TEMPORAL DYNAMICS OF METAZOAN PARASITE INFECTIONS IN THE WHITE MULLET MUGIL CUREMA VALENCIENNES FROM JOYUDA LAGOON, PUERTO RICO

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1 TEMPORAL DYNAMICS OF METAZOAN PARASITE INFECTIONS IN THE WHITE MULLET MUGIL CUREMA VALENCIENNES FROM JOYUDA LAGOON, PUERTO RICO JORGE R. GARCIA AND E RNEST H. WILLIAMS CEER, Marine Ecology Division University of Puerto Rico, Mayaguez, P.R Department of Marine Sciences University of Puerto Rico, Mayag/uez A BSTRACT Temporal variations of prevalence and relative density of metazoan parasites in the white mullet, Mugil curema, were monitored over a 15 month period, along with water temperature, salinity and dissolved oxygen measurements in Joyuda Lagoon, a brackish water system in southwestern Puerto Rico, Possible effects of environmental changes on the metazoan parasitology of the white mullet were examined. Also, the migratory spawning behavior of M. curema as inferred from its relative abundance, size distribution and gonad maturity index at the lagoon was documented. The periodicity displayed by the different parasitic populations was related to changes in relative abundance and sexual maturity of mullet, short-term salinity variations and interspecific associations of parasites occupying similar microhabitats within the host. Three new host-parasite associations were noted for Mugil curema: Pseudohaliotrema mugilinus Hargis (Monogenea), Metamicrocotylea macracantha Alexander (Monogenea), and Lernaeenicus longiventris Wilson (Copepoda). INTRODUCTION The importance of ecological studies in fish parasite populations has been increased by the development of aquiculture programs with freshwater and marine fishes. Artificial culture conditions enhance the transmission of some parasitic species and usually reduce the natural defense mechanism of the hosts against parasitic infections. Knowledge about fish-parasite interactions in their natural ecosystem provides useful baseline information for aquiculture research. Most studies approaching ecological aspects of fish parasite populations in natural ecosystems have been done in sub-tropical Carib J. Sci. 21(1-2) (1985) 39 and temperate areas. Meskal (1966) reported seasonal variations of parasites from the cod in coastal waters of Norway. Overstreet (1968) found significant correlations between monthly means of temperatures, salinity and size of the fish with mean numbers of parasites infecting the inshore lizardfish, Synodus foetens, from an estuarine canal in south Florida. Boxshall (1974) found a regular annual cycle of abundance in the ectoparasitic copepod Lepeophtheirus pectoralis in a population of plaice in Yorkshire. Rawson and Rogers (1972) reported seasonal abundance of monogenetic trematodes in the bluegill, Lepomis macrochirus, in a reservoir in Alabama; and Pomales and Williams (1980) for largemouth bass, Micropterus salmoides (Lacepede), in Puerto Rico. Rawson (1976) described seasonal patterns of infection in-

2 40 J. GARCIA-SAIS AND E. H. WILLIAMS tensity by five species of monogenetic trematodes in Mugil cephalus related to temperature variations in Sapelo Island, Georgia. Other studies demonstrate that differences in the habitat and geographic location are more important than seasonal variables in the parasitic composition of some fishes (Schroeder, 1970; Dowgiallo, 1979). In addition to providing baseline parasitological information about Mugil curema, the aim of this study was to test whether seasonally related factors in Joyuda Lagoon, such as salinity variations dictated the pattern of abundance in the ectoparasitic fauna of the host. The specific objectives of this study were to determine the temporal distribution and relative density of metazoan parasites in the white mullet (Mugil curema) occurring in Joyuda Lagoon; to examine the influence that changes in the external environment had on the parasitic fauna of the white mullet; to determine the effect that spawning and possible migrations of a fish had on its parasitic composition; and to evaluate the role of Joyuda Lagoon in the life cycle of the white mullet (Garcia, 1981 a). M ATERIALS AND M ETHODS The study area Joyuda Lagoon (Fig. 1 ) is a coastal brackish water system located on the southwestern coast of Puerto Rico. The lagoon is approximately 1.6 km long and 0.8 km wide, covering an area of 121 hectares. A conspicuous band of the red mangrove, Rhizophora mangle, borders the lagoon. Black mangrove, Avicenia nitida, and white mangrove, Laguncularia racemosa, also occur in the western section. Water exchanges between the lagoon and the sea through a small channel bordered by mangroves. The channel opens seaward into a sandy patch area of turtle grass and scattered coral growth. The average water depth of the lagoon is 1.3 m, with a maximum depth of approximately 4 m. The bottom substrate is soft mud sediments and organic detritus, mainly derived from the mangroves. Sampling procedures Monthly collections of fishes were made with monofilament and nylon bottom gill nets during the period of February 1979 through April The nets were set at sunset and recovered at dawn from five sta- tions. Fishes were separated according to species, number of individuals of each species noted and total number of fishes in the collection calculated. All fish of each species (or 10 of each species if more than 10 were collected) were examined for total metazoan (multicellular) parasites. Only data collected from the white mullet, Mugil curema are reported here; parasites of the other species will be reported elsewhere, Fish were placed in individual plastic bags and taken directly to the laboratory, held under refrigeration, and examined within 16 hours, Salinity, temperature and dissolved oxygen measurements were obtained every month at five stations in the lagoon. These data were recorded on sampling days at the time of setting the nets (Garcia, 1981a,b). Laboratory procedures The fish samples were taken directly from the field to the laboratory facilities at CEER. All fish were weighed and measured (standard length) and the gonads were removed and weighed. The body surface, gills and alimentary tract of the fish were examined for parasites. Numbers and species of parasites present were recorded for each gill arch. An incision was made on the right side of each fish and the organs separated and placed in petri dishes. Each organ was studied as a whole unit for metazoan parasites. A saline solution was added to the dishes to avoid drying and facilitate the examination. Observations and separation of parasites were made with a dissecting microscope. Standard procedures for relaxation, fixation and preservation of parasited were employed. Statistical analysis Prevalence and relative density of different parasitic species were noted as monthly values for the 15 month period. Prevalence represents the percentage of each species of host infected by a particular parasite in each monthly sample. Relative density is total number of a particular species of parasite divided by the total number of hosts examined (infected and uninfected) in a monthly sample (Margolis et al., 1982). A logarithmic transformation (Log 10 N) was applied to the monthly values of relative density. Simple and multiple linear regression analysis between temperature and salinity means and intensity of infection values were calculated for each species of parasite. Possible interrelations between parasitic

3 PARASITE INECTIONS IN THE WHITE MULLET 41 groups were tested for significance in 2 2 contingency tables. Exact probabilities were calculated by the formula: as suggested by Tate and Clelland (1957 for small N values of less than 40 and expected frequencies of less than 5. Data on the stage of sexual maturity were obtained by using an index of gonad development. This index is a numerical relationship between the weight of the fish and the weight of both ovaries. It is expressed as: where G.I. = Gonad Index w = Weight of both ovaries in grams W = Weight of fish in grams Relative abundance of white mullet in Joyuda Lagoon was expressed as the ratio of number of individuals of white mullet to total collection of fishes in the month. R ESULTS AND D ISCUSSION Hydrological parameters Monthly sample means and range of salinity (ppt), water temperature ( C) and dissolved oxygen (mg.l -l ) in Joyuda Lagoon are presented in Figure 2. Salinity - Average salinity in Joyuda Lagoon for the period between February 1979 and April 1980 was 19.9 ppt. Monthly sample mean values ranged between a minimum of 12.0 ppt in October 1979 to a maximum of 30.0 ppt in April Salinity was lower during the summer months (May-October), averaging 18.6 ppt, than in the winter period (November-April) averaging 20.8 ppt. The salinity pattern in the lagoon was unstable and moderate variability occured between monthly amples. Salinity was probably determined by the amount of precipitation and runoff, the temperature and wind effect on evaporation and the intrusion of sea water during high tides. Temperature- Average water temperature was C. Monthly mean values ranged between a maximum of 30.0 C in May and July 1979 and a minimum of 24.8 C in February Average water temperature was higher during summer months (May-October) with x = 28.8 C as compared to winter months (November-April) with x = 27.0 C. The grad- ual decrease in water temperature started in September and reached its lowest point by February. Water temperature in the lagoon is controlled by air temperature because of the shallow nature of the system and reduced tidal influence. Short-term variations in water temperature may occur as a result of heavy precipitation and draining of cold freshwater from the runoff of adjacent mountains. Dissolved Oxygen - The content of dissolved oxygen in the water ranged between 4.7 ppm in March 1980 and 7.2 ppm in April and December Although moderate variation occured on a monthly basis, the summer months had less variation in dissolved oxygen than the winter months. Relative abundance of white mullet in Joyuda Lagoon Highest relative abundance of white mullet in monthly samples occurred in February 1979 with 41% white mullet in a total collection of 193 fishes. Another high value was recorded in September 1979 with 32% of a sample of 49 fishes. Fig. 3 shows the monthly variation in relative abundance of white mullet. The sudden decrease in abundance of white mullet after February tends to support the theory of an offshore spawning migration of this fish (Anderson, 1957; Moore, 1974; and Yanez-Arancibia, 1976). Index of gonad development (Table 1 ) indicated that 80% of the mullet examined in February 1979 had an advanced stage of gonad development. In March 1979, all individuals examined were mature. Some mature individuals were in the collections until September. The absence of adult white mullet with gonad development in September may be indicative of a return, in part, of the white mullet population after spawning had taken place in offshore waters. Overlapping data for the months of February and March 1980 are not significant because the individuals examined were not adult fishes (Fig. 4). Low values of relative abundance after October 1979 may be due to the effect of hurricanes David and Frederick in September 1979, and to overfishing of the adult mullet population in the lagoon observed during their period of prespawning in February and March Host - parasite interactions Six species of metazoan parasites were found to infect the white mullet during the study period at Joyuda Lagoon. Temporal patterns of prevalence must be interpreted with caution due to small sample size numbers.

4 42 J. GARCIA-SAIS AND E. H. WILLIAMS The acanthocephalan parasite, Floridosentis elongatus an intestinal parasite of the fish, was present in every monthly sample. F. elongatus showed the highest prevalence in March and December 1979, and January and March 1980 (Fig. 5). The pattern of prevalence does not seem to be directly related to any external factor. Two monogenean trematodes were found parasitizing the gill filaments. Pseudohaliotrema mugilinus had the highest prevalence in February and March 1979, and in March and April This monogenean parasite was absent from August to October Nevertheless, it appeared with moderately high prevalence throughout the remainder of the study, especially during the winter period (Fig. 6). Low salinities, or perhaps the sudden decrease in salinity from August to September continuing to October 1979, could have caused the absence of this parasite during these months. Metamicrocotylea macracantha, another monogenetic trematode which infects the gill filaments, peaked in November 1979, and March 1980, and was also common in July and September 1979 and February Metamicrocotylea macracantha appears to be able to withstand the short time salinity variations which occurred in Septembe 1979 (Fig. 7) when salinity reached its lowest point during the study (approx. 12 ppt). The presence of this monogenetic trematode was not noted until May 1979, and appeared irregularly through the rest of the study suggesting that the parasite entered the lagoon either with early spawned adult females, after a sand bar formation opened in April-May 1979, or with juvenile mullet which were probably new recruits in the lagoon. However, after May 1979, the shortterm variations of prevalence may be related to other factors, either environmental, biological or both. Three species of copepods were found on the white mullet. Ergasilus lizae, which occurred on the gill filaments of the fish, had the highest prevalence in February It remained until March 1979, disappeared until October 1979, and reached another high during January 1980 (Fig. 8). Although E. lizae occurred during the winter period, its prevalence in the white mullet seems to be more related to the migratory pattern of the adult fish than to seasonally related hydrological conditions. Ergasilus lizae survived a wide range of temperature and salinity variations in Joyuda Lagoon. Its absence after March 1979 could be due to the migration of adult mullet to offshore waters. As a consequence of this migration, the individuals examined during the remaining summer months, did not possess this parasite because they were new recruits composed mostly of juvenile fish. With the next immigration of adult mullet after September 1979, it again became a regular component of the parasitic population. Lernaeenicus longiventris, was found partially embedded in the fins and body surface of the white mullet. Its prevalence shows a peak during the summer months (Fig. 9). After being absent in November and December 1979, the parasite was collected again in January 1980, reaching another peak during March The pattern of this parasitic species is again indicative of the different populations of mullet sampled during the study period. The parasite first appeared in monthly collections on smaller individuals in June 1979, one month after the apparent offshore migration of adult fish. Reduced prevalence after September 1979, probably was caused by immigration of non-infected adult mullet into the lagoon. Apparently, after being introduced by new recruits into the lagoon during the summer period, the parasite adapted well to the strongly variable hydrological conditions in the lagoon and persisted in the samples despite a change of 17 ppt in salinity between October 1979 and April 1980, as would be expected in a tissue embedded parasite which should be little influenced by external salinities. Bomolochus concinnus occurred mostly in the mucus of the branchiostegal cavity and occasionally in the branchiostegal filaments. It appear in nine out of fifteen monthly samples but showed no distinct peak of prevalence considering the sample size in March 1980 (Fig. 10). Its low prevalence during the rainy period from August to October 1979 may be indicative of low tolerance to the sudden salinity decrease associated with hurricanes David and Frederick. Table 2 presents relative density for each parasite species of M. curema for each month. The monogenean trematode of the gill filaments, P. mugilinus was the most abundant parasite with a relative density of 8.5 parasites per fish. The acanthocephalan F. elongatus had a relative density of 2.2 parasites per fish and was present in 93% of the fish examined. The copepod L. longi-

5 PARASITE INECTIONS IN THE WHITE MULLET 43 ventris caused moderate lesions in the caudal fin because it occurred deeply embedded in the pelvic and caudal fin tissues. No epizootic was observed during the study. Interactions between parasitic species Five species of external parasite and one endoparasite were present in white mullet at different time periods throughout the study. Ectoparasites which occupied similar microhabitats within the fish, such as Metamicrocotylea macracantha and Ergasilus lizae, did not occur together in any of the fishes examined. Fig. 11 shows the similarity in site selectivity of both parasitic species on the branchiostegal arches of the white mullet. The distribution of those species in monthly samples revealed a significant negative association (p=0.017). Possibly, one of these species is excluding the other for food and/or space. The presence of one species or the other in their fish host may be dictated either by water quality related factors and their adaptations to withstand environmental stress or to actual competition and consequent exclusion by one species or the other. Floridosentis elongatus, an acanthocephalan worm, was the only internal parasite observed and was present in all monthly samples. The presence of other endoparasites in the alimentary tract is probably limited by the lack of intermediate hosts such as mollusks, which are rare in Joyuda Lagoon. The possibility of competitive exclusion by the acanthocephalan is contradicted by the presence of digenetic trematodes which occur along with F. elongatus in collections of white mullet examined in La Parguera, Puerto Rico {William, E. H., unpubl. data). The consistent patterns of association between parasites constitute evidence that their temporal occurrence is real and not an artifact of sampling variability. The aspect of competition among parasitic species has been extensively discussed by Halvorsen (1976) and constitutes a significant phenomenon in the ecology of parasites. Parasite - Ecosystem interactions Simple and multiple regression analyses between monthly means of temperature and salinity and the intensity of infection by parasitic species were not significant at the 0.05 level. Evidently, most ectoparasitic species in the white mullet withstand some degree of variation in salinity and temperature (Table 3). Consequently, the spread of points in both sides of the regression lines result in high standard error and low correlation coefficients. Deterministic effects of hydrological parameters on the parasitic composition of the white mullet were observed for abrupt salinity variations in August through October Most species of external parasites had low prevalence or were absent during this period. The effect of shorterm variation is probably more important in determining the prevalence of some parasite species than seasonally related variations which are more gradually exposed to the external parasite fauna. The euryhaline behavior of external parasites in the mullet is probably a coevulationary adaptation to the behavior of the host; it is possible, however, that acute and short-term salinity variations may induce a threshold response on some species of ectoparasites in the white mullet. C ONCLUSIONS The hypothesis that ectoparasites in the white mullet (Mugil curema) display a distribution pattern which is seasonally related to salinity variations in Joyuda Lagoon, was not evident in the present study. However, the ectoparasites Bomolochus concinnus and Pseudohaliotrema mugilinus were apparently affected by the sudden drop in salinity during the rainy season. The range of tolerance shown by parasites to temperature and salinity variations is indicative of the adaptations that these animals have developed in order to withstand similar environmental gradients to which the host is adapted. The migratory behavior of adult mullets to offshore waters, and their eventual return to the lagoon, accounts for much of the variability observed in the distribution of some parasitic species. Negative interspecific interactions between parasitic species occurred between populations which occupy similar microhabitats within the host. This type of association was significant for the copepod, Ergasilus lizae, and the monogenetic trematode, Metamicrocotylea macracantha. Their actual competition and mutual exclusion may explain the short-term variations that these species present in their distribution patterns. Joyuda Lagoon is a detritus-based ecosystem with high food availability and protection for juvenile and adult white mullet. The proportion of adult white mullet is higher during winter prior to their peak of sexual maturity. This fact supports the observation

6 44 J. GARCIA-SAIS AND E. H. WILLIAMS of Yanez-Arancibia (1976) that mullet concentrate in the lagoon in order to feed extensively and store enough energy for their spawning migration. Joyuda Lagoon may also function as shelter to juvenile and adult white mullet during periods of high wave energy and low food availability in the coast. L ITERATURE CITED A NDERSON, W. W Early development, spawning, growth and ocurrence of the silver mullet (Mugil curema) along the South Atlantic coast of the United States. Fishery Bulletin. Number : B OXSHALL, G. A The population dynamics of Lepeophtheirus pectoralis (Muller): seasonal variation in abundance and age structure. Parasitology 69: DOWGIALLO, M. J Variation of metazoan parasites of the french grunt Haemulon flavolineatum (Demarest) (Osteichthyes: Pomadasyidae), by habitat type and season with an analysis of competition among parasites. Unpublished Maester Thesis, Department of Marine Sciences, University of Puerto Rico, Mayaguez, Puerto Rico, 109 p. G ARCIA, J. R. 1981a. Temporal patterns of the metazoan parasites in the white mullet, Mugil curemaa Valenciennes, from Joyuda Lagoon, Puerto Rico. Masters Thesis, Department of Marine Sciences, University of Puerto Rico, Mayagtiez, Puerto RICO, 51 p. G ARCIA, J. R. 1981b. Algunos aspectos eco1ogicos de la comunidad de peces en la Laguna Joyuda. San Juan, Puerto Rico. 8vo. Simposio del Departamento de Recursos Naturales de Puerto Rico. H ALVORSEN, O Negative interaction among parasites. In: Ecological Aspects or Parasitology, C.R. Kennedy (ed.). North-Holland Publishing Co., Armsterdam., p MARGOLIS, L., G. W. ESCH, J. C. HOLMES, A. M. KURIS, AND G. A. SCHAD The use of ecological terms in parasitology. Journal of Parasitology 68: MESKAL, F. H Seasonal fluctuations in the population of two common trematode species from the stomach of the cod. Sarcia 26: M OORE, R. H General biology, distribution and relative abundance of Mugil curema and Mugil cephalus on the south Texas coast. Contributions in Marine Science 18: O VERSTREET, R. M Parasites of the inshore lizardfish Synodus foetens, from South Florida, including a description of a new genus of Cestoda. Bulletin of Marine Science 18: PAPERNA, I. AND R. M. OVERSTREET Parasites and diseases of mullets (Mugilidae). In: H. Oren (Ed. ) Aquiculture of grey mullets. Cambridge University Press, Great Britain, p POMALES, A. D. AND E. H. WILLIAMS JR Yearly parasite variation in the temperature centrarchid, Micropterus salmoides (Lacepede), largemouth bass, twenty-eight years after introduction into a tropical environment. Journal of Parasitology 66:81. RAWSON, M. V Population biology of parasites of striped mullet, Mugil curema L. 1. Monogenea. Journal of Fisheries Biology 9: RAWSON, M. V. AND W. A. ROGERS Seasonal abundance of Arcyrocephalinaen (Monogenoidea) parasites of bluegill, Lepomis macrochirus (RAF). Journal of Wildlife Diseases 8: SCHROEDER, R. E Ecology of the intestinal trematodes of the gray snapper, Lutjanus griseus, near lower matacumbe key, Florida, with a description of a new species. Studies in tropical oceanography 10: TATE, M. W. AND R. C. CLELLAND Nonparametric and short-cut statistics. Interstate Printers and Publishers Inc., Illinois, p Y ANEZ-ARACIBIA, A Observaciones sobre Mugil curema Valenciennes en Areas naturales de crianza, Mexico. Alimentacion, crecimiento, madurez y relaciones eco1ogicas. Anales Centro Ciencias del Mar y Limnologia. Universidad Autonoma de Mexico, 3:

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8 J. GARCIA-SAIS AND E. H. WILLIAMS F IGURE 2. Monthly sample means and range of salinity, water temperature and dissolved oxygen content.

9 PARASITE INECTIONS IN THE WHITE MULLET 47 FIGURE 3. Montly variation in relative abundance of M. curema at Joyuda Lagoon. F IGURE 4. Standard length distribution of monthly collections of M. curema

10 48 J. GARCIA-SAIS AND E. H. WILLIAMS FIGURE 5. Monthly prevalence of Floridosentis elongatus on Mugil curema. FIGURE 6. Monthly prevalence of Pseudohalitrema mugilinus on Mugil curema.

11 PARASITE INECTIONS IN THE WHITE MULLET 49 FIGURE 7. Monthly prevalence of Metamicrocotylea macracantha on Mugil curema. FIGURE 8. Monthly prevalence of Ergasilus lizae on Mugil curema.

12 50 J. GARCIA-SAIS AND E. H. WILLIAMS FIGURE 9. Monthly prevalence of Lernaeenicus longiventris on Mugil curema. FIGURE 10. Monthly prevalence of Bomolochus concinnus on Mugil curema.

13 PARASITE INECTIONS IN THE WHITE MULLET 51 FIGURE 11. Distribution of individuals of Ergasilus lizae (open bars) and Metarnicrocotylea macracantha (shaded bars), mutually exclusive parasites of the gill arches of Mugil curema. TABLE 1. Index of gonad development in Mugil curema for the period between February 1979 and April FEBRUARY MARCH APRIL MAY JUNE JULY AUGUST SEPTEMBER OCTOBER X= NOVEMBER DECEMBER JANUARY FEBRUARY MARCH APRIL X=

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15 PARASITE INECTIONS IN THE WHITE MULLET 53 TABLE 3. Analyses of simple and multiple regression between monthly sample means of relative density and water temperature and salinity. 1.1 Sal Sal Temp. Temp. r; S.E. r; S.E, r; S.E. Pseudohaliotrema mugilinus.126 ; ; ; 1.07 Metamicrocotylea macracantha.116 ; ; ;.56 Ergasilus lizae.006 ; ; ;.58 Lernaeenicus longiventris.063 ; ; ;.67 Bomolochus concinnus.005 ; ; ;.49 Floridosentis elongatus.046 ; ; ;.45

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