The metazoan parasite community of the barred grunt Conodon nobilis (Actinopterygii: Haemulidae) from the coast off Rio de Janeiro, southeastern Brazil

Comunidade de metazoários parasitos do roncador Conodon nobilis (Actinopterygii: Haemulidae) na costa do Rio de Janeiro, sudeste do Brasil

Abstract

The barred grunt, Conodon nobilis (Linnaeus, 1758), is one of the most important marine-estuarine fish along the Brazilian coast. The present study evaluated the parasite fauna of this haemulid fish along the Southern Atlantic coast. From September 2010 to July 2011, a total of 100 specimens of C. nobilis from Angra dos Reis, Rio de Janeiro State, Brazil (23°01′21ʺS, 44°19′13ʺW), were examined. Ninety-seven individuals were parasitized by at least one species of metazoan, with a mean of 4.50 ± 3.54 parasites per fish. Eighteen species of parasites were collected: eight copepods, four digeneans, two cestodes, one acanthocephalan, one aspidogastrean, one isopod and one monogenean. The copepod Lernanthropus rathbuni was the most abundant and dominant species, accounting for 17.77% of all parasite specimens collected. Caligus haemulonis was the most prevalent. Prevalence and abundance of Acantholochus lamellatus and L. rathbuni tended to be higher in smaller fish, whereas those of Torticaecum sp. were higher in larger fish. The mean abundance of C. haemulonis was significantly higher in male hosts. A negative association was observed between two species of ectoparasites. The parasite community of C. nobilis was characterized by dominance of copepods, which can be related to host’s schooling behavior.

Keywords:  Haemulids; marine fish; helminths; parasitic crustaceans; community structure; parasite ecology

Resumo

O roncador, Conodon nobilis (Linnaeus, 1758) é um dos peixes marinho-estuarinos mais importantes do litoral do Brasil. O presente estudo avaliou a fauna parasitária desse peixe, na costa sul do Atlântico. Entre setembro de 2010 a julho de 2011, um total de 100 espécimes de C. nobilis, da costa de Angra dos Reis, Rio de Janeiro, Brasil (23°01′21ʺS, 44°19′13ʺO), foram examinados. Noventa e sete indivíduos estavam parasitados por pelo menos uma espécie de metazoário, com média de 4,50 ± 3,54 parasitos por peixe. Dezoito espécies de parasitos foram coletadas: oito copépodes, quatro digenéticos, dois cestóides, um acantocéfalo, um aspidogastrídeo, um isópode e um monogenético. O copépode L. rathbuni foi a espécie mais abundante e dominante, representando 17,77% do total de parasitos coletados. Caligus haemulonis foi a espécie mais prevalente. A prevalência e abundância de A. lamellatus, L. rathbuni tenderam a ser maiores nos peixes menores, enquanto os valores de Torticaecum sp. maiores em peixes maiores. A abundância média de C. haemulonis foi significativamente maior em hospedeiros do sexo masculino. Associação negativa foi observada entre duas espécies de ectoparasitos. A comunidade parasitária de C. nobilis foi caracterizada pela dominância de copépodes, fato que pode estar relacionado ao comportamento de cardume do hospedeiro.

Palavras-chave:  Haemulideos; peixe marinho; helmintos; crustáceos parasitos; estrutura da comunidade; ecologia parasitária

Introduction

The Brazilian Atlantic coast extends for more than 8,000 km and supports about 1,240 fish species, of which 25 are haemulids (Euparcaria: Haemulidae) belonging to eight genera (Froese & Pauly, 2024). The coastal zone of the state of Rio de Janeiro is one of the largest in Brazil, with 636 km of extension. It forms an important aquatic ecosystem, composed of heterogeneous environments that contain highly diverse marine and estuarine organisms (Araújo et al., 2002; Kjerfve et al., 2021; Souza et al., 2021). However, with the expansion of urbanization and industrial development, anthropic activities have been causing diffuse pollution and a consequent decreased biodiversity off the coast of Rio de Janeiro (Araújo et al., 2017; Souza et al., 2021; Benicio et al., 2022).

Commonly known as grunts, haemulids are a typical group of actinopterygian fish, currently including 137 species from 21 genera, with broad global distribution, mainly inhabiting tropical and subtropical marine waters, while occasionally occurring in brackish water but rarely in freshwater (Nelson et al., 2016; Motta-Neto et al., 2019; Fricke et al., 2024). The genus Conodon Cuvier, 1830 is composed of only three species, all occurring in American marine ecosystems, of which Conodon macrops Hildebrand, 1946 and Conodon serrifer Jordan & Gilbert, 1882 are found in the Pacific Ocean (Froese & Pauly, 2024). The barred grunt Conodon nobilis (Linnaeus, 1758) is the only species occurring in the Atlantic Ocean, with distribution from the Caribbean (coast of Texas, eastern Florida and Jamaica) to Argentina (Froese & Pauly, 2024). Regarding biology, it is a demersal fish, found along sandy shores and over shallow muddy bottoms, feeding on crustaceans, mollusks and small fish (Menezes & Figueiredo, 1980; Froese & Pauly, 2024). In Brazilian waters, C. nobilis is not targeted by local fishers, although it has an important ecological role as a biotic vector, carrying organic matter from reefs to adjacent areas, as well as forming an important link in the coastal food web (Pombo et al., 2014; Da Silva et al., 2019; Motta-Neto et al., 2019).

Currently, more than 240 species of parasites have been recorded in haemulid fish in the coastal zone of North and South America, which indicates the high potential biodiversity of these organisms (Paschoal et al., 2015, 2022; López-Zacarías et al., 2021; García-Teh et al., 2022; Guillén-Hernández et al., 2023). In the South Atlantic Ocean, studies of the community of metazoan parasites of haemulids have been conducted only by Luque et al. (1996a, b), on the parasite fauna of Orthopristis rubra (Cuvier, 1830) and Haemulon atlanticus Carvalho, Marceniuk, Oliveira and Wosiacki, 2020 (reported as H. steindachneri), off Rio de Janeiro, Brazil. Recently, Paschoal et al. (2023) evaluated the parasite communities of three species of haemulid fish – Anisotremus virginicus (Linnaeus, 1758), C. nobilis and O. rubra – in the coastal waters of Rio de Janeiro, Brazil, using a comparative approach.

Based on the ecological importance of haemulid fish, specifically that of C. nobilis, in marine systems, and the scarcity of studies of the parasites of these organisms in Brazil, we analyzed the community structure of metazoan parasites of C. nobilis, in the coastal zone of Rio de Janeiro.

Materials and Methods

Host collection, processing and parasitological procedures

From September 2010 to July 2011, 100 specimens of C. nobilis were obtained along the coast of the city of Angra dos Reis (23°01′21ʺS, 44°19′13ʺW), state of Rio de Janeiro. The fish had been caught by local fishermen and were purchased at a local market. These were mostly fresh, but some were kept frozen at -20 °C until examination. The specimens were identified according to Menezes & Figueiredo (1980). The nomenclature and classification were updated according to FishBase (Froese & Pauly, 2024). Each fish was measured (total length), weighed and sexed. The Student t-test was used to verify possible differences in total length (data were normally distributed) between males and females, since parasite burdens can be correlated with host length (Zar, 2010).

Body surface, nostrils, gills, body cavities, esophagus, stomach, intestine, mesenteries, heart, liver, gonads, swim bladder and musculature of C. nobilis were individually examined for parasites, using a stereomicroscope. Parasite collection and processing were performed according to standard protocols (Eiras et al., 2006). Their identification followed the specific literature pertinent to each taxon.

Ecological and statistical analyses

Prevalence, mean intensity and mean abundance were used as descriptors of the parasite population (at the component population level), according to Bush et al. (1997). The variance-to-mean ratio of parasite abundance (index of dispersion, ID) and the discrepancy index (D) were used to evaluate the distribution patterns of parasites in the host population (Poulin, 1993). The frequency of dominance (percentage of infracommunities in which a parasite species was numerically dominant) and the relative dominance (number of individuals of one species / total number of individuals of all species in the infracommunity) were calculated according to Rohde et al. (1995).

The parasite diversity was calculated using the Brillouin index (HB), because theoretically each fish analyzed corresponded to a fully censused infracommunity (Magurran, 2004; Zar, 2010). Differences in parasite prevalence and abundance between male and female fish were evaluated using Fisher’s exact test (F) and the corrected normal approximation of the Mann-Whitney test (Zc), respectively (Magurran, 2004; Zar, 2010). Difference in parasite diversity according to host sex was also analyzed by the Mann-Whitney test (Magurran, 2004; Zar, 2010). Spearman’s rank correlation coefficient (rs) was used to verify the association (or its lack) of host length with parasite abundance, richness and diversity (Magurran, 2004; Zar, 2010). Host samples were also divided into three length intervals, namely: Class I - < 20.7 cm (immature), Class II - 20.8 cm – 27.9 cm (initial maturity); and Class III - > 28 cm (mature) (see Silva et al., 2019), in order to better evaluate some parasitological indicators according to fish maturity. Since the individuals of Class I were not parasitized, we excluded them from the analysis. Therefore, to test differences of parasite prevalence and abundance between host individuals from Class II and III, Fisher’s exact and Mann-Whitney tests were used, respectively, as previously indicated (Zar, 2010). To evaluate possible effects of concurrent infection (endoparasites) or infestation (ectoparasites), parasites were separated into three groups according to spatial guilds, as follows: adult endoparasites (digeneans infecting the stomach); helminth larval stages (digenean metacercariae and acanthocephalan cystacanths infecting the intestine); and adult ectoparasites (copepods infesting gills and operculum). Then, possible interspecific interferences involving the presence/absence of parasites were evaluated using logistic models, and possible association with interspecific parasite abundance was evaluated using Poisson regression models (Dohoo et al., 2003; Zar, 2010).

The odds ratio (OR) of the statistically significant models (with 95% confidence interval [CI] for OR) was calculated in order to confirm its validity and evaluate the association between variables, in which 0 < OR < 1 indicates negative association, OR = 1 lack of association (invalid model) and OR > 1 denotes positive association (Dohoo et al., 2003). The ecological terminology follows that of Bush et al., (1997) and the analysis included only parasite species with prevalence higher than 10% (Bush et al., 1990). The statistical significance level was p ≤ 0.05. Statistical analyses were performed using the Quantitative Parasitology software (web version QPweb) (Reiczigel et al., 2019) and R software (R Core Team, 2020).

Results

Host samples

Fish mean total body length was 29.79 ± 5.14 (19.6-38.4) cm, and the mean weight was 430.13 ± 211.10 (94.5-880.7) g. The mean total body length of females was (28.92 ± 5.18, n = 56) and that of males was (30.91 ± 4.93, n = 44). The body lengths of males and females were not statistically different (t = 1.946, p = 0.629).

Parasite component community

The parasite community of C. nobilis was composed of 18 species of metazoans (Table 1). The copepod Lernanthropus rathbuni Wilson, 1922 was the most abundant and dominant species, accounting for 17.77% of the total parasite specimens collected, with the highest mean relative dominance and frequency of dominance (Table 2). The copepod Caligus haemulonis Krøyer, 1863 was the most prevalent species (see Table 1).

Table 1
Metazoan parasites of Conodon nobilis associated with their parasitological descriptors, total number of individuals (TNI) and site of infection or infestation (Site), in the coast off Rio de Janeiro, Brazil.

Parasite species	Parasitological descriptors			TNI	Site
	P (%)	MI ± SD	MA ± SD
Digenea
Aponurus laguncula	27	2.03 ± 1.37	0.55 ± 1.14	55	Stomach
Genolopa ampullacea	5	2.21 ± 0.83	0.11 ± 0.51	11	Stomach
Parahemiurus merus	13	2.07 ± 1.55	0.27 ± 0.88	27	Stomach
Torticaecum sp. (matacercariae)	23	1.95 ± 1.58	0.45 ± 1.11	45	Intestine
Aspidogastrea
Lobatostoma ringens	2	4	0.08 ± 0.56	08	Intestine
Cestoda
Calliterarhynchus sp. (plerocercoid)	7	1.14 ± 0.37	0.08 ± 0.30	08	Mesentery
Pterobothrium sp. (plerocercoid)	4	1	0.04 ± 0.19	04	Mesentery
Monogenea
Encotyllabe spari	6	1	0.06 ± 0.23	06	Pharynx
Acanthocephala
Serrassentis sp. (cystacanth)	12	1.16 ± 0.38	0.14 ± 0.40	14	Intestine
Copepoda
Acantholochus lamellatus	32	2.03 ± 1.25	0.65 ± 1.18	65	Gills
Caligus haemulonis	39	1.89 ± 1.42	0.74 ± 1.28	74	Operculum
Caligus longipedis	1	1	0.01	01	Operculum
Caligus robustus	10	1.2 ± 0.42	0.12 ± 0.38	12	Operculum
Caligus rufimaculatus	2	1	0.02	02	Operculum
Caligus xystercus	2	1.5 ± 0.70	0.03 ± 0.22	03	Operculum
Hamaticolax sp.	1	1	0.02	02	Nostril
Lernanthropus rathbuni	37	2.16 ± 1.80	0.81 ± 1.51	80	Gills
Isopoda
Gnathia sp. (larval)	8	4.12 ± 3.56	0.33 ± 1.47	33	Operculum

• P: prevalence; MI: mean intensity; MA: mean abundance; SD: standard deviation.

Table 2
Frequency of dominance and mean relative dominance of metazoan parasites of Conodon nobilis from the coast off Rio de Janeiro, Brazil.

Parasite species	Frequency of dominance	Frequency of dominance shared with one or more species	Mean relative dominance
Lernanthropus rathbuni	17	8	0.179 ± 0.343
Caligus haemulonis	13	9	0.129 ± 0.272
Acantholochus lamellatus	10	10	0.110 ± 0.240
Aponurus laguncula	7	11	0.081 ± 0.184
Torticaecum sp. (metacercariae)	7	5	0.071 ± 0.214
Parahemiurus merus	4	4	0.036 ± 0.142
Serrassentis sp. (cystacanth)	1	3	0.020 ± 0.117

Adult ectoparasites corresponded to 54.44% of all parasite specimens collected, adult endoparasites to 22.44%, larval endoparasites to 15.77% and larval ectoparasites to 7.33%. All parasites of C. nobilis showed the typical aggregate distribution, in which ID and D values were higher than 1.46 and 0.70, respectively (Table 3). The abundance of the copepods L. rathbuni and Acantholochus lamellatus Paschoal, Cezar and Luque, 2013 was negatively correlated with host total body length (rs = -0.23, p = 0.02; rs = -0.20, p = 0.04, respectively), and their abundance (p = 0.007 and p = 0.001, respectively) and prevalence (p = 0.003 and p = 0.002, respectively) were higher in hosts from Class II (Table 4). Regarding endoparasites, the abundance of the digenean Torticaecum sp. was positively correlated with host total length (rs = 0.21, p = 0.03), and its abundance (p = 0.025) and prevalence (p = 0.005) were higher in fish from Class III. The digenean Parahemiurus merus (Linton, 1910) was also more prevalent in hosts from Class III (p = 0.040) (Table 4). The mean abundance of C. haemulonis was significantly higher in male (1.068 ± 1.065) than in female (0.482 ± 0.894) hosts (Zc= 2.23, p = 0.025).

Table 3
Measurements for parasite dispersion within host population, indicated by variance to mean ratio (ID) and index of Discrepancy (D) of metazoan parasites of Conodon nobilis, from the coast off Rio de Janeiro, Brazil.

Parasite species	ID	D	Type of dispersion
Acantholochus lamellatus	2.16	0.774	Aggregate
Aponurus laguncula	2.41	0.808	Aggregate
Caligus haemulonis	2.23	0.737	Aggregate
Lernanthropus rathbuni	2.85	0.756	Aggregate
Parahemiurus merus	2.91	0.907	Aggregate
Serrassentis sp. (cystacanth)	1.46	0.885	Aggregate
Torticaecum sp. (metacercariae)	2.76	0.841	Aggregate

Table 4
Prevalence and mean abundance of metazoan parasites of Conodon nobilis from the coast off Rio de Janeiro, Brazil, associated with hosts body length classes.

Parasite species	Class I (n=03)		Class II (n=30)		Class III (n=67)
	P(%)	MA	P(%)	MA ± SD	P(%)	MA ± SD
Lernanthropus rathbuni	-	-	60*	1.66 ± 2.29**	28.3*	0.44 ± 0.78**
Acantholochus lamellatus	-	-	60*	1.23 ± 1.41**	20.8*	0.41 ± 1**
Caligus haemulonis	-	-	36.6	0.53 ± 0.89	41.7	0.86 ± 1.43
Aponurus laguncula	-	-	26.6	0.43 ± 0.81	28.3	0.62 ± 1.28
Torticaecum sp. (metacercariae)	-	-	6.6*	0.10 ± 0.40**	31.3*	0.62 ± 1.30**
Serrassentis sp. (cystacanth)	-	-	6.6	0.06 ± 0.25	14.9	0.17 ± 0.45
Parahemiurus merus	-	-	3.3*	0.03 ± 0.18	17.9*	0.38 ± 1.05

• P: prevalence; MA: mean abundance; SD: standard deviation; significant differences of the parasite prevalence* and abundance** among the host length classes.

Parasite infracommunities

Ninety-seven specimens (97%) of C. nobilis were parasitized by at least one taxon of metazoan. A total of 450 parasite specimens were collected, with a mean of 4.50 ± 3.54 per host. The total body length of fish and parasite abundance were not correlated (rs = 0.027, p = 0.782). The mean species richness of parasites was 2.32 ± 1.25, and also was not correlated with host total body length (rs = 0.053, p = 0.595). Similarly, mean parasite diversity (HB = 0.411 ± 0.336) was not correlated with host body length (rs = 0.103, p = 0.306), and no significant differences regarding this descriptor were observed between male (HB = 0.418 ± 0.351) and female (HB = 0.406 ± 0.327) hosts (Zc = 0.277, p = 0.390). Twenty-eight host specimens (28%) were infected/infested by a single parasite species; 25 (25%) by two, 29 (29%) by three, 9 (9%) by four, 5 (5%) by five and 1 (1%) by six species.

Interspecific associations among the adult digeneans were possible to evaluate only between the species Aponurus laguncula Looss, 1907 and P. merus. However, no apparent interaction was observed, since their presence/absence and their abundances were not correlated according to the statistical models (p = 0.104 and p = 0.743, respectively). Similar results were observed in concurrent infections by larval forms of Torticaecum sp. and Serrassentis sp. (p = 0.861 and p = 0.318, respectively). Concurrent infestations by copepods were observed among three species, A. lamellatus, C. haemulonis and L. rathbuni, which occurred in permuted pairs. However, the only possible interspecific interaction was observed between C. haemulonis and L. rathbuni, in which the abundances showed negative association (p = 0.036; OR = 0.766; CI = 0.597–0.983).

Discussion

Previous studies of the parasite fauna of C. nobilis have reported 23 taxa (larvae and adults) in the Atlantic Ocean, including Copepoda (10), Digenea (6), Cestoda (2), Acantocephala (1), Aspidogastrea (1), Isopoda (1), Monogenea (1) and Nematoda (1), of which 20 (87%) of these taxa have been reported in Brazil, 2 (8.6%) in the Bahamas and 1 (4.3%) in Puerto Rico (Paschoal et al., 2015, 2023). All parasites found in the present study have been recorded parasitizing C. nobilis, but no previous study has investigated its parasite community structure or any other congener. Therefore, these results indicate C. nobilis has a highly diverse parasite fauna and is a relevant target for investigation to better comprehend these organisms, especially regarding host-parasite and parasite-parasite interactions.

Parasitic copepods were dominant in the present parasite community of C. nobilis. The dominance by ectoparasites has been observed in only a few parasite communities of marine fish from the South Atlantic Ocean, and probably is favored by the crowding behavior of these fish in high population densities, which facilitates the transmission of ectoparasites with direct life cycles, such as copepods (Cezar & Luque, 1999; Tavares et al., 2001; Tavares & Luque, 2004; Alves & Luque, 2006). Haemulids commonly occur in large shoals that may include different species of coral reef fish, e.g., belonging to the Carangidae, Lutjanidae and Scaridae families (Pereira et al., 2011; Cerqueira et al., 2021). Moreover, according to Pombo et al. (2014), C. nobilis has high population density in southeastern Brazil. The copepods found in the present study were represented by species that have been reported on haemulids (C. haemulonis, Caligus xystercus Cressey, 1991 and L. rathbuni), carangids (Caligus longipedis Bassett-Smith, 1898, Caligus rufimaculatus Wilson, 1905 and Caligus robustus Bassett-Smith, 1898) and exclusively on C. nobilis (A. lamellatus) (Luque & Tavares, 2007; Paschoal et al., 2013). Therefore, it is plausible that the high population density of C. nobilis associated with mixed shoals favors the transmission of copepods in the ecosystem evaluated by us.

The copepod L. rathbuni was the most abundant and dominant species in the parasite community of C. nobilis. Currently, about 17 species of lernanthropids have been reported, infesting more than 20 species of marine fish from the Brazilian coast (Luque & Tavares, 2007; Luque et al., 2013). Of these, L. rathbuni is the most commonly recorded and infests five species of haemulids, namely, Anisotremus surinamensis (Bloch, 1791), C. nobilis, H. atlanticus, Haemulopsis corvinaeformis (Steindachner, 1868) and O. rubra (Paschoal et al., 2015, 2023). In the North Atlantic Ocean, L. rathbuni has also been reported parasitizing the haemulid fish Orthopristis chrysoptera (Linnaeus, 1766) along the coast of Florida, USA (Paschoal et al., 2015). Host preference exhibited by parasitic copepods is not uncommon, being a consequence of the capacity of these organisms to locate, identify and establish themselves on their hosts (Mordue & Birkett, 2009). The sea louse Lepeophtheirus salmonis (Kroyer, 1837), for example, infests more than 10 species of salmonid fish in the Northern Hemisphere, using phototropism, chemotropism, and mechanical perception to reach its hosts (Mordue & Birkett, 2009). The host range of L. rathbuni in the Atlantic Ocean, composed by certain species of haemulid fish, can possibly be explained by mechanisms similar to those previously described. However, the host recognition mechanisms used by L. rathbuni are still unknown, since no study of the biology of this species has been published. It should be mentioned that, despite the affinities between L. rathbuni and haemulid fish, its prevalence varies in the South Atlantic Ocean, ranging from 18% in infestations of H. atlanticus, H. corvinaeformis and O. rubra, to 37% in infestations of C. nobilis (Luque et al., 1996a; Cavalcanti et al., 2006), illustrating the host selection by L. rathbuni even among haemulid fish.

Parasite community structure in fish has been related to a series of host factors, such as biology, body size, aggregate distribution (shoaling behavior), hormonal variations and ventilation volume during gas exchange/hemostasis (Boxshall & Halsey, 2004; Poulin et al., 1991; Timi & Lanfranchi, 2006). The influence of host body size on the prevalence and abundance of parasitic copepods has been observed in several natural associations with fish, in which some authors have suggested that increased body and gill surfaces along with higher ventilation volume are key factors influencing these parasitological descriptors (Dogiel et al., 1961; Hanek & Fernando, 1978; Kabata, 1982; Cressey et al., 1983; Timi & Lanfranchi, 2006). Cressey et al. (1983) observed that infestation patterns of Pseudocycnoides spp. on scombrid fish were influenced by the ability of these copepods to adhere to gill filaments. These authors observed that for effective attachment, the appendages of these copepods should partially embrace the gill filament, which was facilitated in hosts measuring 20 to 30 cm. In the present study, the most adequate body size range of C. nobilis for infestations by L. rathbuni and A. lamellatus was 20.8 to 27.9 cm, defined as Class II, since both prevalence and abundance of these parasites were higher in hosts of this class (see Table 4). Moreover, the abundances of these copepods were negatively correlated with host body length, as a consequence of the previously described results. Those observations suggest that the size of gill filaments of C. nobilis allocated in Classes I (too small) and III (too large) is not as suitable for the attachment to the appendages of L. rathbuni and A. lamellatus as are the gill filaments of those fish allocated in Class II, similar to the findings of Cressey et al. (1983).

Changes in endoparasite burdens in fish hosts have been associated with variations in body size and are commonly explained by ontogenetic changes in diet composition and spatial availability within the host organism (Polyanski, 1961; Saad-Fares & Combes, 1992; Sabas & Luque, 2003). Details of the life cycle of most species of digeneans that parasitize fish are unavailable, but it is well known that mollusks are crucial, acting as first intermediate obligatory hosts (Cribb et al., 2001, 2003). The diet of C. nobilis is mainly composed of invertebrates and small bony fish (Lopes & Oliveira-Silva, 1998; Feitosa et al., 2002). Pombo et al. (2014) identified a total of seven prey items in the diet of C. nobilis, in which there was preference for crustaceans of the orders Mysida Boas‎, 1883‎ and Amphipoda Latreille‎, 1816‎, while cnidarians, mollusks and polychaetes were rarely consumed. In the present study, the prevalence and abundance of Torticaecum sp. (metacercariae) were higher in hosts from Class III (the largest), and its abundance was positively correlated with host fish body length. These results are possibly related to cumulative infection, in which the consumption of potential intermediate hosts of this digenean (e.g., mollusks) increases proportionally to fish growth. Such cumulative effect is common in helminth larval forms and similar results have been observed in other marine fish from the South Atlantic Ocean (Luque et al., 1996a; Knoff et al., 1997; Luque & Chaves, 1999; Alves & Luque, 2001; Sabas & Luque, 2003). It should be mentioned that although no statistical differences were observed in the prevalence and abundance of P. merus between hosts from Class II and III, the values of these parasitological descriptors were higher in hosts of Class III. This can also be also explained by the higher consumption of potential intermediate hosts by larger fish, as well as by the fact that in larger hosts, more space is available for parasite colonization.

According to Lizama et al. (2005), fish sex can influence the host-parasite relationships. In the present study, the absence of difference in body length according to sex of C. nobilis was common, since both males and females reach sexual (gonadal) maturity at similar body lengths, as demonstrated by a previous study (da Silva et al., 2019). The fact that the abundance of C. haemulonis was higher in males of C. nobilis may be associated with the relative scarcity of behavioral and physiological differences related to sex. Moreover, such differences of infestation by C. haemulonis between male and female fish observed here most likely is explained by casual factors that commonly influence ectoparasite loads, such as seasonal changes in the composition of the tegument; high testosterone levels, which can cause immunosuppression in males; and/or behavioral differences between sexes (Pickering, 1977; Folstad & Karter, 1992; Poulin, 1996; Tavares & Luque, 2004; Lizama et al., 2005). Associations between host sex and ectoparasite infestations in wild fish populations have been documented in the South Atlantic Ocean (see Luque et al., 1996a; Knoff et al., 1997; Chaves & Luque, 1999; Alves & Luque, 2001).

Regarding parasite species richness (at the component community level) of haemulids studied so far in the South Atlantic Ocean, the parasite community of O. rubra studied by Luque et al. (1996a, b) contained 21 different species, contrasting with that of C. nobilis in the present study, which was composed of 18 species. The parasite community of H. atlanticus, also studied by Luque et al. (1996a, b), was composed of 18 species, and that of A. virgincus was composed of 16 parasite species (see Paschoal et al., 2023). According to some authors, the higher richness observed in the parasite component community of O. rubra may be related to its broader vagility, greater dietary diversity (related to endoparasite infections), and anatomical and physiological particularities (Luque et al., 1996b, 2004; Paschoal et al., 2023). These parasite communities of haemulid fish off the Brazilian coast are all composed by ecto and endoparasites, in which the latter are represented by adult and larval forms (Luque et al., 1996b, 2004; Paschoal et al., 2023). These findings indicate that such fish occupy intermediate positions within the local trophic webs, acting as both intermediate and definitive hosts. Therefore, these haemulids can be considered important trophic links in the ecosystems. It should be mentioned that their parasite communities show varied species composition and particular structures according to the host species. For example, the acanthocephalan cystacanth Serrassentis sp. has been reported in A. virgincus, C. nobilis, H. atlanticus and O. rubra, whereas the copepods C. haemulonis and L. rathbuni have been reported infesting C. nobilis, H. atlanticus and O. rubra, in which parasite burdens vary according to the fish species (Paschoal et al., 2023). In any case, it is important to highlight that knowledge pertaining to parasites of haemulid fish from the South Atlantic Ocean is still incipient, preventing further conclusions on patterns of parasite species richness, since only four species of haemulids, out of 25 that occur in this region, have been studied for parasites (Luque et al., 1996a, b; Paschoal et al., 2023).

Positive or negative associations between parasite species can provide evidence of interspecific interactions and the community structure (Poulin, 2001; Benicio et al., 2022). The low number of concurrent infections/infestations observed in the present study was similar to the results obtained by Luque et al. (1996b), regarding the parasites of H. atlanticus, from the same location as that of the present study. Such findings indicate the isolationist characteristic of these parasite communities (see Luque et al., 1996b). In contrast, the parasite community of O. rubra seems to be more interactive, since concurrent infections were more frequent and there was evidence of interspecific interactions, as also reported by Luque et al. (1996b) in the same area that we studied. According to Poulin (2001), changes in parasite infrapopulation structure, as indicated by mean abundance or prevalence, for example, may be evidence of interaction in cases of interspecific co-occurrence. On the other hand, the literature suggests that interspecific interactions among parasites can only be validated under experimental conditions (see Rohde et al., 1995; Poulin, 2001). The higher interactive nature observed in the parasite community of O. rubra may be a consequence of higher species richness and much higher number of individual parasites (7,282) (see Luque et al., 1996b) in comparison with the parasite communities of the other haemulid species cited previously. It is logical to expect a greater number of species and individuals in a parasite community to be associated with a higher probability of interaction among them. Nevertheless, despite the number of concurrent infections between endoparasites, and infestations between copepod ectoparasites, the only possible indication of interspecific interaction was observed in concurrent infestations by C. haemulonis and L. rathbuni, in which their abundances were negatively associated. These species occupy different, but closely related, sites in the host (operculum and gill, see Table 1), placing them physically close together. However, the cause of such interference cannot be established based on the present results, since more detailed data would be required. The discussion in this paragraph only reinforces the premise that parasite communities of marine fish are stochastic and very complex, making it difficult to define general patterns (Holmes, 1990; Rohde et al., 1995; Tavares & Luque, 2004).

Acknowledgements

Fabiano Paschoal was supported by Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA, process no. 84516/2022), Brazil. Felipe B. Pereira was supported in part by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, process no. APQ-01179-21), Brazil. José L. Luque was supported by a research fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico do Brazil (CNPq).

• Ethics declaration
  All applicable institutional, national and international guidelines for the care and use of animals were followed.
• How to cite:
  Paschoal F, Nunes JLS, Cezar AD, Pereira FB, Luque JL. The metazoan parasite community of the barred grunt Conodon nobilis (Actinopterygii: Haemulidae) from the coast off Rio de Janeiro, southeastern Brazil. Braz J Vet Parasitol 2024; 33(4): e010724. https://doi.org/10.1590/S1984-29612024068

References

• Alves DR, Luque JL. 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. Mem Inst Oswaldo Cruz 2001; 96(2): 145-153. http://doi.org/10.1590/S0074-02762001000200002 PMid:11285488.
  » http://doi.org/10.1590/S0074-02762001000200002
• Alves DR, Luque JL. Ecologia das comunidades de metazoários parasitos de cinco espécies de escombrídeos (Perciformes: Scombridae) do litoral do estado do Rio de Janeiro, Brasil. Rev Bras Parasitol Vet 2006; 15(4): 167-181. PMid:17196121.
• Araújo DF, Peres LGM, Yepez S, Mulholland DS, Machado W, Tonhá M, et al. Assessing man-induced environmental changes in the Sepetiba Bay (Southeastern Brazil) with geochemical and satellite data. C R Geosci 2017; 349(6-7): 290-298. http://doi.org/10.1016/j.crte.2017.09.007
  » http://doi.org/10.1016/j.crte.2017.09.007
• Araújo FG, de Azevedo MCC, de Araújo Silva M, Pessanha ALM, Gomes ID, da Cruz-Filho AG. Environmental influences on the demersal fish assemblages in the Sepetiba Bay, Brazil. Estuaries 2002; 25(3): 441-450. http://doi.org/10.1007/BF02695986
  » http://doi.org/10.1007/BF02695986
• Benicio L, Moreira J, Paschoal F. Community ecology of the metazoan parasites of the Atlantic anchoveta, Cetengraulis edentulus (Actinopterygii: Engraulidae) from the Sepetiba Bay, Rio de Janeiro, Brazil. Zoologia 2022; 39: e21034. http://doi.org/10.1590/s1984-4689.v39.e21034
  » http://doi.org/10.1590/s1984-4689.v39.e21034
• Boxshall GA, Halsey SH. An introduction to copepod diversity London: The Ray Society; 2004.
• Bush AO, Aho JM, Kennedy CR. Ecological versus phylogenetic determinants of helminth parasite community richness. Evol Ecol 1990; 4(1): 1-20. http://doi.org/10.1007/BF02270711
  » http://doi.org/10.1007/BF02270711
• Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://doi.org/10.2307/3284227 PMid:9267395.
  » http://doi.org/10.2307/3284227
• Cavalcanti ETS, Chellappa S, Pavanelli GC, Takemoto RM. Presença de Lernanthropus rathbuni (Copepoda: Lernanthropidae) no coró, Pomadasys corvinaeformis (Osteichthyes: Haemulidae) em águas costeiras do Rio Grande do Norte. Arq Ciênc Mar 2006; 39 (1): 134-137.
• Cerqueira NNCD, Rotundo MM, Marceniuk AP, Cruz VP, Foresti F, Oliveira C. Molecular identification of Brachygenys and Haemulon species (Perciformes: Haemulidae) from the Brazilian coast. Neotrop Ichthyol 2021; 19(2): e200109. http://doi.org/10.1590/1982-0224-2020-0109
  » http://doi.org/10.1590/1982-0224-2020-0109
• Cezar AD, Luque JL. Metazoan parasites of the Atlantic Spadefish Chaetodipterus faber (Teleostei: Ephippidae) from the coastal zone of the State of Rio de Janeiro, Brazil. J Helminthol Soc Wash 1999; 66(1): 14-20.
• Chaves NN, Luque JL. Ecology of metazoans parasites of Menticirrhus americanus (Osteichthyes: Sciaenidae), coast area from Rio de Janeiro State, Brazil. Rev Bras Parasitol Vet 1999; 8(2): 137-144.
• Cressey RF, Collette BB, Russo JL. Copepods and scombrid fishes: A study in host-parasite relationships. Fish Bull 1983; 81(2): 227-266.
• Cribb TH, Bray RA, Littlewood DTJ. The nature and evolution of the association among digeneans, molluscs and fishes. Int J Parasitol 2001; 31(9): 997-1011. http://doi.org/10.1016/S0020-7519(01)00204-1 PMid:11406146.
  » http://doi.org/10.1016/S0020-7519(01)00204-1
• Cribb TH, Bray RA, Olson PD, Littlewood DTJ. Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 2003; 54(1): 197-254. http://doi.org/10.1016/S0065-308X(03)54004-0 PMid:14711086.
  » http://doi.org/10.1016/S0065-308X(03)54004-0
• Dogiel VA, Petrushevski GK, Polyanski YI. Parasitology of fishes Edinburgh & London: Oliver & Boyd; 1961.
• Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research Charlottetown: AVC Inc; 2003.
• Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes 2. ed. Maringá: Editora Eduem; 2006.
• Feitosa CV, Pimenta DAS, Araújo ME. Hábito alimentar de espécies de peixes na área de influência do emissário oceânico de Fortaleza, Ceará, Brasil. Arq Ciênc Mar 2002; 35(1-2): 91-95. http://doi.org/10.32360/acmar.v35i1-2.30910.
• Folstad I, Karter AJ. Parasites, bright males, and the immunocompetence handicap. Am Nat 1992; 139(3): 603-622. http://doi.org/10.1086/285346
  » http://doi.org/10.1086/285346
• Fricke R, Eschmeyer WN, Van der Laan R. Eschmeyer's catalog of fishes: genera, species, references [online]. 2024 [cited 2024 Apr 24]. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
  » http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
• Froese R, Pauly D. FishBase [online]. 2024 [cited 2024 Apr 24]. Available from: www.fishbase.org
  » www.fishbase.org
• García-Teh JG, Vidal-Martínez VM, Mariño-Tapia I, Árcega-Cabrera F, Ordoñez-López U, Aguirre-Macedo ML. Metazoan parasite infracommunities of the Tomtate Grunt (Haemulon aurolineatum) as potential bioindicators of environmental conditions in the Yucatan Continental Shelf, Mexico. Bull Environ Contam Toxicol 2022; 108(1): 49-54. http://doi.org/10.1007/s00128-021-03305-5 PMid:34216226.
  » http://doi.org/10.1007/s00128-021-03305-5
• Guillén-Hernández S, Canto A, Villegas-Hernández H, González-Salas C, Poot-López G, Espínola-Novelo JF, et al. Spatial variation in Helminth Parasite communities of the French grunt, Haemulon flavolineatum (Teleostei: Haemulidae), from the Yucatan Peninsula. J Parasitol 2023; 109(2): 76-86. http://doi.org/10.1645/21-103 PMid:36943229.
  » http://doi.org/10.1645/21-103
• Hanek G, Fernando CH. The role of season, habitat, host age, and sex on gill parasites of Lepomis gibbosus (L.). Can J Zool 1978; 56(6): 1247-1250. http://doi.org/10.1139/z78-178
  » http://doi.org/10.1139/z78-178
• Holmes JC. Helminth communities in marine fishes. In: Esch G, Bush A, Aho J, editors. Parasite communities: patterns and processes New York: Chapman & Hall; 1990. p. 101-130. http://doi.org/10.1007/978-94-009-0837-6_5
  » http://doi.org/10.1007/978-94-009-0837-6_5
• Kabata Z. Copepoda (Crustacea) parasitic on fishes: problems and perspectives. Adv Parasitol 1982; 19: 1-71. http://doi.org/10.1016/S0065-308X(08)60265-1
  » http://doi.org/10.1016/S0065-308X(08)60265-1
• Kjerfve B, Dias GT, Filippo A, Geraldes MC. Oceanographic and environmental characteristics of a coupled coastal bay system: Baía de Ilha Grande-Baía de Sepetiba, Rio de Janeiro, Brazil. Reg Stud Mar Sci 2021; 41: 101594. http://doi.org/10.1016/j.rsma.2020.101594
  » http://doi.org/10.1016/j.rsma.2020.101594
• Knoff M, Luque JL, Amato JFR. Community ecology of the metazoan parasites of grey mullets, Mugil platanus (Osteichthyes: Mugilidae) from the littoral of the State of Rio de Janeiro, Brazil. Rev Bras Biol 1997; 57(3): 441-454. PMid:9430918.
• Lizama MLAP, Takemoto RM, Pavanelli GC. Influence of host sex and age on infracommunities of metazoan parasites of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the Upper Paraná River floodplain, Brazil. Parasite 2005; 12(4): 299-304. http://doi.org/10.1051/parasite/2005124299 PMid:16402561.
  » http://doi.org/10.1051/parasite/2005124299
• Lopes PRD, Oliveira-Silva JT. Notes on the feeding of Conodon nobilis (Linnaeus) and Polydactylus virginicus (Linnaeus) (Actinopterygii: Haemulidae e Polynemidae) in the Jaguaribe Beach (Itamaracá Island), state of Pernambuco. Bioikos 1998; 12(2): 53-59.
• López-Zacarías MN, Herrerías-Diego Y, Tafolla-Venegas D, Domínguez-Domínguez O, Pérez-Ponce de León G. Community structure of intestinal adult trematodes (Platyhelminthes) in six species of Haemulon (Osteichthyes) in Puerto Morelos Reef National Park, Quintana Roo, Mexico. Rev Mex Biodivers 2021; 92: e923602. http://doi.org/10.22201/ib.20078706e.2021.92.3602
  » http://doi.org/10.22201/ib.20078706e.2021.92.3602
• Luque JL, Amato JFR, Takemoto RM. Comparative analysis of the communities of metazoan parasites of Orthopristis ruber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the southeastern Brazilian littoral: I. structure and influence of the size and sex of hosts. Rev Bras Biol 1996a; 56(2): 279-292.
• Luque JL, Amato JFR, Takemoto RM. Comparative analysis of the communities of metazoan parasites communities of Orthopristis ruber and Haemulon steindachneri (Osteichthyes: Haemulidae) from the southeastern Brazilian littoral: II diversity, interspecific associations, and distribution of the gastrointestinal parasites. Rev Bras Biol 1996b; 56(2): 293-302.
• Luque JL, Chaves ND. Ecologia da comunidade de metazoários parasitos da Anchova Pomatomus saltator (Linnaeus) (Osteichthyes, Pomatomidae) do litoral do Estado do Rio de Janeiro, Brasil. Rev Bras Zool 1999; 16(3): 711-723. http://doi.org/10.1590/S0101-81751999000300010
  » http://doi.org/10.1590/S0101-81751999000300010
• Luque JL, Mouillot D, Poulin R. Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 2004; 128(Pt 6): 671-682. http://doi.org/10.1017/S0031182004005050 PMid:15206470.
  » http://doi.org/10.1017/S0031182004005050
• Luque JL, Tavares LER. Checklist of Copepoda associated with fishes from Brazil. Zootaxa 2007; 1579(1): 1-39. http://doi.org/10.11646/zootaxa.1579.1.1
  » http://doi.org/10.11646/zootaxa.1579.1.1
• Luque JL, Vieira FM, Takemoto RM, Pavanelli GC, Eiras JC. Checklist of Crustacea parasitizing fishes from Brazil. Check List 2013; 9(6): 1449-1470. http://doi.org/10.15560/9.6.1449
  » http://doi.org/10.15560/9.6.1449
• Magurran AE. Measuring biological diversity Oxford: Blackwell Publishing; 2004.
• Menezes NA, Figueiredo JL. Manual de Peixes Marinhos do Sudeste de Brasil IV. Teleostei (3) São Paulo: Museu de Zoologia, Universidade de São Paulo; 1980.
• Mordue AJ, Birkett MA. A review of host finding behaviour in the parasitic sea louse, Lepeophtheirus salmonis (Caligidae: copepoda). J Fish Dis 2009; 32(1): 3-13. http://doi.org/10.1111/j.1365-2761.2008.01004.x PMid:19245627.
  » http://doi.org/10.1111/j.1365-2761.2008.01004.x
• Motta-Neto CC, Cioffi MB, Costa GWWF, Amorim KDJ, Bertollo LAC, Artoni RF, et al. Overview on karyotype stasis in Atlantic grunts (Eupercaria, Haemulidae) and the evolutionary extensions for other marine fish groups. Front Mar Sci 2019; 6: 628. http://doi.org/10.3389/fmars.2019.00628
  » http://doi.org/10.3389/fmars.2019.00628
• Nelson JS, Grande TC, Wilson M. Fishes of the world Hoboken: John Wiley & Sons; 2016. http://doi.org/10.1002/9781119174844
  » http://doi.org/10.1002/9781119174844
• Paschoal F, Cezar AD, Luque JL. A new species of Acantholochus (Cyclopoida, Bomolochidae) parasitic on the barred grunt Conodon nobilis (Linnaeus, 1758) (Osteichthyes, Haemulidae) from Rio de Janeiro, Brazil. Crustaceana 2013; 86(2): 212-220. http://doi.org/10.1163/15685403-00003153
  » http://doi.org/10.1163/15685403-00003153
• Paschoal F, Cezar AD, Luque JL. Checklist of metazoan associated with grunts (Perciformes, Haemulidae) from the Nearctic and Neotropical regions. Check List 2015; 11(1): 1-23. http://doi.org/10.15560/11.1.1501
  » http://doi.org/10.15560/11.1.1501
• Paschoal F, Couto JV, Pereira FB, Luque JL. A New Species of Hatschekiid Copepod (Crustacea: Hatschekiidae) Parasitic on the Porkfish Anisotremus virginicus (Linnaeus, 1758) (Actinopterygii: Haemulidae), with Notes on Previously Known Species of Hatschekia Poche, 1902 Collected from Actinopterygians off Brazil. Acta Parasitol 2022; 67(3): 1126-1135. http://doi.org/10.1007/s11686-022-00551-3 PMid:35476261.
  » http://doi.org/10.1007/s11686-022-00551-3
• Paschoal F, Cezar AD, Pereira FB, Luque JL. Structure of the metazoan parasite communities of haemulid fish (Actinopterygii: Perciformes) in the South Atlantic Ocean: a comparative approach. An Acad Bras Cienc 2023; 95(1): e20220205. http://doi.org/10.1590/0001-3765202320220205 PMid:36946810.
  » http://doi.org/10.1590/0001-3765202320220205
• Pereira PHC, Feitosa JLL, Ferreira BP. Mixed-species schooling behavior and protective mimicry involving coral reef fish from the genus Haemulon (Haemulidae). Neotrop Ichthyol 2011; 9(4): 741-746. http://doi.org/10.1590/S1679-62252011005000037
  » http://doi.org/10.1590/S1679-62252011005000037
• Pickering AD. Seasonal changes in the epidermis of the brown trout Salmo trutta (L.). J Fish Biol 1977; 10(6): 561-566. http://doi.org/10.1111/j.1095-8649.1977.tb04088.x
  » http://doi.org/10.1111/j.1095-8649.1977.tb04088.x
• Polyanski YI. Ecology of parasites of marine fishes. In: Dogiel AV, Petrushevski GK, Polyanski YI, editors. Parasitology of fishes Edinburgh: Oliver & Boyd; 1961. p. 1-47.
• Pombo M, Denadai MR, Bessa E, Santos FB, de Faria VH, Turra A. The barred grunt Conodon nobilis (Perciformes: Haemulidae) in shallow areas of a tropical bight: Spatial and temporal distribution, body growth and diet. Helgol Mar Res 2014; 68(2): 271-279. http://doi.org/10.1007/s10152-014-0387-2
  » http://doi.org/10.1007/s10152-014-0387-2
• Poulin R, Curtis MA, Rau ME. Size, behaviour, and acquisition of ectoparasitic copepods by brook trout, Salvelinus fontinalis. Oikos 1991; 61(2): 169-174. http://doi.org/10.2307/3545334
  » http://doi.org/10.2307/3545334
• Poulin R. Interactions between species and the structure of helminth communities. Parasitology 2001; 122(Suppl): S3-S11. http://doi.org/10.1017/S0031182000016991 PMid:11442194.
  » http://doi.org/10.1017/S0031182000016991
• Poulin R. Sexual inequalities in helminth infections: a cost of being a male? Am Nat 1996; 147(2): 287-295. http://doi.org/10.1086/285851
  » http://doi.org/10.1086/285851
• Poulin R. The disparity between observed and uniform distributions: a new look at parasite aggregation. Int J Parasitol 1993; 23(7): 937-944. http://doi.org/10.1016/0020-7519(93)90060-C PMid:8106186.
  » http://doi.org/10.1016/0020-7519(93)90060-C
• R Core Team. R: a language and environment for statistical computing [software]. Vienna: R Development Core Team; 2020 [cited 2024 Apr 24]. Available from: https://www.r-project.org/
  » https://www.r-project.org/
• Reiczigel J, Marozzi M, Fábián I, Rózsa L. Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends Parasitol 2019; 35(4): 277-281. http://doi.org/10.1016/j.pt.2019.01.003 PMid:30713051.
  » http://doi.org/10.1016/j.pt.2019.01.003
• Rohde K, Hayward C, Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol 1995; 25(8): 945-970. http://doi.org/10.1016/0020-7519(95)00015-T PMid:8550295.
  » http://doi.org/10.1016/0020-7519(95)00015-T
• Saad-Fares A, Combes C. Abundance/host size relationships in a fish trematode community. J Helminthol 1992; 66(3): 187-192. http://doi.org/10.1017/S0022149X00014541 PMid:1452993.
  » http://doi.org/10.1017/S0022149X00014541
• Sabas CS, Luque JL. Metazoan parasites of weakfish, Cynoscion guatucupa and Macrodon ancylodon (Osteichthyes: Sciaenidae), from the coastal zone of the state of Rio de Janeiro, Brazil. Rev Bras Parasitol Vet 2003; 12(4): 171-178.
• Silva VEL, Vieira DS, Teixeira EC, Ferreira ACL, Assis IO, Rangely J, et al. Maturity, fecundity, and reproductive cycle of Conodon nobilis (Actinopterygii: Perciformes: Haemulidae) in tropical waters of the Atlantic Ocean. Acta Ichthyol Piscat 2019; 49(3): 235-242. http://doi.org/10.3750/AIEP/02597
  » http://doi.org/10.3750/AIEP/02597
• Souza AM, Rocha DS, Guerra JV, Cunha BA, Martins MVA, Geraldes MC. Metal concentrations in marine sediments of the Rio de Janeiro Coast (Brazil): A proposal to establish new acceptable levels of contamination. Mar Pollut Bull 2021; 165: 112113. http://doi.org/10.1016/j.marpolbul.2021.112113 PMid:33567385.
  » http://doi.org/10.1016/j.marpolbul.2021.112113
• Tavares LER, Luque JL, Botelho SL No. Ecologia da comunidade de metazoários parasitos do olho-de-cão Priacanthus arenatus (Cuvier, 1829) (Osteichthyes, Priacanthidae) do litoral do Estado do Rio de Janeiro, Brasil. Rev Bras Zoociênc 2001; 3(1): 45-59.
• Tavares LER, Luque JL. Community ecology of the metazoan parasites of white sea catfish Netuma barba (Osteichthyes: Ariidae) from the coastal zone of the State of Rio de Janeiro. Brazil. Braz J Biol 2004; 64(1): 169-176. http://doi.org/10.1590/S1519-69842004000100019 PMid:15195376.
  » http://doi.org/10.1590/S1519-69842004000100019
• Timi JT, Lanfranchi AL. Size relationships between the parasitic copepod, Lernanthropus cynoscicola, and its fish host, Cynoscion guatucupa. Parasitology 2006; 132(2): 207-213. http://doi.org/10.1017/S0031182005008905 PMid:16472414.
  » http://doi.org/10.1017/S0031182005008905
• Zar JH. Biostatistical analysis 5th ed. New Jersey: Prentice Hall; 2010.

Publication Dates

• Publication in this collection
  22 Nov 2024
• Date of issue
  2024

History

• Received
  23 May 2024
• Accepted
  24 Sept 2024