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The Functional Roles of Passive Electroreception in Non-Electric Fishes

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The Functional Roles of Passive Electroreception in Non-Electric Fishes AnimalBiology ,Vol.54, No. 1, pp. 1-25 (2004) Ó KoninklijkeBrill NV ,Leiden,2004. Alsoavailable online - www.brill.nl Thefunctional rolesof passive electroreception innon-electric 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 elds.Particular attention hastraditionally focused on cartilaginous shes,but a rangeof teleost and non-teleost shesfrom adiversityof habitats have also been examined. As more species are investigated, it has become apparentthat the role of electroreception in shesis not restricted to locatingprey, but is utilised in othercomplex behaviours. This paper presents the variousfunctional roles of passive electroreception innon-electric 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 conspecics 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 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 living sheswith only some of the majorgroups shown. Example species of somegroups are noted. Groups possessing electroreception arenoted by a check( );non-electroreceptivegroups with a ( ).Modied from von der Emde, 1998. times in variousvertebrate classes (g. 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 elds ( <0.1-25Hz), while tuberousreceptors are tunedto higherfrequency elds from50 Hz to over2 kHz(New, 1997). Thought to bea primitive vertebrate character,the ability to detect weakelectric elds in shes has thus far beenfound in agnathans(lampreys butnot hag 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 paddle sh, Teeter et al., 1980;Northcutt, 1986) and a small numberof species within the osteoglossomorph (knife shes, Braford,1982; Bullock and Northcutt, 1982; Carr andMaler, 1986; Zakon,1988) and three ordersof teleosts; mormyrids(African electric shes, Liss- mann,1958; Bell andSzabo, 1986), gymnotids (South American electric shes, Lissmann,1958; Carr andMaler, 1986;Zakon, 1988), and siluriform (catsh, Parker andvan Heusen, 1917; Roth, 1968; Finger, 1986; Whitehead et al., 1999,2003) groupsof shes (g. 1).Electroreception has also beenfound within the sister group ofthe actinopterygian shes, the Sarcopterygii,which comprises the dipnoanlung- shes (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 elds, bymeasuring minute changesin potential between the water at the skin surface 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 (g. 2). The canal walls are formedby squamous epithelial cells joinedby tight junctions,which create ahighresistance (Waltman, 1966).The canals are lled with amucopolysaccharidejelly andmay radiate in all directions fromthe ampullaryclusters, providinga methodof directionally sam- plingthe electric eld 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 to the headin sharks,but are also distributed overthe pectoral ns 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 to 20in the catsh, Kryptopterus bicirrhus ,in contrast 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 (g. 2),in comparisonwith longcanals andnumerous receptor cells in marine species (Zakon,1986, 1988). One afferent bretypically 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 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 within asingle alveolus are contactedby upto 15afferent bres (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-lled canals comprisingeach electroreceptive organensure that the potential within the ampullarylumen remains close to that at the skin sur- 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 of 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 eld’s intensity,its spatial conguration and possibly the 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 shes are usedin highfrequency electroreception, they are largely Functionalroles of electroreception 5 tunedto the dominantspectral frequenciesof the individual’s ownelectric organ discharges rather thanthe weakelectric elds producedby other organisms or environmentally-inducedelectric elds (see reviews byBullock, 1982; Bullock and Heiligenberg,1986; Turner et al., 1999).This reviewwill concentratesolely onthe roles ofpassive electroreception in non-electric shes 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 elds emanatingfrom prey are detected using ampullaryorgans. These ampullae respondto DCorlow frequency electric elds, e.g.,1-8 Hz in elasmobranchs(Montgomery ,1984)and 6-12 Hz in silurid teleosts (Peters andBewalda, 1972). Elasmobranchs are able to respondphysiologically and behaviourallyto weak,low frequency electric elds of10 nV/ cm and5 nV/cm, respectively (Dijkgraafand Kalmijn, 1962,1966; Kalmijn, 1982).The behavioural relevanceof
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