Abstract
This study examined the metrics of the macroparasite community in fishes from the Jaguaribe River basin, state of Ceará, before and after receiving water from the São Francisco River in Northeastern Brazil. This research assessed the association of environmental factors (water parameters) and the traits of 30 fish species on the parasite richness and abundance across space (river course) and time (seasons, pre- and post-transposition periods). Generalized linear models reveal associations between parasite metrics and host traits, water parameters, and river sub-basin. Host size and body condition positively correlated with parasite richness and abundance, while reproductive phase was negatively related. Water quality impacted ecto- and endoparasites differently, with seasonal and sub-basins variations and differences among sub-basins. The general models also indicate that the period is a significant variable, where parasite richness decreases while abundance increases in the post-transposition period. This study underscores the importance of considering diverse environmental and host variables for understanding parasite dynamics in river ecosystems. These findings could lead to valuable insights for ecosystem management and conservation, elucidating the potential consequences of environmental alterations on parasite-host interactions and ecosystem health.
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Introduction
Understanding which processes and factors shape the structure of wild communities is one of the main issues addressed in ecology (Sutherland et al. 2013). In tropical fish communities, changes in richness and abundance are usually caused by habitat transformation and are generally associated with deforestation and pollution (Barrella and Petrere 2003; Light and Marchetti 2007; Alves et al. 2016; Vendel et al. 2017), etc. Like free-living species, parasites can also respond to disturbances in ecosystems and can provide valuable information about the quality, integrity, and health of ecosystems (Sures et al. 2017). The composition of parasite communities may be influenced by several factors, including environmental conditions (e.g., seasonality, longitudinal gradient, concentration of nutrients), host traits (e.g., feeding, behavior, sex), and the group of parasites studied (e.g., life cycle, availability of intermediate hosts) (Guidelli et al. 2003; Takemoto et al. 2004; Marcogliese 2005; Blasco-Costa et al. 2014; Santoro et al. 2014; Mattiucci et al. 2015; Lacerda et al. 2017; Falkenberg et al. 2019; Villalba-Vasquez et al. 2022). The structure of the fish parasite community is typically influenced by a combination of biotic and abiotic factors (Bommarito et al. 2022). For example, host size can affect parasite abundance and richness, because larger hosts can provide more microhabitats for parasites and support larger infrapopulations (Kuris et al. 1980). Another factor is the reproductive phase of hosts (Santoro et al. 2020). Different ontogenetic stages of hosts explore distinct resources and habitats, leading to variations in parasite composition and abundance (Duneau and Ebert 2012). Similarly, abiotic factors such as water quality parameters, temperature and seasonality also play important roles in influencing hosts and their parasitic load (Marcogliese and Cone 1996; Tack et al. 2015; Paull and Johnson 2018). These abiotic conditions can directly affect the developmental stages of parasites, either because they are free in the aquatic environment or because of alterations in the density of intermediate and definitive hosts (Gordy et al. 2020). According to Poulin (2004), distinguishing between endoparasites and ectoparasites is crucial when analyzing how parasites respond to various biotic and abiotic factors for at least three reasons. First, endoparasites often have complex life cycles, involving at least two host species, and infect hosts predominantly via trophic web, whereas ectoparasites tend to have direct life cycles and infect fish via free-swimming infective stages. Second, the diversity of ectoparasites per host species is typically greater than that of endoparasites (e.g., Rohde and Heap 1998; Rohde 2002). Third, endoparasites often occur at much higher abundances than ectoparasites (Poulin 2004). Human-induced changes in the environment are strongly reflected in parasite community structure (Khan and Thulin 1991; Lafferty 1997; Karvonen et al. 2013). Environmental impacts can have positive, negative, or neutral effects on parasites, depending on the type of impact, or the group of parasites studied (Goutte and Molbert 2022). For example, parasitism may increase if the environmental impact reduces host resistance or increases the density of intermediate or definitive hosts (Valtonen et al. 1997), or parasitism may decrease if host density decreases, and if parasites suffer direct or indirect mortality from environmental impact (Lafferty 1997). Eutrophication can cause an increase in parasite prevalence, intensity, abundance, and species richness (Broeg et al. 1999; Palm and Dobberstein 1999) and organic pollution can decrease the abundance, richness, and intensity of parasites (Dušek et al. 1998; Billiard and Khan 2003). In the absence of an environmental impact, a healthy ecosystem is expected, where the parasites can complete their life cycle and have a richness and abundance that fluctuates within a normal range for that specific environment (Vidal-Martínez et al. 2019).
Recently, in Northeastern Brazil, a major interbasin water transfer is being carried out, the São Francisco Interbasin Water Transfer Project (SF-IWT) (Brazil 2004; Lima 2005). In this project, the São Francisco River (perennial regime) was artificially connected to other hydrographic basins of the Northeastern region (intermittent regime) (Stolf et al. 2012), including the Jaguaribe River, which was studied here. The SF-IWT is a major ongoing water project with the aim of addressing water scarcity in the semi-arid region of Brazil and acting as a socioeconomic development tool (Andrade et al. 2011). Despite its economic and social relevance, this project can have impacts both on the donor and on receiving basins of the transposition (Falkenberg et al. 2024). In addition to altering the entire hydrological dynamics and changing the water properties of semi-arid Brazilian rivers, transposition represents a significant biogeographical event that facilitates biotic exchanges between previously isolated basins (Berbel-Filho et al. 2016). This process can lead to changes in the composition of aquatic fauna, and the homogenization of species in basins involved in transpositions around the world has been identified (e.g., Meador 1992; Moreira-Filho and Buckup 2005; Ellender and Weyl 2014; Zhan et al. 2015; Zhuang 2016; Shelton et al. 2017), including the east channel of the SF-IWT, which transports water to the Paraíba do Norte River basin, State of Paraíba (Ramos et al. 2021; Silva et al. 2023).
In a previous study from the same area on fish parasites and river transposition, the highest total prevalence and mean abundance of parasites were observed after the river transposition. However, the diversity and host specificity index were higher before the transposition (Falkenberg et al. 2024). Given the above, our study aimed to investigate within the complexity of this aquatic system, which host and environmental variables are the most important for determining parasite richness and abundance, considering variation in space (the course of the river) and time (seasons and before and after the transposition), and also considering ecto- and endoparasites together (total), and separately, since they may exhibit different patterns.
In the present study, we investigated the following: (1) whether host factors such as body size, relative condition factor, and reproductive phase are associated with parasite richness and abundance; (2) whether some abiotic parameters of the water are associated with parasite richness and abundance; (3) whether the parasite richness and abundance vary among hosts in different seasons; (4) whether the parasite richness and abundance differed according to the longitudinal gradient of the river (Upper, Middle, and Lower Jaguaribe); (5) whether there was a difference in the parasite richness and abundance between the pre- and post-transposition periods; (6) whether the richness and abundance of ecto- and endoparasites respond differently to all the tested variables.
Material and methods
Study area
The Jaguaribe River basin (Fig. 1) is situated in the Ceará state, Brazil, between the coordinates 4°30′ and 7°45′ South latitude and 37°30′ and 41°00′ West longitude. It is recognized as one of the largest intermittent rivers globally (Castro et al. 2020), covering an area of 72,560 km2, which represents nearly 50% of the total territory of Ceará state (Costa et al. 2016). Its sources are located in the municipality of Tauá, Southwest state, and it flows northeast for approximately 610 km before reaching the Atlantic Ocean, between the municipalities of Aracati and Fortim (Braga and Matushima 2021). The Jaguaribe basin is situated within the Caatinga domain, in the semi-arid region of Brazil. The climate, according to Köppen classification, is BS (semi-arid or steppe climate) (Gaiser et al. 2003). Precipitation in the region is highly variable, ranging from 400 mm in the inland areas to 1200 mm along the coast. Although the rainfall level is relatively higher than in many other semi-arid regions worldwide, the combination of impermeable crystalline rocks in the soil and high temperatures results in significant evapotranspiration rates, exceeding 2000 mm for the basin, and limited water retention and storage (Johnsson and Kemper 2005).
The Jaguaribe River basin is divided into three sub-basins (Upper, Middle, and Lower Jaguaribe) and two tributaries (Salgado and Banabuiú Rivers) and is the largest basin to receive waters from the SF-IWT project. The Upper Jaguaribe sub-basin encompasses a drainage area of 24,636km2, accounting 16.56% of the state’s total area, which covers 24 municipalities. The Middle Jaguaribe sub-basin has 10,509 km2, representing 7.09% of Ceará state’s area, and covers 13 municipalities. The Lower Jaguaribe sub-basin, area most influenced by the ocean, covers 4.64% of the state’s area and nine municipalities (Johnsson and Kemper 2005). In July 2020, an artificial connection was established between the Jaguaribe River and the São Francisco River, allowing water from the donor drainage to enter the Jaguaribe River basin through the channel called North Axis, beginning in the Upper Jaguaribe sub-basin, Atalho dam, in the municipality of Jati (Brazil 2004).
Collection and examination of fish for parasites
The parasite dataset used here was derived from an earlier research by Falkenberg et al. (2024), which provided the foundational data for this study. Nine sampling points were determined along the main course of the Jaguaribe River, with three replicates in each sub-basin (Upper, Middle and Lower Jaguaribe). In each of the nine sampling points, two dragnets (net of 10 m and mesh of 5 mm) and six sets of cast nets (net of 2 m and mesh of 15 mm) were used. Subsequently, the fish were euthanized using eugenol solution, and preserved in a 10% formalin solution for later analysis of the ecto- and endoparasites. The geographic coordinates for each collection point are provided in the Supplementary Information (Table 1SI). Hosts were collected during both dry and rainy seasons, as well as in the pre- and post-transposition periods. In the pre-transposition period, a total of 1032 host specimens were analyzed during the dry season (November 2019), and 777 host specimens were analyzed during the rainy season (March 2020). In the post-transposition period, 574 host specimens were analyzed during the dry season (November 2021), and 580 host specimens in the rainy season (May 2022).
After taxonomic identification and obtaining biometric data of the hosts in the laboratory, an incision was made on the ventral surface of the hosts; all organs were dissected and separated. Each organ was examined under a stereomicroscope to collect the parasites. The preparation of parasites for identification followed the methodology proposed by Kritsky et al. (1986). The reproductive phase of fishes was determined based on macroscopic visualization of the gonads (Soetignya et al. 2016), where fish with developed gonads were considered spawning capable and fish with undeveloped or underdeveloped gonads were considered immature/developing (Brown-Peterson et al. 2011). Due to the inability to distinguish between immature and developing stages of all fishes, the immature and developing host’s reproductive phase were grouped together. The relative condition factor (Kn) was calculated for each host individual, which corresponds to the ratio between the observed weight (Wo) and the theoretically expected weight (We) for a given length, i.e., Kn = Wo/We (Le Cren 1951).
Water quality parameters
At each collection point, water parameters were measured in situ, including temperature, pH, total dissolved solids (TDS), and salinity using a multiparameter probe (Horiba U-50). Still, at each collection point, three samples of water were collected to determine the concentrations of ammonia and phosphate. All measurements were taken three times in different places along the river bank, and then averaged for each collection point. For the analyses of dissolved inorganic nutrients, the methodology described in Standard Methods for the Examination of Water and Wastewater (APHA 2005) was followed.
Statistical analyses
Generalized linear models (GLMs) were constructed to examine the relation between biotic and abiotic variables and the richness and abundance of parasites. We tested the effects of both individual and interacted factors on parasite richness and abundance. The response variables were used: total richness (number of parasite taxa in a single host), total abundance (number of parasite specimens in a single host), total richness of ecto- and endoparasites, and total abundance of ecto- and endoparasites.
In all models, the following variables were tested as possible predictor variables: (1) host traits (total length, Kn, reproductive phase, and species), (2) parameter of water quality (temperature, pH, TDS, salinity, ammonia, and phosphate concentration), (3) river sub-basin (Upper, Middle, and Lower Jaguaribe), (4) season (dry and rainy), and (5) period (pre- and post-transposition). The interactions tested were as follows: host species × total length, host species × Kn, host species × reproductive phase, sub-basin × season, and period × season.
The most adequate models to explain variations in the response variables were selected using backward selection and Akaike information criterion (AIC), where all the variables are initially included in the model, and the least significant variables are sequentially removed from the model. Significant values (p < 0.05) are considered an indication that variations in the response variables can be explained by variations in the predictor variables. The models were made with the Poisson distribution using the R programming environment version 4.2.3 (R Core Team 2023).
Results
The Jaguaribe River: water quality parameters across space and time
The mean values of the environmental variables for both dry and rainy seasons and in the pre- and post-transposition periods are shown in Fig. 2. In the pre-transposition period, the temperature varied between 28.4 °C and 34.7 °C, with pH values around 7.0. After the transposition, the temperature remained close to 29.5 °C, while the pH increased to an average of 8.4, suggesting a more alkaline environment. Total dissolved solids (TDS) increased considerably in the post-transposition period, going from values below 2 g/L to an average of 73 g/L, indicating a higher concentration of salts in the water. The percentage of salinity also increased in the post-transposition period. Ammonia and phosphate concentrations varied in both periods, but the changes were most notable in post-transposition. In pre-transposition, ammonia concentrations varied between 0.03 and 0.63, while phosphate concentrations varied between 0.02 and 0.15. However, in the post-transposition period, ammonia concentrations decreased and, in some cases, reached zero or undetectable. Phosphate concentrations also varied, but the variation was less pronounced compared to ammonia. Along the river, from the sources to the mouth, variations in environmental variables were observed. The temperature remained relatively stable near the river mouth, although it fluctuated at the sources. The pH varied along the river, with an increase towards the mouth, making the water more alkaline. Total dissolved solids (TDS) concentrations have increased considerably, indicating an increase in water mineralization in space. Salinity also increased as the river approached its mouth. Ammonia and phosphate concentrations exhibited fluctuations, but without a clear trend in space.
Fish parasite community of the Jaguaribe River: general aspects and related to the host’s traits
A total of 47 parasite taxa were identified in the 2962 analyzed fish hosts (41 helminth taxa and 6 Crustacea) from the Jaguaribe River, Brazilian semiarid. Among the analyzed fish, which belong to 30 different species, 963 (32.5%) were found to be infested/infected with at least one parasite taxon. The host species Hoplias malabaricus had the highest value of parasites prevalence, with 63.6% of individuals infested/infected. Regarding parasite abundance, Loricariichthys platymetopon had the highest number of parasite specimens, with 6869 individuals. No parasites were found in the hosts species Synbranchus marmoratus and Schizodon dissimilis. Table 1 provides information on the parasite species, parasite abundance, the location where they were found, infestion/infection site, and host species. For the complete host-parasite list and parasitic indexes, see Falkenberg et al. (2024). Detailed information about the analyzed hosts is available in the Supplementary Information (Table 2SI).
The GLMs addressed various aspects of the hosts and the environment to identify the factors that contribute to the determination of richness and abundance of fish parasites in the Jaguaribe River. Table 2 presents the GLM results and the following result sections show how these variables were correlated.
For the models with the response variable parasite richness (total, ecto- and endoparasite), the host’s length, Kn, and reproductive phase exhibited positive or negative correlations with parasite richness (Fig. 3). Nevertheless, upon considering the interaction with the host species, it became apparent that only a limited number of species showed such correlations. Also, the endoparasite richness was correlated with a greater number of host species compared to ectoparasite richness. For the models with response variable parasite abundance (total, ecto- and endoparasite), the total parasite abundance demonstrated significant associations with various fish species and host traits, revealing both positive and negative correlations. In contrast, the abundance of ectoparasites exhibited notably fewer significant correlations with the studied species and host traits. Similarly, endoparasite abundance displayed limited significant associations with the same set of species and host traits, with specific species and host traits showing positive or negative relationships.
Fish parasite community of the Jaguaribe River: aspects related to water quality parameters, spatio-temporal, and transposition period variables
The ectoparasite richness was positively correlated with TDS and phosphate concentration and the endoparasite richness was negatively related with ammonia concentration and positively with phosphate concentration. The ectoparasite abundance had a positive relation with temperature and TDS, while having a negative relation with pH. The endoparasite abundance was positively correlated with temperature, pH, and ammonia concentration, and negatively correlated to salinity, TDS, and phosphate concentration (Table 2).
Seasonality was significantly associated with both ecto- and endoparasite richness and abundance, with high rates occurring in the dry season for all the response variables tested (Table 2; Fig. 4C, D). The longitudinal gradient was significantly associated with both parasite richness and abundance. There was no significant correlation observed between ectoparasite richness and the sub-basin. However, a positive correlation was observed between endoparasite richness and the sub-basin, with higher values found in the Middle Jaguaribe sub-basin. For ectoparasite abundance, higher values were observed in Lower Jaguaribe, while the Upper and Middle Jaguaribe sub-basins did not differ significantly. As for endoparasites, higher richness was observed in the Lower Jaguaribe, while the Upper Jaguaribe sub-basin had lower richness levels (Table 2; Fig. 4B).
Considering the interaction between the sub-basin and season, a significant difference in parasite richness and abundance was observed. Endoparasite richness and ectoparasite abundance showed the highest rates in the combination of Middle Jaguaribe and the rainy season. On other hand, for endoparasite abundance, the highest rates were observed in the combination of Lower Jaguaribe and the dry season and the lowest rates were observed in the combination of Upper Jaguaribe sub-basin and rainy season (Table 2).
Both ectoparasite and endoparasite richness were positively correlated to the transposition period, with higher values observed in the pre-transposition period (Fig. 4E). However, for parasite abundance, the highest values were observed in the post-transposition period (Fig. 4F). Considering the interaction between period versus season, ecto- and endoparasite richness did not differ significantly according to transposition period and season. For ectoparasite abundance, the highest rates were observed in the combination of post-transposition and dry season and lowest rates in the combination of post-transposition and rainy season. For endoparasite abundance, the highest values were observed in the combination of pre-transposition and dry season and lowest values in the combination of pre-transposition and rainy season (Table 2).
Discussion
Our results showed that (1) host traits are important to determine the parasite richness and abundance; (2) abiotic factors are also important to determine parasite richness and abundance, but parasites respond differently to each analyzed factor, and may be positively or negatively correlated; (3) both richness and abundance of parasites were higher in the dry period, with higher parasite richness and abundance in the Upper Jaguaribe in the dry season; (4) parasite richness was higher in Middle Jaguaribe sub-basin and parasite abundance was higher in the Lower Jaguaribe, both in the dry season; (5) the parasite richness was higher in the pre-transposition period, in the rainy season, while the parasite abundance was higher in the post-transposition period, in the rainy season; (6) the responses of ecto- and endoparasites were different for the analyzed variables: host body length, host reproductive phase, TDS, pH, and sub-basin.
Fish parasite community of the Jaguaribe River: aspects related to the host’s traits
In this study, the abundance of ectoparasites was not correlated with host body size and, although this is not common, it has been reported by Poulin (1995, 1999) and Lo et al. 1998. This suggest that, in the Jaguaribe River, the abundance of ectoparasites may be more strongly related to environmental factors than to host’s traits, since ectoparasites are in constant contact with the environment (water) and can be positively or negatively affected by environmental conditions (Lacerda et al. 2017; Sures et al. 2017; Falkenberg et al. 2019). According to Kuris et al. (1980), hosts can be considered islands. This assumption underlies that host-parasite relationships are similar to those that support species-area relationships observed in free-living assemblages (see MacArthur and Wilson 1967). Host body size has been considered a determinant of parasite species richness and abundance, because larger hosts tend to support higher parasite load compared to smaller hosts (Poulin 1997). This is often attributed because larger hosts provide more resources and microhabitats (space) for parasites, making them more suitable for colonization and persistence of these parasites (Poulin 2004). This positive relationship between host body length and parasite richness and abundance was observed in several studies carried out in freshwater system (Lima et al. 2021; Casali and Takemoto 2016; Simková et al. 2001), including in Brazilian semi-arid (Sampaio et al. 2022; Gião et al. 2020; Silva-Neta et al. 2020; Alexandre and Yamada 2022). However, the relationship between host size and parasite load may not always be linear and can depend on specific host-parasite-environment interactions.
The relative condition factor (Kn) is a measure of the overall health and physiological condition of a host (Le Cren 1951). In this study, the parasite total richness was positively correlated to Kn for L. derbyi and L. platymetopon. Notably, the positive correlation between parasite total richness and Kn for these host species suggests a more intricate relationship between these fish species and their parasites. Hosts of the genus Loricariichthys forage in benthic habitats (Ferreira et al. 2013) and this association can be a key factor in this dynamic. Organisms associated with the benthos have a closer interaction with aquatic substrates, which can facilitate exposure to a higher diversity of parasites present in these environments (Hechinger et al. 2007). This is because many parasites live part of their life cycles in sediment or in benthic intermediate organisms (Gibson et al. 2002). Therefore, hosts inhabiting this region have more opportunities to encounter and become infected by a variety of parasites. However, the lack of correlation between parasite richness and Kn in other host species underscores the complexity of host-parasite interactions, demonstrating that the relationship between host health and parasite diversity is not universal and may be species-specific (Poulin 2006b).
The association of parasite abundance and host’s Kn was significant, with hosts with higher Kn value having a greater number of parasites. This suggests that hosts in better health conditions may tolerate higher levels of parasites. Although this pattern seems counterintuitive, similar findings have been observed in other fish-parasite interaction studies (Guidelli et al. 2011; Lizama et al. 2006; Yamada et al. 2008; Moreira et al. 2010). This positive correlation can be attributed to several factors. Firstly, hosts with higher Kn values can provide more physical space for both ectoparasites and endoparasites (Moreira et al. 2010). Additionally, hosts that consume larger quantities of food may come into contact with more infective forms of parasites through trophic transmission (Dias et al. 2004). The effectiveness of the host’s immune system or the limited pathogenesis and expected effects of parasites can also contribute to this positive correlation (Poulin 1998). Furthermore, hosts in better condition typically have more available resources to be used by parasites and occupy more suitable habitats, creating favorable conditions for colonization and survival of parasites. Consequently, hosts with higher Kn can offer a more favorable environment for the reproduction and proliferation of parasites, resulting in a greater abundance (Rynkiewicz et al. 2015).
Another host attribute that covaries with body size and can also show associations with parasite richness and abundance is the host’s sexual maturity. The relationships between host reproductive phase and parasite richness and abundance in various host species were as follows: positive correlation was observed between total parasite richness and reproductive phase in L. derbyi, while negative correlation was found for S. brasiliensis. The host S. heterodon showed a positive correlation with ectoparasite richness. Endoparasite richness exhibited positive correlations with S. brasiliensis, C. jaguaribensis, and M. costae. Regarding parasite abundance, there were positive correlations between total parasite abundance and reproductive phase for C. monoculus, L. derbyi, M. costae, M. intermedia, P. vivipara, S. heterodon, S. piaba, and T. signatus, but negative correlations for S. brasiliensis, C. jaguaribensis, C. orientale, and L. platymetopon. Ectoparasite abundance showed positive correlations with S. brasiliensis, C. orientale, and S. heterodon, and endoparasite abundance showed positive correlations with C. monoculus, L. derbyi, M. costae, M. intermedia, P. vivipara, S. heterodon, S. piaba, and T. signatus, as well as negative correlations with S. brasiliensis, C. jaguaribensis, C. orientale, H. marginatus, and L. taeniatus.
When total parasite richness and abundance show positive correlations with reproductive phase (as seen in species such as L. derbyi, M. costae, M. intermedia, P. vivipara, S. heterodon, S. piaba, and T. signatus), it suggests that as these fish hosts mature, they accumulate more diverse parasite communities and higher parasite numbers. This is because the tendency is for larger hosts to be sexually active and, consequently, more parasitized (Poulin 2000). Some possible explanations for this are that adult fish generally have a longer exposure time to parasites than juvenile fish, a process known as temporal accumulation, where adult fish may have lived more time in contact with parasites, thus increasing their chances of infection over time (Guégan et al. 1992). Adult fish also tend to explore a greater variety of habitats and feed on different prey compared to juveniles (Fernandez 1985). This may increase your exposure to a greater diversity of parasites, including ectoparasites from other individuals or endoparasites from consumption of parasitized prey (Kennedy 1970). In most fish species, there are differences in behavior, physiology, and habitat between adults and juveniles (Esch et al. 1988), which can result in different levels of infestation/parasitic infection. Conversely, when total parasite richness and abundance negatively correlate with reproductive phase (as observed in the host species S. brasiliensis, C. jaguaribensis, C. orientale, H. marginatus, and L. platymetopon), it implies that as these hosts mature, they tend to accumulate fewer parasite species and exhibit lower parasite abundance. This might be linked to the development of stronger immune responses or specific adaptations that limit parasite infestations in mature individuals (Maizels and McSorley 2016). It is possible that these hosts employ more effective immune responses as they mature, reducing their susceptibility to parasites (Morris et al. 2019). Alternatively, they might have specific behaviors or ecological niches that limit their exposure to parasites (Britton and Andreou 2016). These contrasting relationships highlight the complex interplay between host’s traits and parasite dynamics, in shaping the patterns of parasitism in aquatic ecosystems.
Fish parasite community of the Jaguaribe River: aspects related to water quality parameters
The prevalence, richness, and abundance of parasites can be influenced by several water variables (Lafferty 1997). First, the positive correlation between ectoparasite richness and abundance with total dissolved solids (TDS) can suggest that this environmental factor plays a role in promoting the diversity and abundance of these parasites. Higher levels of TDS can indicate that the water turbidity has increased (Putra et al. 2020). The turbidity can affect the host fish physiology and immune responses (Studer et al. 2012). In some cases, increased turbidity can stress or compromise the fish’s immune system, making them more susceptible to parasite infections, and weakened immune responses can lead to increased parasite load and richness (Sures 2008).
The richness of ecto- and endoparasites was higher in environments with higher phosphate concentration, while the abundance of endoparasites was higher in environments with higher ammonia concentration and lower in environments with higher phosphate concentration. Eutrophication is caused by high levels of nutrients in aquatic systems, mainly phosphorus and nitrogen, and is associated with increased primary productivity and water turbidity, and decreased level of oxygen in water (Smith 1998; Bennett et al. 2001). The increase in primary productivity in an environment is related to the increase in the abundance of intermediate and/or definitive hosts (Kennedy and Watt 1994), which can lead to an increase in parasite richness and abundance. However, while the concentration of these nutrients is not directly toxic to animals (Amdur et al. 1991), in sites with higher nutrient inputs, increased proliferation of algae can lead to oxygen depletion, resulting in a decreased abundance of both hosts and parasites species (Overstreet and Howse 1977), which can lead to the negative correlation of endoparasites with the ammonia concentration observed in this study.
Changes in temperature and pH parameters can directly influence the rates of establishment and development of parasites, the release of infectious stages, and also the transmission of parasites between hosts (Koprivnikar et al. 2010; Karvonen et al. 2013). Here, higher temperatures were related with a higher ecto- and endoparasite abundance. In relation to pH, the ectoparasite abundance was negatively correlated and endoparasite abundance showed a positive correlation with pH. The increase in temperature can favor the growth and reproduction of some parasites, leading to an increase in their abundance (Short et al. 2017). For example, in warmer temperatures, many ectoparasite species exhibit accelerated reproduction, leading to an increase in the number of parasites infesting host fish (Brazenor et al. 2020). A warm climate also increases the range of reservoir hosts, vector abundance, biting rates and overall survival, and parasitic transmission rates of vectors (Ostfeld 2009). Another scenario is that the increase in temperature can lead to an increase in fish activity (Volkoff and Rønnestad 2020). This can expose the fish to greater contact with ectoparasites present in the aquatic environment, facilitating the infestation. For endoparasites, temperature has a direct effect on the transmission of larval stages (Poulin 2006a). Most endoparasites use mollusks in their life cycles as the first intermediate host (Gibson et al. 2002; Viney 2009) and the generation of larval stages in these mollusks plays a fundamental role in the overall success of parasite transmission. In the temperature range where hosts and parasites can establish, an increase in this parameter are linked to an increase in the production of larvae in mollusks, causing an increase in the abundance of these infectious stages and a consequent increase in parasitism in definitive hosts (Selbach and Poulin 2020; Achiorno and Martorelli 2016; Paull et al. 2015). Another consequential aspect linked to seasonality is the potential impact of increased temperature on the host’s immune system (Bisset 1948). Increased temperatures can induce stress in fish, compromising their immune response (Bowden 2008), making them more vulnerable to parasite infections. Parasites may exploit the weakened state of the host fish’s immune system, facilitating infections.
Ectoparasite abundance was negatively correlated with pH and endoparasite abundance was positively correlated. In parasitism, pH can influence abundance in two ways: subjecting the host to a stress condition that weakens it, facilitating the establishment of parasites, or providing to parasites a favorable environment for its propagation (Karvonen et al. 2013). In general, it is commonly observed that fish ectoparasites show a negative correlation with pH (Jerônimo et al. 2022). Lower pH levels (acidic conditions) tend to be unfavorable for many ectoparasites. Acidic water can affect the survival and reproduction of parasites, reducing their population size (Tange et al. 2020). Otherwise, for endoparasites, the possible explanation for an increase in abundance in environments with higher pH is that this implies some form of toxicity caused by high pH hence increases in the abundance of parasites and vulnerability of the fish (Karvonen et al. 2013). Extreme pH levels can impair fish immune systems and overall health (Sures and Nachev 2022), weakening fish’s ability to avoid infections, stress their physiology, and disrupt their internal balance. This compromised state creates a more favorable environment for endoparasites in their hosts (Schreck and Tort 2016), thus increasing the abundance of these endoparasites.
Fish parasite community of the Jaguaribe River: aspects related to spatio-temporal and transposition period variables
In this study, the dry season showed higher richness and abundance of ecto- and endoparasites. Studies investigating the relationship between fish-parasites and seasonality demonstrate that the seasonality influences the patterns of infection/infestation in certain species of protozoa, monogeneans, nematodes, and argulids (Malta 1982; Neves et al. 2013). Variations in rainfall levels, for example, lead to changes in water quality and fish behavior, which can alter the parasite-host relationship (Dias and Tavares-Dias 2015). During the dry season, especially in semi-arid regions, water volume decreases significantly, remaining only puddles of water (Tabosa et al. 2012), resulting in increased aggregation of fish and facilitating horizontal transmission of ectoparasites (Arneberg et al. 1998). On the other hand, for endoparasites, who have a heteroxenous life cycle (depend on other invertebrate organisms, fish, and/or birds to complete their life cycle), seasonality is more related to the availability of food items (Lo et al. 1998) and free infective forms in the environment (Faruk 2018). During the dry season, there is greater overlap between intermediate and definitive hosts in a reduced environment (puddles), facilitating the transmission of endoparasites (Tavares-Dias et al. 2014). With the reduction of the water body, the probability of encounter between free infective forms and hosts increases, resulting in a higher acquisition of parasites and explaining the greater richness and abundance of endoparasites in the dry season observed in this study. In addition, environmental variables such as temperature and precipitation are also important when investigating patterns of infection in hosts (Esch et al. 1979; Shope 1991). In the dry period, the temperature is higher and this may accelerate the life cycle of some parasites, generating an increase in infection rates (Pojmanska et al. 1980). Also, high temperatures accelerate the evaporation process and, together with low precipitation indices, reduce the size and depth of water bodies (Schindler 2001), which can lead to the agglomeration of invertebrates (Barbola et al. 2011; Teles et al. 2013), thus contributing to explain the high levels of parasite abundance in the dry season, for both ecto- and endoparasites.
The longitudinal gradient of a river refers to the variation in the characteristics along its course (Hawkes 1975), and this can affect the richness and abundance of parasites (Blasco-Costa et al. 2012). The ectoparasite richness had no significant correlation with the sub-basins. However, the endoparasite richness was correlated, with the Middle Jaguaribe having the highest richness. As previously mentioned, the ectoparasites may be more correlated to environmental factors, since they are in constant contact with the water. In a river, the physical properties change significantly from its source to its mouth in ways that could affect infection patterns. The River Continuum Concept (RCC), proposed by Vanotte et al. (1980), considers the rivers as a spatial gradient, where the structural and functional traits of biological communities adjust along this gradient, in response to the patterns of entry, transport, use, and storage of organic matter in the river. In this concept, the fish community is distributed as follows: the upper portion of the river is predominantly occupied by species that consume aquatic invertebrates (invertivores); the middle portion, piscivorous and invertivores species; and the lower portion, detritivores.
What we found in this study regarding the endoparasite richness can be corroborated by RCC theory, since the presence of aquatic invertebrates in the fish diet is associated with an increase in the richness of endoparasites (Morand et al. 2000). This diversity of feeding habits and trophic interactions within the Middle sub-basin creates a more complex food web and increased opportunities for the transmission of endoparasites (Baia et al. 2018). The presence of invertivores fish in the middle sub-basin is particularly important. The aquatic invertebrates can serve as intermediate hosts for various endoparasites and the consumption of infected invertebrates by invertivores fish can lead to the establishment and transmission of endoparasites, increasing their richness (Marcogliese 2002). Additionally, the middle sub-basin often offers a more diverse range of habitats, including areas with higher substrate heterogeneity, such as riffles, pools, and eddies (Drago et al. 2003). These microhabitats can provide suitable conditions for both invertebrate intermediate hosts and fish hosts, facilitating the transmission of endoparasites.
Higher ectoparasite abundance in the Lower Jaguaribe sub-basin suggests that conditions in this sub-basin are more favorable for ectoparasite colonization and persistence. Abiotic factors can influence the abundance of ectoparasites (Lizama et al. 2013) and, in Jaguaribe River, the ectoparasite abundance had a positive relation with temperature and TDS. Thus, these conditions might provide suitable habitats and resources for the proliferation of ectoparasites, leading to higher abundance. On the other hand, for endoparasites, the higher richness observed in the Lower Jaguaribe sub-basin could be related to the availability of intermediate hosts, suitable environmental conditions for parasite life cycles, and complex trophic interactions (Kennedy 1990).
Significant differences in parasite richness and abundance were observed in this study, with endoparasite richness and ectoparasite abundance peaking in the Middle Jaguaribe sub-basin during the rainy season. This particular richness and abundance of parasites in the Middle Jaguaribe sub-basin suggests the existence of specific ecological niches or environmental conditions that favor the proliferation of these parasites, possibly attributable to increased water volume and the presence of suitable intermediate hosts (Turner et al. 2021). Conversely, endoparasite abundance was highest in the Lower Jaguaribe sub-basin during the dry season, possibly due to ecological factors like reduced water flow or increased host susceptibility during dry conditions, as such the host density increased (Bommarito et al. 2021). In contrast, the lowest rates were recorded in the Upper Jaguaribe sub-basin during the rainy season, indicating less conducive conditions for endoparasite proliferation in this sub-basin. These variations can be attributed to a combination of environmental factors, including habitat suitability, resource availability, and water flow dynamics, across the different sub-basins and seasons (Marcogliese 2016). Additionally, host population dynamics, variations in host species, and their interactions with parasites may also play a role in influencing these observed differences in parasite dynamics. Thus, the study shows the importance of considering both spatial and temporal factors to comprehensively understand the complex dynamics of parasite communities in these sub-basins.
While water transfer projects (transpositions) have been demonstrated to have various effects on animal fauna (Daga et al. 2020), with notable cases observed in different regions worldwide (e.g., Moreira-Filho and Buckup 2005; Ramos et al. 2018; Zhan et al. 2015; Shumilova et al. 2018), the influence of transpositions on parasitic fauna remains incipient (Falkenberg et al. 2024). The observed decrease in parasite richness in the post-transposition period could be attributed to the loss of stability and complexity of the environment, compared to the pre-transposition scenario (not impacted by transposition). It is known that less impacted environments have a higher diversity and species richness (Tilman and Downing 1994). A less impacted environment may also facilitate the establishment and persistence of a wider range of parasite species, since, according to Environmental Parasitology, healthy environments have healthy parasites living in a dynamic equilibrium (Marcogliese 2005). So, our result corroborates that found by Cort et al. (1960) and Keas and Blankespoor (1997) where environments that suffered anthropic impacts showed a lower richness of species of parasites, compared to environments where environmental impacts occurred.
Conversely, the post-transposition period presented higher parasite abundance, indicating potential changes in host-parasite interactions or alterations in environmental conditions that favored parasite proliferation, as observed by Falkenberg et al. (2024). It is possible that the event of transposition has disrupted the existing ecological balance, leading to increased contact rates between parasites and hosts or creating new suitable conditions for parasite survival and reproduction (Patz et al. 2000; Koprivnikar and Redfern 2012). Additionally, some stressors also increase the abundance of intermediate or definitive hosts (Lafferty and Kuris 1999), leading to an increased abundance of parasites. Based on this, the impact of transposition on parasite communities is likely associated with various factors, including altered habitat structure, water quality changes, modifications in host behavior, and interactions with other organisms (Carrera-Játiva and Acosta-Jamett 2023). These factors may have direct or indirect effects on parasite populations, influencing their richness and abundance. These findings agreed with the suggestion of Marcogliese (2005) that disturbances within an ecosystem modify the transmission of parasites, thereby influencing the abundance and composition of parasite species.
In conclusion, our study showed the relationship between parasite richness and abundance and several host’s traits and environmental factors. Parasites are a fundamental part of the environments and natural or anthropogenic variables can influence their richness and abundance. The findings of our study provide valuable insights into the host-parasite-environment relationships. Our results emphasize the significance of considering both biological and ecological factors when studying parasite communities within a specific environment, since understanding the factors that influence parasite dynamics is essential for effectively managing and conserving host populations and their respective ecosystems. This study highlights the predominant role of environmental and space–time variables over host’s traits in shaping the patterns of parasite richness and abundance within the investigated Jaguaribe River basin. The findings suggest that the specific ecological and climatic conditions of this specific ecosystem, as well as ecological factors contributing to heightened parasite richness and abundance during the dry season, play pivotal roles in driving these variations. These results emphasize the dynamic interplay between parasites, their hosts, and the intricate environmental factors within distinct spatial and temporal contexts. This underscores the significance of considering the broader ecological and climatic contexts when seeking to understand and manage parasite dynamics, particularly in the context of aquatic ecosystems that are suffering environmental changes like the Jaguaribe basin.
Data availability
Data is available from the corresponding author upon reasonable request.
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Acknowledgements
The authors are grateful to Nathália Correia Martins for her valuable assistance in laboratory procedures during the research. We extend the thanks to Bruno Anderson Fernandes da Silva and Fábio Hideki Yamada for their support in monogenetic identification. Additionaly, we acknowledge the contributions of Lucca Vilar Sorrentino and Lucas Pessoa for their role in host collection in the field. Marcylenne Santana de Oliveira and Gilson do Nascimento Melo are also thanked for their assistance with nutrient analysis.
Funding
JMF PhD scholarship was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Financing Code: 001). JMF postdoctoral fellowship was funded by the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) (process number: 0213–00077.01.01/23). VMML PhD scholarship was funded by the Fundação de Apoio à Pesquisa do Estado da Paraíba (FAPESQ/PB) (process number: 54515.922.31759.2109/2022). TPAR Senior Postdoctoral fellowship was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (process number: 102460/2022–1).
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Julia Martini Falkenberg and Ana Carolina Figueiredo Lacerda conceptualized the study and developed the analytical procedure. All authors contributed in the field work. Telton Pedro Anselmo Ramos and Julia Martini Falkenberg provided the map of the study areas. Julia Martini Falkenberg and Vitória Maria Moreira de Lima performed the statistical analyses. Julia Martini Falkenberg wrote the original draft. All authors contributed to the reviewing and editing of the manuscript and approved the final version.
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This research was conducted in accordance with the guidelines and regulations of the Brazilian Law for use of animals for scientific research, including the fish collection license number 56416–1/2016 IBAMA (Brazilian Institute of the Environment and Natural Renewable Resources), and protocol 4928110419 CEUA/UFPB (Committee on Ethics in the Use of Animals of the Universidade Federal da Paraíba). Fishes and parasites were registered in the SisGen (National System of Genetic Resource, Management and Associated Traditional Knowledge), code A9EABE2.
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Falkenberg, J.M., de Lima, V.M.M., Ramos, T.P.A. et al. Drivers of richness and abundance of parasites of fishes from an intermittent river before and after an interbasin water transfer in the Brazilian semi-arid region. Parasitol Res 123, 328 (2024). https://doi.org/10.1007/s00436-024-08332-9
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DOI: https://doi.org/10.1007/s00436-024-08332-9