Effects of impoundment on the body condition of fish in the Manso reservoir, Mato Grosso State, Brazil

Efeitos do represamento sobre a condição nutricional de peixes no reservatório de Manso, Mato Grosso, Brasil

Effects of impoundment on the body condition of fish in the Manso reservoir, Mato Grosso State, Brazil

Efeitos do represamento sobre a condição nutricional de peixes no reservatório de Manso, Mato Grosso, Brasil

Sandra Maria Lopes de Moura^I; Elaine Antoniassi Luiz Kashiwaqui^II; Norma Segatti Hahn^I

^INúcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais, Universidade Estadual de Maringá - UEM, Av. Colombo, 5790, CEP 87020-900, Maringá, PR, Brazil, e-mail: [e-mail]; [e-mail]

^IIGrupo de Pesquisa em Ciências Ambientais e Educação - GEAMBE, Universidade Estadual de Mato Grosso do Sul - UEMS, BR 163, Km 20,2, Bairro Universitário, CEP 79980-000, Mundo Novo, MS, Brazil, e-mail: [e-mail]

ABSTRACT

AIM: This study evaluated the body condition de Acestrorhynchus pantaneiro, Auchenipterus osteomystax, Pimelodus maculatus, Psectrogaster curviventris and Schizodon borellii in the Manso reservoir, Mato Grosso State, Brazil, during the first years after its formation (years I, II, III and IV). We hypothesized that sudden environmental changes alter differently the body condition, according to the time (sampling years) and sex of individuals. Also, we checked the influence of the amount of food ingested and the reproductive status on nutritional status of the species.

METHODS: The body condition (Kn), the feeding activity (SRI) and reproductive (GSI) were calculated only for adults. The difference between the sampling years and sexes (used as factors) was assessed using the nonparametric Kruskal-Wallis test. Temporal influence was tested by Spearman correlation and the interaction between both factors by PERMANOVA.

RESULTS: The values of the Kn showed two groups: group 1: species whose body condition decreased in the year II, with a posterior increase (A. pantaneiro, P. curviventris and S. borelli), considered sensitive to the reservoir filling; group 2: species whose body condition increased in the year II (A. osteomystax and P. maculatus), indicating a more rapid adaptation to new environmental conditions. Still, all parameters investigated were somehow affected by the dam, mainly the body condition and gonadosomatic index for several species. On the other hand, the least affected factor was the feeding activity.

CONCLUSIONS: The results did not evidence a same pattern of either increase or decrease of body condition for all species examined, since everything indicates that responses are species-specific. Even with a lack of consistency in some results, we can draw some suggestions for future investigations. Responses to these questions will certainly contribute to aggregate data to help better explain the body condition of fish species in dammed environments.

Keywords: dominant fish fauna, nutritional status, environmental impact, tropical reservoir.

RESUMO

OBJETIVO: O objetivo deste estudo foi avaliar a condição nutricional de Acestrorhynchus pantaneiro, Auchenipterus osteomystax, Pimelodus maculatus, Psectrogaster curviventris e Schizodon borellii no reservatório de Manso, MT, Brasil, durante os primeiros anos após a sua formação (anos I, II, III e IV). Partimos da premissa que, mudanças ambientais repentinas alteram de forma diferente a condição nutricional, de acordo com o tempo e o sexo dos indivíduos. Nós predizemos também que a quantidade de alimento ingerida e o estado reprodutivo são fatores que interferem na condição.

MÉTODOS: A condição nutricional (Kn), a atividade alimentar (IR) e reprodutiva (GSI) foram calculadas somente para indivíduos adultos. As diferenças entre os anos de coleta e sexo (usado como fator) foram testadas através do teste não paramétrico de Kruskal-Wallis, enquanto que a influência temporal foi testada pela Correlação de Spearman e a interação entre ambos pela PERMANOVA.

RESULTADOS: Com os resultados do Kn observam-se dois grupos: grupo 1- espécies cuja condição decresceu no ano II, aumentando nos anos subsequentes (A. pantaneiro, P. curviventris e S. borelli) podendo ser consideradas mais sensíveis ao alagamento; grupo 2- espécies cuja condição aumentou no ano II (A. osteomystax e P. maculatus), mostrando uma adaptação mais rápida as novas condições ambientais. Ainda, os parâmetros avaliados foram influenciados ao longo dos anos, especialmente o fator de condição e a atividade reprodutiva. A atividade alimentar foi o fator com menor influência temporal.

CONCLUSÕES: Os resultados não evidenciaram um mesmo padrão, seja ele de acréscimo ou decréscimo do Kn para todas as espécies, como era esperado, pois tudo indica que as respostas sejam de natureza espécie-específica. Entretanto, a falta de consistência de alguns resultados permitiu levantar algumas suposições para estudos futuros, cujas respostas certamente contribuirão para agregar dados que ajudem a explicar as variações no Kn dos peixes em ambientes represados.

Palavras-chave: ictiofauna dominante, condição nutricional, impacto ambiental, reservatório tropical.

1. Introduction

The nutritional status reflects the health or overall welfare of an animal and is usually associated with physiological parameters related to energy storage in tissues, in the form of carbohydrates, lipids and proteins (Le Cren, 1951).

The energy stored can be measured by diverse criteria that include physiological (weight of liver and gonads), biochemical (lipid or protein content) and morphometric (weight-length) measurements (Lloret et al., 2002). Among morphometric ones, stand out the body condition factors or indices.

Body condition was firstly developed for fish, in order to estimate, indirectly, the energy reserves in tissues from its weight and its length (Bolger and Connolly, 1989; Nash et al., 2006). It is assumed that individuals with greater weight in a given length are in better condition, with growth and survival rates, and reproductive potential higher than those in worst condition, under comparable environmental conditions (Pope and Kruse, 2001).

The nutritional status of the fish can be influenced by abiotic (Oliva-Paterna et al., 2003; Bojsen, 2005; Araújo et al., 2011) and biotic factors (Lima-Junior and Goitein, 2004; Felizardo et al., 2011). In this way, to survive and leave offspring in active systems such as rivers, fish populations face many challenges and respond to changes in the environment with changes in their metabolism. In other words, fish begin to allocate part of the energy to be invested in the maintenance, growth and reproduction to minimize the effects of changing environmental conditions (Wootton, 1998), thereby compromising their nutritional status.

One of the most prominent environmental changes in continental waters is impoundments of rivers. Although important for economic development, they promote irreversible changes in the natural hydrological regime, also altering habitat quality and the dynamics of the whole biota (Baxter, 1977; Agostinho et al., 2008), including fish assemblage.

The initial stages of reservoir formation are highly productive increasing the food supply (Williams et al., 1998; Mérona et al., 2003). Thus, the high food availability in this period possibly affected the nutritional status of fishes. On the other hand, this high availability does not ensure improvements in the nutritional status of fish, considering the quality of the food available (Abujanra et al., 2009) and the ability of fish in using this food. Also, the low nutritional quality of the food negatively affects the reproduction, important for successful colonization and persistence of species in reservoirs (Agostinho et al., 1999).

In this context, the present study assessed five fish species, with distinct feeding habits, based on the assumption that sudden changes in environmental conditions caused by the formation of reservoirs affect the body condition of the fish differently (increasing or decreasing), according to time (sampling years) and sexes (male and female). We also assumed that the amount of food consumed and the reproductive status interfere with the nutritional status of the fish species.

2. Material and Methods

2.1. Study area

The Manso reservoir localized close city Cuiabá, Mato Grosso, formed in November 1999 (the filling phase was short - from November to February), was built on the Manso River (14°32'-15°40'S and 54°40'-55°55'W), in the Cuiabá River basin (State of Mato Grosso, Brazil) (Figure 1). This is the most important river forming the Cuiabá River, which presents a dense drainage network and a regular rainfall regime and flows into the Pantanal of Mato Grosso, one of the largest wetlands of the world. The reservoir has an area of 427 km². The main purpose of this reservoir is the hydropower generation and regulation of flood and drought cycles, in order to protect large cities downstream.

2.2. Fish sampling

Fish were sampled monthly from March 2000 to February 2001 (year I, shortly after the filling of reservoir), March 2001 to February 2002 (year II), March 2002 to February 2003 (year III) and March 2003 to February 2004 (year IV), in six fixed sampling sites, distributed across the Manso reservoir (Figure 1). Fish were collected by a set of gillnets with different mesh sizes (2.4, 3, 4, 5, 6, 7, 8, 9, 10, 12, 14, 16, 18 cm, opposite knots). Nets were assembled simultaneously in open areas, littoral areas and bottom during 24h and fish were removed in the morning, evening and at night. The fishing effort was the same in all sampling sites and during all study period.

Immediately after capture, all individuals were identified, measured (standard length, cm), and weighed (total weight, and gutted weight, g). For the identification of the sexes, gonads were evaluated by visual observation. We also weighed the stomachs (g) and gonads (g).

Representative specimens of the five studied species were deposited in the Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia, Universidade Estadual de Maringá, State of Paraná) with the following catalog number: Acestrorhynchus pantaneiro Menezes, 1992 (Characiformes, Acestrorhynchidae) - NUP 874; Auchenipterus osteomystax (Miranda-Ribeiro, 1918) (Siluriformes, Auchenipteridae) -NUP 928; Pimelodus maculatus La Cepède, 1803 (Siluriformes, Pimelodidae) - NUP 880; Psectrogaster curviventris (Eigenmann and Kennedy, 1903) (Characiformes, Curimatidae) - NUP 896 and Schizodon borellii (Boulenger, 1900) (Characiformes, Anostomidae) -NUP 873.

2.3. Data analysis

The body condition was calculated only for adult individuals, through the relative body condition factor (Kn), for each sampling year and sex, using the formula Kn = W / a * Ls, where W is the weight (gutted weight, g), a and b are parameters of length-weight relationships and Ls is the standard length (cm). Parameters a and b were estimated after logarithmic transformation of length and weight data. In agreement with Le Cren (1951) it is relatively easy to eliminate the effect of length on K and correlated factors, by calculating a "condition factor", which is not based on the "ideal" weight-length relationship (W=aL), but rather on an empirical weight-length relationship (W=aL). On the other hand, the relative body condition factor allows comparisons between different length classes within a single sample, because it represents a real population variation around the average value of the body condition (Baigún et al., 2009).

Beyond the condition factor were analyzed feeding activity and reproductive. Feeding activity was obtained through the stomach repletion index [SRI = (WE / WT) * 100, where, WE is the stomach weight (g) and WT, the total weight (g)]. Reproductive activity was calculated using the gonadosomatic index [GSI = (WG / WT) * 100, where WG is the gonadal weight and WT, total weight].

The difference between the sampling years (used as factors) by sexes was assessed using the nonparametric Kruskal-Wallis (KW) test (the assumptions of homogeneous variances and normality were tested) (Zar, 1999). If significant differences were detected, the pos hoc test multiple comparisons z' values were conducted to determine where the difference occurred. The relationship between body condition (Kn) and the feeding and reproductive activity was assessed by the Spearman rank correlation (Zar, 1999). The permutational multivariate analysis of variance (PERMANOVA, Anderson, 2005) was used to detect any differences in the condition factor, stomach repletion index and gonadosomatic index, between the sexes. In this analysis, year and sexes were treated as factors. The PERMANOVA was run using the software PAST (2.17) (Hammer et al., 2001). All the other analyses and graphs were made using the software STATISTICA 7.0.

3. Results

A total of 11,403 individuals of five species were analyzed. Numerical abundance and feeding habit of each species during all studied period is showed in the Table 1.

Acestrorhynchus pantaneiro showed significant differences in the Kn for both sexes. The condition decreased from the year II. However, females showed a recovery in the year III, similar to values recorded in the year IV (H=1106.70; p<0.01). The males returned to higher values only in the year IV (H=2425.72; p<0.01). For females, the multiple comparisons z' values test differentiated the years I and II from the others. For males, the post hoc test distinguished each year (Figure 2).

The feeding activity for both sexes decreased until the year III, with significant differences between the sampling years (H=652.98; p<0.01 females; H=677.86; p<0.01 males) (Figure 2). The investment in reproduction was also significantly different between the sampling years (H=837.10; p<0.01 females; H=423.90; p<0.01 males), females showed an increase and for males, the increase was small (Figure 2). SRI and GSI differed between the sampling years.

Auchenipterus osteomystax showed an increase in the Kn, for females, with significant variations between the years (H=478.73; p<0.01). For males, the variations were also different (H=518.65; p<0.01) with the highest value in the year III and the lowest in the next year (Figure 3). The post hoc test distinguished all years for both sexes.

The feeding activity was higher in the year II and declined in the following years (H=41.33; p<0.01 females; H=122.61; p<0.01 males), however the values were higher than in the year I (Figure 3). For females, this activity was different in the years II and IV from the other years, and for males, the year IV was different from the others. The reproductive activity of females showed little variation from the median values over the years, yet the differences were significant (H=214.03; p<0.01). To males the differences were significant (H=76.96; p<0.01), the values declined in the year II, being more intense in the year III and IV (Figure 3). Years II and IV were different for both sexes.

Pimelodus maculatus showed variations in the Kn. For females the values were significant (H=109.40; p <0.01); the years II and III were distinct from the years I and IV. The values were also different for males (H=133.44; p <0.01); the year III showed a high body condition, with significant differences between all years (Figure 4).

The feeding activity of females remained relatively constant over the years, but significant differences were found (H=31.73; p<0.01), revealing that the year II was statistically distinct. The years II and III were distinguished by the post hoc test (H=54.86; p<0.01) for males (Figure 4). The reproductive activity was different between years (H=35.81; p <0.01 females; H=40.20; p<0.01 males) since that the year II was different from the other years. For females, the highest value was registered in the year I, and for males remained relatively constant over the years (Figure 4).

Psectrogaster curviventris revealed a similar pattern between the sexes, with a drop in the Kn in the year III, and a increase in the year IV (H=588.98, p<0.01 females; H=362.41; p<0.01 males). For females, significant differences were detected between all the years and for males, the values were different in the year III (Figure 5).

The feeding activity for females (H=149.83; p<0.01) was differentiated and more intense (higher median) in the year I. For males (H=89.47; p<0.01), the greatest values were found in the year II (Figure 5). However, there was distinction between all years for both sexes. For reproductive activity the median values were significantly different (H=243.08; p<0.01 females; H=140.91; p<0.01 males), especially for the years I and III, for both sexes (Figure 5).

Schizodon borellii showed a similar pattern in the Kn for both sexes, with significant differences between sampling years (H=449.52; p<0.01 females; H=528.75; p<0.01 males). Regardless of sexes, there was a drop in the values in the year II, with a subsequent increase in the years III and IV (Figure 6). It is worth noting that the years were distinct from each other, for both sexes.

The highest feeding activity was found in the year I, and significant differences were found (H=46.69; p<0.01 females; H=39.45; p<0.01 males). The years II and III were different from the others, showing lower feeding activity to both sexes (Figure 6). The reproductive activity was different for both sexes (H=28.84; p<0.01 females; H=32.39; p<0.01 males), distinguishing the year IV from the others (Figure 6).

The temporal influence on the analyzed factors (Kn, SRI and GSI) was more evident for A. osteomystax (Table 2) according to the results of the Spearman correlation (r). There was a positive trend and significant correlation for females of this species, for all analyzed factors, mainly for the Kn. For males of this species, the Kn was negatively correlated with years, while SRI and GSI were positive (Table 2).

Females and males of P. maculatus also showed significant correlations between Kn and years analyzed. However, this correlation was negative for females and positive for males (Table 2); for other components evaluated (SRI and GSI) the correlations were positive, but GSI was not significant for males. Schizodon borellii was the species with lower correlation values (r), with emphasis on Kn of the females.

4. Discussion

After filling a reservoir there follows a heterotrophic phase, when all populations reach maximum densities (Straskraba et al., 1993), due to the amount of nutrients released by the submerged organic matter in decomposition (Goldyn et al., 2003; Mérona et al., 2003). The changes are observed in the abundance of all aquatic communities (Agostinho et al., 1999; Hahn and Fugi, 2008) and combined with a large input of allochthonous material (mainly plant and invertebrate), become food resources available for fish (Loureiro-Crippa and Hahn, 2006). In this way, fishes are favored by the large supply of food and according to Agostinho et al. (1999), this phenomenon occurs mainly during filling of reservoirs and in the first years after. It is expected that some populations are more favored than others because they are more or less opportunistic. Thereby, depending on the feeding habit, fish may take advantage and possibly increase the nutritional condition, on the other hand, the feeding habit can be so restrictive to the point of extinguishing a local population. In accordance with Mérona et al. (2003), the trophic limitation is the main factor for the success of fish in tropical reservoirs.

Samplings in the Manso Reservoir were conducted in the first four years after impoundment, therefore, a period when this type of environment is still new and undergoing ecological adjustments (Agostinho et al., 1999). The results of our study revealed variations in nutritional status along the study period, depending on the species and occasionally on the sex of individuals. Some of the results cannot be yet explained because no temporal or sexual pattern was found within a population, which lead us to infer that perhaps four years after filling was not enough for the adaptation of such populations.

First, the condition factor is not an instantaneous measure, and the results will only be detected over a period of time under favorable or unfavorable environmental conditions. In general, it was observed two distinct groups.

Group 1: species whose body condition decreased in the year II, with a posterior increase (A. pantaneiro, P. curviventris and S. borelli), species considered sensitive to the reservoir filling. Environmental conditions were considered favorable for A. pantaneiro from the year II, when there was a remarkable increase in the capture of Moenkhausia dichroura (A.A. Agostinho, unpublished), a potential prey that came to represent 95% of the diet of this fish predator (Cantanhêde et al., 2008). In this way, the increase in body condition was related to the high cost-benefit given by the availability of this prey, thus maximizing the energy gain (Milinsiki and Heller, 1978; Cantanhêde et al., 2009). In turn, for P. curviventris, the reduced body condition from the year II (mainly in females) is explained by its bottom feeding habit. As the reservoir fills up, depth increases, oxygen levels decreases, and the bottom become hostile for species that exploit it. Thus, it is believed that this species has had great difficulty to forage, and may have fed on a food different from usual. Schizodon borelli, a herbivorous species, at first, the formation of a reservoir can be favorable, due to the large amount of submerged plant material, but this is rapidly degraded, which may explain the decline in the body condition from the year II. Studies analyzing this species demonstrated that its diet was predominantly made up of terrestrial plants in the year I, and started to include filamentous algae, aquatic plants and detritus in the year IV (Gimenes, 2011), which may indicate an increase in nutritional value of food available.

Group 2: species whose body condition increased in the year II (A. osteomystax and P. maculatus), indicating a more rapid adaptation to new environmental conditions. For A. osteomystax (mainly females), body condition progressively increased up to the year IV, this is an insectivorous species that changed the composition of its diet over time (between years I and IV) (Barili et al., 2012); at the beginning of the period, this species mainly consumed Chaoboridade larvae, and at the end, Chironomidade pupae, Hymenoptera and Hemiptera. The broadening of the food spectrum over time possibly aggregated nutritional value to the diet of A. osteomystax. Pimelodus maculatus is a species easily adapted to reservoirs and according to some studies, species of this genus have great capacity to establish themselves in lentic environments (Abujanra et al., 1999; Lima-Junior and Goitein, 2004). This ability may be associated with the capacity of this species to explore diverse niches, in addition to the opportunistic feeding behaviour (Abujanra et al., 1999; Lima-Junior and Goitein, 2004). Trophic studies on this species showed that in the year I, its diet consisted mainly of aquatic and terrestrial insects, and in the year, in addition to these items, the diet included fish accounting for 50% of the diet (Gimenes, 2011). The nutritional value of fish preyed combined with insects would probably increase the body condition, however, the results varied little between the sexes with a peak in the year III, which complicates the explanation of results on the basis of its diet.

Moreover, all parameters investigated were somehow affected by the formation of the Manso Reservoir, mainly the body condition and gonadosomatic index for several species. On the other hand, the least affected factor was the feeding activity, that is, the amount of food consumed by fish. The results often very divergent between males and females of the same species are difficult to explain, because variations in population parameters, between the sexes, can be found within a single population, according to Pope and Kruse (2007).

In the present study, we sought to investigate the highest possible number of variables (sampling years, sexes, feeding habit, feeding activity and reproductive activity) to detect the effects of the formation of the Manso Reservoir on the body condition of fish. Nevertheless, the results did not evidence a same pattern of either increase or decrease of body condition for all species examined, since everything indicates that responses are species-specific. Even with a lack of consistency in some results, we can draw some suggestions for future investigations, such as: i) to analyze the degree of parasitism of fish, once parasite populations tend to increase in a confined environment and worsen body condition; ii) to study the digestibility of food, because although it is available, certain species are not adapted to digest it; iii) to examine the nutritional value of the available food, since quantity does not guarantee quality. Responses to these questions will certainly contribute to aggregate data to help better explain the body condition of fish species in dammed environments. According to Godinho (1997) the condition factor, a standard index in fish ecology (Bolger and Connolly, 1989), is used to monitor the environmental influence on populations over time.

Acknowledgements

We express our appreciation to Nupélia (Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura) and to PEA (Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais) for their financial support and infrastructure, and to the Brazilian Council of Research (CNPq and CAPES) for providing grants to SML Moura and NS Hahn.

Received: 28 November 2013

Accepted: 11 September 2014

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Publication Dates

• Publication in this collection
  08 Jan 2015
• Date of issue
  Dec 2014

History

• Received
  28 Nov 2013
• Accepted
  11 Sept 2014