Haimovici, Manuel

Vidal, Erica Alves Gonzalez

English

Repositório Institucional  Universidade Federal do Rio Grande

402Cephalopods play an important rolein the transfer of parasites throughthe food web. They are second andthird intermediate hosts for larvalstages of digeneans, cestodes, andnematodes. The final hosts are usu-ally fishes, sea birds, and marinemammals (Hochberg, 1990). Nev-ertheless, the interactions of cepha-lopods and their parasites are stillpoorly understood, and almostnothing is know about parasitismin cephalopod paralarvae and earlyjuveniles (Vecchione, 1987). Infor-mation on parasitism in the earlystages of cephalopod life cycles canprovide a better understanding ofhost-parasite relationships as wellas the environment and conditionsin which infection first occurs.Ommastrephid paralarvae areamong the smallest cephalopods athatching and are termed “rhyncho-teuthion” because their tentacles arefused into a proboscis-like structure.Three distinct morphological typesof rhynchoteuthion paralarvae(types “A,” “B,” and “C”) are foundcommonly off southern Brazil(Haimovici et al., 1995). “Type C”is Illex argentinus (Castellanos,1960) and “type A” probably isOmmastrephes bartramii (Lesueur,1821). Illex argentinus is distrib-Digestive tract parasites in rhynchoteuthionsquid paralarvae, particularly inIllex argentinus (Cephalopoda:Ommastrephidae)Erica A. G. VidalManuel HaimoviciDepartamento de OceanografiaUniversidade do Rio Grande (FURG)C. P. 474. Rio Grande RS. 96 201-900, BrazilE-mail address (for E. A. G. Vidal): eavidal@utmb.eduPresent address (for E. A. G. Vidal): National Resource Center for CephalopodsMarine Biomedical InstituteUniversity of Texas Medical Branch301 University Blvd., Galveston, Texas 77555-1163Manuscript accepted 19 May 1998.Fish. Bull. 97:402–405 (1999).uted in the southwestern AtlanticOcean from 22° to 54°S (Roper etal., 1984), and it currently supportsthe largest squid fishery in theworld. This species is an importantlink in the trophic relations of thepelagic ecosystem of this region andconstitutes a major element of thediet of several commercial fishes,such as Thunnus obesus, Merlucciushubbsi, Xiphias gladius, and Poly-prion americanus (Santos, 1992;Ivanovic and Brunetti, 1994).The digestive tract contents ofIllex argentinus and the other rhyn-choteuthion types were examinedby Vidal and Haimovici (1998).During examination of the diges-tive tracts, observations on parasit-ism were made. In this note we re-port the parasites (protistans andmetazoans) found in the digestivetract of rhynchoteuthion paralarvae,mainly Illex argentinus.Material and methodsOmmastrephid paralarvae were col-lected in four surveys carried out be-tween Cape of Santa Marta Grande(28°30'S) and Chuí (34°20'S), Brazil,during the spring of 1987, summerof 1990, autumn of 1991, and win-ter of 1988. Paired bongo nets, with60-cm mouth diameter and 0.33-mm mesh were used in oblique towsbetween the surface and depths ofapproximately 300 m. This gearwas towed at a speed of 2 kn anddeployed for 5–15 min. Afterwards,paralarvae were fixed and pre-served in formalin.Digestive tracts were examinedfrom paralarvae of 72 I. argentinus(1.0–8.0 mm of mantle length (ML)),12 “type A” (1.0–5.8 mm ML) and 4“type B” (2.0–4.0 mm ML). Para-larvae were stained with alcianblue and then cleared with trypsin,following the method of Vecchione(1991). This method makes theparalarvae semitransparent andthe parasites in the gut easier tosee. The stomach, caecum, and in-testine of all paralarvae were ex-amined for parasites with a lightmicroscope at a magnification of400×. The esophagus was not exam-ined. Five I. argentinus juveniles(16.0–38.0 mm ML) and 14 para-larvae (1.6–9.7 mm ML) of I. argen-tinus with no previous clearing andstaining treatment were also exam-ined. The prevalence and the meanintensity of infestation (number ofa particular parasite per infectedindividuals) were calculated ac-cording to Margolis et al. (1982).ResultsParasites were not found in the 14untreated paralarvae. The opaquewalls of the internal organs madethe visualization of parasites diffi-cult. A single copepod parasite wasfound in one of the five untreatedjuveniles.Four types of parasites were ob-served in paralarvae and juvenileI. argentinus: coccidians (Apicom-plexa: Sporozoea: Eucoccidiida),didymozoid metacercariae (Platy-helminthes: Trematoda: Digenea),403NOTE Vidal and Haimovici: Parasites in rhynchoteuthion squid paralarvae1 Hochberg, F. G. 1997. Santa Barbara Museum of NaturalHistory, 2559 Puesta del Sol Road, Santa Barbara, CA93105. Personal commun.a nematode (Nematoda) and a copepod (Arthropoda:Crustacea: Siphonostomatoida). About 50 coccidians(Aggregata sp.) were found distributed along the cae-cum wall of a 7.8-mm-ML paralarva collected in win-ter. Because the paralarva was preserved in glycerinfor several months, taxonomic details of the para-sites were not very clear. Cyst capsules (sporocystes)varied in size from 11 to 17 µm. However, the de-tailed structures inside the capsules were obscureand no certainty could be attained about the pres-ence of sporozooites; hence this protozoan was as-signed to the genus Aggregata. The observed para-sites may have been in a very early stage of develop-ment and if the capsules actually represent sporo-cystes they were unusual because only 1 or 2 werepresent inside an amorphous oocyst mass (Hoch-berg1). These parasites are deposited at the SantaBarbara Museum of Natural History.Six I. argentinus paralarvae (2.2–6.7 mm ML) fromautumn, winter, and spring surveys contained 1–3didymozoid metacercariae, probably type Monili-caecum. The body dimensions of the parasites rangedfrom 140 to 200 µm and because of their size and theabsence of testicular anlagen, they appeared to berecently hatched. A single trematode attached to thecaecum wall was found in the smallest paralarva.Three parasites were found in the largest paralarva,two attached to the stomach wall and one near thebuccal mass. In the other paralarvae, the parasiteswere found attached to the caecum wall. Data onprevalence and mean intensity of infestation of dif-ferent paralarval types and surveys of didymozoidsTable 1Results of examinations of rhynchoteuthion paralarvae from four surveys conducted between the spring of 1987 and autumn of1991. + = presence; 0 = absence.SummerSpring 1987 1990 Autumn 1991 Winter 1988Illex argentinus “Type B” “Type A” Illex argentinus “Type B” Illex argentinusParalarvae mantle length (mm) 1.0–8.0 2.8 1.0–5.8 1.3–5.5 2.0–4.0 1.0–7.8Digestive tracts examined 41 1 12 19 3 12Parasites:Nematode + 0 0 0 0 0Aggregata sp. (coccidian) 0 0 0 0 0 +DidymozoidsMonilicaecum sp. + 0 + + 0 +Prevalence (%) 7.3 72.0 10.5 8.3Mean intensity of infestation 2.3 3.5 1.5 1.0are presented in Table 1. We found a single (nematodeattached to the caecum wall of a 7.0-mm-ML rhyncho-teuthion from the spring sample. The copepod para-site was located on the caecum wall of a 38.0-mm-MLjuvenile obtained in spring. The copepod was identi-fied as an adult male of Metacaligus uruguayensis(Siphonostomatoida: Caligidae) (Ho and Bashirullah,1977). Illex argentinus is a newly recorded host forM. uruguayensis.In the summer of 1990, didymozoid metacercariaewere found in “type A” rhynchoteuthions from 2.0 to5.0 mm ML. Prevalence was 72% and the mean in-tensity of infestation was 3.5 (Table 1). All were at-tached to the caecum or stomach walls, except forthree parasites attached to the inner wall of themantle and two others to the caecum wall of a singleparalarva (3.6 mm ML).Parasites were not found in “type B” rhyncho-teuthions. However, only four paralarvae of this typewere examined.DiscussionIllex argentinus first acquire didymozoid metacer-cariae as small rhynchoteuthions. Hatchlings typi-cally are found off southern Brazil at the outer shelfand slope in tropical and subtropical waters (Vidaland Haimovici, 1997). The infestation may be relatedto the fact that paralarvae are distributed mainly intropical waters, where cystophorous cercariae maybe abundant and not necessarily because theparalarvae are eating infected intermediate hosts.Crustacean prey were not found in the digestivetracts of rhynchoteuthions smaller than 3.7 mm ML(Vidal and Haimovici, 1998). However, paralarvae404 Fishery Bulletin 97(2), 1999larger than this size could also be infested by con-suming infected second-intermediate hosts, such ascopepods and other crustaceans.Infestation in the smaller rhynchoteuthions mayoccur when free cystophorous cercariae are releasedinto the plankton and passively enter the mantle cav-ity during respiration (Gaevskaya, 1976) or when thecercariae attach to mucus that covers the mantle andhead of rhynchoteuthions. They may also be ingesteddirectly, in the same way that crustaceans are in-fested. If this is true, ommastrephid paralarvae mayact as second intermediate hosts for some didy-mozoids. The presence of didymozoid metacercariaein the digestive tracts of rhynchoteuthions as smallas 2.0 mm ML shows that the infection occurs wellbefore that previously recorded by Gaevskaya andNigmatullin (1983). Additionally, the size of thedidymozoid metacercariae type Monilicaecum (140–200 µm) found on rhynchoteuthion paralarvae isstrong evidence that they are in an early develop-mental stage in relation to those found on adult I.argentinus from southern Brazil (400–800 µm)(Santos, 1992). Our results are in accordance withthe suggestion of Hochberg (1990) that didymozoidscan grow inside the squid host. Hochberg (1990) alsoreported that a peak of infestation by didymozoidsoccurs in squids from 10 to 25 cm in ML. Nevertheless,infection decreases in adult individuals (Gaevskaya andNigmatullin, 1977, 1983) owing to the fact that thedidymozoids die after they reach a maximum size in aspecific host (Hochberg, 1990). Larger squids maybe reinfected by didymozoid metacercariae when theyfeed on infested fish prey (Hochberg, 1990). Our re-sults indicate that more paralarvae should be exam-ined in the future. If it is correct to assume that re-cently hatched didymozoid metacercariae usuallyinfest early paralarvae, information on size and de-velopmental stage of both host and parasites wouldhelp to understand their relationship better.Didymozoid metacercariae were found in I. argen-tinus rhynchoteuthions from autumn to spring andin “type A” rhynchoteuthions during the summer.This morphotype had a higher prevalence and infes-tation of didymozoids than those of I. argentinus.They were collected in the summer of 1990, whentropical waters dominate the study area (Vidal andHaimovici, 1997). Thus, these larval trematodes arepresent off southern Brazil throughout the year. Thisfinding is in agreement with the occurrence of thehigh prevalence and intensities of didymozoid meta-cercariae in juvenile and immature I. argentinus fromthe same area year around (Santos, 1992).Only the sexual stages of Aggregata occur in cepha-lopods, whereas asexual stages infect the digestivetracts of crustaceans (Hochberg, 1990). Aggregataappears to be host-specific only in cephalopods, notin crustaceans, and is a common parasite of Sepiaand Octopus (Hochberg, 1990). Our study is the firstto report its presence in I. argentinus. This coccidianhas not been found in adults of I. argentinus collectedoff southern Brazil (Santos, 1992) or Argentina(Nigmatullin and Shukhgalter, 1990; Sardella et al.,1990). Martialia hyadesi, a southern Atlantic oceanicspecies, and Todaropsis eblanae and Todarodes sagit-tatus in waters off Spain are the other ommastrephidsquids in which Aggregata have been reported(Gaevskaya et al. 1986, Pascual et al. 1996). It isimportant to stress that infections by Aggregata canonly be established after paralarvae begin to feed oncrustaceans infected with the asexual stages of theparasite. The infected paralarva observed in thisstudy was 7.8 mm ML; however, crustacean prey,mainly copepods, have been found in the gut of I.argentinus paralarvae larger than 3.7 mm ML (Vidaland Haimovici, 1998).Metacaligus uruguayensis was originally describedfrom the gill cavity of Trichiurus lepturus from Ven-ezuela (Ho and Bashirullah, 1977). This genus pre-viously has not been reported from cephalopods (seereview by Hochberg, 1990). Associations betweencopepods and cephalopods appear to be primarilycommensal and not truly parasitic (Hochberg, 1990).In southern Brazil, small and large adult T. lepturus(70–1000 mm TL) occasionally prey on juvenile andadult I. argentinus (22–200 mm ML) (Martins, 1992);however, additional information is required to de-termine whether I. argentinus serves as a final oronly an accidental host for this copepod.AcknowledgmentsWe would like to thank F. G. Hochberg for his valu-able review of the manuscript and for examining thecoccidian parasites. We also thank G. A. Boxshall forhis support and for the identification of the copepodparasite. E. A. G. Vidal was supported by the Brazil-ian National Research Council (CNPq).Literature citedCastellanos, Z. J. A.1960. Una nueva especie de calamar Argentino Omma-strephes argentinus sp. nov. (Mollusca, Cephalopoda).Neotropica 6(20):55–58.Gaevskaya, A.V.1976. On the helminthofauna of the Atlantic squid Omma-strephes bartramii Lesueur. 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Relações tróficas do calamar argentino Illex argen-tinus (Castellanos, 1960) (Teuthoidea: Ommastrephidae)no sul do Brasil. Tese de Mestrado, Universidade do RioGrande (FURG), Rio Grande-RS, Brasil, 83 p.Sardella, N. H., M. I. Roldan, and D. Tanzola.1990. Helmintos parasitos del calamar (Illex argentinus)en la subpoblacion bonaerense-norpatagonica. FrenteMaritimo 7: 53–56.Vecchione, M.1987. Juvenile ecology. In P. R. Boyle (ed.), Cephalopodlife cycles, II, p. 61–84. Academic Press, London.1991. A method for examining the structure and contentsof the digestive tract in paralarval squids. Bull. Mar. Sci.49:300–308.Vidal, E. A. G., and M. Haimovici.1997. Distribution and transport of Illex argentinus para-larvae across the western boundary of the Brazil-Malvinasconfluence front off southern Brazil. In 63rd annual meet-ing—America Malacological Union and 30th annual meet-ing—Western Society of Malacologists, Santa Barbara,California, p 61. [Abstract.]1998. Feeding and the possible role of the proboscis andmucus cover in the ingestion of microorganisms by rhyncho-teuthion paralarvae (Cephalopoda: Ommastrephidae).Bull. Mar. Sci. 63(2):305–316.

Digestive tract parasites in rhynchoteuthion squid paralarvae particularly in Illex argentinus (Cephalopoda; Ommastrephidae)

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Digestive tract parasites in rhynchoteuthion squid paralarvae particularly in Illex argentinus (Cephalopoda; Ommastrephidae)

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Repositório Institucional Universidade Federal do Rio Grande