W. W. Tolbert.
Predator Avoidance Behavior and Web Defensive Structures in the Orb Weavers, Argiope aurantia and Argiope trifasciata (Araneae, Araneidae).
Psyche 82:29-52, 1975.

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PREDATOR AVO1,DANCE BEHAVIORS AND
WEB DEFENSIVE STRUCTURES IN THE
ORB WEAVERS ARGIOPE AURANTIA
AND ARGIOPE TRIFASCIATA
( ARANEAE, ARANEIDAE) *
Graduate Program in Ecology, University of Tennessee, Knoxville, Term. 37916
Many spiders spend virtually all of their lives on orb webs. Orb weavers are known from all continents except Antarctica, as well as many island groups. In addition to a cosmopolitan distribution, in- dividual species are locally abundant in a variety of habitats. The diversity of this assemblage is also quite pronounced with 2500 species of Araneidae, 150 species of Uloboridae and over a dozen species of Tetragnathidae recognized (Levi and Levi, 1968). Since the uloborids are not closely related to the other two orb-weaving families, the ability to construct orb webs probably evolved inde- pendently (Kaston, 1966). It is generally conceded that the orb web is a highly developed type of spider web (Kaston, 1964) which allows exploitation of aerial food sources (insects and other inverte- brates), not readily available to other spiders, with a minimum of wind damage to the web. Despite the apparent success of this web type, it allows exposure of its occupant not only to the exigencies of the abiotic environment but to predators and parasites as well. Orb weavers fall prey to wasps (Muma and Jeffers, 1945; Kurczewski, 1963 ; Kurczewski and Kurczewski, 1968a, 1968b and Dorris, 1970), birds (Robinson and Robinson, 1970 and Royama, 1970) and other spiders (Enders, 1974). Vertebrate predators such as frogs, toads and lizards may be locally important.
While predator avoidance behaviors have been examined in several animal groups (Tinbergen, 1969 and Eibl-Eibesfeldt, 1970), no formal study has been completed on spiders. Several earlier spider workers (Bristowe, 1941 and Cornstock, 1940) noted that web flexing, dropping from the web, color changes and other behaviors were elicited when spiders were disturbed. Gertsch (1949) listed some escape responses of the line weaver Pholcus phalangioides *Manuscript received by the editor January 25, 1975 P5whe Ìö2:2%5 (IW5). hup Y/psychc enlclub org/8882-029 him)



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(Fuesslin) and Savory (1964) discussed web flexing, dropping from the web and death feigning as reflex responses. Robinson and Robin- son ( 1973) ascribed a defensive function to movement by Nephila maculata (Fabricius) up the w'eb, sometimes onto nearby vegetation. Eberhard (1970) was able to relate dropping from the retreat by Araneus cornutus (Clerck) to attack by predatory wasps. This study identifies some of the components of predator avoidance behavior in Argiope aurantia Lucas and A. trifasciata (Forskal), which are known as the black and yellow garden spider and banded garden spider respectively. The frequency of occurrence of various components is determined for both species ; response variation with instar and direction of approach by a predator model is assessed. In addition, specific aspects of web architecture, barrier webs and sta- bilimenta, are examined and the possible relationships to predator avoidance behaviors are discussed.
I wish to thank Mr. David Stair for field assistance, my wife Ginny for preparation of the figures and Drs. Susan E. Riechert and Gordon M. Burghardt for critically reviewing th,e manuscript. Financial support was provided by the NSF (grant BMS 74- 17602) and by the Graduate Program in Ecology at the University of Tennessee, Knoxville.
During the spring of 1974 a field study of mortality factors and migration characteristics of the orb weaver Argiope aurantia was initiated in an overgrown, abandoned pasture 2 mi. west of Glendale, Loudon County, Tennessee.
While engaged in this research, I fre-
quently observed encounters between the two Argiope species, auran- tia and trifasciata, and salticid spiders, Phidippus audax (Hentz)
and P. cZmus (Keyserling).
Some attacks by the salticids were suc-
cessful, some resulted only in leg losses by Argiope and some were unsuccessful. Due to the brevity of these encounters I rarely ob- served complete sequences. Thus, in order to obtain quantitative evidence concerning the nature of predator avoidance in Argiope, an artificial predator was employed. For the purposes of this study, a standard-sized lead pencil with rubber eraser (roughly the cross- sectional diameter of the salticids) was used to simulate an inverte- brate predator. Spiders were approached with the eraser end of a pencil from either the ventral surface, in which case the hub of the web near the eye region was touched 01- from the dorsal surface. When approached dorsally either the eye region or to a lesser extent



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19751 Tolbert - Avoidance Behavior in Orb Weavers 31 ( <5%) the abdomen was touched. I positioned myself approxi- mately 0.5-1.0 m either directly behind or directly in front of the web depending on the direction of model presentation to be used. In employing this model the assumption was made that all spiders tested, regardless of instar and species, recognized the model as a predator. Data on construction of barrier webs or "tangles" and the nature of stabilimenta we're gathered throughout the summer in an attempt to assess possible anti-predator functions. The chi-square test and Cox and Stuart test for trend were used in the statistical analyses. The taxonomy of Argiope follows Levi (1968). The orbs of A. aurantia and A. trifasciata are "typical" araneid webs, consisting of foundation lines, radii, spirals, a free zone and a hub. Neither species constructs a retreat. The spider is normally located at the hub in a head-down position. The web is inclined slightly from the vertical and there may be several stabilirnenta bands in or near the hub (fig. I). Up to two barrier webs (fig. 2) may be associated with each orb web.
Barrier webs or "tangles" were frequently constructed by A. tri- fasciata and to a lesser extent by A. aurantia. Essentially a barrier web is an irregular non-viscid silk mesh connected to the orb web and nearby vegetation or other supports. There can be up to two such tangles, with the primary barrier web positioned behind the dorsum of the spider. The secondary barrier, which is nearly always smaller, is located on the other side of the orb (fig. 2). In early
instar A. trifasciata the primary barrier web is quite cone-like with the orb forming the base of the "cone".
A small gap is left at the
bottom of the orb and the cone through which the spider may drop if disturbed. Since these barriers are connected to the outer edge of the orb, disturbances (vibrations) are transmitted to the spider. It
is generally thought ( Comstock, I 948 ; Gertsch, I 949 and Marples, 1969) that they serve some defensive function. My experience with
these two species confirms this observation. In paint marking spiders on the dorsum I have often accidentally touched the barrier web, alerting the spider and making it more difficult to mark. In addition to an early warning function, the barrier webs, particularly the pri- mary barrier, constitute a physical obstacle to invertebrate predators. Such barriers reduce the direct points of entry that predators might



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32 Psyche [March
otherwise employ. This is not to suggest that barrier webs are im- penetrable ; they are easily penetrated, but in the process the occupant is forewarned.
Barrier webs do not act as prey catching structures per se though they may slow down grasshoppers and other relatively strong prey and thereby facilitate capture. Twenty prey items (leaf-hoppers and flies) were tossed onto the primary barrier webs of 20 different A. trifasciata. In 19 of 20 cases the prey were either ignored or the spider plucked strands of the orb with no subsequent action. In one instance the prey, a leafhopper, struggled to a point very close to the margin of the tangle and the orb web where it was successfully attacked. In the capture the spider did not completely leave the orb web at any time. Incidental field observations during the summer are in close agreement with the results of this test. The occurrence of barrier webs changes markedly with the instar of A. trifasciata (Table I ) . With the increase in secondary barrier webs, the primary webs are made less cone-like and the mesh pro- gressively coarser. Adult males rarely build complete webs since they generally abandon the web building habit upon reaching maturity and begin the search for females. When the male locates a female or penultimate female web site, he remains on the barrier web until mating can take place. Mating occurs generally within a few days, sometimes within a few hours after the female adult molt. Female TABLE 1.
Barrier webs and stabilimenta of all field' instars of A. trifasciata Instar Number Primary
Secondary Stabilimenta :
of barrier barrier mean number
webs1
web web bands/web k S.E.
2
3
4
5
6
Juvenile 9 7
Penulttimate 8 7
Juvenile 9 8
Penultimate 9 9
Adult 9 10
1Represents minimum number of webs examined with no more than one web/spider counted.




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19751 Tolbert - Avoidance Behavior in Orb Weavers 33 A. trifasciata virtually cease construction of barrier webs one to two weeks after becoming adults. The omission of barrier webs by ma- ture adult females may relate to the increased size and strength of the female (size increase is quite rapid at this time), to decreased activity of salticids, to the need to maximize food intake before cold weather (both sides of the orb are available as catching surfaces rather than one side or parts of two sides), to nerve degeneration or some other factor(s). No data are available at this time to determine the relative importance of these various factors. It is interesting to compare the use of barrier webs by the two Argiope species. A. aurantia is the larger of the two and it achieves its larger size in a relatively short time. Larger size probably deters some salticid and other attacks 'by invertebrate predators. I did not observe such attacks on penultimate and adult A. aurantia while they were a frequent occurrence on juvenile A. trifasciata at the same time. A. aurantia construct fewer barrier webs and this activity is restricted primarily to the mid-instars. A. trifasciata is smaller, matures more slowly and constructs barrier webs throughout most of its life (Table r ). Since the primary barrier excludes some prey as well as predators, the inter-relationship between spider size, preda- tor avoidance behavior, food intake and web architecture must be complex. Factors controlling the building of barrier webs need to be determined in order for the niche relations of these two closely related, sympatric species to be properly evaluated. STABILIMENTA
Stabilimenta, the white zigzag lines of silk which form discrete bands in or near the hub of the orb of several spider species, are a common feature in h o p e webs. These structures vary considerably in form and relative size both between A. aurantia and A. trifasciata and within each species.
Since I found stabilimenta to possess some defensive value to these spiders, their structure and frequency of oc- currence are discussed here.
A. aurantia build {extensive disc-shaped stabilimenta as early and mid-instars (fig. I). Up to 7 individual bands were often found in webs but never more than this and usually less (Table 2). A Cox & Stuart test for trend (Conover, 1971) revealed a significant de- crease (p<0.05) in the number of bands occurring from mid-instar to adult female.
This trend is apparent in Table 2. Older spiders construct a thinner "patch" of silk at the hub in place of distinct stabilimenta bands. Adult females make this patch as well as an accompanying linear band b'elow the hub. I also compared adult



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TABLE 2.
Barrier webs and stabilimenta of A. auranti.al N Mean number of Barrier
bands å S.E. webs
Early & mid-instars (study area) 61 4.789 z!c 0.218 9 Penultimate & adult ?'s (study area)
28
2.429 2 0.196 0
Older adult 9's (study area) 29
1.828 å 0.100 0
Older adult 9's (Knox Co., Tenn.) 5 0 1.740 å 0.085 0 1Thin "patch" was not assigned a value and thus was not used in calcu- lations.
female webs in my study area to those of a population near Stock Creek Boat Dock in Knox County, Tenn. The results of a t-test showed no significant difference (p<o.05) in the number of bands in these two populations. It is interesting that Reed, et a!., (1969) found "no obvious pattern or change in complexityn in laboratory- reared A. aurantia. Whether this difference is due to selection pres- sures or possibly some cue(s) existing in field situations that do not exist in the laboratory is not known.
The stabilimenta of A. aurantia can conceal the spider. Conceal- ment of the spider's state (especially when molting) is probably advantageous. Both Argiope species molt at the hub during the day and are completely defenseless during this process. Concealment of the true size of the spider may also be a deterrent to the invertebrate predator since larger orb weavers can ward off and maybe even kill a smaller attacker. It is even possible that stabilimenta conceal attack- eliciting stimuli from certain predators. A. trifasciata constructed substantially fewer bands in their webs than A. aurantia (Tables I & 2). A Cox & Stuart test for trend indicated a significant increase (p<o.o5) in the number of bands with instar of A. trifasciata (20 individuals of .each instar were selected at random prior to testing). These results differ from Com- stock ( 1948) who found that juvenile A. trifasciata built extensive disc-shaped stabilimenta. The reasons for these differences are not known, but I suspect that extensive use of barrier webs and the increase in stabilimenta bands may be related to heavy predation pressure by salticids.
Stabilimenta can also function as physical shields. The heavy silk bands reinforce the hub and make direct penetration more difficult. This is readily demonstrated by forcing a pencil or similar object through the hub of webs with and without such stabilimenta.



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19751
filbert -Avoidance Behavior in Orb Weavers Figure 1.
/Srginfe aurantia and its stabilimentum. Note light color of
spider.




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36 Psyche [March
All descriptions of predator avoidance components apply equally to A. aurantia and A. trifasciata. There are differences in relative usage of these components (discussed in next section) and their com- bination in behavioral sequences.
Web Flexing
Web flexing is accomplished when the spider sets the web in motion along its short axis by rapid extension and retraction of the legs. Spider and web thus swing back and forth parallel to the ground surface, since the long axis of the web is oriented more or less per- pendicular with respect to the ground. Web flexing adds another dimension to the predator's attempt at attack, that of motion. Ob- viously, contact is more difficult to establish and maintain when the spider and web are in motion. In one encounter of a salticid and an Figure 2.
Juvenile A, trifasciata with barrier webs. Note primary bar- rier behind dorsum of the spicier; ariow is pointing to 'ipider's dursum.



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19751 Tolhert - Avoidance Behavior in Orb Weavers 37 A. aurantia, the salticid lost its grip on th,e Argiope's web and body (?) after web flexing was commenced; the salticid (a juvenile P. audax) fell onto the sticky spirals of the orb weaver's web where it became entangled and was treated as a prey item (i.e. wrapped, bitten and fed upon). Web flexing might also distract the potential predator and temporarily conceal the exact location of the orb weaver. Stilting
Stilting results when the spider straightens all four pairs of legs and thus moves the sternum and venter 'further away from the hub surface (fig. 3). The abdomen is often tilted dorsally as well ; the spider when viewed from the ventral side appears smaller because of the reduced surface area exposed.
This response might also change
the sign stimulus to a shape the predator does not readily recognize (Riechert, personal comm.), but additional testing will be required before this is known.
Dropping from web
Dropping or jumping from the web rar'ely occurred in the testing. During the trials it was never followed by leaving the web site though I have observed this behavior in certain field situations. When a web is approached rapidly and it or the vegetation to which it is attached is severely disturbed, the spider may jump from the web and actively leave the site. When dropping or jumping from the web did occur under test situations and when it was normally observed in the field, a dragline was secured to the hub before the spider dropped into the vegetation. Spiders then took up a position underneath a blade of grass, a leaf or along a plant stem where they remained for periods of less than one minute to over an hour (A. aurantia N = 6, 2 time = 3 min. 02 seconds; A. trifasciata N 35,. 2 time = 3 min. 11 seconds). Return to the hub was always via a direct, rapid climb up the dragline to the hub where a head-down position was assumed. If the vegetation near the spider or the spider itself was touched it immediately went back to the hub. Leaving the web is certainly an escape response and hiding undern'eath the vegetation is probably best applied against visual predators. Rapid return to the hub, especially when the vegetation is lightly disturbed, would facilitate escape if the predator was no longer in visual con- tact. Returning directly to the hub immediately places the spider at the center rtf its web. This may be advantageous since the orb weaver is back at the center of its auxiliary information gathering system, the web, and because most predator avoidance options are available at the hub.




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I
Figme 3. Argiope trifasrwia stilting. Note extension of legs and dig- tance of body away from huh surface.




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19751
Tolbert~ Avoidance Behavior in Orb Weavers Switching sides of the web
Switching sides of the web is accomplished when the spider moves between the radii in th,e "free zone" to the other side of the hub. It may be followed by web flexing, stilting, or web flexing later fol- lowed by stilting (fig. 4B). This response results in the interposition of the web as a physical barrier between the orb weaver and a po- tential predator.
Moving away from hub
When moving away from the hub the spider moves directly away from the point of contact : when its eye region is touched, the spider moves up the web and if the abdomen is touched, it moves down the web. Although one component was often immediately followed by another in a single response sequence, individual components were usually easy to identify. One exception is when the spider leaves the hub while simultaneously flexing the web; it is often impossible to tell which is the initial response. In statistical analyses and graphic ,
presentations (figs. 4, 5 and 6) web flexing is treated as the initial ,
response.
This particular behavioral sequence is unusual in another way. Generally web flexing was initiated by rapid spider movement which resulted in considerable web movement and a large amplitude of web displacement. The response gradually subsided with web amplitude decreasing as web and spider movement slowed. In the
hub leaving-web flexing sequence, however, the spider sometimes slowly returned to the hub while web flexing continued. Upon reach- ing the hub or shortly thereafter all motion quickly ceased. An ob- server has to watch closely to detect spider movement toward the hub; this behavior probably serves to distract the predator and then hide the orb weaver.
Rebuff
Rebuff, as used here, should not be confused with elements of the predatory behavior of these species (see Harwood, 1974). It is here defined as actively repulsing (pushing away) the model by using any of the legs of pairs I or I1 and/or briefly grasping the model with these legs. Biting was never observed although chelicerae were sometimes opened and fangs exposed. This may be an intention movement and/or threat posture.
Body flatten
In a few instances when spiders were approached dorsally, they would simply depress their bodies away from the model and flatten against the hub.




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Figure 4A. Arg'iope aurantia behavioral components elicited by presentation of predator model: Ventral ap- proach. [Note: in figures 4, 5 and 6 the width of the arrows is proportional to frequency of response; scale line = 20%.]




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Tolbert -Avoidance Behavior in Orb Weavers 4 1.




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Tolbert -Avoidance Behavior in Orb Weavers



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Figure 6.
A. trifasciata behavioral components elicited by ventral presentation of predator model.



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19751 Tolbert -Avoidance Behavior in Orb Weavers 45 At times no response was observed even with repeated presentation of the model.
Any insect or arachnid that approaches an orb web falls into one of four categories: (I) potential prey, (2) potential predator or parasite, ( 3 ) potential mate and (4) "neutral" (unpalatable prey, too large or strong an animal for the spider to subdue, etc.). An orb weaver that responds incorrectly may fail to obtain sufficient