Arch Environ Contam Toxicol (2015) 69:557–565 DOI 10.1007/s00244-015-0181-4
The Effects of Biodiesel and Crude Oil on the Foraging Behavior of Rusty Crayfish, Orconectes rusticus Ana M. Jurcak1 • Steven J. Gauthier1 • Paul A. Moore1
Received: 25 March 2015 / Accepted: 6 June 2015 / Published online: 27 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Environmental pollutants, such as crude oil and other petroleum-based fuels, inhibit and limit an organism’s ability to perceive a chemical stimulus. Despite the increased use of alternative fuels, such as biodiesel, there have been few studies investigating the impact of these chemicals on the behavior of aquatic organisms. The purpose of this study was to compare the sublethal effects of biodiesel and crude oil exposure on chemically mediated behaviors in a freshwater keystone species. Crayfish (Orconectes rusticus) were tested on their ability to respond appropriately to a positive chemical stimulus within a Y-maze choice paradigm. Behavior was quantified by measuring time spent finding an odor source, duration of time spent at the odor source, percentage of crayfish that found the odor source, and percentage of crayfish that chose the correct arm of the arena. Results indicated negative impacts of both biodiesel and crude oil on the ability of crayfish to locate the food source. However, there were no significant differences between behavioral performances when crayfish were exposed to crude oil compared with biodiesel. Thus, biodiesel and crude oil have equally negative effects on the chemosensory behavior of crayfish. These findings indicate that biodiesel has the potential to
& Ana M. Jurcak [email protected] Steven J. Gauthier [email protected] Paul A. Moore [email protected] 1
Laboratory for Sensory Ecology, Department of Biological Sciences, J. P. Scott Center for Neuroscience, Mind, and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA
have similar negative ecological impacts as other fuel source toxins.
Contamination of aquatic ecosystems by different types of pollutants is becoming more widespread, especially with the thousands of chemicals in common use today (Maugh 1978; Boyd and Massaut 1999; Camargo and Alonso 2006). Due to the increase in demand of oil around the globe (Cooper 2003), the environment is at a heightened risk for detrimental effects that may arise from the increase in transportation of oil. Oil spills are caused by accidents involving tankers, oil rigs, storage tanks, pipelines, and barges (Burns et al. 1993). In a 16-year span from 1974 to 1990, at least 175 major oil spills occurred in the tropics comprising [1000 barrels of oil (Burns et al. 1993). Although coastal spills and oil spills in the tropics are often greatly publicized, a study by Yoshioka and Carpenter (2002) found that 60 % of all spills were inland, and 40 % of spills were coastal. Inland spills constituted 88 % of spills [10,000 gallons, whereas coastal spills constituted only 12 % of spills [10,000 gallons (Yoshioka and Carpenter 2002). The release of oil caused by these spills has had negative impacts such as physiological and behavioral impairments in organisms within aquatic environments. The presence of crude oil in ecosystems can have negative physiological and behavioral effects on animals (Bucas and Saliot 2002; Rodrigues et al. 2010). Crude oil has been found to inhibit and disrupt the chemoreceptive function of freshwater and marine species, specifically invertebrates and coral species (Blumer et al. 1973; Loya and Rinkevich 1980; Suchanek 1993). Freshwater macroinvertebrates can be negatively affected by crude oil when oil coats the gills, thus limiting oxygen exchange as well as causing lesions to develop on respiratory surfaces
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(Crunkilton and Duchrow 1990). Freshwater tropical fish Astyanax sp. had organ and tissue damage when exposed to water-soluble fraction of crude oil (Akaishi et al. 2004). Homarus americanus (American lobster) exposed to crude oil displayed foraging latency. Although given increased motivation, H. americanus shown a weak response or was unable to locate a food source in the presence of crude oil (Atema and Stein 1974; Atema et al. 1982). Polycyclic aromatic hydrocarbon (PAH) contamination in the Patoka watershed in Indiana significantly decreased crayfish assemblages (Simon and Morris 2009). Given the negative effects on animals as a result of environmental crude oil, the production and use of more environmentally safe fuel sources, such as biodiesel, has significantly increased (Bajapi and Tyagi 2006; Bozbas 2008; Januan and Ellis 2010). Biodiesel research and use has increased due to decreased carbon dioxide emissions produced from burning biodiesel compared with crude oil-based products (Ma and Hanna 1999). Biodiesel is processed and made from organic sources such as soybeans, sunflower, palm kernels, castor oil, algae, and animal fats (Ma and Hanna 1999; Pinto et al. 2005). Compared with crude oil, biodiesel has shown a 90 % decrease in the amount of unburned hydrocarbons and a 75–90 % decrease of PAHs and other noxious gases emitted into the environment (Demirbas 2007). Biodiesel is deemed a more sustainable fuel source compared with fossil fuels such as crude oil (Januan and Ellis 2010). Biodiesel has been considered less harmful than crude oil due to biodiesel’s composition of renewable resources as well as significantly decreased particulate emissions compared with crude oil (Demirbas 2003). Although biodiesels decrease the amount of harmful emissions into the atmosphere, these fuels have been shown to negatively impact aquatic species when introduced into aquatic systems (Khan et al. 2007). After Oncorhynchus mykiss (rainbow trout) were exposed to both diesel and B100 (pure biodiesel) for 48 h, the LC50 value of diesel was determined to be 350.30 ppm, whereas that of B100 was 756.68 ppm (Khan et al. 2007). Leite et al. (2011) observed inhibited growth in embryonic and larval stages of Echinometra lucunter (rock-boring urchin) exposed to B100 biodiesel. Materials used in producing biodiesel, such as palm oil, vegetable oil, or fish oil, can cause asphyxiation and blockage in the digestive tracts of mussels, lobsters, fish, and sea birds (McKelvey et al. 1980; Bucas and Saliot 2002). Although there are environmental benefits of using alternative fuels, these benefits must be measured against potential negative impacts, especially at the sublethal level, to aquatic organisms. The purpose of this study was to compare the impacts of exposure to sublethal concentrations of biodiesel and crude oil on chemically mediated behaviors in a freshwater keystone species, Orconectes rusticus (rusty crayfish).
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Rusty crayfish have an extensive range, including the Ohio River drainage to lakes and rivers throughout Midwestern states such as Illinois, Ohio, Michigan, and Minnesota and parts of Ontario, Canada, and the Laurentian Great Lakes (Olden et al. 2006). The range of the rusty crayfish is within the area of the Petroleum Administration for Defense District (PADD) 2: Midwest, which contains 25 petroleum refineries (Frittelli et al. 2014). This area is also part of Region 5 of the 10 Environmental Protection Agency (USEPA) Regions in the United States. With [10,000 gallons of inland crude oil spills, Region 5 had the fourth most occurrences compared with the other USEPA regions (Brody et al. 2012). Because rusty crayfish are abundant in Midwest inland waters and these waters have a susceptibility to oil spills, rusty crayfish make an ideal organism to study potential effects of these spills. Crayfish have been shown to be excellent models for studying the sublethal impacts of pollutants on behavior due to their role as a keystone species in many freshwater habitats and because of their use of chemically mediated behaviors, i.e., behaviors driven by information gained from chemical signals using their chemical senses (Hazlett 1994, 1999; Keller and Moore 1999; Wisenden 2000; Wolf and Moore 2002). Multiple studies have found that O. rusticus were unable to locate a food source when exposed to different types of sublethal concentrations of pollutants such as copper (Sherba et al. 2000; Lahman et al. 2015), metolachlor (Wolf and Moore 2002), and 2,4-dichlorophenoxyacetic acid herbicide (2,4-D) (Browne and Moore 2014). Studies have also shown that pollutants such as metals can damage chemoreceptors of organisms, such as blue crabs and rainbow trout, when animals are exposed at high levels (Bodammer 1979; Julliard et al. 1993). Chemoreception is impaired by toxicants binding to active sites and preventing other signal molecules from being able to bind (Tierney et al. 2010; Blinova and Cherkashin 2012). The inability to use chemoreception as a consequence of exposure to pollutants would negatively impact these aquatic organisms, which rely heavily on chemical signals.
Materials and Methods Animal Collection and Housing Male crayfish [O. rusticus (mean carapace length 2.93 ± 0.6 cm)] were collected from tributaries of the Portage River (41.37°N, 83.65°W) in Ohio through the kick-seine method. Crayfish were individually isolated in flow-through tanks in a controlled environmental chamber at Bowling Green State University. The chamber was kept on a diurnal light-to-dark 12:12-h cycle. All crayfish used in this study had fully intact limbs and sensory appendages.
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Animals were starved for 1 week before the experimental protocol and during the length of the 7-day experiment to provide motivation for the behavioral assay. Fuel Sources Two different types of fuel were used in this experiment: crude oil and biodiesel. Crude oil composition varies depending on the source and location of the oil well (Franklin and Lloyd 1982; Gill and Robotham 1989). Sweet crude oil (Husky Energy, Lima, Ohio, USA) was used due to the refinery’s proximity to the natural ecosystem of the crayfish used in this study. Biodiesel Peter Cremer North America, Cincinnati, Ohio, USA) was selected because the fuel is a pure biodiesel (B100). Experimental Design To investigate the effect of two fuel exposures on the foraging ability of crayfish, a fully 2 9 2 factorial experimental design was run with fuel type (biodiesel and crude oil) and concentration level [32.65 ppm (low) and 326.5 ppm (high)] as the two factors. Experimental conditions consisted of the following: (1) control: exposed to dechlorinated water (N = 10); (2) low: exposed to biodiesel [32.65 ppm (vol/vol)] (N = 10) (3) high: exposed to biodiesel [326.5 ppm (vol/vol)] (N = 10); (4) low: exposed to crude oil [32.65 ppm (vol/vol)] (N = 10); and (5) high: exposed to crude oil [326.5 ppm (vol/vol)] (N = 10). One crayfish was used for each trial with each individual used in a single static-renewal exposure within a random treatment association. A total of 50 crayfish were used in these experiments. Concentrations presented previously were the final concentrations within the entire tank once complete mixing took place. Each test period lasted 7 days and consisted of one 24-h acclimation period, 96 h of exposure to the fuel oil, and a 48-h recovery period. Foraging tests were performed after 48 and 96 h of exposure and 48 h of recovery, thus allowing for testing during exposure as well as during recovery. The high concentrations for this study were chosen by averaging the LC50 of 25 crude oils found in a fisheries technical report (Franklin and Lloyd 1982). In addition, the range of other concentrations (low and high, biodiesel and crude oil) were chosen to mimic the concentrations found within an oil spill (Singer et al. 1991, 1998; Pace et al. 1995). Experimental Exposure All 50 crayfish were exposed to fuel sources in separate exposure tanks with one animal per aquarium [40.6 9 20.9 9 25.7 cm3 (length, width, and height,
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respectively)]. Each aquarium had a water temperature of 22 °C and hardness of 250 ± 25 mg/L. Animals were housed and exposed independently during this process. Thus, a total of 50 different exposure tanks were used for the experiment. Aquariums were fitted with gravel filters and gravel substrate. The design was a static-renewal design. Crayfish were placed within the exposure tank for an acclimation period of 24 h. After acclimation, the correct amount of fuel oil (high or low; biodiesel or crude from stock solutions) was added to the tank to achieve a final dose outlined previously. This stock solution of fuel was added by discharging the fuel on the surface of the water in each aquarium with a syringe pump to simulate a surface runoff spill (Atema and Stein 1974). After 72 h of exposure, animals were removed for behavioral trials (see behavioral tests below), and the exposure aquariums, including the gravel filters and gravel, were emptied. The experimental set-up was implemented again with the same treatment, gravel filters, and gravel. This set-up was to counter the potential effect of oil evaporation decreasing the exposure concentration over time (Stiver and Mackay 1984). After the behavioral trial, crayfish were placed directly into the same fuel concentration without an acclimation period to continue the prolonged exposures. After the 96-h exposure period, the aquariums were emptied; however, instead of recontaminating the aquariums with fuel, the aquariums were filled with clean water to allow for a 2-day recovery phase. A subsequent behavioral trial was run after 48 h of recovery.
Testing Arena Foraging-choice tests were implemented within a Y-maze [tank = 77.5 9 42 9 18 cm3, arm = 56 9 21.5 9 18 cm3 (length, width, and depth, respectively)] (Adams et al. 2005). Two reservoir tanks (25 9 14 9 14 cm3) were used to house the stimulus (described later in the text) (Fig. 1). The reservoir for the food stimulus (Fig. 1) was randomly assigned to one of the two reservoirs using a random numbers table. The food stimulus was held down in a mesh bag with a metal weight [8.89 cm (length) 9 8.89 cm (width)] to keep food from floating within the reservoir. Stimulus flowed from the reservoir tanks through 0.95-cm (i.d.) Tygon tubing. The other reservoir did not contain the food stimulus. Two in-line flowmeters (Monostat Riteflow no. 4) controlled flow water (and stimulus) from both reservoirs at a constant rate of 112 ± 0.5 mL/min. Before testing, fluorescent dye was used to confirm that flow from each holding tank was equal when traveling from the reservoir through the arms of the maze. Speed of the outflow water was controlled by five outflow tubes (0.95-cm (i.d.) Tygon tubing) with valves located 6 cm above the
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Experimental Design, Data, and Statistical Analysis
Fig. 1 Y-maze set-up used for behavioral trials. Fuel sources and food stimulus flowed from the reservoirs through the Y-maze arena and exited out the end
bottom of the maze. Clamps were used to start and stop flow before, during, and after trials. Behavioral Tests Crayfish were rinsed before each trial with dechlorinated water. Animals were then placed and held at the end of the Y-maze for a 15-min acclimation period by a Plexiglas wall. After this period of time, flow was started, and crayfish were allowed to orient for a total of 10 min. Trials were recorded using a digital camera (Panasonic HDC-H250) mounted above the Y-maze. Between each behavioral test, the Y-maze and reservoirs were rinsed for 10 min with hot water followed by deionized water and subsequently filled with clean dechlorinated water. A different individual was used for each trial. Stimulus The food stimulus used in this study was fish gelatin, which has been used as a food stimulus in previous foraging studies (Moore and Grills 1999; Keller et al. 2001). Fish gelatin was prepared by mixing 53 g of sardines, 28 g of unflavored gelatin (Kroger brand), and 0.7 L of boiling water in a high speed blender. This mixture was placed into a baking pan (34.0 9 21.5 cm2) to solidify and was subsequently cut in 2 9 2 9 1 cm3 blocks for use. A new food gelatin square was used for each trial.
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Behavioral measures quantified for individual test trials (n = 50) used in this study included the following: time spent in the food stimulus odor arm (defined when the entire body of the crayfish crossed a line drawn perpendicular from the end of the Y-maze middle arm to the side of the tank); time at stimulus nozzle (defined as the amount of time the crayfish touched the odor-source nozzle (i.e., the opening in one arm of the Y-maze with a nozzle from whence came the odor source from the tubing connected to the reservoir) with one or both chelae; time to locate stimulus nozzle source; and stimulus arm choice. Arm choice was taken as the initial arm entered, and a choice was quantified when the entire carapace of the crayfish crossed a line drawn perpendicular from the end of the Y-maze middle arm to the side of the tank. Each subsequent period of time that the crayfish was in contact with the source was summed such that ‘‘time at nozzle’’ represents the cumulative time throughout the trial. Similarly, time to locate odor source was calculated from the start of the trial until the crayfish either came in contact with the odor nozzle or the trial ended. Orientation parameters were statistically analyzed using two-way repeated-measures multivariate analysis of variance (MANOVA) with time point and exposures as the two factors. Fisher least significant difference (LSD) post hoc analysis was used to determine any specific differences between the treatment groups (Version 9; STATISTICA, Statsoft Inc., Tulsa, OK). Correct arm choice, as well as successful location of the odor source, was analyzed using v2 test for overall differences and Tukey comparison for multiple proportions test for specific comparisons to a random expectation (Zar 1999).
Results Overall Univariate Results: Fuel Exposure There was no overall significant effect of fuel exposure on the chemically mediated behavior of crayfish (F(8, 54, 0.05) = 0.914, p [ 0.05). There were no significant differences in the amount of time crayfish spent locating the stimulus source or the amount of time spent in the arm of the Y-maze between the different fuel exposures (Fisher LSD post hoc test, p [ 0.05). Overall Univariate Results: Exposure Time The exposure time had a significant effect on foraging behavior regardless of fuel exposure (F(4, 25, 0.05) = 4.419, p \ 0.05). The amount of time crayfish in the control group took to locate the food stimulus odor source significantly
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decreased from 48 to 96 h of unpolluted water compared with 48 h of recovery (Fisher LSD post hoc test, p \ 0.05; Fig. 2). There was no difference between the amount of time crayfish in the control group took to locate the stimulus source between those in unpolluted water for 48 and 96 h (Fisher LSD post hoc test, p [ 0.05). Crayfish shown no difference in the time to locate the stimulus across exposure times when exposed to either high or low concentrations of crude oil or biodiesel (Fisher LSD post hoc test, p [ 0.05).
source after 48 h of exposure compared between the control, either concentration of crude oil (low and high), and either concentration of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). There was also no significant difference in the amount of time crayfish took to find the food stimulus odor source after 96 h of exposure between control, either concentrations of crude oil (low and high), and either concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05).
Overall Univariate Results: Interaction Between Exposure Time and Fuel Exposure
Time in Stimulus Arm
There was a significant interaction between fuel exposure and exposure time (explained in detail later in the text) on chemically mediated search behaviors (F (16, 77.01, 0.05) = 1.834, p \ 0.05). Time to Find Stimulus Source Crayfish in the control group took significantly less time to find the food stimulus odor source after 48 h of recovery compared with crayfish that had been exposed to low concentrations of crude oil and biodiesel (Fisher LSD post hoc test, p \ 0.05; Fig. 2). Crayfish exposed to either low or high concentrations of either fuel source did not significantly differ in the amount of time to find the stimulus source between all 3-day trials (Fisher LSD post hoc test, p [ 0.05). There was no significant difference in the amount of time crayfish took to find the food stimulus odor
Crayfish exposed to low concentrations of crude oil spent significantly more time in the arm of the Y-maze with the stimulus after 96 h of exposure than crayfish exposed to high concentrations of crude oil, crayfish exposed to low concentrations of biodiesel, or crayfish in the control group (Fisher LSD post hoc test, p \ 0.05). There were no significant differences between the amount of time crayfish spent in the arm of the Y-maze with the food stimulus odor after 48 h of exposure between the control, both concentrations of crude oil (low and high), and both concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). Crayfish did not significantly differ between the amount of time crayfish spent in the arm of the Y-maze with the stimulus after 48 h of recovery between control, both concentrations of crude oil (low and high), and both concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). Time at Odor Source There was no significant difference between the amount of time the crayfish spent at the food stimulus odor source between the various exposure time lengths and exposure trials (Fisher LSD post hoc test, p [ 0.05). Exposure time length did not have a significant impact on the amount of time the crayfish spent at the stimulus source (Fisher LSD post hoc test, p [ 0.05). Fuel concentrations did not have a significant impact on the amount of time crayfish spent at the stimulus source across all concentrations and the control (Fisher LSD post hoc test, p [ 0.05). Correct Arm Choice
Fig. 2 Mean (±SEM) of time to find stimulus source for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (two-way MANOVA Fisher’s LSD post hoc, p \ 0.05, N = 10 for each treatment)
After 48 h of exposure, there was no significant difference between the three exposure groups and the ability of the crayfish to choose the correct arm. After 96 h of exposure, a significant difference existed between the control and high exposure of biodiesel on the ability of the crayfish to correctly choose the arm with the stimulus source (v2 = 21.9, q = 4.42 p \ 0.05; Fig. 4). After 48 h of recovery, there was a significant difference between the
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Fig. 3 Mean (±SEM) of time to find stimulus source for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (two-way MANOVA Fisher’s LSD post hoc, p \ 0.05, N = 10 for each treatment)
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Fig. 5 Percentage of success in locating the food odor for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Significant differences within treatments are indicated by upper-case letters and significant differences across treatments indicated by lower-case letters. Bars with different letters are significantly different from each other (v2 test, p \ 0.05, N = 10 for each treatment)
Successful Foraging
Fig. 4 Percentage of success in correct stimulus arm choice for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (v2 test, p \ 0.05, N = 10 for each treatment)
There was an overall significant difference between exposure and the ability of the crayfish to successfully locate the food stimulus odor source ((v2 = 24.9, p \ 0.05); Fig. 5). Crayfish in the control group were significantly more successful in locating the stimulus source after 48 h of recovery compared with both concentrations of biodiesel and crude oil. After 96 h of exposure, crayfish exposed to low concentrations of crude oil were significantly more successful than crayfish exposed to low concentrations of biodiesel (v2 = 21.5, q = 4.42, p \ 0.05). Within the control treatment, crayfish were significantly more successful after 48 h of recovery than after 48 and 96 h of exposure (v2 = 30.96, q = 4.42, p \ 0.05). Within the high concentration of crude oil treatment, crayfish were significantly more successful after 48 h than individuals after 96 h (v2 = 21.9, q = 4.42, p \ 0.05).
Discussion high concentration of crude oil compared with all other exposure treatments (v2 = 23.6, q = 4.42, p \ 0.05). A comparison between high concentration of biodiesel and crude oil showed a significant difference for both after 96-h exposure and 48-h recovery (v2 = 21.9, q = 4.42, p \ 0.05; v2 = 40.2, q = 4.42, p \ 0.05).
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Our results show two significant findings. First, both fuels negatively affect chemically mediated behavior in crayfish. Second, for this behavior, there was no significant difference in the detrimental effects caused by biodiesel or crude oil. This is shown by the results indicating that crayfish exposed
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to the two fuel types were less successful in choosing the correct arm of the Y-maze and less successful in finding the food source than the control (v2 = 21.5, p \ 0.05, Fig. 5). In addition, crayfish spent more time locating the food source when exposed to both types of fuel sources, especially those with longer durations of exposure (LSD post hoc test p \ 0.05 (Fig. 3) and p \ 0.05 (Fig. 5)). Crude oil and biodiesel may act as a sensory pollutant and prevent crayfish from using chemoreception to locate the food source. Both fuels may bind to chemoreceptors of the crayfish, thus blocking or masking the food odors, like many environmental pollutants such as copper or metolachlor (Tierney et al. 2010; Olse´n 2011; Blinova and Cherkashin 2012; Wolf and Moore 2002). Low concentrations of copper (20 lg L-1) inhibited Camvarus bartonii from locating a food source (Sherba et al. 2000). O. rusticus were less efficient in locating a food source when exposed to metolachlor (Wolf and Moore 2002). The chemoreceptors of crayfish may also become structurally damaged due to crude oil, which would prevent the binding of food odors to the chemoreceptors. Crude-oil exposure damaged the chemoreceptors of lobster (Atema and Stein 1974). The inability of crayfish to use chemoreception due to fuel sources can have negative impacts on their fitness and survival. For many aquatic macroinvertebrates, the ability to detect and respond appropriately to odors is integral for their survival and evolutionary fitness (Carr and Derby 1986; Hazlett 1994, 1999; Bergman et al. 2003; Webster and Weissburg 2009). To differentiate between starved or satiated predators, dytiscid beetles use chemoreception to distinguish the hunger status of perch (Abjornsson et al. 1997). Macroinvertebrates, such as amphipods that use chemical cues to locate food sources such as detritus and algae (De Lange et al. 2006), also use chemoreception for foraging. Crayfish also use chemical stimuli for all aspects of their ecology including foraging, mating, and predator avoidance (Hazlett 1994, 1999; Zulandt Schneider et al. 1999; Bergman et al. 2003). A chemosensory deficit would have severe consequences for the survival of crayfish, which play an integral role in many freshwater aquatic food webs. Aquatic food webs are influenced by movement of detritus, nutrients, prey, and predators (Nakano et al. 1999). Crayfish are considered keystone species in many aquatic ecosystems due to the central role they play in shredding allochthonous material (Covich et al. 1999; Usio 2000; Usio and Townsend 2004), preying on insect larvae (Charlebois and Lamberti 1996), and serving as prey for higher trophic levels (Momot et al. 1978; Momot 1995; Stein and Magnuson 1976; Stein 1977; Shave et al. 1994; Hazlett and Schoolmaster 1998). As consumers, crayfish influence energy flow through the food web by grazing on
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plants, detritus, and macroinvertebrates (Momot et al. 1978; Momot 1995; Covich et al. 1999; Usio and Townsend 2004). Because crayfish have many roles within an aquatic ecosystem, an inability to perform these roles due to sublethal behavioral impairments can affect the population structures of prey and predators alike. An inability of crayfish to perform their keystone role due to pollutants can cause food web shifts or trophic cascading. A decrease in predation pressure on macroinvertebrates can cause a subsequent increase in grazing pressure on aquatic macrophytes. The change in primary productivity due to increased grazing can decrease the amount of carbon being assimilated in the stream, which can have far-reaching effects. A decrease of carbon, specifically the dissolved organic carbon (DOC) being released by primary producers, will negatively impact microbial plankton communities that use DOC as a major carbon source (Williamson et al. 1999). With a decrease of crayfish shredding, fewer nutrients will be released and thus unavailable for use by algae in primary production (Flint and Goldman 1975). These impacts would alter the structure and function of aquatic ecosystems. Pollutants in aquatic systems have affected aquatic food webs by causing both top-down and bottom-up effects by decreasing different trophic levels. Hydrocarbons have been shown to affect primary producers, such as phytoplankton, thus causing a decrease in phytoplankton assemblages, which may elicit a bottom-up effect on the rest of the food web (Sargain et al. 2005). Conversely, a decrease in predators due to pollutants can have a top-down effect on a trophic cascade, thus altering the abundance and growth of prey. The abundance of rotifers in ponds increased when the number of larger zooplankton decreased after exposure to carbaryl (Hanazato 1998). Microalgae blooms increased when meiofaunal grazers were negatively affected by exposure to high diesel levels (Carman et al. 1997). Taken together, these impacts and alteration in aquatic food webs will alter ecosystem function by decreasing primary and secondary productivity. Our study is one of few to explore the effects of biodiesel on aquatic systems. Recent studies have started exploring the potential toxicity of biodiesel (Hollebone et al. 2007; Khan et al. 2007; Poon et al. 2009). These studies focused more on toxicity and found that biodiesel and biodiesel blends were less toxic than diesel. Our study examined the behavioral impacts that biodiesel had on aquatic organisms and showed that biodiesel negatively affected the behavior of crayfish in the same way that crude oil does at sublethal levels. Although biodiesel may be processed from renewable biological substances and have less of a negative impact on the atmosphere compared with crude oil, both fuels have the same negative impact on behavior in aquatic systems. Investigating the sublethal
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effects of pollutants on crayfish behavior is critical in understanding the potential implications a change in behavior of organisms may have on aquatic ecosystems. Acknowledgments We thank members of the Laboratory for Sensory Ecology for their assistance in experimental set-up and review of this manuscript. We also thank four anonymous reviewers for their review of this manuscript.
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The Effects of Biodiesel and Crude Oil on the Foraging Behavior of Rusty Crayfish, Orconectes rusticus Ana M. Jurcak1 • Steven J. Gauthier1 • Paul A. Moore1
Received: 25 March 2015 / Accepted: 6 June 2015 / Published online: 27 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Environmental pollutants, such as crude oil and other petroleum-based fuels, inhibit and limit an organism’s ability to perceive a chemical stimulus. Despite the increased use of alternative fuels, such as biodiesel, there have been few studies investigating the impact of these chemicals on the behavior of aquatic organisms. The purpose of this study was to compare the sublethal effects of biodiesel and crude oil exposure on chemically mediated behaviors in a freshwater keystone species. Crayfish (Orconectes rusticus) were tested on their ability to respond appropriately to a positive chemical stimulus within a Y-maze choice paradigm. Behavior was quantified by measuring time spent finding an odor source, duration of time spent at the odor source, percentage of crayfish that found the odor source, and percentage of crayfish that chose the correct arm of the arena. Results indicated negative impacts of both biodiesel and crude oil on the ability of crayfish to locate the food source. However, there were no significant differences between behavioral performances when crayfish were exposed to crude oil compared with biodiesel. Thus, biodiesel and crude oil have equally negative effects on the chemosensory behavior of crayfish. These findings indicate that biodiesel has the potential to
& Ana M. Jurcak [email protected] Steven J. Gauthier [email protected] Paul A. Moore [email protected] 1
Laboratory for Sensory Ecology, Department of Biological Sciences, J. P. Scott Center for Neuroscience, Mind, and Behavior, Bowling Green State University, Bowling Green, OH 43403, USA
have similar negative ecological impacts as other fuel source toxins.
Contamination of aquatic ecosystems by different types of pollutants is becoming more widespread, especially with the thousands of chemicals in common use today (Maugh 1978; Boyd and Massaut 1999; Camargo and Alonso 2006). Due to the increase in demand of oil around the globe (Cooper 2003), the environment is at a heightened risk for detrimental effects that may arise from the increase in transportation of oil. Oil spills are caused by accidents involving tankers, oil rigs, storage tanks, pipelines, and barges (Burns et al. 1993). In a 16-year span from 1974 to 1990, at least 175 major oil spills occurred in the tropics comprising [1000 barrels of oil (Burns et al. 1993). Although coastal spills and oil spills in the tropics are often greatly publicized, a study by Yoshioka and Carpenter (2002) found that 60 % of all spills were inland, and 40 % of spills were coastal. Inland spills constituted 88 % of spills [10,000 gallons, whereas coastal spills constituted only 12 % of spills [10,000 gallons (Yoshioka and Carpenter 2002). The release of oil caused by these spills has had negative impacts such as physiological and behavioral impairments in organisms within aquatic environments. The presence of crude oil in ecosystems can have negative physiological and behavioral effects on animals (Bucas and Saliot 2002; Rodrigues et al. 2010). Crude oil has been found to inhibit and disrupt the chemoreceptive function of freshwater and marine species, specifically invertebrates and coral species (Blumer et al. 1973; Loya and Rinkevich 1980; Suchanek 1993). Freshwater macroinvertebrates can be negatively affected by crude oil when oil coats the gills, thus limiting oxygen exchange as well as causing lesions to develop on respiratory surfaces
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(Crunkilton and Duchrow 1990). Freshwater tropical fish Astyanax sp. had organ and tissue damage when exposed to water-soluble fraction of crude oil (Akaishi et al. 2004). Homarus americanus (American lobster) exposed to crude oil displayed foraging latency. Although given increased motivation, H. americanus shown a weak response or was unable to locate a food source in the presence of crude oil (Atema and Stein 1974; Atema et al. 1982). Polycyclic aromatic hydrocarbon (PAH) contamination in the Patoka watershed in Indiana significantly decreased crayfish assemblages (Simon and Morris 2009). Given the negative effects on animals as a result of environmental crude oil, the production and use of more environmentally safe fuel sources, such as biodiesel, has significantly increased (Bajapi and Tyagi 2006; Bozbas 2008; Januan and Ellis 2010). Biodiesel research and use has increased due to decreased carbon dioxide emissions produced from burning biodiesel compared with crude oil-based products (Ma and Hanna 1999). Biodiesel is processed and made from organic sources such as soybeans, sunflower, palm kernels, castor oil, algae, and animal fats (Ma and Hanna 1999; Pinto et al. 2005). Compared with crude oil, biodiesel has shown a 90 % decrease in the amount of unburned hydrocarbons and a 75–90 % decrease of PAHs and other noxious gases emitted into the environment (Demirbas 2007). Biodiesel is deemed a more sustainable fuel source compared with fossil fuels such as crude oil (Januan and Ellis 2010). Biodiesel has been considered less harmful than crude oil due to biodiesel’s composition of renewable resources as well as significantly decreased particulate emissions compared with crude oil (Demirbas 2003). Although biodiesels decrease the amount of harmful emissions into the atmosphere, these fuels have been shown to negatively impact aquatic species when introduced into aquatic systems (Khan et al. 2007). After Oncorhynchus mykiss (rainbow trout) were exposed to both diesel and B100 (pure biodiesel) for 48 h, the LC50 value of diesel was determined to be 350.30 ppm, whereas that of B100 was 756.68 ppm (Khan et al. 2007). Leite et al. (2011) observed inhibited growth in embryonic and larval stages of Echinometra lucunter (rock-boring urchin) exposed to B100 biodiesel. Materials used in producing biodiesel, such as palm oil, vegetable oil, or fish oil, can cause asphyxiation and blockage in the digestive tracts of mussels, lobsters, fish, and sea birds (McKelvey et al. 1980; Bucas and Saliot 2002). Although there are environmental benefits of using alternative fuels, these benefits must be measured against potential negative impacts, especially at the sublethal level, to aquatic organisms. The purpose of this study was to compare the impacts of exposure to sublethal concentrations of biodiesel and crude oil on chemically mediated behaviors in a freshwater keystone species, Orconectes rusticus (rusty crayfish).
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Rusty crayfish have an extensive range, including the Ohio River drainage to lakes and rivers throughout Midwestern states such as Illinois, Ohio, Michigan, and Minnesota and parts of Ontario, Canada, and the Laurentian Great Lakes (Olden et al. 2006). The range of the rusty crayfish is within the area of the Petroleum Administration for Defense District (PADD) 2: Midwest, which contains 25 petroleum refineries (Frittelli et al. 2014). This area is also part of Region 5 of the 10 Environmental Protection Agency (USEPA) Regions in the United States. With [10,000 gallons of inland crude oil spills, Region 5 had the fourth most occurrences compared with the other USEPA regions (Brody et al. 2012). Because rusty crayfish are abundant in Midwest inland waters and these waters have a susceptibility to oil spills, rusty crayfish make an ideal organism to study potential effects of these spills. Crayfish have been shown to be excellent models for studying the sublethal impacts of pollutants on behavior due to their role as a keystone species in many freshwater habitats and because of their use of chemically mediated behaviors, i.e., behaviors driven by information gained from chemical signals using their chemical senses (Hazlett 1994, 1999; Keller and Moore 1999; Wisenden 2000; Wolf and Moore 2002). Multiple studies have found that O. rusticus were unable to locate a food source when exposed to different types of sublethal concentrations of pollutants such as copper (Sherba et al. 2000; Lahman et al. 2015), metolachlor (Wolf and Moore 2002), and 2,4-dichlorophenoxyacetic acid herbicide (2,4-D) (Browne and Moore 2014). Studies have also shown that pollutants such as metals can damage chemoreceptors of organisms, such as blue crabs and rainbow trout, when animals are exposed at high levels (Bodammer 1979; Julliard et al. 1993). Chemoreception is impaired by toxicants binding to active sites and preventing other signal molecules from being able to bind (Tierney et al. 2010; Blinova and Cherkashin 2012). The inability to use chemoreception as a consequence of exposure to pollutants would negatively impact these aquatic organisms, which rely heavily on chemical signals.
Materials and Methods Animal Collection and Housing Male crayfish [O. rusticus (mean carapace length 2.93 ± 0.6 cm)] were collected from tributaries of the Portage River (41.37°N, 83.65°W) in Ohio through the kick-seine method. Crayfish were individually isolated in flow-through tanks in a controlled environmental chamber at Bowling Green State University. The chamber was kept on a diurnal light-to-dark 12:12-h cycle. All crayfish used in this study had fully intact limbs and sensory appendages.
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Animals were starved for 1 week before the experimental protocol and during the length of the 7-day experiment to provide motivation for the behavioral assay. Fuel Sources Two different types of fuel were used in this experiment: crude oil and biodiesel. Crude oil composition varies depending on the source and location of the oil well (Franklin and Lloyd 1982; Gill and Robotham 1989). Sweet crude oil (Husky Energy, Lima, Ohio, USA) was used due to the refinery’s proximity to the natural ecosystem of the crayfish used in this study. Biodiesel Peter Cremer North America, Cincinnati, Ohio, USA) was selected because the fuel is a pure biodiesel (B100). Experimental Design To investigate the effect of two fuel exposures on the foraging ability of crayfish, a fully 2 9 2 factorial experimental design was run with fuel type (biodiesel and crude oil) and concentration level [32.65 ppm (low) and 326.5 ppm (high)] as the two factors. Experimental conditions consisted of the following: (1) control: exposed to dechlorinated water (N = 10); (2) low: exposed to biodiesel [32.65 ppm (vol/vol)] (N = 10) (3) high: exposed to biodiesel [326.5 ppm (vol/vol)] (N = 10); (4) low: exposed to crude oil [32.65 ppm (vol/vol)] (N = 10); and (5) high: exposed to crude oil [326.5 ppm (vol/vol)] (N = 10). One crayfish was used for each trial with each individual used in a single static-renewal exposure within a random treatment association. A total of 50 crayfish were used in these experiments. Concentrations presented previously were the final concentrations within the entire tank once complete mixing took place. Each test period lasted 7 days and consisted of one 24-h acclimation period, 96 h of exposure to the fuel oil, and a 48-h recovery period. Foraging tests were performed after 48 and 96 h of exposure and 48 h of recovery, thus allowing for testing during exposure as well as during recovery. The high concentrations for this study were chosen by averaging the LC50 of 25 crude oils found in a fisheries technical report (Franklin and Lloyd 1982). In addition, the range of other concentrations (low and high, biodiesel and crude oil) were chosen to mimic the concentrations found within an oil spill (Singer et al. 1991, 1998; Pace et al. 1995). Experimental Exposure All 50 crayfish were exposed to fuel sources in separate exposure tanks with one animal per aquarium [40.6 9 20.9 9 25.7 cm3 (length, width, and height,
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respectively)]. Each aquarium had a water temperature of 22 °C and hardness of 250 ± 25 mg/L. Animals were housed and exposed independently during this process. Thus, a total of 50 different exposure tanks were used for the experiment. Aquariums were fitted with gravel filters and gravel substrate. The design was a static-renewal design. Crayfish were placed within the exposure tank for an acclimation period of 24 h. After acclimation, the correct amount of fuel oil (high or low; biodiesel or crude from stock solutions) was added to the tank to achieve a final dose outlined previously. This stock solution of fuel was added by discharging the fuel on the surface of the water in each aquarium with a syringe pump to simulate a surface runoff spill (Atema and Stein 1974). After 72 h of exposure, animals were removed for behavioral trials (see behavioral tests below), and the exposure aquariums, including the gravel filters and gravel, were emptied. The experimental set-up was implemented again with the same treatment, gravel filters, and gravel. This set-up was to counter the potential effect of oil evaporation decreasing the exposure concentration over time (Stiver and Mackay 1984). After the behavioral trial, crayfish were placed directly into the same fuel concentration without an acclimation period to continue the prolonged exposures. After the 96-h exposure period, the aquariums were emptied; however, instead of recontaminating the aquariums with fuel, the aquariums were filled with clean water to allow for a 2-day recovery phase. A subsequent behavioral trial was run after 48 h of recovery.
Testing Arena Foraging-choice tests were implemented within a Y-maze [tank = 77.5 9 42 9 18 cm3, arm = 56 9 21.5 9 18 cm3 (length, width, and depth, respectively)] (Adams et al. 2005). Two reservoir tanks (25 9 14 9 14 cm3) were used to house the stimulus (described later in the text) (Fig. 1). The reservoir for the food stimulus (Fig. 1) was randomly assigned to one of the two reservoirs using a random numbers table. The food stimulus was held down in a mesh bag with a metal weight [8.89 cm (length) 9 8.89 cm (width)] to keep food from floating within the reservoir. Stimulus flowed from the reservoir tanks through 0.95-cm (i.d.) Tygon tubing. The other reservoir did not contain the food stimulus. Two in-line flowmeters (Monostat Riteflow no. 4) controlled flow water (and stimulus) from both reservoirs at a constant rate of 112 ± 0.5 mL/min. Before testing, fluorescent dye was used to confirm that flow from each holding tank was equal when traveling from the reservoir through the arms of the maze. Speed of the outflow water was controlled by five outflow tubes (0.95-cm (i.d.) Tygon tubing) with valves located 6 cm above the
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Experimental Design, Data, and Statistical Analysis
Fig. 1 Y-maze set-up used for behavioral trials. Fuel sources and food stimulus flowed from the reservoirs through the Y-maze arena and exited out the end
bottom of the maze. Clamps were used to start and stop flow before, during, and after trials. Behavioral Tests Crayfish were rinsed before each trial with dechlorinated water. Animals were then placed and held at the end of the Y-maze for a 15-min acclimation period by a Plexiglas wall. After this period of time, flow was started, and crayfish were allowed to orient for a total of 10 min. Trials were recorded using a digital camera (Panasonic HDC-H250) mounted above the Y-maze. Between each behavioral test, the Y-maze and reservoirs were rinsed for 10 min with hot water followed by deionized water and subsequently filled with clean dechlorinated water. A different individual was used for each trial. Stimulus The food stimulus used in this study was fish gelatin, which has been used as a food stimulus in previous foraging studies (Moore and Grills 1999; Keller et al. 2001). Fish gelatin was prepared by mixing 53 g of sardines, 28 g of unflavored gelatin (Kroger brand), and 0.7 L of boiling water in a high speed blender. This mixture was placed into a baking pan (34.0 9 21.5 cm2) to solidify and was subsequently cut in 2 9 2 9 1 cm3 blocks for use. A new food gelatin square was used for each trial.
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Behavioral measures quantified for individual test trials (n = 50) used in this study included the following: time spent in the food stimulus odor arm (defined when the entire body of the crayfish crossed a line drawn perpendicular from the end of the Y-maze middle arm to the side of the tank); time at stimulus nozzle (defined as the amount of time the crayfish touched the odor-source nozzle (i.e., the opening in one arm of the Y-maze with a nozzle from whence came the odor source from the tubing connected to the reservoir) with one or both chelae; time to locate stimulus nozzle source; and stimulus arm choice. Arm choice was taken as the initial arm entered, and a choice was quantified when the entire carapace of the crayfish crossed a line drawn perpendicular from the end of the Y-maze middle arm to the side of the tank. Each subsequent period of time that the crayfish was in contact with the source was summed such that ‘‘time at nozzle’’ represents the cumulative time throughout the trial. Similarly, time to locate odor source was calculated from the start of the trial until the crayfish either came in contact with the odor nozzle or the trial ended. Orientation parameters were statistically analyzed using two-way repeated-measures multivariate analysis of variance (MANOVA) with time point and exposures as the two factors. Fisher least significant difference (LSD) post hoc analysis was used to determine any specific differences between the treatment groups (Version 9; STATISTICA, Statsoft Inc., Tulsa, OK). Correct arm choice, as well as successful location of the odor source, was analyzed using v2 test for overall differences and Tukey comparison for multiple proportions test for specific comparisons to a random expectation (Zar 1999).
Results Overall Univariate Results: Fuel Exposure There was no overall significant effect of fuel exposure on the chemically mediated behavior of crayfish (F(8, 54, 0.05) = 0.914, p [ 0.05). There were no significant differences in the amount of time crayfish spent locating the stimulus source or the amount of time spent in the arm of the Y-maze between the different fuel exposures (Fisher LSD post hoc test, p [ 0.05). Overall Univariate Results: Exposure Time The exposure time had a significant effect on foraging behavior regardless of fuel exposure (F(4, 25, 0.05) = 4.419, p \ 0.05). The amount of time crayfish in the control group took to locate the food stimulus odor source significantly
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decreased from 48 to 96 h of unpolluted water compared with 48 h of recovery (Fisher LSD post hoc test, p \ 0.05; Fig. 2). There was no difference between the amount of time crayfish in the control group took to locate the stimulus source between those in unpolluted water for 48 and 96 h (Fisher LSD post hoc test, p [ 0.05). Crayfish shown no difference in the time to locate the stimulus across exposure times when exposed to either high or low concentrations of crude oil or biodiesel (Fisher LSD post hoc test, p [ 0.05).
source after 48 h of exposure compared between the control, either concentration of crude oil (low and high), and either concentration of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). There was also no significant difference in the amount of time crayfish took to find the food stimulus odor source after 96 h of exposure between control, either concentrations of crude oil (low and high), and either concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05).
Overall Univariate Results: Interaction Between Exposure Time and Fuel Exposure
Time in Stimulus Arm
There was a significant interaction between fuel exposure and exposure time (explained in detail later in the text) on chemically mediated search behaviors (F (16, 77.01, 0.05) = 1.834, p \ 0.05). Time to Find Stimulus Source Crayfish in the control group took significantly less time to find the food stimulus odor source after 48 h of recovery compared with crayfish that had been exposed to low concentrations of crude oil and biodiesel (Fisher LSD post hoc test, p \ 0.05; Fig. 2). Crayfish exposed to either low or high concentrations of either fuel source did not significantly differ in the amount of time to find the stimulus source between all 3-day trials (Fisher LSD post hoc test, p [ 0.05). There was no significant difference in the amount of time crayfish took to find the food stimulus odor
Crayfish exposed to low concentrations of crude oil spent significantly more time in the arm of the Y-maze with the stimulus after 96 h of exposure than crayfish exposed to high concentrations of crude oil, crayfish exposed to low concentrations of biodiesel, or crayfish in the control group (Fisher LSD post hoc test, p \ 0.05). There were no significant differences between the amount of time crayfish spent in the arm of the Y-maze with the food stimulus odor after 48 h of exposure between the control, both concentrations of crude oil (low and high), and both concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). Crayfish did not significantly differ between the amount of time crayfish spent in the arm of the Y-maze with the stimulus after 48 h of recovery between control, both concentrations of crude oil (low and high), and both concentrations of biodiesel (low and high) (Fisher LSD post hoc test, p [ 0.05). Time at Odor Source There was no significant difference between the amount of time the crayfish spent at the food stimulus odor source between the various exposure time lengths and exposure trials (Fisher LSD post hoc test, p [ 0.05). Exposure time length did not have a significant impact on the amount of time the crayfish spent at the stimulus source (Fisher LSD post hoc test, p [ 0.05). Fuel concentrations did not have a significant impact on the amount of time crayfish spent at the stimulus source across all concentrations and the control (Fisher LSD post hoc test, p [ 0.05). Correct Arm Choice
Fig. 2 Mean (±SEM) of time to find stimulus source for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (two-way MANOVA Fisher’s LSD post hoc, p \ 0.05, N = 10 for each treatment)
After 48 h of exposure, there was no significant difference between the three exposure groups and the ability of the crayfish to choose the correct arm. After 96 h of exposure, a significant difference existed between the control and high exposure of biodiesel on the ability of the crayfish to correctly choose the arm with the stimulus source (v2 = 21.9, q = 4.42 p \ 0.05; Fig. 4). After 48 h of recovery, there was a significant difference between the
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Fig. 3 Mean (±SEM) of time to find stimulus source for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (two-way MANOVA Fisher’s LSD post hoc, p \ 0.05, N = 10 for each treatment)
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Fig. 5 Percentage of success in locating the food odor for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Significant differences within treatments are indicated by upper-case letters and significant differences across treatments indicated by lower-case letters. Bars with different letters are significantly different from each other (v2 test, p \ 0.05, N = 10 for each treatment)
Successful Foraging
Fig. 4 Percentage of success in correct stimulus arm choice for crayfish in control (white), low concentration of crude oil (grey), high concentration of crude oil (black), low concentration of biodiesel (diagonal stripe), and high concentration of biodiesel (cross-hatched) exposure. Bars with different letters are significantly different from each other (v2 test, p \ 0.05, N = 10 for each treatment)
There was an overall significant difference between exposure and the ability of the crayfish to successfully locate the food stimulus odor source ((v2 = 24.9, p \ 0.05); Fig. 5). Crayfish in the control group were significantly more successful in locating the stimulus source after 48 h of recovery compared with both concentrations of biodiesel and crude oil. After 96 h of exposure, crayfish exposed to low concentrations of crude oil were significantly more successful than crayfish exposed to low concentrations of biodiesel (v2 = 21.5, q = 4.42, p \ 0.05). Within the control treatment, crayfish were significantly more successful after 48 h of recovery than after 48 and 96 h of exposure (v2 = 30.96, q = 4.42, p \ 0.05). Within the high concentration of crude oil treatment, crayfish were significantly more successful after 48 h than individuals after 96 h (v2 = 21.9, q = 4.42, p \ 0.05).
Discussion high concentration of crude oil compared with all other exposure treatments (v2 = 23.6, q = 4.42, p \ 0.05). A comparison between high concentration of biodiesel and crude oil showed a significant difference for both after 96-h exposure and 48-h recovery (v2 = 21.9, q = 4.42, p \ 0.05; v2 = 40.2, q = 4.42, p \ 0.05).
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Our results show two significant findings. First, both fuels negatively affect chemically mediated behavior in crayfish. Second, for this behavior, there was no significant difference in the detrimental effects caused by biodiesel or crude oil. This is shown by the results indicating that crayfish exposed
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to the two fuel types were less successful in choosing the correct arm of the Y-maze and less successful in finding the food source than the control (v2 = 21.5, p \ 0.05, Fig. 5). In addition, crayfish spent more time locating the food source when exposed to both types of fuel sources, especially those with longer durations of exposure (LSD post hoc test p \ 0.05 (Fig. 3) and p \ 0.05 (Fig. 5)). Crude oil and biodiesel may act as a sensory pollutant and prevent crayfish from using chemoreception to locate the food source. Both fuels may bind to chemoreceptors of the crayfish, thus blocking or masking the food odors, like many environmental pollutants such as copper or metolachlor (Tierney et al. 2010; Olse´n 2011; Blinova and Cherkashin 2012; Wolf and Moore 2002). Low concentrations of copper (20 lg L-1) inhibited Camvarus bartonii from locating a food source (Sherba et al. 2000). O. rusticus were less efficient in locating a food source when exposed to metolachlor (Wolf and Moore 2002). The chemoreceptors of crayfish may also become structurally damaged due to crude oil, which would prevent the binding of food odors to the chemoreceptors. Crude-oil exposure damaged the chemoreceptors of lobster (Atema and Stein 1974). The inability of crayfish to use chemoreception due to fuel sources can have negative impacts on their fitness and survival. For many aquatic macroinvertebrates, the ability to detect and respond appropriately to odors is integral for their survival and evolutionary fitness (Carr and Derby 1986; Hazlett 1994, 1999; Bergman et al. 2003; Webster and Weissburg 2009). To differentiate between starved or satiated predators, dytiscid beetles use chemoreception to distinguish the hunger status of perch (Abjornsson et al. 1997). Macroinvertebrates, such as amphipods that use chemical cues to locate food sources such as detritus and algae (De Lange et al. 2006), also use chemoreception for foraging. Crayfish also use chemical stimuli for all aspects of their ecology including foraging, mating, and predator avoidance (Hazlett 1994, 1999; Zulandt Schneider et al. 1999; Bergman et al. 2003). A chemosensory deficit would have severe consequences for the survival of crayfish, which play an integral role in many freshwater aquatic food webs. Aquatic food webs are influenced by movement of detritus, nutrients, prey, and predators (Nakano et al. 1999). Crayfish are considered keystone species in many aquatic ecosystems due to the central role they play in shredding allochthonous material (Covich et al. 1999; Usio 2000; Usio and Townsend 2004), preying on insect larvae (Charlebois and Lamberti 1996), and serving as prey for higher trophic levels (Momot et al. 1978; Momot 1995; Stein and Magnuson 1976; Stein 1977; Shave et al. 1994; Hazlett and Schoolmaster 1998). As consumers, crayfish influence energy flow through the food web by grazing on
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plants, detritus, and macroinvertebrates (Momot et al. 1978; Momot 1995; Covich et al. 1999; Usio and Townsend 2004). Because crayfish have many roles within an aquatic ecosystem, an inability to perform these roles due to sublethal behavioral impairments can affect the population structures of prey and predators alike. An inability of crayfish to perform their keystone role due to pollutants can cause food web shifts or trophic cascading. A decrease in predation pressure on macroinvertebrates can cause a subsequent increase in grazing pressure on aquatic macrophytes. The change in primary productivity due to increased grazing can decrease the amount of carbon being assimilated in the stream, which can have far-reaching effects. A decrease of carbon, specifically the dissolved organic carbon (DOC) being released by primary producers, will negatively impact microbial plankton communities that use DOC as a major carbon source (Williamson et al. 1999). With a decrease of crayfish shredding, fewer nutrients will be released and thus unavailable for use by algae in primary production (Flint and Goldman 1975). These impacts would alter the structure and function of aquatic ecosystems. Pollutants in aquatic systems have affected aquatic food webs by causing both top-down and bottom-up effects by decreasing different trophic levels. Hydrocarbons have been shown to affect primary producers, such as phytoplankton, thus causing a decrease in phytoplankton assemblages, which may elicit a bottom-up effect on the rest of the food web (Sargain et al. 2005). Conversely, a decrease in predators due to pollutants can have a top-down effect on a trophic cascade, thus altering the abundance and growth of prey. The abundance of rotifers in ponds increased when the number of larger zooplankton decreased after exposure to carbaryl (Hanazato 1998). Microalgae blooms increased when meiofaunal grazers were negatively affected by exposure to high diesel levels (Carman et al. 1997). Taken together, these impacts and alteration in aquatic food webs will alter ecosystem function by decreasing primary and secondary productivity. Our study is one of few to explore the effects of biodiesel on aquatic systems. Recent studies have started exploring the potential toxicity of biodiesel (Hollebone et al. 2007; Khan et al. 2007; Poon et al. 2009). These studies focused more on toxicity and found that biodiesel and biodiesel blends were less toxic than diesel. Our study examined the behavioral impacts that biodiesel had on aquatic organisms and showed that biodiesel negatively affected the behavior of crayfish in the same way that crude oil does at sublethal levels. Although biodiesel may be processed from renewable biological substances and have less of a negative impact on the atmosphere compared with crude oil, both fuels have the same negative impact on behavior in aquatic systems. Investigating the sublethal
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effects of pollutants on crayfish behavior is critical in understanding the potential implications a change in behavior of organisms may have on aquatic ecosystems. Acknowledgments We thank members of the Laboratory for Sensory Ecology for their assistance in experimental set-up and review of this manuscript. We also thank four anonymous reviewers for their review of this manuscript.
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