BehavioralEcology Behav Ecol Sociobiol (1987) 21:401-406 and Sociobiology ? Springer-Verlag1987 Host location and exploitation by the cleptoparasiticwasp Argochrysis armilla: the role of learning(Hymenoptera: Chrysididae) Jay A. Rosenheim Departmentof Entomological Sciences, University of California, Berkeley,CA 94720, USA Received May 27, 1987 / Accepted August 31, 1987 Summary. The nesting behaviors of many solitary (Evans 1977); but it is also significant in temporal- ground-nesting wasps incorporate temporal bar- ly separating the stage of the nesting cycle that riers against would-be cleptoparasites. Nests being is most conspicuous to parasites, nest digging, excavated are conspicuous but relatively invulner- from the stage that is most vulnerable to exploita- able to parasites, while nests being provisioned, tion, nest provisioning (Rosenheim 1987a). In this often several hours to days later, are inconspicuous way host behavior challenged potential cleptopara- but highly vulnerable. Argochrysisarmilla, a clep- sites to bridge the temporal gap between nest exca- toparasite of solitary ground-nesting wasps, Am- vation and nest provisioning. Here I present exper- mophila spp., bridges the temporal gap between imental results for one cleptoparasite, Argochrysis nest excavation and provisioning by (i) visually lo- armilla Bohart (Hymenoptera: Chrysididae), that cating digging hosts, (ii) learning the locations of has adapted to this temporal gap; Argochrysisar- associated nests, (iii) maintaining surveillance on milla (i) orients visually to digging hosts, (ii) learns a series of nests during the hosts' absence, and the locations of associated nests, (iii) attends a se- (iv) ovipositing in nests when the host returnswith ries (or "trapline") of nests for up to several days provisions. Patterns of surveillanceand parasitism while the host hunts for provisions, and (iv) suc- of Ammophiladysmica nests were generated by the cessfully oviposits in attended nests during nest number of cleptoparasitesdiscovering and learning provisioning. Observations of a nesting aggrega- the nest's location during excavation. These results tion of Ammophiladysmica Menke (Hymenoptera: support recent suggestions that learning may play Sphecidae) revealed the significance of the learned an important role in shaping foraging strategies foraging strategy in generatingpatterns of nest sur- of insect parasites. veillance and parasitism. This study is the first demonstrating a strategy of host exploitation based upon locality learning by an insect parasite and supports recent suggestions of the importance of in insect and Rausher Introduction learning foraging (Papaj 1983; Gould 1985, 1986; Menzel 1985; Lewis Early comparative ethologists used landmark dis- 1986; Papaj 1986; Jermy 1986). placement techniques to establish the ability of sol- the of itary digger wasps to learn "topography" Methods their nest-site and thereby relocate previously con- structed nests (van Iersel 1975). Locality learning Argochrysisarmilla was studied from 1982-1986 at Sagehen Creek Field Nevada where enabled to change Station, County, California, USA, solitary ground-nesting wasps it developed as a cleptoparasitein the nests of solitary ground- their nesting behavior from the primitive prey-nest nesting wasps of the genus Ammophila.The study site was lo- sequence, in which the nest is excavated after the cated on a broad ridgetop, elevation 2000 m, where Ammophila provisions are collected, to the more advanced spp. nested in several aggregations along a dirt road. Ammo- nests with one to several nest-prey sequence, in which the frequentlylengthy phila provision unicellular lepidop- after the nest is teran larvae, and both species discussed here, Ammophiladys- hunting process begins dug (Evans mica and Ammophilaazteca Cameron, exhibited nest-prey be- 1958). This reordering avoids the risk of theft or havior patterns.Argochrysis armilla achieved annual parasitism parasitism of the provisions during nest excavation rates of 21.3-43.5% in nests of Ammophiladysmica, despite This content downloaded from 128.120.194.195 on Tue, 23 Sep 2014 01:53:03 AM All use subject to JSTOR Terms and Conditions 402 the fact that nest provisioning occurred an average of host's absence. Observationsmade before this experimenthad 10.4 + 8.5 h after nest excavation (n = 128) (Rosenheim 1987a). indicated that only parasites that had discovered a nest during No other parasites achieved parasitism rates in excess of 4%. excavationwere able to reorientto the nest in the host's absence For a more detailed descriptionof the site, the nesting behavior (see below). Ammophilaazteca initiating nest excavations were of Ammophiladysmica, and interactionsof Ammophiladysmica surroundedby four artificiallandmarks (white plastic LEGO? with Argochrysisarmilla see Rosenheim (1987a). blocks, 32 x 16 x 19 mm with eight small cylindrical knobs on the upper surface) each placed 3 cm from the nest entrance in a Parasite surveillance host nests square array. These landmarksremained in place for the of duration of the digging. The presence and identity of marked The abundance of Argochrysisarmilla attending Ammophila Argochrysisarmilla as well as the presence of unmarkedpara- dysmica nests was assessed during three stages of the nesting sites attracted to the nest were recorded. Parasite identity was cycle by scoring the maximum number of parasites present si- recorded as a means of (i) distinguishing between initial and multaneouslyat any time during the samplingperiod. Parasites subsequentvisits and (ii) increasingthe replicatenumber, since were consideredto be in attendenceif they landed on or hovered only the first return of an unmarkedparasite could be scored directly above the nest entrance, or if they perched at least as an initial return, and all subsequentvisits by any unmarked twice sequentially facing the nest entrance from a distance of parasites had to be lumped in the total visits column. At the less than 30 cm. The period of nest digging was monitored conclusion of the nest excavationthe host and parasitesgeneral- to yield the first sample; nest digging required an average of ly departed. If all Argochrysisarmilla had not departed within 63.5 + 35.6 minutes (n = 102). During the absence of the hunting ten minutes, those remainingwere flushed from the nest. Two wasp, 3-min nest surveys were performed hourly during the false nests, each consisting of a short vertical tunnel provided period of high parasite activity, 1100-1600 h. These surveys with a single loose-fitting pebble closure similar to that of Am- were made for five days after nest excavation or one day after mophilaazteca, were then constructed6 cm from, and on oppo- the completion of nest provisioning, whichever occurred first. site sides of, the true nest. The artificial landmarkswere then Finally, parasite abundance was monitored during the period removed. A coin flip determinedwhich of the two false nests of the nest's greatest vulnerability,when the nest closure had would be surrounded by an identical array of clean artificial been removed by the host wasp to deposit the caterpillarpro- landmarks. During the following hour, or until the return of vision, oviposit, clean the nest, and find a pebble with which the host, returnsof Argochrysisarmilla to membersof the nest to re-plug the nest. The duration of this period averaged array were scored when parasites hovered directly over or 185.7+ 130.3 s (n= 50). Because Argochrysisarmilla quit the landed on a nest. The scoring method was chosen because it nest-site after ovipositing in a host nest, the parasiteabundance was unambiguous and avoided the possibility of false positive score during provisioning was slightly modified: if the maxi- scores associated with attraction to the LEGO? blocks inde- mum number of parasitessimultaneously present was observed pendent of their role as landmarks. Twelve trials were con- after n parasites had oviposited and departed, the score was ducted from 1 July 1986 to 14 July 1986. increasedby n. At the end of the nesting season all Ammophiladysmica nests were excavated and scored as parasitized (Argochrysis Results armilla cocoon(s) present) or unparasitized(host cocoon pres- ent); nests whose contents were destroyed by mold or other Host Location parasitesor predatorswere not included in the analysis. A sample of Argochrysisarmilla was marked individually The manipulated Ammophilalure employed in the with enamel paints spotted onto the thoracic dorsum (n =47). attraction experiment increased both the number The identity of these individuals could be determinedwithout disturbancein the field. of Argochrysis armilla and the duration of their stay in the experimental plots (Table 1). Parasites Host location were observed to reposition themselves on their perches to continue facing the moving lure. Ar- Digging Ammophiladysmica were rapidly discovered by Ar- armilla within the gochrysis armilla, most nests being attended by one or more gochrysis searching nesting ag- parasiteswithin the first 10 min of digging (Rosenheim 1987b). gregation detected the moving lure only if they To determine if parasites were using visual cues to orient to were perched nearby (maximum distance of detec- digging wasps, an artificial Ammophilalure was employed in tion appeared to be ca. 0.5 m) and were facing an attraction experiment.The lure consisted of a dead female towards the lure. Parasites in approximately moving Ammophilaazteca sealed a coat of clear nail polish and sus- the lure