Relative Condition Factor and Parasitism in Anostomid ﬁshes from the ﬂoodplain of the Upper Paraná River, Brazil

Veterinary Parasitology 177 (2011) 145–151

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Relative condition factor and parasitism in anostomid ﬁshes from the ﬂoodplain of the Upper Paraná River, Brazil

Gislaine Guidelli a,∗, Washington Luiz Gomes Tavechio a, Ricardo Massato Takemoto b, Gilberto Cezar Pavanelli b

a Universidade Federal do Recôncavo da Bahia (UFRB), Centro de Ciências Agrárias, Ambientais e Biológicas (CCAAB), Núcleo de Estudos em Pesca e Aquicultura (NEPA), Brazil b Universidade Estadual de Maringá (UEM), Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Brazil

article info abstract

Article history: Individuals of four species of Leporinus were captured in the floodplain of the Upper Paraná Received 26 July 2010 River and their metazoan parasites were collected. Fifty-eight taxa of ectoparasites and Received in revised form endoparasites were recorded: 31 in Leporinus lacustris,32inLeporinus friderici,28inLep- 19 November 2010 orinus obtusidens and 25 in Leporinus elongatus. The aim of this paper was to study the Accepted 23 November 2010 relationship between the host’s condition and the parameters of infrapopulations and infracommunities. The health of the host was represented by the relative condition factor (Kn). Keywords: Richness and number of individuals in the infracommunities of ectoparasites covariated Relative condition factor Ectoparasites with the Kn of the hosts in one species of fish. Some infrapopulations of ectoparasites Endoparasites covariated negatively and/or the mean Kn of parasitized individuals was lower than those Leporinus without parasites. The abundance in some infrapopulations of endoparasites covariated Floodplain positively with the Kn and/or the mean Kn of parasitized fish was better. These results may Paraná river be related to different transmission strategies used by ecto and endoparasites. © 2010 Elsevier B.V. Open access under the Elsevier OA license.

1. Introduction The condition factor, both relative or alometric, and the presence or abundance of certain species of parasites are The condition factor represents a quantitative indicator related variables (Ranzani-Paiva et al., 2000; Tavares-Dias of the well-being of fish (Vazzoler and de, 1996). Analysis et al., 2000; Lizama, 2003; Isaac et al., 2004). But often, of variations in this indicator between populations or indi- fish are naturally infected by many coexisting species that viduals can be used to demonstrate the effects of different demonstrate inter-relationships, i.e. each host individual factors, such as environmental quality and food resources harbors an infracommunity of parasites (sensu Bush et al., (Bolger and Connolly, 1989). Because it is a measure regard- 1997). Thus, it is also important to consider the effect of ing health, it can also be effective to indicate the effects these sets of species on the condition of the hosts. Accord- of parasites on their hosts, both in natural and confined ing to Brasil-Sato (1999), knowledge of the influence of this environments. mixed type of parasitism can be a useful tool in ichthyopar- asitology, in particular applied to fish farming. The studied species of the genus Leporinus harbor numerous species of parasites (Guidelli, 2006; Guidelli et al., 2006) and have potential or are already important for ∗ Corresponding author at: Universidade Federal do Recôncavo da aquaculture (Froese and Pauly, 2009). Knowledge of the Bahia, Centro de Ciências Agrárias, Ambientais e Biológicas, Rua Rui Bar- amplitude of fauna that these fish are capable of harboring, bosa, Campus Universitário, 44380-000 Cruz das Almas, Bahia, Brazil. Tel.: +55 75 3621 1558; fax: +55 75 3621 1558. as well as the indication of the possible effects that parasite E-mail address: [email protected] (G. Guidelli). species or communities may have on them are useful infor-

0304-4017 © 2010 Elsevier B.V. Open access under the Elsevier OA license. doi:10.1016/j.vetpar.2010.11.035 146 G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151 mation for handling these animals in captivity, especially of each parasite species. Analyses in the infrapopulations in regard to ectoparasites, monoxenic life cycles and infest- were applied to species with prevalence higher than 10%, ing forms that can be easily transported in water from one as suggested by Bush et al. (1990). The Mann–Whitney’s habitat to another. U-test with correction for ties – Z(U) – was used to This study aimed to evaluate how the infracommuni- test differences between the mean Kn of males and ties and infrapopulations of parasites of four species of females and parasitized and non-parasitized fish for each Anostomid fishes from the floodplain of the Upper Paraná species (Zar, 1996). The level of significance adopted was River are related to the condition of these hosts, repre- p < 0.05. sented by the relative condition factor (Kn). We chose to use the relative condition factor as an indicator of the health status of animals because this index is not affected by 3. Results reproductive events or the formation of gonads (Le Cren, 1951). Fifty-eight taxa of metazoan ecto and endoparasites were identified. Leporinus lacustris harbored 31 species, 2. Materials and methods Leporinus friderici 32, Leporinus obtusidens 28 and Leporinus elongatus 25 species. Taxa recorded in the four host species, Samplings of hosts were carried out between May 2001 sites of infection/infestation and parasitism indicators are and June 2004 in lentic, lotic and semilotic environments of presented in Table 1. the floodplain of the Upper Paraná River (22◦50–22◦70S The mean values of the host’s Kn for total sam- and 53◦15–53◦40W). Information about the study area ple are presented in Table 2, where the means for can be found in Thomaz et al. (2004). Fish were cap- males and females are also shown. The Kn did not dif- tured, labeled, placed in plastic bags and transported on fer significantly between males and females (L. lacustris: ice to the laboratory of the Advanced Research Base of the Z(U) = 1.776, p = 0.075–L. friderici: Z(U) = 1.849, p = 0.064–L. Research Nucleus in Limnology, Ichthyology and Aquacul- obtusidens: Z(U) = 0.693, p = 0.486–L. elongatus: Z(U)= ture (Nupélia), where they were identified for later record 0.477, p = 0.632). It also did not differ between hosts col- of biometric and sex data. lected in three types of environments (L. lacustris: H = 0.359, The necropsy of the hosts, collection, preservation p = 0.825–L. friderici: H = 1.410, p = 0.493–L. obtusidens: and preparation of ecto and endoparasites were con- H = 1.162, p = 0.559–L. elongatus : H = 0.812, p = 0.661). Thus, ducted based on methodology suggested by Eiras et al. all fish of each species were treated as one data set. (2000). The terms infracommunity and infrapopulation, Among the analyzed specimens of L. lacustris, 4 and as well as the infrapopulation descriptors (prevalence, 45 were unparasitized by ecto and endoparasites, respec- intensity and abundance) were used according to Bush tively. For L. friderici these numbers were 4 and 27, et al. (1997). All parasites were collected, counted and for L. obtusidens 4 and 17, and for L. elongatus 2 and recorded separately for each individual host. Richness in 9, respectively. The mean Kn ± standard deviation of infracommunities refers to the total number of parasite parasitized and unparasitized fish, respectively, were: species in each fish. The identification of parasite taxa L. lacustris, ectoparasites = 1.026 ± 0.181, 0.844 ± 0.500; was performed using specialized literature and consulting endoparasites = 1.040 ± 0.200, 0.978 ± 0.172; L. friderici, paratypes. ectoparasites = 1.005 ± 0.114, 1.043 ± 0.125; endopar- Values of the relative condition factor were obtained for asites = 1.006 ± 0.119, 1.008 ± 0.100; L. obtusidens, all individual as described by Le Cren (1951). With the loga- ectoparasites = 0.999 ± 0.107, 1.087 ± 0.062; endopar- rithms of the values of standard length (Ls) and total weight asites = 1.003 ± 0.113, 1.010 ± 0.094; L. elongatus, (Wt) of each individual host, the curve was adjusted for ectoparasites = 1.025 ± 0.282, 1.048 ± 0.196; endopar- Wt/Ls (Wt = a·Ltb) and the values of the regression coef- asites = 1.002 ± 0.237, 1.105 ± 0.388. ficients a and b were estimated. The values of a and b were used for estimating values theoretically predicted of body weight (We) by using the equation: We = a·Ltb. Then 3.1. Infracommunities the relative condition factor (Kn) was calculated, which corresponds to the ratio between the observed weight Mean richness in the infracommunities of ectoparasites and the theoretically expected weight for a given length of L. lacustris was 3.42 ± 1.84 (1–10) and of endoparasites (Kn = Wt/We). was 1.38 ± 1.23 (1–4), for L. friderici these values were The non-parametric test Kruskal–Wallis (H) was used to 3.12 ± 1.66 (1–7) and 1.52 ± 1.36 (1–6), for L. obtusidens test differences of the mean Kn between the environments 4.02 ± 2.48 (1–10) and 1.15 ± 0.98 (1–3) and L. elongatus in the floodplain of the Upper Paraná River, considering 2.87 ± 1.94 (1–9) and 1.56 ± 1.26 (1–4), respectively for that different biotopes can influence the Kn. To assess ecto and endoparasites. the relationship between infracommunities and infrapop- Correlating the Kn of the hosts with species richness and ulations of parasites with the relative condition factor, total number of individuals of ectoparasites, only L. lacustris the nonparametric Spearman’s rank correlation coefficient presented significant results. In this host, the more species (rs) was applied for the variables Kn of each parasitized and individuals of ectoparasites in the infracommunities, fish × total number of species in the infracommunities, the lower the Kn. For the other hosts the results were not Kn of each parasitized fish × total number of individuals significant. For endoparasites, no result of the correlation in the infracommunities and Kn of each fish × abundance between variables was considered significant (Table 3). G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151 147 – – – – – – 39) = – – – – – – MA MI ( n 7.69 0.41 5.33 – L. elongatus 25.6 5.25 20.5 % – MI 54) = 4.576.11 10.7 9.421.40 66.6 35.8 3.04 4.64 1.84 48.7 6.96 5.14 1.20 2.47 1.06 7.12 7.69 0.20 2.66 1.570.74 4.25 2.50 17.94.64 – 0.51 22.8 0.66 2.85 3.27 17.9 0.35 2.00 – MA ( n –––––– –––––– –––––– –––––– –––––– –––––– –––––– –––––– – –––––– –––––– –––––– –––––– –––––– 3.70 0.03 1.00 – 9.25 3.511.85 38.0 1.85 0.01 0.05 1.00 3.00 – – 1.85 0.01 1.00 – L. obtusidens 20.3 29.6 MI % – – – – – – – 104) – –––––––– –––––––– –––––––– –––––––– –––––––– –––––––– –––––––– –––––––– MA – – – – – – – = ( n 0.960.96 0.009 0.009 1.00 1.00 0.96 0.02 3.00 – – – – – – 1.92 0.01 1.00 6.73– 0.14 2.14 4.803.84 0.04 0.04 1.00 1.25 14.8 3.70 0.07 2.00 5.12 0.05 1.00 3.84 0.07 2.006.73 37.0 0.14 2.14– 20.3 – 1.92 0.01 1.00 1.92– 0.04– 2.50 – 6.73– 2.19 32.5 – – 5.76 0.38 6.66 – 1.925.76 0.18 0.11 9.50 2.00 1.85 0.01 1.00 2.56 0.05 2.00 50.9 1.96 3.84 46.2 10.5 0.82 7.81 40.7 61.3 150.6 28.2 4.35 15.4 L. friderici 28.8 0.49 1.70 46.115.358.6 2.6061.5 0.4335.6 4.39 5.64 2.54 2.81 2.38 7.49 53.7 4.14 42.5 6.70 64.8 11.2 20.9 56.4 4.69 8.31 % 13.4 0.90 6.71 3.70 0.03 1.00 5.12 0.10 2.00 – – – – – – – – – – – – – – – – 150) MA MI – – – – – – – – – – – – – – – – = ( n collected between May 2001 and June 2004, in the floodplain of the Upper Paraná River, Brazil, with their respective prevalences (%), mean abundances 0.66 0.006 1.00 0.660.66 0.006 0.006 1.00 1.00 0.660.66 0.02 0.0060.66 3.00 1.00 0.0060.66 1.00 0.006 1.00 – – 8.66– 0.10–––7.69 –––––– 1.15 6.00 0.20 0.10 2.66 – 1.77 1.33– – 0.024.00– 1.50 – 2.51– – – 62.8 – –––2.56 –––––– 0.128.00 5.00 0.14–––2.56 –––––– – 1.83 0.02– – – 1.00 20.0 0.25 1.26 % 33.311.3 0.96 0.22 2.90 2.00 32.023.362.0 1.0922.6 0.6034.6 10.3 3.41 48.0 0.62 2.57 1.50 16.6 2.54 2.76 4.34 5.29 34.0 7.78 22.9 18.012.6 0.32 0.18 1.77 1.42 L. lacustris Leporinus C I C ,PC * I, C I, C ,SB I, C S G I I , 2, Go, Me, M , 1, M, Me, SB, AT sp.* G ,VC NC ,G G G G G ,Go ,Me I, C ,Me G G sp.* * I ,VC S sp.* G G G G I S, C I ,VC sp.* sp.* Type 1* sp. 3 sp. 1 sp. 2 sp. 4 UB, MD sp.* sp. 1 sp. 2 sp. sp. sp. 2 sp. 3 sp. 1 sp. 4 UB, MD sp.* G G sp. sp. 2 sp. 1 Tereancistrum Creptotrema creptotrema Cystodiplostomum Tylodelphis Brevimulticaecum Eustrongylides Proteocephalus vazzolerae Cystidicoloides Cleidodiscus Cleidodiscus Urocleidoides Urocleidoides Jainus Kritskyia eirasi Kritskyia Megacoelium Capillostrongyloides sentinosa Chalcinotrema thatcheri Ancyracanthus schubarti Urocleidoides paradoxus Saccocoelioides magnus Contracaecum Tereancistrum Jainus Clinostomum complanatum Diplostomum Cleidodiscus Tereancistrum Cleidodiscus Saccocoelioides saccodontis Saccocoelioides magniovatus Goezia spinulosa Echinostomatidae* Herpetodiplostomum Dycheline leporini Rhinoxenus arietinus Creptotrema lynchi Tereancistrum Tereancistrum parvus Creptotrema Neodiplostomum Paralecithobotrys brasiliensis Goezia brevicaeca Cestoda Digenea Nematoda Parasite taxa Monogenea Table 1 Taxa of metazoan parasites of four species of (MA), mean intensities (MI) and sites of infection/infestation. 148 G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151

Table 2 Mean relative condition factor (Kn) and standard deviation of four species – – of Leporinus from the ﬂoodplain of the Upper Paraná River, Brazil, from May 2001 to June 2004.

Hosts Total sample Male Female

39) L. lacustris 1.022 ± 0.194 1.068 ± 0.241 0.992 ± 0.162 = – – MA MI L. friderici 1.007 ± 0.114 1.030 ± 0.118 1.001 ± 0.109 ( n L. obtusidens 1.125 ± 0.192 0.958 ± 0.094 1.259 ± 1.596 L. elongatus 1.026 ± 0.276 1.030 ± 0.272 1.021 ± 0.288 L. elongatus %

3.2. Infrapopulations

Among ectoparasites, the monogenean Urocleidoides MI paradoxus and the copepod Gamispatulus schizodontis had their abundances negatively correlated with the Kn of L. obtusidens and L. elongatus, respectively. Furthermore, the

54) mean Kn of individuals parasitized and non-parasitized 0.68 4.11 2.56 0.07 3.00 = MA

( n by these species differed significantly, with parasitized individuals presenting lower mean Kn. The mean Kn of individuals of L. lacustris parasitized by Jainus sp. 1 was also significantly lower than that of individuals parasitized by Moravec (1998) . G = gills, SB = swimming bladder, C = caeca, NC = nasal cavity, –––––– 3.70 0.12 3.50 5.12 0.51 10.0 3.70 0.031.85 1.00 0.01 – 1.00 5.12 0.05 1.00 L. obtusidens other species (Table 4). Significant correlations were not observed for other hosts. Among endoparasites, Procamallanus (Spirocamallanus) inopinatus in L. friderici and Herpetodiplostomum sp. in L. – – – MI % obtusidens had their abundances positively correlated with the Kn of the hosts. In L. obtusidens and in L. lacustris the means of Kn were significantly higher in individuals parasitized by Herpetodiplostomum sp. (Table 4). 104) –––––––– –––––––– –––––––– – MA – – = ( n 4. Discussion 0.96 0.009 1.00 0.960.96 0.009 0.01 1.00 2.00 3.70 3.70 0.03 0.05 1.00 1.50 – 2.56 0.02 1.00 8.65 0.13 1.55– 7.40– 0.24 3.25 23.0 2.48 10.7 L. friderici % 19.2 0.33 1.75 7.40 0.33 4.50 25.6Negative 4.28 effects 16.7 on the hosts are expected, because they are inherent in parasitism. These effects have a direct influence on the reproduction and feeding conversion effi- ciency, and therefore on the maintenance of health (Gibbs, – – – – – – – 1985). However, the possible effects that pathogens have larva of Moravec, Kohn and Fernandez (1995) both cited by 2 on their hosts are difficult to assess or quantify, especially in fish under natural conditions. Chubb (1973) highlighted that due to the ubiquity of parasites, a major difficulty is to 150) – – – – – – – MA MI = define a normal or control to compare parasitized individ- ( n uals. Brasil-Sato (1999) and Lizama (2003), among others, suggested that the relative condition factor of fish, being a 0.66 0.0060.66 1.00 0.006 – 1.00 – – 2.56––––––––– – 0.02– 1.00 1.33– 0.02– – – 1.502.002.00 – 0.12 0.07 6.00 3.66 – 0.96 0.009 1.00 16.6 20.6 0.33 1.61 29.8 0.65 2.19 1.85 0.01 1.00 7.69 0.07 1.00 % 68.6 7.52 10.9 26.9 1.86 6.92 68.5 30.2 44.1 28.2 1.64 5.81 L. lacustris measure or a quantitative indicator of welfare, can serve as a tool to study the relationship between health and natural parasitism. There are many studies on the effects of certain species of parasites on the condition of their hosts. But often, fish I, C are parasitized by several species that form communities. I I NC According to Chubb (1973), each of these many species con- ,L,Me * larva of Moravec, Prouza, and Royero (1997) and ,SB G 1 tributes to the stress on the host population and, therefore, NC iheringi inopinatus sp. sp.* G ,SB it is important to consider the influence of the whole set of ( Spirocamallanus ) ( S. ) ( S. ) ,NC , NC, G

sp.* species of parasites. BS, NC, G ,G

I, C Negative and signiﬁcant covariations observed between sp. 2** sp. 1** sp.** the Kn of L. lacustris and richness and the number of specimens of ectoparasites indicate that hosts with lower Kn amarali Vaigamidae gen. n. Octospiniferoides incognita Dolops nana Procamallanus Porrocaecum Dolops Gamispatulus schizodontis Hysterothylacium Quadrigyrus torquatus Argulus Argulus Procamallanus Procamallanus Amplexibranchius Ergasilus bryconis harbored more species and more individuals of parasites. Acanthocephala Parasite taxa Crustacea Table 1 ( Continued ) * Larval forms; ** young; PC = pericardic cavity, VC = visceralbladder, cavity, MD S = = mesonefric stomach, duct. L = liver, Go = gonads, I = intestine, M = muscles of stomachThese and/or intestine, Me = mesentery, BS = body surface, AT = perivisceral adipose tissue, UB = urinary correlations can then be evidence of possible nega- G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151 149

Table 3 Values of Spearman’s rank correlation coefﬁcient (rs) between the relative condition factor (Kn) of individuals of four species of Leporinus from the ﬂoodplain of the Upper Paraná River, Brazil, and the number of species (NS) and individuals (NI) of metazoan ecto and endoparasites in each infracommunity.

Hosts Ectoparasites Endoparasites

NS NI NS NI

rs p rs p rs p rs p

L. lacustris −0.189* 0.020 −0.171* 0.036 0.112 0.171 0.138 0.090 L. friderici −0.006 0.940 0.055 0.574 0.148 0.132 0.117 0.233 L. obtusidens −0.258 0.059 −0.214 0.118 0.188 0.173 0.153 0.268 L. elongatus −0.197 0.227 −0.110 0.502 0.006 0.968 0.069 0.675

* Values signiﬁcant at 95% probability.

tive effects of a group of species parasitizing individuals of several species of ecto and endoparasites and some possi- L. lacustris. ble influences of them. However, the relative condition factor is an indicator For the negative significant correlations between Kn of health that also reflects recent nutritional conditions and abundance of ectoparasites in L. obtusidens and L. (Vazzoler and de, 1996). According to Rohde (1993), elongatus and lower mean Kn of parasitized individu- immune responses of fish are dependent on nutrition, als of these species and of L. lacustris, one can propose among other things. Thus, an alternative explanation for that hosts with worse health condition could also be these negative relations between these variables would easier targets for these parasites that present the active be that individuals in better conditions, healthier, would route of transmission. Ectoparasites usually infect their be able to react more effectively to infestation by most hosts actively, in contrast to endoparasites that mostly species of ectoparasites, which their immune systems infect using the food chain. Moreover, the presence of were able to combat. This way they would be parasitized gill ectoparasites in high abundances can impair breath- mainly by those ectoparasites that showed a more adjusted ing (Pavanelli et al., 2008) and, consequently, all other relationship, which were less pathogenic or those whose activities necessary for the maintenance of good health as mechanisms of escape from the host immune system are nutrition, for example, with implications on the Kn. Two more effective, characteristics that should arise over co- species of ectoparasites with significant results are mono- evolutionary processes. In contrast, fish in worse condition geneans. should be more susceptible to infection by several species. Negative effects of endoparasites on the condition of the Allied to this, many of the parasites observed in L. lacus- hosts are widely known and expected (Bauer, 1970; Lemly, tris are rare or accidental, what may represent recent or 1980; Tavares-Dias et al., 2000). These effects, according unstable relationships, for which the fish would have less to Bauer (1970) are more prominent in infections by lar- capacity to specific reaction. vae. There are, on the other hand, many reports of better The lack of significant covariations between parame- relative condition factor among fish infected with endopar- ters of infracommunities of endoparasites and Kn, unlike asites (Lizama, 2003; Isaac et al., 2004; Machado et al., for ectoparasites, could be explained by the different 2005). In the present study this type of covariation between forms in which endo and ectoparasites are related to the abundance of P. (S.) inopinatus and Kn in individuals their hosts, both by the way of acquisition of the infes- of L. friderici was also observed. In addition, considering tation, as by the possibility of ectoparasites being more endoparasites, we found that individuals of L. lacustris pathogenic. Differential capacity of immune response to infected by Herpetodiplostomum sp. had, on average, higher ectoparasites and endoparasites could also generate these Kn, possibly because individuals with better Kn were able results. According to Bryant and Behm (1988), the per- to resist to the abundant infections by Herpetodiplosto- formance of the immune system differs between the mum sp. Despite being a larva, Herpetodiplostomum sp. may organs and tissues and, according to Williams and Jones not cause significant pathology and reduction in the Kn of (1994) and Whittington et al. (2000) fish have effec- the host as expected. This may occur because the organ tive immune mechanisms against ectoparasites such as parasitized by the metacercaria is not directly related to monogeneans. vital functions and because the larva remains free in this The occurrence of only one significant association organ. between the Kn and the number of species and individuals In the case of P. (S.) inopinatus that is acquired through must be due to little variation in the Kn between individu- the food chain, the highest Kn presented by the more als of the four species of hosts. Thus, despite the observed heavily infected fish may be due to the fact that fish that significant covariation, the Kn seems to have been greatly consume larger quantities of food and can display bet- influenced by the characteristics of the infracommunities ter health, may also have eaten more infective forms of of parasites. Considering the low variation of the Kn, we these parasites that use the trophic route of transmission. can propose that the environmental conditions during the This is more likely if the immune system does not act study period should have provided adequate conditions for effectively on intestinal parasites or if the pathogenesis the majority of individuals of these species of fish to gain or the expected effects of infection by intestinal para- weight appropriately to their sizes in spite of parasitism by sites are small. According to Rohde (1993), these effects 150 G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151

Table 4 Spearman’s rank correlation (rs) between the abundance of the ectoparasite and endoparasite species and the Kn of individuals of four Leporinus species from the Upper Parana River ﬂoodplain, Brazil; Mann–Whitney’s U-test, with correction for ties Z(U) to compare the averages of Kn of parasitized and unparasitized ﬁsh. For species that present prevalence > 10% according to Bush et al. (1990).

Hosts Parasite species rs pZ(U) P Kn parasitized Kn unparasitized

L. Ectoparasites lacus- Cleidodiscus sp. 1 −0.079 0.336 1.006 0.314 1.014 1.025 tris Cleidodiscus sp. 2 −0.037 0.650 0.468 0.639 1.011 1.023 G. schizodontis −0.116 0.154 0.417 0.676 1.013 1.040 Jainus sp. 2 −0.063 0.442 0.819 0.412 1.021 1.022 Jainus sp. 1 −0.110 0.178 2.478* 0.013 1.003 1.053 R. arietinus 0.0007 0.992 0.389 0.697 1.012 1.031 Tereancistrum sp. 1 −0.026 0.750 0.269 0.810 1.015 1.023 Urocleidoides sp. 1 −0.142 0.081 1.490 0.136 1.030 1.019 U. paradoxus −0.106 0.193 1.072 0.313 1.010 1.027 Endoparasites Brevimulticaecum sp. 0.053 0.515 0.574 0.565 1.038 1.018 Contracaecum sp. 0.042 0.609 0.593 0.553 1.044 1.019 Herpetodiplostomum sp. 0.142 0.081 2.009* 0.044 1.046 1.009 K. eirasi 0.091 0.264 1.143 0.252 1.055 1.004 P. (S.) inopinatus 0.078 0.341 0.951 0.341 1.075 1.008

L. friderici Ectoparasites G. schizodontis −0.111 0.260 1.424 0.154 0.975 1.019 Jainus sp. 1 −0.076 0.439 1.178 0.238 0.996 1.022 Jainus sp. 2 −0.094 0.339 0.735 0.462 1.002 1.014 R. arietinus 0.058 0.554 0.380 0.703 1.009 1.005 Tereancistrum sp. 2 0.129 0.190 1.549 0.121 1.029 0.997 Urocleidoides sp. 1 0.137 0.164 1.504 0.132 1.005 0.998 U. paradoxus 0.001 0.990 0.110 0.911 1.007 1.007 Endoparasites Herpetodiplostomum sp. 0.033 0.734 0.185 0.853 0.996 1.008 K. eirasi 0.063 0.521 0.723 0.469 1.019 1.000 P. brasiliensis 0.049 0.618 0.438 0.661 1.021 1.004 P. (S.) iheringi −0.168 0.087 1.534 0.125 0.976 1.014 P. (S.) inopinatus 0.195* 0.046 1.709 0.087 1.038 0.994

L. Ectoparasites obtusi- G. schizodontis −0.132 0.338 1.443 0.148 0.995 1.029 dens Jainus sp. 1 −0.167 0.226 1.584 0.113 0.990 1.035 R. arietinus −0.056 0.685 0.095 0.924 1.002 0.976 Tereancistrum sp. 3 −0.134 0.333 0.814 0.415 0.983 1.204 T. parvus −0.078 0.573 0.734 0.462 0.991 0.975 U. paradoxus −0.327* 0.015 2.558* 0.010 0.980 1.035 Urocleidoides sp. 2 −0.065 0.636 0.375 0.707 1.031 0.999 Urocleidoides sp. 1 −0.260 0.056 1.793 0.073 0.977 1.027 Vaigamidae −0.017 0.902 0.011 0.990 1.003 1.006 Endoparasites Brevimulticaecum sp. 0.105 0.447 0.608 0.542 1.017 1.004 Herpetodiplostomum sp. 0.267* 0.050 2.024* 0.042 1.033 0.987 Kritskyia sp. −0.085 0.539 0.569 0.569 1.026 1.001

L. Ectoparasites elon- Urocleidoides sp. 1 0.078 0.633 1.221 0.221 1.065 0.947 ga- T. parvus −0.256 0.114 1.610 0.107 0.892 1.055 tus Jainus sp. 1 −0.167 0.307 0.966 0.334 1.006 1.037 U. paradoxus −0.082 0.619 0.509 0.610 1.009 1.048 G. schizodontis −0.364* 0.022 2.278* 0.022 0.902 1.075 R. arietinus 0.071 0.667 0.168 0.866 1.067 0.986 Endoparasites C. creptotrema 0.010 0.948 0.096 0.923 0.982 1.041 Herpetodiplostomum sp. −0.135 0.411 0.686 0.492 0.955 1.054 Kritskyia sp. −0.185 0.258 0.988 0.323 0.928 1.047 P. (S.) iheringi 0.175 0.284 1.029 0.303 1.031 1.024 P. (S.) amarali 0.211 0.195 1.133 0.257 1.019 1.028

* Signiﬁcant values to the 95% level of probability.

include inhibiting the action of vitamins, digestive activity, 5. Conclusion metabolism and growth. Isaac et al. (2004) observed similar correlations between the abundance of nematodes and Infracommunities of ectoparasites seem to have neg- the Kn of ﬁsh in the same ﬂoodplain. ative effect on the condition of some studied species of G. Guidelli et al. / Veterinary Parasitology 177 (2011) 145–151 151

Leporinus, mainly L. lacustris and L. obtusidens. But it is also Froese, R., Pauly, D. (Eds.), 2009. FishBase: World Wide Web elec- possible that healthier fishes are resistant to infestation tronic publication, 2008, Accessed in: April 13, 2009 http://www. fishbase.org. by different species. Experimental investigations on the Gibbs, H.C., 1985. Effects of parasites on animal and meat production. In: interactions between parasites and possible synergies are Gaafar, S.M., Howard, W.E., Marsh, R.E. (Eds.), World Animal Science necessary. B2: Parasites, Pests and Predators. Elsevier, Holanda, pp. 7–27. Guidelli, G.M., 2006. Comunidades parasitárias em espécies de peixes con- Ectoparasites and endoparasites, both in infracommu- genéricas de diferentes categorias tróficas e ambientes da planície de nities and infrapopulations, with some exceptions, are inundação do Alto rio Paraná. Ph.D. Thesis, State University of Maringá, inversely related to the condition of the hosts of the genus Brazil, 69 pp. Leporinus in natural environments. The majority of ectopar- Guidelli, G.M., Tavechio, W.L.G., Takemoto, R.M., Pavanelli, G.C., 2006. Fauna parasitária de duas espécies de Leporinus da planície de asites were negatively related with the condition factor. In inundação do Alto rio Paraná. Acta Sci. 28 (3), 281–290. contrast, most of the endoparasites tended to relate pos- Isaac, A., Guidelli, G.M., França, J.G., Pavanelli, G.C., 2004. Composiçãoe itively with this health indicator. This may be related to estrutura das infracomunidades endoparasitárias de Gymnotus spp. (Pisces: Gymnotidae) do rio Baía, Mato Grosso do Sul, Brasil. Acta Sci. infection/infestation strategies of these two categories of 26 (4), 453–462. parasites. Le Cren, E.D., 1951. The length-weight relationship and seasonal cycle in gonad weight and condition perch Perca fluviatilis. J. Anim. 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