Abstract: Samples of Merluccius australis (1 13 fish) and of M. hubbsi (195 fish) were collected from 16 positions on the Falklands and Argentine shelves and 1 ...
Parasites of the hakes Merluccius australis and M. hubbsi in the waters around the Falkland Islands, southern Chile, and Argentina, with an assessment of their potential value as biological tags K. MacKenzie and M. Longshaw
Abstract: Samples of Merluccius australis (1 13 fish) and of M. hubbsi (195 fish) were collected from 16 positions on the Falklands and Argentine shelves and 1 off southern Chile. Twenty-eight fungal, protozoan, and metazoan parasite taxa, of which 19 were identified to the species level, and cysts of unknown etiology, were found. These included one new species of myxosporean protozoan found in both host species, three species that are new to both species of hake, three species not previously reported from M. australis, and one not previously reported from M. hubbsi. The most promising biological tags for stock identification, where long life spans are important, are an unidentified fungus; the protozoans Alatospora merluccii Kalavati, Longshaw and MacKenzie, 1995, Goussia sp., Kudoa rosenbuschi (Gelormini, 1944), Microsporidium ovoideum (ThClohan, 1895), Myxidium baueri Kovaleva and Gaevskaya, 1982, and Myxoproteus meridianalis Evdokimova, 1977; the metacestodes Grillotia sp. and Hepatoxylon trichiuri (Holten, 1802); and the parasitic copepod Trifur tortuosus Wilson, 1917. The adult digenean Elytrophalloides oatesi (Leiper and Atkinson, 1914) showed some potential as a tag for following seasonal migrations of hake. Resume : Nous avons prClevC des Cchantillons de Merluccius australis (113 poissons) et M. hubbsi (195 poissons) B 16 endroits sur le plateau continental des Malouines et de l'Argentine, et B un endroit au large du sud du Chili. Nous avons trouvC 28 taxons parasites, champignons, protozoaires et mktazoaires, dont 19 ont CtC identifiCs jusqu'au niveau spCcifique, ainsi que des kystes d'ktiologie inconnue. I1 s'agissait notamment d'une nouvelle espbce de protozoaire myxosporidien trouvCe chez les deux hhtes, de trois espbces qui sont nouvelles chez ces deux merlus, de trois espbces qui n'avaient pas CtC signalCes jusqu-18 chez M. australis, et d'une espbce qui n'avait pas CtC signalee chez M. hubbsi. Les marques biologiques les plus prometteuses pour l'identification des stocks, lorsque la IongCvitC est importante, sont : un champignon non identifiC; Ies protozoaires Alatospora merluccii Kalavati, Longshaw et MacKenzie, 1995, Goussia sp., Kudoa rosenbuschi (Gelormini, 1944), Microsporidium ovoideum (ThClohan, 1895), Myxidium baueri Kovaleva et Gaevskaya, 1982, et Myxoproteus meridianalis Evdokimova, 1977; les mCtacestodes Grillotia sp. et Hepatoxylon trichiuri (Holten, 1802); enfin, le copCpode parasite Trifur tortuosus Wilson, 1917. Le digCnien adulte Elytrophalloides oatesi (Leiper et Atkinson, 1914) presentail un certain potentiel comme marque pour suivre les migrations saisonnibres des merlus.
Introduction T h e hake of the southwest Atlantic Ocean were considered t o comprise the two species Merluccius hubbsi (Argentine hake) a n d M . polylepis (Patagonian h a k e ) until I n a d a ' s (1981) s t u d y o f m o r p h o m e t r i c a n d m e r i s t i c c h a r a c t e r s
J 12807 K. MacKenzie and M. Longshaw. SOAFD Marine Laboratory, P.O. Box 101, Aberdeen AB9 8DB, Scotland.
resulted in M. polylepis being relegated t o a junior syno n y m of Merluccius australis (New Zealand hake). Inada considered that the N~~ Zealand and Patagonian bakes had not diverged sufficiently to warrant their recognition as separate species. In the Atlantic, the geographical distributions of M. hubbsi and M. australis overlap around the Falkland Islands, while i n t h e Pacific, t h e distribution of M. australis overlaps that of a third species, Merluccius gayi (Chilean hake), off the coast of southern Chile. Morphologically the three species a r e very similar a n d identification of individual
Can. J. Fish. Aquat. Sci. 52(Suppl. 1): 213-224 (1995). Printed in Canada / ImprimC au Canada
Can. J. Fish. Aquat. Sci. Vol. 52(Suppl. I ) , 1995
fish is difficult. Important commercial fisheries are based on all three species, but little is known about their population biologies. The hake fishery in the waters around the Falkland Islands is particularly important to the economy of the islands, but no nursery grounds have been identified in the area, and the migratory ranges of the M. hubbsi and M. australis caught on the Falklands Shelf are unknown. The purpose of this study was to survey the parasite faunas of M. australis and M. hubbsi in the waters around and adiacent to the Falkland Islands and to assess the feasability of using some of these parasites as biological tags to identify different stocks and to follow the migrations of hake populations in the area. Parasites have been used as biological tags to distinguish stocks of many species of both marine and freshwater fishes (see reviews by Sindermann (1961, 1983); Kabata (1963); MacKenzie (1983, 1 9 8 7 ~ )Lester ; (1990); Moser (1991); Williams et al. (1992)). Guidelines to the selection of parasite species likely to make the best tags are given in these reviews.
Materials and methods Samples of hake from the Atlantic part of the study area were caught by trawl, while the Chilean sample was caught by long-line. Because the samples were taken by commercial fishing vessels and only small numbers of hake were usually caught in individual hauls, it was not possible to follow a pre-planned sampling program with any degree of accuracy. The samples detailed in Table 1 are therefore what were available to us from the areas where the fishing vessels were operating at the time. The fish were deep-frozen at sea and transported by sea and road to the SOAFD Marine Laboratory in Aberdeen, where they were defrosted. Individual fish were identified to species according to the criteria of Cousseau and Cotrina (1980) and Inada (1981). These identifications were subsequently checked against biochemical analyses of tissue samples using enzyme electrophoresis (J. Murphy, I. Wilson, and E. Verspoor, SOAFD Marine Laboratory, Aberdeen, Scotland, unpublished data). The length of each fish was measured to the nearest centimetre. Eleven samples of M. australis (113 fish) came from southern Chile (1) and the Falklands Shelf (10). Thirteen samples of M. hubbsi (195 fish) came from Argentinian waters (4) and from the Falklands Shelf (9). Sampling positions are shown in Fig. 1 and sampling details given in Table 1. All the external surfaces of the fish, including the buccal and opercular cavities, were examined for macroparasites using a dissecting microscope at 10X magnification. The visceral cavity was then opened, the internal organs removed, and each examined for macroparasites using a dissecting microscope. The stomach and intestine were opened longitudinally and examined. Smears were taken from all organs and examined for protozoan parasites at magnifications of 300-500X. Representative samples of all parasite species found were preserved in either 8% buffered formal-saline or 70% ethanol and voucher specimens were deposited at the Natural History Museum in London, U.K.
The measures of level of infection used were ( i ) prevalence, defined as the number of fish infected by a particular parasite species divided by the total number of fish in the sample, expressed as a percentage, and ( i i ) abundance, defined as the total number of individuals of a particular parasite species in a sample of hosts divided by the total number of individuals of the host species in the sample (see Margolis et al. 1982).
Results Twenty-eight parasite taxa were found in the two species of hake, of which 19 were identified to species level (Table 2). Also recorded were cysts of unknown etiology (CUES) in the gill filaments. The myxosporean protozoan Alatospora merluccii Kalavati, Longshaw and MacKenzie, 1995 was found for the first time during the present study and was described by Kalavati et al. (1995). Aporocotyle australis Fernandez and DurBn, 1985 and a single metacercaria of Zoogonus sp. were found only in M. australis. Aporocotyle argentinensis Smith, 1969 was found only in M. hubbsi, as was the single specimen of Echinorhynchus sp., which is also a new finding for this host. Goussia sp., Lecithochirium genypteri Manter, 1954, and Gonocerca phycidis Manter, 1925 are new findings for both species of hake, while Myxoproteus meridianalis Evdokimova, 1977, Microsporidium ovoideum (Thtlohan, 1895); and Zoogonus sp. have not been previously reported from M. australis. The hake samples examined in the present study were characterized by a predominance of one sex, usually females (258 females to 50 males in total), except for the Chilean sample of M. australis, which consisted of 23 males and 6 females. It was therefore not possible to carry out a meaningful comparison between the parasite faunas of the two sexes in any individual sample. Most of the samples contained less than 10 individuals of each hake species and showed large variations in mean length and length range. Tests of statistical significance on differences in prevalence and abundance between samples were therefore considered to be inappropriate.
Merluccius hubbsi (Tables 3-5) Of the 26 parasites and pathological conditions found, several showed marked variations in prevalence and abundance between samples, particularly between those from the Falklands study area to the south and the Argentinian to the north. Fungal infections were relatively common around the Falklands, but only one fish from the Argentinian samples was infected. The only finding of Alatospora merluccii from M. hubbsi was in a fish caught to the east of the Falklands, while the other gall bladder myxosporean, Myxidium baueri Kovaleva and Gaevskaya, 1982, was found only around the Falklands. In contrast, the four other protozoan species were present only in samples taken to the west and north of the Falklands and in Argentinian waters. The blood-fluke A. argentinensis was most common in the Argentinian samples and was absent from those taken to the east and south of the Falkland Islands. Samples 1 and 3, taken 3 weeks apart from positions within 3 miles of one another, showed a remarkable difference in prevalence and abundance of the digenean Elytrophalloides oatesi (Leiper
MacKenzie and Longshaw
Table 1. Details of hake samples in chronological order.
Length of fish (cm) Sample No.
No. of fish
200-300 308 Unknown Unknown Unknown 300
Unknown Unknown Unknown Unknown Note: A, Merluccius australis; H , Merluccius hubbsi. See Fig. 1 for samplling positions.
and Atkinson, 1914). Sample 1 was the only sample with no E. oatesi, whereas all eight fish in sample 3 were infected with from 10 to 73 parasites each (Table 3). All the cestodes, except for phyllobothriid plerocercoids, and the nematodes, were more common in the Falklands samples. Prevalence and abundance of CUES were markedly greater in the two southern-most Argentinian samples than elsewhere.
Merluccius australis (Tables 6-7) Twenty-seven parasite species and pathological conditions were recorded from M. australis. Some of the parasites showed apparent host preferences and discontinuous geographical distributions. Alatospora merluccii was much more common in M. australis than in M. hubbsi and was the only protozoan recorded from the Chilean sample, whereas Goussia sp. was much less common in M. australis. Microsporidium ovoideum was also much less common in M. australis than in M. hubbsi and was only found in samples from the north and west of the Falklands. Anthocotyle merluccii van Beneden and Hesse, 1863 was found only in the Chilean sample, while Lacistorhynchus sp. was found in only two fish, one from Chile and one from southwest of the Falkland Islands. Sample 1 contrasted markedly with sample 3 in prevalence and intensity of E. oatesi (Table 7 ) , although the difference was not so great as in M. hubbsi from the same samples. Samples 1 and 4 (Chile)
were the only samples without E. oatesi. The adult cestode Clestobothrium crassiceps (Rudolphi, 1819) was much more common in M. australis than in M. hubbsi.
Discussion The parasite faunas of these two sympatric species of hake are very similar, with 23 of the 28 parasite taxa recorded in this study being common to both host species. One more parasite species was recorded from Merluccius australis than from M. hubbsi, although fewer M. australis were examined. More parasite species were also recorded from M. hubbsi caught around the Falkland Islands than from Argentinian waters. Both host species were caught around the Falkland Islands, but only M. hubbsi was present in the Argentinian samples, so the differences between their parasite faunas may be due more to differences in the geographical distributions of the parasites than to differences in host biology. There is evidence that male and female hake have different post-spawning migratory patterns in some areas (Di Giacomo et al. 1993), but the pronounced sex bias in our samples prevented us from testing for differences in parasite faunas between the sexes. The fungal infection was found in hake from Chile and all Falklands areas except the west, but only one fish from the Argentine samples was infected. The infection is likely to be of long duration and it may prove to be a useful tag for M. hubbsi.
Can. J. Fish. Aquat. Sci. Vol. 52(Suppl. I ) , 1995
Fig. 1. Hake sampling positions.
All six protozoan species appear to have restricted distributions within the study area and all are potentially useful biological tags. The four myxosporeans are easily identified by their distinctive spore shapes and some myxosporean infections are known to persist for years (Lom and Dykovii 1992). All are site specific; although Kudoa rosenbuschi (Gelormini, 1944) can occur anywhere in the musculature it is easily seen because of the black pigment associated with it. Alatospora merluccii and M. baueri both appear to have southern distributions in the Atlantic study area, while Goussia sp., K. rosenbuschi, M. ovoideum, and M. meridianalis appear to have northern distributions. Kudoa rosenbuschi may have a northern distribution because Sardella
(1988) found it in M. hubbsi from northern Argentine waters, whereas neither Reimer and Jessen (1981) nor Stott (1982) found it in M. hubbsi or M. australis from Falkland waters. Okada et al. (1980) found Kudoa sp. to be much more common in M. gayi from the more northern of two sampling stations along the coast of Peru, prevalences of infection being 40 and 14.4%. We did not find Kudoa in our Chilean sample of M. australis. The Goussia sp. found in the livers of both species of hake is similar to Goussia clupearum (ThClohan, 1895). Morrison and Marryatt (1990) found a coccidian that they considered might be G. clupearum in the livers of Merluccius bilinearis in the northeast Atlantic, but our record may be the first of this coccidian from the Southern
MacKenzie and Longshaw Table 2. Parasites and pathological conditions recorded from Merluccius australis (Ma) and Merluccius hubbsi (Mh). Host species Parasite Fungus Unidentified fungus Protozoa Alatospora merluccii Kalavati, Longshaw, and MacKenzie, 1995 Goussia sp. Kudoa rosenbuschi (Gelormini, 1944) Microsporidium ovoideum (ThClohan, 1895) Myxidium baueri Kovaleva and Gaevskaya, 1982 Myxoproteus meridianalis Evdokimova, 1977 Monogenea Anthocotyle merluccii van Beneden and Hesse, 1863 Digenea Aporocotyle argentinensis Smith, 1969 A. australis Fernandez and Durin, 1985 Derogenes varicus (O.F. Miiller, 1784) Elytrophalloides oatesi (Leiper and Atkinson, 1914) Gonocerca phycidis Manter, 1925 Lecithochirium genypteri Manter, 1954 Zoogonus sp. metacercaria Cestoda Clestobothrium crassiceps (Rudolphi, 18 19) Grillotia sp. plerocercoid Hepatoxylon trichiuri (Holten, 1802) plerocercoid Lacistorhynchus sp. plerocercoid Diphyllobothriidae plerocercoid Phyllobothriidae plerocercoid Nematoda Anisakis simplex (Rudolphi, 1809) larva Hysterothylacium aduncum (Rudolphi, 1802) Hysterothylacium and Contracaecum larva Acanthocephala Echinorhynchus sp. Copepoda Chondracanthus palpifer Wilson, 1912 Neobrachiella insidiosa f. lageniformis Kabata, 1979 Trifur tortuosus Wilson, 1917 Other pathological conditions Cysts of unknown etiology (CUES)
Site of infection All soft tissues, especially liver
Gall bladder Liver Musculature Liver Gall bladder Urinary bladder
Voucher specimen No. None
1994:3:15:1 None 1994:6:13:3 1994:6:13:1 1994:3:15:2 1994:6: 13:2
Gills Heart, blood vessels Heart, blood vessels Stomach, oesophagus, buccal cavity Stomach, oesophagus, buccal cavity Stomach, oesophagus, buccal cavity Stomach wall Liver
Intestine Visceral cavity, stomach wall Visceral cavity Musculature Stomach wall Intestine
19220.127.116.11-41 None 1918.104.22.168-65 1922.214.171.124-63
Visceral cavity Stomach, intestine Stomach, intestine
None None None
Buccal cavity Gills Body surface Gill filaments
Hemisphere. Myxidium baueri was originally described from Coryphaenoides holotrachys and M. hubbsi caught in the southwest Atlantic by Kovaleva and Gaevskaya (1982). Kalavati et al. (1995) drew attention to some anomalies between their observations and the original description and suggested that material from the two hake species
and C. holotrachys requires further comparative study to determine if one or more species of Myxidium is involved. The only monogenean found on these hake, Anthocotyle merluccii, was not particularly common at any of the sampling locations but was widely distributed in M. hubbsi. In M. australis, however, it was only found in the Chilean
Table 3. Prevalence (P, %) and abundance (A, metazoan parasites only) of parasites and CUEs in samples of Merluccius hubbsi from east and south of the Falkland Islands (see Fig. 1 and Table 1). Sample 1 ( n = 8)
E + SD
Fungus Unidentified fungus Protozoa Alatospora merluccii Myxidium baueri Monogenea Anthocotyle merluccii Digenea Derogenes varicus Elytrophalloides oatesi Gonocerca phycidis Cestoda Clestobothrium crassiceps Grillotia sp. Hepatoxylon trichiuri Diphyllobothriidae Phyllobothriidae" Nematoda Anisakis simplex Hysterothylacium + Contracaecum spp. Copepoda Chondracanthus palpifer Neobrachiella insidiosa f. lageniformis Trifur tortuosus Others CUEs "Numbers of Phyllobothriidae were not counted.
Sample 5 ( n = 5)
Sample 3 ( n = 8)
i k SD
Sample 9 (n = 3)
Sample 7 (n = 6) A
i k SD
E k SD
Table 4. Prevalence (P, %) and abundance ( A , metazoan parasites only) of parasites and CUES in samples of Merluccius hubbsi from south, west, and north of the Falkland Islands (see Fig. 1 and Table 1). Sample 10 ( n = 8) A
Sample 13 ( n = 37)
Sample 12 ( n = 3)
Sample 11 ( n = 30) A
E. (D 3 a,
x k SD
Z k SD
Z k SD
0 r 3
Fungus Unidentified fungus Protozoa Goussia sp. Kudoa rosenbuschi Microsporidium ovoideum Myxidiur~zbaueri Myxoproteus meridianalis Monogenea Anthocotyle merluccii Digenea Aporocotyle argentinensis Derogenes varicus Elytrophalloides oatesi Gonocerca phycidis Lecithochirium genypteri Cestoda Clestobothrium crassiceps Grillotia sp. Hepatoxylon trichiuri Diphyllobothriidae Phyllobothriidaea Nematoda Anisakis simplex Hysterothylaciurn + Contracaecum spp. Acanthocephala Echinorhynchus sp. Copepoda Chondracanthus palpifer Neobrachiella insidiosa. f. lageniforrnis Trijiur tortuosus Others CUEs - -- -
"Numbers of Phyllobothriidae were not counted
Can. J. Fish. Aquat. Sci. Vol. 52(Suppl. I ) , 1995
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