Daily cycle and environmental factors influence fish assemblage structure in an Amazonian conservation unitAbstract
We investigated the influence of daily cycle cycleand local environmental factors on fish assemblages in a terra firme stream in southwestern Amazonia during the rainy season. We collected fish by using sieves and hand-nets over three days and local environmental variables were measured throughout the collection period as well. We employed Generalized Linear Models to examine the impact of daily cycle and local environmental variables on fish species richness and abundance. We used PERMANOVA to assess changes in fish assemblage composition and Redundancy Analysis to understand variations in fish species composition in response to daily cycle and local environmental factors. We collected 18 species and 271 individuals, 111 at night and 160 during the day. Dissolved oxygen (DO) had a positive influence on species richness and abundance and species composition differed between daily cycles. Redundancy Analysis revealed associations between fish species composition, environmental variables (temperature, pH and DO), and daily cycle. These findings underscore the significance of the local environment and daily cycle in predicting variations in fish assemblage structure in Amazonian streams. Understanding how stream fish assemblages are organized temporally is important for devising effective conservation strategies in a region facing increasing human pressures on aquatic ecosystems.
Keywords:
Antimary State Forest; ichthyofauna; dissolved oxygen; Terra firme stream
Resumo
Investigamos a influência do ciclo diário e dos fatores ambientais locais nas assembleias de peixes em um riacho de terra firme no sudoeste da Amazônia durante a estação chuvosa. Coletamos peixes usando peneiras e redes manuais implantadas continuamente a cada quatro horas ao longo de três dias, e as variáveis ambientais foram medidas durante o período de coleta. Utilizamos Modelos Lineares Generalizados para examinar o impacto dos ciclos diários e das variáveis ambientais locais na riqueza e abundância de espécies de peixes. Utilizamos PERMANOVA para avaliar as mudanças na composição das assembleias de peixes e Análise de Redundância para compreender as variações na composição de espécies de peixes em resposta aos ciclos diários e aos fatores ambientais locais. Coletamos 18 espécies e 271 indivíduos, 111 à noite e 160 durante o dia. O oxigênio dissolvido (DO) teve uma influência positiva na riqueza e abundância de espécies, e a composição de espécies diferiu entre os ciclos diários. A Análise de Redundância revelou associações entre a composição de espécies de peixes, variáveis ambientais (temperatura, pH e DO) e ciclos diários. Essas descobertas destacam a importância do ambiente local e do ciclo diário na previsão de variações na estrutura das assembleias de peixes em riachos amazônicos. Compreender como as assembleias de peixes de riachos são organizadas temporalmente é importante para desenvolver estratégias eficazes de conservação em uma região que enfrenta crescentes pressões humanas sobre os ecossistemas aquáticos.
Palavras-chave:
Floresta Estadual do Antimary; ictiofauna; oxigênio dissolvido; riacho de terra firme
1. Introduction
The Amazon basin is the largest watershed in the world, covering an area of approximately seven million square kilometers, with more than five million square kilometers located within Brazil (Val, 2019). This vast basin contains the world's most extensive tropical forest ecosystems, comprising 40% of the total area of tropical forests worldwide (Laurance et al., 2001; Aragão et al., 2014; Weng et al., 2018). It includes a vast array of aquatic environments, such as rivers and lakes, as well as numerous small streams known locally as 'igarapés' (Bührnheim, 2002; Beltrão et al., 2019).
An increasing number of studies have reported on the ecology and diversity of these small water bodies (see Montag et al., 2019). These investigations have revealed that these streams exhibit exceptionally high fish species beta-diversity (Santos et al., 2019; Albert et al., 2020). Previous studies have indicated that approximately half of all fish species in the Amazon inhabit streams of small orders, where there are significant levels of endemism (Junk and Piedade, 2004; Frederico et al., 2018; Dagosta and Pinna, 2019; Albert et al., 2020). This endemism is particularly pronounced among small and medium-sized species, especially Characiformes and Siluriformes (Dagosta and Pinna, 2019; Albert et al., 2020).
Factors such as luminosity can influence both the diversity of fish species inhabiting a stream and their behavior. In the middle and upper reaches of a stream, for instance, the channel is typically fully or nearly entirely covered by the canopy of the riparian forest. This situation may lead to the fish community relying more heavily on allochthonous resources, as the stream itself might be relatively unproductive due to reduced sunlight penetration, which is necessary to support plant growth (Corrêa et al., 2012).
Another factor contributing to the diversity and structure of stream fish communities is the daily variation in environmental conditions and activity patterns, which leads to distinct occurrences of various organisms (Volpato and Trajano, 2005; Carvalho et al., 2009). This daily variation strongly influences fish activity patterns and is directly linked to internal and external factors. Some species, such as those belonging to the Characiformes and Cichliformes orders, tend to be more active during daylight hours, while some members of the Gymnotiformes Siluriformes orders, exhibit higher activity levels at night (Kavaliers, 1980; Helfman, 1986). Diurnal characiforms and cichliforms are visually oriented fish that require daylight to detect and capture their prey. In contrast, nocturnal gymnotiforms and siluriforms do not rely on visual cues; instead, they use electrical and chemical signals, respectively, to detect their prey.(Brejão et al., 2013).
Streams present a diverse availability of habitats than can significantly impact fish diversity, particularly considering the extensive environmental heterogeneity in the Amazon region (Bührnheim, 2002; Winemiller et al., 2008; Corrêa et al., 2012). Notably, local environmental variables have been demonstrated a strong influence on the richness and abundance of Amazonian stream fish (Montag et al., 2019; Benone et al., 2020; Vieira and Tejerina-Garro, 2020) Where fluctuations in temperature can significantly influence concentrations of dissolved oxygen (Dowling and Wiley, 1986; Bulbul Ali and Mishra, 2022). Conversely, acidity levels can influence biomass, with an observed increase in biomass occurring in waters with a pH above 6.3 (Warren et al., 2010).
In recent years, there has been a growing body of research focusing on the impact of habitat complexity and heterogeneity on fish community structure in the Amazon region. These studies have consistently shown that streams are crucial in sustaining aquatic communities (Montag et al., 2019; Benone et al., 2020). However, in some areas of the Amazon, such as the western basin, limited research has specifically addressed this question, as most studies in the Brazilian state of Acre have primarily involved species inventories (see Claro-García et al., 2013; Virgílio et al., 2019; Silva et al., 2020). Ramalho et al. (2014) also examined variations in water quality and fish species diversity and composition in the open Campinarana ecosystems of northwestern Acre.
Daily cycle is directly linked to the activity period of fish species and is supported by morphological and physiological adaptations that ensure their ability to function during their preferred photoperiods (Arrington and Winemiller, 2003). Nevertheless, a systematic assessment of the influence of local environmental variables and photoperiod on fish assemblages in southwestern Amazonia streams is currently lacking. This is an important gap in determining how the environment shapes the composition, richness, and abundance of fish assemblages in this region.
Therefore, we investigated the impact of photoperiod and local environmental factors on fish species richness, abundance, and composition in a southwestern Amazonian stream. We hypothesized that both daily cycle and the local environment play significant roles as limiting factors in shaping local fish assemblage structure (Vieira and Tejerina-Garro, 2020).
2. Materials and Methods
2.1. Study area
The Floresta Estadual Antimary (FEA) is situated in the southwestern Amazon basin, between Rio Branco and Sena Madureira cities, in the Brazilian state of Acre (Figure 1). The regional annual precipitation is approximately 2000 mm and its average annual temperature is 25 °C. It has distinct dry (June through September) and rainy (October through May) seasons (D’Oliveira et al., 2013).
The FEA encompasses three distinct forest types: dense tropical forest, open tropical forest, and bamboo forest. The FEA's maximum elevation is 300 meters, and the soils are primarily yellow dystrophic (FUNTAC, 1989). The bamboo forest consists of relatively open vegetation, allowing for increased sunlight penetration, which contributes to the prevalence of bamboo in the area. The investigated site was a freshwater stream within the FEA, situated amidst a dense bamboo forest and surrounded by riparian vegetation, featuring clear waters, predominantly clayey substrate with little sand. The mean height of the bank was 1.5 meters, with a depth of 22 cm, reaching up to 1.2 meters in some areas, and a mean channel width of 1 meter. This stream is a tributary of the Antimary River, within the territorial limits of Sena Madureira, Acre.
2.2. Sampling of the fish fauna and the environmental variables
We collected fish in a 250 m long stream stretch, during the rainy season in April. Fish were captured by using both a seine (80 cm × 50 cm) and a hand-net (50 cm × 30 cm) for each 30-min sampling session (Corrêa et al., 2015). We collected fish over three-day, totaling nine hours of sampling at intervals of four hours. These intervals were divided into day (09:00, 13:00, and 17:00) and night shifts (21:00, 01:00, and 05:00). Captured fish were anesthetized in a lidocaine solution, fixed with 10% formalin, and placed in plastic bags for 24 hours before being transferred to 70% alcohol. Species identification was carried out using taxonomic keys and, when necessary, with the assistance of specialists (Queiroz et al., 2013; Claro-García et al., 2013). All individuals were taken to the laboratory for taxonomic measurement because the morphological diversity within Amazonian species is very large, requiring careful investigation to differentiate species accurately. Voucher specimens were deposited in the ichthyological collection of the Laboratory of Ichthyology and Aquatic Ecology at the Federal University of Acre (UFAC). The specimens were collected under a license from the Biodiversity Information and Authorization System – SISBio / Chico Mendes Institute for Biodiversity Conservation – ICMBio, number 11185/3. We also measured temperature (°C), dissolved oxygen concentration (mg/l), and hydrogenic potential (pH) (Table 1).
2.3. Data analysis
We used generalized linear models (GLMs) with richness and abundance as response variables and daily variation (day and night) and local environmental variables as predictor variables. We checked the following assumptions to use the most appropriate GLM: normality, outliers, and overdispersion through the ‘simulateResiduals’ function of the ‘DHARMa’ package (Hartig, 2022). In the species richness GLM, none of the assumptions were violated with the Gaussian distribution, therefore, we used this model. In abundance GLM, we used a negative binomial distribution and the ‘MASS’ package (Venables and Ripley, 2002) because of data overdispersion. The partial determination coefficients of each GLM predictor were calculated by using the 'rsq.partial' function of the 'rsq' package (Zhang, 2022).
We tested for significant changes in fish assemblage composition between sampling bout sand local environmental variables with a permutational multivariate analysis of variance (PERMANOVA: (Anderson, 2001), using the adonis2 function. We used 9999 permutations for this analysis. Before performing PERMANOVA, the multivariate homogeneity of group dispersions was tested using the ‘betadisper’ function, which indicated that there was no difference in dispersion between groups (F = 2.06; p = 0.18) as measured by Euclidean distance.
We used redundancy analysis (RDA, Legendre and Anderson, 1999) to assess variations in fish species composition to the photoperiod) and local environmental variables. We determined the global significance of the RDA and that of each axis using permutation tests (9999 permutations). We evaluated the contribution of each species, site, and photoperiod to the RDA using the envfit procedure (Oksanen et al., 2022). The fish composition matrix (RDA and PERMANOVA response matrix) was standardized using Hellinger distance to reduce the effects of very abundant species (Peres-Neto and Legendre, 2010) and local environmental variables were log10 transformed (except pH). All these analyses were carried out using the vegan package in R software (R Core Team, 2022).
3. Results
We collected 18 species and 271 individuals, representing 11 families and four orders (Table 2). Characiformes were the most abundant order, with 182 individuals, followed by Cichliformes (62 individuals) and Siluriformes (22 individuals). The Characidae family was the most abundant, with 162 individuals, followed by Cichlidae (62 individuals) and Lebiasinidae (13 individuals). Characiformes were also the most speciose order, with 12 species, followed by Siluriformes with six species, and Cichliformes and Gymnotiformes, each with two species. The most abundant species was Astyanax bimaculatus, (79 individuals), followed by Chrysobrycon hesperus (63 individuals), Apistogramma acrensis (60 individuals), and Pyrrhulina australis (13 individuals).
Species collected from the study stream The species were classified fol-lowing (Fricke et al., 2023).
Most fish were collected (n = 160) during the day, peaking at 13:00 (n = 75) (Figure 2A). Fewer individuals (n = 111) were collected at night, peaking at 01:00 (n = 44). Most species collected in a single period was at 01:00 (12 species; Figure 2B).
A) Fish abundance collected in the FEA at various times. B) Fish species richness collected in the FEA at various times. The solid line represents the median, the dashed line represents the mean, and the boxes are quartiles.
Dissolved oxygen had a significantly positive influence on species richness (R2 = 0.25; p = 0.04; Figure 3A) and abundance (R2 = 0.42; p < 0.01; Figure 3B; Table S1 – Supplementary Material). The other predictor variables did not significantly influence richness or abundance.
PERMANOVA indicated significant changes in species composition between diurnal bouts (F = 3.08; R2 = 0.15; p = 0.02), but local environmental variables had no significant influence (Table S2 – Supplementary Material). However, Redundancy Analysis (RDA) reflected the influence of both environmental variables and photoperiod on fish species composition (F 4, 13 = 1.365; p = 0.04). The first and second RDA axes explained 24.90% of the total variation in fish species composition. RDA-1, explaining 14.1% of the variation, was primarily influenced by the nocturnal period and water temperature. RDA-2, explaining 10.8% of the variation, was influenced by pH and dissolved oxygen. Apistogramma acrensis tended to be more abundant in warmer environments and during the day, while Chrysobrycon hesperus tended to be more abundant in higher oxygen concentrations. pH had a negative influence on Gymnotus coropinae, and Helogenes marmoratos tended to occur more frequently at night (Figure 4).
Variation in fish species composition relative to temperature, pH, dis-solved oxygen concentration, and photoperiod (day or night) ordered by Redun-dancy Analysis (RDA).
4. Discussion
We determined that the dissolved oxygen and daily cycle play important roles in predicting short-term temporal variations in fish assemblage structure in southwestern Amazonian streams. Oxygen had a significant influence on both fish species richness and abundance. Additionally, species composition was significantly influenced by daily cycle.
We found fewer fish species compared with previous Amazonian stream studies (Claro-García et al., 2013; Dutra et al., 2020). This reduced richness can be attributed to the relatively small sample size rather than any major influence of the daily or environmental variables (Pompeu et al., 2021). Despite the small sample size, the data were consistent with previous studies of small streams (e.g., Dias et al., 2016; Dutra et al., 2020), which also showed a prevalence of small characids and dominance by characiform and siluriform. Fish species in small streams typically have limited dispersal capabilities, generally remaining mobile within the micro basin but not dispersing over long distances (Palheta et al., 2021).
Local environmental variables are known to influence the structure of fish assemblages and specific attributes, such as richness and abundance. These variables work in conjunction with other hydrological parameters, forming an environmental filter (Poff, 1997; Costa et al., 2018; Vieira and Tejerina-Garro, 2020). We found that higher dissolved oxygen concentrations were associated with greater richness and abundance of fish species. Oxygen levels influence feeding and reproduction because values below or above species optima lead to physiological and behavioral changes, prompting species to adjust their feeding and reproductive tactics (Castro et al., 2020; Mendes et al., 2021). Streams with intact forest cover tend to maintain stable dissolved oxygen concentrations, whereas those subjected to deforestation often exhibit fluctuating and lower oxygen concentrations (Reis Oliveira et al., 2019). Although some Amazonian fish species can survive in hypoxic or anoxic environments through behavioral and morphological adaptations (Braz-Mota and Almeida-Val, 2021), others are more sensitive to dissolved oxygen levels, which can be a limiting factor affecting fish survival.
Surprisingly, PERMANOVA revealed that daily cycle, rather than local environmental variables, was responsible for changes in fish species composition. The circadian variation in fish species composition is linked to the activity patterns and visual acuity of these organisms (Ortega et al., 2020). Daytime conditions favor species that have visual strategies that facilitate prey detection, as well predator avoidance (Utne-Palm, 2001; Caves et al., 2017). In contrast, nighttime conditions are conducive to species with well-developed tactile sensory structures, such as barbels, which are used for prey detection (Gatz, 1981; Arrington and Winemiller, 2003). The variation in these attributes plays a pivotal role in shaping the structure and function of fish assemblages within freshwater ecosystems. Fish were more abundant during the day, with a peak between 13:00 and 17:00 (Figure 4), coinciding with the highest water temperatures. This observation suggests that warmer waters are associated with a greater abundance of fish, which is in line with previous studies (Rosset et al., 2010; Bailly et al., 2014).
During the daytime, there were more species that are more active in well-lit environments, like Astyanax bimaculatus. In contrast, at night, we saw more species adapted to poorly illuminated environments, such as Ituglanis amazonicus and Helogenes marmoratus. The latter species exhibits coloration resembling decomposing leaves and the streambed substrate (Sazima et al., 2006). This coloration enables them to camouflage during the day and become active foragers during the night, which aligns with their peak activity period (Sazima et al., 2006; Soares et al., 2023).
According to the RDA, we observed associations between certain species and specific local environmental variables and daily cycle. For instance, the dwarf cichlid Apistogramma acrensis was more abundant in warmer waters. This observation aligns with its apparent tolerance for warmer environments, a trait also observed in other cichlids like Cichlasoma paranaense (Brandão et al., 2018 and Geophagus brasiliensis (Rantin and Petersen, 1985). Maintaining optimal temperatures is important to ensure a species' metabolic balance and the proper functioning of its physiological processes (Pörtner, 2010).
Chrysobrycon hesperus tended to be more abundant in areas with higher oxygen levels despite characids' known tolerance for significant variations in oxygen levels. Characids are generally capable of surviving in water with low oxygen concentrations, for example, Soares et al., (2006), experimentally described an increase in behaviors such as superficial respiration, aerial respiration and capture of oxygen under the aquatic macrophyte roots in some characid’s species subjected to different levels of hypoxia. In addition, some species may develop morphological adaptations such as dermal lip protuberances to improve their performance during superficial respiration (Scarabotti et al., 2009)
Certain groups of species, such as electric fish, are inclined to inhabit more acidic waters. These fish can be found in a wide range of substrate types, with species like Gymnorhamphicfhys rondoni foraging in sandy areas (Virgilio et al., 2019), while others in the same group, like Gymnotus, tend to forage in locations with more extreme conditions, characterized by low oxygen concentrations and pH levels (de Resende et al., 2006). Gymnotiforms possess the ability to emit electrical impulses, aiding in navigation, foraging, and feeding. Being primarily nocturnal carnivorous-piscivorous species, these strategies enhance their ecological success (Sazima et al., 2006; Carvalho et al., 2009; Zuanon et al., 2015).
We found significant influences of local environmental conditions and daily cycle on fish assemblage structure in a dryland stream in western Amazonia. This highlights the capacity of different fish species to respond differently to short-term changes in stream environmental conditions, which facilitates the co-existence of multiple non-competing species in small spaces. Understanding how fish assemblages organize in stream sites is important for developing effective conservation strategies for aquatic ecosystems in a region facing increasing human pressures.
Supplementary Material
Supplementary material accompanies this paper.
Table S1.
Table S2.
This material is available as part of the online article from https://doi.org/10.1590/1519-6984.279923
Acknowledgements
We extend our gratitude to CAPES for providing master's and doctoral scholarships and to the management of the Floresta Estadual do Antimary. We also thank the Class of 2016 of the UFAC Masters Programa de Pós-Graduação em Ecologia e Manejo de Recursos Naturais (MECO/UFAC). FC is grateful to the Maranhão State University (Grant No. 18/2023 - PPG/UEMA) for a visiting researcher stipend. LFAM received a CNPq Research Productivity Scholarship (code 302881/2022-0).
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Publication Dates
-
Publication in this collection
14 Feb 2025 -
Date of issue
2024
History
-
Received
26 Oct 2023 -
Accepted
21 Mar 2024
