on 2, 4 (5%) on 3, 4 (5%) on 4, and I (1%) on 5 host species. 61 (78%) species were limited to I genus, 68 (87%) to I family, and 76 (97%) to I order of fish.

All the data support the hypothesis that Monogenea have a high degree of host-specificity at all latitudes, and that trematodes have a reduced host- specificity at high latitudes.

fit even better into the gradient. Mis- identification of species is possible only in a small fraction of the total and cannot affect the results significantly. The latitudinal trend in host- specificity does not change, even if all similar congeneric species and those congeneric species not illustrated or described by the various authors are assumed to be identical, an assumption which is quite unrealistic because only well-known species are usually listed without descriptions (Table 6).

The Black Sea has Digenea with a some- what higher degree of host-specificity than would be expected. However, the Black Sea is exceptional in many re- spects (Ekman, 1953). Generally, the diversity of its fauna is strongly reduced compared with the Mediterranean Sea, from


Table 6. Host-specificity of adult trematodes of marine fishes, if all similar congeneric species and all those congeneric species not described or illustrated by the various authors, are assumed to be identical

Locality No. of trematode Total no. of species in I and trematode 2 host species species

Florida 84(64%) 132

Hawaii 186(80%) 233

Gulf of Panama and Bimini 61(80%) 76

Galapagos 46(68%) 68

New Zealand 51(89%) 57

Woods Hole 28(60%) 47

South Kuril Islands 15(42%) 36

Barents Sea 7(29%) 24

White Sea 8(42%) 19

East Kamtchatka 6(26%) 23

which most of it is derived, and the ab- sence of suitable alternative hosts may explain the high host-specificity of Digenea.

Atlantic compared with the Pacific, i.e., to a smaller number of available alternative hosts (see below).

Misidentifications of Monogenea are less probable than of Digenea. A careful examination of the data showed that errors, if present at all, are minor and cannot significantly affect the conclusions. Because of the great species- richness, an error is most likely in tropical waters. However, Yamaguti' s very careful and detailed descriptions and figures of Monogenea at Hawaii (1968) indicate that, even if all similar species are considered to be identical (species of Haliotrema, Al!opseudaxine, Allopseu- daxinoides), the error is less than 5%.

Host-specificities given in Tables 4 and 5 are based on the fishes examined in each particular sea, they do not in- clude records from other seas. The data given by Polyanski (1966), in his discussion of the survey in the Barents Sea, show that inclusion of such records re- duces the proportion of species found on one host species from 86 to 52.4%.

Octodactylus minor, for instance, has been found in the Barents Sea only on Sicromesistus poutassou (family Gadidae) , but it is also known from Gadus merlangus on the coasts of Norway and Ireland. Diclidophora denticulata is known to occur in the Barents Sea only on Pollachius vi- rens, but it has also been recorded from

We may conclude, then, that the gradi- Merluccius merluccius and G. minutus, all ent in host-specificity of Digenea with latitude (as an approximate indicator of sea temperature) is real. Reduction of host-specificity at high latitudes is all the more surprising because so few host species are present in cold waters.

With the exception of the surveys in

species belonging to the Gadidae, in the European and American Atlantic. Similar- ly, 5 species of Monogenea were found on I or 2 species of the genus Scomberomorus (family Scombridae) on the Great Barrier Reef, but 4 of them are also known from other species of the same genus and in

N.E. Australia (Lizard and Heron Islands, one case even from a related genus in Queensland), the surveys of Monogenea are also comprehensive and permit reliable conclusions. In spite of the small number of fish species examined, the degree of host-specificity of Monogenea in N.E. Australia is slightly less than in most other seas, and it is very probable that more extensive surveys will reveal an even more reduced host-specificity. It must be pointed out that the total number of fish species estimated to occur in the vicinity of Heron Island is approximately 1OO0, and that at Lizard Island is probably even greater (for references see Rohde, 1977a); only a very small fraction of these fishes has been examined. A reduced host-specificity has also been demonstrated by Yamaguti (1968) at Hawaii, but it does not exist in the Gulf of Mexico, where Hargis (1957) made a very extensive survey. This difference may be due to the smaller species-diversity of fish in the

the South China Sea and the Indian Ocean (Rohde, 1976).

All surveys contained in Tables 4 and 5 were made at restricted localities of comparable size. However, the surveys on the Great Barrier Reef are very small and it can, therefore, be expected that more extensive surveys will reveal a reduced specificity there.

We may conclude that, in Monogenea, there is no gradient of reduced host- specificity towards higher latitudes. Host-specificities are similar at different latitudes in the Atlantic but probably reduced in the warm Pacific.

Reasons for Difference between Digenea and Monogenea

The different ecological "strategies" of species of the two groups may result in different host specificities. Distinc-


tion of "r" and "K" strategies will be used to find an explanation. According to MacArthur and Wilson (1967), the fitness in an uncrowded environment with little competition approaches r, the in- trinsic rate of natural increase (Mac- Arthur, 1972), the fitness in a crowded environment with much competition approaches K, the carrying capacity of the environment. In the first type of environment, selection favours productiv- ity (r-selection), in the second it favours efficiency (K-selection). r- selection is likely to predominate in an unstable seasonal environment (opportu- nistic species), K-selection in a stable uniform environment, for instance in

increased by an extreme restriction of the host and microhabitat range (Rohde, 1977b). Only one host or a few closely related hosts can usually be infected, and as more related host species are present in warm waters and particularly in the warm Pacific, host-specificity there is reduced.

Digenea follow an opposite strategy. They are much simpler in structure, although in some groups, for instance in the Microphallidae, the copulatory organs are remarkably complex, and the number of offspring is enormously increased, partly by parthenogenetic or asexual re- production in intermediate hosts. One aspect of this strategy is infection of

many tropical habitats (for further char- many hosts in a particular environment, acteristics of r- and K-selection see Pianka, 1972, and Esch et al., 1977). Jennings and Calow (1975) claimed that, although both groups follow r- and K- strategies at the same time, Digenea are more r-strategists and Monogenea more K-strategists with regard to two charac- ters: Digenea have a low calorific value (rough average of 5.2 Kcal g ash-free dry weight-l) and produce large numbers of eggs (rough average of approximately 10 million), whereas Monogenea have a high calorific value (5.5 Kcal g-l) and produce much less eggs (approximately 1OOO). The data for calorific values have been disputed by Boddington and Mettrick (1975; see also discussion by Esch et al., 1977, pp 34-35), but there are other features of the Monogenea which indicate more emphasis on the in- dividual and less on the production of large numbers of offspring than in Di- genea: usually larger and often more complex eggs; a much more complex structure of the copulatory organs, which probably reaches the extreme in complex- ity in the Heteromicrocotylidae (Rohde, 1977c), with many types of accessory re- productive gland cells also found in other families (Rohde and Ebrahimzadeh, 1969); a much more complex structure of the adult attachment organs (many authors, for instance Rohde, 1977c) ; a variety of oral glandular and sensory structures (own unpublished electron- microscope studies on Heteromicrocoty- lidae) ; a direct life cycle which does not lead to a further multiplication of offspring at various larval stages as in the Digenea, etc. Altogether, rela- tively more energy is spent on maintain- ing the adult and producing fit larvae

i.e., an ecological as opposed to a phylogenetic specificity, because this increases the number of offspring even further. Host-specificity in cold and temperate seas is reduced because of the less patchy and ecologically less restricted distribution of hosts, which facilitates infection of many species in the same habitat.

MacArthur (1965, 1969) showed that tropical species (must) often have a spottier distribution than species at higher latitudes, although this has been disputed for instance for fish. Evidence for more restricted habitats in tropical intertidal animals is given by Moore (1972): the average tropical species occupies about half as much of the intertidal zone as the average temperate species. Kohn (1959) demonstrated a high degree of microhabitat partitioning in tropical Conus species, etc.

Both Digenea and Monogenea live in en- vironments with a certain variability (changes in pH, food contents etc. in the digestive tract, changes in temperature, water currents etc. on the gills), but nevertheless with a high degree of predictability, i.e., the changes occur within a strictly limited range. These changes cannot explain the fundamentally different strategies of the two parasite groups. The reason why Digenea generally produce more offspring is apparently their indirect life cycle involving at least two hosts, which may have evolved because Digenea were originally parasites of molluscs and incorporated vertebrates in their life cycle only second- arily (Rohde, 1971). Contact between the hosts is sporadic and largely unpredict- able, and the chances of infection are

than on the production of much offspring, enhanced by large numbers of eggs and A high degree of host-specificity and infective larval stages (see for in- site-specificity on the host is the stance Esch et al., 1977). Monogenea direct result of this strategy. The prob- evolved as parasites of vertebrates and ability of intraspecific contact and do not have to compensate for the risks thus mating in the small populations is of an indirect life cycle by a great


number of offspring. Each group was ap-

parently forced into its respective ecological strategy by its evolutionary

history. This conclusion is supported by the finding that a digenean with the same microhabitat as Monogenea, Syncoelium filiferum on the gill arches of marine fishes, produces a large number of small

eggs and has a wide range of hosts. It has been found on many fish species be-

longing to different families (Lebedev,

1968; and own observations). The ecological "strategy" of this parasite is not determined by its habitat but by its history as indicated by its taxonomic

status.

Acknowledgements. I wish to thank Dr. D.

Hoese, Australian Museum, Sydney, and Dr. G. Allen, Western Australian Museum, Perth, for

identifying most of the fishes from Heron and Lizard Islands. I thank the Nuffield Foundation, the Australian Research Grants Committee, the

University of Queensland, the University of New England, and the Deutsche Forschungsgemeinschaft for support. D. Bender and P. Rowles provided

technical assistance. S. Domm, Resident Director of the Lizard Island Research Station, kindly helped in getting many of the fish at Lizard Is-

land. I thank the Trustees of the Lizard Island Research Station for the use of their facilities at Lizard Island, Mr. R. Hobbs for critically

reading the manuscript, and Mrs. V. Watt for

typing it.

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Dr. K. Rohde

Department of Zoology

University of New England Armidale

New South Wales 2351 Australia

Date of final manuscript acceptance: March 3, 1978. Communicated by G.F. Humphrey, Sydney

Documents

Latitudinal differences in host-specificity of marine Monogenea and digenea