Niche partitioning of two piscivorous fish species in a river in the western Brazilian Amazon

Particionamento de nicho de duas espécies de peixes piscívoros em um rio na Amazônia Ocidental Brasileira

ABSTRACT

We analyzed the seasonal variation in the diet, trophic niche breadth (Levins index), the partitioning of food resources (Pianka’s symmetric index) and trophic level (weighed average of trophic level of each prey determined in FishBase and SeaLifeBase platform) of Plagioscion squamosissimus (Heckel, 1840) and Hydrolycus scomberoides (Cuvier, 1819) in the Machado River, Rondônia, Brazil. Fish samplings were conducted bimonthly from June 2013 to May 2015 in five sites, using eight sets of gillnets. The occurrence frequency and volumetric frequency were used to quantify the food items. We analyzed the stomach contents of 283 individuals, 134 of H. scomberoides and 149 of P. squamosissimus. Fish were the most consumed food item by both piscivorous species. However, H. scomberoides mostly ingested pelagic fish (e.g. Characiformes fishes and Prochilodus nigricas Spix & Agassiz, 1829), while P. squamosissimus mostly consumed benthic fish [e.g. Pimelodus blochii Valenciennes, 1840 and Tenellus trimaculatus (Boulenger, 1898)]. Hydrolycus scomberoides presented the trophic level 3.55 for both periods analyzed, while P. squamosissimus 4.01 in the flood period and 3.82 in the drought period. Seasonal variations in the diet of H. scomberoides and P. squamosissimus were observed (PERMANOVA). Specifically, P. squamosissimus consumed mainly “Siluriformes” fishes and P. blochii in the drought period. The trophic niche breadth of P. squamosissimus was greater than that of H. scomberoides in the flood period. The species P. squamosissimus and H. scomberoides had low (0.35) food niche overlap in both seasons analysed. The data indicated that P. squamosissimus has a generalist feeding habit, while H. scomberoides is specialized in prey selection. The overlap of food niche between the species in both periods of the hydrological cycle was low, indicating that niche partitioning was probably the main mechanism of coexistence of these species, with little relationship with variations of the hydrological cycle.

KEYWORDS
Diet; trophic niche; Machado River; seasonal variation

RESUMO

Nós analisamos a variação sazonal na dieta, a amplitude do nicho trófico (Índice de Levins), a partição dos recursos alimentares (Índice simétrico de Pianka) e o nível trófico (média do nível trófico de cada presa determinada pela plataforma FishBase e SeaLifeBase) de Plagioscion squamosissimus (Heckel, 1840) e Hydrolycus scomberoides (Cuvier, 1819) no rio Machado, Rondônia, Brasil. As amostragens de peixes foram realizadas bimestralmente de junho de 2013 a maio de 2015 em cinco locais, utilizando oito conjuntos de redes de emalhar. A frequência de ocorrência e a frequência volumétrica foram utilizados para quantificar os itens alimentares. Analisamos o conteúdo estomacal de 283 indivíduos, 134 de H. scomberoides e 149 de P. squamosissimus. Peixes foram o item alimentar mais consumido pelas duas espécies piscívoras. No entanto, H. scomberoides ingeriu principalmente peixes pelágicos (ex. peixes Characiformes e Prochilodus nigricas Spix & Agassiz, 1829), enquanto P. squamosissimus consumiu principalmente peixes bentônicos [ex. Pimelodus blochii Valenciennes, 1840 e Tenellus trimaculatus (Boulenger, 1898)]. Hydrolycus scomberoides apresentou nível trófico de 3,55 para ambos os períodos analisados, enquanto para P. squamosissimus o nível trófico foi de 4,01 no período da cheia e 3,82 no período de seca. Variações sazonais na dieta de H. scomberoides e P. squamosissimus foram observadas (PERMANOVA). Especificamente, P. squamosissimus consumiu principalmente peixes “Siluriformes” e P. blochii no período de seca. A largura do nicho trófico de P. squamosissimus foi maior que a de H. scomberoides no período da cheia. Plagioscion squamosissimus e H. scomberoides apresentaram baixa (0,35) sobreposição de nicho alimentar nas duas estações analisadas. Os dados indicaram que P. squamosissimus tem hábito alimentar generalista, enquanto H. scomberoides é especializado na seleção de presas. A sobreposição de nicho alimentar entre as espécies em ambos os períodos do ciclo hidrológico foi baixa, indicando que a partição de nicho foi provavelmente o principal mecanismo de coexistência dessas espécies, com pouca relação com as variações do ciclo hidrológico.

PALAVRAS-CHAVE
Dieta; nicho trófico; rio Machado; variação sazonal

The Amazon basin covers approximately 6,000,000 km², discharging about 16% of the world’s freshwater into the Atlantic Ocean (Venticinque et al., 2016; Latrubesse et al., 2017), and have high global freshwater biodiversity (Tisseuil et al., 2013). Specifically, the fish fauna is represented by 2,257 species described (including over 1,000 endemic species; not found anywhere else in the world). Consequently, in the Amazon basin making up approximately 15% of the described global freshwater ichthyofauna (Tedesco et al., 2017).

The theories related to species coexistence, which consequently try to explain high species diversity, mostly in Amazonia, are based on two competing theories, Hutchinson’s niche theory (Hutchinson, 1957) and Hubbell’s neutral theory (Hubbell, 2001). Niche theory states that guilds of competing species will diverge, leading to reduced niche overlap. The ubiquity of ecological niches provides a general explanation for the positive relationship between diversity and functioning: through competitive divergence each species only covers some part of the total niche space available in a community (Tilman et al., 1997). The neutral theory considers that groups of trophically similar species typically can occur in sympatry and compete for similar resources, because the diversity of the assemblage results from stochastic processes acting on both local and regional scales (Gaston & Chown, 2005).

However, MacArthur (1965) described that gradients of richness could be explained by two contrary patterns of niche occupation: (i) the niche expansion model, where an increase in richness is linked to the occupation of new regions of niche space (habitat dimensions and resources), which are not available or still need to be explored by more assemblages (MacArthur, 1965; Karr & James, 1975); and (ii) the niche packing model that proposes higher diversity is associated to denser niche packing, which arises through more restricted specialization or greater overlap in resource use (Klopfer & MacArthur, 1961; Karr & James, 1975) that, in turn, may reflect differences in the ecological capacity of coexistence or regional differences in speciation rates (Hubbell, 2006).

One approach for evaluating interactive processes in aquatic assemblages (Esteves & Aranha, 1999), is the investigation of the diet of fishes (Reis & Santos, 2014), whose feeding habits can be influenced by environmental conditions, the biological traits of the species (Abelha et al., 2001) and spatial-temporal variations (Ximenes et al., 2011). According to Junk et al. (1989), the hydrological cycle plays an important role in controlling natural fluvial systems by affecting the structure of habitats and the life cycle of species. Seasonal river fluctuations unite large extensions of terrestrial environments in the fluvial system, which promotes greater availability of habitats and food (Agostinho et al., 2007), supports a high diversity of species with distinct morphological traits (Willis et al., 2005), and facilitates the coexistence of species via resource partitioning (Winemiller et al., 2000).

Piscivorous fish represent a high percentage of the total biomass of Neotropical aquatic environments (Pereira et al., 2017). Piscivorous fish play an important role in the dynamics and structuring of fish assemblages (Petry et al., 2010), coupled with the fact that flooding affects inter- and intraspecific relationships between synoptic species (Pereira et al., 2017). Species belonging to this guild are usually top predators and are able to sustain biodiversity and prevent strong trophic cascades (Monteiro & Faria, 2016). Species with similar diets, such as piscivores, but with different feeding strategies, should behave differently in relation to the hydrological cycle and resource availability (Luz-Agostinho et al., 2009).

Large piscivorous fishes show notable versatility in their feeding habits and high plasticity in feeding due to the high variation in aquatic environments of tropical regions (Lowe-McConnell, 1999; Moyle & Cech, 2004; Correa & Winemiller, 2014; Barbosa et al., 2018). In several environments and biomes (Hahn et al., 1999; Bennemann et al., 2000, 2006; Santos et al., 2016), Plagioscion squamosissimus (Heckel, 1840), the South American silver croaker is piscivorous (Barbosa et al., 2018) or a generalist carnivore (Neves et al., 2015). This species is a sedentary fish native to the Amazonian region (Santos et al., 2006), a valuable resource for human consumption and recreational fishing (Barros et al., 2012) and preferentially dwells in the water column and at the bottom of rivers and lakes (Teixeira & Bennemann, 2007). In recent studies by Barbosa et al. (2018), this species consumed preferably species of the order Siluriformes. Similarly, Hydrolycus scomberoides(Cuvier, 1819), the dogtooth characin, is distributed throughout the Amazon basin (Queiroz et al., 2013), has a piscivore dietary habit, consumes entire fish, but has insignificant commercial importance (Santos et al., 2006).

Considering their ecological importance, this study aimed to evaluate piscivorous fish feeding in a stretch of the Machado River, Amazônia, comparing flood and drought periods. The questions that this survey aims to investigate are: i) The hydrological periods change the diet and trophic niche breadth of P. squamosissimus and H. scomberoides in the river? ii) There are trophic relationships (niche overlap) between fish species. Whereas water level changes, and the allochthonous and autochthonous inputs varies in their importance for fish assemblages (Vazzoler, 1996; Junk et al., 1989, 2010), we hypothesized that the diet composition of both species of fish varies between the seasons of the hydrological cycle (flood and drought periods), in a river in southwestern Amazonia. Considering the occurrence and high abundance of both species in the Machado river, we infer that such species have specialized food habits, however, a smaller niche partitioning between P. squamosissimus and H. scomberoides occurs.

MATERIAL AND METHODS

Study area. We carried out the study in the Machado River (commonly known as Ji-Paraná River) basin, which covers 75,400 km² in the State of Rondônia, Brazil (Fig. 1).

Fig. 1.
Sampling site (black circles), Ji-Paraná Town (black triangle) and Machado River basin, Madeira River drainage, Brazil. Samples taken in June 2013 to May 2015. REBIO Jaru = Jaru Biological Reserve; Rondônia State = black square

This seventh-order river annually drains about 700 m³.s^-1 into the middle course of the Madeira River (Krusche et al., 2005). The Machado River has large individual rocks, rocky portions, as well as trunks and branches observed during the drought season with low sediment loads, typifying it as a clear-water Amazonian river (Goulding et al., 2003).

The climate of the region is characterized by temperatures that vary between 19 and 33ºC and annual precipitation of around 2,500 mm (Krusche et al., 2005). The hydrological regime is characterized by the peak of the flood in March and the minimum level in September (Companhia de Pesquisa de Recursos Minerais, 2012). The Machado River runs through the Jarú Biological Reserve (ReBio Jaru, Fig. 1), which has a total area of 47,733 km² (MMA, 2010), with a preserved riparian zone covered by ombrophylous forest that is mainly open and has low floristic variations (IBGE, 1992).

Fish sampling. Samplings were performed bimonthly from June 2013 to May 2015 in five sites (Carmita, Farofa, Suretama, São Sebastião and Poção) (Fig. 1). A total of 12 samples were taken (four samples in 2013, six in 2014 and two in 2015; flood season = six samples and drought season: six samples). Eight sets of gillnets (2 x 20 m with mesh sizes varying from 30 to 100 mm) were used. Sampling effort was standardized, and scientific fishing was carried out for 24 hours continuously at each sampling site. The gillnets reviews were carried out every three hours. Some specimens were fixed in 10% formalin and preserved in 70% ethanol. Subsequently, these specimens were deposited in the Ichthyology collection at the Universidade Federal de Rondônia (voucher: UFRO-ICT 023107) and Universidade Federal de Mato Grosso (voucher: CPUFMT 3390). License for fish collections was provided by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA # 4355-1).

Stomach content analysis. In all analyzed individuals, the standard length (L_S in cm) was measured. A total of 283 stomachs were analyzed: 134 stomachs of H. scomberoides and 149 of P. squamosissimus (Tab. I).

Tab. I
Sampling site, abundance (N) and standard length (L_{S; mean} ± standard deviation) of Hydrolycus scomberoides (Cuvier, 1819) and Plagioscium squamosissimus (Heckel, 1840) at flood and drought periods of Machado River, Brazil (June 2013 to March 2015).

Site	H. scomberoides				P. squamosissimus
	Flood		Drought		Flood		Drought
	N	L S	N	L S	N	L S	N	L S
Carmita	8	57.5 ± 7.4	10	59.6 ± 5.0	8	49.4 ± 4.9	13	47.2 ± 6.8
Farofa	7	49.7 ± 3.9	13	57.2 ± 4.2	22	46.3 ± 3.8	10	47.0 ± 2.2
Suretama	9	50.2 ± 2.9	14	58.6 ± 4.8	19	48.5 ± 5.1	8	48.1 ± 1.8
São Sebastião	26	58.7 ± 3.4	32	51.3 ± 4.9	12	49.3 ± 2.1	40	46.9 ± 1.2
Poção	5	57.9 ± 2.4	10	56.2 ± 4.0	12	48.9 ± 1.6	5	47.3 ± 3.2

Fish abdominal cavities were opened and their stomachs were removed. After, the gut contents were stored in 70% alcohol, and food items were analyzed and identified to the lowest taxonomic level (Hamada & Ferreira-Keppler, 2012; Hamada et al., 2014). The occurrence frequency (Fi%) and the method of volumetric frequency (Vi%) were used to quantify the gut contents (Hyslop, 1980). The occurrence frequency method, whereby the number of stomachs in which a particular item is found, is expressed as the percentage of the total number of examined stomachs containing food. For the volumetric frequency, the volume of each item was obtained using the percentage in relation to the total value of all gut contents. The volume was obtained using a gridded dish, and cubic millimeters were converted to milliliter (Hellawell & Abel, 1971). This value was combined in a feeding index (IAi) proposed by Kawakami & Vazzoler (1980). The index is given by the equation IAi = (Fi*Vi)/Σ Fi*Vi)*100, where i = 1 to number of food items; Fi = Frequency of occurrence of food item i; and Vi = Volume of food item i. Food items were grouped according to type (animal or plant) and origin (autochthonous or allochthonous). Fullness index (FI) was determined according to Hahn et al. (1999) and gut contents were coded as follows: 0 (empty), 1 (volume < 25%), 2 (25% < volume < 75%) and 3 (75% < volume < 100%).

Data analysis. A Permutational Multivariate Analysis of Variance (two-way PERMANOVA - Anderson et al., 2005) was performed to test the null hypothesis that diet composition of P. squamosissimus and H. scomberoides does not differ between hydrological periods. Was applied to a matrix of food items of individual fish, with volume values log transformed. The significance of multivariate dispersion generated by PERMANOVA was assessed using a Monte Carlo test with 9999 permutations, followed by a post hoc pair wise comparison between hydrological seasons.

A non-metric multidimensional scaling analysis (nMDS) was used to examine multidimensional temporal variation in diet using the total volume of each item. The dissimilarity matrix used in the ordination was built using the Bray-Curtis index.

To estimate the trophic niche breadth, we used the standardized Levins index (Ba): Ba = [(ΣjP2ij)]-1(n-1)-1, where Ba = niche breadth, Pij = proportion of item j in the diet of species i, and n = total number of items (Krebs, 1998). This index ranges from zero (when the species consumes only one type of item) to one (when the species consumes all items in equal proportions). Species feeding overlap in each period was calculated using Pianka’s symmetric index (Pianka, 1974) that varies in a scale from 0 to 1, with 1 indicating complete overlap. Overlap values were arbitrarily set at the following levels: high (> 0.6), intermediate (0.4 - 0.6) or low (<0.4) (Grossman, 1986). This index assumes prey to be equally available to all predators (Reinthal, 1990).

The differences in the niche breadth between species and periods were tested using one-way analysis of variance (ANOVAs), when normality (Shapiro-Wilks test) and homoscedasticity (Levene’s test) assumptions were met. The nonparametric Kruskal-Wallis test was used for data with non-normal distributions.

The trophic level (TL) was calculated using the formula TL = 1 + (weighed average of TL’s of each prey) (Pauly & Christensen, 1995). Trophic level and maximum length of P. squamosissimus and H. scomberoides fish prey were determined using FishBase platform (Froese & Pauly, 2019) and SeaLifeBase (http://sealifebase.org).

The niche breadth was performed using the software PAST (version 2.1.7) (Hammer et al., 2001). Statistical tests were performed using the software R (version 3.5.2) (R Development Core Team, 2018), with the package’s vegan, MASS for ANOVA, PERMANOVA, NMDS and SPAA for niche overlap. Results were considered significant when p ≤ 0.05.

RESULTS

Both species ingested a wide variety of food items, such as fishes, shrimps, terrestrial and aquatic insects at different life stages, and plants. Hydrolycus scomberoides consumed a total of 14 food items (flood season: eleven items; drought season: eight items), while P. squamosissimus consumed a total of ten items (flood season: ten items; drought season: eight items) (Tab. II). We highlight that H. scomberoides mainly ingested pelagic fish and P. squamosissimus mainly ate benthic fish.

Tab. II.
Trophic level (TL), occurrence frequency (Fi%), volumetric frequency (Vi%), and feeding index (IAi) for diet items from Hydrolycus scomberoides (Cuvier, 1819) and Plagioscium squamosissimus (Heckel, 1840) at flood and drought periods of Machado River, Brazil (June 2013 to March 2015). Allochthonous items^†; autochthonous items^‡.

Food item	TL	H. scomberoides						P. squamosissimus
		Flood			Drought			Flood			Drought
		Fi%	Vi%	IAi	Fi%	Vi%	IAi	Fi%	Vi%	IAi	Fi%	Vi%	IAi
Animal origin
Characiformes‡	3.2	0.371	0.057	0.385	0.286	0.259	0.501	0.111	0.041	0.033
Acestrohynchus falcatus ‡	4.2	0.057	0.037	0.038
Prochilodus nigricans ‡	2.4	0.029	0.815	0.424
Moenkhausia sp.‡	3.2	0.029	0.004	0.002
Siluriformes‡	3.2	0.057	0.008	0.008	0.143	0.074	0.072	0.111	0.077	0.061	0.176	0.300	0.358
Pimelodus blochii ‡	3.2	0.029	0.020	0.011	0.071	0.111	0.054	0.074	0.152	0.080	0.176	0.013	0.016
Tenellus trimaculatus ‡	2							0.111	0.077	0.061	0.118	0.140	0.111
Gymnotyformes‡	3.2							0.111	0.049	0.039	0.176	0.035	0.042
Fish no identified‡	3.2	0.200	0.029	0.107	0.071	0.037	0.018	0.185	0.483	0.639	0.176	0.345	0.412
Shrimp‡	2							0.111	0.067	0.053	0.059	0.022	0.009
Scales‡	3.2	0.086	0.009	0.013	0.071	0.037	0.018	0.111	0.046	0.037	0.059	0.002	0.001
Nematodes‡	2				0.214	0.111	0.161
Aquatic insects‡	2							0.037	0.005	0.001
Terrestrial insects†	2				0.071	0.296	0.143	0.037	0.003	0.001	0.059	0.142	0.056
Coleoptera†	2	0.057	0.008	0.008
Annelida‡	2	0.057	0.008	0.008
Plant origin
Seeds†	1	0.029	0.004	0.002
Unidentified Material
Detritus/mud‡	1				0.071	0.074	0.036

Prochilodus nigricans Spix & Agassiz, 1829 was the most important food item (high IAi) for H. scomberoides in the flood period, as well as Characiformes fishes and unidentified fish fragments (Tab. I; Fig. 2A). For the drought period, Characiformes fish, nematodes and terrestrial insects were the main items (high IAi) encountered in the diet of H. scomberoides (Tab. I; Fig. 2B). Unidentified fish fragments were the most important food item for P. squamosissimus in the flood period, as well as Pimelodus blochii Valenciennes, 1840 and Siluriformes fishes (Tab. I; Fig. 2C). In the drought period, unidentified fish fragments, Siluriformes fishes and Tenellus trimaculatus (Boulenger, 1898) were the most important items in the diet of P. squamosissimus (Tab. I; Fig. 2D).

Fig. 2.
Simplified food chain for Hydrolycus scomberoides (Cuvier, 1819) (Hs) in the flood (A) and drought (B), and for Plagioscion squamosissimus (Heckel, 1840) (Ps) in the flood (C) and drought (D) periods in Machado River (Brazil), June 2013 to May 2015. Arrow width illustrates importance in the diet Y-axis = trophic level (TL), X-axis: maximum length (cm). TL and maximum length are from fishbase.org and and Casatti (2003). Ps = Plagioscion squamosissimus (Heckel, 1840), Hs = Hydrolycus scomberoides (Cuvier, 1819), Af = Acestrohynchus falcatus (Bloch, 1794), Pn = Prochilodus nigricas Spix & Agassiz, 1829, Pb = Pimelodus blochii Valenciennes, 1840, Tt = Tenellus trimaculatus Boulenger, 1898, Ch = Characiformes, Si = Siluriformes, Gy = Gymnotiformes, Fni = Fish no identified, Sc = Scales, Ne = Nematoda, Sr = Shrimp, Ti = Terrestrial insect and De = Detritus.

The PERMANOVA indicated that the diet between H. scomberoides and P. squamosissimus for both periods analyzed was significantly different (pseudo-F = 2.54, p = 0.02) (Tab. III). “Siluriformes” (PERMANOVA, pseudo-F = 2.00; df = 3; p = 0.006) and Pimelodus blochii (PERMANOVA, pseudo-F = 1.77; df = 3; p = 0.01) were the food items consumed mainly by P. squamosissimus in the drought period.

Tab. III.
Results of Two-way PERMANOVA applied to diet of Hydrolycus scomberoides (Cuvier, 1819) and Plagioscium squamosissimus (Heckel, 1840) in flood and drought periods of Machado River, Brazil (June 2013 to March 2015). F = Flood; D = Drought.

Species	Pseudo-F = 2.75; p = 0.0002
Hydrological periods	Pseudo-F = 2.54; p = 0.02
H. scomberoides (F) x H. scomberoides (D)	p = 0.172
H. scomberoides (F) x P. squamosissimus (D)	p < 0.0001
H. scomberoides (D) x P. squamosissimus (F)	p = 0.014
P. squamosissimus (F) x H. scomberoides (F)	p = 0.001
P. squamosissimus (D) x H. scomberoides (D)	p = 0.009
P. squamosissimus (F) x P. squamosissimus (D)	p = 0.786

In the NMDS analysis, clustering was observed based on the distinct use of food resources between H. scomberoides and P. squamosissimus for both seasonal periods, with a “stress” of 0.12 (Fig. 3).

Fig. 3.
Non-metric multidimensional scaling analysis (nMDS) of IAi data of Plagioscion squamosissimus (Heckel, 1840) and Hydrolycus scomberoides (Cuvier, 1819) in the flood and drought periods in the Machado River, Rondônia State, Brazil, June 2013 to May 2015. Hydrolycus scomberoides (Cuvier, 1819)/flood (square); Hydrolycus scomberoides/drought (square opened); Plagioscion squamosissimus (Heckel, 1840)/flood (circle) and Plagioscion squamosissimus (Heckel, 1840)/drought (circle opened).

Mean values for niche breadth were lower as follows: 0.181 and 0.172 for H. scomberoides in the flood and drought periods, respectively. For P. squamosissimus the mean of niche breadth was high, 0.813 and 0.632 in the flood and drought periods, respectively. The trophic niche breadth of P. squamosissimus was greater than that of H. scomberoides in the flood period (ANOVA, F = 7.1; p < 0.05; df = 3) (Fig. 4).

Fig. 4.
Values of trophic niche breadth (mean±standard error) of Plagioscion squamosissimus (Heckel, 1840) (Ps) and Hydrolycus scomberoides (Cuvier, 1819) (Hs) in the flood (F) and drought (D) periods in the Machado River, Rondônia State, Brazil, June 2013 to May 2015.

The general niche overlap between P. squamosissimus and H. scomberoides was low (0.35). There was no niche overlap between the species in the flood period (overlap = 0), whereas in the drought period it was 0.03. Considering the periods, the average overlap between the diets was low (0.10), showing a high degree of food resource partitioning (Fig. 5).

Fig. 5.
Trophic niche overlap between Plagioscion squamosissimus (Heckel, 1840) (Ps) and Hydrolycus scomberoides (Cuvier, 1819) (Hs) in the flood (F) and drought (D) periods in the Machado River, Rondônia State, Brazil, June 2013 to May 2015.

In both periods, H. scomberoides showed similar trophic level values (mean of TL_flood = 3.55; TL_drought = 3.55; χ2 = 0.0; df = 1; p = 0.95), which was also found for P. squamosissimus (mean of TL_flood = 4.01; TL_drought = 3.82; χ2 = 0.0; df = 1; p = 0.99).

DISCUSSION

In our study, H. scomberoides and P. squamosissimus consumed different food items. For each fish species analyzed, we did not observe significant differences in the items ingested between the periods. Further, the trophic level values for both species were similar between the drought and flood periods. Our results could indicate that the high TLs and the similarity between them refer to habitat use, which is used by H. scomberoides in the pelagic region, to capture prey, and to P. squamosissimus in the benthic region. According to Bennemann & Shibatta (2002), variations in the pelagic and benthic food chains and opportunistic behavior was already identified for these species in other environments. The competitive exclusion and limiting similarity are expected to favor the co-occurrence of dissimilar species by promoting the exploitation of different resources (“niche partitioning” hypothesis; Pianka, 1974). However, microhabitat heterogeneity or resource availability can greatly influence the partitioning of resources among species (Mouquet et al., 2002). We highlight that structurally complex environments, such as the Machado River (comprising rapids, rocks, trunks, and branches from the forest margin), are stable and have resources (Pelicice et al., 2005; Willis et al., 2005), favoring the exploration of resources in a compartmentalized way.

Generalist carnivorous species has large feeding spectrum, consuming different food resources that are appropriate for its feeding behavior, digestive capacity and morphology (Neves et al., 2015). The greater consumption of pelagic fish by H. scomberoides can be explained by the ecomorphological traits of the species. In general, H. scomberoides is able to eat whole prey due their large mouth with underslung jaw (Beaumord, 1991; Cardoso et al., 2019), but have also been shown to capture their prey using their long canine teeth (Howes, 1976). Due to their large and upward-oriented mouths, these species focus prey-capture at the water surface or at the limnetic zone (Saint-Paul et al., 2000). The H. scomberoides is predator with surface-oriented vision that have remarkably similar morphology. The narrow head allows stereoscopic vision anteriorly, ventrally, and dorso-anteriorly (Howes, 1976). The enlarged pectoral fins of these fish probably are used for rapid upward acceleration, followed by prey capture either by impalement on large inferior canines in the upturned mouth, or by suction caused by expansion of the buccal cavity (Howes, 1976; Goulding, 1980).

Given their morphology, P. squamosissimus is efficient swimmer and have the capacity of expanding their mouths to ingest entire prey (Rodrigues & Menin, 2006; Teixeira & Bennemann, 2007). These characteristics allow this species to exploit the most accessible and abundant feeding items, which could change seasonally from fish to shrimp, insects, among others (Prudente et al., 2016). The P. squamosissimus is a silvery fish with a large mouth and a flattened ventrum. This species often lives in turbid waters and have elaborate sound producing and receiving systems and a well-developed lateral line (Moyle & Cech, 2004). Also, Nico & Taphorn (1984) have shown that P. squamosissimus feeds near or on the bottom during the night.

Thus, fish is the main food item for P. squamosissimus, but with reduced fish availability this species becomes opportunistic (Bennemann & Shibatta, 2002). However, the optimal foraging theory must be considered, this predicts that optimal patterns of behavior based on the costs and benefits are associated with various strategies of species survival (Broughton, 2002). According to predictions of optimal foraging theory, foragers are expected to have more specialized diets when preferred resources are abundant, and to broaden their diets during periods of food scarcity (Stephens & Krebs, 1986; Perry & Pianka, 1997). Aside from the differences between pelagic and benthic food webs, it is common to associate deforestation with increased inputs of organic matter (Thomaz et al., 2004), as well as upwelling organic matter to eutrophication (Brasil et al., 2016), which could lead to blooms of toxin-producing microalgae and force detritivory (Bezerra et al., 2018), limiting the pelagic trophic network (Paerl & Paul, 2012). Under these circumstances, resources are available to benthic organisms and other generalist species that could drive the omnivorous fishes to benthivory (Bezerra et al., 2018). Such alternative state increases energy dissipation in the upper trophic levels (D’Alelio et al., 2016), which is also linked to omnivory (González-Bergonzoni et al., 2016) and the consumption of benthos (Bezerra et al., 2018). This phenomenon can be described as “benthification” in oligotrophic waters (Mayer et al., 2014), representing a sudden change from turbidity to clarity caused by invertebrate filter feeders consuming phytoplankton, a change which benefits generalist fish (Karatayev et al., 2007). This concept could also be used in environments as the Machado River.

The relation between Amazonian ichthyofauna and the hydrological cycle has been discussed in many studies (Junk et al., 1989; Freitas et al., 2010). The period with high water is expected to be advantageous to prey species, since there is more space for dispersal and refuge (Gomes et al., 2012), and flooded forest areas with tree roots, trunks, branches, rocks and holes (Araújo-Lima & Goulding, 1998; Claro-Jr et al., 2004). Drought season favors predators because of the restricted environment in the region of the river channel and low availability of refuge areas, making it easy to find prey (Luz-Agostinho et al., 2009).

In our study, significant differences were not identified for the diet of H. scomberoides and P. squamosissimus between the drought and flood periods. The consumed items were compatible with ecomorphological of each species, as previously described. The only exception was the greater contribution, but not statistically significant, of terrestrial insects in the diet of H. scomberoides in the drought period. The increased presence of terrestrial insects in the diet of fish during a flood period has been reported in many studies (Angermeier & Karr, 1983; Winemiller, 1990; Zavala-Camin, 1996; Lowe McConnell, 1999; Yamamoto et al., 2004), which is because these insects are carried by rain water and water courses expand along marginal areas during this period. Our results were contrary to those described in the literature and the consumption of terrestrial insects by H. scomberoides could be related to the life cycle of the arthropods eaten by this species.

Additional studies have shown that seasonal variation in the overlap of species’ niches can occur within some systems (Pokharel et al., 2015). As a result, there have been renewed efforts to explore species’ trophic plasticity and the influence natural and/or human factors have on the adaptability of food web structures (Corrêa et al., 2011). Opposite to that described by Pokharel et al. (2015), the overlap of food niche between H. scomberoides and P. squamosissimus in both periods of the hydrological cycle was low, showing that niche partitioning was probably the main mechanism promoting the coexistence of these species, with little relationship with variations of the hydrological cycle. According to Pereira et al. (2017), low diet overlap between species would reflect the high heterogeneity of habitats that these species are able to reach; this fact is highlighted by the consumption of and selectivity for different prey types. The niche differentiation will lead to a reduction in the niche overlap between possible competitors, reducing competition and allowing coexistence (MacArthur, 1958; Pianka, 1974). These differences in niche might involve changes in some combination of strategies for habitat use, such as feeding time, energy allocation, defense, and diet restrictions, through feeding selectivity or niche retraction (Winemiller et al., 2015).

Thus, understanding and predicting how extreme inundation and flood events (which are increasing with climate change) influence the diet of fish assemblages are of relevant importance to the development of control programs and reducing impacts on ichthyofauna. As fishing pressure is eased through management efforts to restore overexploited stocks, making it necessary to enter information about interactions between species, especially trophic interactions between prey and predators, in models that promote the prediction and management of recovered fish stocks effectively (Jennings & Kaiser, 1998). For this, it is necessary to understand the trophic relationships between species and the factors that influence prey-predator interactions.

Acknowledgments

Alan Mendonça of the Universidade Federal de Rondônia assisted with designing figure 1 and the fieldwork, respectively. We are grateful to Dr. Willian Ohara of the Universidade Federal de Rondônia for their help with identification of the specimens.

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Publication Dates

• Publication in this collection
  04 Feb 2022
• Date of issue
  2022

History

• Received
  13 Mar 2021
• Accepted
  02 Dec 2021