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First study on infestation of Excorallana berbicensis (Isopoda: Corallanidae) on six fishes in a reservoir in Brazilian Amazon during dry and rainy seasons/Primer estudio de la infestacion de Excorallana berbicensis (Isopoda: Corallanidae) en seis peces en un embalse del Amazonas brasileno durante las estaciones seca y lluviosa.


Excorallana Stebbing, 1904 (Corallanidae) are isopods consisting of 24 species (Schotte, 2014) occurring predominantly in marine environments of tropical and subtropical latitudes (Guzman et al., 1988; Delaney 1989). They are associated especially with substrates (Delaney, 1984; Hendrickx & Espinosa-Perez, 1998; Morgado & Tanaka, 2001). Corallanids of this genus have also been occasionally described associated to zooplankton (Guzman et al., 1988), also collected from the intertidal zone (Kensley et al., 1995) and to marine fish species from different environments (Williams Jr. & Bunkley-Williams, 1994; Semmens et al., 2006; Alvarez-Leon, 2009). Some species of Excorallana occur especially in environments of great depth (Delaney, 1989), but only Excorallana berbicensis Boone, 1918, E. tricornis occidentalis Richardson, 1905, E. quadricornis Hansen, 1890 and E. longicornis Lemos de Castro, 1960 have been collected from mangroves (Delaney, 1984). Corallanids are voracious carnivore isopods that act as predators and also as scavengers (Brusca & Wehrtmann, 2009). E. tricornis occidentalis is a facultative parasite for many marine fish and, when in massive infestations, it causes serious damage to fishing of Epinephelus striatus Bloch, 1792 (Semmens et al., 2006). However, information on Excorallana spp. on freshwater fish is scarce (Van Name, 1925; Monod, 1969; Thatcher, 1995). Excorallana spp. has mostly been studied regarding their taxonomy (Van Name, 1925; Monod, 1969; Delaney, 1984, 1989; Kensley et al., 1995; Thatcher, 1995; Hendrickx & Espinosa-Perez, 1998), but a few studies on their epidemiology in fish have been conducted (Semmens et al., 2006).

Excorallana berbicensis was described parasitizing Lycengraulis grossideus Spix & Agassiz, 1829 in rivers from French Guiana (Van Name, 1925); a species of shark in freshwater from Guyana (Monod, 1969); and Ageneiosus inermis Linnaeus, 1766 from Amazon River basin, in Brazil (Thatcher, 1995). However, in addition to the small number of studies on E. berbicensis in association with fish, there are no reports regarding seasonal variation in infestation levels of these isopods in host fish population.

In the Amazon region, seasonality influenced by precipitation is characterized by two cycles, the rainy and dry season (Souza & Cunha, 2010; Cunha et al., 2013). These seasonal dynamics greatly influence in ichthyofauna community structures (Galacatos et al., 2004) and can also influence infracommunities of parasites in fish populations. For different fish species from Amazon, low levels of infestation by argulids species have been reported in the dry season (Malta, 1982; Malta & Varella, 1983). In contrast, parasitism by Dolops nana (Neves et al., 2013), Miracetyma sp. (Vital et al., 2011) and Ergasilus turucuyus Malta & Varella, 1996 (Vasconcelos & Tavares-Dias, 2014) have not been found to be influenced by the dry season or rainy season. However, Bauer & Karimov (1990) argued that, in regions between the tropics, the relatively constant climate does not favor seasonal fluctuations of parasitism. In temperate climatic regions, temperature has been considered to be the most important factor influencing the seasonality of parasite infracommunities. Consequently, it can directly or indirectly influence ectoparasites crustacean infestations (Jones, 1974; Guzman et al., 1988; Kadlec et al., 2003; Pech et al., 2010; Alsarakibi et al., 2014). In the Reservoir of the Coaracy Nunes hydroelectric power plant in Araguari River basin, in the eastern Amazon region (Northern Brazil), Ageneiosus ucayalensis Castelnau, 1855; Hemiodus unimaculatus Bloch, 1794; Serrasalmus gibbus Castelnau, 1855; Geophagus proximus Castelnau, 1855, Acestrorhynchus falcirostris Cuvier, 1819 and Psectrogaster falcata Eigenmann and Eigenmann, 1889 are the most abundant fish species (Sa-Oliveira et al., 2013, 2015). These six fish species presents different life habits, once H. unimaculatus has omnivorous diet, mainly consuming algae, detritus and other aquatic invertebrates, and P. falcata is detritivorous, feeding on detritus and microorganisms associated with the substrate. Geophagus proximus is omnivorous, mainly feeding of plant material, mollusks, insects and other aquatic invertebrates, and A. ucayalensis is carnivorous, consuming fish, insects and other aquatic invertebrates. Acestrorhynchus falcirostris and S. gibbus are piscivorous fish (Santos et al., 2004). However, the parasites fauna on fish of this reservoir is few known (Vasconcelos & Tavares-Dias, 2014). Thus, the aim of study was to investigate the prevalence and abundance of E. berbicensis in these six species of fish from this Amazonian reservoir during rainy and dry seasons.


Study area

The water Reservoir of the Coaracy Nunes Hydroelectric Power Plant (Fig. 1) is located in the municipality of Ferreira Gomes, Amapa State, in the eastern Amazon region (northern Brazil). Its area is 23.5 [km.sup.2], capacity 138 H[m.sup.3] and average depth 15 m. This reservoir began its operations in 1974 and is connected to the Araguari River basin, which originates south of the Lombada and Tumucumaque mountain ranges and flows to the Atlantic Ocean (Barbara et al., 2010; Sa-Oliveira et al., 2013). This reservoir is a transition area between lotic and lentic environments and has marginal areas with only a few aquatic macrophytes, especially Eichhornia crassipes and Eleocharis sp., and great quantities of decomposing arboreal vegetation, due to non-deforestation of the area that was destined for the reservoir.

Fish and collection procedures

For study of parasites, specimens of Acestrorhynchus falcirostris (Acestrorhynchidae), Ageneiosus ucayalensis (Auchenipteridae), Geophagus proximus (Cichlidae), Hemiodus unimaculatus (Hemiodontidae), Serrasalmus gibbus (Serrasalmidae) and Psectrogaster falcata (Curimatidae) were collected in the Coaracy Nunes Reservoir (Fig. 1), a long-established ecosystem, about 40 years (Sa-Oliveira et al., 2015). A total of 296 fish specimens were caught during the dry season (October 2012 to February 2013) and rainy season (April to August 2013) at six sampling points, located at a distance of 889 [+ or -] 498 m (range: 544-1777 m) from each other (Fig. 1), for analysis on the seasonal level of E. berbicensis infestation. A total of 65 P. falcata, 63 A. ucayalensis, 62 A. falcirostris, 56 H. unimaculatus, 36 S. gibbus and 14 G. proximus were examined. The fish were caught using simple gill nets (20, 30, 40, 50 and 60 mm mesh), grouped into lengths of 100 m. These nets were installed near the reservoir margins and were left in the water for 12 h, with inspection every two hours. This study was developed in accordance with the principles adopted by the Brazilian College of Animal Experimentation (COBEA).

Collection procedures and analysis of parasites

After the fish had been removed from the nets, the mouth, integument and fins of each fish were immediately examined for the presence of crustacean parasites. The gills were collected and fixed in 5% formalin, and then were examined with the aid of a stereomicroscope to collect and count the parasites. The crustacean species were conserved in 70% glycerinated alcohol and were prepared for identification, following the recommendations of Eiras et al. (2006).

The ecological descriptors used followed the recommendations of Bush et al. (1997). Differences in the prevalence of E. berbicensis between the rainy and dry seasons, as well as between months were evaluated using the chi-square test ([chi square]) with the Yates correction. Differences in the abundance of E. berbicensis between rainy and dry seasons were evaluated using the Mann-Whitney (U) test, and between months using Kruskal-Wallis test (H). The Shapiro-Wilk test was used to determine whether the parasite abundance presented normal distribution. Each fish was measured for body weight (g) and length (cm), which were used to determine the relative condition factor of the hosts/Kn (Le-Cren, 1951). The Kn of the overall hosts was compared with the Kn of the hosts during dry and rainy seasons, using the Kruskal-Wallis test (Zar, 2010).

Water temperature, electric conductivity and dissolved oxygen in water were obtained by means of the YSI 85 multiparameter measuring device, and pH by means of the YSI 60 pHmeter. Turbidity was determined using the obtained by means of the Plus II microprocessing turbidimeter. Transparency was measured using Secchi's disc. Rainfall levels were obtained through the National Environmental Data System (SINDA-INPE), from the Coaracy Nunes dam hydrometeorological station.


The body parameters and number of the examined fish by seasons are showed in Table 1. The physical and chemical parameters, with the exception of rainfall levels, were similar during the dry and rainy seasons (Table 2).

Excorallana berbicensis infestations occurred on the mouth, gills and integument of the hosts, except for S. gibbus, which only had infestation on its integument. Differences in the prevalence and abundance of this corallanid only occurred in P. falcata, which were greater during the rainy season (Table 3). In G. proximus, infestations occurred only during the rainy season, but the number of hosts examined was low.

In A. ucayalensis, A. falcirostris, H. unimaculatus, S. gibbus, G. proximus and P. falcata, there was seasonal fluctuation of E. berbicensis, with highest prevalence in April and highest abundance in April and August (Fig. 2). Considering all the hosts examined, 262 specimens of E. berbicensis were collected during the dry season and 600 during the rainy season.

The Kn of the hosts parasitized by E. berbicensis did not differ between the grouped hosts (overall), or between the rainy season and dry season (Table 4). In addition, for A. falcirostris (t = -0.014; P = 0.989), A. ucayalensis (t = -0.058; P = 0.954), H. unimaculatus (t = 0.006; P = 0.995), P. falcata (t = -0.005; P = 0.996) and S. gibbus (t = -0.155; P = 0.877), the grouped Kn also did not differ from the standard (Kn = 1), thus indicating that the hosts presented good body condition.


In P. falcata, the levels of infestation by E. berbicensis were greater during the rainy season. Similar seasonal patterns were reported for abundance of infestations by Dolops discoidalis Bouvier, 1899, D. bidentata Bouvier, 1899 (Malta, 1982), D. striata Bouvier, 1899 and D. carvalhoi Lemos de Castro, 1949 (Malta & Varella, 1983), in different fish of the Amazon region. Pech et al. (2010) also reported that seasonal fluctuation in rainfall levels influenced the levels of infestation by Argulus sp. and Ergasilus sp. in Cichlasoma urophthalmus Gunther, 1862 from Yucatan Peninsula (Mexico). In the Amazon region, the environmental conditions during the rainy season are favorable for reproduction of some ectoparasite species, thus providing opportunities for encountering infectious forms with their hosts and contributing towards completing their life cycle (Vital et al., 2011). However, in piranha Pygocentrus nattereri Kner, 1858, Serrasalmus spilopleura Kner, 1858 and S. marginatus Valenciennes, 1837 from Pantanal of Mato Grosso (Brazil), infestation by D. carvalhoi, Argulus elongatus Heller, 1857 and Argulus juparanaensis Lemos de Castro, 1950 was greater during the dry season (Carvalho et al., 2003).

Seasonal dynamics influence the environmental quality of different natural ecosystems such as the Araguari River basin, which has pH and dissolved oxygen levels that are lower during the dry season in the Amazon basin (Barbara et al., 2010). During the period of the present study, the water level in the reservoir of the Coaracy Nunes hydroelectric power plant was relatively constant during the entire year, as also were the water temperature, electric conductivity, dissolved oxygen, pH, turbidity and transparency, which were similar during the rainy and dry seasons. Thus, these factors did not influence the levels of infestation by E. berbicensis in A. falcirostris, A. ucayalensis, H. unimaculatus, G. proximus and S. gibbus. However, Alsarakibi et al. (2014) reported that the occurrence of A. japonicus Thiele, 1900 was strongly influenced by pH, temperature, biochemical oxygen demand, ammonia and dissolved oxygen levels in the water. In river reservoirs, such as the one of the present study, the reduction in water speed contributed towards decreasing the turbidity, which consequently could increase the population of parasite crustaceans, in comparison with the river itself (Morley, 2007). Carvalho et al. (2003) suggested that the behavior of S. marginatus favored greater levels of infestation by ectoparasite crustaceans in environments with higher turbidity. Water turbidity also negatively affects ectoparasite crustaceans, because particulate material in suspension can cause damage to filtration and to delicate feeding organs in planktonic stages (Morley, 2007). Therefore, crustacean ectoparasites seem to have strong interaction with the environment and host fish population, because these factors are directly involved in their different life cycles and may cause different responses to seasonal fluctuations in water levels.

The dry season was from September to February and the rainy season was from March to August. However, the lowest rainfall rates occurred from September to November and the highest rates occurred from March to May, while the months of June through to August and December through to February were transitional periods between the two seasonality seasons. Although the levels of infestation by E. berbicensis were influenced by seasonality only in P. falcata, it was found when considering all hosts together that the prevalence of this ectoparasite presented a peak in the month of April, while the abundance showed two peaks, one in April and the other in August. These results possibly indicate that there are two reproductive cycles for E. berbicensis: one occurring in the rainiest month (April) and the other at the beginning of the transition period (August). Furthermore, the prevalence and abundance peaks of E. berbicensis also coincided with the reproduction period of these fish in the Araguari River basin region (Favero et al, 2010). Massive infestation of E. tricornis occidentals was reported in E. striatus soon after their spawning (Semmens et al., 2006).

In the region from Costa Rica, Guzman et al. (1988) observed that E. tricornis occidentalis has a migration cycle over the course of the day, because were found mostly in the water column during the night and it migrates to the benthos during the day, particularly to coral habitats or rocky substrates, in areas under strong thermocline influence. Moreover, this marine corallanid presented an influence weaker during the dry season (December to February). The high densities of these corallanid parasites also suggested that there was a seasonal effect relating to the beginning of the dry season. These authors concluded then that the nocturnal migration of these ectoparasites might be a form of behavior aimed at saving resources and might be related to predation of this isopod by fish and planktonic invertebrates. Despite of the life history of E. berbicensis is still little known, almost 70% of the specimens of this parasite on fish we collected during the rainy season. Although the migration of E. berbicensis to the water surface was not evaluated here, it was also found that there was greater presence of these parasites during nighttime. However, this migratory pattern still needs to be investigated.

The condition factor is a quantitative parameter of fish wellbeing that is used in studies on the parasite-host relationship (Lizama et al., 2006; Guidelli et al., 2011; Vasconcelos & Tavares-Dias, 2014). It was not influenced by the rainy and dry seasons among the fish investigated here, due to low abundance of parasites. Similar results were reported for A. falcirostris and H. unimaculatus from eastern Amazon parasitized by E. turucuyus (Vasconcelos & Tavares-Dias, 2014). However, high infestation of E. tricornis occidentalis reduced the body condition of E. striatus in Costa Rica (Semmens et al., 2006), due to the high cost of parasitism to the hosts. Corallanid species have been considered to be temporary parasites that change hosts to feed (Bunkley-Williams & Williams Jr., 1998).

Therefore, the lack of studies on the biology of isopods of the genus Excorallana makes exact interpretation of their relationship with their hosts difficult.

In summary, since the physical and chemical characteristics of the artificial ecosystem investigated were relatively homogeneous, except for rainfall levels, this latter can be a factor causing the levels of infestation of E. berbicensis in P. falcata. Moreover, as P. falcata, A. falcirostris, A. ucayalensis, H. unima-culatus, G. proximus and S. gibbus presented seasonal variation of infestation by E. berbicensis on a temporal scale, and biological factors relating to these hosts and parasites seemed to be influencing these infestations.

Since homogeneous conditions among environmental parameters in the Amazon region are uncommon, additional studies using more than one seasonal cycle must be conducted to better comprehend the biology and ecology of this Corallanidae in fresh water. Investigation of whether the levels of infestation of E. berbicensis in fish in this long-established reservoir in the eastern Amazon are higher than the infestation in fish in the Araguari River is also needed, because water stability can restrict occurrences of these ectoparasites in different aquatic systems, i.e., infestations are possibly lower in fish in an environment of running water, like the Araguari River.

DOI: 10.3856/vol43-issue5-fulltext-13


The authors are grateful to the National Council for Technological Research and Development (CNPq), for the research scholarship granted to Tavares-Dias, M.; to ICMBio, for the authorization for fish specimen collection (License: 35636-1); and to Eletronorte-AP, for logistic support.


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Received: 22 June 2015; Accepted: 21 September 2015

Huann Carllo Gentil-Vasconcelos (1) & Marcos Tavares-Dias (1,2)

(1) Postgraduate Program on Tropical Biodiversity (PPGBIO) Federal University of Amapa Macapa, AP, Brazil (2) Aquatic Organism Health Laboratory, Embrapa Amapa, Rodovia Juscelino Kubitschek No 2600, 68903-419, Macapa, AP, Brazil

Corresponding Author: Marcos Tavares Dias (

Corresponding editor: Mauricio Lateria

Caption: Figure 1. Fish collection locality, in a reservoir from Araguari River basin, in the eastern Amazon region (Brazil).
Table 1. Body parameters of six fish of a reservoir from Araguari
River basin, in the eastern Amazon region (Brazil).


Fish species         Length (cm)         Weight (g)

Acestrorhynchus   18.2 [+ or -] 3.2   62.4 [+ or -] 36.0
Ageneiosus        16.3 [+ or -] 2.8   39.7 [+ or -] 18.3
Geophagus         14.4 [+ or -] 4.2   84.9 [+ or -] 77.5
Hemiodus          14.8 [+ or -] 2.3   51.5 [+ or -] 19.9
Serrasalmus       10.9 [+ or -] 2.5   26.9 [+ or -] 36.6
Psectrogaster     18.2 [+ or -] 3.9   138.4 [+ or -] 96.7

Season             Dry   Rainy

Fish species       N     N

Acestrorhynchus    44    18
Ageneiosus         48    15
Geophagus          4     10
Hemiodus           42    14
Serrasalmus        12    24
Psectrogaster      35    30

Table 2. Physical and chemical parameters of the water in a
reservoir from Araguari River basin, in the eastern Amazon
region (Brazil). Different values in the same column indicate
differences according to the Mann-Whitney test (U) at the 5%
probability level. Precipitation: rainfall. NTU: nephelometric
turbidity units.

                    Precipitation             Transparency
                         (mm)                     (m)

Dry season      87.6 [+ or -] 52.4 (b)    1.3 [+ or -] 0.3 (a)
Rainy season   317.5 [+ or -] 194.1 (a)   1.1 [+ or -] 0.1 (a)

                    Turbidity                  pH

Dry season     6.7 [+ or -] 1.9 (a)   6.2 [+ or -] 0.5 (a)
Rainy season   4.9 [+ or -] 2.1 (a)   6.5 [+ or -] 0.2 (a)

                   Conductivity             Temperature
                 (pS/[cm.sup.-1])          ([degrees]C)

Dry season     21.6 [+ or -] 2.8 (a)   28.9 [+ or -] 1.6 (a)
Rainy season   19.5 [+ or -] 0.9 (a)   26.5 [+ or -] 0.5 (a)

               oxygen (mg [L.sup.-1])

Dry season      5.2 [+ or -] 1.5 (a)
Rainy season    5.2 [+ or -] 0.5 (a)

Table 3. Seasonal variation of infestation by Excorallana
berbicensis in fish species in a reservoir from Araguari River
basin, in the eastern Amazon region (Brazil). P: prevalence,
MA: mean abundance, [chi square]: chi-square test for prevalence, U:
Mann-Whitney test for mean abundance, P: probability.

                      Dry season                Rainy season

Hosts fish         P            MA           P            MA
                  (%)                       (%)

Acestrorhynchus   15.9   0.9 [+ or -] 3.0   38.9   5.1 [+ or -] 17.3
Ageneiosus        33.3   1.7 [+ or -] 3.6   40.0   2.9 [+ or -] 17.4
Hemiodus          35.7   1.3 [+ or -] 3.6   7.1    0.5 [+ or -] 19.1
Psectrogaster     25.7   2.2 [+ or -] 4.3   53.3   6.8 [+ or -] 17.4
Serrasalmus       33.3   0.3 [+ or -] 4.3   12.5   0.1 [+ or -] 18.4
Geophagus          0            0           40.0   8.5 [+ or -] 11.8

Hosts fish         [chi       P       U     P

Acestrorhynchus    3.859    0.103   299.0   0.133
Ageneiosus         0.224    0.871   342.0   0.771
Hemiodus           4.200    0.087   215.0   0.135
Psectrogaster      5.206    0.043   373.0   0.045
Serrasalmus        2.217    0.297   114.0   0.314
Geophagus          2.240    0.134   12.0    0.129

Table 4. Relative condition factor (Kn) for fish species in
a reservoir from Araguari River basin, in the eastern Amazon
region (Brazil). Values in the same line with different
letters indicate differences according to the Kruskal-Wallis
test (H). P: probability.

Hosts fish               Overall                 Dry season

Acestrorhynchus   1.00 [+ or -] 0.06 (a)   1.00 [+ or -] 0.03 (a)
Ageneiosus        1.00 [+ or -] 0.07 (a)   1.00 [+ or -] 0.06 (a)
Hemiodus          0.99 [+ or -] 0.04 (a)   1.00 [+ or -] 0.03 (a)
Psectrogaster     1.00 [+ or -] 0.06 (a)   1.00 [+ or -] 0.04 (a)
Serrasalmus       1.00 [+ or -] 0.14 (a)   1.00 [+ or -] 0.11 (a)

Hosts fish             Rainy season          H       P

Acestrorhynchus   1.00 [+ or -] 0.09 (a)   0.272   0.873
Ageneiosus        1.00 [+ or -] 0.07 (a)   0.159   0.923
Hemiodus          1.00 [+ or -] 0.03 (a)   0.008   0.996
Psectrogaster     1.00 [+ or -] 0.05 (a)   0.091   0.955
Serrasalmus       1.00 [+ or -] 0.08 (a)   0.134   0.935

Figure 2. Seasonal fluctuation of infestation by Excorallana
berbicensis in fish species in a reservoir from Araguari River
basin, in the eastern Amazon region (Brazil). Values above each
column indicate the total number of hosts examined. Different
letters in each line indicate differences according to the Dunn
test (P < 0.05). * Indicate differences between prevalence
according to the [chi square] test (P < 0.05).

      Abundance   Prevalence

Feb   58           b
Apr   20           a
Jun   46           b
Aug   45
Oct   70           b
Dec   57

Note: Table made from bar graph.
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Title Annotation:Research Article
Author:Gentil-Vasconcelos, Huann Carllo; Tavares-Dias, Marcos
Publication:Latin American Journal of Aquatic Research
Date:Nov 1, 2015
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