Visually mediated responses in the lycosid spider Rabidosa rabida: the roles of different pairs of eyes PDF
Preview Visually mediated responses in the lycosid spider Rabidosa rabida: the roles of different pairs of eyes
VISUALLY MEDIATED RESPONSES IN THELYCOSID SPIDER RABIDOSA RABIDA: THEROLES OFDIFFERENTPAIRS OFEYES ROVNER LS. Rovner,J.S. 1993 11 11:Visuallymediatedresponsesinthe\ycos\dspiterRabidosarahida: the roles of different pairs ofeyes. Memoirs ofthe Queensland Museum 33(2):635-638. Brisbane.ISSN0079-8835. Video images ofconspeciflcs were presented toRabidosa rabida (Walckenacr) (Arantne: Lycosidae)tostudytherolesofdifferentpairsofeyesinawolfspider.Fourgroupsofspiders hadonepairofeyesoccluded,andfourhadallbutonepairoccluded.Variouscontrolgroups were also tested. The PLE wereessential for sizeableorientation turnsofuptoabout 160° ThePMEservedforrapid,longdistanceapproachestowardthestimulus;they alsoinitiated orientation turnsofuptoabout 50°. Ifclose tothestimulus, theALEinitiated smallturnsof up to about 20° and mediated small approaches. The AMEdid not mediate any responses. Courtship could be triggered in males via the PLE orthe PME. In females, only the PME mediated receptive display responses to temporally patterned leg 1 movement* seen in anteriororlateralviewsofacourtingmale.[JAraneae, Lycoshlut. eyes, visii'n. communica- tion JeromeS.Rovner,DepartmentofBiologicalSciences, IrvineHalt. OhioUnivt Itotft Ohio45701 U.S.A.; 3Juh\ 1992 Very little behavioural research has been car- 1991) in Athens County, Ohio, USA I he dedoutonvisionin lycosidspiders, comparedto methods ofmaintenance and the laboratory con- the extensive studies on salticid spiders ditions during testing have been described pre- (reviewed in Forster, 1985). In lycosid spiders, viously(Rovnen 1989). Spiderswere notusedin occlusion of the eyes has been used to test for testing until 1 week after the final moult. Tests differences in the roles ofthemain vs. secondary were conducted between 1000 and 2200 hours. eyes (Homann, 1931) as well as the anterior vs. For each test the spider's home cage, with its posterioreyes(Acosta*?/«/., 1982);however, the resident within, was placed with its narrow front results ofboth ofthese studies were confounded sidefacingasmall televisionset(blackandwhite by the lack ofcontrols for vibratory stimuli. The Magnavox BH-3907; screen = 9.2cm wide, only successful behavioural investigation ofthe 6.6cm high), which received a playback signal role of particular eyes in lycosids (Magni eAtMalE.y from a Sony recorder (SL-HFR70). The clear 1964) demonstrated the importance ofthe frontsideoftheplasUccage(theothersideswere in astronomical orientation and was ac- opaque)was7cmwideandwaslocated3cmfrom unuplished by covering all but a single pair of the screen. 1 removed the cage cover and, if eyes in each group tested. Occlusion ofonly one necessary, gently positioned the spider with an pairofeyesatatimehasproven useful in several artist brush to insure that the screen would be behavioural studies of salticid vision (e.g., within the visual field of the spiders useable Fofster, 1979) eyes (1 used separate brushes for males and In the present study of the lycosid spider females). Then, a glass cover Tone foreach sex) Rabidosa rabida (Walckenacr), I used both was placed on top of the cage. A front-silvered methods of occlusion to examine the roles of mirror fixed at 45° to the floor was 0.5m above different pairs ofeyes in detecting visual stimuli the cage. A video camera (JVC GX-8NU'i and mediating appropriate responses. By using aimedatboththe mirrorandan adjacent, second, video images as stimuli (Clark and Ueiz, 1990), identical television set receiving the same signal 1 eliminated the possibility that vibrations or from the playback recorderas the first set. Ttus chemicals from conspecifics couldconfound the yielded(onasecond,identicalrecorder)akindof results. split-screen recording. On the left was a dorsal view ofthespider, which facilitatedthemea METHODS ANDMATERIALS ment ofturningangles (accuratetothe nearest 5° ) and speeds of locomotion. On the right was a PenultimateRabidosarabida (formerlyLycosa view of the video image concurrently being rabida) were collected in late June (1990 and presented to the spider Thui, therelationshipof 636 MEMOIRS OFTHEQUEENSLANDMUSEUM the video stimulus tothe spider's response could assumed wouldonly occurin this study as visual laterbe analyzed. responses. Subjects used for video presentations were There were eight experimental groups, each recorded against a plain, pale background and having 10spidersofeachsex.Infourexperimen- illuminated evenly by a 32-W, circular fluores- tal groups a single pairofeyes was occluded; in centbulb0.5mabovethe arena. Thecamera was fourothers, all but one pair was occluded. Since located at a distance yielding a screen image the one oftheuntreatedcontrol spiders hadfailed to size ofthe actual subject (average body lengths: respond to video playback within two trials and female=18mm; male=12mm). The 15-min video since the preliminary tests had indicated that playback for females was a pheromone-stimu- painting the eyes can reduce responsiveness, I lated, courting male; his occasional position gave unresponsive experimental spiders addi- changes provided nearly equal proportions of tional opportunities to respond, up to a limit of anterior and lateral views of his display (total five trials. One or more days separated consecu- number of courtship bouts = 51). The 10-min tivetrials undergone by any individual spider. video playback for males was a lateral view ofa female walking to and fro in an elongate glass RESULTS arena (passes across the screen =15 leftward and 15 rightward). Some preliminary tests made use During testing of control groups, all of the othfreperecyriicmkaetgses(Apcrhoevtiadeddombeystaicu1s0,-m1in0mvmideboodoyf umnatlreesatsedhofweemadle'sorainedntaaltliobnu'toanned/oofrth'elounngt-rreaantgeed length) walking toand fro. approach.' Most (16/20) did so in the first trial. To cover the eyes of spiders, I painted them 'Orientation' involved a single, rapid pivot that withtwocoatsofwater-basedenamel (TopColor resultedinthespiderfacingtheimage.Thispivot Hobbylack, Pelikan AG). Thatthis insured com- hadameanspeed(SD)of121 ±51.77s(N= 12), plete occlusion had been established previously about eight times faster than turns that occurred (Rovner, 1989). Spiders were tested oneormore duringwandering, 16± 12.47s(N= 11).A 'long- days later. range approach' covered a distance of up to I ran two preliminary tests to see ifpainting or 10cm, themaximumbeing limitedbycagedepth its related procedures lowered responsiveness. (12.5cm). The speed of an approach, 5.9±3.32 All the eyes of five females were covered with cm/s (N = 22), was about ten times faster than two separately applied coats ofclear paint. Five walking during wandering, 0.6±0.31cm/s (N = otherfemales were briefly anaesthetised (carbon 36). (The above speeds are not the maxima at- dioxide) and then restrained for 6 hr, thereby tained, since I included the acceleration and duplicatingtheprocedureusedwhenpaintingthe deceleration phases in each boutoflocomotion.) eyes. However, at the twotimesthatpaintwould Noorientationorapproachresponsesoccurredin have been applied (0 hr and +3 hr), I used water theempty arena orfully blind controls. instead. The next day, when exposed to video Results of the eye occlusion experiments are imagesofcrickets, theclear-paintedspiderswere summarized in Table 1. Spiders with any one of less responsive than were the water-brushed thefourpairsofeyes occluded werestillcapable spiders. The latter seemed as responsive as un- oforientation; those with occluded PMEdid not treated spiders. showapproach.Whenallbutonepairofeyeswas There were three control groups, each with 10 occluded, theonly groupfailing toshow orienta- females and 10 males; these 60 individuals were tion was the one limited to use ofthe AME; and given two trials apiece. One group consisted of the only group that still showed long-range ap- untreated spiders exposed to the conspecific proach was the one with useable PME. When video playback, to determine how readily fully closetothe cagefront, a few spidershavingonly sighted spiders respond. A second group, also useable ALE did perform a near-field approach untreated, was exposed to a 10-min video of an response, edging forward less than one body empty arena, to determine if that alone had a length. For all the responding experimental stimulatingeffect. (Lightfromthescreen=about groups,themeannumberoftrials (±SD) needed 800 lux; incident light from above = about 350 to obtain either an orientation or a long-range lux.). The third group consisted offully blinded approachtotheimagewas 1.2±0.53 (N=63)for spiders exposed to the conspecific playback, to femalesand2.4± 1.24(N=55)formales(Mann- see if such spiders would perform behaviours Whitney CMest,Z= -6.545, P<0.0001). (orientation, rapid approach, or display) that I Spiders with useable PLE showed orientation VISUAL RESPONSES IN RABIDOSARAB1DA 637 Oncnlation Longrange Display may have prevented some visually stimulated ('.indtti.-n approach males that were facing thestimulusat theoutset 9 r* 9 s 5 J from being included in the courtship tcnal for Untreated 6 6 8 7 3 5 someexperimentalgroups.)Onlymaleswithuse- Rmpiyrircna ablePLEOfPMEshowedcourtshipaccompanied Fullyblind D D byorientation,andonlymaleswithnon-occluded N0PLE5 6 7 ID 4 5 : PME showed courtship accompanied by ap- NoPMEs in 6 U 4 proach (Tabic 1 1 NoALE* 10 7 9 5 4 1 NnAMEs 10 6 9 6 4 3 DISCUSSION Dills PL! i 11! 7 D 5 OnlyPMEs 9 6 19 5 3 2 Data presented here indicate that R. rabida's OnlyALE* 3 1 posterior eyes play major roles in mediating OnlyAMEs u D n I) responses toimportant Visual stimuli,aswasear- TvAiBdeLoEpl1.ayNbuamckb.erNo=f 1?0asnpdid6crss/psiedxe/resonrdeistpioonnd.inEgactho l(iHeormpraendni,ct1e9d3f1o;rLlayncods,id1s98o3n).anTahteomPiLcaElsgerroveuntdhse spider was allowed more man one [rial to respond: samefunctionthattheydoinsalueid spiders, thai controls, up to two trials: experimental*, up to five ofdetecting stimuli in an extensive visual field (rials. Only 63 that also performed orientation or and initiating the largest orientation turns. They approachareincludedunder 'Display*. cannotmediate approachbehaviour.Ontheother PME hand, the are essential formediating rapid, turns of up to about 160°. Those with only the long-rangeapproaches to stimuli. Theycan also PMEuseableperformedorientationturnsofupto initiate oncnlation turnsofup to5(F. about 50°. If near the stimulus, those with only As tothe anterioreyes, m close range the ALE the ALE useable showed orientation turns of up canplay smallroles in orientationandapproach. toabout 20°. This contradicts Land's (1981) suggestion that During playback ofmale courtship, onlythose only the large posterioreyes are involved inprey females with non-occluded PME performed leg- capture.AspredictedforlycosidsbyLand[ibid,), waving receptive displays (Table I). Trus brief theAMEof/?. mhuhplay no role by themselves display occurred 3.0±1.9s (.V = 30) after the inmediating turnsorapproachestoward atarget. abrupt termination ofthe male'scourtship bout. Whetherthey serve forotherthanpolarized light The receptive display was sometimesperformed detection (Fvlagni ct ai. 1964) remains tobe ex- unimpeded, this being the case in females which plored. had not yet reached the front ofthe cage. How- The present findings on the anterioreyes ofR. ever, it was usually constrained, since most rabida may not apply to all lycosids. For ex- females quickly approached the cage front and ample, unlike ft rabida inArctosa variarm the edtheij anteriorlegsagaiosi thewail. Still,the AME are largerthanthe>ALE {ibid.). Also, local timing of their response remained precise. tiering is found tn Ihe retinae of the AME ol Females showed this display while seeing Geolycosa godefftoyt hut not in the type genus anterior or lateral views ofthe-courting male. Lycvsa(BlestandO*Carroll, 1989),Furthermore, Upto6/1 ofthemalestestedineachcondition the finding of high nocturnal sensitivity in the performed courtship display, which occurred in anterioreyesofLycosatarcntula(Carncaburu el everygroup.Itevenoccurredintwomalesduring qL, 1990) suggests that an understanding of the theemptyarenaplaybackand inthreeofthefully capabilities ofthe anterior eyes oflycosids will blinded males, such daUi reflecting a previously requireexaminingdifferentspeciesundervarious noted readiness ofR. rablda to sometimes court illuminationconditions. Finally, Imust point out inresponsetosubnormal stimuli (Rovncr, 1968). that I did not test for any possible collaboration Perhaps these non-visuallystimulatedcourtships between different pairs of eyes. Collaborative weretriggeredbymechanicalcuesresultingfrom visual mechanisms were revealed in salticid my movingthecagetothe testingsiteorfrommy spiders by ipsilalcralblinding (Fofster, 1979). positioning the spider with a brush (to duplicate As in the salticuls (Forster, I985)> orientation iheprocedure usedonexperimental spiders). For and approach arc the initial behavioural respon- this reason, only courtships occurringduring tri- sesoflycosid spiders to moving images, whether alsinwhichorientationorapproachalsooccurred prey or mating partners. Thus, the perform. were scored as visually initiated displays. (This ofsuch behaviours docs not specify the spider's 63* MEMOIRSOFTHEQUEENSLAND MUSEUM motivational state. However, the fact that twice LITERATI/RECITED as many trials were needed to obtain these be- havioursinmalesasinfemalessuggeststhatsuch ACOSTA. J., ORTEGA, J. & RODRIGUEZ- initialresponsesrelateprimarilytopredation,i.e., SANABRA, F. 1982. Vision and predatory' be- thatadultfemales,onaveragebeinghungrierthan haviour in Lycosa JasciivetUris. 6th European males,are moreresponsivetovisual stimulation. Neuroscience Congress. Malaga. Spain: 21-22. A subsequent occurrence of display behaviour BLEST,A.D.&G'CARROLL,D. 1989.Theevolution indicates a switch to sexual motivation. o(fArtahneeateie:reSdalptriicindcaiep)a.lPrpe,ti1n5a5e-o1f70j,umIpniRngN.sSpiidnegrhy For display to occurin females the PME have and N.J. Strausfeld (eds). 'Neurobiology ofsen- tobeuseable, and they aresufficientbythemsel- sorysystems', tPlenum Press: New York). ves for mediating this response. The fact that CARRICABURU. P.. MUNOZ-CUEVAS, A. & OR- lateral as well as anterior views ofthe courting TEGA-ESCOBAR, J- 1990. Elcctrorctinography male elicited responses suggests that the cue is and circadian rhythm in Lycosa taremula movement of the male's black leg I: it extends I'1A9r0a:n6e3a-e6.7Lv"cosidae). Acta Zoologiea Fennica forward in a pumping-like motion ofincreasing CLARK, D.L. & UETZ, G.W. 1990. Video image frequency and then abruptly flexes back. Unlike recognitionbythejumpingspiderMaeviainclem- csaehiivceiddffoarcme-otfo-tfhaecemaclouertmsahyip,beinaswhimipcohrttahentpefro*r 'Araneae: SaJticidae). Animal Behaviour40: -S90. the female as his behaviour {ibid.), female R, FORSTER: ,L.M. 1979. Visual mechanismsofhunting rabida need not view the male's anterior. Ap- behaviour in Trite ptaniceps, a jumping spider parently,detectionofatemporalpatternofmove- (Araneae: Salticidae). New Zealand Journal of ment suffices forrecognition. Zoology6: 79-93. As tnvisual!y-!riggeredcourtshipdisplay,male 198l5A.ranTeaareg:eStaitdiicsicdraiem)i.naPtpi.o2n49i-n27j4u.mpIinnRgG.spBiadretrhs R. rabida differ from male salticids, which re- (ed). 'Neurobiology of arachnids'. (Springer- quireoneparticularpairofeyes, theAMEU/^/.i. Verlag: New York). Stimulation of either pair of a male R. rabuhi S HOMANN.H. l93I.BeitragezurPhysiologiederSpin- posterioreyessufficesfortriggering courtship. If nenaugen. HI. Das Sehvermogen der Lyeosiden. the PLE are involved, orientation precedes dis- Zeuschritt lurVergleiehendePhysiologie 14: 40- play. If the PME are involved, approach can 67. precede display, although it need notdo so. LAND, M.F. 1961. Optics and vision in invertebrates. Pp. 471-592. In H. Autrum (ed). 'Comparative Given that the movement-detecting PLH arc physiology and evolution of vision in inver- sufficient for courtship onset rn R, rabida, an tebrates. Handbook of sensory physiology adequate stimulus in this species may be any VI1/6B\ (Sprinuer-Vexlag: New York). object ofan appropriate size, speed, and perhaps MAGNLF..PAPLR,SAVELY, H.E.&TONGIORGI, movement pattern entering the extensive visual P. 1964.Researchonthestructureandphysiology field of the PLE. Since the other three pairs of of the eyes of a lycosid spider. I!. "The role of lycosid eyes are also assumed to be movement differentpairsofeyesinastronomicalorientation. detectors (Land, 1981), there may be no need to Archives llaliennes de Biologie 102: 123136. require- their involvement in additional visual ROVNF.R, J.S 1968. An analysis of display in the analysis before initiating courtship. However, lycosidspiderLycosarabidaWalckenaer.Animal thismay notbe trueforall lycosids.In particular. 198B9e.haWvoilofursp1i6d:er3s58l-a3c6k9.mirror-image responsive- femalePardosalaura have been hypothesized to ness seen injumping spiders. Animal Behaviour useformvisionforspeciesdiscrimination(Suwa, 3S: 526-533. (984), [folate R hutra likewise do m>, eyes other SUWA, M. 1984. Courtship behavior of three new than the PLE would be have to be used lor such formsin the wolfspiderPardosa laum complex. form analysis in orderto inititatc courtship. Journal ofEthology2: 99-107.
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