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2 C.P. O’Connell et al. / Ocean & Coastal Management xxx (2012) 1e10 system, detecting bioelectric fields only centimeters away from prey to help the elasmobranch better pinpoint that prey prior to feeding (Kajiura and Holland, 2002; Kajiura, 2003). Evidence also supports that elasmobranchs use this sensory system to detect geomagnetic fields assisting in the determination of geolocation and navigation (Klimley, 1993; Klimley et al., 2002). The latter, semiochemicals, appear to target the olfactory senses of elasmobranchs and appear to function as a Schreckstoff, or chemical alarm signal (von Frisch, 1938; Stroud, 2008b), producing a Schreckreaktion, or flight reaction, that is highly selective. Each potential repellent; magnets, EPMs, and semiochemicals, are hypothesized to operate under different mechanisms, each of which are described below. 1.1. Ampullae of Lorenzini Elasmobranchs differ from bony fishes (teleosts) in various ways, but a key difference is that an elasmobranch possesses an electrosensory system known as the ampullae of Lorenzini. The ampullae of Lorenzini were first discovered by Marcello Malpighi in 1663, but described in detail by Stephano Lorenzini in 1678 (Budker, 1971), after whom they were named. However, the function of these receptors remained unknown until Dijkgraaf and Kalmijn (1963, 1966; cited by Kalmijn, 1971, 1982) demonstrated the electrosensitivity of these receptors, with additional experimentation showing these receptors have mechanical and thermal sensitivities (Boord and Campbell, 1977; Brown et al., 2003; Murray, 1957, 1960). The ampullae of Lorenzini are acute electrosensory organs composed of minute jelly-filled pores located around the cephalic region of elasmobranchs (Fig. 1). Each ampullae contains a pore at the surface of the skin, which connects to a subcutaneous canal filled with conductive jelly (Kalmijn, 1966, 1971, 1974, 2000; Bastian, 1994). As an elasmobranch encounters a weak electrical impulse, such as that associated with muscle contraction (e.g. a fish’s heartbeat) or the associated electrical charges originating from gill movement, the voltage external to the pores of the ampullae differs from the interior voltage potential. This voltage gradient is perceived and a sensory message is sent to the brain via an impulse from the afferent neurons. It has been suggested that elasmobranchs detect magnetic fields in a similar manner using this electrosensory system, but through a different mechanism known as indirect-based magnetoreception via electromagnetic induction (Kalmijn, 1973, 1974, 1982, 1984; Carey and Scharold, 1990; Klimley, 1993; Holland et al., 1999) which will be described in more detail in the following section. 1.2. Magnetic repellent concept Magnets vary by composition, strength, axis of polarization, size and shape. More specifically, the permanent magnets typically used in the current shark behavioral studies are ceramic magnets that do not degrade in seawater (e.g. bariumeferrite magnets-BaFe 12 O 19 ; Rigg et al., 2009; O’Connell et al., 2010, 2011a, 2011b) and rare-earth magnets that degrade in seawater (e.g. neodymiumeironeboron magnets-Nd 2 Fe 14 B; O’Connell et al., 2011b; Robbins et al., 2011). The magnetic flux associated with ceramic magnets is generally weaker (e.g. 3850 G) than rare-earth magnets (e.g. 14,800 G), whereas the axis of polarization exists in a variety of combinations regardless of magnet-type. The most current explanation as to how elasmobranchs detect magnetic fields is through the process of indirect magnetoreception by electromagnetic induction, or induced electric fields that arise when an object moves through a magnetic field (Kalmijn, 1973, 1982, 1984). Through electromagnetic induction there are two proposed mechanisms on how elasmobranchs can detect magnetic fields: (1) active mode and (2) passive mode (Kalmijn, 1981, 1984; Montgomery and Walker, 2001). In active mode, as an elasmobranch is swimming with a horizontal velocity through the horizontal component of the Earth’s geomagnetic field, a vertical electromotive field is induced (Fig. 2a; Kalmijn, 1997; Montgomery and Walker, 2001). Paulin (1995) modified the concept of the active mode and stated that directional cues could originate from variations in induced electroreceptor voltage produced during turns (Montgomery and Walker, 2001). In passive mode, as electrically charged seawater moves through the vertical component of the Earth’s geomagnetic field, an electromotive field, which may be detected and utilized by an elasmobranch, is produced in the horizontal direction (Fig. 2b). The geomagnetic field on the Earth’s surface ranges from 0.25 to 0.65 G (G). In comparison, the magnetic field associated with a bariumeferrite magnet (BaFe 12 O 19 ), produces a maximum flux of approximately 1000 G. It is hypothesized that a much stronger electromotive field will be induced by a permanent magnet and therefore will overstimulate the ampullae of Lorenzini of an approaching elasmobranch, thus producing a repellent response (WWF, 2006). Although electromagnetic induction is the current explanation as to how elasmobranchs detect the Earth’s geomagnetic field, firm evidence that this process governs magnetic field detection in elasmobranchs has yet to be presented and therefore further experimentation is needed. 1.3. Electropositive metal concept Fig. 1. The ampullae of Lorenzini of a tiger shark (Galeocerdo cuvier). The ampullary pores are represented by the black dots located around the cephalic region of the shark. Ó Craig O’Connell. Electropositive metals (EPMs) can be found in Group I (e.g. Lithium), Group II (e.g. Magnesium), Group III (e.g. Yttrium), Group IIIA (the Lanthanides), and Group IIIB (the Actinoids) of the Periodic Table of the Elements. Magnesium and the lanthanide metals find the most practical application in shark bycatch reduction, producing standard reduction potentials of approximately 1.8 eV in water, a voltage that is orders of magnitude greater in strength than the bioelectric fields (i.e. nanovolts) that are encountered by elasmobranchs in search of prey. As an elasmobranch approaches the metal through the conductive seawater electrolyte, three potential scenarios exist: (1) the shark, whose skin is much more electronegative than the metal, completes a galvanic cell, or electrochemical cell that derives energy from spontaneous reductione Please cite this article in press as: O’Connell, C.P., et al., The emerging field of electrosensory and semiochemical shark repellents: Mechanisms of detection, overview of past studies, and future directions, Ocean & Coastal Management (2012), http://dx.doi.org/10.1016/ j.ocecoaman.2012.11.005
C.P. O’Connell et al. / Ocean & Coastal Management xxx (2012) 1e10 3 Fig. 2. a) ‘Active mode’ e Vertical induced electrical currents are produced as the shark swims through the horizontal component of the Earth’s magnetic field. The induced electrical current moves in a direction which opposes the change in magnetic field (Lenz’s Law). Illustration modified from Kalmijn (1974). b)‘Passive mode’ e Horizontal induced electrical currents are produced by the movement of ocean streams (i.e. currents) through the vertical component of the Earth’s magnetic field. Illustration modified from Montgomery and Walker (2001). oxidation (redox) reactions, to the metal and experiences a net charge increase that is detected by the ampullae and perceived as repellent, (2) the hydrated metal cation (aquo ion) is a weak Lewis acid, or electron pair acceptor, and therefore repellent to the shark purely on low pH/irritancy effects, and (3) a shark retreats due to induced currents which are generated perpendicular to the resultant electric field (Rice, 2008; Stroud, 2008a: Fig. 3). 1.4. Semiochemical repellent concept Elasmobranchs are considered to have a highly developed sense of smell which is evidenced by their large olfactory epithelial surface area (Schluessel et al., 2008). Due to this, elasmobranchs are highly responsive to very small concentrations of odor molecules, particularly those of amino acids (Tricas et al., 2009). Beginning in 1990, several studies aimed to take advantage of an elasmobranchs acute sense of smell and demonstrated that elasmobranchs are chemically aware of semiochemicals derived from decaying sharks (Stroud, 2008b) and predatory heterospecifics (Rasmussen and Schmidt, 1992). Semiochemicals are signals which animals may utilize to assist with mate selection (Nieberding et al., 2008), foraging (Tumlinson et al., 1993), aggregation (Verheggen et al., 2010) or navigation within their respected ecosystems, but semiochemical derived from decaying shark tissue causes a reaction which is reminiscent of a “Schreckreaktion”, originally termed by von Frisch (1938) and is defined by the fright reaction of European minnows (Phoxinus phoxinus) when detecting the chemicals from an injured conspecific. Thus far, no published field work in the scientific literature exists on the newly discovered elasmobranchderived semiochemicals. 2. Brief overview of electrosensory repellent studies To date, a total of eleven studies have been conducted which aimed to determine the effects of magnetic (Table 1) and EPM alloy (Table 2) stimuli on elasmobranch behavior. These studies can be classified into three categories based on the experimental focus and/or potential applications: (1) basic or proof-of-concept research, (2) recreational and commercial fishing applications, and (3) beach net applications. The findings from each of these eleven studies were highly inconsistent, which may stem from inexperience with using these materials. As with many new emerging fields, there is a learning curve, and the field of electrosensory repellents is in its infancy and requires substantially more field and laboratory investigations prior to the dismissal or implementation of any of these materials. 2.1. Basic or proof-of-concept research Fig. 3. This figure represents the mechanism behind electropositive metal detection in elasmobranchs. When an electropositive metal is placed in seawater, it undergoes spontaneous hydrolysis generating hydrogen gas and metal hydroxide which precipitates out of solution. The hypothesized mechanism behind the repellent capabilities of the EPM alloys occurs as the cations transfer to the approaching electronegative shark (i.e. a galvanic cell). This build up of positively charged ions overwhelms the ampullae of Lorenzini and is the most current explanation for the observed deterrent capabilities of the repellents; however, another hypothesized explanation is that a shark may retreat due to the associated induced current which is produced from the electric field/ magnetic field. Illustration modified from Rice (2008). Four studies have been conducted which serve as proof-ofconcept experiments, or basic experiments exploring the efficacy of electrosensory repellents, on several elasmobranch species. In 2008, a study was conducted which examined the behavior of Galapagos (Carcharhinus galapagensis) and sandbar (Carcharhinus plumbeus) sharks to NdePr (neodymiumepraseodymium) metal, a type of EPM (Wang et al., 2008). Results demonstrate that sharks fed more frequently from the lead-weight controls with a significantly greater quantity of aversive behaviors (e.g. sharp turns and cease feeding) toward the NdePr metal illustrating the potential utility of these electrosensory stimuli for recreational and commercial fishing applications (Fig. 4a). In a laboratory study, Rigg et al. (2009) evaluated the effects of ferrite magnets on five elasmobranch bycatch species; scalloped hammerhead shark (Sphyrna lewini), Australian blacktip shark (Carcharhinus tilstoni), gray reef shark (Carcharhinus amblyrhynchos), milk shark (Rhizoprionodon acutus), and speartooth shark (Glyphis glyphis), as well as the teleost species, the seabass (Lates calcarifer). Results from this study demonstrated that all elasmobranch species responded at distances ranging from 0.26 to 0.58 m from the magnets and no signs of habituation were observed, with Please cite this article in press as: O’Connell, C.P., et al., The emerging field of electrosensory and semiochemical shark repellents: Mechanisms of detection, overview of past studies, and future directions, Ocean & Coastal Management (2012), http://dx.doi.org/10.1016/ j.ocecoaman.2012.11.005
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