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Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 90(3): 319-324 may/jun. 1995 Occurrence of Sciadicleithrum mexicanurn Kritsky, Vidal-Martinez et Rodriguez-Canul, 1994 (Monogenea: Dactylogyridae) in the Cichlid Cichlasorna urophthalrnus from a Flooded Quarry in Yucatan, Mexico EF Mendoza-Franco, V Vidal-Martinez, R Sima-Alvarez, R Rodriguez-Canul, C Vivas-Rodriguez, T Scholz/+ Centro de Investigacion y de Estudios Avanzados del Instituto Politecnico Nacional (CINVESTAV-IPND, Urndad Menda, Carretera Antigua a Progreso Km. 6, A.P. 73 Cordemex, Merida, Yucatan, Mexico *Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31,370 05 Ceske Budejovice, Czech Republic
Cichlids, Cichlasoma urophthalmus, collected in a flooded quarry in the Yucatan Peninsula, Mexico, from January through June 1992, had high levels of infection with the ancyrocephaline Sciadicleithrum mexicanum (Monogenea: Dactylogyridae) in all monthly samples. Neither occurrence nor maturation of the worms exhibited any pronounced monthly fluctuation. The infection rate was found to be sizedependent, greater in longer risk The worms occurred on primary lamellae of gill filaments of all arches, with lower numbers of parasites attached to the fourth gill arch. Otherwise, there was no significant site preference of worms. Only nanor histopathological changes were found at the sites of attachment, and these were restricted to the epithelial cells of the primry lamellae of the gill filaments. The lack of seasonal periodicity in lhis tropical monogenean is compared to seasonal cycles typical of temperate species. Key words: Monogenea - occurrence - maturation - Ancyrocephalinae - cichlid fishes - Mexico Very limited information is available about ecology, including seasonality in the occurrence and maturation, of monogeneans from the Neotropical Region, including Mexico (see Chubb 1977, 1988). During parasitological examination of the cichlid Cichlasona urophthabnus (Gunther, 1862), from a flooded quarry in the Yucatan Peninsula, Mexico, the monogenean Sciadicleithrum mexicanurn Kritsky, Vidal-Maninez et Rodriguez-Canul, 1994 was found on the gills of these fish (Kritsky et al. 1994). Data on the occurrence and ecology of this ancyrocephaline parasite are presented in this paper. MATERIALS AND METHODS The study site was a flooded quarry in the Mitza limestone factory, 30 km north of Metida, Yucatan (21^o 15'N, 89^o 40'W). The total area of water body is 9.3 ha and average depth of the water is 5.2m, with a maximum depth of 8.5m (Flores-Nava 1990). The only helminth' recorded from the gills of C. urophthahnus was S. mexicanum.
A total of 104 fish was sampled, using a cast net from January to June 1992, i.e. during the dry season. Intervals between individual samples fluctuated from 6 to 25 days, and number of specimens in individual months varied from 6 to 36 (Table I). The fishes were transported live to the laboratory, where they were kept together in aerated swamp water in 1000 l aquaria. Over the following 1-3 days, they were killed, their gills removed and placed in Berland solution and immediately transferred to petri dish with 70% alcohol. After fixation, each gill arch was examined separately under a dissecting microscope and the number of worms was counted. Data were ana- lyzed according to the parameters recommended by Margolis et al. (1982): prevalence of infection and mean intensity of infection. To evaluate their state of maturity, worms were stained with trichrom of Gomori (modification by Salgado-Maldonado 1979) and mounted in Canada balsam as permanent preparations. They were divided into the following three categories: (1) juveniles: body length (without haptor) less than 0.10 mm; eye-spots not fully developed, with diffused margins, eye- spots of the anterior pair considerably smaller than these of posterior pair;, testis, cirrus, ovary, vitellaria, vagina 0.10-0.15 mm; eye-spots well developed, compact, eye-spots of the anterior pair the same size as those of the posterior pair, testis, ovary and vagina all fully formed; ckrrus and vitellaria not fully developed; (3) adults: body larger than 0. 15 mm; all sexual organs fully developed. The specimens used in the microscopic evaluation (18,633 specimens, i.e. 83.7% of the total number collected) were those which showed clear characteristics of only one of these maturation classes; those specimens with inadequate preparation, or showing transitional morphological states were not used. To examine the relationship between infection intensity and host body size, all fish were analyzed using correlation coefficients diagram of dispersion. Differences in numbers of helminths in individualgiill arches and sides (left, right) was tested using x^2. To evaluate the histopathological effects of the monogeneans on the host, an additional 30 C. urophthalmus from Mitza were collected and each infected gill filament was cut off and immediately fixed in 10% buffered formalin. Subsequently, these were embedded in paraffin wax, and sections 5 pm thick were taken from three levels of each block, and stained with haematoxylin-eosin (Sommerville 1982). RESULTS Infection level - Of 104 fish examined, 99 were infected with S. mexicanum. A total of 22,125 worms was counted, yielding a mean intensity of infection of 223 worms/fish, with a range of 5-1334 parasites (Table I). With the exeeption of April, when only one of six fish was infected, all hosts haeooured parasites, i.e. prevalence was 100%. Mean intensity of infection varied from 67 in January to 327 parasites/host in June (Table I; Fig. 1). There were no statistically significant differences in mean intensity values between individual sampling dates (P = 0.7197; Fig. 1). Monthly variation in maturation - A total of 5,735 worms (i.e. 31%) were juveniles, 6,177 (34%) immatures and 6,721 (36%) adults. Although the percentages of monogeneans in different maturation groups fluctuated between months (Fig. 2), there was no distinct pattern in the monthly variations, with the exception of dominant proportion (73%) of juvenil worms in sample from March (Fig. 2). Infeclion intensity-body length relationship Comparison of the level of infection between fish of different length groups revealed that larger fish carried heavier parasite loads (Fig. 3). TABLE I Occurrence of Sciadicleithrum mexicanum in Cichlasoma urophthalmus in Mitza, Yucatan, Mexico
Fig. 2: distribution of Sciadicleithrum mexicanum of different age groups in Cichlasoma urophthalmus from a swamp in Mitza, Yucatan, Mexico. White-juvenile worms, stippled-immature, black-mature. Numbers above bars represent wonns evaluated.
Histopathology - Parasites were found attached to epithelial cells of primary lamellae of gill filaments, where they caused slight necrosis of these cells due to both the attachment of their opisthaptor (Fig. 4) and penetration of their median hooks (anchors; Fig. 5).
DISCUSSION Since the review of Chubb (1977), in which a shortage of studies on monogeneans in the tropics was mentioned, only two papers dealing with the ecology and development of ancyrocephaline monogeneans in South and Middle America have been published (Suriano 1989a,b). Her results showed a heavy infection of the fish host, Corydoras paleatus, with Philocorydoras platensis (Suriano 1989b), and distinct seasonality in both the occurrence and maturation of this worm, with new infections restricted to December and to July (Suriano 1989b). In contrast, during the present study, no pronounced monthly variations in the occurrence or maturation of S. mexicanum were recorded and juveniles as well as mature specimens were found in all months sampled. This fact might indicate a continuous recruitment of the parasite during this period of the dry season. Nevertheless, it must be pointed out that the present observations were limited to six months, while Suri- ano's study (1989b) lasted one year. In addition, Suriano (1989a,b) studies were in a subtropical zone 2b after Chubb (1977), where pronounced fluctuations of temperature and seasons occur, whereas the present observation was performed in the tropical zone lb during the dry season, typified by relatively stable climatic conditions with only slightly increasing mean temperatures from January to May (CaSa Hidrologica de Climas 1981). The life-span of dactylogyrid monogeneans parasitizing fishes in temperate zones is repoVted to be from two to six months (Euzeby 1966). Reof the oresent study, even though preliminary seem to tally with this statement, indicating a relatively shorl life-span of the parasites.
Section through gill filamenls with attached Sciadicleithrum mexicanum worm; hematoxylin-eosin. Magnification: Fig. 4:40 x. Fig. 5:25 x.
TABLE 11 Number of parasites on hemibranches (left - L, right - R) on differera gills arches of Cichlasoma urophthalmus from Mitza
-------------------------------------------------------------
Arch 1 2 3
-------------------------------------------------------------
Months R L R L R L
-------------------------------------------------------------
Jan. 68 63 66 79 99 95
Feb. 641 655 729a 575b 596 637
Mar. 532 538 502 450 451a 302b
Apr. 16 24 19 24 23 25
May 1544 1461 1442a 1314b 1427a 1129b
Jun. 582a 478b 433 392 451 368
Total 3383a 3219b 3191s 2834b 3047a 2556b
-------------------------------------------------------------
Arch 4
-------------------------------------------------------------
Total
Months R L No.
worms
-------------------------------------------------------------
Jan. 85 53 608
Feb. 519 490 4842
Mar. 342 271 3388
Apr. 17 20 168
May 803 734 9854
Jun. 260 301 3265
-------------------------------------------------------------
Total 2026a 1869b 22,125
3895
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a, b = significant difference (P<0.05; x^2)The present study also revealed that larger fish harboured significantly higher numbers of monogeneans, but differences in infection rates between fish of individual size groups were not so markedly pronounced as in other species of monogeneans (see, e.g., Chubb 1977, Buchmann 1989, Suriano 1989b). Evaluation of attachment sites revealed lower numbers of worms on the fourth gill arch, similar to results of Mackenzie (1970). Otherwise no differences were found in the site of attachment of S. mexicanum on other gill arches of C. urophthalmus. As indicated by some authors (Mack- enzie 1970, Rohde 1981, Buchmann 1988), this site preference could be explained by smaller size (surface) of the fourth arch and, consequently, smaller area available for attachment. Higher numbers of S. mexicanum attached to gill arches on the fight side compared to that on the left side can hardly be explained. Rohde (1979) mentioned different sides of gills as possibly niches for attachment of ectoparasites, but no details have been provided about this. Sufiano (1989b) did not report any differences in microhabitat of Philocorydoras platensis on the gills of its fish host. There are several studies on the effects of monogeneans to their fish hosts (Paperna & Steinitz 1980, Wells & Cone 1990). However, almost all of these have been performed in temperate areas. Histological evaluation showed that S. mexicanum damaged tissues of the gills of C. urophthalmus almost exclusively at the site of attachment and this damage was recorded only in epithelial cells. Consequently, the pathogenic effect of attached wonns was found to be only slight. ACKNOWLEDGMENTS To the staff of the Mitza limestone factor/for permiting the collection of fish. To MSc. Leopoldina Aguirte-Macedo, Dr Jack Frazier, MSc. Miguel A Olvera-Novoa and MSc. Joaqu/n Vargas- Vazquez, all CINVESTAV-IPN Menda, for their help and advice. To critical comments of Prof. CR Kennedy, University of Exeter, England, to an early draft of the manuscript. To Dr Iva Dostailkova, University of South Bohemia, Ceske Budejovice, for statistical evaluation of the data. REFERENCES Buchmann K 1988. Spacial distribution of Pseudodactylogyrus anguillae and P. bini (Monogenea) on the gill of the European eel, Anguilla anguilla. J Fish Biol 32:801-802. Buchmann K 1989. Relationship between host size of Anguilla anguilla and the infection level of the monogeneans Pseudodactylogyrus spp. J Fish Biol 35: 599-601. Carta Hidrologica de Climas 1981. Direccion General de Geografia del Territorio Nacional. SPP, Menda, Mexico. Chubb JC 1977. Seasonal occurrence of helminths in freshwater fishes. Part 1. Monogenea. Adv Parasitol 15: 133- 199. Chubb JC 1988. A comparison of the seasonal biology of the life cycle of helminths of freshwater fishes from midlatitude and tropical conditions, p.156-163. In Diseases and Parasites in Warm Water Fish Cultures. Euzeby J 1966. Les maladies vermineuses des animaux domestiques et leurs incidences sur la pathologie humaine. Vigot Freres Editeum, Pans, 664 pp. Flores-Nava A 1990. Water resources and freshwater aquaculture development of Yucatan Mexico. Ph.D. thesis. Institute of Aquaculture, Univemity of Stirling. U.K. 338 pp. Kritsky DC, Vidal-Martinez VM, Rodriguez-Canul R 1994. Neotropical Monogenoidea. 19. Dactylogyridae of cichlids (Perciformes) from the Yucatan Peniusula, with descnptious of three new species of Sciadicleithrum Kritsky, Thacher and Boeger, 1989. J Helminthol Soc Wash 61: 26-33. Margolis L, Esch GW, Holmes JC, Kuns AM, Schad GA 1982. The use of ecological tenns in parasitology. (Report of an ad hoc committee of the American Society of Parasitologists). J Parasitol 69: 131-133. Mackenzie K 1970. Gyrodactylus unicopula Glukhova, 1955, from young plaice Pleuronectes platessa L. with notes on the ecology of the parasite. J Fish Biol 2: 23-34. Paperna I, Steinitz H 1980. Parasites, infections and diseases of fish in Africa. FAO, Rome, 216pp. Rohde K 1979. A critical evaluation of intriusic and extrinsic factors respousible for niche restriction in parasites. Am Natur 114: 648-671. Rohde K 1981. Niche width of parasites-rich and species-poor communities. Experentia 37: 359-361. Salgado-Maldonado G 1979. Procedimientos y tecnicas generales empleados en los estudios helmintologicos. Departamento de Pesca, Mexico City, 53 pp Sommerville C 1982. The pathology of Haplorchis pumilio (Looss, 1876) infectious in cultured tilapias. J Fish Dis 5: 243-250. Suriano DM 1989a. Ontogeny of Philocorydoras platensis Suriano, 1986 (Monogenea: Ancyrocephalidae) gill parasite of Corydoras paleatus (Jenyus) (Pisces: Callichthyidae) in Laguna Chascomus - Provincia de Buenos Aires - Republica Argentina. Rev Ibdr Parasitol 49:11- 18. Suriano DM 1989b. Population biology of Philocorydoras platensis Suriano, 1986 (Monogenea: Ancyrocephalidae) from Corydoras paleatus (Jenyus) (Pisees: Callichthyidae) in Laguna Chascomus, Republica Argentina. Rev Iber Parasitol 49: 19-26. Wells PR, Cone DK 1990. Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on density of mucous cells in the epidemus of fry of Oncorhynchus mykiss. J Fish Biol 37: 599- 603. Copyright 1995 Fundacao Oswaldo Cruz
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