Spatial and temporal variation of the diet of the flag tetra Hyphessobrycon heterorhabdus (Characiformes: Characidae) in streams of the Eastern Amazon

Naraiana Loureiro Benone Cleonice Maria Cardoso Lobato Bruno Eleres Soares Luciano Fogaça de Assis Montag About the authors

ABSTRACT

Spatial and temporal variations in streams promote large fluctuations of resource availability, thus affecting the diet of fishes. We evaluated the effects of hydrological periods and stream order within periods on the diet of the flag tetra Hyphessobrycon heterorhabdus. We analyzed 160 stomachs in eight streams ranging from 1st to 3rd order between dry and flood period. Sampled streams belonged to a well-preserved area in the Eastern Amazon. The flag tetra is omnivorous, with a tendency towards insectivory. During the dry period, the species exhibited a higher amount of autochthonous than allochthonous items. Fish consumed more allochthonous items in 1st and 2nd order streams in the dry period and in 1st and 3rd order streams in the flood period. These results reflect the interactions between temporal and longitudinal factors on resource availability and its influence on fish diet. This pattern is probably dependent on the extensive riparian vegetation as a direct and indirect source of food for stream fish.

Keywords:
Feeding; Floodplain; Hydrological period; Riparian vegetation; Stream order

RESUMO

Variações espaciais e temporais em habitats de riachos promovem grandes flutuações na disponibilidade de recursos, afetando assim a dieta dos peixes. Avaliamos os efeitos dos períodos hidrológicos e da ordem do riacho em cada período na dieta do tetra Hyphessobrycon heterorhabdus. Analisamos 160 estômagos em oito riachos variando de 1ª a 3ª ordem entre o período de seca e cheia. Todos os riachos foram amostrados em uma área bem preservada na Amazônia Oriental. O tetra é onívoro com tendência à insetivoria. Durante o período seco, a espécie exibiu maior quantidade de itens autóctones do que itens alóctones. Os peixes consumiram mais itens alóctones nos riachos de 1ª e 2ª ordem no período de seca e nos riachos de 1ª e 3ª ordem no período de cheia. Esses resultados refletem as interações entre fatores temporais e longitudinais na disponibilidade de recursos e sua influência na dieta de peixes. Este padrão é provavelmente dependente da extensa vegetação ripária como fonte direta e indireta de alimento para peixes de riachos.

Palavras-chave:
Alimentação; Ordem dos riachos; Período hidrológico; Planície de inundação; Vegetação ripária

INTRODUCTION

Fish play an essential role in nutrient cycling by linking aquatic and terrestrial ecosystems (Milardi et al., 2016Milardi M, Käkelä R, Weckström J, Kahilainen KK. Terrestrial prey fuels the fish population of a small, high-latitude lake. Aquat Sci. 2016; 78(4):695-706. http://dx.doi.org/10.1007/s00027-015-0460-1
http://dx.doi.org/10.1007/s00027-015-046...
). They prey on terrestrial plants and invertebrates that fall on streams, incorporating terrestrial carbon in streams (Brejão et al., 2013Brejão GL, Gerhard P, Zuanon J. Functional trophic composition of the ichthyofauna of forest streams in eastern Brazilian Amazon. Neotrop Ichthyol. 2013; 11(2):361-73. https://doi.org/10.1590/S1679-62252013005000006
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; Milardi et al., 2016). On the other hand, fish also prey on the early stages of aquatic invertebrates (Pinto, Uieda, 2007Pinto TLF, Uieda VS. Aquatic insects selected as food for fishes of a tropical stream: are there spatial and seasonal differences in their selectivity?. Acta Limnol Bras . 2007; 19(1):67-78.), impairing the amount of aquatic carbon transferred to terrestrial ecosystems in the form of winged adults. Since headwater stream fish are mainly dependent on terrestrial subsidies, studying their diet and how it changes in time and space is vital to understand the food web connecting both systems (Deus, Petrere-Junior, 2003Deus CP, Petrere-Junior M. Seasonal diet shifts of seven fish species in an Atlantic rainforest stream in southeastern Brazil. Braz J Biol . 2003; 63(4):579-88. https://doi.org/10.1590/S1519-69842003000400005
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; Wesner, 2013Wesner JS. Fish predation alters benthic, but not emerging, insects across whole pools of an intermittent stream. Freshw Sci. 2013; 32(2):438-49. http://dx.doi.org/10.1899/12-124.1
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; Wolff et al., 2013Wolff LL, Carniatto N, Hahn NS. Longitudinal use of feeding resources and distribution of fish trophic guilds in a coastal Atlantic stream, southern Brazil. Neotrop Ichthyol . 2013; 11(2):375-86. https://doi.org/10.1590/S1679-62252013005000005
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).

Spatial and temporal variations in the conditions of rivers and streams account for large fluctuations of resource availability (Thomaz et al., 2006Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia . 2006; 579(1):1-13. http://dx.doi.org/10.1007/s10750-006-0285-y
http://dx.doi.org/10.1007/s10750-006-028...
; Lisboa et al., 2015Lisboa LK, Silva ALL, Siegloch AE, Gonçalves Júnior JF, Petrucio MM. Temporal dynamics of allochthonous coarse particulate organic matter in a subtropical Atlantic rainforest Brazilian stream. Mar Freshw Res . 2015; 66(8):674-80. http://dx.doi.org/10.1071/MF14068
http://dx.doi.org/10.1071/MF14068...
). Lotic systems are highly heterogeneous due to their open nature and their interactions with their surrounding landscape (Ward, 1989Ward JV. The four-dimensional nature of lotic ecosystems. J North Am Benthol Soc. 1989; 8(1):2-8. https://doi.org/10.2307/1467397
https://doi.org/10.2307/1467397...
). The variations on the longitudinal and temporal dimensions have profound effects on the diet of fishes (Deus, Petrere-Junior, 2003Deus CP, Petrere-Junior M. Seasonal diet shifts of seven fish species in an Atlantic rainforest stream in southeastern Brazil. Braz J Biol . 2003; 63(4):579-88. https://doi.org/10.1590/S1519-69842003000400005
https://doi.org/10.1590/S1519-6984200300...
; Wolff et al., 2013Wolff LL, Carniatto N, Hahn NS. Longitudinal use of feeding resources and distribution of fish trophic guilds in a coastal Atlantic stream, southern Brazil. Neotrop Ichthyol . 2013; 11(2):375-86. https://doi.org/10.1590/S1679-62252013005000005
https://doi.org/10.1590/S1679-6225201300...
).

In the longitudinal dimension, changes in the channel morphology and riparian cover can alter the type and variability of food items, with the increasing importance of autochthonous items downstream (Vannote et al., 1980Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE. The river continuum concept. Can J FishAquat Sci . 1980; 37:130-37. https://doi.org/10.1139/f80-017
https://doi.org/10.1139/f80-017...
; Wolff et al., 2013Wolff LL, Carniatto N, Hahn NS. Longitudinal use of feeding resources and distribution of fish trophic guilds in a coastal Atlantic stream, southern Brazil. Neotrop Ichthyol . 2013; 11(2):375-86. https://doi.org/10.1590/S1679-62252013005000005
https://doi.org/10.1590/S1679-6225201300...
). Small forested streams are typically oligotrophic because of the extensive shading by the riparian vegetation. Given this, the aquatic fauna of headwaters relies on allochthonous input to sustain the trophic network. Fishes usually feed on terrestrial insects or larvae of aquatic insects that, by its turn, depend on allochthonous organic matter (Kemenes, Forsberg, 2014Kemenes A, Forsberg BR. Factors influencing the structure and spatial distribution of fishes in the headwater streams of the Jaú River in the Brazilian Amazon. Braz J Biol . 2014; 74(3):23-32. https://doi.org/10.1590/1519-6984.06812
https://doi.org/10.1590/1519-6984.06812...
; Montag et al., 2019Montag LFA, Leão H, Benone NL, Monteiro-Júnior CS, Faria APJ, Nicacio G et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia. 2019; 826(1):263-77. http://dx.doi.org/10.1007/s10750-018-3738-1
http://dx.doi.org/10.1007/s10750-018-373...
). However, reduced riparian cover in larger streams allows increased light input to the aquatic environment. This light stimulates primary production, allowing consumers to survive on autochthonous resources and enhancing the variety of food items to the fish fauna (Pouilly et al., 2006Pouilly M, Barrera S, Rosales C. Changes of taxonomic and trophic structure of fish assemblages along an environmental gradient in the Upper Beni watershed (Bolivia). J Fish Biol . 2006; 68(1):137-56. https://doi.org/10.1111/j.0022-1112.2006.00883.x
https://doi.org/10.1111/j.0022-1112.2006...
).

Temporal changes markedly shape large rivers (Flood Pulse Concept, Junk et al., 1989Junk WJ, Bayley PB, Sparks RE. The flood pulse concept in river-floodplain systems. In: Dodge DP, editor. Proceedings of the international large river Symposium. Ontario: Canadian special publication in fisheries and aquatic sciences; 1989. p.110-27.), but are deemed less important in small streams since local stochastic rainfall events affect stream dynamics (Saito, Mazão, 2012Saito VS, Mazão GR. Macroinvertebrates under stochastic hydrological disturbance in Cerrado streams of Central Brazil. Iheringia Ser Zool. 2012; 102(4):448-52. http://dx.doi.org/10.1590/S0073-47212012005000008
http://dx.doi.org/10.1590/S0073-47212012...
). However, due to sea-level changes during the Holocene, the lower courses of several clear- and blackwater rivers in the Amazon are lake-like (“ria lake”, “river-lake” or “drowned streams”, Sioli, 1967Sioli H. Studies in Amazon waters. Atas do Simpósio sôbre a Biodiversidade Amazônica. 1967; 3:9-50.). Their tributaries have slow flows and large widths permanently associated with broad floodplains (Behling, Costa, 2000Behling H, Costa ML. Holocene environmental changes from the Rio Curuá record in the Caxiuanã region, eastern Amazon Basin. Quat Res. 2000; 53(3):369-77. https://doi.org/10.1006/qres.1999.2117
https://doi.org/10.1006/qres.1999.2117...
; Benone et al., 2018Benone NL, Ligeiro R, Juen L, Montag LFA. Role of environmental and spatial processes structuring fish assemblages in streams of the eastern Amazon. Mar Freshw Res. 2018; 69(2):243-52. http://dx.doi.org/10.1071/MF17103
http://dx.doi.org/10.1071/MF17103...
). In the Anapu river basin (Eastern Amazon), Benone et al. (2018) showed that the width of such streams and their floodplains widely differed between the dry and the flood period, offering an opportunity for fish to explore several new environments and find more resources during the flood period.

To investigate the spatial and temporal variations in the diet of fishes in drowned streams, we chose the flag tetra Hyphessobrycon heterorhabdus (Ulrey, 1894) (Characiformes: Characidae), a common species in the lower Amazon river basin, as a model study. This gregarious species is nektonic and inhabits the backwaters predominantly, picking food particles in the upper layer of the water column (Brejão et al., 2013Brejão GL, Gerhard P, Zuanon J. Functional trophic composition of the ichthyofauna of forest streams in eastern Brazilian Amazon. Neotrop Ichthyol. 2013; 11(2):361-73. https://doi.org/10.1590/S1679-62252013005000006
https://doi.org/10.1590/S1679-6225201300...
). We hypothesized that: 1) the smaller shading in downstream direction may allow increasing importance of autochthonous items to the food webs; thus, the diet of H. heterorhabdus would change from 1st to 3rd order streams, and 2) streams will be much broader during the flood period than during the dry period, increasing the availability of allochthonous items in the floodplain and their relative importance to the species’ diet during this period.

MATERIAL AND METHODS

Study area. We sampled fish in streams within the Caxiuanã National Forest, a federal protected area located in Portel and Melgaço, State of Pará, Brazil, in the lower Anapu region, Eastern Amazon (Fig. 1). The Caxiuanã National Forest is covered predominantly by a dense lowland Terra-Firme rainforest (85% of its total area). The mean air temperature is 26.7°C, ranging from a minimum of 23°C to a maximum of 32.7°C (Lisboa, 2002Lisboa PLB. Caxiuanã: populações tradicionais, meio físico e diversidade biológica. Belém: Museu Paraense Emílio Goeldi; 2002.). The local climate is tropical hot and humid, corresponding to Köppen’s Am type, with a well-defined seasonality and a short dry period (Peel et al., 2007Peel MC, Finlayson BL, McMahon TA. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci. 2007; 4(2):439-73.), with a dry season from July to November and a rainy season between December and June (Oliveira et al., 2008Oliveira LL, Costa RF, Sousa FAS, Costa ACL, Braga AP. Precipitação efetiva e interceptação em Caxiuanã, na Amazônia Oriental. Acta Amaz . 2008; 38(4):723-32. https://doi.org/10.1590/S0044-59672008000400016
https://doi.org/10.1590/S0044-5967200800...
). The lower Anapu River reaches its highest water level in April and May (180 cm), dropping to a minimum of 120 cm in November and December. Due to the drowning of local valleys in the Holocene, the lower Anapu is impounded and gained lacustrine features (i.e., ria lakes) (Behling, Costa, 2000Behling H, Costa ML. Holocene environmental changes from the Rio Curuá record in the Caxiuanã region, eastern Amazon Basin. Quat Res. 2000; 53(3):369-77. https://doi.org/10.1006/qres.1999.2117
https://doi.org/10.1006/qres.1999.2117...
). It resulted in slow-flowing streams with acidic water and a dense amount of leaf packs and trunks covering the streambed. Their main channels are associated with broad floodplains that can reach > 100 m during the flood period (Benone et al., 2018Benone NL, Ligeiro R, Juen L, Montag LFA. Role of environmental and spatial processes structuring fish assemblages in streams of the eastern Amazon. Mar Freshw Res. 2018; 69(2):243-52. http://dx.doi.org/10.1071/MF17103
http://dx.doi.org/10.1071/MF17103...
).

FIGURE 1
| Streams sampled during the dry period of 2010 and the flood period of 2011 in the Caxiuanã National Forest, Eastern Amazon, State of Pará, Brazil.

Fish sampling. We selected eight streams, three of 1st order, two of 2nd order, and three of 3rd order. Each stream was sampled twice, one during the dry period (November 2010) and one in the flood period (April 2011). We sampled fish specimens with hand sieves of 55 cm and 3 mm mesh in a 50 m stretch for 6h divided among three or four collectors. Specimens were fixed in 10% formalin and preserved in 70% ethanol under voucher number MPEG 23389 (Ichthyological Collection, Museu Paraense Emílio Goeldi, Belém, PA, Brazil).

Diet description. To assess diet composition of H. heterorhabdus, we selected ten individuals in each stream, with 160 specimens divided into 80 per hydrological period. We analyzed their stomach contents under a stereoscopic microscope. We identified food items using the literature (Mugnai et al., 2010Mugnai R, Nessimian JL, Baptista DF. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro. Rio de Janeiro: Technical Books Editora; 2010.; Hamada et al., 2014Hamada N, Nessimian JL, Querino RB. Insetos Aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Manaus: INPA; 2014.) and with the input from specialists. To obtain the percentage composition of each food item, we placed the stomach contents in a dish over a graph paper and then counted the grid cells covered by each food item. Dataset is available in the Figshare digital repository (10.6084/m9.figshare.12967901). We converted counts into percentages by comparing then to the total grid cells covered by all items in each stomach (Hynes, 1950Hynes HBN. The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol. 1950; 19(1):36-58. Available from: https://www.jstor.org/stable/1570
https://www.jstor.org/stable/1570...
). Dominance is the percentage that an item occupied most of the content of each stomach related to the total number of stomachs, while the frequency of occurrence is the percentage of the number of stomachs in which an item occurs over the total number of stomachs (Hyslop, 1980Hyslop EJ. Stomach contents analysis - a review of methods and their application. J Fish Biol . 1980; 17(4):411-29. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
https://doi.org/10.1111/j.1095-8649.1980...
). We combined these indices to calculate the Alimentary index (Ai%, Kawakami, Vazzoler, 1980Kawakami E, Vazzoler G. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Oceanog. 1980; 29(2):205-07. https://doi.org/10.1590/S0373-55241980000200043
https://doi.org/10.1590/S0373-5524198000...
) for hydrological periods and orders. Ai% estimates the relative importance of each food item to the species’ diet.

We analyzed the feeding strategy of H. heterorhabdus using the graphical method of Amundsen et al. (1996Amundsen PA, Gabler HM, Staldvik FJ. A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. J Fish Biol. 1996; 48(4):607-14. https://doi.org/10.1111/j.1095-8649.1996.tb01455.x
https://doi.org/10.1111/j.1095-8649.1996...
) based on the frequency of occurrence and prey-specific abundance of food items, which is calculated using their dominance. We plotted food items in a bivariate space to analyze the species’ feeding strategy, and the contribution of individual niche breadth and niche overlap among individuals to the niche breadth of the population. Higher values in the horizontal axis indicate common use of the food item by the population. Higher values in the vertical axis indicate specialization in the food item. The importance of individuals’ strategies to the niche breadth of the population may be assessed from a diagonal axis, starting in the minimum value in the horizontal axis and maximum value in the vertical axis. The high between-phenotype component indicates a population composed of specialist individuals, and a high within-phenotype component shows a population consisting of generalist individuals.

Statistical analysis. We used the square-rooted percentage composition of each specimen to build a dissimilarity matrix based on the Bray-Curtis index (Legendre, Legendre, 2012Legendre P, Legendre L. Numerical ecology. Oxford: Elsevier; 2012.). To evaluate if the diet of H. heterorhabdus varied between hydrologic periods and stream orders, we used a permutational multivariate analysis of variance (PERMANOVA, Anderson et al., 2008Anderson MJ, Gorley RN, Clarke K R. PERMANOVA+ for PRIMER: Guide to software and statistical methods. Plymouth: PRIMER-E; 2008.). To assess differences in diet heterogeneity within factors (hydrologic periods and stream orders), we used a permutational analysis of multivariate dispersions (PERMDISP, Anderson et al., 2008). For both analyses, we considered stream orders nested within periods and applied pairwise posthoc tests. P-values were obtained through Monte-Carlo procedures. We performed a similarity percentage breakdown (SIMPER) to evaluate the contribution of each food item to the dietary dissimilarities between periods and stream orders (nested within periods). Data variation was visualized by running a principal coordinate analysis (PCoA, Legendre, Legendre, 2012). We ran all analyses using 999 permutations in the R environment (R Core Team, 2016R Core Team. R: A language and environment for statistical computing. [Computer software manual - Internet]. Vienna: R Foundation for Statistical Computing; 2016.), using the vegan package (Oksanen et al., 2016Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al. vegan: Community ecology package. [Computer software manual - Internet]. R package 2.4. 2016. Available from: https://cran.r-project.org/web/packages/vegan/index.html
https://cran.r-project.org/web/packages/...
) and codes provided by Soares et al. (2020Soares BE, Benone NL, Rosa DCO, Montag LFA. Do local environmental factors structure the trophic niche of the splash tetra, Copella arnoldi? A test in an Amazonian stream system. Acta Amaz . 2020; 50(1):54-60. http://dx.doi.org/10.1590/1809-4392201802681
http://dx.doi.org/10.1590/1809-439220180...
).

RESULTS

From the 160 stomachs, one was empty, so we used 159 stomachs for further analysis. The species diet was composed of 18 items, ten allochthonous, seven autochthonous, and one of unknown origin (Tab. 1). The diet of H. heterorhabdus is mainly composed of exoskeleton fragments and by a variety of insect groups, such as Odonata, Hemiptera, and Trichoptera, followed by allochthonous vegetal fragments. The species consumed higher amounts of autochthonous items than allochthonous ones in the dry period (Ai%: 33.30 vs. 29.09), but the inverse occurred in the flood period (Ai%: 42.60 vs. 49.56). Fish consumed more allochthonous items in 1st and 2nd order streams in the dry period and in 1st and 3rd order streams in the flood period (Tab. 1).

TABLE 1
| Alimentary index (Ai%) per hydrological period and stream order for Hyphessobrycon heterorhabdus. Bold values indicate items with a strong contribution to diet (≥ 20%).

In the Amundsen graph (Fig. 2), most items were positioned in the lower and upper left, indicating that this species has a generalist diet based mostly on rarely consumed food items (frequency of occurrence % < 50%) and some specialized individuals. The predominance of food items with a low frequency of occurrence supports the importance of the between-phenotype component for the niche breadth of the population. This pattern was similar in both hydrological periods and stream orders.

FIGURE 2
| Feeding strategy revealed by Amundsen diagram of Hyphessobrycon heterorhabdus sampled in eight streams of a protected area in the Eastern Amazon, Brazil. A, C, E, and G represent feeding during the dry period, while B, D, F, and H represent the flood period. A and B show the diet considering all streams, whilst C and D represent 1st order streams, E and F represent 2nd order streams, and G and H represent 3rd order streams. V01 = Ephemeroptera (nymph); V02 = Odonata (larvae); V03 = Coleoptera (larvae); V04 = Diptera (larvae); V05 = Diptera (eggs); V06 = Diptera (pupae); V07 = Exoskeleton fragments (autochthonous source); V08 = Exoskeleton fragments (unknown source); V09 = Exoskeleton fragments (allochthonous source); V10 = Isoptera; V11 = Formicidae; V12 = Trichoptera; V13 = Hemiptera; V14 = Ephemeroptera; V15 = Orthoptera; V16 = Coleoptera; V17 = Heteroptera; V18 = Vegetal fragments (allochthonous source).

We found differences between periods (pseudo-F = 2.60, p < 0.01) and order (pseudo-F = 4.95, p < 0.01) for the diet of H. heterorhabdus (Figs. 3-4). Within dry period, diet varied between 1st and 3rd orders and 2nd and 3rd orders, while it varied among all pairs of orders within flood period (Tab. 2). The PERMDISP analysis showed no difference in diet heterogeneity for period (F = 1.63, p = 0.20) or for orders within the dry period (Dry: F = 0.17, p = 0.83). Orders within the flood period showed distinct levels of heterogeneity (Flood: F = 6.23, p < 0.01), resulting from 2nd and 3rd order streams difference (average distance to median: 1st = 0.57, 2nd = 0.51, 3rd = 0.62) (Tab. 3).

FIGURE 3
| Ordination of the diet of Hyphessobrycon heterorhabdus between hydrological periods in eight streams of a protected area in the Eastern Amazon, Brazil.

FIGURE 4
| Variation of the diet of Hyphessobrycon heterorhabdus among stream orders during A. dry and B. flood periods in eight streams of a protected area in the Eastern Amazon, Brazil.

TABLE 2
| Results of pairwise PERMANOVA for stream orders nested within periods. Data refers to the diet of Hyphessobrycon heterorhabdus sampled in eight streams in a protected area in the Eastern Amazon. *significant values at α < 0.05.

TABLE 3
| Results of pairwise PERMDISP for stream orders during the flood period. Data refers to the diet of Hyphessobrycon heterorhabdus sampled in eight streams in a protected area in the Eastern Amazon. *significant values at α < 0.05.

Differences in the diet composition of H. heterorhabdus between periods were related to the higher consumption of vegetal fragments and adult Trichoptera during the flood period and higher consumption of exoskeleton fragments of unknown origin and adult Hemiptera during the dry period (SIMPER; Tab. 4). This analysis confirmed the higher ingestion of autochthonous items during the dry period than in the flood period.

TABLE 4
| Results of SIMPER analysis. Values represent the contribution of food items for the diet of Hyphessobrycon heterorhabdus per hydrological periods and stream orders.

During the dry period, fish in the 1st and 2nd order streams consumed more allochthonous items than fish in 3rd order streams. The most consumed items in lower orders were Hemiptera, exoskeleton fragments, and vegetal fragments. Coleoptera and Diptera (egg) were exclusively consumed in 3rd orders streams. In the flood period, 1st order eggs had five exclusive items, four of them of allochthonous origin. Fish in 2nd order streams consumed large amounts of exoskeleton fragments (autochthonous source), whereas fish in 3rd order streams largely ingested vegetal fragments and two exclusive items (eggs of Diptera and adults Ephemeroptera).

DISCUSSION

Our results show that H. heterorhabdus is omnivorous and tends towards insectivory, feeding both on autochthonous and allochthonous items. Regarding our hypotheses, we found that the fish diet differs between stream orders and hydrological periods. We believe these results reflect temporal and spatial changes in the resources’ availability. However, since we evaluated temporal changes only within a single year, we recognize that our results must be taken with caution.

The generalist diet of H. heterorhabdus is similar to the reported to other congeneric species, which feed on a large variety of items. Although species of this genus are usually classified as invertivores (Casatti et al., 2003Casatti L, Mendes HF, Ferreira KM. Aquatic macrophytes as feeding site for small fishes in the Rosana Reservoir, Paranapanema River, Southeastern Brazil. Braz J Biol . 2003; 63(2):213-22. https://doi.org/10.1590/S1519-69842003000200006
https://doi.org/10.1590/S1519-6984200300...
; Pelicice, Agostinho, 2006Pelicice FM, Agostinho AA. Feeding ecology of fishes associated with Egeria spp. patches in a tropical reservoir, Brazil. Ecol Freshw Fish. 2006; 15(1):10-19. http://dx.doi.org/10.1111/j.1600-0633.2005.00121.x
http://dx.doi.org/10.1111/j.1600-0633.20...
; Prado et al., 2016Prado AVR, Goulart E, Pagotto JPA. Ecomorphology and use of food resources: inter-and intraspecific relationships of fish fauna associated with macrophyte stands. Neotrop Ichthyol . 2016; 14(4):e150140. http://dx.doi.org/10.1590/1982-0224-20150140
http://dx.doi.org/10.1590/1982-0224-2015...
), previous reports detected omnivorous diets (Coutinho et al., 2000Coutinho AB, Aguiaro T, Branco CWC, Albuquerque EF, Souza-Filho IF. Alimentação de Hyphessobrycon bifasciatus Ellis, 1911 (Osteichthyes, Characidae) na lagoa Cabiúnas, Macaé, RJ. Acta Limnol Bras. 2000; 12:45-54.; Sánchez-Botero et al., 2007Sánchez-Botero JI, Leitão RP, Caramaschi EP, Garcez DS. The aquatic macrophytes as refuge, nursery and feeding habitats for freshwater fish from Cabiúnas Lagoon, Restinga de Jurubatiba National Park, Rio de Janeiro, Brazil. Acta Limnol Bras . 2007; 19(2):143-53.; Soneira et al., 2016Soneira PA, Díaz FJR, Casciotta JR, Almirón AE. Diet of Hyphessobrycon auca (Pisces, Characidae) in Iberá Wetland (Northeastern, Argentina). FACENA. 2016; 27:3-8. http://dx.doi.org/10.30972/fac.270923
http://dx.doi.org/10.30972/fac.270923...
), paralleling our results and confirming the high plasticity of characids (Abelha et al., 2001Abelha MCF, Agostinho AA, Goulart E. Plasticidade trófica em peixes de água doce. Acta Sci. 2001; 23(2):425-34.; Portella et al., 2016Portella T, Lobón-Cerviá J, Manna LR, Bergallo HG, Mazzoni R. Eco-morphological attributes and feeding habits in coexisting characins. J Fish Biol . 2016; 90(1):129-46. https://doi.org/10.1111/jfb.13162
https://doi.org/10.1111/jfb.13162...
). Insects were the most important items in the stomachs of H. heterorhabdus in our study, a result commonly reported for the diet of tropical stream fish, either as falling items drifting on the surface (Silva et al., 2016Silva NCS, Costa AJL, Louvise J, Soares BE, Reis VCS, Albrecht MP et al. Resource partitioning and ecomorphological variation in two syntopic species of Lebiasinidae (Characiformes) in an Amazonian stream. Acta Amaz . 2016; 46(1):25-36. http://dx.doi.org/10.1590/1809-4392201501024
http://dx.doi.org/10.1590/1809-439220150...
) or as aquatic insects in multiple stages of development associated to the streambed (Pinto, Uieda, 2007Pinto TLF, Uieda VS. Aquatic insects selected as food for fishes of a tropical stream: are there spatial and seasonal differences in their selectivity?. Acta Limnol Bras . 2007; 19(1):67-78.; Rolla et al., 2009Rolla APPR, Esteves KE, Ávila-da-Silva AO. Feeding ecology of a stream fish assemblage in an Atlantic Forest remnant (Serra do Japi, SP, Brazil). Neotrop Ichthyol . 2009; 7(1):65-76. https://doi.org/10.1590/S1679-62252009000100009
https://doi.org/10.1590/S1679-6225200900...
). This finding shows the importance of the quality and amount of the riparian vegetation for the diet of stream-dwelling fish since aquatic invertebrates depend on allochthonous organic matter to thrive (Malmqvist, 2002Malmqvist B. Aquatic invertebrates in riverine landscapes. Freshw Biol. 2002; 47(4):679-94. https://doi.org/10.1046/j.1365-2427.2002.00895.x
https://doi.org/10.1046/j.1365-2427.2002...
).

The diet of H. heterorhabdus changed between the dry and flood period, which could be linked to the temporal fluctuations of the insect communities detected in other studies in the tropical region (Deus, Petrere-Junior, 2003Deus CP, Petrere-Junior M. Seasonal diet shifts of seven fish species in an Atlantic rainforest stream in southeastern Brazil. Braz J Biol . 2003; 63(4):579-88. https://doi.org/10.1590/S1519-69842003000400005
https://doi.org/10.1590/S1519-6984200300...
; Peterson et al., 2017Peterson CC, Keppeler FW, Saenz DE, Bower LM, Winemiller KO. Seasonal variation in fish trophic networks in two clear-water streams in the Central Llanos region, Venezuela. Neotrop Ichthyol . 2017; 15(2):e160125. http://dx.doi.org/10.1590/1982-0224-20160125
http://dx.doi.org/10.1590/1982-0224-2016...
). Some studies did not observe variation in the diet between periods (Pinto, Uieda, 2007Pinto TLF, Uieda VS. Aquatic insects selected as food for fishes of a tropical stream: are there spatial and seasonal differences in their selectivity?. Acta Limnol Bras . 2007; 19(1):67-78.; Costa, Soares, 2015Costa ID, Soares MO. The seasonal diet of Aequidens tetramerus (Cichlidae) in a small forest stream in the Machado River basin, Rondônia, Brazil. Acta Amaz. 2015; 45(4):365-72. http://dx.doi.org/10.1590/1809-4392201500223
http://dx.doi.org/10.1590/1809-439220150...
), which was associated with the wide availability of food items all year round, mainly insects (Rezende, Mazzoni, 2006Rezende CF, Mazzoni R. Disponibilidade e uso de recursos alóctones por Bryconamericus microcephalus (Miranda-Ribeiro) (Actinopterygii, Characidae), no córrego Andorinha, Ilha Grande, Rio de Janeiro, Brasil. Rev Bras Zool. 2006; 23(1): 218-22. https://doi.org/10.1590/S0101-81752006000100014
https://doi.org/10.1590/S0101-8175200600...
). We believe that the temporal differences in our results are primarily caused by fluctuations of the water level that promote seasonal variability of stream physical conditions in the lower Anapu river (Benone et al., 2018Benone NL, Ligeiro R, Juen L, Montag LFA. Role of environmental and spatial processes structuring fish assemblages in streams of the eastern Amazon. Mar Freshw Res. 2018; 69(2):243-52. http://dx.doi.org/10.1071/MF17103
http://dx.doi.org/10.1071/MF17103...
; Montag et al., 2019Montag LFA, Leão H, Benone NL, Monteiro-Júnior CS, Faria APJ, Nicacio G et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia. 2019; 826(1):263-77. http://dx.doi.org/10.1007/s10750-018-3738-1
http://dx.doi.org/10.1007/s10750-018-373...
), thus affecting the availability of insects and plant material.

Due to the natural impoundment in the Anapu river, the streams present wide floodplains covered by large extensions of primary forest (Benone et al., 2018Benone NL, Ligeiro R, Juen L, Montag LFA. Role of environmental and spatial processes structuring fish assemblages in streams of the eastern Amazon. Mar Freshw Res. 2018; 69(2):243-52. http://dx.doi.org/10.1071/MF17103
http://dx.doi.org/10.1071/MF17103...
), a prolific source of allochthonous material. The increased lateral connectivity between the stream channel and the floodplain during the flood period offers new areas for fish to explore and feed (Thomaz et al., 2006Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia . 2006; 579(1):1-13. http://dx.doi.org/10.1007/s10750-006-0285-y
http://dx.doi.org/10.1007/s10750-006-028...
). This increased connectivity may explain the large proportion of terrestrial plant material ingested by H. heterorhabdus, especially in 3rd order streams during the flood period due to its increased accessibility in the forested floodplains (Thomaz et al., 2006; Junk et al., 2007Junk WJ, Soares MGM, Bayley PB. Freshwater fishes of the Amazon River basin: their biodiversity, fisheries, and habitats. Aquat Ecosyst Health Manag. 2007; 10(2):153-73. http://dx.doi.org/10.1080/14634980701351023
http://dx.doi.org/10.1080/14634980701351...
) together with stronger winds and heavy rains (Pinto, Uieda, 2007Pinto TLF, Uieda VS. Aquatic insects selected as food for fishes of a tropical stream: are there spatial and seasonal differences in their selectivity?. Acta Limnol Bras . 2007; 19(1):67-78.). Although we did not measure the resource availability, we believe our points are valid since the studied area is highly preserved, and it shows large variations in stream width (Benone et al., 2018).

Diet composition changed between all orders within the flood period, being more heterogeneous in 3rd order streams. The increasing size of streams could encompass a growing variability of food items for fish because they are larger, have maximum habitat diversity, and contain more food sources (Cargnin-Ferreira, Forsberg, 2000Cargnin-Ferreira E, Forsberg BF. Trophic structure of macroinvertebrate communities in the Jaú River System (Central Amazon, Brazil). Braz J Biol. 2000; 3:59-66.; Wolff et al., 2013Wolff LL, Carniatto N, Hahn NS. Longitudinal use of feeding resources and distribution of fish trophic guilds in a coastal Atlantic stream, southern Brazil. Neotrop Ichthyol . 2013; 11(2):375-86. https://doi.org/10.1590/S1679-62252013005000005
https://doi.org/10.1590/S1679-6225201300...
). Additionally, the floodplains should be more extensive in downstream water bodies, offering refugia to aquatic insects, and retaining falling terrestrial material (Braccia, Batzer, 2001Braccia A, Batzer DP. Invertebrates associated with woody debris in a southeastern U.S. forested floodplain wetland. Wetlands. 2001; 21(1):18-31.).

Fish are expected to change their diet from allochthonous to autochthonous items in the downstream direction (Vannote et al., 1980Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE. The river continuum concept. Can J FishAquat Sci . 1980; 37:130-37. https://doi.org/10.1139/f80-017
https://doi.org/10.1139/f80-017...
; Angermeier, Karr, 1983Angermeier PL, Karr JR. Fish communities along environmental gradients in a system of tropical streams. Environ Biol Fishes. 1983; 9(2):117-35. https://doi.org/10.1007/BF00690857
https://doi.org/10.1007/BF00690857...
; Pouilly et al., 2006Pouilly M, Barrera S, Rosales C. Changes of taxonomic and trophic structure of fish assemblages along an environmental gradient in the Upper Beni watershed (Bolivia). J Fish Biol . 2006; 68(1):137-56. https://doi.org/10.1111/j.0022-1112.2006.00883.x
https://doi.org/10.1111/j.0022-1112.2006...
; Wolff et al., 2013Wolff LL, Carniatto N, Hahn NS. Longitudinal use of feeding resources and distribution of fish trophic guilds in a coastal Atlantic stream, southern Brazil. Neotrop Ichthyol . 2013; 11(2):375-86. https://doi.org/10.1590/S1679-62252013005000005
https://doi.org/10.1590/S1679-6225201300...
). We observed such a change for both periods, although not as evident in the flood. The smaller canopy provided by trees downstream limits the fall of terrestrial invertebrates (Pouilly et al., 2006). The autochthonous diet is favored by the large accumulation of organic material in these naturally impounded streams due to the low water flow. The richness and composition of aquatic insects are strongly associated with large woody debris and leaf litter since they provide cover and food (Smith et al., 1993Smith RD, Sidle RC, Porter PE, Noel JR. Effects of experimental removal of woody debris on the channel morphology of a forest, gravel-bed stream. J Hydrol. 1993; 152(1-4):153-78. https://doi.org/10.1016/0022-1694(93)90144-X
https://doi.org/10.1016/0022-1694(93)901...
; Braccia, Batzer, 2001Braccia A, Batzer DP. Invertebrates associated with woody debris in a southeastern U.S. forested floodplain wetland. Wetlands. 2001; 21(1):18-31.; Montag et al., 2019Montag LFA, Leão H, Benone NL, Monteiro-Júnior CS, Faria APJ, Nicacio G et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia. 2019; 826(1):263-77. http://dx.doi.org/10.1007/s10750-018-3738-1
http://dx.doi.org/10.1007/s10750-018-373...
). Individuals in 3rd order streams exhibited distinct diet composition, which could also be related to the longitudinal supply of food resources (Wolff et al., 2013).

The analysis of the feeding strategy showed generalist populations with specialized individuals, but our sampling design does not allow direct explanations for this pattern. Nevertheless, we raised some possibilities. First, resources may have clumped distributions (Bolnick et al., 2003Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD et al. The ecology of individuals: incidence and implications of individual specialization. Am Nat. 2003; 161(1):1-28. https://doi.org/10.1086/343878
https://doi.org/10.1086/343878...
), such as patterns of distribution of eggs and larvae from aquatic insects (Wesner, 2013Wesner JS. Fish predation alters benthic, but not emerging, insects across whole pools of an intermittent stream. Freshw Sci. 2013; 32(2):438-49. http://dx.doi.org/10.1899/12-124.1
http://dx.doi.org/10.1899/12-124.1...
). In this scenario, stomach contents would reflect punctual prey availability instead of long-term processes. Second, differential resource use might reflect individual variation in morphology, behavior, and physiology (Bolnick et al., 2003Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD et al. The ecology of individuals: incidence and implications of individual specialization. Am Nat. 2003; 161(1):1-28. https://doi.org/10.1086/343878
https://doi.org/10.1086/343878...
; 2011Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M et al. Why intraspecific trait variation matters in community ecology. Trends Ecol Evol. 2011; 26(4):183-92. http://dx.doi.org/10.1016/j.tree.2011.01.009
http://dx.doi.org/10.1016/j.tree.2011.01...
). Trade-offs regarding resource recognition, prey capture efficiency, or resource handling ability generate individuals with different degrees of specialization and could be a result of the diversifying effect of intraspecific competition (Bolnick et al., 2011Bolnick DI, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M et al. Why intraspecific trait variation matters in community ecology. Trends Ecol Evol. 2011; 26(4):183-92. http://dx.doi.org/10.1016/j.tree.2011.01.009
http://dx.doi.org/10.1016/j.tree.2011.01...
). Moreover, the studied streams also contain several species of Hemigrammus Gill, 1858 and Hyphessobrycon Durbin, 1908 (Benone et al., 2018Benone NL, Ligeiro R, Juen L, Montag LFA. Role of environmental and spatial processes structuring fish assemblages in streams of the eastern Amazon. Mar Freshw Res. 2018; 69(2):243-52. http://dx.doi.org/10.1071/MF17103
http://dx.doi.org/10.1071/MF17103...
; Freitas et al., 2018Freitas TMS, Prudente BS, Freitas DTH, Benone NL, Leão H, Dutra GM et al. Fishes of Caxiuanã: 20 years (1993 to 2012) of sampling in a protected area in the Eastern Amazon. Bol Mus Para Emílio Goeldi, Sér Ciênc Nat. 2018; 13(2):185-204.). Both genera occupy similar niches (Brejão et al., 2013Brejão GL, Gerhard P, Zuanon J. Functional trophic composition of the ichthyofauna of forest streams in eastern Brazilian Amazon. Neotrop Ichthyol. 2013; 11(2):361-73. https://doi.org/10.1590/S1679-62252013005000006
https://doi.org/10.1590/S1679-6225201300...
), indicating a role for interspecific competition. However, to elucidate the reasons behind individual specialization, it is necessary to conduct studies on a larger timescale to evaluate the temporal consistency of observed patterns.

In conclusion, our study evidenced the temporal and spatial changes in the diet of a regionally common characid species. Although these patterns are predicted in ecological theories such as the River Continuum Concept (Vannote et al., 1980Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE. The river continuum concept. Can J FishAquat Sci . 1980; 37:130-37. https://doi.org/10.1139/f80-017
https://doi.org/10.1139/f80-017...
), few studies have been conducted in small tropical streams. These temporal and spatial fluctuations can affect the natural history of individual species (Costa, Soares, 2015Costa ID, Soares MO. The seasonal diet of Aequidens tetramerus (Cichlidae) in a small forest stream in the Machado River basin, Rondônia, Brazil. Acta Amaz. 2015; 45(4):365-72. http://dx.doi.org/10.1590/1809-4392201500223
http://dx.doi.org/10.1590/1809-439220150...
; Silva et al., 2016Silva NCS, Costa AJL, Louvise J, Soares BE, Reis VCS, Albrecht MP et al. Resource partitioning and ecomorphological variation in two syntopic species of Lebiasinidae (Characiformes) in an Amazonian stream. Acta Amaz . 2016; 46(1):25-36. http://dx.doi.org/10.1590/1809-4392201501024
http://dx.doi.org/10.1590/1809-439220150...
) and the trophic structure of fish assemblages (Pouilly et al., 2006Pouilly M, Barrera S, Rosales C. Changes of taxonomic and trophic structure of fish assemblages along an environmental gradient in the Upper Beni watershed (Bolivia). J Fish Biol . 2006; 68(1):137-56. https://doi.org/10.1111/j.0022-1112.2006.00883.x
https://doi.org/10.1111/j.0022-1112.2006...
; Peterson et al., 2017Peterson CC, Keppeler FW, Saenz DE, Bower LM, Winemiller KO. Seasonal variation in fish trophic networks in two clear-water streams in the Central Llanos region, Venezuela. Neotrop Ichthyol . 2017; 15(2):e160125. http://dx.doi.org/10.1590/1982-0224-20160125
http://dx.doi.org/10.1590/1982-0224-2016...
), and should be considered in future studies. Additionally, our study was conducted in a well-preserved area, offering an opportunity to observe natural patterns and contrast them with the alterations in fish diet promoted by human disturbances.

ACKNOWLEDGMENTS

We would like to thank the employees of the Estação Científica Ferreira Penna (ECFPn) for their assistance in the fieldwork; the Conselho Nacional para o Desenvolvimento Científico e Tecnológico (CNPq) (BES: 151743/2019-3, LFAM: 302406/2019-0), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (NLB: 88887.475625/2020-00, CMCL: 1660508/2016-11); and the Programa Nacional de Biodiversidade (PPBio) provided logistic support.

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  • HOW TO CITE THIS ARTICLE

    Benone NL, Lobato CMC, Soares BE, Montag LFA. Spatial and temporal variation of the diet of the flag tetra Hyphessobrycon heterorhabdus (Characiformes: Characidae) in streams of the Eastern Amazon. Neotrop Ichthyol. 2020; 18(4):e200078. https://doi.org/10.1590/1982-0224-2020-0078

Publication Dates

  • Publication in this collection
    04 Dec 2020
  • Date of issue
    2020

History

  • Received
    08 Aug 2020
  • Accepted
    06 Nov 2020
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E-mail: neoichth@nupelia.uem.br