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Diel variation in the structure of fish assemblages in south western Amazon streams

Variação diária na estrutura de assembleias de peixes em igarapés da Amazônia Sul Ocidental

Abstract:

Aim

We investigate the influence of luminosity, habitat conservation and pluviometric periods in fish assemblages of in pasture and forest small streams in western amazon.

Methods

Sampling was conducted every two months from July 2013 to April 2014 in nine first- and second-order streams using seine nets and dip nets during the day and night. Fish composition, richness and total abundance were determined for each sampling period. The PERMANOVA was used to evaluate the effects of land use, season, and photoperiod, on fish assemblages. Fish assemblage structure for each stream in the presence and absence of photoperiod was ordered by NMDS analysis.

Results

In the light period, 3,484 specimens from 69 species were collected, while 4,574 specimens from 71 species where collected in the dark period. No significant differences in abundance and species richness were recorded between the presence and absence of luminosity periods, rainy and dry seasons and streams in forest and deforested areas. We found evidence of the dark phase composition and richness of exclusive species (22% of species collected were found at night), which were greater than in the light period (20% of species).

Conclusion

Despite our failure to identify any nycterohemeral segregation, the results complement existing knowledge of regional ichthyofauna and help provide a better understanding of the distributional, behavioral and functional ecological patterns of fish assemblages.

Keywords:
day-night shifts; fish assemblages; Rondônia; Machado River

Resumo:

Objetivo

Investigamos a influência da luminosidade, conservação do habitat e períodos pluviométricos nas assembleias de peixes de igarapés em pastagem e floresta na Amazônia Ocidental.

Métodos

A amostragem foi realizada bimestralmente, de julho de 2013 a abril 2014 em nove igarapés de primeira e segunda ordem, utilizando redes de arrasto e puçá durante o dia e a noite. A composição, riqueza e abundância total da ictiofauna foram determinadas para cada período de amostragem. A PERMANOVA foi utilizada para avaliar os efeitos do uso da terra, estação e fotoperíodo sobre assembleias de peixes. A estrutura das assembleias de peixes para cada igarapé com presença e ausência de fotoperíodo foi ordenada através de NMDS.

Resultados

No período de presença de luminosidade, 3.484 exemplares de 69 espécies foram coletadas, enquanto 4.574 exemplares de 71 espécies, foram coletados no período com ausência de luminosidade. Não foram encontradas diferenças significativas na abundância e riqueza de espécies entre os períodos de presença e ausência de luminosidade, estação chuvosa e seca e para igarapés em áreas florestadas e desmatadas. Nós encontramos evidências da composição de espécies exclusivas no período com ausência de luminosidade (22% das espécies), que foi maior do que no período com presença de luminosidade (20% das espécies).

Conclusão

Apesar de nossa incapacidade de identificar qualquer segregação nictemeral, os resultados complementam o conhecimento existente da ictiofauna regional e ajudam a fornecer uma melhor compreensão dos padrões ecológicos distribucionais, comportamentais e funcionais de assembleias de peixes.

Palavras-chave:
substituição diurna-noturna; assembleias de peixes; Rondônia; rio Machado

1 Introduction

Diel activity patterns are among the most evident and detectable rhythms in animals and the main subject of many chronobiological naturalistic and experimental studies (Naruse & Oishi, 1996Naruse, M. and Oishi, T. Annual and daily activity rhythms of loaches in an irrigation creek and ditches around paddy fields. Environmental Biology of Fishes, 1996, 47(1), 93-99. http://dx.doi.org/10.1007/BF00002382.
http://dx.doi.org/10.1007/BF00002382...
; Anras et al., 1997Anras, M.L.B., Lagardere, J.P. and Lafaye, J.Y. Diel activity rhythm of seabass tracked in a natural environment: group effects on swimming patterns and amplitudes. Canadian Journal of Fisheries and Aquatic Sciences, 1997, 54(1), 162-168. http://dx.doi.org/10.1139/f96-253.
http://dx.doi.org/10.1139/f96-253...
; Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). These patterns have already been investigated in different ecosystems such as seagrass beds, coral reefs and mangroves (Nagelkerken et al., 2000Nagelkerken, I., Dorenbosch, M., Verberk, W.C., De La Moriniere, C.E. and Van Der Velde, G. Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae e Lutjanidae. Marine Ecology Progress Series, 2000, 194(1), 55-64. http://dx.doi.org/10.3354/meps194055.
http://dx.doi.org/10.3354/meps194055...
; Pereira et al., 2010Pereira, P.H.C., Ferreira, B.P. and Rezende, S.S.M. Community structure of the ichthyofauna associated with seagrass beds (Halodule wrightii) in Formoso River estuary-Pernambuco, Brazil. Pernambuco: Academia Brasileira de Ciências, 2010, pp. 617-628.). Many organisms studied, from protists to plants and animals, provide strong evidence of a more or less tight control of activity patterns by internal clocks (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.).

Aquatic organisms are not exceptions; many studies have been devoted to different kinds of rhythms these organisms show (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). In fishes, there is evidence of endogenous and exogenous circadian rhythms in some species, which affects activity patterns, vision and the growth of scales and otoliths (Boujard & Leatherland, 1992Boujard, T. and Leatherland, J.F. Circadian rhythms and feeding time in fishes. Environmental Biology of Fishes, 1992, 35(1), 109-131. http://dx.doi.org/10.1007/BF00002186.
http://dx.doi.org/10.1007/BF00002186...
; Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). It has been shown that the teleost circadian system encompasses multiple self-sustained oscillators and that at least two organs, the pineal organ and retina, contain oscillators (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). Photoreceptors in the retina and pineal organ and deep in the brain are believed to be involved in photosignal transduction to establish circadian rhythms in fish (Iigo & Tabata, 1996Iigo, M. and Tabata, M. Circadian rhythms of locomotor activity in the goldfish Carassius auratus.Physiology & Behavior, 1996, 60(3), 775-781. PMid:8873250. http://dx.doi.org/10.1016/0031-9384(96)00131-X.
http://dx.doi.org/10.1016/0031-9384(96)0...
). Each of these organs may be involved individually in the entrainment of locomotor activity in certain fish species (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.).

Diel activity rhythms are expressed by locomotor activity patterns associated with alternating phases (active period vs. rest period), exploitation of habitat, feeding and intra- and interspecific interactions (formation of shoals, agonistic behavior, territory defense, breeding and predator-prey interactions) (Kavaliers, 1980Kavaliers, M. Circadian locomotor activity rhythms of the burbot, Lota lota: seasonal differences in period length and the effect of pinealectomy. Journal of Comparative Physiology, 1980, 136(3), 215-218. http://dx.doi.org/10.1007/BF00657535.
http://dx.doi.org/10.1007/BF00657535...
; Helfman, 1986Helfman, G.S. Fish behaviour by day, night and twilight. In: T. J. PITCHER, ed. The behaviour of teleost fishes. London: Croom Helm, 1986, pp. 366-387.). Taking into account the circadian rhythms, fish can be classified as active during nocturnal, diurnal or crepuscular (mixed types, for which between 35% and 65% of activity occurs in the dark phase) periods (Iigo & Tabata, 1996Iigo, M. and Tabata, M. Circadian rhythms of locomotor activity in the goldfish Carassius auratus.Physiology & Behavior, 1996, 60(3), 775-781. PMid:8873250. http://dx.doi.org/10.1016/0031-9384(96)00131-X.
http://dx.doi.org/10.1016/0031-9384(96)0...
). For instance, in inland Neotropical waters, Siluriformes and Gymnotiformes are more active at night, whereas most Characiformes and Cichlidae feed and migrate during the day (Lowe-McConnell, 1999Lowe-Mcconnell, R.H. Estudos ecológicos de comunidade de peixes tropicais. São Paulo: Edusp, 1999.; Carvalho, 2008Carvalho, L.N. História natural de peixes de igarapés amazônicos: utilizando a abordagem do Conceito do Rio Contínuo. Manaus: INPA, 2008.).

Species-specific photoperiod variations can mean that the abundance of individuals and species in a given habitat changes over the course of 24-hours, as determined by feeding activities (Piet & Guruge, 1997Piet, G.J. and Guruge, W.A. Diel variation in feeding and vertical distribution of ten co-occurring fish species: consequences for resource partitioning. Environmental Biology of Fishes, 1997, 50(3), 293-307. http://dx.doi.org/10.1023/A:1007390516552.
http://dx.doi.org/10.1023/A:100739051655...
), predation and the need to escape from predators (Gibson et al., 1998Gibson, R.N., PIHL, L., Burrows, M.T., Modin, J., WENNHAGE, H. and NICKELL, L.A. Diel movements of in. Marine Ecology Progress Series, 1998, 165, 145-159. http://dx.doi.org/10.3354/meps165145.
http://dx.doi.org/10.3354/meps165145...
; Grossman et al., 1998Grossman, G.D., Ratajczak JUNIOR, R.E., Crawford, M. and Freeman, M.C. Assemblage organization in stream fishes: effects of environmental variation and interspecific interactions. Ecological Monographs, 1998, 68(3), 395-420. http://dx.doi.org/10.1890/0012-9615(1998)068[0395:AOISFE]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9615(1998...
). According to Lowe-Mcconnell (1999)Lowe-Mcconnell, R.H. Estudos ecológicos de comunidade de peixes tropicais. São Paulo: Edusp, 1999. the presence of predators and large species at dark phase, while small species protect themselves in the vegetation, is a common observation in Neotropical rivers. Many ecological studies of Neotropical fish assemblages have been carried out in larger water bodies, such as rivers and lakes (Arrington & Winemiller, 2003Arrington, D.A. and Winemiller, K.O. Diel changeover in sandbank fish communities in a neotropical floodplain river. Journal of Fish Biology, 2003, 63(1), 442-459. http://dx.doi.org/10.1046/j.1095-8649.2003.00167.x.
http://dx.doi.org/10.1046/j.1095-8649.20...
; Pelicice et al., 2005Pelicice, F.M., Agostinho, A.A. and Thomaz, S.M. Fish communities associated with Egeria in a tropical reservoir: investigating the effects of plant biomass and diel period. Acta Oecologica, 2005, 27(1), 9-16. http://dx.doi.org/10.1016/j.actao.2004.08.004.
http://dx.doi.org/10.1016/j.actao.2004.0...
; Willis et al., 2005Willis, S.C., Winemiller, K.O. and Lopez-Fernandez, H. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia, 2005, 142(2), 284-295. PMid:15655689. http://dx.doi.org/10.1007/s00442-004-1723-z.
http://dx.doi.org/10.1007/s00442-004-172...
; Saccol-Pereira & Fialho, 2010Saccol-Pereira, A. and Fialho, C.B. Seasonal and diel variation in the fish assemblage of a Neotropical delta in southern Brazil. Iheringia: Série Zoologia, 2010., 100(2), 169-178. http://dx.doi.org/10.1590/S0073-47212010000200013.
http://dx.doi.org/10.1590/S0073-47212010...
; Costa & Freitas, 2010Costa, I.D. and Freitas, C.E.C. Variação nictemeral na composição e abundância da ictiofauna em um trecho do rio Urucu – Coari/Amazonas/Brasil. Revista Colombiana Ciencia Animal, 2010, 2(2), 355-364.; Duarte et al., 2010Duarte, C., Rapp Py-Daniel, L.H. and Deus, C.P. Fish assemblages in two sandy beaches in lower Purus river, Amazonas, Brazil. Iheringia: Série Zoologia, 2010., 100(4), 319-328. http://dx.doi.org/10.1590/S0073-47212010000400006.
http://dx.doi.org/10.1590/S0073-47212010...
, 2012Duarte, C., Souza, V.S. and Nunes, C.O. Variação nictemeral na composição da ictiofauna no lago Catalão (confluência dos rios Solimões e Negro). Amazon Science, 2012, 1(1), 18-27.; Costa et al., 2011Costa, I.D., Rocha, A.C.P.V., Lima, M.L.C. and Zuanon, J.A. Composição e abundância de peixes da interface entre as águas abertas e bancos de macrófitas e sua dinâmica nos períodos de crepúsculos matutino e vespertino, no lago Catalão, Amazonas, Brasil. Biotemas, 2011, 24(2), 97-101. http://dx.doi.org/10.5007/2175-7925.2011v24n2p97.
http://dx.doi.org/10.5007/2175-7925.2011...
, 2015Costa, I.D., Nogueira, W.V., Rocha, V.M., Albuquerque, P.D.T.F., Almeida Pereira, J.M. and Ribeiro Filho, R.A.R. Variação nictemeral na assembleia de peixes de um trecho de rio na Amazônia ocidental brasileira. Biotemas, 2015, 28(3), 79-92. http://dx.doi.org/10.5007/2175-7925.2015v28n3p79.
http://dx.doi.org/10.5007/2175-7925.2015...
).

Despite the immense literature on this topic, little is found regarding fishes - and even less regarding the tropical ones (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). Especially when related to studies of diurnal and nocturnal assemblages in Amazon small streams (e.g., Bührnheim, 2002Bührnheim, C.M. Heterogeneidade de habitats: rasos x fundos em assembleias de peixes de igarapés de terra firme na Amazônia Central. Revista Brasileira de Zoologia, 2002, 19(3), 889-905. http://dx.doi.org/10.1590/S0101-81752002000300026.
http://dx.doi.org/10.1590/S0101-81752002...
). Thus, studies in amazon small streams are necessary, considering the high number of species, the accelerated deforestation and the degradation to the streams, mainly in Rondônia State. It very important acquire the taxonomic, geographical, and ecological knowledge of the ichthyofauna. As a potential additional threat to this fish fauna we can cite the expansion of hydroelectric power plants (Casatti et al., 2013Casatti, L., Pérez-Mayorga, M.A., Carvalho, F.R., Brejão, G.L. and Costa, I.D. The stream fish fauna from the rio Machado basin, Rondônia State, Brazil. Check List, 2013, 9(6), 1496-1504. http://dx.doi.org/10.15560/9.6.1496.
http://dx.doi.org/10.15560/9.6.1496...
).

Based on the premise that Characiformes is the most abundant and rich group species in amazon small streams, and is more active during the diurnal period, Siluriformes and Gymnotiformes, are most active during the nocturnal period (Lowe McConnell, 1999) and species-specific in the daily cycle variations can mean that the abundance and species in a given habitat changes, determined by intra-interspecific relationships (Gibson et al., 1998Gibson, R.N., PIHL, L., Burrows, M.T., Modin, J., WENNHAGE, H. and NICKELL, L.A. Diel movements of in. Marine Ecology Progress Series, 1998, 165, 145-159. http://dx.doi.org/10.3354/meps165145.
http://dx.doi.org/10.3354/meps165145...
; Grossman et al., 1998Grossman, G.D., Ratajczak JUNIOR, R.E., Crawford, M. and Freeman, M.C. Assemblage organization in stream fishes: effects of environmental variation and interspecific interactions. Ecological Monographs, 1998, 68(3), 395-420. http://dx.doi.org/10.1890/0012-9615(1998)068[0395:AOISFE]2.0.CO;2.
http://dx.doi.org/10.1890/0012-9615(1998...
), we tested the hypothesis that photoperiod influences fish activity, resulting in changes in the composition, abundance and species richness of the icthyofauna in pasture and forest small streams in the rainy and dry seasons, in the Machado River basin, state of Rondônia, Brazil.

2 Material and Methods

2.1 Study area

The Machado River is approximately 1,243 km long. It starts at the confluence of the Pimenta Bueno River and Comemoração River and flows in to the Madeira River in the north of the state of Rondônia (RO) (Fernandes & Guimarães, 2002Fernandes, L.C. and Guimarães, S.C.P. Atlas geoambiental de Rondônia. Porto Velho: SEDAM, 2002.). First to third order streams are predominat in the Machado River basin and have a total length of 27,497 km (Krusche et al., 2005Krusche, A.V., Ballester, M.V.R., Victoria, R.L., Bernardes, M.C., Leite, N.K., Hanada, L., Victoria, D.C., Toledo, A.M., Ometto, J.P., Moreira, M.Z., Gomes, B.M., Bolson, M.A., Gouveia NETO, S., Bonelli, N., Deegan, L., Neill, C., Thomas, S., Aufdenkampe, A.K. and Richey, J.E. Efeitos das mudanças do uso da terra na biogeoquímica dos corpos d’água da bacia do rio Ji-Paraná, Rondônia. Acta Amazonica, 2005, 35(2), 197-205. http://dx.doi.org/10.1590/S0044-59672005000200009.
http://dx.doi.org/10.1590/S0044-59672005...
). The climate is characterized by temperatures ranging from 19 to 33 °C and annual rainfall is around 2,500 mm (Krusche et al., 2005Krusche, A.V., Ballester, M.V.R., Victoria, R.L., Bernardes, M.C., Leite, N.K., Hanada, L., Victoria, D.C., Toledo, A.M., Ometto, J.P., Moreira, M.Z., Gomes, B.M., Bolson, M.A., Gouveia NETO, S., Bonelli, N., Deegan, L., Neill, C., Thomas, S., Aufdenkampe, A.K. and Richey, J.E. Efeitos das mudanças do uso da terra na biogeoquímica dos corpos d’água da bacia do rio Ji-Paraná, Rondônia. Acta Amazonica, 2005, 35(2), 197-205. http://dx.doi.org/10.1590/S0044-59672005000200009.
http://dx.doi.org/10.1590/S0044-59672005...
) and there are two well-defined seasons: the dry season (from late May to October) and rainy season (from November to May) (Fernandes & Guimarães, 2002Fernandes, L.C. and Guimarães, S.C.P. Atlas geoambiental de Rondônia. Porto Velho: SEDAM, 2002.).

2.2 Fish collections

A series of 18 samplings was conducted during three rainy and three dry months: June, August and October 2013 (dry season) and December, February and April 2014 (rainy season). Each sampling included the fish abundance in the nine first- and second-order streams in the middle section of the Machado River basin (Table 1) during high luminosity period (12:00-13:00 hours) and once again during dark period (19:30-20:30 hours).

Table 1
Identification of collection site, abbreviation, land use in the adjacent matrix, geographical coordinates and number of samples of the nine streams in the Machado river basin, from July 2013 to May 2014.

To prevent the potential negative effects of sampling, samples of the absence luminosity period were conducted 20 m upstream and 10 days after high luminosity period samplings. We highlight out that both the samples collected during absence luminosity period, as in the high luminosity period, obeyed the minimum distance of 20 m. Failing to collect samples in the same location. Noting that the sites are similar in terms of habitat condition and heterogeneity.

In total, 108 samples were obtained (Table 1). Fishes were collected using a seine net (1.5 × 2 m, 2 mm mesh) and dip net (0.5 × 0.8 m, 2 mm mesh) along a 50 m stretch for three people for one hour. Flashlights were used for the nocturnal sampling to find and capture the fishes following Bührnheim (1999)Bührnheim, M.C. Habitat abundance patterns of fish communities in three Amazonian rain forest streams. In A.L. VAL and V.M.F.A. VAL, eds. Biology of tropical fishes. Manaus: INPA, 1999, pp. 63-74..

Fish specimens were euthanized using a lethal dose of clove oil and immediately preserved in a 10% formalin solution. After two days they were transferred to 70% alcohol and identified by specialists. Voucher specimens were deposited in the fish collection at the Federal University of Rondônia, Porto Velho, RO, Brazil (Vouchers: UFRO-ICT 023980 to 024000).

In order to better understand the state of those environments, we describe in Table 2 the physical conditions of each sampling site. Environmental variables at each sampling site were characterized following visual observation; substrate composition (i.e., the relative proportion of each substrate component) was visually estimated according to Cummins (1962)Cummins, K.H. An evaluation of some techniques for the collection and analysis of benthic samples with special emphasis on lotic waters. American Midland Naturalist, 1962, 67(2), 477-504. http://dx.doi.org/10.2307/2422722.
http://dx.doi.org/10.2307/2422722...
, and the volume occupied by the submerged vegetation (roots, leaves and stems of the submerged terrestrial vegetation) on each side of the stream was estimated based on the height and width of the vegetation on the banks.

Table 2
Physiographic descriptors of each stream in the Machado River basin, July 2013 to May 2014.

2.3 Data analysis

Fish composition, richness (S) and absolute abundance (N) were determined for presence and absence of luminosity periods. The Shapiro-Wilk normality test and Levene’s test were applied to determine whether the assumptions used in the parametric (t test) or nonparametric (Mann-Whitney U test) analyses of abundance (log10) and species richness (log10) for each photoperiod.

The Permutational Multivariate Analysis of Variance (PERMANOVA, Anderson, 2001Anderson, M.J. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 2001, 26, 32-46. http://dx.doi.org/10.1046/j.1442- 9993.2001.01070.x.
http://dx.doi.org/10.1046/j.1442- 9993.2...
) was used to evaluate the effects of land use (forest and pasture), season (rainy and dry seasons), and photoperiod (presence and absence of luminosity), on biological assemblages, and the interactions between these factors (Anderson, 2001Anderson, M.J. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 2001, 26, 32-46. http://dx.doi.org/10.1046/j.1442- 9993.2001.01070.x.
http://dx.doi.org/10.1046/j.1442- 9993.2...
). PERMANOVA is a multi-factorial ANOVA based on any measured distance using permutation methods (Anderson, 2001Anderson, M.J. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 2001, 26, 32-46. http://dx.doi.org/10.1046/j.1442- 9993.2001.01070.x.
http://dx.doi.org/10.1046/j.1442- 9993.2...
). The analysis was based on dissimilarity coefficients using Bray-Curtis index (richness and abundance data, were previously Log-transformed) and under 10,000 permutations.

Fish assemblage structure for each stream in the presence and absence of photoperiod was ordered by nonmetric multidimensional scaling (NMDS) analysis, a method for bi- or tridimensional arrangement which represents the association among samples in a similarity matrix (Clarke & Warwick, 1994Clarke, K.R. and Warwick, R.M. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory, 1994.). The method is considered robust and suitable for ordination ecological data (Minchin, 1987Minchin, P.R. An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio, 1987, 69(1), 89-107. http://dx.doi.org/10.1007/BF00038690.
http://dx.doi.org/10.1007/BF00038690...
). To quantify the similarity between sites we used the Bray-Curtis distance measure applied data previously Log-transformed (Clarke & Gorley, 2001Clarke, K.R. and Gorley, R.N. PRIMER v5: user manual/tutorial. PRIMER-E. Plymouth: Plymouth Marine Laboratory, 2001.). We performed Mann-Whitney tests with NMDS axis 1 and 2 scores, to detect differences in fish assemblages in the presence and absence of photoperiod.

The PERMANOVA and Mann-Whitney test were performed in the R environment (R Development Core Team, 2013R DEVELOPMENT CORE TEAMR: a language and environment for statistical computingonlineViennaR Foundation for Statistical Computing2013viewed 27 May 2016Available from: http://www.R-project.org
http://www.R-project.org...
). The NMDS analyses was carried out using PAST version 2.17 (Hammer et al., 2001Hammer, Ø., Harper, D.A.T. and Ryan, P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 2001, 4(1), 1-9.). Differences were considered significant when p ≤ 0.05.

3 Results

A total of 8,058 specimens representing 4 orders, 20 families and 88 species were collected. For both periods, Knodus heteresthes (Eigenmann, 1908) (Nlight = 1,425, Ndark = 2,210), Serrapinnus notomelas (Eigenmann, 1915) (Nlight = 357, Ndark = 413) and Bryconops giacopinii (Fernández-Yépez, 1950) (Nlight = 258, Ndark = 272) were the most abundant species. A total of 18 species (20%) were not found during the diurnal period and 20 (22%) were not found during the nocturnal period (Table 3).

Table 3
Abundance data for species collected in presence of luminosity (PL) and absence of luminosity (AL) in each stream in the Machado River basin, July 2013 to May 2014.

Sampling during the presence of luminosity period accounted for 3,484 specimens, 4 orders, 15 families and 69 species. During the absence of luminosity period, 4,574 specimens belonging to 4 orders, 20 families and 71 species were collected. No statistically significant differences were found in abundance (U = 869.0, p = 0.90) or species richness (U = 867.0, p = 0.89) between periods of presence and absence of luminosity. Considering all the samples together, Characiformes had the highest abundance and species richness, followed by Siluriformes, Perciformes and Gymnotiformes (Table 4).

Table 4
Data of numerical abundance (N) and richness (S) for each fish order in periods of presence and absence of luminosity of the nine streams in the Machado river basin, July 2013 to May 2014.

The fish assemblages no differed significantly between seasons, type of land use and luminosity, both when considering the abundance and richness of species (Table 5). NMDS analysis of samples based on species abundance did not reveal any separation on axis 1 and 2 retained for interpretation (Stress = 0.41). Scores on axis 1 (U = 820.50, p = 0.58) and axis 2 (U = 845.00, p = 0.74) of the NMDS no differed with respect to period for fish assemblages.

Table 5
PERMANOVA (Permutational Multivariate Analysis of Variance, Pseudo-F value) for fish assemblages in stream in the Machado River basin, July 2013 to May 2014.

4 Discussion

According to Lowe-McConnell (1999)Lowe-Mcconnell, R.H. Estudos ecológicos de comunidade de peixes tropicais. São Paulo: Edusp, 1999., the predominant groups in the Amazon basin are Characiformes (43%), Siluriformes (36%) and Gymnotiformes (3%), which account for approximately 82% of the Amazonian fish assemblage. The predominance of these orders has been reported in several rivers and small streams in the Neotropics (Sabino & Zuanon, 1998Sabino, J. and Zuanon, J.A.S. A stream fish communities in Central Amazonia: distribution, activity patterns and feeding behavior. Ichthyological Exploration of Freshwaters, 1998, 8(3), 201-210.; Lowe-McConnell, 1999Lowe-Mcconnell, R.H. Estudos ecológicos de comunidade de peixes tropicais. São Paulo: Edusp, 1999.; Castro, 1999Castro, R.M.C. Evolução da ictiofauna de riachos sul-americanos: padrões gerais e possíveis processos casuais. In E.P. CARAMASCHI, R. MAZZONI and R. PERES-NETO, eds. Ecologia de peixes de riachos. Rio de Janeiro: UFRJ, 1999, pp. 139-155. Série Oecologia Brasiliensis, vol. 6.; Pouilly et al., 2004Pouilly, M., Yunoki, T., Rosales, C. and Torres, L. Trophic structure of fish communities from Mamoré River floodplain lakes (Bolivia). Ecology Freshwater Fish, 2004, 13(1), 245-257. http://dx.doi.org/10.1111/j.1600-0633.2004.00055.x.
http://dx.doi.org/10.1111/j.1600-0633.20...
; Casatti et al., 2013Casatti, L., Pérez-Mayorga, M.A., Carvalho, F.R., Brejão, G.L. and Costa, I.D. The stream fish fauna from the rio Machado basin, Rondônia State, Brazil. Check List, 2013, 9(6), 1496-1504. http://dx.doi.org/10.15560/9.6.1496.
http://dx.doi.org/10.15560/9.6.1496...
). The most abundant families in the present study were Characidae, Crenuchidae and Loricariidae, a group widely distributed throughout the Amazon basin (Ferreira et al., 1998Ferreira, E.J.G., Zuanon, J.A.S. and Santos, G.M. Peixes comerciais do Médio Amazonas: região de Santarém, Pará. Brasília: IBAMA, 1998.; Santos et al., 2006Santos, G.M., Ferreira, E. and Zuanon, J. Peixes comerciais de Manaus. Manaus: IBAMA, 2006.).

Our results corroborating the study by Mojica et al. (2014)Mojica, J.I., Lobón-Cervia, J. and Castellanos, C. Quantifying fish species richness and abundance in Amazonian streams: assessment of a multiple gear method suitable for Terra firme stream fish communities. Fisheries Management and Ecology, 2014, 21(3), 220-233. http://dx.doi.org/10.1111/fme.12067.
http://dx.doi.org/10.1111/fme.12067...
in Colombian Amazon streams, who found no significant differences in abundance and species richness between light and dark phase. A dual phasing capacity, which is characteristic of a highly adaptable circadian system, appears to be a common fish trait, especially in temperate species, and an adaptation to marked seasonal changes in photoperiod, temperature and food availability (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). In tropical regions, however, where seasonal changes are not as marked as in temperate zones, this capacity does not appear to be adaptive, corroborating the pattern observed in our study. In tropical areas with well-defined rain cycles, there may be important annual fluctuations in the quantity and quality of food available (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.).

Temporal niche partitioning predicts that different species may be limited by the same resources but differ in terms of when they exploit the resource (Chesson, 1985Chesson, P. Coexistence of competitors in spatially and temporally varying environments: a look at the combined effects of different sorts of variability. Theoretical Population Biology, 1985, 28(1), 263-287. http://dx.doi.org/10.1016/0040-5809(85)90030-9.
http://dx.doi.org/10.1016/0040-5809(85)9...
). Previous studies have shown that the composition of fish populations can vary between light and dark periods (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). Arrington & Winemiller (2003)Arrington, D.A. and Winemiller, K.O. Diel changeover in sandbank fish communities in a neotropical floodplain river. Journal of Fish Biology, 2003, 63(1), 442-459. http://dx.doi.org/10.1046/j.1095-8649.2003.00167.x.
http://dx.doi.org/10.1046/j.1095-8649.20...
found that Characiformes were a dominant group in both periods, accounting for 80% and 97% of abundance during diurnal and nocturnal periods, respectively. This was also observed in the present study, where 82% and 84% of the abundance of Characiformes was represented in the diurnal and nocturnal periods, respectively, composed mainly by species K. heteresthes, S. notomelas and B. giacopinii (Characiformes order) which represented 60% of total abundance. These species need of high visual acuity, given that these are nektonic species that collect food items drifting at mid-water and at the surface, predominantly in the main channel (Ceneviva-Bastos & Casatti, 2007CENEVIVA-BASTOS, M. and Casatti, L. Oportunismo alimentar de (Teleostei, Characidae): uma espécie abundante em riachos do noroeste do Estado de São Paulo, Brasil. Knodus moenkhausiiIheringia: Série Zoologia, 2007, 97(1), 7-15. http://dx.doi.org/10.1590/S0073-47212007000100002.
http://dx.doi.org/10.1590/S0073-47212007...
; Carvalho, 2008Carvalho, L.N. História natural de peixes de igarapés amazônicos: utilizando a abordagem do Conceito do Rio Contínuo. Manaus: INPA, 2008.; Brejão et al., 2013Brejão, G.L., Gerhard, P. and Zuanon, J. Functional trophic composition of the ichthyofauna of forest streams in eastern Brazilian Amazon. Neotropical Ichthyology, 2013, 11(2), 361-373. http://dx.doi.org/10.1590/S1679-62252013005000006.
http://dx.doi.org/10.1590/S1679-62252013...
; Nogueira & Costa, 2014Nogueira, V.W. and Costa, I.D. Aspectos da alimentação de (Characiformes, Characidae) no igarapé do Nove, bacia do rio Machado, Rondônia, Brasil. Knodus heteresthesBiotemas, 2014, 27(3), 97-108. http://dx.doi.org/10.5007/2175-7925.2014v27n3p97.
http://dx.doi.org/10.5007/2175-7925.2014...
). Characiformes collected exclusively during nocturnal samplings belong to species that have large eyes, which presumably increase visual acuity in environments with limited light (Shand, 1997Shand, J. Ontogenetic changes in retinal structure and visual acuity: A comparative study of coral-reef teleosts with differing post-settlement lifestyles. Environmental Biology of Fishes, 1997, 49(3), 307-322. http://dx.doi.org/10.1023/A:1007353003066.
http://dx.doi.org/10.1023/A:100735300306...
). This anatomical modification is described as an adaptation for foraging in deep water, where diurnal light is limited (Stewart et al., 2002Stewart, D.J., Ibarra, M. and Barriga-Salazar, R. Comparison of deep-river and adjacent sandy-beach fish communities in the Napo River Basin, Eastern Ecuador. Copeia, 2002, 2(2), 333-343.) and capturing food in shallow waters with reduced nocturnal light (Arrington & Winemiller, 2003Arrington, D.A. and Winemiller, K.O. Diel changeover in sandbank fish communities in a neotropical floodplain river. Journal of Fish Biology, 2003, 63(1), 442-459. http://dx.doi.org/10.1046/j.1095-8649.2003.00167.x.
http://dx.doi.org/10.1046/j.1095-8649.20...
).

The variations are related to the different activities that these fishes perform, such as feeding, breeding and moving (Lowe-McConnell, 1999Lowe-Mcconnell, R.H. Estudos ecológicos de comunidade de peixes tropicais. São Paulo: Edusp, 1999.). Characiformes and Perciformes are visually oriented fish with diurnal habits and are found mostly in clear-water environments, while fish guided by chemical, electrical or tactile stimulus, such as Siluriformes and Gymnotiformes, are more active at night and found mostly in turbid waters (Matthews, 1998Matthews, W.J. Patterns in freshwaters fish ecology. Oklahoma: University of Oklahoma Press, 1998. http://dx.doi.org/10.1007/978-1-4615-4066-3.
http://dx.doi.org/10.1007/978-1-4615-406...
). Siluriformes from the genera Trichomycterus (Trichomycteridae) and Ancistrus (Loricariidae), which are generally nocturnal (Buck & Sazima, 1995Buck, S.M.C. and Sazima, I. An communities of mailed catfishes (Loricariidae) in southeastern Brazil: Distribution, activity, and feeding. Ichthyological Exploration of Freshwaters, 1995, 6(4), 325-332.; Casatti & Castro, 1998Casatti, L. and Castro, R.M.C. A fish community of the São Francisco River headwaters rifles, southeastern Brazil. Ichthyology Explore Freshwaters, 1998, 9(3), 229-242.), were reported during the diurnal period, which is uncommon among small loricariids (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.).

The absence of temporal segregation of fish assemblages in our study, corroborates the results of Arrington & Winemiller (2003)Arrington, D.A. and Winemiller, K.O. Diel changeover in sandbank fish communities in a neotropical floodplain river. Journal of Fish Biology, 2003, 63(1), 442-459. http://dx.doi.org/10.1046/j.1095-8649.2003.00167.x.
http://dx.doi.org/10.1046/j.1095-8649.20...
. Many fish species have a daily movement pattern from marginal areas to open waters and vice versa and they are often members of different spatially defined assemblages (Matthews, 1998Matthews, W.J. Patterns in freshwaters fish ecology. Oklahoma: University of Oklahoma Press, 1998. http://dx.doi.org/10.1007/978-1-4615-4066-3.
http://dx.doi.org/10.1007/978-1-4615-406...
; Arrington & Winemiller, 2003Arrington, D.A. and Winemiller, K.O. Diel changeover in sandbank fish communities in a neotropical floodplain river. Journal of Fish Biology, 2003, 63(1), 442-459. http://dx.doi.org/10.1046/j.1095-8649.2003.00167.x.
http://dx.doi.org/10.1046/j.1095-8649.20...
; Costa et al., 2011Costa, I.D., Rocha, A.C.P.V., Lima, M.L.C. and Zuanon, J.A. Composição e abundância de peixes da interface entre as águas abertas e bancos de macrófitas e sua dinâmica nos períodos de crepúsculos matutino e vespertino, no lago Catalão, Amazonas, Brasil. Biotemas, 2011, 24(2), 97-101. http://dx.doi.org/10.5007/2175-7925.2011v24n2p97.
http://dx.doi.org/10.5007/2175-7925.2011...
). This spatial segregation makes it more difficult to detect nycterohemeral differences when assemblages of fish from specific habitats are analyzed. The lack of segregation between the periods analyzed is accounted for by the high similarity in the fish assemblages in both periods, as a large number of individuals from some taxa (e.g., Characiformes, Characidae and Perciformes) are active during the day and night (Barthem, 1987Barthem, R.B. Uso de redes de espera no estudo de ritmos circadianos de algumas espécies de peixes nos lagos de várzea do rio Solimões. Revista Brasileira de Zoologia, 1987, 3(7), 409-422.; Sazima & Machado 1990Sazima, I. and Machado, F.A. Underwater observations of piranhas in western Brazil. Environmental Biology of Fishes, 1990, 28(4), 17-31. http://dx.doi.org/10.1007/BF00751026.
http://dx.doi.org/10.1007/BF00751026...
; Hahn et al., 1999Hahn, N.S., Loureiro, V.E. and Delariva, R.L. Atividade alimentar da curvina Plagioscion squamosissimus (Heckel, 1940) (Perciformes, Scianidae) no rio Paraná. Acta Scientiarum, 1999, 21(1), 309-314. http://dx.doi.org/10.4025/actascibiolsci.v21i0.4438.
http://dx.doi.org/10.4025/actascibiolsci...
; Costa et al., 2009Costa, S.A.G.L., Peretti, D., PINTO JÚNIOR, J.P.M., Fernandes, M.A. and GURGEL JÚNIOR, A.M. Espectro alimentar e variação sazonal da dieta de (Heckel, 1840) (Osteichthyes, Sciaenidae) na lagoa do Piató, Assu, Estado do Rio Grande do Norte, Brasil. Plagioscion squamosissimusActa Scientiarum, 2009, 31(3), 285-292.; Duarte et al., 2010Duarte, C., Rapp Py-Daniel, L.H. and Deus, C.P. Fish assemblages in two sandy beaches in lower Purus river, Amazonas, Brazil. Iheringia: Série Zoologia, 2010., 100(4), 319-328. http://dx.doi.org/10.1590/S0073-47212010000400006.
http://dx.doi.org/10.1590/S0073-47212010...
).

Therefore, for fish assemblages in which most of the species are active during both periods, no significant differences between these periods can be expected. Additionally, Willis et al. (2005)Willis, S.C., Winemiller, K.O. and Lopez-Fernandez, H. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia, 2005, 142(2), 284-295. PMid:15655689. http://dx.doi.org/10.1007/s00442-004-1723-z.
http://dx.doi.org/10.1007/s00442-004-172...
described a low degree of species replacement between diurnal and nocturnal periods (absence of light/dark period variation), especially during the dry season in structurally complex environments. In these environments, fishes make fewer movements toward marginal areas (refuges) at night time (Willis et al., 2005Willis, S.C., Winemiller, K.O. and Lopez-Fernandez, H. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia, 2005, 142(2), 284-295. PMid:15655689. http://dx.doi.org/10.1007/s00442-004-1723-z.
http://dx.doi.org/10.1007/s00442-004-172...
), by the fact that structurally more complex environments show a higher stability of resources intrahabitat, resulting in the greater concentration of resources results in less movement between marginal areas and open waters for foraging during the day (Willis et al., 2005Willis, S.C., Winemiller, K.O. and Lopez-Fernandez, H. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia, 2005, 142(2), 284-295. PMid:15655689. http://dx.doi.org/10.1007/s00442-004-1723-z.
http://dx.doi.org/10.1007/s00442-004-172...
; Pelicice et al., 2005Pelicice, F.M., Agostinho, A.A. and Thomaz, S.M. Fish communities associated with Egeria in a tropical reservoir: investigating the effects of plant biomass and diel period. Acta Oecologica, 2005, 27(1), 9-16. http://dx.doi.org/10.1016/j.actao.2004.08.004.
http://dx.doi.org/10.1016/j.actao.2004.0...
). This is corroborated by the structural conditions of the small streams analyzed in our study, which are composed mainly of rocks, logs, branches, exposed roots and emergent and submerged macrophytes (see Table 2).

The homogeneity of the assemblages in the light and dark periods, can also be related the artifact collection resulting from differences in sampling techniques and data analysis mainly in the case of independent studies (Volpato & Trajano, 2006Volpato, G.L. and Trajano, E. Biological rhythms. In L.A. VAL, V.M.F.A. VAL and D.J. RANDAL, eds. Fish physiology. San Diego: Elsevier, 2006, pp. 101-153.). We use methods of active collection, which consists in catching fish with use of instruments that affects the environment by altering the structure of the microhabitat (e.g., submerged litter banks, trunks) (Uieda & Castro, 1999Uieda, V.S. and Castro, R.M.C. Coleta e fixação de peixes de riachos. In E.P. CARAMASCHI, R. MAZZONI and P.R. PERES-NETO, eds. Ecologia de peixes de riachos. Rio de Janeiro: UFRJ, 1999, pp. 1-22. Série Oecologia Brasiliensis.). The greater fish capture efficiency with active methods results in a higher probability of record low abundant species and cryptobiotic habits (Ribeiro & Zuanon, 2006Ribeiro, O.M. and Zuanon, J. Comparação da eficiência de dois métodos de coleta de peixes em igarapés de terra firme da Amazônia Central. Acta Amazonica, 2006, 36(3), 389-394. http://dx.doi.org/10.1590/S0044-59672006000300017.
http://dx.doi.org/10.1590/S0044-59672006...
), active or inactive (sheltered) in each photoperiod.

Despite our failure to identify any segregation based on photoperiod, we provided evidence of the nocturnal composition and richness of exclusive species (S = 20; 22%) of Machado river. While only a few studies have analyzed the fish assemblages in Amazonian streams in absence/presence of luminosity periods, it is reasonable to suppose that temporal niche partitioning could explain the high fish diversity in these assemblages. Hence, more studies on the temporal segregation of Amazonian fish are needed to understand the distributional, behavioral and functional ecological patterns of these assemblages.

Acknowledgements

We are grateful to PIBIC/UNIR for providing an undergraduate research project scholarship for WVN, an undergraduate student in the Fisheries Engineering Department. We would also like to thank the Instituto Chico Mendes de Conservação da Biodiversidade for providing sampling permits (no. 311560-1/2011) and the Ichthyology and Fish Laboratory at the Federal University of Rondônia, in particular W. Ohara and J. Lima Filho, for assistance with the taxonomic identification. Statistica serial number: AX505B150718FA.

  • Cite as: Costa, I.D. and Nogueira, W.V. Diel variation in the structure of fish assemblages in south western Amazon streams. Acta Limnologica Brasiliensia, 2016, vol. 28, e16.

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Publication Dates

  • Publication in this collection
    2016

History

  • Received
    27 May 2016
  • Accepted
    23 Sept 2016
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