Mem Inst Oswaldo Cruz, Rio de Janeiro, 96(2) February 2001
Original Article

Community Ecology of the Metazoan Parasites of White Croaker, Micropogonias furnieri (Osteichthyes: Sciaenidae), from the Coastal Zone of the State of Rio de Janeiro, Brazil

Dimitri R Alves
++, José L Luque

Curso de Pós-Graduação em Parasitologia Veterinária, Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Caixa Postal 74508, 23851-970 Seropédica, RJ, Brasil

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One hundred specimens of white croakers,u00a0Micropogonias furnieriu00a0(Desmarest 1823) (Osteichthyes: Sciaenidae) collected from Pedra de Guaratiba (23u00b001'S, 43u00b038'W), State of Rio de Janeiro, Brazil, from September 1997 to August 1999, were necropsied to study their parasites. The majority of the fish (95%) were parasitized by metazoan. Twenty-eight species of parasites were collected. The nematodes were the 40.5% of the total number of parasites specimens collected.u00a0Dichelyne elongatusu00a0was the most dominant species. Lobatostoma ringens, Pterinotrematoides mexicanum, Corynosoma australe, D. elongatus, andu00a0Caligus haemulonisu00a0showed a positive correlation between the host's total length and parasite prevalence and abundance. The monogeneanu00a0P. mexicanumu00a0had differences in the prevalence and abundance in relation to sex of the host. The mean diversity in the infracommunities ofu00a0M. furnieriu00a0was H=0.499±0.411, with correlation with the host's total length and without differences in relation to sex of the host. One pair of ectoparasites showed positive covariation, and two pairs of endoparasites showed positive association and covariation between their prevalences and abundances, respectively. Negative association or covariations were not found. The dominance of endoparasites in the croakers parasite infracommunities reinforced the differences found in sciaenids from the South American Pacific Ocean, in which the ectoparasites are dominant.

Micropogonias furnieri (Desmarest 1823) is a demersal and benthic sciaenid fish with known distribution from Gulf of Mexico, Antilles to Gulf of San Matías, Argentina (Menezes & Figueiredo 1980). In the life cycle of M. furnieri, the juvenile individuals migrate to estuarine areas and the adults reach the adjacent coastal zone to reproduce (Vazzoler 1991). M. furnieri is very common in the southern Brazilian coastal zone and has significant commercial importance.

Several taxonomic papers on the parasites of M. furnieri from Brazil were published: Amato (1983a, b), Fabio (1988), Fernandes and Goulart (1992), Pereira Jr. et al. (1996), Alves and Luque (2000a) on digeneans and aspidobothreans; Kohn et al. (1989), Alves and Luque (2000a) on monogeneans; Oliveira (1985), São Clemente (1986a, 1987), Pereira Jr. (1993) and Alves and Luque (2000a) on cestodes; Pereira Jr. and Neves (1993) and Alves and Luque (2000a) on acanthocephalans; Pereira Jr. and Costa (1996), Alves and Luque (2000a) on nematodes. Additional taxonomic records of parasites of Mfurnieri in the South American Atlantic Ocean were made by Suriano (1966, 1975) from Argentina, and Vicente et al. (1989) from Venezuelan coastal zone.

Studies on quantitative aspects of the parasites of M. furnieri from the Brazilian coastal zone were restricted to larval stages of trypanorhynch cestodes and acanthocephalan (São Clemente 1986b, Pereira Jr. 1993, Pereira Jr. & Neves 1993). Recently, Alves and Luque (1999, 2000b) made preliminary quantitative studies, at the parasite infrapopulation level, in adult and juvenile M. furnieri from the State of Rio de Janeiro. Additional quantitative studies of parasites of M.furnieri from the South American Atlantic Ocean were made by Suriano (1966), Sardella et al. (1995), and Rohde et al. (1995) from Argentina.

Other Brazilian sciaenid fishes were studied for quantitative and ecological aspects of their parasites: Oliveira (1985) recorded quantitative aspects of the infection by trypanorhynch larval in Macrodon ancylodon (Bloch) from the State of Rio Grande do Sul, and Cezar and Amato (1998) recorded infection by cystacanths of Corynosoma sp. in Umbrina canosai Berg from the State of Rio Grande do Sul. Chaves and Luque (2000) studied the parasite community ofMenticirrhus ame-ricanus Linnaeus from the State of Rio de Janeiro, Brazil. Recently, Luque and Oliva (1999) made an amphi-oceanic comparative analysis with the parasite infracommunities of M. americanus from Rio de Janeiro and M. ophicephalus Jenyns from Lima, Peru.

In this report, we analyzed the metazoan parasite community of M. furnieri from the coastal zone of the State of Rio de Janeiro, at the component and infracommunity levels, and compared our results with those on the parasite communities of marine sciaenid fishes from the Neotropical region.



From September 1997 to August 1999, 100 specimens of M. furnieri were examined. Local fishermen collected fish from Pedra de Guaratiba (23°01'S, 43°38'W), coastal zone of the State of Rio de Janeiro, Brazil. Fishes were identified according to Menezes and Figueiredo (1980) and measured 10_66 cm (mean=33.2±16.4 cm) in total length. The average total length of male (29.3±14.9 cm, n=53) and female (37.6±17.2 cm, n=47) fishes in the study sample were significantly different (t= 2.589, P=0.011).

The analysis included only parasite species with prevalence greater than 10% (Bush et al. 1990). The quotient between variance and mean of parasite abundance (index of dispersion) was used to determine distribution patterns. Overdispersion or degree of aggregation was determined with the Green index (Ludwig & Reynolds 1988). The dominance frequency and the relative dominance (number of specimens of one species/total number of specimens of all species in the infracommunity) of each parasite species were calculated according to Rohde et al. (1995). Spearman's rank correlation coefficient rs was calculated to determine possible correlations between the total length of hosts and abundance of parasites. Pearson's correlation coefficient was used as an indication of the relationship between the host's total length and the prevalence of parasites, with previous arcsine transformation of the prevalence data (Zar 1996) and partition of host samples into three length intervals, according to Haimovici (1987) and Pereira Jr. (1993). The effect of host sex on abundance and prevalence of parasites was tested using the Z normal approximation to the Mann-Whitney test and the Fisher exact test, respectively. Parasite species diversity was calculated using the Brillouin index (H), because each fish analyzed corresponded to a fully censused community (Zar 1996). The probable variation of diversity in relation to host sex (Mann-Whitney test) and to host total length (Spearman's rank correlation coefficient) was tested. For each infracommunity, the evenness (Brillouin-based evenness index) was calculated. The possible interspecific association between concurrent species was determined using the chi-square test. Possible covariation among the abundance of concurrent species was analyzed using the Spearman rank correlation coefficient. Ecological terminology follows Bush et al. (1997). Statistical significance level was evaluated at P<0.05.

Voucher specimens of helminths were deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil; copepods were deposited in the Coleção de Crustacea do Museu Nacional (MNRJ), Quinta da Boa Vista, Rio de Janeiro, RJ, Brazil.



Component community - Twenty-eight species of metazoan parasites were collected (Table I). Nematodes were the most abundant with five species and they accounted for 40.5% of the total parasites collected. Dichelyne elongatus (Tornquist) was the dominant species, with 601 specimens collected (36.8% of all parasites); and showed the highest values of mean relative dominance and frequency of dominance (Table II). All parasites of M. furnieri had the typical overdispersed pattern of distribution observed in many parasite systems. Cystacanths of Corynosoma australe Johnston showed the highest values of dispersion indices (Table III).

Abundance and prevalence of Lobatostoma ringens (Linton), Pterinotrematoides mexicanum Caballero and Bravo-Hollis, C. australe, D. elongatus, and Caligus haemulonis Krøyer were positively correlated with the host total length (Tables IV, V). The mean abundance and the prevalence of P. mexicanum were significant higher in the female (5.8 and 46.8%) than in the male (1.6 and 26.4%) hosts (= -2.605, = 0.009; = 0.039).

Infracommunities - Ninety-five percent of croakers were parasitized by at least one parasite species. A total of 1,631 individual parasites was collected, with mean of 16.3 parasites/fish. The values of the dispersion and Green indices for the total individual parasites were 36.828 and 0.382, respectively. Relationships between the total parasite abundance and the total body length (rs = 0.784, P<0.001) of fish were observed. The mean parasite species richness 2.9±2 (1-9), was correlated with total body length of fish (rs = 0.698, P<0.001). Twenty hosts (20%) showed infection with one parasite species and 30 (30%), 12 (12%), 14 (14%), 9 (9%), 5 (5%), 0 (0%), 4 (4%) and 1 (1%) had multiple infections with 2, 3, 4, 5, 6, 7, 8 and 9 parasite species, respectively. The mean parasite species diversity (H) was 0.499±0.411 and the maximum diversity was 1.383. The Brillouin-based evenness index (J) had a mean of 0.533±0.355. Parasite diversity was correlated to host total length (rs=0.652; P<0.001) and no significant differences (= -1.820, = 0.071) in parasite diversity were observed between male (= 0.431±0.391) and female croakers (= 0.578±0.423).

Parasite infracommunities were separated into two groups _ ectoparasites (monogeneans and copepods) and adult endoparasites (aspidobothrid, digeneans acanthocephalans and nematodes) _ to determine possible interspecific associations. Larval stages were not included in this analysis because only one species (C. australe) showed prevalence higher than 10%. Among the ectoparasites, only one species pair, P. mexicanum and C. haemulonis, shared significant positive covariation (Table VI). The infracommunities of endoparasites had one pair of species that exhibited significant positive association and covariation, L. ringens and D. elongatus (Table VII).



The present study detected some patterns in the structure of the infracommunities of metazoan parasites of M. furnieri: (1) endoparasite dominance; (2) correlation of parasite abundance at the infracommunity level with the size of the host; and (3) low number of parasite species associated pairs.

The nematodes (adult and larval stages) were the main component of the parasite infracommu-nities of M. furnieri. The feeding habits and wide diet spectrum of demersal fishes, bringing them in contact with several potential intermediate hosts of marine digenean, acanthocephalan and nematodes, might favor the presence of endoparasites in fishes. M. furnieri has a highly diversified diet with components of the demersal and benthic communities, and with polychaetes as most frequent item (Amaral & Migotto 1980, Vazzoler 1991).

Helminth larval stages infecting M. furnieri may show the possible intermediate trophic level of this fish and may be part of the diet of marine mammal or birds (definitive hosts of C. australe and anisakids), and elasmobranch fishes (definitive hosts of tetraphyllidean and trypanorhynch cestodes). The highest values of dispersion of C. australe cystacanths detected in M. furnieri from the State of Rio de Janeiroare in agreement with the results obtained by Pereira Jr. and Neves (1993) and Sardella et al. (1995) in M. furnieri from Brazil and Argentina, respectively; and by Cezar and Amato (1998) in U. canosai from Brazil.

The prevalence and abundance of helminth larval stages recorded in this paper were lower than the ones recorded by São Clemente (1986b), Oliveira (1985) and Pereira Jr. (1993) for trypanorhynch cestodes in M. furnieri from the States of Rio de Janeiro and Rio Grande do Sul, and by Pereira Jr. and Neves (1993) for C. australe in Rio Grande do Sul. According to Fernandez and Esch (1991a, b) the role of the parasite species in their communities would be studied considering their particular distribution strategies. Infections by trypanorhynch cestodes and polymorphid acanthocephalans in marine fishes are strongly influenced by the diet of the fishes and mainly by the regional distribution and density of the hosts (George-Nascimento 1987). Also, differences with data furnished by São Clemente (1986b) from the State of Rio de Janeiro, might be attributed to local changes in distribution of the hosts along the time. Kennedy (1990, 1993) stated that the majority of studies on parasite ecology is restricted to short period times, under three years. This situation can be considered a limiting factor to detect community and population patterns, because ecological perturbations and changes are also influencing the composition and density of the host communities. Moreover, the host samples studied by São Clemente (1986b) were highly heterogeneous because were collected subsamples from ten localities from Rio de Janeiro, including Cabo Frio, locality strongly influenced by an upwelling system (Valentin 1994).

According to Vazzoler (1991) and Haimovici et al. (1994), the populations of M. furnieri along the Brazilian coastal zone showed different patterns of relative abundance, aggregation and behavior, possibly originated by the influence of the southern Brazil Subtropical Convergence Ecosystem. These ecological differences might explain the highest parasitism level by larval stages of cestodes and acanthocephalans in M. furnieri from the coastal zone of Rio Grande do Sul, recorded by Oliveira (1985), Pereira Jr. (1993), and Pereira Jr. and Neves (1993). M. furnieri from Rio Grande do Sul has higher population density (sometimes in 8:1 rate) than the white croaker populations from the coastal zone of the State of Rio de Janeiro (Vazzoler 1991, Haimovici & Umpierre 1996). This factor appears to be one of the responsible for the high level of prevalence and abundance by C. australe in white croakers from Rio Grande do Sul. Cezar and Amato (1998) also recorded high values of prevalence and abundance of Corynosoma sp. cystacanths in U. canosai, another sciaenid fish common in the coastal zone of Rio Grande do Sul, with high similarity with M. furnieri in their feeding habits (Vazzoler 1975).

The correlation among the total length of M. furnieri and the prevalence and abundance of several parasite species, possibly originated by accumulative infection. This is a pattern anteriorly found in other marine fishes from Rio de Janeiro (Luque et al. 1996, Knoff et al. 1997, Luque & Chaves 1999). The digeneans Lecithochirium microstomum Chandler andPachycreadium gastrocotylum (Manter) were exceptions, with the highest values of prevalence and abundance in the intermediate length class, when the fish inhabiting 25-30 m deep-waters. As pointed out in the classic study by Polyanski (1961), quantitative and qualitative changes in parasitism are expected with the fish growth. In the case of the digeneans, this relationship is strongly influenced by changes in the feeding habits of the fish correlated with the age (Saad-Fares & Combes 1992). M. furnieri along its life cycle inhabits three different ecosystems and has strongly changes in its diet composition (Vazzoler 1991).

The correlation of the sex of M. furnieri with the abundance and prevalence of the monogenean P. mexicanum was surprising because differences in biological conditions of male and female croakers are unknown. However, this pattern can be explained because of the prevalence and the abundance of this parasite were positively correlated with host's total length. Moreover, the lengths of male and female croakers were significantly different; thus, this relationship is confounded with the apparent inequalities between female and male infection levels. A similar situation was detected inM. americanus, with the monogenean Rham-nocercus stichospinus Seamster and Monaco, but in this case, the total lengths of female and male hosts were not significantly different (Chaves & Luque 2000). Quantitative relationships of the sex of the host with the infection levels of some components of the parasite infracommunities were also detected in other benthic fishes from Brazil (Luque et al. 1996, Knoff et al. 1997).

The low number of parasite species associated pairs detected in M. furnieri is in agreement with the data obtained from other Neotropical sciaenids fishes, where was observed dominance of generalist species (Luque 1996, Oliva & Luque 1998, Chaves & Luque 2000). However, these data could be used with caution to explain the parasite community structure. According to Rohde et al. (1995), interspecific relationships only can be considered valid when are tested under experimental conditions.

Chaves and Luque (2000) studied the structure of the parasite infracommunities in 115 M. americanus from the State of Rio de Janeiro. Some patterns observed were similar to M. furnieri, but some quantitative differences were detected: M. americanus showed mean parasite richness and parasite diversity higher than M. furnieri, and the mean parasite abundance and prevalence were higher in M. furnieri at the infracommunity level. These differences might be attributed to differences in the ecological relationships (behavior, habitat, and diet) recorded for M. americanus, benthic, inhabiting shallow, "surf-zone" waters (Lunardonet al.1991), and M. furnieri, benthic-demersal, inhabiting deeper waters (Vazzoler 1991) from Brazil.

Some of the patterns detected by Thoney (1991, 1993) in the parasite infracommunities of M. undulatus (Linnaeus) from North American Atlantic Ocean, are close to those detected in M. furnieri. According to Thoney (1991, 1993), the parasite community of M. undulatus is dominated by endoparasites and the young fishes showed similar parasite diversity in relation to adults croakers, but the parasites recorded by Thoney (1991, 1993) showed higher values of prevalence and parasite abundance. Luque (1996), and Oliva and Luque (1998) studied the characteristics of the parasite infracommunities in five sciaenids from Peru, in the South American Pacific Ocean. These sciaenids showed absolute dominance by ectoparasites, mainly diplectanid monogeneans and lerneopodid copepods, while M. americanus and M. furnieri from South American Atlantic Ocean had dominance by endoparasites. Luque and Oliva (1999) discussed these amphi-oceanic differences for M. ophicephalus (Pacific Ocean) and M. americanus (Atlantic Ocean). The parasite community of M. furnieri can be included as another example of these differences.



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+Corresponding author and CNPq researcher. Fax: +55-21-682.1617.
++CAPES fellowship
Received 19 January 2000
Accepted 20 August 2000
This work was partially supported by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro.

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