1090 Disturbancebehaviors in the Uloborusglomosus (Araneae, ): possiblepredator avoidancestrategies

Pluln E. CusHrNG AND BnrNr D. Oprll Department of Biology, Virginia PolytechnicInstitute and State University, Blacksburg, VA 24061, U.S.A. ReceivedMay 25, 1989

CusHtNc, P. E., and OpEu-, B.D. 1990. Disturbancebehaviors in the spider glomosus(Araneae, Uloboridae): possiblepredator avoidancestrategies. Can. J. Zool. 68:1090-1097. When disturbed, Uloborus glomosuseither remain in position at the hub of their orb webs,jump from the web, move to the edgeof the web, or shakethe web. Juvenilesmore frequentlyexhibited moving andjumping responses,whereas the majority of adultsjumped from the web or remainedin position. Adults with linear stabilimentatended to shaketheir webs in the morning and to jump from their websin the evening. Juvenileswith linear stabilimentashook their webs in the afternoonand evening, whereas thosewith circular stabilimentatended to move to the edgeof the web or shakethe web during all times of day. Adult femaleswith egg-sacchains were usually alignedwith the egg sacsand tendedto remain in position when disturbed.Both adults andjuveniles lacking stabilimentaor egg-sacchains tendedto jump from their webs or move to the edge of their webs. filmed in a natural settingresponded to contactby insects.Predatory wasps repeatedly flew near the spiderswithout eliciting a response.A tetheredpredatory wasp held aboveboth juveniles and adultsin the laboratoryalso failed to elicit responsesfrom the spiders.The data agree with the hypothesisthat moving to the edge of, shaking, and jumping from the web may be predator avoidance strategieselicited by direct contact.

CustttNc, P. 8., et OPELL,B. D. 1990.Disturbance behaviors in the spider (Araneae, Uloboridae): possible predatoravoidance strategies. Can. J. Zool.68: 1090-1097. En casd'aletle, Uloborus glomosuss'accroche au centrede sa toile, sautehors de satoile, seddplace vers sa bordureou la fait vibrer. Les araign6esjuv6niles ont surtoutdes r6actions de d6placementou de saut, alorsque la majoritd des adultessautent hors de leur toile ou ne bougentpas. Les adultesi stabilimenturrislin6aires ont tendanced faire vibrer leur toile le matin et h sauterhors de leur toile le soir. Les juvdniles h stabilimentums lin6aires font vibrer leur toile I'aprds-midi, alors que les juv6niles h stabilimentumscirculaires ont tendancei se d6placervers la bordureou i faire vibrer leur toile en tout temps de la journ6e. Les femellesadultes qui portentdes cocons ovigdres se tiennent ordinairement en ligne avecleurs cocons et ont tendanced garderleur position en casd'alerte. Les adulteset lesjuv6niles sansstabilimentums ou sanscocons ont tendanced sauterhors de leur toile ou i se d6placer vers sa bordure. Des araign6esfilm6es dans leur habitat naturel ont r6agi au contact d'insectes. Des gu6pes prddatricesont vol6 plusieursfois vers les araigndessans susciter de r6action. En laboratoire,les araigndesjuv6niles et adultes sontrest6es sans rdaction en pr6senced'une gu6pepr6datrice attachde et maintenueau-dessus de la toile. Les donn6esconoborent I'hypothEseselon laquelle les d6placementsvers la bordure de la toile, le tremblementde la toile ou les sautshors de la toile constituentprobablement des stratdgiesde fuite en r6action i un contact direct avec des pr6dateurs. lTraduit par la revue]

Introduction web'shub (Fig. lB). The legsof thesespiders display disruptive Although spiders are important prey items of some wasps, coloration and the first legs are beset with a setal brush birds, and other spiders (Bristowe l94l; Krombein 1967; (Fie. 1A). Robinson and Valerio 1977: Pyke 1980; Johnsgard 1983; Mature female U. glomosas and juvenile spidersoften add Coville 1987), few studiesinvestigate the defensivemecha- linear bands of silk stabilimentato the hubs of their orb webs nisms they use to avoid predation. This study has four objec- (Fig. lB). Somejuveniles add a circularstabilimentum platform tives: (f) to define more precisely and describethe responsesto to the hubs of their webs (Fig. lD) (Cushing 1988). Mature disturbanceshown by an orb-weaving , (ii) to survey female U. glomosusdeposit their stellateegg sacsin a chainthat adult and juvenile populations of the species to determine extendsalong a radius from the web's perimetertoward its hub. what factors influence the expression of the disturbancebe- When an egg-sacchain is present,a femaletypically positions haviors, (iii) to document on film actual encountersbetween herself adjacentto the most recently deposited(most centripe- the orb weaver and its natural predators,and (iv) to determine tal) egg sac where her linear posture makes it very difficult to what stimuli (vibratory, visual, or contacQelicit the disturbance distinguishspider from egg-sacchain (Fig. 1C). During this behaviors. time, femalescontinue to feed and maintain their webs. The We studiedthe orb weaverUloborus glomosus (Walckenaer), linear and circular stabilimentaand the linear chain of egg sacs family Uloboridae. These horizontal orb weaving spiders are may function as cryptic devices, concealing the spider from common throughoutthe easternUnited Statesand are abundant visually hunting predators(Hingston 1927; Bristowe l94l; on the shrubberyof the Virginia PolytechnicInstitute and State Marson 1947a, 1947b; Marples 1969; Ewer 1972; Eberhard University(vptsu) campus (Cushing 1988). Spiderlings emerge 1973;Tolbert 1975;Levi 1977;Lubin 1980). from egg sacsas 2nd instarsand reachmaturity in the 6th instar. We formulated three hypotheses:(i) the disturbancebehaviors Mature females have a cephalothorax-abdomen length of shown by U. glomosus are predator avoidancestrategies and 10-12 mm. Uloborids build their webs at night, but monitor will be expressedat different frequenciesthroughout the day, them and capture prey during both day and night. During the reflecting changesin predatorypressure; (ii) the stabilimentr day, both juvenile and adult Uloborus hang from the underside and egg-sac chains are functioning as cryptic devices anci of their orb webs in what appearsto be a twiglike cryptic posture spidersthat have thesestructures and are aligned with them are (Opell and Eberhard 1984) (Fig. lA). They remain in this lesslikely to show activeavoidance behaviors when disturbed; posture excep: when wrapping prey and when feeding at the and (ni) becausethese disturbancebehaviors protect spiders

Prinrcd in Canada / Imprimd au Canada CUSHING AND OPELL l09l

Frc. l. (A) Adult female U. glomosush^cryptic posture.(B) Femalefeeding at the hub ofa web alignedwith a linear silk stabilimentum.(C) Femalealigned with an egg-sacchain (anow points to the spider). (D) Circular stabilimentumplatform of a juvenile web. Bar, 5 mm. from hunting wasps, they are elicited by the vibratory stimuli of the observer's presence.The rubber bulb was consideredan approxi- a flying wasp. mately standardizedstimulus, similar in sizeto the rubberpencil eraser used by Tolbert (1975) in his study of predator avoidancebehaviors. Methods This stimulus was assumedto simulate the sudden contact of an attacking predator. The data were analyzedusing a log-linear analysisdesigned Description of the behaviors for multivariate categoricaldata (Bishop et al. 1975;Fienberg 1987). To more preciselydefine and describethe disturbancebehaviors, we collectedadult femaleson campusand establishedthem on framesin a ofjuveniles greenhousewhere we filmed them with a Super 8 mm movie cameraas Survey During August and September1987, we conducteda similar survey they jumped from and shook their webs in responseto contact stimuli ofjuvenile U . glomosu.sin the field. To determinethe stadiaofjuvenile (the tip of a finger). Since uloborids often shaketheir webs during prey spiderswe collected every l0th individual and measuredthe length of capture,we also filmed the shakingbehavior of an adult female when its carapace and first femur. We compared these data with the values fruit flies were placed in her web. usedby Opell (1987) to assessthe stadiaof U. glomosasfrom the same Survey of adults population. Adult spiders living in shrubbery at three sites on the vplsu campus This survey differed from the adult survey in four ways. (i) As were studiedduring June and July, 1986. We made 222 obsewations juvenile U. glomosas males spin typical capture webs, this survey during the morning (08:00-10:00), 227 dunng the afternoon (12:00- includedboth malesand females.As male and femaleuloborids cannot 14:00), and 146 during the evening (17:00-19:00) for a total of 595 be easily distinguisheduntil they enter the penultimate(5th) instar, the observations. Since adult male U. glomosas do not build typical sex of the individuals tested could not be determined. (li) Being capturewebs (Opell1979), we usedonly adult femalesin this survey. juveniles, thesespiderlings never had egg-sacchains in their webs and Temperature was inadvertently recorded during only one of three some individuals had circular rather than linear silk stabilimenta.(iii) mornings during which observationswere made (25.9'C) and two of The stimulus usedfor this juvenile survey was a 4 mm diameterplastic three afternoons(mean : 35.6oC, SD : 2.62). The mean evening sphere affixed to the end of a 15 cm long wooden applicator stick. temperaturewas 28.5oC(SD : 0.38, n : 3). Relative to spider size, this stimulus was approximatelythe samesize Fourvariableswere recordedduring the adult survey:(i) time of day, as that used in the adult survey. Although predatorsprobably feed on (tt) the presenceof a stabilimentumor of an egg-sacchain, called stab both adult andjuvenile spiders,the smaller stimulus usedfor juveniles sac, (iir) alignment of the spider with either stabilimentumor egg-sac allowed us to better observetheir responses.(iv) Morning, afternoon, chain, and (iv) responseof the spiderto disturbance.Each variablehad and evening subsurveys were conducted at different busheswithin the severalcategories, each assigneda number for the analysis(Table l). limits of each site, ensuring that no individual was testedmore than As a stimulus, we lightly touchedthe venter of each spiderthrough once. Adults and juveniles from the different sites on campus were the web with a 13 mm diameter rubber pipette bulb on the end of a assumedto be samples from a single population, although dispersal 45 cm long dowel rod. Using the dowel rod minimized the influence of distances for these spiders have not been determined. r092 CAN. J ZOOL. vol-. 68.1990

Tnslr l. Categoriesof each of the four variablesused to contact by a probe. Pipettesused for juveniles had an averagetip in the log-linear analyses diameterof 0.51 mm andthose used for adults,1.20 mm. Severaldays after testing for the effects of the contact stimulus, we testedfor the Variable Category effectsof visual and vibrational stimuli by slowly lowering the buzzing waspover eachspider until its legs were within 1-3 cm of the spider. Time l. Morning Severaldays later, we again tested all23 spidersfor their responsesto 2. Afternoon contact with a water droplet. The data were analyzedusing two-way 3. Evening contingencytable analyses. To determine the wingbeat frequency of tethered spider-hunting Stab sac l Linear silk stabilimentum Sphecidaewasps and of the Pompilidae wasp used in this experi- 2a. Egg-sacchain (adults) ment, we made direct recordings on a Sona-Graph 7029-A sound 2b. Ctcular stabilimentum(uveniles) spectrograph. 3. Neither Analysis Alignment l. Aligned* variablesrecorded 2. Not alignedt To evaluate the associationbetween the during we fitted the data to a log-linear model using the BMDP 3. No web structureto align with the surveys, statisticalsoftware package (Bishop et al. l9'75;Fienberg 1987;Dixon Response l. Jumpedfrom the web 1981). This analysis is designedfor multidimensionalcontingency 2. Moved to the edge of the web tables. The log-linear analysis provides a model that describesthe 3. Remainedin position entire data set, defining any associations(two-way and higher order 4. Shookthe web associations)between variables. Using this analysis,the magnitudeof the interaction among the categoriesof the associatedvariables in the *Long axis of the spider's body aligned with the web structure. -ll-ong chosenmodel can alsobe assessedby calculatingratios of the log-linear axis of the spider's body not aligned with the web structureor the spider away from the hub. parameterestimates to the standardenors. Parameterestimates are calculated under the assumptionof norrn- ality. Therefore, ratio terms > 11.961(corresponding to p values There were 1800 total observationsin this survey: 600 each during <0.05 in a normal Z-table) indicate categoriesthat contribute signifi- the morning, afternoon, and evening. At the times observationswere cantly to the associationbetween the variables(Bishop et ol. l9l5:- made,the meanmorning temperature was20.2"C (SD : 3.24, n : 9); Kennedy 1983). Positive and negative ratios indicate a positive and the meanafternoon temperature was 25.3"C(SD : 2.09, n: 10);and negativeassociation between the categories,respectively. the mean evening temperaturewas 24.3"C (SD : 3 .07, n : 8). As in the adult survey, at eachsite we recordedtime of day, presence of a silk stabilimentum, alignment with the stabilimentum, and Results disturbancebehavior shown by the spiderling. These data were also Description of the behaviors analyzedusing a log-linear analysis. The Super-8films showedthat jumping behaviorhas several Predatory encounters distinct elements. (i) The spider propels itself off the web We used a VHS (video home system) camerato obtain qualitative anteriorly, at an angleof approximatelyl6o to the vertical. (rr) It information on the adaptive value of these behaviors as predator releasesa variable length of dragline silk attachedto the web's avoidancestrategies. The camera was set up on a tripod on the open hub and hangs at the end of this dragline in a cryptic posture. porch of a farmhousein rural Montgomery County, VA, that supported Both at the hub and at the end of the dragline, the spider glomosus.An glomosusfemale was a naturalpopulation of U . adult U. maintains an approximately horizontal orientation, althoughat allowed to build a web within a22 x 22 cm squarehorizontal frame the hub the long front legs arebent at the tibiae-metatarsusjoint constructedof wooden dowel rods. This frame was then hung from the rafters of the porch directly beneath an active mud dauber nest about 80o,whereas at the end of the dragline the legsare bent at (TryporyIor?sp.). When a spiderdisappeared or refusedto build a web this joint only aboutzs" . (iii) After an interval of a few seconds for severaldays, it was replacedwith another adult female. Each day to 20 min, the spider swings upward and graspsthe dragline after filming, spiderswere fed with fruit flies (Drosophila sp.) blown with the first two pairs of legs. It usesthese legs to ascendthe into their webs. Eight femaleswere filmed for approximately50 days draglineto the web's hub. (iv) The spiderstops from oneto five from about 08:00 to 19:00, from late June through August, 1987. We times on its assent. At each stop, it reassumesthe cryptic used6-h VHS videocassettetapes to minimize disturbanceduring the posture,orienting itself vertically ratherthan horizontally, with filming episodesand reviewed them in fast-forward mode. the long first legs directed toward the web and bent at the Stimulus experiment tibiae-metatarsusjoint about 90o. We establishedfourteen 2nd- and 3rd-instar spiderlings (rearedin The shaking behavior, induced by touching the spider's the laboratory from a single egg sac) and nine adult females in an venter,consists of rhythmic oscillationsthat continuefor several experimentalroom with an averagetemperatureof 22.3"C (SD : 3.13, seconds.It also hasunique features:the spideralternately flexes n: 12).Each spiderling was placed in a 10.5 x 10.5 x 8.5 cm plastic and extendsits long front legs and, to a lesserextent, the second freezercontainer with wooden applicator sticks glued inside for web pair of legs. Thesesudden flexion-extension sequences result placed in x 16.5 x 9 cm plastic attachment.Each adult was a 31 in the rhythmic movement of the spider's body and set up web shoeboxwith wooden dowel rods glued inside. oscillations. We useda tetheredspider-hunting wasp of the family Pompilidaeto shakingbehavior prior to prey test the combined effects of visual and vibratory stimuli. A long piece Super-8films showedthat the of thread was glued to the wasp's thorax and insertedthrough a clear wrapping consists of a different set of movements,resulting plastic drinking straw so that the wasp could be controlled without principally from alternateflexion and extensionof the third pair impairing its wing movement. of legs and from alternatelowering and raising of the abdomen. To testthe responsesof the spidersto a contactstimulus, we dropped The fourth pair of legs primarily servesto hold onto the web. water on the venter of each using Pasteurpipettes. This stimulus was suggestedby W. G. Eberhard(personal communication), as it is more Frequency of avoidance behaviors easily standardizedthan touching spiders with a probe. Preliminary Tables 2 and 3 presentthe observedfrequencies of adult and observations showed that spidersresponded similarly to a water drop as juvenile behaviorspermitting comparisonswith the behavioral CUSHING AND OPELL 1093

Tenle 2. Survey of adult responsesto contact stimuli (total number of observations was 595)

Responses

Stab sac Alisnment Time Jumped Moved Remained Shook

Linear Yes Morning 307 J 5 Afternoon 19 t2 5 I Evening 21 7 t 0 No Morning 42 0 0 Afternoon 80 I 0 Evening 1l I 0 0

Egg sac Yes Morning 37r 744 Afternoon 233 57 I Evening 166 380 No Morning t0 20 Afternoon 60 10 Evening 50 0l

Neither Morning 32 ll I 2 Aftemoon 58 t7 7 8 Evening 28 9 0 2 Total 299 76 196 24 Vo 50 l3 33 4

Tlnln 3. Survey of juvenile responsesto contact stimuli (total number of observations was 1800)

Responses

Stab sac Alignment Time Jumped Moved Remained Shook

Linear Yes Morning 90 t2r l3 40 Afternoon 85 r24 82 Evening tr4 156 t7 119 No Morning 8 20 0 7 Afternoon 25 42 I l9 Evening t4 27 4 27

Circular Yes Morning 9 23 J 6 Afternoon l3 23 0 l4 Evening 8 13 2 t2 No Morning 0 0 0 2 Afternoon 0 0 0 0 Evening 0 0 0 I

Neither Morning 63 r52 ll 32 Afternoon 34 79 J 49 Evening 22 37 4 23 Total 485 817 65 433 Vo 27 45 4 24 tendenciessuggested by log-linear analyses (below). The their webshad no web structureswith which to align. Therefore, majority of adultsjumped from their webs in responseto contact the data for thesespiders were analyzedseparately. A two-way and most of the spidersthat remained in position had egg-sac contingency table analysis comparing the associationbetween chains in their webs. The majority of juveniles moved to the the time of day and the responsevariables indicated indepen- edgeof the web in responseto contactand very few remainedin dencebetween the two variables(G' : 9.94,p : 0.1273,df : 6). position. Therefore, a log-linear analysis fitted these data to a model that treatedthe time and the responsevariables separately (i.e., Survey of adults two-way or higher order associationterms were omitted from Spiders that had neither silk stabilimenta nor egg sacs in the model). t094 cAN. J. ZOOL. VOL. 68, 1990

Tlsrn 4. Ratio terms (Z-values) for the responseX time, responseX stabsac, responseX alignment, time X alignment, and stab sac x alignment associationsof adultswith linear stabilimentaand adults with egg-sacchains

Response Alignment

Jumped Moved Remained Shook Yes No

Time Morning -0.785 -2.879* -0.733 2.432* 2.733* -2.733* Afternoon -0.32r 0.817 0.703 -0.564 -0.946 0.946 Evening 0.864 1.819 -0.056 -1.t49 -2.168* 2.168* Stab sac Linear l .839 4.674* -7.856* 0.967 -2.tt7* 2.r17'r Egg sac - 1.839 -4.674* 7.856* -0.961 2.117* -2.117* Alignrnent Yes -2.711* 0.726 1.886 -0.482 No 2.7r1* -0.726 - 1.886 0.482

*P < 0.05.

The ratio of the log-linear parameterestimate to its standard Tnnln 5. Ratio terms (Z-values) for the time x responseand time enor showed that spiderswith no web structurestend to ju-p X alignment associationsof adults with linear stabilimenta from their webs when disturbed (ratio : 10.979), tend not to remainin position(ratio : -3.379), and tend not to shakethe Time web (ratio - -3 .852). For this andall othermodels in which the time and responsevariables were analyzedseparately, only the Morning Afternoon Evening ratios of the responsevariable are reported, since the ratios of Response the time variable simply reflect samplingpatterns which do not Jumped -r.939 -1.942 2.119* affect the resultsof the responseanalysis. Moved -2.t78* - 1.119 r.829 A log-linearmodel selectedfor adultswith linear stabilimenta Remained - 1.488 0.000 1.488 or egg-sacchains in the hubs of their webs indicatedthat there Shook 2.t69* 1.580 -2.031* were two-way associationsbetween the following five pairs of Alignment and response, response variables:time time and alignment, and Yes r.724 -0.075 -1.862 alignment, responseand stab sac, and stab sac and alignment No -r.724 0.075 r.862 (G' : 30.99, P : 0.1892, df : 25). Adding the two-way associationsbetween time and stabsac did not improve the fit of the model. No higher order associations(i.e., three-way) contribute significantly to the fit of the model. to shake the web. In the evening, these spiderstend to ju-p This model indicated that adults with egg-sacchains exhibit from the web and tend not to shaketo web (Table 5). different behaviorswhen disturbedthan do femaleswith linear Of 276 adultswith egg-sacchains in the hubsof their webs, stabilimentaand that they are aligned with their egg sacs far only 16 (6Vo) were not aligned with those web structures. more often than spiderswith linear stabilimentaare aligned with Therefore, the data for all 276 spiderswas analyzedregardless thesestructures (Table 4). Only 6Voof the spiderswith egg-sac of alignment. A two-way contingencytable analysiscomparing chains were not aligned, whereas 20Voof spiders with linear the association between the time of day and the response stabilimentawere not aligned. This is a significant difference variablesdid not indicate associationbetween the two variables (G2:7.92, p < 0.005, df - 1). Becauseof thesefindings (G' : 9.27, p : 0.1590,df : 6). A log-linearanalysis fitted and becauseCushing (1988) found that females remaining thesedata to a model that treatedthe time andresponse variables aligned with their egg sacs actively protected them against separately(i.e., the two-way associationterm was omitted). parasitoidwasps, we deemedit inappropriateto equatethe func- The ratio termsindicated that adultswith egg-sacchains show tional significance of egg-sac chains and linear stabilimenta. a strongtendency to remain in position when disturbed(ratio : Therefore, we analyzed the data for spiders with linear 11.954)or to jump from the web (ratio : 6.845).They tend stabilimentaseparately from the data for spiderswith egg-sac neither to move to the edge of the web (ratio : -4.331) nor to chains. shakethe web (ratio - -5.152\. The log-linear model selectedfor adults with linear stabili- We also conducted a two-way contingency table analysis mentain the hubs of their webs indicatedtwo pairwise associa- comparing the responsesof femaleswith linear stabilimentato tions amongthe variables(G' : 12.40,p : 0.1344, df : 8): those without stabilimentaor egg-sacchains. The responsesof one betweentime and responseand anotherbetween time and spiderswas independentof the presenceof linear stabilimenta alignment. Adding a two-way associationterm between re- (G2 :0.84, p :0.8409, df : 3). Both spiderswith andwithout sponse and alignment or a three-way term among time, stabilimentatend to jump (ratio : 14.724)or move to the edge response,and alignmentdid not significantly increasethe fit of (ratio : 2.353) when disturbed and tend not to remain in the model. This model indicated that, in the morning, spiders position(ratio : -4.318) or shakethe web (ratio : -5.402). with linear stabilimentatend not to move to the edge,but do tend Spidersalso tend not to build stabilimenta(ratio : -2.400). CUSHING AND OPELL I 095

Tnnu 6. Ratio terms (Z-values)for the time x responseassociation Tlu-E 7. Ratio terms (Z-values)for the responsex stabsac associa- of juveniles with no stabilimentaand for the time X responseand time tion of juveniles with linear stabilimentaand those with no web x alignmentassociations of juveniles with linear stabilimenta structures

Time Response

Morning Afternoon Evening Jumped Moved Remained Shook

No stabilimentum Stab sac Linear 1.393 -2.824* -0.161 1.360 Response Neither -t.394 2.824* 0.161 - l.361 Jumped 0.463 -0. 130 -0.246 Moved r.696 0.540 - l .850 Remained 1.103 -t.491 0.703 : :0.2609, : Shook -3.752" 2.850* 0.575 time andalignment (G2 11.22,p df 9). Adding a three-way association term among time, response, and Linearstabilimentum alignment,or a two-way term betweenresponse and alignment Response did not significantly increasethe fit of the model. This model Jumped 1.094 0.798 -2.112+ indicatedthat, in the morning, spiderlingswith linear stabili- -2.535* Moved 1.004 1.241 mentado not tendto shaketheir websand tend to be alignedwith -1,.987* Remained l.280 t.072 their stabilimenta;in the afternoon,they do not tendto remainin -4.004* Shook 2.268* 2.279* position, do tend to shaketheir webs, and do not tend to be Alignment alignedwith the stabilimenta;and in the evening,they do not Yes 2.695* *3.9n* 0.619 tend to eitherjump from the web or move to the edgeof the web, -2.695* -0.619 No 3.917* but do tend to shakethe web (Table 6). We also conducteda two-way contingencytable analysis *P < 0.05. comparingthe responsesof spiderlingswith linearstabilimenta Surveyof juveniles to thosewithout stabilimenta.The responsesofjuveniles varied : Carapacelength and first femur length measurementsindi- depending upon the presenceof linear stabilimenta(G2 : : catedthat all juveniles were in either the 3rd or 4th stadia. 16.09,p 0.0011,df 3). When disturbed,spiderlings with Becausespiderlings with neither linear not circular stabili- linear stabilimenta tend not to move to the edge of the web menta in their webs had nothing to align with, their responses whereasthose without stabilimentado Oable 7). were analyzedseparately. A two-way contingencytable analy- Predatory encounters siscomparing the associationbetween time of day and response During approximately 280 h of filming, three maturefemale indicatedthat responsesof the spiderlingswith no stabilimenta U. glomoru.r responded 15 times to contact. All responses in their websvary dependingupon the time of day (G' : 24.46, occurred between ll:45 and 19:00 and were exhibited by p : 0.0004, df - 6). This model indicatedthat spiderlings femaleswithout egg sacsor stabilimenta.One femalejumped with no stabilimenta do not tend to shake their webs in the from her web in responseto contact by the long antennaeof a morning, but do tend to shakethem in the afternoon(Table 6). grasshopper(suborder Ensifera) that walked along the dowel Of the 1800 spiderlingsobserved, 129 (7Vo)had a circular frame, and anotherjumped to escapean unquestionablewasp stabilimentumat the hub of their webs. Unlike a linear stabili- attack. At about 14:50, this female was resting in a cryptic mentum,which follows a singleradial line, a circularstabilimen- posture at the hub of the web when a wasp flew toward the tum coversthe entirehub (Fig. lD). Of these129 spiderlings, spider, momentarily hovered a short distance above her, and only 3 (ZVo)were not positioned beneath this silk platform. thendropped, contacting the spider'sventer. The spiderjumped, Sincea spiderlingcould be orientedin any direction and still be successfullyeluding the wasp; then, approximately20 s later, beneaththis stabilimentum,we consideredthis orientationdif- she began ascendingher dragline to the hub. The attacking ferent than the alignment of adults or juveniles with a linear wasp was not a Trypoxylon; however, we were unable to stabilimentumor an egg-sacchain. Therefore,the datafor these identify it with certainty from the film (perhapsSphecidae or 129 spiderlingswere analyzedseparately, regardless of "align- Pompilidae). ment" beneaththe stabilimentum. One femalepropelled herselfto anotherpart of the web seven A two-way contingencytable analysisof spiderlingswith times in responseto contactby insects(ants and a grasshopper) circular stabilimentaindicated that responseto disturbancewas and two times to unobservedstimuli. In other females,we noted independentofthetimeof day (G2:8.84,p:0.1825, df :6). three instancesof web shaking, one in responseto an insect To detect which responseswere most likely to be shown, we approximately 3 mm long contacting the web and two in conducteda log-linear analysisthat fitted thesedata to a model responseto unknown stimuli. On 16 occasions,wasps flew that treatedthe time and responsevariables separately (i.e., the within 3 cm of spiderswithout elicitingdefensive behaviors. On two-way association term was omitted). The ratio terms one occasion,a wasp crawling from its nest along the ceiling indicatedthat, when disturbed,spiderlings with circular stabili- contactedthe spider, causing her to move from the hub to the mentatend to move to the edgeof the web (ratio : 5.696) or to edge of the web. shake the web (ratio : 2.215). They tend not to remain in position(ratio : -4.527). Stimulus experiment To detect associationsbetween the time, alignment, and A spider's responseto visual-vibratory and contact stimuli responsevariables for juveniles with linear stabilimenta, the was recordedas either active (umped from, moved to the edge data were fitted to a log-linear model. This model indicated of, or shookthe web) or asremaining in position(Table 8). Four two-way associationsbetween time and responseand between two-way contingency table analyseswere conductedto deter- 1096 CAN. J. ZOOL. vol-. 68, 1990

Tnsln 8. Responsesof juveniles and adults to contact by water jumping from the web can protect a spiderfrom visually hunting dropletsand to a tetheredwasp; active responsesinclude jumping from, predators. moving to the edge of, and shaking the web Some spider-hunting predators, such as wasps and birds, more actively hunt in the afternoonand evening (Bristowe 1948; Stimulus Stiles and Wolf 1979; Coville 1987) whereasothers, such as hunting spiders,are active throughoutthe day (Anderson 1970; Droplet Droplet Gardner 1965;Abraham 1983). The effect of time of day upon Response (initial) Wasp (subsequent) Total the responsesexhibited by both adult andjuvenile U. glomosus Active is consistent with the hypothesis that the activity patterns of Juvenile 10 2 l4 26 spider predators have influenced the spiders' behaviors. The Adult 7 0 7 l4 alternative explanation that temperature affects thesebehaviors Total t7 2 2l 40 is not supportedin U. glomosus (Cushing and Opell 1990). Remainin position The results are also consistent with the hypothesisthat an Juvenile 4 t2 0 r6 adult female aligned with an egg-sacchain is concealedfrom Adult 2 9 2 13 visually hunting predators, as these spiders tend to remain Total 6 2l 2 29 alignedwith their egg sacswhen disturbed(Fig. lC). However, Cushing (1988) found that U. glomosus females aligned with their egg sacsalso exhibit unique, apparentlydefensive behav- iors in responseto parasitoidwasps walking on their egg sacs. mine if spidersexhibited different frequenciesof active responses The majority of juveniles with circular stabilimenta were to the water drop stimulus and the stimuli produced by the positionedbeneath the stabilimentum,suggesting that they may tethered wasp. The comparisons analyzed were initial drop utilize the cryptic potential of these web structures(Fig. 1D). versuswasp and wasp versussubsequent drop (forjuveniles and However, spiderlings with circular stabilimentastill tendedto for adults in both comparisons). Yates correction for small actively respond when disturbed. This tendency to position sample sizes was applied to all the frequency data (Sokal and themselvesbeneath the stabilimentamay, instead,be an artifact Rohlf 198l). All four analysesresulted tn G2 valuesgreater than of their usual tendencyto monitor their webs from the hub, as 7 .52, p valuessmaller than 0.01, and df valuesequal to l. For this is the position from which spiders can best detect and both adults and juveniles, the wasp (i.e., the visual and respond to prey intercepted anywhere in the orb web (Barth vibratory stimuli) elicited significantly fewer active responses 1982). At the hub, juveniles with circular stabilimentamay be than the contact stimulus. oriented in any direction and still be hidden by this structure. Sceliphron (Sphecidae)wingbeat frequency rangedfrom 75 This study doesnot supportthe hypothesisthat the vibrational to 275 Hz, Tryporylon (Sphecidae) from 200 to 300 Hz, and visual stimuli produced by a wasp elicits disturbance Chalybion (Sphecidae) had a frequency of 7O Hz, and the behaviorsin U . glomosus.The experimentcomparing spiders' pompilid wasp producedfrequency values between 136 and 480 responsesto a contact stimulus and to the combined vibratory Hz. and visual stimuli of a tetheredwasp indicatedthat the contact stimuli used in both the adult and the juvenile surveys were Discussion appropriate disturbance stimuli. In both adult and juvenile We found that time of day, presenceof a web structure spiders,contact is required to elicit disturbancebehaviors. The (stabilimentumor egg-sacchain), and alignment with the web wingbeat frequencies of the examined sphecid and pompilid structureseach influence the disturbancebehaviors shown by wasps are all within the range detectableby trichobothria, the U. glomosus adults and juveniles. However, adults and juve- long sensoryhairs that adorn the legs of uloborids (Opell 1979) niles (3rd and 4th stadia) are affected differently by these and detect airborne vibrations (Barth 1982). The wasp used in factors. The majority of adults jump from the web when the stimulus experiment was held within the visual field disturbed,whereas the majority ofjuveniles move to the edgeof coverageof U . glomosus(Opell andWare 1987). Therefore,the the web. Time of day and the presenceof stabilimenta also spiderswere probably able to perceivethe wasphovering above affect adults andjuveniles differently. Theseresults agree with them. the hypothesesthat (i) the disturbancebehaviors are predator Spidersmay conservetheir energyresources when facedwith avoidance strategies influenced by time of day and (ii) the ambivalentor harmlessstimuli, suchas a largeinsect flying near egg-sacchains function as cryptic devices that make spiders them, but readily react to potentially life-threateningstimuli aligned with them less likely to show active avoidancebehav- posedby direct contact, or they may remain in position to avoid iors when disturbed. detectionuntil it is clearthey havebeen discovered. This may be Although theseresults do not excludealternative hypotheses, why adults and juveniles aligned with linear stabilimentaalso severallines of evidencesuggest that the observeddisturbance tended to show active avoidance behaviors when disturbed. behaviors are distinct predator avoidance strategies. Both Alternatively, thesedisturbance behaviors may haveevolved in shaking and jumping behaviors are characterizedby elements responseto a spider predator other than wasps. not found in the spiders' primary activities of web monitoring The different frequenciesof disturbancebehaviors exhibited and prey capturing. The active responses(umping, shaking, by adults and juveniles may reflect ontogeneticchanges, dif- and moving to the edgeof the web) areexhibited by membersof ferences in predation pressure, and (or) differences in the other orb-weaving and non-orb-weaving spider tamilies and have energeticor strategiccosts of eachbehavior. For example,50Vo often beenreported as responsesto predatorattacks, usually by of adult spidersjumped from the web when disturbed,but only waspsor hunting spiders(Pekham and Pekham 1887; Marples 27Voof the juveniles showed this behavior. Juvenilesare both 1969; Eberhard 1970, 1973; Robinson and Robinson 1970, more clusteredand more denselydistributed than adults (P. E. 1978; Ewer 1972; Edmunds 1974; Tolbert 1975; Levi 1977; Cushingand B. D. Opell, personalobservation). Because adults Hoffmaster 1982). The video filming in this study shows that and 3rd- and 4th-stadiajuveniles have little temporal overlap CUSHING AND OPELL to97

(P. E. Cushing and B. D. Opell, personalobservation), any 1973. Stabilimentaon the websof Uloborusdiversus (Araneae: intraspecific interactions occur between similar age (size) Uloboridae) and other spiders. J . Zool. l7l: 367 -384. classes.Therefore, it may be more costly forjuveniles to jump EotrluNos, M. 1974. Defense in : a survey of antipredator from the web, since under their relatively crowded conditions, defenses.Longmans, Essex. they have a greater risk of intercepting a neighbor's web and EwER, R. F. 1972. The devicesin the web of the West African spider J. Nat. Hist. 6: 159-167 . being treated as prey. Uloborus glomosus spiderlings do flavipalpis FrrNBEnc, S. E. 1987. The analysisof cross-classifiedcategorical cannibalizeeach other in captivity (P. E. Cushingand B. D. data.2nd,ed. M.I.T. Press,Cambridge. Opell, personalobservation) and may do so in natureas well. GTRDNEn,B. T. 1965. Observationson three speciesof Phidippus (1952) Crane defined sevendistinct defensivemechanisms in jumping spiders(Araneae:Salticidae). Psyche,72: 133-147 . invertebrates:crypsis, active escape, startle response, with- HlxcsroN, P. W. G. 1927. Protectivedevices in spiders'snares, with a drawal into protected position, attack, unpalatability, and description of seven new species of orb-weaving spiders. Proc. chemicalconcealment. uloborus glomosusexhibit the first four Zool. Soc. London, 1927(18):259-293. of thesemechanisms. (t) These spidershave cryptic coloration Horrunsrrn, D. K. 1982. Predator avoidance behaviors of five and posture. They also enhancetheir morphological crypsis by speciesof Panamanianorb-weaving spiders (Araneae; Araneidae, incorporating silk stabilimenta and egg-sac chains into their Uloboridae).J. Arachnol. 10: 69-73. JoHNsceno, P. A. 1983. The hummingbirds of North webs. (ii) When disturbed, some spiders actively escapeby America. SmithsonianInstitution Press, Washington, D.C. jumping from their webs. (iii) Others shake rhe web, which KTNNEDy, J. J. 1983. Analyzing qualitative data: introductory probably servesto blur the outline of the spider or to startlean log-linear analysisfor behavioral research.Praeger Scientific, New affacking predator (Edmunds 1974). (iv) Some U. glomosus York. withdraw to the edge of the web, where they are probably Knounsrx, K. V. 1967. Trap-nestingwasps and bees:life histories, concealedfrom attackby surroundingvegetation. These mecha- nests,and associates.Smithsonian Institution Press, Washington, nisms are common to many different web-weaving spiders. D.C. LevI, H. W. 1977. The American orb-weaver genera Cyclosa, Ackowledgments Metazygia andEustala north of Mexico (Araneae:Araneidae). Bull. We are grateful to Richard D. Fell, Thomas A. Jenssen,and Mus. Comp. Zool. 148:61-127. LUBIN, Y. D. 1980. The predatory behavior of Cyrtophora (Araneae, David A. 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