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Article

Swimming under Pressure: The Sub-Lethal Effects of a Pesticide on the Behaviour of Native and Non-Native Cypriniformes Fish

by
Tamara Leite
*,
Daniel Mameri
,
Paulo Branco
,
Inês Vieira
,
Margarida Oliveira
and
José Maria Santos
Forest Research Centre (CEF), Associate Laboratory TERRA, School of Agriculture, University of Lisbon, Tapada da Ajuda, 1349-017 Lisboa, Portugal
*
Author to whom correspondence should be addressed.
Fishes 2023, 8(9), 462; https://doi.org/10.3390/fishes8090462
Submission received: 7 August 2023 / Revised: 6 September 2023 / Accepted: 12 September 2023 / Published: 15 September 2023
(This article belongs to the Special Issue Behavioral Responses of Fishes to Environmental Stressors)
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Abstract

:
River ecosystems are exposed to a multitude of stressors, including increasing pesticide run-off driven by precipitation and irrigation. Pyrethroids are the fourth major group of insecticides in use worldwide and have extremely negative effects on aquatic fauna. In this study, we aimed to assess the effects of an acute 2 h sub-lethal exposure to different levels of the pyrethroid esfenvalerate on the swimming behaviour of two Cypriniformes species: the native Iberian barbel (Luciobarbus bocagei) and the non-native invasive bleak (Alburnus alburnus). The experimental set-up consisted of previous exposure to three esfenvalerate concentrations (control, 1.2 (low), and 2.0 (high) μg/L) before being stocked in a three-artificial-flume-channel mesocosm for behavioural trials through direct observation. Monitored behaviours included (i) routine activity, (ii) shoal cohesion, and iii) boldness. Significant differences in fish behaviour were detected for the native species (barbel), as individuals spent significantly more time holding position (i.e., resting) in the control (44.9%) than in the high esfenvalerate concentration (25.2%). Concordantly, control barbels were also found to perform more directional changes than the ones exposed to high esfenvalerate concentrations. Behavioural changes were also found for boldness, measured by the proportion of fish attempts to negotiate the upstream ramp, which were significantly higher in the control (37.4%) and in the high concentration (41.5%) compared to the low one (21.1%). Finally, regarding shoal cohesion of the barbel, it was tighter in the control (81.3%) than in the low- (70.5%) and high- (71.1%) esfenvalerate treatments. For the invasive bleak, there were no significant differences in any of the behavioural traits upon previous exposure to an increasing esfenvalerate concentration. This experimental study demonstrated that even short-term exposure to the pyrethroid esfenvalerate was sufficient to alter the behaviour of a native Cypriniformes fish species while not affecting the non-native species. This may confer greater competitive advantages to non-native fish species in the context of global changes.
Keywords:
pesticides; esfenvalerate; activity; boldness; shoaling cohesion; Cypriniformes
Key Contribution: Short-term exposure to the pyrethroids may be enough to impair the behaviour of a native Cypriniformes fish species while not affecting the non-native species. This gives greater competitive advantages to non-native fish species in the context of global changes.

1. Introduction

Freshwater ecosystems provide vital resources and services and are home to a great diversity of fish species, which play a crucial role in maintaining ecological health and balance [1,2]. However, the integrity of these vulnerable systems is increasingly compromised by human activities [3]. The IUCN identified “Invasive Non-Native/Non-native Species/Diseases” (33.6% of evaluated European freshwater fish species are threatened by this threat) and pollution from “Agricultural & Forestry Effluents” (24.4%) as major threats affecting European freshwater fish species, half of which are from the Cyprinidae family [4,5].
Pyrethroids are pesticides used in agriculture and urban areas to kill or control harmful insect pests [6]. The use of this type of pesticide has increased over the past decades due to its broad-spectrum effects and low toxicity to mammals and birds [7], and it is now the fourth major group of insecticides in use worldwide [8]. Esfenvalerate is one of the most commonly used pyrethroid insecticides in agriculture [9,10]. These types of organic residual pesticides can leach and enter aquatic environments through direct application or run-off [11,12]. Environmental analysis has shown that esfenvalerate concentrations in freshwater systems can amount to up to 0.76 μg/L [13,14,15]. Water contamination of this sort poses an environmental threat since the elimination rate of pyrethroids in aquatic organisms is low, and esfenvalerate has been found to have toxic effects on a wide range of aquatic organisms, particularly fish [6,16]. Exposure to esfenvalerate can cause a range of neurological, physiological, and genetic damage in fish and has been shown to accumulate in fish tissues [17,18,19]. Nonetheless, while measured concentrations of esfenvalerate are often below acute toxic levels for aquatic organisms, potential sub-lethal effects resulting in energy reallocation or behavioural and swimming activity abnormalities should be of concern because they can compromise the ecological fitness of species and ultimately may contribute to altering food webs and ecosystem dynamics [20,21]. However, addressing sub-lethal effects in the wild is very difficult, either because species require continuous behavioural observations or because affected individuals may not survive therein.
Another major global threat to freshwater fish species is the wide expansion of non-native species, especially in the Mediterranean region [4,22,23]. When such species establish self-sustaining populations, spread to new environments, and negatively interact with native species, they become invasive, leading to the decline of native fish populations, compromising the structure and dynamics of freshwater ecosystems [24], as they outcompete native species for habitat and resources [25,26]. In addition, the impacts of these pressures on freshwater fish species will be amplified by climate change and other interacting stressors present in the environment [27,28,29,30,31]. Thus, it is essential to understand the toxicological effects of sub-lethal exposure to pyrethroids on native and non-native species at an individual scale since it might potentially lead to effects on the health of fish populations [32].
Overall activity (i.e., resting, searching, and fleeing) is a significant and commonly evaluated trait in fish behavioural studies and is often related to foraging and growth [33,34]. Boldness (i.e., the tendency to leave a refuge and explore an unknown exposed environment) is another significant behavioural trait observed in fish [35,36] and is linked to responses to stimuli [37,38], predator inspection in school leaders, and predator evasion [39,40], dispersion [41,42,43], and activity [44,45,46]. Shoaling cohesion and other social behaviours are known to affect the survival of fish living in groups [47,48] by improving threat perceptions [49,50] and reducing individual risks and physical costs of movement [51,52,53]. Aggregation has other benefits, such as improved foraging efficiency [54], predator encounter dilution, and predator confusion [55,56,57]. Therefore, monitoring fish behaviour can be an incredibly relevant tool to link the impairment of individual behavioural responses to species interactions and population processes as a result of esfenvalerate exposure [12,21,32,58,59].
This paper aims to evaluate the effects of the pyrethroid pesticide esfenvalerate on freshwater fish species’ behaviour, specifically the native Iberian barbel Luciobarbus bocagei (Steindachner, 1864) and the non-native bleak Alburnus alburnus (Linnaeus, 1758). The behaviour parameters observed included routine activity, boldness, and shoaling cohesion. The research on these Cypriniformes species focused on the sub-lethal impacts of toxicity caused by pesticides and the potential ecological consequences esfenvalerate might have in freshwater wild fish communities, which could help recognize the implications for the management and conservation of the vulnerable aquatic ecosystems. Specifically, we expect that exposure to increasing concentrations of esfenvalerate will (a) reduce activity in both fish species, (b) reduce shoal cohesion in both species, (c) reduce boldness in both species, and (d) the effects will be more pronounced in the native fish species than in the non-native.

2. Materials and Methods

2.1. Pyrethroid Insecticide

In this study, we used esfenvalerate, a broad-spectrum nonselective pyrethroid insecticide, commercially acquired as Flower’s SUMIFIVE® PLUS as an oil in water emulsion (15 mL volume, formulated based on a combination of esfenvalerate 5% concentration, phenylethyl-xylene isomers, and ethyl phenylethyl-, i.e., 50 g/L, concentration). The use of pyrethroid insecticides has been increasing in the past decades [60] due to their generally low half-life periods and, consequently, low persistence in the environment. Specifically, for esfenvalerate, experiments revealed that its half-life period could range from 7.8 to 100 days in soil exposed to sunlight and 150.0 to 553.4 days in dark soil [61]. Some studies suggest that exposure to esfenvalerate can affect fish hatching and larvae viability [9], while others revealed changes in swimming behaviour in Atherinopsidae [32] and osmerids [20]. Other effects of this pyrethroid were also reported, including increased vulnerability to predation in the fathead minnow Pimephales promelas [62] and increased mortality in rainbow trout larvae Oncorhynchus mykiss [10].

2.2. Target Species and Life Stages

Representatives of native and non-native Cypriniformes were chosen for the present study: the native Iberian barbel Luciobarbus bocagei (Steindachner, 1864) (henceforth barbel), a cyprinid species endemic to the Iberian Peninsula, with a “Least Concern” status and a widespread distribution in Portuguese rivers [63], and the non-native bleak Alburnus alburnus (Linnaeus, 1758), recently reclassified into the Leuciscidae family [64]. The barbel is a medium-sized species with a bottom trophic strategy; it mostly inhabits lotic environments but has the ability to live in reservoirs. The bleak is an invasive opportunist that feeds mostly on zooplankton and algae but occasionally eats fish larvae [65]. It inhabits preferably lentic environments but can spread across river networks and occupy lotic ones. It is known to hybridize with native species from the Squalius genus. A previous assessment by Miranda et al. [66] revealed that the maximum size attained by bleak did not surpass 151 mm (total length), while Masó et al. [67] reported juvenile bleak with total lengths ranging from 48 to 100 mm, sizes that can be attained by juvenile barbels [66,67,68]. Therefore, to allow for comparisons between the two species, and as both taxa do not overlap in their size range concerning specific life stages (e.g., juveniles, adults), the life stages that were used in this study included juvenile barbels and adult bleaks due to their comparable sizes and frequency of occurrence in Iberian streams. The former has been recently studied in the mesocosm facility at the School of Agriculture campus [69,70,71].

2.3. Fish Sampling and Holding Facilities

Fish sampling took place in May 2021 during two sampling events (each targeted for a different species) where a total of 36 native barbel Luciobarbus bocagei (Steindachner, 1864) and 36 non-native bleak Alburnus alburnus (Linnaeus, 1758) were captured in Rivers Lizandro (barbel) and Sor (bleak) (Central Portugal), respectively. For both sampling events, a 150 m long river stretch was chosen based on habitat representativeness and accessibility. Electrofishing was carried out by means of wadable electrofishing (Hans Grassl IG-200, Schönau am Königsee, Germany), moving upstream in a zig-zag manner, following the recommendations of the European Committee of Standardization (CEN, 2003). After being sampled, fish were transported to the campus of the School of Agriculture (ISA), University of Lisbon, in a fish transport box (Hans Grassl, 190 L) filled with river water from the rivers from which fish were sampled. The box also featured a portable aeration device (ELITE, KG HAGEN Deutschland GmbH & Co., Holm, Germany) to reduce transportation stress.
At the ISA campus, individuals were kept for 48 h in a quarantine tank (800 L) featuring a High-performance Cannister Filter FX5 (Fluval, Baie-d’Urfé, QC, Canada) and PVC tubes to promote shelter for fish and hence reduce stress [71,72]. Nutrafin Aqua+ was added immediately before fish were placed in the tank to create a suitable biological media with bacteria and reduce ammonia and nitrate levels resulting from fish waste. Fish feeding (TetraPond sticks) was interrupted 24 h prior to behavioural trials. Water quality (temperature, pH, and dissolved oxygen (DO)) in the acclimation tank was monitored daily with a multiparametric probe (HANNA, HI 9812-5).

2.4. Mesocosm Facility

The effects of esfenvalerate on fish swimming behaviour were assessed in the mesocosm facility located at the campus of the School of Agriculture, University of Lisbon, Portugal. Mesocosms are outdoor experimental systems that allow studying the natural environment under controlled conditions, avoiding the interference of confounding factors and incorporating natural variations (photoperiod and air temperature, for instance), hence providing a link between field surveys and highly controlled laboratory experiments [69,70].
The present mesocosm facility consisted of a set of 3 tinplate-lined outdoor artificial flume channels, 0.4 m wide, 4 m long, and 0.2 m deep (Figure 1a, II and III). Each flume channel was separated from an upstream tank (70 L, Figure 1a, V) by a 47 cm long and 36 cm high ramp at a slope of 50% (Figure 1a, IV) and delimited downstream (Figure 1a, II) by a fixed mesh panel to prevent fish from dropping out of the channel. Water distribution and recirculation were achieved with a PEAD pipe system that allowed water to run from the supply tank to the upstream ones, main channels, and to 70 L downstream tanks (Figure 1a, I). The downstream tanks were connected to pumps (Kripsol OK-71 B, 0.56 kW), operating in a recirculation flow system towards the upstream tanks, allowing upholding water conditions independently of the source tank.

2.5. Experimental Set-Up

After quarantine, fish were randomly selected into groups of 4 individuals and transferred to 50 L tanks, with natural light conditions and featuring stones for shelter to avoid stress. In these tanks, fish were exposed for 2 h to three different esfenvalerate concentrations: 0.0 μg/L (control, without the insecticide), 1.2 μg/L (low concentration), and 2.0 μg/L (high concentration) (Table 1). It should be noted that while there are no reference levels of esfenvalerate for surface water bodies in the European Union, a previous study by Floyd et al. [62] determined the effects of a short-time exposure (4 h) of low levels of esfenvalerate (ranging from 0.455 to 1.142 μg/L) in the swimming behaviour of larval fathead minnows Pimephales promelas. Similarly, in a study by DeMicco et al. [18], a concentration of either 1 μg/L deltamethrin or cypermethrin for a 6-day period post-hatching induced body spasms and uncontrolled swimming in young zebrafish Danio rerio. Considering that juvenile (and not larval) individuals were used in this study and that the period of exposure to the pyrethroid (2 h) was shorter than in previous studies using pyrethroid concentrations up to 1 μg/L [18,20,32,61], a concentration of 2.0 μg/L was adopted as the high-concentration treatment, with 1.2 μg/L being selected as the midpoint (and approximately half of the highest value) of the gradient and 0.0 μg/L as the control (no esfenvalerate). Water quality was checked with a multiparametric probe (HANNA, HI 9812-5). Each one of the 3 experimental groups had 3 replicates, with a total of 9 behavioural trials per species.
After being exposed to each treatment, fish were transferred to the flume channels, allowing us to assess the behavioural traits in the three different treatment groups (control, low and high esfenvalerate concentrations). All behavioural trials were performed under similar weather conditions. Replicates were conducted, with these involving a school of 4 wild-caught fish of each species in the experimental unit (number of replicates = 3 schools of 4 fish per treatment, totalling 12 fish per treatment, and 72 fish overall). Following an initial acclimation period of 10 min at the lowermost section of the channels, delimited by a removable net (Figure 1a, section II, 1b), fish were allowed to move freely in the channels (Figure 1c) or attempt to negotiate the ramp (Figure 1d). Each observer (one per channel) stood still at an approximate distance of 0.5 m downstream of each channel, with a full view of it, approaching and leaving the observation points discreetly whenever necessary. This procedure was followed in previous experiments in this mesocosm facility with barbels and was considered adequate since no changes in fish behaviour were noted [69,71,73].
Monitored behavioural traits included the following: (1) activity (ecologically relevant for looking for shelter and feeding, for instance [34]), classified as “resting” (holding position), “searching”, “fleeing”, or “directional changes” (90° change in swimming direction); (2) boldness, equivalent to the total counts of fish that actively attempted to negotiate the ramp (Figure 1d), based on the idea that a novel environment is considered dangerous and suggests willingness to undertake risks [33]; and (3) shoaling cohesion, given by the ratio of the number of fish in the flume (Figure 1a, II and III) that were within one body length of each other [74]), divided by the total number of fish in the flume, excluding the ones in the upstream tank [73]. Trials lasted one hour each and consisted of the instantaneous sampling of the behavioural traits every 3 min (with the exception of boldness, which was recorded continuously). Fish were only tested once, and after each trial, they were removed from the channels, measured (TL, to the nearest mm), and later released at their previous capture locations (barbel), except for the non-native bleak, which were not returned to the river and later euthanized with an overdose of benzocaine.

2.6. Data Analyses

Data normality and homoscedasticity were tested using the Shapiro–Wilk test and F-test of variances, respectively. Both activity and boldness data were fitted into generalized linear models (GLM) with a Poisson distribution (considering the absolute frequencies of each of these behavioural traits), with treatment (esfenvalerate concentration) as a predictor. Shoaling cohesion between treatments was compared using the non-parametric Kruskal–Wallis test, followed by the Dunn post hoc test. All analyses were conducted in R (version 4.1.0).

3. Results

Regarding fish activity, “searching” was the most observed trait in both species, representing between 54 and 63% and 59 and 60% of all activity traits observed in the barbel and bleak, respectively, while fleeing was the least observed, accounting for 2% for both barbel and bleak (Figure 2). No significant differences between treatments were observed for the bleak for any of the traits: resting (β = −0.099, z = −0.312, p = 0.755); searching (β = −0.149, z = −1.307, p = 0.191); fleeing (β = 17.21, z = 0.005, p = 0.996); and directional changes (β = −0.475, z = −1.790, p = 0.074) (Figure 2). While “searching” and “fleeing” did not significantly differ between treatments in the barbel, the observed frequency of the two remaining activity traits significantly differed between the control and high concentration of esfenvalerate for “resting”: (β = −0.684, z = −1.073, p < 0.01) and “directional changes” (β = −2.080, z = −3.396, p < 0.01).
Concerning boldness, mean observed frequencies ranged between 21 and 42% in the barbel and 32 and 35% in the bleak (Figure 3). Significant differences were found for the barbel exposed to the low-esfenvalerate-concentration treatment regarding both the control (β = −0.522, z = −3.531, p < 0.01) and high-concentration treatments (β = −0.679, z = −4.728, p < 0.01), with the low concentration of esfenvalerate fish showing fewer attempts to pass the ramp (Figure 2). Similar to the activity traits, no significant differences in boldness were observed for the bleak (β = 0.049, z = 0.312, p = 0.755) (Figure 3).
Overall, shoaling cohesion was lower in barbel (0.74 ± 0.22) when compared to the bleak (0.93 ± 0.15) (Figure 4). The barbel showed significant differences in shoal cohesion among treatments (χ2 = 7.185, df = 2, p = 0.028), specifically between the control (0.813 ± 0.207) and both low (0.705 ± 0.213; p < 0.01, Dunn post hoc) and high esfenvalerate concentrations (0.711 ± 0.211; p = 0.014, Dunn post hoc). For the bleak, there were no significant differences in shoal cohesion between the control (0.938 ± 0.142), low (0.958 ± 0.104), and high (0.896 ± 0.184) concentrations (χ2 = 3.493, df = 2, p = 0.174).

4. Discussion

Emergent stressors in rivers, such as pesticide exposure, potentiate existing threats to native aquatic fauna [6,75], which can be manifested not only in terms of direct effects, such as mortality, but also through sub-lethal effects when concentrations are below threshold values. These disturbances might have an immediate, medium-, or long-term effect on individuals and ultimately on population viability, and some effects can be measured as behavioural changes. Esfenvalerate is a synthetic pyrethroid insecticide commonly used in agriculture [8,20] and is especially toxic to fish, even at lower concentrations [12,32]. This pesticide is known to cause adverse biochemical responses in organisms by blocking sodium and potassium channels, resulting in neurological damage [19]. Sub-lethal effects include reduced growth, reproductive success [76], and erratic swimming behaviour [21,77], thereby compromising the survival of aquatic species [59,62,78]. Understanding these sub-lethal effects in river systems where non-native species are also present is essential to evaluate the response of both native and non-native species, thus determining if any competitive advantage can result from different performances in native and non-native species after pesticide exposure [20]. Moreover, climate change is expected to intensify current threats to freshwater ecosystems [79], such as increasing temperatures [80,81], pollution [4,82], salinization [83,84,85], and the pressures of non-native and invasive species on native fish communities [29,86,87,88]. This work aimed to understand the behavioural effects of the three concentrations of the pyrethroid insecticide esfenvalerate on the native barbel (Luciobarbus bocagei) and the non-native invasive bleak (Alburnus alburnus) by studying routine activity, boldness, and shoaling behaviour of the fish.
The swimming behaviour of the barbel differed with different levels of esfenvalerate upon prior exposure to this pesticide. Specifically, concerning activity, the frequency of resting fish was higher in the high-esfenvalerate-exposed groups than in the control ones; concomitantly, the percentage of fish performing directional changes was lower in the high-esfenvalerate treatment as opposed to the control. These changes suggest that barbel activity is, in general, lower when exposed to higher concentrations of esfenvalerate. Similar results were found in other studies where swimming abnormalities and other significant effects on motion activity have been detected in larval fathead minnows after 4 h of exposure [20] and in juvenile bluegill after pulse exposure to 0.025 μg/L of esfenvalerate [89].
Regarding boldness, measured by the number of attempts to negotiate the ramp, significant differences were also observed for the barbel, with less bold behaviour in the low-esfenvalerate treatment than in the control and high-esfenvalerate fish groups. These results partially agree with our initial expectations of boldness reduction in fish previously exposed to a stressor when compared to control groups. This has been shown in previous experimental studies with the barbel ((wildfire ashes, heatwaves, and salinity) [69,71,73]). However, a subsequent increase in the proportion of bolder individuals in response to a higher esfenvalerate concentration (from 1.0 to 2.0 μg/L) was unexpected, as previous studies with the same species have reported that individuals decreased their bolder character and become shyer upon previous exposure to a higher concentration of stressors, such as fire ashes [69] or salinity [70]. In the present study, shy behaviour peaked at the intermediate value of the esfenvalerate concentration gradient, being minimal at both extremes, i.e., at the control (no stressor), when fish are expected to display a naturally bolder behaviour, venturing and exploring new habitats for spawning, feeding, or sheltering purposes) and at the highest concentration, when it is expected that most fish adopt a bolder, more erratic behaviour after exposure to a harmful esfenvalerate environment [90]. However, this deserves further clarification with longer-term experiments and extending the gradient of insecticide concentration. The shoaling behaviour of the barbel was significantly affected by both treatments with low and high concentrations of the stressor. This response was to be expected since previous studies with cyprinids demonstrated great effects on group behaviour caused by anthropogenic pressures; for example, when exposed to increasing salinity levels, barbel shoals were less active and more dispersed [73]. Under stressful conditions, as simulated in these experiments, barbels tended to separate from the group, as individual boldness increased in the higher concentration treatment and searched for a more favourable environment [91,92]. Individual variation in schooling and boldness behaviour may influence the dispersal of species and consequently affect spatial population dynamics [93,94,95]. Oppositely, it should be noted that the bleak’s overall behaviour seemed to be unaltered by higher concentrations of esfenvalerate. Considering searching behaviour, we could graphically observe a slight upward tendency of this swimming pattern with increasing pyrethroid concentrations inversely to the barbel’s observed behaviour. Likewise, exposure to a high concentration of insecticide showed no significant effects on the bleak’s boldness and shoaling cohesion throughout behavioural trials.
Less active and less bold fish may not be as prone to migrate in search of new habitats for refuge, feeding, and reproduction [39,96,97]. Furthermore, following exposure to esfenvalerate, less active species may lose competitive advantage to others that are not affected (or less affected) by this stressor. The bleak is a non-native species that can occur in sympatry and compete for resources with native Cypriniformes species (e.g., with the saramugo Anaecypris hispanica: [98]). The competitive disadvantage of native fish species in comparison to the bleak (and other non-native species) may be further potentiated in the face of other stressors, such as flow regulation, which can benefit non-native species with higher ecological plasticity [99].
Esfenvalerate and other pesticides are neurotoxic to fishes, and their effects on behaviour are rarely investigated relative to sub-lethal endpoints [32]. Thus, pesticides in aquatic systems are a threat to biodiversity, as impacts can cascade from individuals to populations [21,100]. Insecticides can modify food web dynamics [20] and community structure [101,102] by creating a more advantageous environment for more tolerant species, hence compromising the ability of more sensitive species to compete, deal with invasive species, or other vital behaviours, for example [103,104,105]. The barbel and other species living in seasonally harsh environmental conditions, as in Mediterranean rivers, are particularly known for their resilience to various stressors [106,107,108]; this would grant native species a competitive advantage in relation to non-natives. However, fish have different tolerances to different kinds of stressors [109,110], and the apparent tolerance, demonstrated by bleak and the impact demonstrated for barbels, clearly promotes a shift in the competitive balance between the species, favouring the non-native. In the wake of global changes, with the increasing temperatures and agriculture pressure due to climate change and human population growth, the potential effect of pesticides will be augmented by the increase in usage and a magnification effect of the concentration of pesticides in rivers under water scarcity swell.
Ultimately, behavioural impairment in fish can reflect alterations in ecological conditions and ecosystem dynamics. Thus, the behavioural responses of fish caused by exposure to pollutants such as esfenvalerate should be further researched, in addition to the interaction with other environmental stressors, to understand the true scope of the consequences of pesticide contamination for fish species. Maintaining well-structured native riparian galleries, as well as encouraging their restoration or rehabilitation when they are degraded, may, in the future, constitute an effective management measure that will certainly reduce, through filtration, the impacts arising from the increase of these substances in riverine ecosystems [111].

5. Conclusions

In this work, the swimming behaviour of a native and a non-native invasive species was assessed under mesocosms conditions, following a previous 2 h sub-lethal exposure to a concentration gradient of a widespread pyrethroid esfenvalerate. Results showed that short-term previous exposure to the pyrethroid esfenvalerate was able to significantly affect the behaviour of the native species (barbel), mainly by increasing the amount of time resting while decreasing the shoaling cohesion and boldness partially. Contrarily, no significant changes in behavioural metrics to increasing amounts of esfenvalerate were detected for the non-native invasive species (bleak). As less active and shier fish may be less prone to migrate in search of new habitats for refuge, feeding, or reproduction [39], the present findings suggest that common native species, such as the barbel, may lose competitive advantages towards other fishes that are not affected (or are less affected) by the presence of esfenvalerate. This work contributed to improving the knowledge regarding esfenvalerate effects in freshwater fish, thus providing an enhanced understanding of the effects of this pyrethroid insecticide on organisms and consequent effects at the population and ecosystem levels. Future studies should consider testing the effects of other stressors that naturally co-occur with pesticide contaminations (e.g., hypersaline conditions, warming temperatures, decreased habitat availability) to understand if their interactions have additive, antagonistic, or synergistic effects and whether they intensify the effects of pesticides in isolation. The fact that exposure to the chosen concentrations of esfenvalerate did not affect the behaviour of the non-native invasive bleak reinforces the need to further understand the tolerance of such species to this type of disturbance and to create measures that restrict the application of pesticides, which might give them competitive advantages as outlined above.

Author Contributions

T.L.: methodology, investigation, and writing—original draft; D.M.: formal analysis, data curation, and writing—original draft; I.V.: methodology, investigation, and writing—review and editing; M.O.: methodology, investigation, and writing—review and editing; P.B.: supervision, methodology, investigation, and writing—review and editing; J.M.S.: supervision, conceptualization, methodology, investigation, and writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

Tamara Leite was supported by a Ph.D. grant from the FLUVIO–River Restoration and Management program funded by Fundação para a Ciência e a Tecnologia I. P. (FCT), Portugal (UI/BD/15052/2021). Daniel Mameri was supported by a Ph.D. scholarship from the FLUVIO—River Restoration and Management program funded by Fundação para a Ciência e a Tecnologia I.P. (FCT) (PD/BD/142885/2018). Paulo Branco was financed by national funds via FCT (LA/P/0092/2020). The study was partially funded by the project Dammed Fish (PTDC/CTA-AMB/4086/2021). Forest Research Centre (CEF) is a research unit funded by Fundação para a Ciência e a Tecnologia I.P. (FCT), Portugal (UIDB/00239/2020). The Associate Laboratory TERRA (LA/P/0092/2020) is also funded by FCT.

Institutional Review Board Statement

All proceedings involving fish sampling and handling strictly complied with the European standards (Directive 2010/63/EU) and Portuguese legislation (Decree-Law 113/7 August 2013, article 35, no. 5, transposing the European Directive for animal experimentation (Directive 2010/63/EU)). Licenses for capture, transportation, detention, and handling (no. 299/2021/CAPT and 300/2021/CAPT), as well the fishing permits (no. 38-A/2021 and no. 39/2021), were issued by the Portuguese Institute for Nature Conservation and Forests (ICNF). Fish handling and experimentation were coordinated by J. M. Santos, who holds a FELASA C certification to perform animal experimentation. All procedures were adopted to minimize fish distress.

Data Availability Statement

The data presented in this study is available upon request from the corresponding author. The data are not publicly available due to potential use in future works.

Acknowledgments

The authors would like to thank the Institute for Nature Conservation and Forests (ICNF), which provided the necessary fishing and handling permits.

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

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Figure 1. Scheme of the experimental set-up in the mesocosm facility. (a) Sections composing each flume channel, operating in a recirculating system: I—downstream tank; II—acclimation section; III—flume channel; IV—ramp; V upstream tank; VI—pump Kripsol OK-71 B, 0.56 kW; VII—holding tank. (b) Acclimation phase lasting 10 min, with fish being kept in the lowermost section of each channel delimited upstream by a net; (c) free movement of the fish during 1 h trials, with one observer per channel; (d) attempts to negotiate the ramp (boldness).
Figure 1. Scheme of the experimental set-up in the mesocosm facility. (a) Sections composing each flume channel, operating in a recirculating system: I—downstream tank; II—acclimation section; III—flume channel; IV—ramp; V upstream tank; VI—pump Kripsol OK-71 B, 0.56 kW; VII—holding tank. (b) Acclimation phase lasting 10 min, with fish being kept in the lowermost section of each channel delimited upstream by a net; (c) free movement of the fish during 1 h trials, with one observer per channel; (d) attempts to negotiate the ramp (boldness).
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Figure 2. Relative frequency (%) of activity traits (resting, searching, fleeing, and directional changes) displayed in the barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus) for each concentration of esfenvalerate: control (0.0 μg/L, white fill), low (1.2 μg/L, light grey), and high (2.0 μg/L, dark grey). For each activity trait, significant differences (GLM Poisson, p < 0.05) between treatments are expressed by different letters (“a”, “b”); when treatments “share” the same letter, there are no statistical differences.
Figure 2. Relative frequency (%) of activity traits (resting, searching, fleeing, and directional changes) displayed in the barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus) for each concentration of esfenvalerate: control (0.0 μg/L, white fill), low (1.2 μg/L, light grey), and high (2.0 μg/L, dark grey). For each activity trait, significant differences (GLM Poisson, p < 0.05) between treatments are expressed by different letters (“a”, “b”); when treatments “share” the same letter, there are no statistical differences.
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Figure 3. Relative frequency (%) of boldness (measured as the number of attempts made by barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus) to overcome the ramp in the flume channels) for each concentration of esfenvalerate: control (0.0 μg/L, light grey), low (1.2 μg/L, dark grey), and high (2.0 μg/L, black). Significant differences (GLM Poisson, p < 0.05) between treatments are expressed by different letters (“a” and “b”); when treatments “share” the same letter, there are no statistical differences.
Figure 3. Relative frequency (%) of boldness (measured as the number of attempts made by barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus) to overcome the ramp in the flume channels) for each concentration of esfenvalerate: control (0.0 μg/L, light grey), low (1.2 μg/L, dark grey), and high (2.0 μg/L, black). Significant differences (GLM Poisson, p < 0.05) between treatments are expressed by different letters (“a” and “b”); when treatments “share” the same letter, there are no statistical differences.
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Figure 4. Shoaling cohesion index for the barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus), for each concentration of esfenvalerate: control (0.0 μg/L, white fill), low (1.2 μg/L, light grey), and high (2.0 μg/L, dark grey). Mean values and medians are represented by “×” and bold lines, respectively. For each activity trait, significant differences (Kruskal–Wallis followed by Dunn post hoc for pairwise comparisons, p < 0.05) between treatments are expressed by different letters (“a” and “b”); when treatments “share” the same letter, there are no statistical differences.
Figure 4. Shoaling cohesion index for the barbel (Luciobarbus bocagei) and bleak (Alburnus alburnus), for each concentration of esfenvalerate: control (0.0 μg/L, white fill), low (1.2 μg/L, light grey), and high (2.0 μg/L, dark grey). Mean values and medians are represented by “×” and bold lines, respectively. For each activity trait, significant differences (Kruskal–Wallis followed by Dunn post hoc for pairwise comparisons, p < 0.05) between treatments are expressed by different letters (“a” and “b”); when treatments “share” the same letter, there are no statistical differences.
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Table 1. Fish length (TL, mm) and body mass (g) measured at the end of each trial, and physical-chemical parameters, including water temperature (°C), pH, and conductivity (mS/cm), for each of the esfenvalerate treatments administrated (control, low, and high) within each tested species (barbel and bleak) measured prior to the trials in the flume channels. Water quality was checked with a multiparametric probe (HANNA, HI 9812-5). Values shown are averages ± standard deviation.
Table 1. Fish length (TL, mm) and body mass (g) measured at the end of each trial, and physical-chemical parameters, including water temperature (°C), pH, and conductivity (mS/cm), for each of the esfenvalerate treatments administrated (control, low, and high) within each tested species (barbel and bleak) measured prior to the trials in the flume channels. Water quality was checked with a multiparametric probe (HANNA, HI 9812-5). Values shown are averages ± standard deviation.
ParameterControl (0.0 μg/L)Low (1.2 μg/L)High (2.0 μg/L)
Barbel (Luciobarbus bocagei)
Fish length (TL, mm)145.3 ± 17.1138.8 ± 21.3146.0 ± 14.8
Fish body mass (g)29.81 ±11.5128.33 ±9.3630.75 ± 9.22
Water temperature (°C)17.37 ± 0.2117.37 ± 0.0617.57 ± 0.06
pH7.92 ± 0.117.79 ± 0.337.96 ± 0.06
Conductivity (mS/cm)0.86 ± 0.100.86 ± 0.080.80 ± 0.02
Bleak (Alburnus alburnus)
Fish length (TL, mm)132.3 ± 11.6126.3 ± 10.2128.6 ± 12.8
Fish body mass (g)15.00 ± 3.9514.08 ± 3.4214.58 ± 3.85
Water temperature (°C)18.43 ± 0.7218.43 ± 0.6718.63 ± 0.85
pH7.93 ± 0.037.93 ± 0.037.93 ± 0.02
Conductivity (mS/cm)0.81 ± 0.010.81 ± 0.000.82 ± 0.02
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MDPI and ACS Style

Leite, T.; Mameri, D.; Branco, P.; Vieira, I.; Oliveira, M.; Santos, J.M. Swimming under Pressure: The Sub-Lethal Effects of a Pesticide on the Behaviour of Native and Non-Native Cypriniformes Fish. Fishes 2023, 8, 462. https://doi.org/10.3390/fishes8090462

AMA Style

Leite T, Mameri D, Branco P, Vieira I, Oliveira M, Santos JM. Swimming under Pressure: The Sub-Lethal Effects of a Pesticide on the Behaviour of Native and Non-Native Cypriniformes Fish. Fishes. 2023; 8(9):462. https://doi.org/10.3390/fishes8090462

Chicago/Turabian Style

Leite, Tamara, Daniel Mameri, Paulo Branco, Inês Vieira, Margarida Oliveira, and José Maria Santos. 2023. "Swimming under Pressure: The Sub-Lethal Effects of a Pesticide on the Behaviour of Native and Non-Native Cypriniformes Fish" Fishes 8, no. 9: 462. https://doi.org/10.3390/fishes8090462

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