1995. The Journal of Arachnology 23 :1—8

PHILOPONELLA REPUBLICANA (ARANEAE, ULOBORIDAE) AS A COMMENSAL IN THE WEBS OF OTHER S

Ann L. Rypstra and Greta J . Binford : Department of Zoology, Miami University , 1601 Peck Blvd., Hamilton, Ohio 45011 USA

ABSTRACT. Juvenile individuals of the spider species, republicana, were common in the web s of the social spider, Anelosimus eximius, and the solitary spider, Architis sp., in the forest habitats of the SE Peru. The abundance, size and location of P. republicana individuals were surveyed in each host web . Although the host webs were similar in size and conformation, more P. republicana individuals were found in the social spider webs than in the solitary host webs. Likewise, the number of P. republican in the social spider webs was correlated with host web size . The mean size of prey captured by P . republicana was 2.1 mm, which was significantly smaller than the prey taken by the social spider, and, in feeding trials, Architis sp. individuals reacted only infrequently to prey of that size . This separation in the size of prey taken caused us to conclude that P. republicana acted as a commensal for the most part; however, they were observed to prey on the social occasionally. Small P . republicana were the most common in both host webs and tended to be high i n the barrier webbing. The largest individuals in the social host webs were located under the sheet area, and thes e individuals were observed to feed more frequently than spiders in other size classes and in other areas of th e host webs. We conclude that juvenile P. republicana are commensals in both host webs but that they benefit more from the greater amount of activity in webs of the social spiders.

Mounting evidence from phylogenetically di - teract with the host in both positive and negativ e verse species shows that grouping behavior ma y ways (Rypstra 1979; Bradoo 1989 ; Cangialosi simultaneously reduce individual risk of preda- 1991 ; Hodge & Uetz 1992). tion and enhance feeding efficiency (Pulliam & A commensal association occurs when on e Caraco 1984 ; Uetz 1988; Uetz & Heiber 1994) . species reaps some benefits by association wit h Heterospecific interactions within social group s a host species but the host species is essentiall y can bring advantages to individuals in thos e unaffected, positively or negatively, by the as- groups that do not accrue to individuals in singl e sociation. Commensalism has been reported with species aggregations (Morse 1970 ; Barnard & some frequency among spider species in the fam - Thompson 1985) . Slightly different foraging ily Uloboridae (Struhsaker 1969 ; Opell 1979 ; modes and food preferences may lead to more Bradoo 1986 ; 1989). Bradoo (1989) conclude s efficient resource usage by mixed species group s that ferokus Bradoo (Araneae, Ulobor- which can simultaneously take advantage of oth- idae), living in the webs of the social spider Ste- er kinds of advantages of being in a group . godyphus sarasinorum Karsch (Araneae, Erisi- A wide variety of heterospecific relationship s dae), receives protection, support and increase d have been reported among spider species rangin g prey capture which increases its lifespan and fit- from predation (Larcher & Wise 1985 ; Jackson ness. The spider species, Philoponella republi- & Whitehouse 1986 ; Jackson 1990) to klepto- cana (Simon) (Araneae, Uloboridae), is frequent - parasitism (Vollrath 1987 ; Cangialosi 1990), t o ly found in single species aggregations (Smith commensalism (Rypstra 1979 ; Bradoo 1986 , 1985; Binford & Rypstra 1992); but, in addition , 1989). In many of these instances, host spider s we have found immature individuals of the spe- have large complex webs that can provide a liv- cies in the interstices of the webs of almost al l ing space with some support and protection for complex, semi-permanent spider webs at ou r the second spider species (Rypstra 1979 ; Bradoo study area in SE Peru . P . republicana were par- 1986, 1989; Hodge & Uetz 1992) . In particular, ticularly common in the webs ofAnelosimus ex- the webs of communal or social spiders tend to imius Simon (Araneae, Theridiidae), a cooper- provide habitat for other spider species who in- atively social species in this area. The goal of this

Present address: Dept, of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 8572 1 USA 1

THE JOURNAL OF ARACHNOLOGY

study is to describe the abundance and distri- within the host web, we also attempted to de- bution of P. republicana in the large webs of this termine the feeding frequency of P. republicana social spider in comparison with its distributio n spiders located in different positions. A spherical in the webs of a solitary species, Architis sp. (Ara- bundle in the chelicerae of the spider was evi- neae, Pisauridae), whose web is of similar siz e dence that it had captured a prey item recently . and structure (Nentwig 1985) . One complication that arises in determining th e likelihood of feeding is that the spider will feed METHODS longer on large prey than on small prey so a Data were collected on spider populations in- survey sampling technique would have biased habiting the subtropical moist forest of the Tam- the results toward large prey. In the case of A. bopata Reserved Zone, 35 km southwest of Puer- eximius webs, we typically spent two or more to Maldonado in Madre de Dios, Peru . Data were hours observing so, for this study, we only count- collected in the dry season : July and early August ed the prey items that were captured during ou r of 1987, 1988 and 1989 (see Erwin 1985 for observation times. For Architis webs, we sur- complete description of the habitats) , veyed a second time 2-3 hours after the first The webs of both host spiders were very sim- observation to estimate a feeding rate in a simila r ilar in overall appearance. They consisted of a fashion. dense sheet of webbing subtended by a maze o f To determine whether the two species were barrier webbing encompassing neighboring veg- actively competing for prey that entered the we b etation (Brach 1975 ; Christenson 1984; Nentwig or if there was a division of resources based on 1985). A. eximius is a cooperatively social species prey size, we needed to determine the range of so each web contained several hundred to several prey sizes taken by each of the host species . The thousand individuals that worked together to distribution and frequency of prey capture were capture prey (Brach 1975; Christenson 1984). obtained for A. eximius in the course of a si- Architis sp. is a solitary spider and a single in- multaneous study (Rypstra 1990 ; Rypstra & Tr- dividual monitors insects arriving in the web from ey 1991). In order to determine whether the sol- a funnel-shaped retreat at one end of the shee t itary Architis sp. actively preys on insects in th e area of the web (Nentwig 1985). Adults of A. size class that P. republicana handles, we con- eximius are 4-6 mm in length, which is substan- ducted a feeding experiment. Field-caught fruit tially smaller than Architis adults which are 8- flies (Drosophila spp. 1.5-2.0 mm in length, th e 12 mm in length. mean size of prey taken by P. republicana) were Surveys were conducted of all A . eximius webs gently blown into each of ten webs of Architis. found, a total of 46 webs, between 4 July and 4 In all cases the Architis individual was at the August in 1987 (18 webs), 1988 (16 webs) an d opening of its retreat in a feeding position at the 1989 (12 webs) . To avoid the confounding factor time the prey were introduced. If the Architis of repeated measures only one survey per socia l spider retreated before the prey was in the we b was included in the data set . In order or if it was apparent that we had disturbed her to standardize for season and temperature acros s in the process, no data were taken. If we suc- the years we selected the first survey conducte d cessfully introduced the fly without disturbin g on a web after 4 July on a dry day on which the the host spider and we were able to detect that temperature was between 24-28 °C. A total of the fly contacted the sheet in a way sufficient to 12 Architis sp. webs were surveyed a single tim e vibrate the threads, we recorded the reactions o f and under similar weather circumstances in July the Architis. Between 8-42 flies were tested in of 1989. During each survey, P. republicana were each often Architis webs. After each trial, a large r classified into three size categories : large (4-6 fly or grasshopper was introduced into the web mm in length), medium (2-4 mm in length), and to see if the host spider was receptive to any prey . small (less than 2 mm in length). P. republicana If we could not get the spider to respond, the were also categorized by position in the host web . results of the trial were excluded from the anal- That categorization included spiders located un- ysis. der the sheet, just above the sheet (within 2 cm) , in the low barrier of the web (2-20 cm above the RESULTS sheet) and in the high barrier (20 cm or more All of the webs that we found in all three year s above the sheet). had some P. republicana in them. On average, In order to obtain one measure of site quality there were 8 .4 ±3.3 (mean ± standard deviation)

RYPSTRA BINFORD—SPIDER COMMENSAL S 3

20

15

0 1987 • 1988 1989 ARCHITIS

0 50 100 150 20 0 WEB DIMENSION (CM) Figure 1 .—The number of commensal Philoponella republicans individuals vs . the longest horizontal dimen- sion of the host web . Data points indicated for the three years (1987, 1988, and 1989) are all for the social host, Anelosimus eximius . Data for the solitary host, Architis sp ., were all gathered in 1989 . The correlation between web size and number of commensals is significant for the social Anelosimus eximius but is not significant for the solitary Architis sp.

P. republicana individuals in the 46 A . eximius The distribution of P. republicana individuals webs we surveyed over three years . There were in the various size classes we identified was not no differences among the years (Kruskal-Walli s even within either host web (x2 Test, P < 0.05). Multiple Comparisons, P > 0 .05). There were In both web types, small spiders were most abun- significant positive relationships between social dant and large spiders the least abundant (Fig. spider web size and the number ofP. republicana 2).The size distributions of P. republicana in the in the web both within each year and when the two host types were significantly different from data for all years were pooled. The strongest re- one another (x2 Test, P < 0.05). Most noticeably , lationship was between the longest horizontal di- there were more large individuals in A . eximius mension and number of spiders (for all years webs than there were in the webs ofArchitis together: Spearman's r = 0 .85, P < 0,05) (Fig. (Fig, 2). The distribution of P. republicana webs 1). across the four positions we identified in the host We found a mean of 4.17 ± 2.6 P. republicana webs was also skewed (x2 Test, P < 0 .05). In individuals in the 12 webs of Architis sp . that we Architissp. webs, most of' the P, republicana (40 surveyed in 1989 . This was significantlyless than of 63 total) were located in the barrier area (Fig. the numbers we found in the social spider webs 3). However, in A. eximius webs, P. republicana (Mann-Whitney U-Test, P < 0 .05). The webs of were evenly distributed between areas close to Architis and A. eximius were similar in all th e the sheet and barrier areas (Fig. 3). Specifically, dimensions we measured : longest horizontal, the P. republicana in the social spider webs were perpendicular or web height, and height of the most abundant under the sheet and in the high sheet above ;ground (Mann-Whitney U-Test for bather; and they were least abundant just above all, P > 0.25). However, there was no relation- the sheet arid in the low barrier (Fig . 3). The ship between web size and number of P. repub- distributions of P. republicana webs in the two licana individuals in Architis sp. webs (longest host species we observed in 1989 were signifi- horizontal web dimension and spider number : r cantly different from one another (x2 Test, P < 0.4, .P > 0.2) (Fig. 1). 0.05).

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m 80 W

N 60 - 0 S - z 40 - ARCH/TIS F- - A. EX/ANUS z V 20 cc w

SMALL MEDIUM LARGE SIZ E Figure 2 .—The size distribution of Philoponella republicana individuals in the webs of the two host species , Architis sp. and Anelosimus eximus . "Small" spiders were all less than 2 mm in length; "Medium" spiders ranged from 2—4 mm in length, and "Large" spiders were between 4—6 mm in length .

We had sufficient data to look specifically a t 5 of the 63 spiders censused in Architis sp . webs the distribution of the different size classes and captured prey, and all of those were spiders in their feeding frequencies for P. republicana in the the large size category located in the barrier web- social spider webs. Small P. republicana were bing. abundant in the high barrier but a very few were The prey captured by P. republicana in these located just above the sheet (Fig . 4). Only 15 of host webs was 2 .1 ± 1 .2 mm in length which is the 172 small spiders we censused captured any much smaller than the mean prey size capture d prey item and fed during our observations, and by A. eximius (5.9 ± 2.1 mm) (Mann-Whitne y the distribution of those individuals was not sig- U-Test, P < 0.05) (Rypstra 1990) . In our prey nificantly different from the distribution of all introduction trials with Architis sp., spiders re - small spiders within the host webs (x2 Test, P > acted to only 17 of the 112 insects in this siz e 0.3) (Fig. 4). Medium-sized P. republicana were class that we introduced into 10 different webs evenly distributed across the positions within th e and the fruit flies were captured on only six oc- social spider webs (x2 Test, P > 0.3); however, casions. In most of the introductions, the Architis those located close to the sheet were more likel y web resident did not move at all when the pre y to be observed feeding than those in the barrie r were introduced but then would respond to th e areas (25 of the 30 spiders that captured prey) larger prey item at the end of the trial . (Fig. 4). Forty-seven of the 77 large spiders we The cribellar silk of the P. republicana was able observed were located under the sheet of the hos t to detain A. eximius quite effectively if they hap - web so the distribution of individuals in this siz e pened into one of the webs. On three occasions , class was not even across the positions (x2 Test, a P. republicana individual, located in the bar- P < 0.05) (Fig. 4). Twenty-four of the 77 large rier, successfully captured and killed a penulti- spiders we censused fed during our observations mate or adult A. eximius female. In no case did and 80% of those were located under the shee t we observe A. eximius capture a P. republicana . (x2 Test, P < 0.05) (Fig. 4) . At dusk, A. eximius has a period of web cleaning Our sample size of P. republicana in Architis and maintenance; and, at that time, they woul d sp. webs was not large enough to make the com- cut out and remove many of the webs of P . re- parisons of position, size and feeding that we publicana that were located above the sheet an d were able to make in the social spider host . Only in the barrier webbing. When they did this, the

RYPSTRA BINFORD—SPIDER COMMENSALS 5

40 - ARCHITIS A. EXIMIUS

UNDER ABOVE LOW HIG H POSITIO N Figure 3. —The distribution of Philoponella republicana in the various positions in the host webs. The identified positions were "Under" the sheet, just "Above" the sheet (within 2 cm), in the "Low" barrier webbing (betwee n 2—20 cm above the sheet) and in the "High" barrier (greater than 20 cm above the sheet) .

P. republicana would evacuate their web and hang we observed between P. republicana and A. ex- motionless near the location . In only one in - imius. stance did we observe A . eximius destroying a P. There are more commensals located in the so- republicana web located below the sheet durin g cial spider webs than in the solitary spider's web . this activity. Likewise, as the social spider web becomes large r more potential web sites are formed and more P. republicana colonize them resulting in a cor- DISCUSSION relation between their number and web size . Our observations suggest that P. republicana However, even though more web sites would is a commensal in the webs of A. eximius and presumably be available as the Architis webs in- Architis sp. since they capture prey much smaller creased in size as well, no additional commensa l than those captured by the host species. They spiders colonized them . We suspect that the in- appear to use the webs of other species as sup - creased activity in the social webs deflects more port, perhaps to enable them to locate their small prey into the commensal's webs, which woul d orb webs in areas otherwise unavailable to them . make those sites preferable . Unfortunately, prey It is also possible that the webs of the host species capture by P. republicana in Architis sp. webs enlarge the effective size of their own web allow - was sufficiently uncommon in our observations ing them to detect insects sooner and at a greater that we cannot verify that difference statistically . distance . Perhaps there is some ricochet effect a s The fact that there were more large individual s small insects are deflected and detained by strand s in the social spider webs suggests that they feed of the large host web which could increase the more successfully there . In addition, the fact that rate of capture by the commensal spider (Uetz they are occasional predators on the host in th e 1989) . Bradoo (1986) observed U. ferokus mov- social spider's web indicates that more potential ing out of their orbs to capture prey on the surfac e food is available there . of the host web but we never observed this sort On the other hand, the density of commensal s of behavior by P. republicana. Bradoo's (1986 ) in the webs of the social spider may not be related descriptions suggest that the relationship be- to prey capture at all . At some point in the evo- tween that commensal and its social spider hos t lution of sociality, spiders must become more is much more interdependent than that which tolerant of other spiders (Kullmann 1972 ; Wil-

6 THE JOURNAL OF ARACHNOLOGY

SMALL SPIDERS

W/ PREY NO PREY

UNDER ABOVE LOW HIGH POSITIO N

MEDIUM SPIDERS

W/ PREY U NO PREY 011FAICK02

,''AWAIM111F,11F.W

UNDER ABOVE LOW HIGH POSITIO N

LARGE SPIDERS

12] WI PREY NOPREY P.M

UNDER ABOVE LOW HIGH POSITION Figure 4 .-The distribution of various size classes in the various positions in the social spider webs and th e proportion of individuals which were observed to capture prey within a three-hour time period.

RYPSTRA & BINFORD—SPIDER COMMENSALS 7

son 1975) . It may be that A . eximius webs are for U. ferokus which suggests that there is a con- easier to colonize because of this factor . The so- tinuum of dependence on other spider species cial spider regularly associates with lots of othe r within the family Uloboridae . It is important to spiders and therefore must have relaxed its ag- conduct more detailed studies of these relation - gressive tendencies toward them, whereas the ships in order to understand more fully the evo- solitary species can afford to rid aggressively its lution of these various behavior patterns. web of all other spiders indiscriminately except during the restricted circumstances when it i s ACKNOWLEDGMENTS being courted by a male . The fact that the social thank K. Cangialosi, A . McCrate, S. Tirey, species is predisposed to tolerate other spider s We J. Whitis and the staff of the Explorer's Inn for may mean that it is easier for heterospecifie re - . We are grateful for th e lationships to perpetuate in their company . assistance in the field cooperation of the staff at the Ministerio de Agri- Locations under the sheet in the social spider' s cultura de Peru in issuing authorization to work webs seem to attract the largest P. republicana, with the spiders of Tambopata . Voucher speci- and those locations also seem to be the areas of mens were placed at the Museo de Historia Nat- highest prey capture (Fig. 4). It could be . that ural, Lima, Peru and at the Smithsonian Insti- juveniles that happen to select web sites in that tution, Washington, D. C. M. A. Hodge and G. location capture more prey and thereby grow large W. Uetz made many useful suggestions on a n more quickly and/or remain longer in the host earlier draft of this manuscript. Financial sup- web that those in other areas . It is also possible f that, as the spiders grow, they are more able t port for this research came from the Society o o Sigma Xi, the Frizzell-Exline Fund for Arach- compete for these high quality sites. Our data nological Research, a Miami University Under - suggest that sites under the sheet afforded bot h graduate Research Award (all to G . J. B.) and an higher prey capture rates and more protection NSF grant BSR86-04782 (to A. L. R.). from disturbance in the host webs of the socia l spider. One disadvantage to these sites may be LITERATURE CITE D that P . republicana that located there would en - Barnard, C. J. & D. B. A. Thompson. 1985. Gulls counter fewer of the social spider individuals an d and Plovers: the Ecology and Behaviour of Mixed- therefore be less successful as a predator . Species Feeding Groups. Columbia Univ. Press, New It is curious to note that we never found a n York, New York . adult in the interstices of these complex host Binford, G. J. & A. L. Rypstra. 1992. Foraging be- webs, even though adults were present in at th e havior of the communal spider, Philoponella re- study site at the time these data were collected. publicana (Araneae: Uloboridae) . J. Ins. Behay., Interestingly, in our study area we found adult s 5:321-335 . only in aggregations composed exclusively of P . Brach, V. 1975 . The biology of the social spider Ane- republicana individuals. Lubin (1980) suggested losimus eximius (Araneae, Theridiidae) . Bull. So. that the single species aggregations of P. repub- California Acad . Sci., 74:37-41. licana were sibling groups arising from a single Bradoo, B. L. 1986. Feeding behaviour of a non- poisonous spider Uloborus ferokus Bradoo (Arane - egg case, and our surveys of P. republicana col- ae: Uloboridae) . Zool. Anz., 217:75-88. onies over the years support that idea (unpub. Bradoo, B. L. 1989. Advantages of commensalism data). However, we have also observed that a in Uloborus ferokus Bradoo (Araneae : Uloboridae). large number of juveniles are commensals fo r J. Bombay Nat. Hist. Soc., 86:232-328. some portion of their life. If this commensal state Cangialosi, K. R. 1990. Kleptoparasitism in colonies is a phase that many juveniles pass through, then of the social spider Anelosimus exirnius (Ar it would be interesting to discover what cues the y Theridiidae) . Acta Zool . Fennica, 190:51-54. use to reaggregate with conspecifics in this com- Cangialosi, K. R. 1991 . Attack strategies of a spider plicated habitat. Nyffleler & Benz (1980) report kleptoparasite: effects of prey availability and host colony size. Anim. Behay., 41 :639-647 . that juvenile stages of several other species o f Behaviour of colonial an orb weavers act as kleptoparasites and commen- Christenson, T. E. 1984. d solitary spiders of the theridiid species Anelosimus sals in the webs of other spiders . They consider eximius. Anim. Behay., 32:725-734 . the commensal relationship as a transition to a Erwin, T. L. 1984. Tambopata Reserved Zone, Ma- more invasive kleptoparasitism . We have al- dre de Dios, Peru: history and description ready mentioned the more active prey captur e reserve. Rev. Peruana Ent ., 27:1-8. out of the host web that Bradoo (1986) reports Hodge, M . A. & G. W. Uetz. 1992. Antipredator

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benefits of single- and mixed-species grouping by ed. (J. R. Krebs N. B. Davies, eds .). Sinauer As- Nephila clavipes (L.) (Araneae, Tetragnathidae) . J. sociates, Sunderland, Massachusetts . Arachnol ., 20:212—216. Rypstra, A. L. 1979. Foraging flocks of spiders : a Jackson, R. R. 1990. Predator-prey interactions be- study of aggregate behavior in Cyrtophora citricola tween jumping spiders (Araneae, Salticidae) and Forskal (Araneae: Araneidae) in west Africa . Behay. Pholcus phalangioides (Araneae, Pholcidae) . J. Zool., Ecol. Sociobiol., 5:291—300 . London, 220:553—559. Rypstra, A. L. 1990. Prey capture and feeding effi- Jackson, R. R. M. E. A. Whitehouse . 1986. The ciency of social and solitary spiders : a comparison. biology of New Zealand and Queensland pirate spi- Acta Zool . Fennica, 190:339—343 . ders (Araneae, Mimetidae): aggressive mimicry, ar- Rypstra, A . L. R. S. Tirey. 1991. Prey size, prey aneophagy and prey specialization . J. Zool., Londo n perishability and group foraging in a social spider . (A), 210:279-303. Oecologia, 86 :25—30 . Kullmann, E. J. 1972. Evolution of social behavior Smith, D. R. R. 1985. Habitat use by colonies of in spiders (Araneae ; Eresidae and Theridiidae) . Philoponella republicana (Araneae, Uloboridae). J. American Zool ., 12:419—426 Arachnol., 13:363—373. Larcher, S. R. D. H. Wise. 1985. Experimental Struhsaker, T . T. 1969. Notes on the spiders Uloborus studies of the interactions between a web-invadin g mundiorand Nephila clavipes in Panama . American spider and two host species . J. Arachnol., 13:43—59. Midl. Nat., 82:611—613. Lubin, Y. D. 1980. Population studies of two colonia l Uetz, G. W. 1988. Risk sensitivity and foraging in orb-weaving spiders . Zool. J. Linn. Soc., 70:265— colonial spiders. Pp. 353-377, In The Ecology of 287. Social Behavior. (C. N. Slobodchikoff, ed .), Aca- Morse, D. H. 1970. Ecological aspects of some mixed- demic Press, San Diego, California . species foraging flocks of birds . Ecol. Monogr., 40: Uetz, G . W. 1989. The "ricochet effect" and prey 119—168. capture in colonial spiders. Oecologia, 81 :154—159. Nentwig, W. 1985 . Architis nitidopilosa as a neo- Uetz, G. W. C. S. Heiber. 1994. Group size and tropical pisaurid with a permanent catching web. predation risk in colonial web-building spiders : Bull. British Arachnol . Soc., 6:297—303. analysis of attack abatement mechanisms . Behay. Nyffeler, M . G. Benz. 1980. Kleptoparasitismus Ecol., 5:326—332. con juvenilen Kreuzspinnen and Skorpionsfliegen Vollrath, F. 1987 . Kleptobiosis in spiders. Pp. 274— in den Netzen adulter Spinnen. Rev. Suisse Zool., 286, In Ecophysiology of Spiders . (W. Nentwig, ed.) 87:907-918 . Springer-Verlag, Berlin . Opell, B. P. 1979. Revision of the genera of tropical Wilson, E. O. 1975. Sociobiology — The new synthe- American species of the spider family Uloboridae . sis. Harvard Univ . Press, Cambridge, Massachu- Bull. Mus. Comp . Zool., 148 :443—549 . setts. 697 pp. Pulliam, H. R., T. Caraco. 1984. Living in groups: Is there an optimal group size? Pp. 122-147, In Be- Manuscript received 26 November 1994, revised 1 De- havioural Ecology: An Evolutionary Approach . 2nd cember 1994 .