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Results of analyses of variance on tadpole activity before and after predator cue additions

Results of analyses of variance on tadpole activity before and after predator cue additions

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The ability to detect chemical cues is often critical for freshwater organisms to avoid predation and find food and mates. In particular, reduced activity and avoidance of chemical cues signaling predation risk are generally adaptive behaviors that reduce prey encounter rates with predators. Here, we examined the effects of the common herbicide atr...

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Context 1
... tadpole avoidance of the predator cue seemed to last for approximately as long as the cue gradient persisted. Before any predator cues were added, tadpoles exposed to atrazine were significantly more active than tadpoles exposed to solvent control (F 1,67 ¼ 7.84, p ¼ 0.007; Figure 1B); but activity levels did not differ significantly between tadpoles assigned to receive predator cue or not (Table 2). After the predator cue was introduced, tadpoles exposed to atrazine remained significantly more active than tadpoles exposed to solvent control (F 1,67 ¼ 7.13, p ¼ 0.009; Figure 1B). ...
Context 2
... tadpoles, however, did not significantly reduce their activity in response to the predator cue ( Figure 1C) but did tend to exhibit less activity later than earlier in the trial (F 3,201 ¼ 4.45, p ¼ 0.005; Figure 1C). There were no significant statistical interactions on tadpole activity (Table 2). ...

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... In the 100 mg/L treatment, tadpoles moved significantly more without predator cues, which is the expected result if ammonium nitrate has no effect on the sensory system of the toads. The lack of significance in the rest of the treatments, however, could be due to the fact that as a result of the ammonium nitrate tadpoles could not detect the presence of predator cues in the water and exhibited no difference in behavior, which has been demonstrated in previous studies that exposed tadpoles to chemicals in the water [36]. For the Control treatment, we can argue that, as with R. dalmatina, these are the largest tadpoles in and as such have no significant decrease in movement due to predator cue detection. ...
... Freshwater organisms specially rely on chemical communication for their survival and most of their behaviors. ATR compromises the olfactory abilities of amphibians and fish, affecting their behavior, impairing detection of food source odors, possible mates, and predators, altering their physiology, growth, survival, and reproduction (Ehrsam et al., 2016;Tierney et al., 2007;Moore and Waring, 1998;Moore and Lower, 2001;Hussein et al., 1996;Belanger et al., 2016). For instance, in the Cuban tree frog tadpoles ATR exposure impairs the detection of chemical cues of predators (Ehrsam et al., 2016). ...
... ATR compromises the olfactory abilities of amphibians and fish, affecting their behavior, impairing detection of food source odors, possible mates, and predators, altering their physiology, growth, survival, and reproduction (Ehrsam et al., 2016;Tierney et al., 2007;Moore and Waring, 1998;Moore and Lower, 2001;Hussein et al., 1996;Belanger et al., 2016). For instance, in the Cuban tree frog tadpoles ATR exposure impairs the detection of chemical cues of predators (Ehrsam et al., 2016). In salmons, ATR exposure decreases the response of the male to reproductive hormones released in the urine of female salmon, promoting adverse effects on imprinting, homing, and migratory behaviors (Moore and Waring, 1998;Moore and Lower, 2001). ...
... Also, pesticides may enter the body via the digestive tract and initiate synucleinopathy in the gut, which may later spread to the brain (Braak et al., 2006). Several studies evaluating the toxicity of ATR exposure on olfaction have been performed on vertebrates, such as fish, crayfish, and frogs (Ehrsam et al., 2016;Tierney et al., 2007;Moore and Waring, 1998;Moore and Lower, 2001;Hussein et al., 1996;Belanger et al., 2016). In fish, low-level exposure to ATR changes the electrical response within the olfactory epithelium, measured by electro-olfactogram, and impairs the olfactory preference/avoidance to some amino acids (Tierney et al., 2007). ...
... ATZ as an endocrine disruptor has also been shown to cause sex specific behavioral outcomes in various model organisms. A study in tadpoles observed hyperactivity in ATZ exposed tadpoles, and these tadpoles were also less likely to avoid predatory chemical cues (Ehrsam et al. 2016). A gestational ATZ exposure in C57BL/6 mice found dams had decreased novel object recognition and displayed hyperactivity, while juvenile offspring were hyperactive with an increase in anxiety-like behavior (Lin et al. 2014). ...
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Atrazine (ATZ) is an herbicide commonly used on crops in the Midwestern US and other select global regions. The US Environmental Protection Agency ATZ regulatory limit is 3 parts per billion (ppb; μg/L), but this limit is often exceeded. ATZ has a long half-life, is a common contaminant of drinking water sources, and is indicated as an endocrine disrupting chemical in multiple species. The zebrafish was used to test the hypothesis that an embryonic parental ATZ exposure alters protein levels leading to modifications in morphology and behavior in developing progeny. Zebrafish embryos (F1) were collected from adults (F0) exposed to 0, 0.3, 3, or 30 ppb ATZ during embryogenesis. Differential proteomics, morphology, and behavior assays were completed with offspring aged 120 or 144 h with no additional chemical treatment. Proteomic analysis identified differential expression of proteins associated with neurological development and disease; and organ and organismal morphology, development, and injury, specifically the skeletomuscular system. Head length and ratio of head length to total length was significantly increased in the F1 of 0.3 and 30 ppb ATZ groups (p < 0.05). Based on molecular pathway alterations, further craniofacial morphology assessment found decreased distance for cartilaginous structures, decreased surface area and distance between saccular otoliths, and a more posteriorly positioned notochord (p < 0.05), indicating delayed ossification and skeletal growth. The visual motor response assay showed hyperactivity in progeny of the 30 ppb treatment group for distance moved and of the 0.3 and 30 ppb treatment groups for time spent moving (p < 0.05). Due to the changes in saccular otoliths, an acoustic startle assay was completed and showed decreased response in the 0.3 and 30 ppb treatments (p < 0.05). These findings suggest that a single embryonic parental exposure alters cellular pathways in their progeny that lead to perturbations in craniofacial development and behavior.
... Given this disparity in results, we would recommend that further study is needed to investigate the effects of 17β-trenbolone on amphibian behaviour before we can make any definitive conclusions about the impacts of this pollutant on amphibians, more generally. However, whilst literature investigating the effects of 17β-trenbolone on tadpole behaviour is scarce, other studies have, in agreement with the present study, found that tadpoles exposed to chemical pollutants (including EDCs) can exhibit higher levels of activity, and following a predator threat, reduce activity and swimming speed (Ehrsam et al., 2016;Gabor et al., 2019;Rohr and McCoy, 2010;Sievers et al., 2018b). The differences between our present and previous study (Orford et al., 2022) could therefore be due to species-specific responses to chemical exposure. ...
Article
Endocrine-disrupting chemicals-compounds that directly interfere with the endocrine system of exposed animals-are insidious environmental pollutants that can disrupt hormone function, even at very low concentrations. The dramatic impacts that some endocrine-disrupting chemicals can have on the reproductive development of wildlife are well documented. However, the potential of endocrine-disrupting chemicals to disrupt animal behaviour has received far less attention, despite the important links between behavioural processes and population-level fitness. Accordingly, we investigated the impacts of 14 and 21-day exposure to two environmentally realistic levels of 17β-trenbolone (4.6 and 11.2 ng/L), a potent endocrine-disrupting steroid and agricultural pollutant, on growth and behaviour in tadpoles of an anuran amphibian, the southern brown tree frog (Litoria ewingii). We found that 17β-trenbolone altered morphology, baseline activity and responses to a predatory threat, but did not affect anxiety-like behaviours in a scototaxis assay. Specifically, we found that tadpoles exposed to our high-17β-trenbolone treatment were significantly longer and heavier at 14 and 21 days. We also found that tadpoles exposed to 17β-trenbolone showed higher levels of baseline activity, and significantly reduced their activity following a simulated predator strike. These results provide insights into the wider repercussions of agricultural pollutants on key developmental and behavioural traits in aquatic species, and demonstrate the importance of behavioural studies in the ecotoxicological field.
... Moreover, chemical cues are usually more effective in aquatic environments (Ferland-Raymond et al. 2010), particularly in turbid ones (Ferrari et al. 2010). However, the presence of other chemical compounds in the water can impair cue detection or risk assessment, which may consequently affect the prey response to avoid the predator (Lürling and Scheffer 2007;Ehrsam et al. 2016). ...
Article
The capacity to identify predator chemical cues is extremely advantageous as it allows prey to avoid the predation sequence from the beginning. However, for aquatic organisms, identification can be constrained by the presence of other substances, such as plant chemical compounds. Despite its ecological implications, there is a lack of knowledge on the potential chemical interference of sympatric plants to the surrounding aquatic fauna. In this context, our study aims to understand the consequences that chemical interference can entail in the anti-predator responses of tadpoles of the Cope's toad (Rhinella diptycha). We conducted an outdoor experiment, where we compared the anti-predator responses of R. diptycha tadpoles to a natural predator (giant water bug) with and without adding chemicals of a potentially toxic native plant (Microlobius foetidus) to the water. Tadpoles showed an increase in grouping behaviour and a reduction in activity in the predator treatment. Moreover, our results indicate that the chemical compounds of the sympatric plant modified tadpole behavioural responses, disrupting grouping behaviour while maintaining reduced activity. These findings help understand the complexity of chemical communication in aquatic habitats and the consequences on animal-plant interactions and conservation.
... Cuban tree frogs appear to be highly tolerant to variation in environmental stressors such as acidic water [76], temperature [77], and elevated salinity [78]. However, they do not appear to be generally more tolerant than native species to chemical contaminants including atrazine [79] and the fungicide Diversity 2023, 15, 215 7 of 10 chlorothalonil [14]. Cuban tree frogs exposed to agrochemicals can also experience increased susceptibility to the chytrid fungus well after exposure [80]. ...
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Exposure to agrochemicals can have lethal and sublethal effects on amphibians. Most toxicology studies only examine exposure during the aquatic larval stage. Survival of the juvenile stage is the most important for population persistence and it is critical to understand the potential impacts of exposure during this life stage. We investigated how short-term exposure to triclopyr, an herbicide commonly used in forestry management, might impact several juvenile traits. To determine if juveniles perceived exposure as an environmental stressor, we measured their release of corticosterone. We also examined dispersal traits by measuring foraging and hopping behavior. We found no evidence that exposure negatively impacted these traits or was a stressor. Our results provide a preliminary assessment of the potential impact of triclopyr on juvenile amphibians, but we recommend additional research on the effects of agrochemicals on juvenile amphibians.
... Atrazine also interferes with the signaling of intraspecific and interspecific relationships in aquatic ecosystem. For example, atrazine makes tadpoles (Osteopilus septentrionalis) unable to sense the chemical signals of their predators, dragonfly larvae, thereby increasing the probability of encounters with predators (Ehrsam et al., 2016). After exposure to atrazine for 96 h, the ability of male rusty crayfish (Orconectes rusticus) to distinguish the source of the odor of female was weakened or even completely lost (Belanger et al., 2017). ...
Article
Full-text available
Herbicide pollution is persistent, which not only has a negative impact on individual organisms, but also may alter population dynamics and stability of interspecific relationships. Cladocerans, an important part of zooplankton, are often simultaneously exposed to environmental pollutants and predation risk in the aquatic environment. To evaluate the combined effects of atrazine and fish predation risk on the population traits of cladocerans, we exposed Daphnia pulex to different concentrations of atrazine (0, 0.05, 0.10, and 1.0 mg L⁻¹) with or without fish (Rhodeus ocellatus) kairomone, recorded the key population traits, and fitted Gaussian model to population dynamics. Results showed that fish kairomone increased the population density at the end of the experiment and resting eggs production, and tended to decrease the total biomass and the average dry weight per individual of D. pulex. Atrazine reduced the total biomass, the average dry weight per individual, and resting eggs production of D. pulex populations. Atrazine also decreased the population density at the end of the experiment of D. pulex in fish kairomone treatment, and attenuated the promoting effect of fish kairomone on resting eggs production and the reduction of the total biomass. The findings highlighted the importance of considering the combined impact of environmental pollutants and predation risks on zooplankton populations.
... We converted all concentrations to toxic units (TUs) using SPEAR Calculator software (v0.8.1, Department System Ecotoxicology -Helmoltz Center for Ehrsam et al., 2016) to account for variation in absolute toxicity among chemicals, as described by Halstead et al. (2015). Standardized chemical concentration was used as a continuous fixed effect in the model, and random intercepts for each chemical were nested within their respective chemical classes (pyrethroid or organophosphate). ...
... However, water conductivity is an indicator of agricultural runoff (Harwell et al., 2008). Eutrophication associated with nutrients in runoff can increase the chances of hypoxia at sites (Dodds and Whiles, 2019) and eutrophication from nutrients has been observed in our study system (Cogels et al., 2001). Fertilizers, which are used at all 16 villages, are also positively associated with invasive macrophytes, such as Typha spp., that were the most common emergent aquatic plant in our study and are distributed worldwide (Bansal et al., 2019). ...
... Importantly, although the prawns were caged in this study and thus unable to avoid any unfavorable conditions, many animals in nature move towards preferred levels of dissolved oxygen and thermoregulate (Cohen et al., 2017;Sauer et al., 2018). In contrast, some species have been shown not to avoid pesticides at concentrations with adverse effects on these same species (Araujo et al., 2016) and pesticides can also damage or interfere with olfaction preventing contaminant detection and avoidance (e.g., Ehrsam et al., 2016). ...
Article
Use of agrochemicals, including insecticides, is vital to food production and predicted to increase 2-5 fold by 2050. Previous studies have shown a positive association between agriculture and the human infectious disease schistosomiasis, which is problematic as this parasitic disease infects approximately 250 million people worldwide. Certain insecticides might runoff fields and be highly toxic to invertebrates, such as prawns in the genus Macrobrachium, that are biocontrol agents for snails that transmit the parasites causing schistosomiasis. We used a laboratory dose-response experiment and an observational field study to determine the relative toxicities of three pyrethroid (esfenvalerate, λ-cyhalothrin, and permethrin) and three organophosphate (chlorpyrifos, malathion, and terbufos) insecticides to Macrobrachium prawns. In the lab, pyrethroids were consistently several orders of magnitude more toxic than organophosphate insecticides, and more likely to runoff fields at lethal levels according to modeling data. At 31 water contact sites in the lower basin of the Senegal River where schistosomiasis is endemic, we found that Macrobrachium prawn survival was associated with pyrethroid but not organophosphate application rates to nearby crop fields after controlling for abiotic and prawn-level factors. Our laboratory and field results suggest that widely used pyrethroid insecticides can have strong non-target effects on Macrobrachium prawns that are biocontrol agents where 400 million people are at risk of human schistosomiasis. Understanding the ecotoxicology of high-risk insecticides may help improve human health in schistosomiasis-endemic regions undergoing agricultural expansion.
... Even at sublethal levels, these contaminants indirectly affect amphibian populations by causing physiological stress, reduced growth, developmental or reproductive impairment, increased susceptibility to diseases, and behavioral alterations (Hayes et al., 2010;Relyea, 2009;Shinn et al., 2008;Snodgrass et al., 2008;reviewed in Walls & Gabor, 2019). Pollutants alter the chemical environment of freshwater ecosystems, interfering with the olfaction of aquatic organisms including amphibians, and impairing chemoreception (Ehrsam et al., 2016;Fabian et al., 2007;Lürling, 2012;Mandrillon & Saglio, 2007;Polo-Cavia et al., 2016). Such contaminants disrupting the transmission of chemical information within and between organisms are referred to as infodisrupters (Ehrsam et al., 2016;Lürling, 2012;Polo-Cavia et al., 2016). ...
... Pollutants alter the chemical environment of freshwater ecosystems, interfering with the olfaction of aquatic organisms including amphibians, and impairing chemoreception (Ehrsam et al., 2016;Fabian et al., 2007;Lürling, 2012;Mandrillon & Saglio, 2007;Polo-Cavia et al., 2016). Such contaminants disrupting the transmission of chemical information within and between organisms are referred to as infodisrupters (Ehrsam et al., 2016;Lürling, 2012;Polo-Cavia et al., 2016). ...
... Disruption of information transfer between organisms affects detection by interfering with cue recognition systems and may affect the production of chemical signals between senders and receivers, whereas disruption of information transfer within the organism leads to improper functioning of communication systems (Ehrsam et al., 2016;Lürling, 2012;Lürling & Scheffer, 2007;Mandrillon & Saglio, 2007;Polo-Cavia et al., 2016). Interorganismal info-disrupters can interfere with the location of prey, predators, food, and mates in many organisms (Lürling, 2012;Lürling & Scheffer, 2007;Schmidt et al., 2010). ...
Article
Atrazine, an info disruptor, interferes with the olfaction of aquatic organisms by impairing the chemosensory system. Consequently, it affects behavior, physiology, and growth increases mortality and infections, and suppresses the immune system of aquatic animals. In this study, we wanted to determine the sensitivity of larval Euphlyctis cyanophlyctis to different concentrations of atrazine by assessing their antipredator behavior, growth, morphology, and metamorphic traits. The results indicate that exposure to atrazine did not affect the survival of tadpoles. However, it caused retarded growth at higher concentrations. Interestingly, the antipredator behavior of tadpoles toward conspecific alarm cues decreased in a dose-dependent manner with an increase in the concentration of atrazine. Tadpoles exposed to low concentrations of atrazine had deeper, wider bodies and tails while those exposed to higher concentrations had shallower and narrower bodies with shallower tail muscles. However, at low and moderate concentrations atrazine did not affect size at metamorphosis, it extended the larval duration at higher concentrations.
... Such chemicals were reported to impact larval protective behavior, induce hyperactivity, makes it difficult for them to recognize predator chemical cues. (Ortiz-Santaliestra et al., 2010;Ehrsam et al., 2016). ...