Road crossings disrupt feeding, reproduction, and body condition of a forest stream fish in the Amazon

M. Bárbara Mascarenhas¹ , Sidinéia Amadio², Camila S. dos Anjos³, Cristhiana P. Röpke², Jansen Zuanon^2,4 and Cláudia P. de Deus²

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Associate Editor: Caroline Arantes

Section Editor: José Birindelli

Editor-in-chief: Carla Pavanelli

Abstract​

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Introduction​

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In recent decades, human population growth has driven the demand for services and space, intensifying the exploitation of natural resources, primarily through land use and occupation (Roy et al., 2022). These activities result in environmental disturbances that promote habitat homogenization and fragmentation, thereby reducing biological diversity (Prakash, Verma, et al., 2022). Bevan et al. (2024) emphasize that practices such as the conversion of natural areas into agricultural lands, urban expansion, and the construction of large infrastructure projects have degraded various tropical ecosystems, which host high environmental heterogeneity and biodiversity. Freshwaters are among the most vulnerable ecosystems to anthropogenic impacts, with primary effects including alterations to their physical structure, deterioration of water quality, and reduced hydrological connectivity (Allan, 2004; Castello, Macedo, 2016). These alterations significantly affect the composition and biotic dynamics of these environments and the viability of natural populations of many migratory fish species (Reis et al., 2016; Duponchelle et al., 2021). Organisms sensitive to landscape-induced impacts are directly affected by disruptions to essential biological processes such as reproduction and feeding, which can lead to population decline and, in extreme cases, local extinction (Beltrão et al., 2018; Dutra et al., 2022).

Although essential for economic and social development, infrastructure projects often cause severe (and sometimes irreversible) impacts on ecological cycles and ecosystem services. For instance, the expansion of the road network, the construction of highways and secondary roads provides access routes and connectivity that facilitate human population development, but also generates significant environmental impacts (Forman, Alexander, 1998; Daigle, 2010). Habitat fragmentation harms ecological connectivity and increases the risk of local extinctions by restricting gene flow between populations. Furthermore, edge effects result in changes to temperature, humidity, and light conditions within habitat fragments, affecting sensitive species and facilitating the invasion of non-native species (Laurance et al., 2009). Increased pollution is also a common consequence of the impacts caused by linear infrastructure projects (for a synthesis on the deleterious effects of road construction on forest ecosystems, see Laurance et al., 2009). Paving roads in forest areas enables or intensifies the process of deforestation (Fearnside, 2005, 2006), which severely impacts water bodies due to the deterioration or removal of riparian vegetation. This often results in the direct blockage of stream channels, drastically altering water flow, promoting sediment accumulation, and increasing water temperature (Macedo et al., 2013; Touma et al., 2020). Smith et al. (2018) discuss the effects of stream-road crossing inducing damming in Brazil and highlight the inefficiency of mechanisms such as culverts and drainpipes as water passage structures, which impair (and often prevent) the longitudinal movement of ichthyofauna.

Structural degradation and hydrodynamic alterations in streams affect the dynamics and composition of the ichthyofauna (Diebel et al., 2015; Brejão et al., 2020), with repercussions on the biological aspects of remnant fish populations (Barros et al., 2024). Ilha et al. (2018) observed a reduction in body size associated with increased temperature in fish populations inhabiting deforested Amazonian streams. Thermal stress in deforested streams drives physiological changes as an adaptive mechanism to cope with the impact (Campos et al., 2024). Since food availability and temperature influence the metabolism and energy management of organisms (Wootton, 1990), changes in riparian cover and temperature can impact the diet, body condition, size, and fecundity of individuals. Additionally, biotic interactions, such as parasitism, can be modified due to changes in the body condition of organisms and environmental disturbances (Moreira et al., 2010; Guidelli et al., 2011). The reduction in fish body condition caused by alterations in the availability or nutritional quality of food increases their susceptibility to parasitic infections (Moreira et al., 2010). At high densities, parasites can cause pathologies that compromise essential biological functions (Quist et al., 2007). These infections elicit responses in hosts, directly affecting their physiological resistance and facilitating new infections in a two-way interaction. Therefore, studies aiming to understand the relationship between body condition and parasitic intensity in fish are particularly important in landscapes altered by anthropogenic disturbances (Tavares-Dias et al., 1999; Takemoto et al., 2009; Moreira et al., 2010; Guidelli et al., 2011; Santos, 2013).

Some species, however, demonstrate greater adaptive capacity in the face of environmental impacts, whether natural or anthropogenic (Wootton, 1990). Species with high phenotypic or trophic plasticity exhibit greater adaptability to new conditions (Abelha et al., 2001; Chevin et al., 2010). Their survival depends on the efficient exploitation of available resources (Suzuki, 1999), utilizing them for somatic growth and reproduction (Vazzoler, 1996). Biotic and abiotic pressures also influence reproductive strategies, such as a reduction in size at first maturation and increase in fecundity once age specific may reduce, compromising population sustainability (Vazzoler, 1996).

Amazonian terra-firme streams exhibit high structural complexity, with trophic chains strongly dependent on allochthonous material from riparian vegetation, highlighting their intrinsic relationship with the forest (Knöppel, 1970; Bührnheim, Cox Fernandes, 2001; Mendonça et al., 2005). In this study, we evaluate how the degradation of these streams, caused by the construction of a highway, negatively impacts several aspects of the biology of a nektonic small fish with a generalist diet, Bryconops giacopinii Fernández-Yépez, 1950 (Iguanodectidae, Characiformes). Bryconops giacopinii is considered an ecological indicator due to its abundance, trophic flexibility, and sensitivity to habitat disturbances. Populations were sampled in both well-preserved terra-firme streams and degraded streams affected by road crossings, where culverts, pipes, and bridges were constructed, altering the flow regime and local habitat structure. We expect that the overflow of the channel, resulting from the partial blockage of flow, and the changes in the stream-riparian forest interface will negatively affect the diet, reproductive biology, and body condition of the species. Based on this, we expect that fish in streams altered by road construction will exhibit the following changes compared to fish from pristine environments: 1. Substitution of allochthonous food items with autochthonous items in the diet; 2. Reduction in the condition factor of individuals; 3. Increase in parasitic infestation rate; 4. Reduction in first maturity size and oocyte diameter, and increased fecundity.

Material and methods

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Study area. The collections were conducted in terra-firme streams of the Central Amazon that drain into the Tarumã-Açu basin, located north of Manaus, Amazonas, Brazil (Fig. 1). Eight independent streams were selected, four of which are headwaters located in the Adolpho Ducke Forest Reserve (RFAD) (02°55’–03°01’S; 59°53’–59°59’W). This region is characterized as a humid tropical forest, with an average temperature of 26°C and little annual variation, with a dry season from July to October and a rainy season from November to June (Araújo, 1967). The western part of the reserve contains three microbasins: Acará, Bolívia, and Barro Branco, which drain into the Tarumã-Açu River, a tributary of the left bank of the Negro River. These streams are of 1st, 2nd, and 3rd order and have dark water, with a predominantly sandy bed but with submerged dead leaves. The waters are acidic (pH between 3.5 and 5.0), and the average dissolved oxygen content is 5.9 mg/l (Mendonça et al., 2005). The other four streams are located in the stretch between the city of Manaus and Presidente Figueiredo, AM (03°02’30”S 60°30’00”W) and were intercepted by the Brazilian federal highway BR-174. Between 1970 and 1997, culverts, pipes, and bridges were installed at certain points to allow water flow. However, these installations altered the water flow, leading to damming and overflow of the channel, followed by a decrease in discharge and water velocity upstream. These areas are deforested, without canopy cover, with higher water temperatures, creating environments with semi-lentic characteristics. The characterization of the areas was carried out by recording limnological information, including pH, dissolved oxygen, conductivity, water temperature, and water velocity, measured with a multiparameter probe and a flow meter, respectively. Additional information on substrate type and canopy openness was also recorded.

FIGURE 1| Location of the sampled streams situated north of Manaus (Amazonas, Brazil). Pristine streams are located within the Reserva Florestal Adolfo Ducke (RFAD), and the impacted streams are those intersected by the federal highway BR-174. All streams drain into the Negro River basin.

Model species. The species Bryconops giacopinii is a small-sized fish belonging to the family Iguanodectidae with an average standard length of 10 cm. Commonly known as “piaba” or “lambari”, it has diurnal habits and is considered trophically generalist (Barros et al., 2017), without seasonal reproductive activity (Mendonça-Cardoso, 2012; Espírito-Santo et al., 2013).

Sampling. The collections took place during the rainy season, between February and April of 2018, with 15 individuals captured in each stream (N total = 120). The fishing gear used included cast nets, seine nets (5 mm mesh between knots), and gill nets (30 mm and 40 mm between opposite knots), all applied along a 100-meter stretch, delimited with block nets to prevent the escape of individuals and optimizing the sampling effort. In the field, the captured individuals were euthanized by submersion in solution of the anesthetic Eugenol, or clove oil (AVMA, 2013), then fixed with 10% formalin for approximately 24 hours, and subsequently preserved in 70% alcohol. Part of the collected specimens was deposited as voucher material in the Fish Collection of the Instituto Nacional de Pesquisas da Amazônia (INPA), vouchers: INPA-ICT 61193 and 61194.

Biometry and estimation of biological parameters. For all specimens, total (TL-cm) and standard length (SL-cm) were obtained using a digital caliper, while total (TW-g) and eviscerated weight (EW-g) were measured with a scale with 0.5 g precision. Gonads were macroscopically analyzed for gender and reproductive phases according to the categories defined by Brown-Peterson et al. (2011). Females were classified into six categories: immature, maturing, mature, spawning, spawned, and recovering, based on the percentage of the abdominal cavity occupied by the ovaries and the presence, size and looseness of the oocytes. Mature gonads were fixed with formaldehyde solution at the time of fish collection, and oocyte dissociation was performed by handling the oocytes in a Sodium Hypochlorite (2.5% concentration) solution, followed by conservation in ethanol solution (70%) thereafter (Mendonça-Cardoso, 2012).

The condition factor was estimated by the body condition (Kn) (Le Cren, 1951) through the equation Kn = EW/a*SL^b, where Kn = Condition Coefficient, SL = standard length, a and b = constants of the EW-SL relationship, and EW = eviscerated weight (Le Cren, 1951). The eviscerated weight (EW) was used to eliminate potential bias related to the degree of stomach fullness and the weight of the gonads. Dissociated oocytes were counted and all measured (diameter in mm in the longest dimension). under a stereomicroscope with a micrometric scale in the ocular. For the estimation of batch fecundity, we counted the oocytes in the cohort, which includes those at stages ranging from incomplete to complete vitellogenesis (Murua, Saborido-Rey, 2003; Brown-Peterson et al., 2011; Lowerre-Barbieri et al., 2011). These oocytes were assumed to comprise the batch that would be released during the next reproductive bout (Brown-Peterson et al., 2011). Non-vitellogenic oocytes were considered to contribute to future spawning and were not considered in fecundity estimates. A graphical representation of frequency of occurrence by size class was used to distinguish the minimal diameter of oocytes included to estimate batch fecundity (i.e., vitellogenic oocytes). Based on the graphical representation, the mean oocyte size in the ovary was also estimated, by the arithmetic mean size of fully mature (vitellogenic) oocytes.

Stomach content analysis. The diet analysis of the fish was based on the identification of food item types present in the stomach contents, observed under a stereomicroscope. Items were classified taxonomically at order level whenever possible, using identification keys (Hamada, Ferreira-Klepper, 2012; Hamada et al., 2014). The Relative Volume (RV) was visually estimated by observing the relative abundance of each item, with the total volume in each stomach considered as 100% (Dary et al., 2017).

Presence and abundance of parasites. All specimens were subjected to a visual inspection for parasites, considering the body surface and coelomic cavity (including the swim bladder, gonads, and intestinal tract). The digestive tract and swim bladder were removed and examined under a stereomicroscope. All parasites were identified to the level of major groups (Moravec, 1998). Abundance was estimated by counting the total number of parasites found. The prevalence index of parasites was used for characterization and was estimated using the formula: P = (HI / HE) * 100, where P = prevalence; HI = number of infected hosts; HE = number of examined hosts (Bush et al., 1997).

Data analysis. Based on individual data (120 individuals of B. giacopinii) and the relative volume of each item, differences in diet between sites (RFAD and BR-174) were tested by applying a multivariate permutation analysis of variance (PERMANOVA) based on Bray-Curtis distance. The results were visually presented by plotting a Principal Coordinate Analysis (PCoA) based on Bray-Curtis distance with polygon delimitation of multidimensional food resource use at each site. For this analysis, items belonging to some taxonomic orders were pooled and seven groups of food items were considered (Tab. S1). To test the importance of resource sources according to origin (allochthonous and autochthonous), canopy invertebrates and seeds were classified as allochthonous, while aquatic insect larvae, microcrustaceans, and filamentous algae were classified as autochthonous. The detritus item was excluded from this classification once its origin can be mixed and only determined by isotopic analysis. The relative volume of each item was summed by category of source origin (allochthonous and autochthonous) at each sampling site and area (RFAD and BR-174). The effects of habitat integrity on the importance of source origin was tested using a Two-way ANOVA, with Gaussian distribution on the sum of relative volume regarding source origin classification, area and the interaction between these variables (source origin x area).

The effect of habitat integrity on standard length was tested by t-tests, comparing mean values between areas (BR-174 and RFAD). The effects of habitats integrity on relative body condition (Kn) was tested by a Generalized Linear Model (GLM) with Gamma error distribution and log-linkage comparing values between areas (BR-174 and RFAD).

Difference in the total abundance of parasites in relation to habitat integrity was tested by t-tests. Abundance of parasites was also tested in relation to Kn using a simple linear regression with natural logarithmic transformation for the abundance of parasites, but only with data from BR-174 once abundance of parasites was near zero in the RFAD.

Length at maturity (L₅₀ and L₁₀₀) was estimated based on the frequency of juveniles (with immature gonads) and adults (with gonads classified as maturing, mature, spawning, spent/regressing, and regenerating) by fitting a generalized linear model (GLM) with logistic regression, using Binomial error distribution and the LOGIT link function. The L₅₀ sizes were considered as those corresponding to a 50% probability, and L₁₀₀ as those corresponding to a 100% probability of a mature population. Differences in L₅₀ and L₁₀₀ between areas (BR-174 and RFAD) were tested by one-sample t-tests.

Difference in the mean oocyte size between areas was tested by Wilcoxon non- parametric test. Batch fecundity (30 individuals) was tested by a GLM model with Gaussian error distribution as a function of standard length, Kn, abundance of parasites, mean oocytes diameter, area (BR-174 and RFAD), the interaction of oocyte diameter and area and the interaction of standard length and area. All analyses were performed in R software and checked for assumptions and model validation.

Results​

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Environmental characteristics. The pristine streams (RFAD) exhibited a relatively low average temperature (24.26°C ± 0.17), acidic water (pH 3.8 ± 0.49), water velocity around 0.43 m/s, and a higher dissolved oxygen rate (32.4%). On the other hand, the altered streams (BR-174) showed an average temperature of 28.15°C ± 1.71, pH 5.05 ± 0.53, water velocity (measured downstream of the road) of 0.48 m/s, and a lower dissolved oxygen rate (23.37%). Furthermore, the streams sampled along BR-174 had a bed predominantly composed of sand and clay, while the streams in RFAD had a bed mainly composed of sand and coarse litter of leaves, branches, and decomposing organic material.

Diet. Diet composition of B. giacopinii was significantly different between areas (PERMANOVA – F = 32.509; R² = 0.18; p-value = 0.001). Fish in the RFAD area predominantly consumed allochthonous invertebrates, with a predominance of terrestrial insects from the orders Hymenoptera, Hemiptera, and Isoptera(Fig. S2). Canopy seeds were also relevant in the diet composition, being the second most consumed category by B. giacopinii in the RFAD. For fish from BR-174, although allochthonous items had a significant presence, filamentous algae and autochthonous invertebrates were found in higher quantities compared to the intact streams RFAD. Diet differences detected in the PCoA suggest that a higher diversity of items was consumed by B. giacopinii in the altered environment BR-174, as well as higher inter-individual differences in diet (Fig. 2).

FIGURE 2| Principal Coordinates Analysis (PCoA) showing the distribution of food resources for Bryconops giacopinii specimens collected from streams in a pristine area (RFAD) and from road-crossed streams along the BR-174 highway.

The relative importance of resource source categories consumed by the fish from RFAD and BR-174 highlights the significant difference in the origin of items in the diet of individuals between the two environments. Although the consumption of allochthonous resources and was relatively higher than that of autochthonous resources in both areas, the proportion of allochthonous items was significantly higher in RFAD (Two-Way ANOVA F_{(Area x Resource)} = 32.32; p-value 0.001; Fig. 3; Tab. 1).

FIGURE 3| Relative Volume (RV) of food items consumed by Bryconops giacopinii (N = 120) according to its origin (autochthonous and allochthonous) in altered (BR-174) and pristine (RFAD) environments.

TABLE 1 | Results of a Two-Way ANOVA for differences in the diet of Bryconops giacopinii considering the food resource sources (allochthonous and autochthonous) and areas (BR-174 and RFAD).

Variable	SS	Gl	F	p-value
Area	205.234.00	1	7.44	0.015
Resource source	2.936.845.00	1	106.41	<0.001
Area × Resource source	892.109.00	1	32.32	<0.001
Residual	441.593.00	16

Fish size, condition factor (Kn), and parasites. There was no difference in standard length (t = -1.830, p-value = 0.057, N = 120; Tab. S3) between the specimens from the two areas. In the comparison of the body condition (condition factor – Kn) there was a significant difference between areas (GLM coefficients = 0.19 ± 0.057, t= 3.293, p-value = 0.0013, N = 120), with lower values in streams impacted by road crossings (Tab. 2; Fig. 4).

TABLE 2 | Results from GLM model with Gaussian distribution of the relationship of absolute batch fecundity and predictors. Significant p-values are presented in bold. For the site comparison the free-flowing pristine streams (RFAD) were taken as the level for comparison.

	Estimate	Std. Error	t-value	Pr(>|t|)
(Intercept)	100.751	0.31152	3.234	0.00342
Standard length (SL)	0.10029	0.03418	2.934	0.00707
Mean oocyte diameter	0.09934	0.07490	1.326	0.19674
Site (RFAD)	0.66376	0.29719	2.233	0.03470
SL: Site (RFAD)	-0.08979	0.03591	-2.501	0.01932

FIGURE 4| Comparison of the mean relative condition factor (Kn) of specimens of Bryconops giacopinii from road-crossed streams the BR-174 highway (N = 60) and from pristine streams in the RFAD (N = 60).

All the specimens analyzed had parasites in the digestive tract (Prevalence Index = 100%). However, less than 50% of the specimens had parasites in the swim bladder, all of which belonged to the Phylum Nematoda, with a Prevalence Index of 87.3%. Black spot disease (parasites from the subclass Digenea) was observed only in fish from streams impacted by the BR-174, with a prevalence of 46.6%. The parasites were encysted in the form of metacercariae, which were identified as belonging to the genus Neascus (Niewiadomska, 2002).

There was a significant difference in the occurrence of parasites between the two areas (t = 9.7233, p-value <0.001, N = 120), with a higher total abundance of parasites in specimens collected from altered streams (BR-174: mean = 3.21; RFAD: mean = 0.838). A significant negative relationship was found between the total abundance of parasites and the condition factor (Kn) for fish collected from streams impacted by the BR-174 road, with R = 0.14 and p-value = 0.002 (Fig. 5).

FIGURE 5| Relationship between total parasite abundance (log-transformed data) and the relative condition factor (Kn) of Bryconops giacopinii (N = 60) from road-crossed streams the BR-174 highway.

Length at maturity (L₅₀ and L₁₀₀), oocyte diameter and fecundity. Males and females from RFAD are sexually mature at 7.23 cm (L₁₀₀ = 10.3) and 6.76 cm (L₁₀₀ = 10.8 cm), respectively. Males from the BR-174 streams matured at 6.21 cm (L₁₀₀ = 9.49 cm) and females at 6.34 cm (L₁₀₀ = 8.23 cm) (Figs. 6A–B; see Fig. S4 for fish frequency by size class). There was no difference in the mean length of sexual maturity (L₅₀) for both sexes between areas (mean L₅₀ RFAD – 6.995; BR-174 – 6.275; t = 3.064, p-value = 0.20), but a significant difference in the L₁₀₀ of sexual maturity (mean L₁₀₀ RFAD – 10.20; BR-174 – 8.86; t = 13.40, p-value = 0.047).

FIGURE 6| Logistic curves fitted to estimate the length at first sexual maturation (L₅₀) of males (blue line) and females (pink line) of B. giacopinii in two environments: A. Pristine streams (RFAD); B. Road-crossed streams (BR-174). Dashed vertical lines indicate the estimated L₅₀ values for each sex.

No difference was observed in the average size of oocytes in the spawning batch of females between areas (Wilcoxon rank sum test, W = 119.5, p-value = 0.79; Fig. S5). Absolute fecundity of the batch varied according to standard length (SL), area, and the interaction between these variables, with the model explaining about 50% of the total fecundity variance (GLM Pseudo-R² = 0.497, DF = 25). Model selection based on Akaike information criterion (AIC) indicated that the best model was batch fecundity as a function of standard length, mean oocytes diameter, area (BR-174 and RFAD) and the interaction of standard length and area (Tab. S6). Considering the significant effect of the interaction, fecundity varied differently between areas, with a significant increase in fecundity with fish size in the road-crossed streams (BR-174), but not in the pristine environment (Fig. 6).

When considering only the area, females from the pristine (RFAD) environment had a significantly lower absolute fecundity of the batch compared to females from the road-crossed streams BR-174 (RFAD 867 oocytes; BR-174 1483 oocytes, Fig. 7).

FIGURE 7| Relationship between standard length (SL) and fecundity (log-transformed data) of Bryconops giacopinii (N = 30) collected from streams in a pristine area (RFAD) and from road-crossed streams along the BR-174 highway.

Discussion​

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Changes in the aquatic environment trigger a series of effects on organisms, particularly fish. When exposed to these changes, fish tend to express mechanisms that may eventually lead to adaptations, allowing them to remain in the area and complete their life cycle (Winemiller, 1989). However, the persistence and generation of new offspring in an altered environment are closely related to colonization capacity and efficiency in exploiting new types of resources (Kolonin et al., 2022). Our results indicate that alterations in the aquatic environment caused by highway crossings over streams significantly affect many aspects of the biology and ecology of Bryconops giacopinii. These results also highlight the processes that may limit the local persistence of the original fauna, including trophic and reproductive disturbances, as well as increased susceptibility to pathogen infections related to structural changes.

Results of the diet of B. giacopinii demonstrated not only the species broad capacity for exploiting trophic resources but also the differences in the contribution of food items based on their origin (allochthonous and autochthonous) in pristine streams (RFAD) and those affected by road crossing (highway BR-174). In pristine streams, a relatively higher consumption of allochthonous items, mainly insects, was observed. The predominance of arthropods in the diet may be related to their wide distribution and abundance in tropical forests and the close relation with the riparian vegetation, making them a readily available food source for fish (Esteves, Aranha, 1999; Cardoso, Couceiro, 2017). The predominance of allochthonous insects and the occurrence of few autochthonous items were also observed by Barros et al. (2017, 2024) in the same pristine streams of the RFAD. Vannote et al. (1980) state that, in pristine streams, the tree canopy cover from the riparian vegetation reduces sunlight incidence in the channel and limits autochthonous production, characterizing these environments as oligotrophic. Barros et al. (2017) correlated the diet composition of B. giacopinii with the positioning of individuals in the middle and upper thirds of the water column during foraging, which was explained as a way to quickly intercept food items fallen from the riparian forest canopy.

For populations in altered environments, the consumption of autochthonous items was proportionally higher, indicating a reduced influence of the remaining riparian vegetation. High exposure to sunlight and elevated temperatures lead to increased autochthonous primary productivity (Gerking, 1994). The increase in aquatic primary productivity may have been intensified by the absence of riparian forest in the dammed stream stretch, caused by the permanent flooding of the margins and death of the trees in these environments. The resulting open canopy in altered streams likely contributed to this effect and may also explain the greater presence of algae in the diet of individuals collected from these sites.

The abundant occurrence of filamentous algae in the diet of B. giacopinii in altered streams likely reflects the species’ generalist and opportunistic feeding habits (Barros et al., 2024). Such dietary flexibility is common among fish exposed to unpredictable food availability, as it allows them to exploit alternative resources when preferred items are scarce (Abelha et al., 2001; Hahn, Cippra, 2006; Ceneviva-Bastos, Casatti, 2007). This trophic flexibility is particularly important in altered environments, where shifts in habitat structure often lead to fluctuating resource availability (Hahn, Fuji, 2007) and can help explain the success of B. giacopinii in persisting in such altered environments (Barros et al., 2024). The predominant consumption of widely available items such as plant material and algae may result in lower energy and protein intake compared to animal-based food sources (Bowen et al., 1995; Castro, Vari, 2004), which may negatively impact individual fitness (Cruz-Rivera, Hay, 2000). To compensate for the lower nutritional value of these items, individuals often ingest large amounts of available food resources relative to their body weight (Faria, Benedito, 2011). As a long-term effect, some species may develop physiological adaptations to better assimilate the energy and nutrients present in these resources (Fiori et al., 2016). Beyond diet, body condition also differed between the two types of environments. Fish collected from altered streams exhibited lower body condition compared to those from pristine streams. Dietary shifts are known to affect the body condition, often leading to a decline in condition factor. This effect, when associated with anthropogenic impacts, has been documented in the lambari Astyanax lacustris (Pereira et al., 2016), for example. The authors reported a decline in the condition factor of this species following a dietary shift (from herbivory to piscivory), resulting from the formation of a reservoir due to river damming in southeastern Brazil. For B. giacopinii it is likely that changes in feeding patterns and the reduction in the consumption of animal-based food sources (such as allochthonous insects, which have higher energy and protein content) in altered streams possibly contributed to the observed decline in body condition. Such observations reinforce the role of diet as a strong determinant of the nutritional and physical state of fish in nature (Vazzoler, 1996).

The altered and pristine environments also showed different responses regarding the presence of parasites, a factor that may also influence the body condition of fish in the BR-174 streams. The lentic conditions and increased temperatures, resulting from channel blockage by road crossing, can lead to a higher density of infected snails (an intermediate host of several parasites; Flores-Lopes, 2014; Flores-Lopes, Thomaz, 2011), favoring the proliferation of digenean parasites in altered environments (Ondračková et al., 2004; Souza et al., 2008; Dumbo et al., 2020).

Hoffman (1956) emphasized the damage caused by digenean parasites, particularly those responsible for black spot disease, which negatively affects fish growth and weight gain, and can also lead to mortality in juvenile individuals when present in high numbers (Harrison, Hadley, 1982; Cairns et al., 2005).

Comparatively, pristine environments have free-flow water with an average temperature of 24°C and presence of riparian vegetation, while altered environments present nearly still water with 28°C in average. Differences in these factors (mainly temperature) may explain the apparent absence of black spot disease in fish from the RFAD and its high abundance in fish from the BR-174. However, the presence of another group of parasites (Nematoda) was observed in the pristine areas. Nematode parasites, when in high numbers, can negatively affect fish body condition, as observed in Gadus morhua (Podolska et al., 2024), or have no influence, as seen in Metynnis lippincottianus (Carvalho et al., 2020). However, poor body condition and unfavorable environmental conditions can both lead to increased susceptibility to opportunistic parasitic infections and negatively impact fish fitness (Hoffman, 1956; Pavanelli, 1998). Under high parasitic density, the host diverts energy toward sustaining the parasites, to the detriment of its own body condition (Guidelli et al., 2011; Hasik, Siepielski, 2022), or host energy is usurped by the parasites that use it for their own growth and reproduction (Poulin, George-Nascimento, 2007).

The pressures caused by abiotic factors (physical changes in habitat that affect food availability) and biotic factors (biological interactions, including parasite-host interactions) can drive modifications in fish size and body condition, contributing to changes in the reproductive traits of a population (Wootton, 1990; Vazzoler, 1996). Alterations in temperature, pH fluctuations, and salinity changes can affect most life history aspects of fish, interfering with female growth, fecundity, or oocyte development (Orsi et al., 2002). In our study, a difference in fecundity was observed, with females from altered streams exhibiting higher fecundity, but no difference in oocyte diameter. These results suggest that differences in energy allocation strategies, rather than reproductive energy limitation, may explain the observed patterns. Fecundity varied with fish size in different ways between sites, but this variation was not associated with female body condition. Although differences in size and the intensity of parasitic infection were not evaluated in the present study, it is expected that the cost of infection is much higher in smaller individuals (Harrison, Hadley, 1982), accentuating the trade-off between survival and reproduction. If the cost of survival becomes higher and energy intake does not increase sufficiently, the investment in fecundity must necessarily be reduced (Stearns, 1992). On the other hand, larger females in altered streams invested much more in fecundity compared to females of the same size in the preserved area, which may also be a response to demographic changes (Reznick et al., 1990), such as higher mortality rates in altered areas, reducing the chances of future reproductive events.

Alterations in reproductive parameters have been reported for large-scale disturbances, such as river damming for hydroelectric projects. Amadio et al. (2012) found changes in the size of first maturity, oocyte diameter, and fecundity of fish in the Balbina Hydroelectric reservoir. However, population responses to small-scale disturbances, such as the road crossings reported here, are scarce or absent in the literature regarding Amazonian streams. These changes in reproductive parameters indicate greater flexibility of individuals to adjust to environmental impacts, ensuring their own survival and the potential generation of viable offspring, as well as the establishment of populations in the new environment. In this sense, the pressures exerted by biotic and abiotic factors possibly act by selecting individuals who invest more energy to increase fitness (Wootton, 1990; Stearns, 1992), which could explain the higher fecundity observed in female B. giacopinii from altered streams along BR-174.

This study highlights the significant impacts of stream road crossings resulting from the construction of the BR-174 highway on the biological and ecological parameters of a fish species found in streams of terra-firme forest in the Amazon. The populations from dammed streams showed alterations in diet, indicating a greater dependence on autochthonous resources, as well as reduced relative body condition, increased parasitic intensity, and changes in fecundity, with increased reproductive investment in larger females. These changes reflect the sensitivity of the fish fauna to environmental modifications and emphasize the need for mitigation and conservation measures to minimize the effects of such anthropogenic disturbances on Amazonian aquatic ecosystems. The study underscores the importance of integrated research that evaluates multiple biological and ecological parameters to better understand the consequences of human activities on biodiversity.

Acknowledgments​

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We thank the PPG Biologia de Água Doce e Pesca Interior and INPA for logistical and facility support, the Projeto Igarapés, and Fabiano Emmet for producing the map.

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Authors

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M. Bárbara Mascarenhas¹ , Sidinéia Amadio², Camila S. dos Anjos³, Cristhiana P. Röpke², Jansen Zuanon^2,4 and Cláudia P. de Deus²

^[1]    Programa de Pós-Graduação em Biologia de Água Doce e Pesca Interior, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 6911-830, Manaus, AM, Brazil. (MBM) barbaramasc19@gmail.com (corresponding author).

^[2]    Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 69011-830, Manaus, AM, Brazil. (CPR) crisropke@gmail.com, (SA) sidamadioinpa@gmail.com, (JZ) jzuanon3@gmail.com, (CPD) claudiapereiradedeus@gmail.com.

^[3]    Instituto de Desenvolvimento Florestal e da Biodiversidade do Estado do Pará, Av. João Paulo, 66610-770, Curió-Utinga, Belém, PA, Brazil. (CSA) casanjos@gmail.com.

^[4]    Senior Visiting Researcher at Universidade Santa Cecília (UNISANTA), Rua Oswaldo Cruz, 11045-907, Santos, SP, Brazil.

Authors’ Contribution

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M. Bárbara Mascarenhas: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Software, Validation, Visualization, Writing-original draft, Writing-review and editing.

Sidinéia Amadio: Conceptualization, Methodology, Supervision, Validation, Visualization, Writing-review and editing.

Camila S. dos Anjos: Methodology, Supervision, Validation, Visualization, Writing-review and editing.

Cristhiana P. Röpke: Formal analysis, Methodology, Software, Supervision, Validation, Visualization, Writing-review and editing.

Jansen Zuanon: Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Visualization, Writing-review and editing.

Cláudia P. de Deus: Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Visualization, Writing-review and editing.

Ethical Statement​

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The collection of fish specimens was authorized by SISBIO (license number 22121–1) and research activities involving fish at INPA were authorized by the institution’s Animal Research Ethics Committee (license number 039/2018).

Competing Interests

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The author declares no competing interests.

Data availability statement

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The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

AI statement

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The authors did not use any AI-assisted technologies in the creation of this manuscript or its figures.

Funding

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The authors were supported by the ADAPTA Project and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), which provided a master’s scholarship to MBM (grant 132302/2017–9).

Supplementary Material

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Supplementary material S1

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How to cite this article

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Mascarenhas MB, Amadio S, Anjos CS, Röpke CP, Zuanon J, Deus CP. Road crossings disrupt feeding, reproduction, and body condition of a forest stream fish in the Amazon. Neotrop Ichthyol. 2025; 23(4):e250054. https://doi.org/10.1590/1982-0224-2025-0054

Copyright​

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This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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© 2025 The Authors.

Diversity and Distributions Published by SBI

Accepted November 9, 2025

Submitted March 30, 2025

Epub February 2, 2026