AnimalBiology ,Vol.54, No. 1, pp. 1-25 (2004) Ó KoninklijkeBrill NV ,Leiden,2004. Alsoavailable online - www.brill.nl

Thefunctional rolesof passive electroreception innon-electricŽ shes

SHAUNP .COLLIN 1 andDARR YLWHITEHEAD 2;

1 Departmentof Anatomyand Developmental Biology, School of Biomedical Sciences 2 Centrefor Marine Studies, The University of Queensland, Brisbane 4072, Queensland, Australia

Abstract—Passiveelectroreception is a complexand specialised sense found in a largerange of aquaticvertebrates primarily designed for the detection of weak bioelectric Ž elds.Particular attention hastraditionally focused on cartilaginous Ž shes,but a rangeof teleost and non-teleost Ž shesfrom adiversityof habitats have also been examined. As more species are investigated, it has become apparentthat the role of electroreception in Žshesis not restricted to locatingprey, but is utilised in othercomplex behaviours. This paper presents the variousfunctional roles of passive electroreception innon-electric Ž shes,by reviewing much of the recent research on the detection of prey in thecontext ofdifferencesin species’habitat (shallow water, deep-sea, freshwater and saltwater). A specialcase studyon the distribution and neural groupings of ampullary organs in the omnihaline bull shark, Carcharhinusleucas ,isalsopresented and reveals that prey-capture, rather than navigation, may be animportant determinant of pore distribution. The discrimination between potential predators and conspeciŽcs and the role of bioelectric stimuli in social behaviour is discussed, as is the ability tomigrate over short or long distances in order to locate environmentally favourable conditions. Thevarious theories proposed regarding the importance and mediation of geomagnetic orientation byeither an electroreceptive and/ ora magnetite-basedsensory system receives particular attention. Theimportance of electroreception to manyspecies is emphasisedby highlighting what still remains tobe investigated, especially with respect to the physical, biochemical and neural properties of the ampullaryorgans and the signals that give rise to the large range of observedbehaviours.

Keywords:ampullaeof Lorenzini; electric Ž elds;migration; orientation; passive electroreception; predation.

1.INTRODUCTION Electroreceptionis anancient sensorymodality ,havingevolved more than 500 million years ago,and has beenlost andsubsequently ‘ re-evolved’a numberof

Correspondingauthor; e-mail: [email protected]. au 2 S.P.Collin& D.Whitehead

Figure 1. Schematicdistribution of electroreceptionin groupsof livingŽ sheswith only some of the majorgroups shown. Example species of somegroups are noted. Groups possessing electroreception arenoted by a check( );non-electroreceptivegroups with a ( ).ModiŽed from von der Emde, 1998. times invarious vertebrate classes (Žg. 1) (New, 1997; von der Emde, 1998; Alves-Gomez,2001). The multiple andindependent evolution of electroreception emphasises the importanceof this sense in avariety ofaquatic environments. Electroreceptive sensoryorgans can be broadly categorised intotwo distinct classes, ampullaryand tuberous, based primarily uponthe cellular morphologyof Functionalroles of electroreception 3 the receptororgans and secondarily on their respective frequencytuning character- istics (Szabo,1974; Zakon, 1986; New and Tricas, 1997).Ampullary receptors are broadlytuned to lowfrequency Ž elds ( <0.1-25Hz), while tuberousreceptors are tunedto higherfrequency Ž elds from50 Hz to over2 kHz(New, 1997). Thought to bea primitive vertebrate character,the ability to detect weakelectric Želds in Žshes has thus far beenfound in agnathans(lampreys butnot hagŽ shes, Bullocket al., 1983),chondrichthyans (sharks, skates, rays andchimeras, Bullocket al., 1983; Bodznickand Boord, 1986; Fields et al., 1993;New and Tricas, 1997),cladistians (bichirs, Jørgensen, 1982), chondrosteans (sturgeons and paddleŽ sh, Teeter et al., 1980;Northcutt, 1986) and a small numberof species within the osteoglossomorph (knifeŽ shes, Braford,1982; Bullock and Northcutt, 1982; Carr andMaler, 1986; Zakon,1988) and three ordersof teleosts; mormyrids(African electric Žshes, Liss- mann,1958; Bell andSzabo, 1986), gymnotids (South American electric Žshes, Lissmann,1958; Carr andMaler, 1986;Zakon, 1988), and siluriform (catŽsh, Parker andvan Heusen, 1917; Roth, 1968; Finger, 1986; Whitehead et al., 1999,2003) groupsof Žshes (Žg. 1).Electroreception has also beenfound within the sister group ofthe actinopterygianŽ shes, the Sarcopterygii,which comprises the dipnoanlung- Žshes (Northcutt,1986; Watt et al., 1999)and the actinistian coelacanth(Bemis and Hetherington,1982). Inmost ofthese groups,the ampullaryelectroreceptors are usedto detect animate andinanimate electric Želds, bymeasuring minute changes in potential between the water at the skinsurface andthe basal surface ofthe receptorcells. Inelasmo- branchs,ampullae ofLorenzini (Lorenzini, 1678) typically consist ofan elongated epithelial canal terminating in anumberof alveoli eachcontaining hundreds of re- ceptorcells andlocated belowthe surface ofthe epidermis, communicatingwith the surroundingwater via acanal (Žg. 2). The canal walls are formedby squamous epithelial cells joinedby tight junctions,which create ahighresistance (Waltman, 1966).The canals are Žlled with amucopolysaccharidejelly andmay radiate in all directions fromthe ampullaryclusters, providinga methodof directionally sam- plingthe electric Želd surroundingthe animal (Kalmijn, 1974;Murray ,1974).In some marine elasmobranchs,up to 400ampullary tubes radiate froma single clus- ter (Chuand W en,1979). The clusters are restricted tothe headin sharks, but are also distributed overthe pectoral Žns in skates andrays. The typical ampullae in teleosts are similar butare characterised byshorter canals (e.g.50-200 ¹m in Plo- tosus tandanus and Ameiurusnebulosus ,in contrast to upto 20cm longin some species ofrays,Murray, 1974; Whitehead et al., 2003)and typically fewerreceptor cells perampulla (eight to20 inthe catŽsh, Kryptopterus bicirrhus ,incontrast to hundredsper sensory organ in the elasmobranchs; Zakon,1986). In both groups, the structure ofelectroreceptors varies with habitat. Freshwater species haveshort canals andlow numbers of receptorcells (Žg. 2),in comparisonwith longcanals andnumerous receptor cells inmarine species (Zakon,1986, 1988). One afferent Žbretypically innervates eachorgan or cluster oforgansin teleosts (see reviewin Zakon,1986, 1988) in contrast to the situation in elasmobranchs,where up to thou- 4 S.P.Collin& D.Whitehead

Figure 2. Schematicdiagram of sensory organs utilised in electroreception in Ž shes.A: Representa- tiveform of anampulla common to freshwater teleosts; B: Genericexample of an ampullaof Lorenzini froma freshwaterstingray; C, canal;E, epidermis;N, nerve;RC, receptorcells; SC, supportivecells. sands ofreceptor cells withina single alveolus are contactedby upto 15afferent Žbres (Szabo,1974). Thearrangement of electroreceptors distributed overthe headof elasmobranchs are groupedinto discrete subdermalclusters innervatedprimarily bydifferent branchesof the anterior lateral line nerve(Norris, 1929; Northcutt, 1978). Epider- mal poresand the jelly-Žlled canals comprisingeach electroreceptive organensure that the potential withinthe ampullarylumen remains close tothat at the skinsur- face.The hair cells ofeach receptor act as voltagedetectors andrelease neuro- transmitter ontothe primaryafferent neuronsaccording to the differencebetween the basal andapical potentials (Tricas, 2001).The primary afferent neuronsen- codestimulus amplitude andfrequency data that is sent to the brain(Montgomery, 1984;Tricas andNew, 1998), where a sophisticated set ofŽ lter mechanisms are usedfor extracting the weakelectrosensory signals froma muchstronger back- groundnoise, predominantly created bythe animal’s ownmovements (see review byBodznicket al., 2003).Therefore, the distribution ofthe ampullaryorgans may provideinformation about the electric Želd’s intensity,its spatial conŽguration and possiblythe direction ofits source(Tricas, 2001).However, only a fewworkers haveinterpreted the spatial arrangementof the electroreceptors in the contextof the natural ecologyof the animal (Rashi, 1986;Raschi andAdams, 1988; Fishelson and Baranes,1998; Kajiura, 2001; Raschi et al., 2001;Tricas, 2001). Althoughthe tuberouselectroreceptors foundin the mormyridand gymnotiform groupsof Ž shes are usedin high frequency electroreception, they are largely Functionalroles of electroreception 5 tunedto the dominantspectral frequenciesof the individual’s ownelectric organ discharges rather thanthe weakelectric Želds producedby other organisms or environmentally-inducedelectric Želds (see reviews byBullock, 1982; Bullock and Heiligenberg,1986; Turner et al., 1999).This reviewwill concentratesolely onthe roles ofpassive electroreception innon-electric Žshes and,for the sake ofbrevity, active electroreception andelectrocommunication will notbe examined.

2.LOCALISING PREY INDIFFERENT HABITATS Behaviouralstudies haverevealed that electroreception has evolvedto detect prey, wherelow frequency bioelectric Želds emanatingfrom prey are detected using ampullaryorgans. These ampullae respondto DC orlow frequency electric Želds, e.g.,1-8 Hz inelasmobranchs (Montgomery ,1984)and 6-12 Hz insilurid teleosts (Peters andBewalda, 1972). Elasmobranchs are able to respondphysiologically and behaviourallyto weak, low frequency electric Želds of10 nV/ cm and5 nV/cm, respectively (Dijkgraafand Kalmijn, 1962,1966; Kalmijn, 1982).The behavioural relevanceof this level ofsensitivity was uncoveredin aseries ofexperiments involvingboth experimental andfree-living elasmobranchs,which induce feeding responses towardseither buriedŽ sh ora pair ofburied electrodes that couldnot otherwise bedetected usingother sensory modalities. Feedingwas subsequently terminated whenthe bioelectric Želd ofeither sourcewas maskedby thin plastic Žlm (Kalmijn, 1971,1982). Therefore, the highsensitivity ofelectroreceptors enables them to localise preyby detecting the veryfaint potentials associated with the ionic leakageof the gills (modulatedby ventilatory movements) of buriedteleosts. Woundedcrustaceans producehigh bioelectric Želds (1000 ¹V/cm, Kalmijn, 1972).W att et al. (1999)have also shownthat the ampullaryorgans in the Australian lungŽsh, Neoceratodusforsteri use passive electroreception to perceiveweak electric Želds emanatingfrom hidden prey in muchthe same way as elasmobranchs.A major differencemay be in the morphologyof the receptor cell, whichin N. forsteri possesses asingle apical cilium (as in elasmobranchs)but with apronouncedswelling (Jørgensen, 1984) in contrast to the receptorcells in the AfricanlungŽ sh, Protopterus dolloi ,whichpossesses asingle kinocilium and several short microvilli (Rothand Tscharntke, 1976). Preydiscrimination andfeeding behaviour in electroreceptive vertebrates varies enormously(see reviewby Motta andWilga, 2001, for elasmobranchs). In both the stingray, Dasyatis sabina, andthe swell shark, Cephaloscylliumventriosum , electroreceptors are usedto locate concealedprey in additionto enablingnocturnal predation(Tricas, 1982;Blonder and Alevizon, 1988). The paddleŽ sh, Polyodon spathula,possesses arostrum (notunlike that ofthe platypus; Pettigrew and Wilkens,2003) that is adornedwith ampullaryelectroreceptors whichact as an antenna,a sensorydevice with sufŽcient sensitivity to detect the electric Želds of planktonicprey with a sensitivity thresholdof 10 ¹V/cm,a considerablyhigher sensitivity thanthe sensitivity ofindividualelectroreceptors (Wilkens et al., 1997; 6 S.P.Collin& D.Whitehead

Figure 3. Thelocalisation of preyby an elasmobranch using its electroreceptors to detect bioelectrical Želds.A: Anexample of the dipole Ž eldradiating from a preyspecies. A typicalshark will be guided toattack the source according to thechanges in the direction of the electrical Ž eldit encounters;B: A representativedipole Ž eld,with 2-5 nV/ cmmarkers,and the approach pass predicted by Kalmijn’ s algorithm.The radiating Ž eldlines correlate with the loops drawn in A.Afeedingshark will recognise theelectrical Ž eldsat the position of the Ž rstmarker (2 nV/ cm)and willdirect an attackupon reaching theapproximate position of thefourth marker (5 nV/ cm).Figure adapted from Kalmijn (1997).

Russell et al., 1999).The paddleŽsh uses this rostrum tolaterally strike at planktonic preyusing its electric sense passively withoutthe use ofvisual, chemical and hydrodynamicsenses at distances of8-9 cm. A theoretical mechanism inwhich sharks orrays process directional informationin the immediate vicinity has also beenpresented by Kalmijn (1988,2003). This approachalgorithm predicts that as ananimal enters alocal electric Želd (emanatingfrom potential prey)it corrects its swimmingcourse to keepthe anglebetween its rostro-caudalbody axis and the detected electric Želd constant (Žg. 3). Kalmijn (1974,1988) suggests that all behaviouraltrials are consistent with this algorithm,which is insensitive to the angleof approach, the polarity ofthe prey’s Želd,changes in the strength andthe direction ofthe Želd andto the positionof its source(Kalmijn, 2003).Recently, bioelectric Želds andlow frequency acoustic Želds havebeen compared and it is thoughtthat elasmobranchsuse similar algorithms tolocalise preysince innerear hair cells donot detect the straight line direction to the source,but the direction ofthe curvedmultipole Želd lines at the position ofthe headand along the sides ofthe body(Kalmijn, 2000,2003). A combinationof olfactory and electrosensory inputis hypothesisedto beresponsible forthe exploratoryfeeding behaviour in the reef-dwellingepaulette shark, Hemiscyllium ocellatum (Heupeland Bennett, 1998).

2.1.Spatial distribution of electroreceptors andits role in prey detection Manyelectroreceptive species showa widevariation in receptornumber and distribution, reecting differences in habitat andfeeding strategies rather thanany phylogeneticrelationships. Skates andrays are dorsally compressed,while the bodyform of sharks is moreconical. Therefore, the distribution ofpores over the headof skates andrays are most sensitive toonly the horizontalcomponent of anelectric Želd,while the poresin sharks are able to providesensitivity in three dimensions (Tricas, 2001).After anextensive analysis of40 species ofskates, Functionalroles of electroreception 7

Table 1. Meantotal counts and the ratio of ampullarypores over the dorsal and ventral regions of a rangeof elasmobranchs

Species(Number examined) Dorsal % Ventral% Total Source Sphyrnalewini (9) 126141.12 1806 58.88 3067 Kajiura,2001 Sphyrnalewini (9) 142550.46 1399 49.54 2824 Daniels,1967 Sphyrnatiburo (19) 92145.41 1107 54.59 2028 Kajiura,2001 Carcharhinusplumbeus (9) 116850.41 1149 49.59 2317 Kajiura,2001 Carcharhinusplumbeus (9) 118453.19 1042 46.81 2226 Raschiet al., 2001 Carcharhinusleucas (4) 84441.13 1208 58.87 2052 This study Carcharhinusobscurus (7) 86848.46 923 51.54 1791 Raschiet al., 2001 Cacharhinusamblyrhynchos (1)722 50.14 718 49.86 1440 Daniels,1967 Triakissemifasciata (2) 76652.18 702 47.82 1468 Daniels,1967 Odontaspistaurus (2) 47846.41 552 53.59 1030 Raschiet al., 2001 Galeoerdocuvier (5) 37142.40 504 57.60 875 Raschiet al., 2001

Raschi (1986)revealed spatial differences inthe density ofampullae. Species that feedpredominantly on benthicinvertebrates possess highdensities ofpores on the ventral surface,especially aroundthe mouth,providing a greater resolution for locating,manipulating and ingesting preyexcavated from the substrate (Raschi, 1986;Tricas, 2001).On the otherhand, skates that feedon more mobile Žsh prey possess lowpore densities, wherethe needfor increased resolutionis notas critical andmay be concomitantly mediated bythe visual system (Collin, 1988). Hammerheadsharks (Sphynidae),with their uniquecephalofoil head morphology (Compagno,1984; Kajuira, 2001) constitute anintermediary betweenthe attened disc ofskates andrays andthe conical headshape of pelagic carcharinids.Sphyrnids possess ahighernumber of pores on the ventral surface ofthe head(table 1),while the sandbarshark Carcharhinusplumbeus possesses aneven distribution overboth the dorsal andventral surfaces ofthe head(Kajiura, 2001). Thesedifferences in poredistribution mayrelate to feedingecology in these species ofsharks, where the addedability to capturesmall Žshes in the water columnby the sandbarshark, in additionto benthiccrustaceans, mayrepresent a speciŽc adaptation(Medved et al., 1985;Cortes et al., 1996).Juvenile scalloped hammerheadpups possess highdensities ofelectrosensory poresproviding Ž ner spatial resolution that enables the sharkto determine the location ofanelectrical stimulus nearthe bodysurface, especially inthe turbidbays in whichvision maybe limited (Raschi, 1978;Compagno, 1984; Kajiura, 2001). With age,the poredensity decreases, spacedfurther apart presumablyto increase the amountof lateral area sampled bythe head.The decreased spatial resolution mayalso notbe required giventhe role visionplays in the clearer oceanicwater this species frequentsas an adult (Compagno,1984). Incontrast, the arrangementof poresover the headof the white shark, Carchar- odoncarcharias, reveals that manyof the ampullae (especially the superŽcial oph- thalmic canals) are located withinthe frontal visual Želd (Litherland,2001; Tricas, 8 S.P.Collin& D.Whitehead

2001),and may be utilised ina different typeof feeding strategy .Tricas (2001) hypothesisedthat speciŽc ampullarysystems maymediate different electrosensory behaviours.The dorsal,lateral andventral superŽcial ophthalmiccanal systems may providegood spatial resolution fordetection andtracking of nearbyprey at night, whenthe eyes are closed (i.e. duringthe Žnal stages ofpredatory attack) orwhen the preylies beneaththe snout(Tricas, 2001).Therefore, there maybe aclose relation- ship betweenthe relative developmentof the visual andelectroreceptive systems. Feedingpreferences for benthic prey favour enhanced electroreceptive inputwhile feedingpreferences for pelagic preytend to favour enhanced visual input(Raschi andAdams, 1988; Raschi et al., 2001).However, further study is requiredto relate differences in ampulla size, location,density andprojection pattern with behaviour. Irrespective ofthe location andspatial resolution ofthe ampullae,the electrosense is onlya short rangesense forprey detection withthe ability to detect bothAC andDC bioelectric potentials at close range(at least formarine elasmobranchs) andis most likely augmentedby visual (Collin, 1988;Bozzano and Collin, 2000), chemoreceptive(Kleerekoper et al., 1975)and mechanoreceptive (Montgomery and Skipworth,1997) input in the localisation andsuccessful captureof prey(Haine et al., 2001).

2.2.A case study onthe distribution ofampullaryorgans in the bullshark, Carcharhinusleucas Thebull shark, Carcharhinusleucas is relatively uniquesince it cantravel freely betweenboth saltwater andfreshwater andis knownto navigate long distances in bothenvironments (Thorson, 1971; Compagno and Cook, 1995). Here we present adetailed description ofboth pore distribution andthe location ofclusters of ampullaryorgans in this omnihalinespecies tohelp elucidate apparentdifferences inpore distribution betweenskates andrays (with anuneven distribution) andmany sharks (with aneven distribution). Poredistribution andthe neuralgroupings of ampullae ofLorenzini in juvenile, freshwater specimens ofthe bullshark, Carcharhinusleucas (SL534-680 mm), wereexamined by placing a squarecm gridof monoŽ lament overthe skinsur- face offourspecimens. Porepositions weresubsequently transferred to gridpaper. Specimens wereconsidered dorso-ventrally  attened to assist in the placement of grids.Ampullae in all fourspecimens weretraced fromtheir poreto the alveoli andsite ofinnervation.These studies reveal that the poresare widelyspread over the skin ofthe head.Resembling those describedfor other indiscriminate feeding sharks (table 1), C. leucas possesses fewerdorsal (41.5%)than ventral poreswith the antero-ventralsurface ofthe headcontaining the highest densities (Žg. 4).The ampullaryorgans are organisedinto three neuralgroups; the superŽcial ophthalmic, the outerbuccal, and the mandibular(Ž g. 5)basedupon their innervationby primary branchesof the anterior lateral line nerve,as describedby Norris (1929). TheŽ rst ofthese groups,the superŽcial ophthalmic,consists ofŽveindependent clusters ofampullary organs, most ofwhichare located in the proximalregion of the Functionalroles of electroreception 9

Figure 4. Distributionof theampullae of Lorenzini(dots) on thedorsal (right hand panels) and ventral (lefthand panels) surface of three species of elasmobranchs. A: Sphyrnalewini; B: Carcharhinus plumbeus; C: Carcharhinusleucas. AandB areadapted from Kajiura (2001). 10 S.P.Collin& D.Whitehead

Figure 5. Lateralview of thehead of abullshark, Carcharhinusleucas showinga longitudinalview oftheampullary system from an 840 mm TL, femalespecimen. The neural groupings of ampullae ofLorenzini are represented according to their position in the head. M, mandibular;OB, outer buccal;SOd, superŽ cial ophthalmic dorsal; SOp, superŽ cial ophthalmic proximal; SOv, superŽ cial ophthalmicventral. The superŽ cial ophthalmic lateral groups are omitted due to theirabsence along themidline. The relative position of the nare and eye are included in this drawing for points of reference. head.Ampullary organs within eachcluster conveyafferent inputto the superŽcial ophthalmicbranch of the anterior lateral line nerve.The Ž rst cluster ofampullary organs,the superŽcial ophthalmicproximal, is situated betweenthe snouttip andthe rostrum (Žg. 5).This cluster joins canals that extendboth to the dorsal andventral areas ofthe snoutapex. The second cluster ofampullae,the superŽcial ophthalmic dorsal,consists ofa pair ofampullary clusters connectedto canals, whichterminate alongthe dorsal surface ofthe shark’s headfrom the snoutto anarea just proximal tothe Žrst gill slit. Asmall numberof ampullarycanals extendto the lateral edges ofthe snout.A third groupof ampullae is positioneddirectly ventral to the previous cluster ofampullae (Žg. 5). These ampullae are chiey encircled bythe tripodal rostrum.This subgroup of ampullae connectsto canals that terminate alongthe ventral area ofthe snoutposteriorly to the maxillary jaw.T woadditional clusters ofampullae are located in this regionof the headof C. leucas.ThesesuperŽ cial ophthalmiclateral groupsof ampullae are located proximalto the lateral wall of Functionalroles of electroreception 11 the anterior fontanelle slightly abovethe lateral rostral cartilage. Theampullae containedin these functionalunits are attached to canals that extendto the ventral, lateral, anddorsal surface areas ofthe snout. Thesecond grouping of ampullary organs is located betweenthe anterior wall ofthe preorbital process andthe posterior wall ofthe nasal capsules. Ampullae containedin these groupsare connectedchie y to the outerbuccal nerves. The ampullae ofthese buccalclusters are adjoinedto poresfrom the lateral headareas, bothanterior andposterior to the eyes (Žg. 5). The last groupingof ampullae ofLorenzini comprises apair ofsmall mandibularclusters ofampullae located posterior to the medial regionof the mandible(Ž g. 5). Theuneven distribution ofampullary pores over the dorsal andventral surfaces of C. leucas suggests this species uses electroreception primarily forspatial discrim- ination ofprey and secondarily for migratory purposes (Kalmijn, 1978;Raschi et al., 2001),yet C. leucas are knownto movevast distances alongcoastal shorelines, inaddition to movements between marine andfreshwater habitats (Thorson1971; Bass, 1978).These travels betweenmarine andfreshwater conditionsmay hold an important clue tothe variation ofampullarypore distribution observedin otherstud- ies. Wepredict that the determinant ofporedistribution is principally preycapture, rather thannavigation. The higher density ofampullary organs in the antero-ventral areas ofthe headsuggests ahighdependence on electroreception inthe captureof Žshand other prey in dark,murky waters characteristic ofmanycoastal estuaries andriverways. The average number of ampullary organs (2052) found in juvenile C. leucas is in agreementwith the characteristically highnumbers of organs in other carcharhinids(table 1).These high concentrations of ampullary organs are indica- tive ofspecies that frequentmurky inshore waters and,therefore, do notrely heavily on vision.

2.3.Localising prey in saltwater andfreshwater Canal lengthvaries signiŽcantly in the electroreceptors ofsaltwater andfreshwater vertebrates andis thoughtto bean adaptation for increasing sensitivity (Bennett, 1971;Szabo et al., 1972;Kalmijn, 1974;Whitehead et al., 1999,2003). The longcanals ofelasmobranchs enable low frequency electric Želds to bevirtually unattenuateddue to the highresistance ofthe canal walls andthe lowresistance ofthe jelly core.Therefore, marine ampullaryreceptors enhancethe sensitivity to voltagegradients since there is arelatively small transepidermal voltagedifference dueto a relatively lowskin resistance. Incontrast, the resistance ofthe skinof freshwater Žshes is veryhigh, due to its role in osmoregulation.Since the skin in these teleosts has amuchlarger resistance thanthe internal tissues, alongcanal is unnecessary,wherea more‘ superŽcial’ organ will detect alarge voltagedrop (Zakon,1988). Despite the twomethods of measuringpotential differences,marine elasmobranchsare sensitive tovoltage gradients ofat least 5nV/cm,while the freshwater ray, Potamotrygoncircularis, is sensitive to gradients between50 and 100 ¹V/cm (Szaboet al., 1972).Similarly ,some marine catŽsh are at least oneorder 12 S.P.Collin& D.Whitehead ofmagnitude more sensitive (0.08 ¹V/cm,Kalmijn, 1988)than some freshwater teleosts (1 ¹V/cm,Finger, 1986; Zakon, 1988). Theeffects ofhabitat salinity onthe structure ofthe ampullaryorgans have re- cently beenexamined in a study,which reveals that ‘microampullae’occur in fresh- water plotosidcatŽ sh ( Plotosus tandanus ,Whiteheadet al., 2003).These microam- pullae consist ofshort canals (50 ¹m) andcontain low numbers (10-15) of receptor cells andappear different to the ampullaryorgans described for marine Plotosusan- guillaris, whichare characteristically deŽned as resembling ampullae ofLorenzini (Obara,1976; Zakon, 1986). The canals ofthe ampullaryorgans in P.anguillaris measure incms andthe ampullae includehundreds of receptor cells. Whiteheadet al. (1999,2000) described three morphologicaltypes ofampullary organs in the estuarine catŽsh, Arius graeffei. Thesethree forms mayrepresent adaptations for changesin habitat (freshwater,estuarine andmarine) duringthe Žsh’s lifecycle. Similarly,elasmobranchssuch as the bullshark, Carcharhinusleucas , which mi- grate betweensaltwater andfreshwater rivers, also reveal differences in receptor types. Juvenile C. leucas collected fromfreshwater reaches ofthe Brisbane River in Australia possess ampullae ofLorenzinithat differ fromthose previouslydescribed forother elasmobranchs (Whitehead, 2002). The major differences are small regions of‘cloverleaf’ampullarywall nearthe multiple ampullaryalveoli andthe inverted supportivecells that possess apically positionednuclei. These structural variations mayoptimise the ampullae to functionmost effectively in freshwater habitats by shuntinga portionof the electrical signal passingthrough the ampulla andlimiting the Želds receivedby the receptorcells. Asimilar ecomorphologicaldifference has also beendescribed for the ampullae in the freshwater stingray, Himantura signifer (Raschi et al., 1997).These ‘ miniampullae’are relatively simple witha short canal anda reducedsensory epithelial surface area andpresumably are adapted foroperating in afreshwater environment. Inaddition to differences in canal length,receptor structure andtopographic arrangementin species that frequentboth saltwater andfreshwater, the associated changesin temperature andthe ionic compositionof the water mayalso haveeffects onsensitivity (Loewensteinand Ishiko, 1962; Akoev et al., 1980;Peters et al., 1995; Heijmen et al., 1996;Braun et al., 1997).Electrophysiological recordings show that the sensitivity ofthe apical microvilli in the freshwater catŽsh, Ameiurusnebulosus is reducedby 80%when exposed to ahyperosmoticsolution (Heijmen et al., 1996). Dischargerates ofampullae ofLorenziniappear to betemperature sensitive over awidephysiological range (Sand, 1938), where sensitivity appearsto increase as the temperature rises, providinga potential forthe electric sense to beuseful as a biomonitoringsystem forwater pollution(Akoev et al., 1980;Peters et al., 1995).

2.4.Localising prey in the deep-sea Acomparisonof 40skate species, rangingfrom depths of 63to 2058m, byRaschi (1986)reveals that boththe numberof alveoli andthe overall size ofthe ampulla Functionalroles of electroreception 13 increases signiŽcantly with depth.This trendsuggests that species inhabitingdeeper regionsof the water column,where sunlight may fail to penetrate,possess higher numbersof receptor cells andmay rely moreheavily on electroreception inthis relatively prey-depauperateenvironment (Raschi andAdams, 1988). The depth- related modiŽcations to the ampullae in the deep-seaskate, Rajaradiata , are mostly restricted to the mouthregion (along the superŽcial ophthalmicand mandibular clusters), emphasising the importanceof prey localisation. Anincrease inthe numberof alveoli andampulla size in this regionwill enhanceboth receptor sensitivity andthe signal-to-noise ratio, therebymediating the perceptionof a slightly weakerbioelectric Želd thanits shallow water counterpart(Raschi and Adams,1988). The resultant reductionin the signal-to-noise ratio mayalso allow these deeperdwelling species to search forprey higher in the water columnand hencecover a greater area perunit time (Raschi andAdams, 1988; Raschi et al., 2001).Interestingly, the regionof the dorsal nucleusin the medulla that receives inputfrom the superŽcial ophthalmicampullae occupiesa disproportionatelylarge (40%)area (Bodznickand Schmidt, 1984).

3.DETECTING POTENTIALPREDA TORS Occupyingan apex position in the foodchain, adult elasmobranchshave few natural predators.Therefore, the selection pressures toevolve elaborate mechanisms for the detection ofpotential predatorsmay not be as intense oncethese animals have reacheda certain size. However,elasmobranch embryos, pups and juveniles are particularly susceptible to predation.Embryos of egg-laying elasmobranchs are naturally predatedupon by teleosts, otherelasmobranchs and marine mammals (Coxand Koob, 1993; summarised bySisneros et al., 1998 /.Atthis earlier stage in development,the stimulus invokinga predatoryattack is inducedby the embryo circulating water aroundthe eggcase alerting potential predators,which presumably use their mechanoreceptivelateral line tolocalise these stationary delicacies (Luer andGilbert, 1985).Predation is avoidedby ceasing all ventilatory streaming, afreezingbehaviour elicited bythe embryoelectrosense, whichhas beenfound to respondto sinusoidal electric Želds between0.5 and 1 Hz,a frequencyband which correspondswith the ventilatory pulses producedby large predators(Tricas et al., 1995;Sisneros et al., 1998;Sisneros andTricas, 2002). Pupsand juvenile elasmobranchsalso possess increased sensitivity (Žve times that ofembryos) due to anincrease in the ampullarycanal lengthbrought about inthe skate, Rajaerinacea, bya two-foldincrease indisc size (Sisneros et al., 1998).This relationship betweencanal lengthand voltage sensitivity wouldenhance the ability ofthese vulnerablestages todetect potential differences betweenthe skin surface andthe internal ampullarycluster in orderto avoidpredation. In the catŽ sh, Clarias gariepinus ,anincrease in the numberof ampullaryreceptors forms the basis ofnearly a four-foldincrease in sensitivity duringthe Žrst 4monthsof 14 S.P.Collin& D.Whitehead developmentand would similarly providea Žnerspatial resolution forthe detection ofanelectrical stimulus in the formof apredator(Peters andIeperen, 1989). Thescalloped hammerhead, Sphyrnalewini ,the bonnethead, Sphyrnatibur o, and the sandbarshark, Carcharhinusplumbeus all possess maximal electrosensory pore densities (15-20pores cm 2/ between40-50 cm precaudallength (Kajiura, 2001). Thesedensities fall to 2.5pores cm 2 in adult C. plumbeus andmay emphasise the increasing role playedby othersenses (suchas vision,see above)as eachspecies approachesmaturity .

4.THEROLEOF BIOELECTRICSTIMULI INSOCIAL BEHAVIOUR Thesensory specialisations ofperipheral electrosensory receptors enableprey detection bystimulation ofindividualampulla bybioelectric stimuli at close range. Althoughfew studies haveconcentrated on the role ofelectroreception insocial behaviour(Mortenson and Whitaker, 1973; Bratton andA yers,1987), a study byTricas et al. (1995)has revealedthat weakbioelectric Želds canprovide the stimulus forthe localisation ofmates andconspeciŽ cs (Žg. 6). By modulatingthe ionic potentials producedby the spiracles, mouthand gill slits duringventilation (Kalmijn, 1974;Bodznick and Montgomery ,1992),buried female roundstingrays (Urolophushalleri )canbe located byactively searchingmales in the absenceof anyother sensory cues. Female rays also use this weakstimulus to locate buried consexuals.This ability is mediated in bothskates, whichcan also encodethe weak electric organdischarges producedby conspeciŽcs duringsocial andreproductive interactions (New,1994; Sisneros et al., 1998),and stingrays, suchas the Atlantic stingray, Dasyatis sabina ,whichdo notpossess electric organsfor communication (Sisneros andTricas, 2002).Tricas et al. (1995)found that the primaryafferent neuronsare most sensitive to stimuli that varysinusoidally at the same frequencyas the natural respiratory movements.In elasmobranchs that donotbury themselves, the neuroendocrine(Demski, 1990) and olfactory systems mayalso beimportant precopulatorysensory cues that ofteninitiate elaborate motordisplays (Bres, 1993 andsee reviewby Pratt andCarrier, 2001).

5.MIGRATION ANDGEOMAGNETIC ORIENTATION Elasmobranchsare knownto regularly migrate overshort andlong distances, whereindividuals return to favourable environmental conditions and/ orapreferred habitat overa rangeof time frames. Onamacroscale, white sharks, Carcharodon carcharias,are able to migrate upto 3800km, showing a bimodalpreference for depthsof 0.5 m and300-500 m (Boustanyet al., 2002;Klimley et al., 2002).On amicroscale, some species migrate in andout of a regionwith changesin daily tidal owor light/darkcycles, while others exhibit some sort ofhoming behaviour, returningto particular regionson an annual or seasonal basis (Klimley andNelson, Functionalroles of electroreception 15

Figure 6. Therole of bioelectricstimuli in socialbehaviour. In thestingray, Urolophushalleri mating individualsorient to artiŽcially produced low frequency electrical Ž elds,mimicking those recorded fromfemale stingrays. Males will approach, dig and attempt to mate with the model and females will locatethe source and bury in close proximity. Figure adapted from Bodznick et al. (2003).

1984;Klimley, 1987;Klimley et al., 1988;Castro, 1993;Taylor, 1996). According to Montgomeryand W alker (2001),true navigationor the ability ofan animal to knowits positionin relation to some speciŽc destination, has notbeen demonstrated convincinglyin elasmobranchs. However, a numberof studies showinghighly directional swimmingsuggests that these animals must beable to sense andreact to anumberof environmental factors, suchas light irradiance,temperature and directional landmarkslike ridges,valleys andeven the sun(Carey et al., 1982; Gruberet al., 1988;Klimley, 1993,2002). Many of these orientational behaviours overlong distances donotinvolve the electroreceptive sense butmay involve visual (Collin, 1988;Bozzano and Collin, 2000),olfactory (Doving et al., 1985;Doving andStabell, 2003)and/ orlateral line (Montgomeryet al., 1997;Montgomery and Walker,2001) input. Kalmijn (1982,1984, 2000, 2003) postulates that the electroreceptive system is the basis forgeomagnetic orientation in elasmobranchs.In the ocean,sharks and rays are exposedto electric Želds resulting fromtwo sources: 1)electric Želds 16 S.P.Collin& D.Whitehead producedby their ownmotion through the water in the presenceof the earth’s magnetic Želd,where the horizontalcomponent of the animal interacting withthe horizontalcomponent of the magnetic Želd producesa vertical electromotive Želd; and2) electric Želds associated with oceanstreams andionospheric circulation, whereanimals are thoughtto use the horizontalelectric Želd producedby the interaction ofthe horizontalmovement of the oceanstream with the vertical componentof the earth’s magnetic Želd (Kalmijn, 2003).T ype1 Želds mayprovide ‘active electro-orientation’, wherean animal couldmaintain aheadingby avoiding anychange in the electric Želd inducedby a changein direction throughthe horizontalcomponent of the earth’s magnetic Želd (Kalmijn, 1984,2003). T ype 2Želds mayprovide ‘ passive electro-orientation’, wherean animal mayascertain its course(e.g., its currentspeed and direction) bydetecting the voltageinduced by the motionof saltwater throughthe vertical componentof the earth’s magnetic Želd. Accordingto Paulin (1995),ampullae ofLorenzinicannot measure DCvoltages, andan induced voltage due to water owin the oceanis notuniquely interpretable interms ofthe speedand direction of owat the pointwhere the electrical measurement is made.A newtheory presented suggests that the electric sense is usedto determine acompass bearingas it swims bycomparingthe inputsof both the electroreceptors andthe hair cells in the semicircular canals. Accordingto this theory,the direction cueis the directional asymmetry ofthe changein induced electroreceptor voltageduring turns (Paulin,1995). At least forscalloped hammerheads( Sphyrnalewini ),both active andpassive electro-orientation cannotcompletely accountfor the directional swimmingof this species (e.g.,between Espiritu Santoseamount and Las Animas Island,Ž g.7). An alternative explanation,proposed by Klimley (1993),suggests that the directional movementpatterns trackedby sharks is dueto atypeof ‘topotaxis’, anorienting behaviourto boundariesbetween different geomagneticlevels in sea-oor magneti- sation. Thetracks madeby sharks actually matchedtopographic features suchas ridges andvalleys where,at 100m abovethe sea oor,geomagnetic intensity varied by1400nT/ movera distance of1 km(Macdonaldet al., 1980).While sharks bask- ingat the surface wouldswim ina straight line while orientingto the earth’s main magnetic Želd,individuals shown to swim upanddown in the water columnswim alongmore tortuous paths, orienting to local magnetic topography(Klimley et al., 1993,2002). Therefore, these sharks maypossess amethodof trackingaccording to geomagneticintensity ,whereminerals suchas oxidesof iron and titanium in the earth’s crust formpatterns inassociation withseamounts andbands, providing the ability to detect geomagneticgradients in seaoor magnetisation (Klimley, 1993; Klimley et al., 2002).How could this gradientbe detected? Theelectrosensory sys- tem is certainly acandidate(see above)and it is also possible that these deposits ofmagnetic minerals orsimply different bottomtypes mayproduce both local and regionalelectric Želds that couldfacilitate orientational cues (Pals et al., 1982). However,an alternative mechanism maybe mediated directly via amagnetite-based sensorysystem (Walkeret al., 1997;Montgomery and Walker, 2001; Walker et al., Functionalroles of electroreception 17

Figure 7. Directionalhoming movements of Sphyrnalewini inthearea of EspirituSanto Seamount inthe Gulf of California.Arrows mark routes with broader lines indicating movement of one shark overthe same geographic path used by another. A primarypath (Number 1) passing North-South overthe seamount was heavily used by several sharks. Other paths (designated 2-4) coincide with thelocations of ridgesand valleys leading away from the Seamount that have been measured to have deŽned topographic geomagnetic intensity gradients. Figure adapted from Klimley (1993).

2003).Although single domainmagnetite is notyet describedin elasmobranchs, magnetite crystals havebeen identiŽ ed in bothteleosts andbirds, and are associated with the olfactoryepithelium. Incontrast to this magnetite-based magnetoreceptive system, there is as yet noevidence for specialised receptors that are selective for magnetic Želds ineither the visual orthe electoreceptive systems (Walker et al., 2003).Other evidence to support a single mechanism forlong distance orientation andmigration reveals that magnetic Želd discrimination in short-tailed stingrays is abolishedby magnets overlyingthe predictedregion of magnetite in the head.The possibility remains that the lengthof the ampullarycanals in the electroreceptive system maynot provide the highsensitivity (bothmeasured and predicted) for mag- netic Želd detection (Kirschvinkand Walker, 1985; W alker et al., 2003).

6.FUTURE DIRECTIONS: MICRO AND MACRO COMPLEXITY AND BIOMIMETIC MODELLING Ampullaryorgans can signal modality-speciŽc informationin responseto different stimuli, e.g.magnetic Želds andenvironmental temperature changes(Braun et al., 1994).Thermal, but not electrical, stimuli alter the oscillation frequencyallowing dualsensory messages to beconveyed in a single spike train. Morerecent studies 18 S.P.Collin& D.Whitehead haverevealed that the interplay ofpositive andnegative conductances generated byion channels in apical andbasal membranesof receptor cells results in signal ampliŽcation, thereby enhancing the electric Želd sensitivity ofthe wholeampullary organ(Lu and Fishman, 1994, 1995). However, there is still aneedto expandthese experimental andtheoretical studies ofthe physics ofexcised ampullaryorgans tothe wholeampullae in vivo andperform studies ona numberof ampullae of Lorenzinifrom a variety ofspecies fromdifferent habitats. Theseexperiments shouldfocus on measuring the DCandAC electrical responses andthe effects of geomagneticand artiŽ cial magnetic Želds with the aim ofdeveloping an accurate andpredictive modelto explainthe performanceof the organ.

6.1.The distribution andfunction of groupsof electroreceptors in elasmobranchs Furtheranalysis ofthe distribution andfunctional grouping of ampullaryorgans is requiredto elucidate the large variations in manyinter- andintra-speciŽ c studies (Raschi et al., 2001).If the diet andfeeding habits ofspeciŽ c sharks andrays has an effect onthe electroreceptive system, awiderdescription ofclosely-related species is essential toestablish howthe placement ofgroupsof receptors overthe headis organisedon the basis offunction.This formof analysis will supportor negate any relationship betweenthe environmentalfactors that inuence each species’ survival andboth the total numberand distribution ofelectroreceptors. Whenthe innervation patterns are describedmore fully ,manipulative experiments shouldbe attempted to examineany changes in morphologicalgroupings and/ orbehaviouralactivity .These inducedchanges will providestrong evidence for the functionalroles ofspeciŽ c groupsof ampullaryorgans.

6.2.The biochemical nature of the ampullarygel Modernchemical analysis ofthe ampullarygel reveals that it is predominantly ( 97%/ water inaddition to a numberof sulfated glycoproteinmolecules such as sodium,calcium, chlorideand potassium ions(Murray and Potts, 1961;Doyle, 1967).This material is asub-class ofpolysaccharideoften found in extra cellular structures acting as asupportfor connective tissues andmucous membranes. Thechemical natureof the mucopolysaccharideis basedupon the isolation of glucosamines,galactosamines, hexosamine,and sulphates (hyaluronicacid and chondroitin)from the material (Waltman,1966; Doyle, 1967). However, to date there has beenno analysis undertakenof sugar,protein, amino acid orlipid content. Thegel inampullae ofLorenzini is acritical componentof ampullary organs and the process ofelectroreception. The elastic gel maysimply maintain the geometryof the canals orserve to preventinfection, but Brown et al. (2002)suggest that agel-Žlled canal mayalso functionas alowfrequency antenna that is toosluggish to respond to frequenciesabove 1 kHzand sluggish enoughto allow stimulation ofthe afferent nerve.As the glycoprotein-basedgel possesses electrical characteristics similar to those ofa semiconductor(Brown et al., 2002),the gel is likely able to translate Functionalroles of electroreception 19 subtle changesin temperature into anelectrical stimulus (Sand,1938; Wissing et al., 1988;Brown, 2003). However, these studies oftemperature sensitivity were all performedon gel extracted fromampullary canals andstudied in vitro. Future studies shouldinvestigate temperature conductanceof the gel in vivo simultaneously with efforts to determine the biological functionand relevance to behaviourof a highthermal sensitivity sensorysystem. Furtherwork on the chemical andphysical structure ofthe Lorenzinigel will also undoubtedlyhelp us to understandits role in electroreception.

6.3.Biomimetic modellingof the electroreceptive system Inrecent years,signiŽ cant progresshas beenmade in understanding the neuralcom- putationsunderlying the ability ofelectroreceptive Žshes todetect andlocate prey (Bodznicket al., 1999;Montgomery and Bodznick, 1999; Bodznick et al., 2003).A numberof workers have gone one step furtherand developed computational mod- els ofelectroreceptors andelectrosensory neuronsin orderto understandthe sen- soryprocessing in the dorsal octavolateral nucleus(Berquist andPaulin, 2001). This typeof mathematical modellingis nowbeing used to quantitatively linkthe physical geometryand movement of an elasmobranch (for example) to its neural input(Brown, 2002). By linking behaviour and the morphologicalorientation of individualampullary organs, an approximate picture ofbody-wideelectrosensory inputor the electrosensed landscapefor a predatoris assessed. Otherworkers are usingthese same theories inthe developmentof artiŽcial electrosensor arrays with the hopeof exploring remote submarineregions using robots (Maciver andNelson, 2001).Future research will undoubtedlyreveal the mechanisms underlyingthe roles ofelectroreception butthe variousmodels beinginvestigated still requireintense in- vestigation if theyare to bedeciphered.

ACKNOWLEDGEMENTS Wewould like to thankLisa Merrick Bartels, Keith Feigerson,Rebecca Frolander, Falland Tascanoand Lindsay Weiland for assistance with the collection andanalysis ofthe distribution ofthe ampullaryorgans in the ampullae ofthe bull shark, Carcharhinusleucas. Wealso wish tothank Dr Rob Peters onbehalf of the International Congressof Comparative Physiology and Biochemistry forinviting this reviewand the participation ofDr DarrylWhitehead in the conference.

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