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Literature on fish responses to electricity is extensive, and electrofishing is a common and effective tool employed to collect fishery data (Snyder, 2003; Hardie et al., 2006; Poos et al., 2007; Ruetz et al., 2007; Rabeni et al., 2009). Electrofishing has been used to conduct surveys in lentic habitat for amphibians of the order Caudata (Fitch, 1959; Shoop, 1965; Williams et al., 1981; Hawkins et al., 1983; Corn and Bury, 1989; Jung et al., 2000; Sagar et al., 2007; Foster et al., 2008; Cossel et al., 2012), with fewer of those surveys targeting amphibians of the order Anura (Olson and Rugger, 2007; R. A. Ptolemy and K. Paige, in litt.). However, anurans in the family Ranidae (true frogs) might be in contact with electrofishing more often than are other amphibian species, as ranids inhabit many of the same waters where fish occur. Even though ranids can be impacted by, or the focus of, electrofishing, information on the interaction between electricity and frog response (behavior and injury) is sparse and largely limited to agency reports (M. Allen and S. Riley, in litt.; M. Layhee, in litt.).

Although electrofishing is one of the best tools available to sample many fish species, it can injure both target and nontarget species. Wahl et al. (2007) reported increased susceptibility of bluegill, Lepomis macrochirus, to predation at power densities of ~1,050 [micro]W/[cm.sup.3], and Miranda and Kidwell (2010) induced injury (mortality, spinal injury, and tissue hemorrhage) to four nongame species (creek chub, Semotilus atromaculatus; bluntnose minnow, Pimephales notatus; tadpole madtom, Noturus gyrinus; and redfin darter, Etheostoma whipplei) at higher power densities between 1.0 x [10.sup.5] and 6.8 x [10.sup.7] [mu]W/[cm.sup.3]. It is likely that similar responses to those observed in fish, such as taxis and immobilization (narcosis to tetany), are induced in frogs. Applying results of research on electrofishing and its effects on frogs may reduce adverse effects from electrofishing and further inform management regarding use of this tool as part of conservation actions for frogs and the larger amphibian taxon (Committee on the Status of Endangered Wildlife in Canada, 2000; Knapp et al., 2007; Olson and Rugger, 2007; Whittier et al., 2007; Orchard, 2011).

Herein, we report on our laboratory study in March and April of 2012, where we immobilized early life stages (tadpoles and recently metamorphosed frogs) of American bullfrog, Lithobates catesbeianus, and Southern leopard frog, Lithobates sphenocephalus, using low-voltage electrical current. We used tadpoles that ranged in size from 30-45 mm total length (snout to vent) and which had developed into stages 21-30 (Gosner, 1960). Recently metamorphosed frogs used were ~70 mm total length. We quantified the lowest immobilization threshold as measures of power density ([micro]W/[cm.sup.3]) and voltage gradient (V/cm). In this study, we used a uniform electrical field created in a 57-L aquarium by fitting each end with a plate electrode (distance between electrodes = 52.5 cm). We applied a pulsed direct current using an ETS ABP-3 (ETS Electrofishing Systems LLC, Madison, Wisconsin) backpack electrofisher using a 20% duty cycle. Because pulse frequency can affect the response of fish (Snyder, 2003; Dolan and Miranda, 2004; Kolz, 2006), we used different pulse frequencies (15, 30, 60, and 120 Hz) in trials with tadpoles (Table 1). Ambient water conductivity values in trials using tadpoles were 854 and 1,381 [micro]S/cm (Table 1). In trials of leopard frogs we tested the effect of water conductivity by using water with conductances of 250 and 1,291 [micro]S/cm. We used two pulse frequencies (30 and 60 Hz) in these trials (Table 1). For all trials, we measured the voltage at the ETS backpack with a peak voltmeter and confirmed the uniformity of the electric field with a voltage gradient probe connected to an oscilloscope.

To conduct the trials, we placed individual specimens in the aquarium and applied a low electrical current for approximately 3 s. For tadpoles, we characterized immobilization as the movement of that individual from its resting position on the bottom of the tank to a slightly higher position in the water column and a rigid extension of its tail. We characterized frog immobilization as the extension of both front and hind limbs. If the specimens did not exhibit these behaviors, voltage was slightly increased and again applied for 3 s. No more than three increases were required to induce immobilization.

We conducted the trials on bullfrogs in New Mexico and the trials on leopard frogs occurred in Louisiana. The former species is introduced in New Mexico whereas the latter taxon is native to Louisiana. In March 2012, during a Principles and Techniques of Electrofishing course (U.S. Fish and Wildlife Service National Conservation Training Center) taught by this author (JCD) and A. J. Temple, we tested the response of bullfrog tadpoles to an electrical current. Bullfrog tadpoles were collected from the Rio Grande, below Elephant Butte Reservoir, Sierra County, New Mexico. We subjected individuals to 1 trial (multiple currents) and then held them for 24 h to document survival.

We continued this investigation by collecting leopard frog tadpoles from Natchitoches National Fish Hatchery ponds, Natchitoches Parish, Louisiana in April 2012. They were held at Natchitoches National Fish Hatchery for 2 wk and provided boiled lettuce ad libitum as food. During that 2-wk period, tadpoles completed metamorphosis (stage 46; Gosner, 1960). As opposed to bullfrogs, we used both tadpoles and recently metamorphosed leopard frogs in multiple trials. We did not observe mortality in bullfrogs, but mortalities occurred during trials of leopard frogs. We were unable to specify the cause of mortality (nutrition, disease, or effects of trials). We returned surviving leopard frogs (approximately 90% of individuals) to hatchery ponds at the end of the experiment.

Current understanding of the effects of electricity on aquatic organisms is based on the maximum power transfer theorem, as it explains much of the behavioral variability observed in fish when electricity is applied in an aquatic system (Kolz et al., 1998; Kolz, 2006). To induce a response (i.e., immobilization) from the target animal, electrical power (energy/time) must be transferred into the animal. The maximum power transfer principle poses that voltage or current (amperes) by themselves are not good indicators of the amount of power transferred into the given organism and the resulting observed behaviors such as immobilization, taxis, or narcosis (Kolz, 2006). Power density is the power dissipated in a given volume of water. It is maximally transferred to aquatic organisms when the organism's effective conductivity matches the ambient water conductivity (Kolz and Reynolds, 1989). Hence, we used power density to measure the least amount of energy transferred that would cause tadpole or frog immobilization. We calculated power density (D; [micro]W/[cm.sup.3]) as:

D = [sigma] *[E.sup.2] (1)

where [sigma] = the ambient water conductivity ([micro]S/cm) and E = the voltage gradient [V/cm] (Kolz, 2006).

Because we conducted trials with tadpoles in New Mexico and Louisiana in different ambient water conductivities, we standardized the power density thresholds for bullfrog and leopard frog tadpoles to an ambient water conductivity of 100 [micro]S/cm using the formula:

[D.sub.100] = [D.sub.1] x [[(100 1 [C.sub.f])/([C.sub.1] + [C.sub.f])].sup.2] x ([C.sub.1]/100) (2)

where [D.sub.100] = power density at an ambient water conductivity of 100 [micro]S/cm, [D.sub.1] = power density threshold resulting in immobilization at experimental trial ambient conductivity, [C.sub.f] = effective tadpole or frog conductivity, and [C.sub.1] = ambient water conductivity of experimental trial (Kolz et al., 1998). The effective conductivity of fish has been experimentally determined to be about 115 [micro]S/cm (Miranda and Dolan, 2003), but a comparable value for tadpoles or frogs has not been reported. Using data from trials with leopard frogs, and incorporating the maximum power transfer model (Kolz, 1989), we determined 85 [micro]S/ cm a reasonable estimate of a tadpole or frog's effective conductivity. We applied the following formula to standardize the voltage gradient (E) to an ambient water conductivity of 100 [micro]S/cm

[E.sub.100] = [square root of ([D.sub.100]/[C.sub.a])] (3)

where [E.sub.100] = voltage gradient at an ambient water conductivity of 100 [micro]S/cm and [C.sub.a] = the ambient water conductivity to which voltage is standardized (in this case 100 [micro]S/cm).

Pulse frequency (Hz) affected the immobilization power density threshold for both tadpole species (Table1). Standardized to an ambient water conductivity of 100 [micro]S/cm, the highest power densities were for pulse frequencies of 15 Hz (283 and 321 [micro]W/[cm.sup.3] for bullfrogs and leopard frogs, respectively). The power density required to elicit immobilization decreased as pulse frequencies increased (Fig. 1). Although the lowest power density threshold for bullfrog tadpoles ([D.sub.100] = 59 [micro]W/[cm.sup.3]) occurred at a pulse frequency of 60 Hz and then increased at 120 Hz ([D.sub.100] = 91 [mu]W/ c[m.sup.3]), we observed the inverse for leopard frog tadpoles; the lowest power density threshold occurred at 120 Hz ([D.sub.100] = 93 [micro]W/[cm.sup.3]). At all pulse frequencies, it took slightly more power to immobilize leopard frog tadpoles than bullfrog tadpoles (Fig. 1). The difference between the power densities ([D.sub.100]) eliciting immobilization in either species of tadpole at 120 Hz was negligible (2 [micro]W/[cm.sup.3]).

Different water conductivity values affected the amount of power required to immobilize leopard frog frogs (Table 1; Fig. 2). As predicted by the power transfer theory at higher water conductivity, a higher density of power (207-263 [micro]W/[cm.sup.3]) was required than at lower water conductivity (58-87 [micro]W/[cm.sup.3]). When a pulse frequency of 30 Hz was applied, 33% more power was needed to elicit immobilization in high-conductivity as compared to low-conductivity water. This percentage decreased slightly (to 28%) when a 60-Hz pulse frequency was applied.

The range of voltage gradients eliciting leopard frog immobilization was 0.45-1.03 V/cm for tadpoles and 0.40-0.59 V/cm for recently metamorphosed frogs (Table 1). These values were slightly higher when standardized to a conductivity of 100 [micro]S/cm (0.67-1.68 V/cm) and, in general, the voltage gradient threshold was higher for tadpoles than for frogs (Fig. 3). Similar to power density, the voltage gradient resulting in immobilization of both species decreased from 15 to 60 Hz and was variable between frequencies of 60 and 120 Hz whereas the power density threshold increased as the voltage gradient decreased, as a function of higher ambient water conductivity, for leopard frog frogs (Fig. 2).

Among pulse frequencies of 15, 30, and 60 Hz, we observed an inverse relationship between pulse frequency and power density immobilization thresholds for the early life stages of bullfrogs and leopard frogs. A similar relationship between pulse frequency and immobilization power density thresholds, as well as voltage gradient thresholds, has been documented for fish (Taylor et al., 1957; Ruppert and Muth, 1997; Meismer, 1999; Miranda and Dolan, 2003).

We can identify similarities and differences in the effects of electricity between fishes and frogs by comparing the power density thresholds we derived in this investigation to those reported for fish. Using a large range of conductivities, Miranda and Dolan (2003) found the mean power density required to immobilize channel catfish, Ictalurus punctatus, (27-35 cm total length), using 15 Hz was 1,089 [micro]W/[cm.sup.3], similar to power density thresholds we derived for tadpoles. At pulse frequencies of 30, 60, and 110 Hz, the power density threshold required to immobilize channel catfish (D = 15-31 [micro]W/ [cm.sup.3]) was lower than for the 2 species of tadpoles we assessed (D = 175-762 [micro]W/[cm.sup.3]). The closest threshold to the lowest power densities observed for channel catfish was for leopard frog frogs (D = 58 [micro]W/[cm.sup.3]) in water conductivity of 250 [micro]S/cm and a pulse frequency of 60 Hz. Overall, channel catfish threshold values are lower than what we observed for tadpoles but not too different from frogs.

Voltage gradient is more-often reported in studies investigating the effects of electricity on fish than is power density. In our investigation, the lowest voltage gradients that elicited immobilization were 0.40-1.00 V/cm and, when standardized to 100[micro]S/cm, were 0.69-1.79 V/cm. Miranda and Dolan (2003) found the voltage gradient required to immobilize 95% of channel catfish was often <1.00 V/cm in water with conductivity >200 [micro]S/cm; the exceptions were trials conducted in lower ambient water conductivity and pulse frequencies of 15 and 20 Hz, where the gradient was as great as 8.00 V/cm. With pulse frequencies of 30 and 60 Hz and ambient water conductivity of 700 [micro]S/cm, Ruppert and Muth (1997) induced immobilization in humpback chub, Gila cypha, at gradients of 0.56-0.63 V/cm; a lower threshold than required for bonytail, Gila elegans, 0.61-0.73 V/cm. Similar to humpback chub and bonytail, voltage gradients <1.00 V/cm resulted in immobilization of rainbow trout, Oncorhynchus mykiss, (0.22 and 0.32 V/cm) and Colorado pikeminnow, Ptychocheilus lucius, (0.63 and 0.20 V/cm) using pulse frequencies of 15 and 60 Hz, respectively, in ambient water conductivity of 530 [micro]S/cm (Meismer, 1999). Although the voltage gradient thresholds derived from the literature can be compared to those derived in this investigation, it is still of limited use in understanding the quantity of energy transferred to an organism that results in immobilization.

Thus, we can employ formula (1) to obtain the power density threshold resulting in immobilization from the reported voltage gradients and associated water conductivities. For humpback chub the power density threshold would be 220-278 [micro]W/[cm.sup.3] and 260-373 [micro]W/[cm.sup.3] for bonytail. The conversion to power density for rainbow trout is 26-54 [micro]W/[cm.sup.3] and 21-203 [micro]W/[cm.sup.3] for Colorado pikeminnow. Considering pulse frequencies and ambient water conductivities, the density of power required to immobilize these fish is lower than what we observed for tadpoles but somewhat similar to that observed for frogs.

Research conducted to measure the susceptibility of various life stages of fish to injury and mortality from electrofishing has generated concern that electrofishing may adversely affect all life stages of frogs (Southwest Endangered Species Act Team, 2008). When reviewing such research, it is important to note the range of voltage gradients and resulting power densities. In many of the investigations of fish injury and mortality from electrofishing, voltage gradients used are often much greater than that necessary to induce immobilization. For example, work by Holliman et al. (2003), Henry and Grizzle (2004), and Henry et al. (2004) showed injury at power densities of 217-1,875 [micro]W/[cm.sup.3], 1,600-25,600 [mu]W/ c[m.sup.3], and 289-25,600 [micro]W/[cm.sup.3], respectively (power densities calculated using formula 1). Layhee (in litt.) studied sublethal and lethal effects of electricity on frogs by exposing two species of tadpoles to voltage gradients of 1.3-22.6 V/cm for 45 s using ambient water conductivity of ~654 [micro]S/cm (power density threshold ~1,105-334,037 [micro]W/[cm.sup.3]). While caution should always be used when electricity is employed to capture an organism, voltage gradients, power densities, and exposure time in several of the aforementioned studies are greater than what may be necessary to use in the field to immobilize fish or frogs. Indeed, based on equations provided by Novotny (1990), the voltage gradient for a spherical electrode ranging in diameter from 12.54-14.61 cm dissipates to <1.0 V/cm at approximately 35-40 cm from the electrode (J. C. Dean, pers. obser.; A.J. Temple, pers. comm.). Thus, to expose a frog to voltage gradients >1.0 in a stream or river environment, an electrode would have to be proximal to the animal.

Based on this work, the behavioral effect of low voltages on the early life stages of two ranids appears similar to that of fishes subjected to similar power densities. When we standardized immobilization power density thresholds by water conductivity for both species of tadpoles, the magnitude of power was similar. This preliminary study suggests that electrofishing power levels which induce immobilization in fishes are near the threshold for immobilization of young American bullfrogs and Southern leopard frogs and thus are likely lower than the threshold for injury or harm.

The following additional experiments would better allow assessment of electrofishing in waters containing frogs at various life stages: (1) Conduct studies in tanks with uniform electrical fields over a wide range of water conductivity to determine the effective conductivity for each species and life stage of interest; (2) Determine power density thresholds for injury and stress to tadpoles and frogs of selected species or surrogates; and (3) Develop injury and stress risk models for frog life stages over a range of power density thresholds and shock times. Once completed, it would be possible to make better predictions of risk to frog species and life stages when subjected to electrofishing activities designed to immobilize and capture target species.

We thank A. J. Temple for support of the experimental trials while at the New Mexico Principals and Techniques of Electrofishing Course. New Mexico Department of Game and Fish organized the course and financially supported EIG's participation. A. L. Barkalow, D. L. Propst, N. R. Franssen, and S. P. Platania provided helpful comments on prior versions of this manuscript.

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Submitted 5 September 2016. Accepted 4 April 2017.

Associate Editor was Neil B. Ford

Eliza I. Gilbert, * Jan C. Dean, and Mischele R. Maglothin

American Southwest Ichthyological Researchers, 800 Encino Place, Albuquerque, NM 87102; and Division of Fishes, Museum of Southwestern Biology, 1 University of New Mexico, Albuquerque, NM 87131 (EIG) Natchitoches National Fish Hatchery, 615 South Drive, Natchitoches, LA 71457 (JCD, MRM)

* Correspondent:

Caption: Fig. 1--Peak power density thresholds resulting in immobilization of tadpoles of American bullfrog, Lithobates catesbeianus (AB), and Southern leopard frog, Lithobates sphenocephalus (SLF), standardized to 100 [micro]S/cm ambient water conductivity using 4 pulse frequencies (15, 30, 60 and 120 Hz). Study was conducted in March and April 2012.

Caption: Fig. 2--Peak power density (closed symbols) and voltage gradient (open symbols) thresholds resulting in immobilization of Southern leopard frog, Lithobates sphenocephalus, frogs in low (250 [micro]S/cm) and high (1,291 [micro]S/cm) ambient water conductivities using 2 pulse frequencies (30 and 60 Hz). Study was conducted in March and April 2012.

Caption: Fig. 3--Peak voltage gradient thresholds resulting in immobilization of American bullfrog, Lithobates catesbeianus (AB) and Southern leopard frog, Lithobates sphenocephalus (SLF), in ambient water conductivity ([micro]S/cm) using 4 pulse frequencies (15, 30, 60, and 120 Hz) for tadpoles and two (30 and 60 Hz) for frogs. Study was conducted in March and April 2012.
Table 1--Low voltage trial conditions for experiments with American
bullfrog, Lithobates catesbeianus (AB), and Southern leopard frog,
Lithobates sphenocephalus (SLF), including peak power density and
voltage gradient thresholds resulting in immobilization of 2 tadpole
species (AB and SLF) and 1 frog species (SLF). Peak power density
(D; [micro]W/[cm.sup.3]) and voltage gradient (E; V/cm) standardized
to water conductivity of 100 [micro]S/cm, [D.sub.100] and
[E.sub.100], respectively. Study was conducted in March and April

                                    Ambient water
                           No.      conductivity    Water temp
Species and life stage   subjects   ([micro]S/cm)   ([driver]C)

American bullfrog           1             854          21.5
Tadpole                     1
Southern leopard frog       3           1,381          22.0
Tadpole                     2
Southern leopard frog       5             250          20.9
Frog                        5
Southern leopard frog       5           1,291          19.4
Frog                        5

                           No.      Frequency
Species and life stage   subjects     (Hz)       E       D

American bullfrog           1          15       1.00     854
Tadpole                     1          30       0.72     439
                            2          60       0.45     175
                            1         120       0.57     274
Southern leopard frog       3          15       1.03   1,461
Tadpole                     2          30       0.74     762
                            2          60       0.61     513
                            2         120       0.55     421
Southern leopard frog       5          30       0.59      87
Frog                        5          60       0.48      58
Southern leopard frog       5          30       0.45     263
Frog                        5          60       0.40     207

Species and life stage   subjects   [D.sub.100]   [E.sub.100]

American bullfrog           1           283       1.68
Tadpole                     1           147       1.21
                            2            59       0.76
                            1            91       0.95
Southern leopard frog       3           321       1.79
Tadpole                     2           168       1.29
                            2           113       1.06
                            2            93       0.96
Southern leopard frog       5            66       0.82
Frog                        5            44       0.67
Southern leopard frog       5            61       0.78
Frog                        5            48       0.69
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Title Annotation:Notes
Author:Gilbert, Eliza I.; Dean, Jan C.; Maglothin, Mischele R.
Publication:Southwestern Naturalist
Geographic Code:1USA
Date:Jun 1, 2017

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