The Ecology of Inquilinism in Communally Parasitic Tamalia Aphids (Hemiptera: Aphididae)

Home , Anthocoris whitei, Arctostaphylos patula, Arctostaphylos viscida, Colophina clematis, Inquiline, Polistes sulcifer

ECOLOGY AND POPULATION BIOLOGY The Ecology of Inquilinism in Communally Parasitic Tamalia Aphids (Hemiptera: Aphididae)

DONALD G. MILLER III1

Department of Biological Sciences, California State University, Chico, CA 95929Ð0515

Ann. Entomol. Soc. Am. 97(6): 1233Ð1241 (2004) ABSTRACT I report the Þrst example of communal parasitism in galling aphids and quantify the effects of gall invasion by the inquiline aphid Tamalia inquilina Miller on its host, Tamalia coweni (Cockerell). On populations of the host plants Arctostaphylos spp., both T. coweni and T. inquilina exhibited facultatively communal behavior and co-occupied galls with no apparent agonistic interactions. Although total reproductive output of adult offspring was similar between galls containing T. coweni alone and galls with both species, the allocation of brood was skewed toward that of the inquiline; hence, T. inquilina is a parasite of T. coweni. The presence of T. inquilina had no signiÞcant effect on survivorship of T. coweni in mixed-species galls. T. inquilina successfully reproduced in open galls abandoned by T. coweni, and under these circumstances was best characterized as commensal rather than parasitic. My data indicated T. inquilina was signiÞcantly more likely to move between galls, supporting the hypothesis that the inquiline actively seeks galls to invade. As frequent occupants of unsealed galls, T. inquilina may incur higher risks of predation and desiccation than T. coweni: experimental evidence showed that at least one specialist predator preferred T. coweni to T. inquilina and that T. inquilina withstood experimental dessication for signiÞcantly longer periods than did T. coweni. I suggest the distinctive morphology of T. inquilina is a correlate of the ecology of its parasitic life history on T. coweni.

KEY WORDS Tamalia, communal, inquiline, aphid, parasite

THE ECOLOGY OF EXPLOITATION is a diverse and impor- 2003). Among the more specialized of insect social tant theme in the evolution of animal behavior. Among parasites are inquilines, which obligately invade nests the forms of exploitation are brood parasitism, in of their hosts because they are unable to establish their which conspeciÞcs or heterospeciÞcs reduce their pa- own. The social Hymenoptera and staphylinid beetles rental investment by depositing young or eggs into provide numerous examples of inquiline species, all of nests of other individuals (Friedmann 1928, Yom-tov which are highly specialized and often overlooked 1980, Tallamy 1985, Rothstein 1990). A variation on because of their cryptic habits and frequent close the theme of brood parasitism is social parasitism, resemblance to their host species (Fisher 1983, Reed which in a broad sense, involves the exploitation of and Akre 1983, Kistner 2004). As a historically under- social behavior through appropriation of brood care or studied group comprising multiple, independent ori- useful nesting space by often closely related species gins of social behavior, sociality and its exploitation in (Schmid-Hempel 1998, Savolainen and Vepsa¨la¨inen aphids have only recently received much attention 2003). The success of both brood and social parasitism from behavioral ecologists (Ozaki 1995, Abbot et al. is likely to be dependent on their frequency relative 2001, Foster 2002). Although there is a growing liter- to the exploited individuals or species (Barnard and ature on the ecology and evolution of aphid sociality, Sibly 1981, May and Robinson 1985). However, social few if any published examples of interspeciÞc social parasitism is more intrusive in that it may involve the parasitism exist for this group. continued presence not only of juvenile stages but Sociality in aphids is typically associated with galls, adults of the parasitic species (Wilson 1971, Busch- adventitious growths of plant tissue induced by the inger 1986). speciÞc feeding activities of these sap-sucking insects. Social parasitism is known from a variety of taxa, As nutritious, protective domiciles, aphid galls consti- especially the termites, ants, social bees, and wasps tute an essential resource typically occupied and de- (Wheeler 1919, Michener 1974, Field 1992), although fended by solitary females (foundresses) against in- it has been reported in groups as diverse as mammals trusion by competitors (Price et al. 1987, Wool and and myxobacteria (Jones 1997, Fiegra and Velicer Burstein 1991, Moran 1993). Like thrips galls, but unlike dipteran and hymenopteran galls, aphid galls are 1 Corresponding author, e-mail [email protected]. typically hollow: the resultant gall space constitutes an

0013-8746/04/1233Ð1241$04.00/0 ᭧ 2004 Entomological Society of America 1234 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 6

the still-open gall. During the trophic phase of development, the gall is sealed and foundresses complete their growth and reproduction. After about 4 wk, the gall dries and splits open, releasing adults with wings, marking the mature phase (Mani 1964) of gall development. Offspring are either winged asexual females, which disperse and deposit a second generation of foundresses on the host plant, or winged, sexual females and males, which disperse, mate, and produce the overwintering eggs, thus completing the life cycle (Miller 1998a). Mature-phase galls are again vulnerable to intrusion not only by predators of T. coweni but potentially by inquiline Tamalia aphids. Both inquilines and foundresses require at least temporary resi- dence within galls for their survival, as do all known Tamalia (Remaudie`re and Stroyan 1984). Like T. coweni, the Þrst generation of T. inquilina is wingless and emerges from overwintering eggs: these wingless females enter galls as Þrst instars during the early phase of induction and begin reproducing alongside T. coweni after reaching adulthood. At least some of their offspring develop wings, which emerge from mature- phase galls before dispersing to larviposit another generation of wingless females that will in turn enter still-available galls of T. coweni. An unknown fraction of T. inquilina offspring apparently remains wingless throughout development and may disperse from their natal galls as Þrst instars, possibly invading other early- or mature-phase galls of T. coweni and maturing and reproducing therein. Like T. coweni, T. inquilina com- Fig. 1. Inquiline aphid, T. inquilina (top), co-occupying pletes its life cycle with the production of winged a gall on A. viscida with its host, T. coweni (bottom). T. males and winged sexual females, the latter of which inquilina is markedly more pubescent and sclerotized than T. mate and oviposit after dispersing from their natal coweni. Both specimens Ϸ1 mm in length. galls. In this study, I characterize and quantify commu- arena in which behavioral interactions among gall nally parasitic behavior by T. inquilina on T. coweni. I inhabitants can occur relatively freely; furthermore, show that the inquiline signiÞcantly reduces produc- these galls may house numerous individuals repre- tion of host offspring but has only a negligible effect senting overlapping generations (Rohfritsch and on host survivorship. I show that inquilines occupy Shorthouse 1982, Forrest 1987, Crespi and Worobey and reproduce within abandoned galls, with no direct 1998). In some aphid species, females invade galls impact on the host species. Strong circumstantial ev- intra- or interspeciÞcally, expelling or even killing the idence has implicated T. inquilina as an obligate asso- occupant in the process (Aoki and Makino 1982, Aki- ciate of T. coweni (Miller and Sharkey 2000); here, I moto 1989, Akimoto and Yamaguchi 1997, Inbar 1998). provide experimental evidence directly conÞrming In contrast, foundresses of the manzanita leaf-gall this. As obligate invaders of galls, Tamalia inquilines aphid, Tamalia coweni (Cockerell), can establish galls are more likely to move between galls under experi- solitarily or with other females. Thus, T. coweni be- mental and natural conditions, hence they may incur haves as a facultatively communal species (Miller additional risks of exposure to predation and dessica- 1998a). A recently described species, Tamalia in- tion outside the gall. I show experimentally that inquilina Miller, specializes in entering occupied or quilines are less attractive to at least one important abandoned galls of T. coweni (Miller and Sharkey predatory species and withstand dessication signiÞ- 2000) (Fig. 1). cantly longer than do foundresses. These behavioral The life cycles of T. coweni and T. inquilina are and morphological attributes appear as part of an closely coordinated where they co-occur in western adaptive syndrome in this novel form of social para- North America. Newly emerged foundresses of T. co- sitism. weni induce galls singly or in groups by repeated probing with their mouthparts along the edges of Materials and Methods leaves or on incipient ßower buds on the host plant, Arctostaphylos spp. (Ericaceae), during spring and Study Populations. Foundresses (T. coweni), inqui- summer. The early phase of gall induction (Mani 1964) lines (T. inquilina), and associated predators were provides a period of at most a few days for possible studied on populations of the host plants Arctostaph- intrusion by predators or by other Tamalia aphids into ylos manzanita C. Parry and Arctostaphylos viscida C. November 2004 MILLER:COMMUNALLY PARASITIC APHIDS 1235

the cage design in MacGillivray and Anderson (1957). I collected and identiÞed all adult offspring emerging from galls, following the key provided in Miller and Sharkey (2000). Using adult offspring as estimates of reproductive success afforded not only greater accu- racy in their identiÞcation but helped control for juvenile mortality within the gall, which increases to signiÞcant levels, especially late in the growing season. Once galls had matured and dried, I dissected them and identiÞed all occupants, dead and alive. Separa- tion of foundresses from inquilines can be done readily Fig. 2. Clip cage design used for experimental manipu- even in a desiccated state, because inquilines bear the lation and collection of Tamalia aphids emerging from galls. recognizable features of greater sclerotization (the Cage Þts over gall and contains aphids without injuring host degree of rigidity of the cuticle; Chapman 1982), plant. greater pubescence, and longer antennal length than do foundresses (Miller and Sharkey 2000). To monitor Parry at the California State University Big Chico productivity of late-season galls, I caged a separate Creek Ecological Reserve (BCCER), Butte County, sample of 20 mature-phase galls and collected and CA; A. viscida and Arctostaphylos patula E. Greene at identiÞed all emergent aphids over a 4-wk period. At the University of California Blodgett Forest Research the end of the growing season, I collected these galls Station, El Dorado County, CA; and Arctostaphylos and recorded their contents. glauca Lindley at the University of California Deep Life History and Behavioral Syndromes of the In- Canyon Research Station, Riverside County, CA dur- quiline. To test whether inquilines can induce galls ing AprilÐAugust 1995Ð2003. As is typical of most spe- under experimental conditions, I marked 13 treatment cies of Arctostaphylos, these populations are subject to groups, each comprising three Þrst-instar inquilines a pronounced seasonal drought, presenting physiolog- (aphids generally Ͻ1 wk old), and 11 control groups ical challenges both to the host plant and to plant- of three Þrst-instar foundresses with ßuorescent ani- feeding insects (Price et al. 1987, Hileman et al. 2001). mal tracking powder, and caged them over developing Although their life histories and ecology are clearly inßorescences of A. patula. In the laboratory, aphids distinct and here treated as such, both T. coweni and were dissected from galls and transferred with a Þne T. inquilina may represent species complexes (Miller artistÕs brush to cages consisting of 20-mm-long sec- and Crespi 2003). tions of clear plastic drinking straws (5 mm in diam- Impact of Inquilines on Host Fecundity and Fitness. eter) that were stoppered with cotton wool at both Samples of galls were taken over the entire growing ends and that Þt snugly over the lowermost secondary season from host plants, and gall contents were ex- stalk of each experimental inßorescence; trials were amined by means of a stereoscopic dissecting micro- transported to the Þeld on ice. After transfer to inßo- scope. Particular attention was paid to the timing of rescences, I placed spring-clip cages over each trial: both gall establishment by T. coweni and the appear- these protected them and helped maintain position of ance of inquilines in galls; as far as possible, I classiÞed the cotton wool as the inßorescences expanded. I all aphids by developmental stage (instar). As used assigned trials randomly to test plants, except that in here, “foundress” refers to either the Þrst or second no case were experimental aphids placed on the same galling generation of T. coweni, and “inquiline” to any individual plants from which they were collected. The wingless individual of T. inquilina. Maximum length cages were collected after 4 wk, and aphid survival and and width of galls were measured to the nearest 0.1 gall establishment rate were recorded. Because any mm using a reticle mounted on a stereoscopic dissect- survivors had molted and were thus no longer iden- ing microscope: gall volume was estimated assuming tiÞable by ßuorescent powder, the presence of galls approximated an ellipsoid with volume marked exuvia (shed exoskeletons remaining from the ␲ 2 4/3 R1R2 , where R1 is one-half the long axis of the Þrst molt) was used to identify aphids and their most gall and R2 is one-half the transverse axis of the gall. In recent location before molting. a general predator survey, the frequency and identity To monitor dispersal of any aphids from, and po- of any predators were noted: particular attention was tentially between, galls, I placed 250 cages over tro- paid the timing of the appearance of predators relative phic-phase galls in the Þeld and inspected them every to development of the gall. 2Ð3 d for 4 wk: all aphids emerging were collected and Production of offspring by foundresses both in the identiÞed to species and instar. To determine whether presence and absence of inquilines was compared inquilines, foundresses, or both enter galls under ex- using spring-clip cages placed over 44 trophic-phase perimental conditions, I collected aphids from galls galls in the Þeld and monitored weekly. Cages were and marked them with ßuorescent animal-tracking constructed of sections of 25-mm-diameter plastic powder, using a Þne artistÕs brush. I caged 22 groups tubing, covered on one end with Þne netting (0.3 mm of three Þrst-instar inquilines and six groups of three mesh) and attached to spring-loaded hair pins that Þrst-instar foundresses over mature galls. Gall and were glued to a 30-mm square piece of foam on alu- cage contents were collected after 1 wk, and the lo- minum backing (Fig. 2); these were modiÞcations of cation of any marked individuals was recorded. 1236 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 6

Table 1. Effect of the presence of inquilines on productivity of Tamalia galls

Gall occupants Gall phase n Adult foundress offspring produced Adult inquiline offspring produced Foundresses only Trophic 24 8.9a (3.0) Ñ Foundresses with inquilines Trophic 20 1.2b (0.7) 7.8 (2.9) Inquilines only Mature 10 Ñ 2.7 (1.4)

a and b signiÞcantly different (Mann-Whitney test, P Ͻ 0.05; two-tailed).

The potential adaptive value of the morphology of of inquilines than when inquilines co-occupied galls ϭ Ͻ inquilines relative to foundresses was explored (Mann-Whitney test: U20, 24 344; two-tailed P through manipulations of exposure to predators and 0.05), although the number of offspring reared to experimental dessication. Leucopis sp. larvae (Diptera: adulthood for foundresses and inquilines combined Chamaemyiidae), which are common natural preda- was about the same for parasitized and unparasitized tors of T. coweni (Miller 1998a), inquilines, and found- galls (Mann-Whitney test, not signiÞcant; Table 1). resses were collected from mature galls. In each of 10 Inquiline production of adults exceeded that of found- trials prepared, Þve adult inquilines and Þve adult resses in parasitized galls, but not signiÞcantly so foundresses were transferred with a Þne brush to an ϭ ϭ (Mann-Whitney test: U20, 20 268.5; two-tailed P opened (and emptied) gall in a 100 by 15-mm petri 0.07; Table 1). Of 20 mature-phase galls monitored, 10 dish. Five Leucopis larvae, ranging anywhere from the contained at least one foundress or inquiline and 7 second to the Þfth instar, were introduced to the gall, contained at least one living inquiline; none contained and each trial was observed continuously for up to 120 living foundresses. Inquiline production of adult off- min under a dissecting microscope. Once positioned, spring continued 2 wk after the last foundress off- each experimental animal was free to move out of the spring were recorded and ranged from 1 to 12 per gall gall. I recorded all direct contacts with the mouthparts (Table 1). by Leucopis larvae on the aphids and scored the rate Although the presence of inquilines was associated of successful attachment and penetration of the cuti- with a decrease in the reproduction of foundresses, cle (once Þrmly attached, the larva feeds by ingesting inquilines had no measurable effect on foundress mor- body ßuids of the aphid, resulting in a noticeable tality rates. In samples of 149 galls containing solitary decrease in the size of the aphid). No animal was used foundresses and 36 galls with a single foundress and in more than one trial; successive attacks by the same one or more inquilines, 21.1% of foundresses failed to predator on the same aphid were not recorded. reach adulthood in the absence of inquilines; 20.0% To compare the ability of inquilines and foundresses died prematurely when at least one inquiline was to withstand dessication, therefore simulating evapo- present in the gall (␹2 test for independence; ␹2 ϭ 0.01, rative demand outside the gall, 21 adult foundresses n ϭ 185, df ϭ 2; not signiÞcant). Similarly, the pres- and 26 adult inquilines were obtained from trophic- ence of multiple inquilines in galls had no signiÞcant phase galls and transferred to a petri dish, which was effect on inquiline mortality rates: in 42 galls sampled placed in a convection (drying) oven at 40ЊC. The aphids were monitored every 5 min, and their survival containing at least one inquiline, there was no ob- rates were recorded: an aphid was scored as still alive served mortality before adulthood in any inquilines if its legs or antennae showed movement. collected, although as many as nine co-occupied a Statistical Analysis. Statistical procedures were per- single gall. formed with SYSTAT (Wilkinson 1989) and Biostats The presence of inquilines had no signiÞcant effect Basics (Gould and Gould 2002). Nonparametric sta- on gall size (volume) in early- and trophic-phase galls tistical methods were applied in the analysis of results (early-phase galls containing solitary foundresses Ϯ 3 ϭ when data were non-normally distributed (Kolmog- only; 79.5 17.1 mm , n 11; galls with one or more orov-Smirnov goodness-of-Þt tests on original or trans- inquilines present in addition to solitary foundresses, Ϯ 3 ϭ formed data, Lilliefors P Ͻ 0.01). 112.7 46.9 mm , n 32; for trophic-phase galls, 984.2 Ϯ 106.6 mm3, n ϭ 62 and 1,003.9 Ϯ 182.7 mm3, n ϭ 27, respectively; t-tests, P Ͼ 0.5). Mature-phase Results galls, by deÞnition, no longer respond with further Impact of Inquilines on Host Fecundity and Fitness. growth to feeding by galling aphids. When present, The contents of 200 galls on A. viscida at BCCER were additional foundresses do not signiÞcantly increase sampled. Of these, 178 contained at least one found- gall size beyond that achieved by solitary foundresses ress or inquiline: predation or abandonment may ac- (unpublished data). count for the remaining 22 empty galls. One hundred The gall-induction experiments provided no evi- sixty-one galls contained at least one foundress, and dence that inquilines can induce galls in the absence the mean foundresses per occupied gall was 1.10 Ϯ of foundresses. Twenty of 39 inquilines were recov- 0.03 (SE; range, 1Ð5); 58 galls contained at least one ered 1 wk after trials were set up: all died before inquiline, and mean inquilines per occupied gall was establishing galls. In contrast, 21 of 33 foundresses 2.09 Ϯ 0.23 (range, 1Ð9). Production of adult offspring survived long enough to establish 18 galls (test of by foundresses was signiÞcantly higher in the absence proportions; Z ϭ 5.53, P Ͻ 0.0001); taken together, November 2004 MILLER:COMMUNALLY PARASITIC APHIDS 1237 these experimental data conÞrm that T. inquilina is Discussion obligately associated with T. coweni. Most published examples of social parasitism in- Life History and Behavioral Syndromes of the In- volve the exploitation of the eusocial (highly social) quiline. Although both inquilines and foundresses dis- taxa (Michener 1974, Ho¨lldobler and Wilson 1990). persed from galls and were trapped in cages, inquilines For example, inquiline ants exploit the elaborate re- were signiÞcantly more likely to do so: 15/42 (36%) of productive division of labor in ant societies, often with all inquilines collected in cages or caged galls were the result that offspring of the inquilines are reared by outside galls; 16/160 (10%) of all foundresses collected their adoptive colony (Aron et al. 1999). Although were outside galls (test of proportions; Z ϭ 4.11, P Ͻ Tamalia societies are relatively simple and exhibit no 0.0001). Of 15 marked inquilines recovered from the apparent specialized behaviors or morphologies dis- gall invasion experiment, 6 had entered galls; of three tinctive of eusocial systems, T. inquilina obligately marked foundresses recovered, none had entered invades galls and reduces Þtness of its facultatively galls. These data are consistent with the hypothesis communal host T. coweni. In this inclusive sense, T. that inquiline dispersal rates between galls exceed inquilina acts as a social parasite (Wilson 1971, Bus- those of foundresses. In Þeld-collected samples of 100 chinger 1986, Bourke and Franks 1995, Schmid- early-phase, 270 trophic-phase, and 430 mature-phase Hempel 1998). Like its host, the inquiline facultatively galls, Þrst-instar inquilines were the sole occupants of occupies galls communally: multiple females share four mature-phase galls and never occupied early- or galls and breed together, but apparently not through trophic-phase galls in the absence of foundresses. active cooperation. Although inquilines may compete First-instar inquilines occurred alongside foundresses directly with foundresses for host plant resources by in 7 early- and 10 mature-phase galls, but in only 1 feeding and reproducing within the gall, no overt trophic-phase gall. These data support the possibility agonistic behavior occurs. This is the Þrst report of that the trophic-phase gall, being relatively well communal parasitism in social aphids in the frame- sealed, is the stage of gall development during which work of a quantiÞed cost and beneÞt analysis of the overall effects of parasitism on Þtness. invasion by inquilines is least likely. At least six of the seven known species of Tamalia In samples of 83 early-phase, 31 trophic-phase, and exhibit facultative communal behavior in which fe- 63 mature-phase galls inspected for predators of Ta- males co-occupy galls and breed jointly within the gall malia, Anthocoris whitei Reuter (Heteroptera: Antho- space (unpublished data). Recent molecular evidence coridae), a common predator at all stages of its de- indicates the inquiline clade branched off after the velopment, and Leucopis sp., a common predator galling life history evolved in ancestral Tamalia, pos- during its juvenile stages, were observed exclusively in sibly in association with a shift in host plant species mature-phase galls (one or more A. whitei in 16/63 and (Miller and Crespi 2003). Gall invasion involving Leucopis in 7/63 galls). This suggests that aphids in closely related species is seen also in the facultative mature galls are not only vulnerable to invasions by inquiline aphid Eriosoma yangi Takahashi, which sim- inquilines but also to predation. The single sampling ilarly may have evolved inquiline behavior in con- date of galls representing all phases of development junction with a host plant shift (Akimoto 1988). The from the same population of the host plant controlled close phylogenetic afÞliation of Tamalia inquilines for effects of seasonality in the appearance of preda- and foundresses parallels the hypothesized origins of tors. numerous socially parasitic species from ancestral In the predator choice experiments using Leucopis clades of the host species: such labels as agastopara- larvae on adult foundresses and inquilines, successful sitism or adelphoparasitism have been applied in these Leucopis attacks resulted in continuous feeding for at cases (Ronquist 1994, Hunter and Woolley 2001, least 1 min to a maximum of Ͼ120 min before obser- Foitzik et al. 2003). In Tamalia, communal behavior vations ended (one larva was still feeding on a Tamalia may be considered an ancestral state with mutual aphid after Ͼ232 min of discontinuous observation). tolerance of group members an important Þrst step in Although larvae were equally likely to encounter and the evolution of social behavior (Krafft et al. 1994). contact foundresses and inquilines (29 contacts with Such intraspeciÞc communal behavior, with its atten- foundresses versus 26 with inquilines, ␹2 ϭ 0.16, df ϭ dant risks of intraspeciÞc brood parasitism, may have facilitated invasion and exploitation by incipient in- 1, not signiÞcant), larvae preferentially attacked and quilines at the origins of interspeciÞc parasitism consumed foundresses over inquilines (11/29 ob- (Brockman 1993, Zink 2000, Neumann and Moritz served contacts between Leucopis and foundresses led 2002). to successful attacks versus 0/26 for inquilines; G-test A parallel is found in the socially parasitic ants, ϭ Ͻ for goodness-of-Þt, G 16.55, P 0.001). When Leu- where polygyny (meaning multiple reproductive fe- copis larvae contacted T. inquilina, they seemed to males in a single colony: common in ants, Buschinger reject them quickly, unlike most contacts with T. co- 1986; but rare in galling aphids, Miller 1998a) in the weni. In the dessication trials, inquilines survived out- host is a likely precondition for the evolution of in- side galls at 40ЊC signiÞcantly longer than did found- quilinism (Bourke and Franks 1991). Like Tamalia resses (200 Ϯ 71 versus 130 Ϯ 46 min); Wilcoxon inquilines, inquiline ant species tend to occupy po- signed-ranks test, Z ϭ 3.42, one-sided P Ͻ 0.001). lygynous colonies and are themselves polygynous 1238 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 6

(Buschinger 1986). Unlike many or most species of survival, reproduction, or both (Roskam 1992, Ron- ants, and apparently all described species of galling quist 1994, Heard and Buchanan 1998, Sanver and aphid, Tamalia societies exhibit no overt agonistic Hawkins 2000, Yang et al. 2001). However, Tamalia behavior. In the case of intraspeciÞc communal gall- inquilines not only invade occupied galls but regularly ing, this can be understood readily as additional found- enter mature, abandoned galls and survive long resses impose only a minor demonstrable cost in Þt- enough to reproduce, with no direct effect on the host ness to their adopters, and indeed may be acting aphid species. Thus this interspeciÞc interaction does mutualistically under the possibility they constitute not constitute parasitism but may instead be charac- clonal groups (Miller 1998b). However, the inquiline terized as commensalism, in which one species ben- competes effectively with its host, implying that se- eÞts while the other is unaffected (Begon et al. 1990); lection should favor territorial behavior in Tamalia Wilson (2000) further reÞnes commensalism involv- foundresses. The lack of territoriality in Tamalia ing nests as nest commensalism. The commensal guild foundresses is striking and parallels the evolutionary of arthropods occupying galls abandoned by the gall- puzzle of how various brood and social parasites in a inducers has been described as “successori” by Mani number of taxa, including birds (Yom-tov 1980), Þsh (1964), many of which enter galls seeking shelter, food (Sato 1986), mammals (Jones 1997), wasps and bees or both. A multitude of animal species, including not (Field 1992), ants (Buschinger 1986), and lace bugs only insects but other arthropods, reptiles, amphibi- (Tallamy and Horton 1990) succeed in deceiving and ans, birds, and mammals will take advantage of aban- exploiting their hosts (Wilson 1971, Johnsgard 1997). doned nests, burrows, and other protective domiciles, There are at least three possible reasons why such but typically few such successori are specialists in territorial behavior has not evolved. First, no evidence exploiting domiciles created by close phylogenetic of discrimination by Tamalia aphids has yet been relatives (Friedmann 1928, Mani 1964, Trenham 2001, shown, and these and other aphids may simply lack the Averill-Murray et al. 2002, Mendonc¸a and Ro- necessary neurological and genetically mediated manowski 2002). Apparently, Tamalia inquilines are mechanisms needed for precise discrimination of kin capable of using resources in mature galls abandoned (Aoki et al. 1991, Stern and Foster 1996, Miller 1998b, by foundresses possibly for reasons of predation, re- Abbot et al. 2001). In a co-evolutionary arms race duced nutrient quality, or increased evaporative de- between parasite and host species (Dawkins and mand. These late-season, senescent galls are unlikely Krebs 1979), any ability evolving in the host species to to be highly productive, as shown by the low number recognize parasites comes at a potential cost of dis- of offspring produced by inquilines in mature galls, but crimination against the host itself (Johnsgard 1997, this opportunistic life history strategy is consistent Lotem and Nakamura 1998). Hence foundresses at- with the ability of inquilines to compete successfully tempting to eject inquilines from their gall risk eject- in galls still occupied by foundresses. ing other foundresses as well, some of which may be It is important to note the nonmanipulative nature clone-mates (Miller 1998b). Second, by invading galls of this portion of the study. By caging and monitoring early and remaining within them, inquilines may be naturally occurring galls rather than attempting con- masked as aliens by adsorbing any chemical signature trolled releases of inquilines into existing galls, it was of the gall or its colony on their cuticle, as occurs in assumed that inquilines entered galls based primarily socially parasitic butterßies and wasps (Akino et al. on their availability and not based on any preference 1999, Sledge et al. 2001). Third, although establishing for poorly defended galls harboring decrepit found- a gall represents a signiÞcant investment in time and resses. That any evidence for agonistic interactions energy, the risks of Þghting may discourage territorial between foundresses and inquilines has yet to be behavior by foundresses against conspeciÞcs or inqui- found, in examinations of thousands of galls (unpub- lines (Price et al. 1987, Zahavi and Zahavi 1997, but see lished data), is support for this assumption. However, Whitham 1979). experimental releases of inquilines into caged galls When inquilines invaded galls occupied by found- would permit controlled tests of the alternative hy- resses, they reduced host reproductive success but pothesis that T. inquilina invades galls in a discrimi- had only a negligible effect on host survival rates. natory fashion, based on an assessment of the likeli- Although the proportion of host offspring raised to hood of successful reproduction therein. adulthood was signiÞcantly lower in parasitized versus Tamalia inquilines show a signiÞcantly greater de- unparasitized galls, total offspring output was about gree of mobility than foundresses, as evidenced by the same for both outcomes. This situation is similar to their exit rates and the capacity to enter galls. Al- that of intraspeciÞc brood parasitism in the burying though foundresses likely disperse between galls as beetle Necrophorus vespilloides Hbst., in which fe- well, the distinctly greater rates of mobility in inqui- males rear the same number of offspring irrespective lines reßect substantial differences in their respective of whether they are parasitized, even though parasit- life-history strategies. Selection of aphid clones com- ized females raise signiÞcantly fewer of their own prising single genotypes may favor risk-reducing strat- offspring (Mu¨ ller et al. 1990). Like the ecology of egies such as dispersal and developmental plasticity, inquilinism in Tamalia galls, the few previously pub- both of which occur in Tamalia and in other parthe- lished studies quantifying the impacts of inquilinism in nogens (Hamilton and May 1977, Janzen 1977, Miller other plant-feeding hemipterans, cynipid wasps and 1998a, Poulin 2003). Inter-gall dispersal has been well cecidomyiid ßies have reported reduced rates of host documented in an array of galling aphids with such November 2004 MILLER:COMMUNALLY PARASITIC APHIDS 1239 techniques as sticky traps and molecular markers foundresses only and with mixed-species galls. Finally, (Setzer 1980, Aoki 1982, Akimoto 1989, Ozaki 1995). similar examples of inquiline parasitism probably exist The lack of evidence for discrimination by gall occu- in other communal galling societies, e.g., galling thrips pants against such interlopers is thought to facilitate (Morris et al. 1999), but perhaps have been over- this mode of exploitation (Abbot et al. 2001). looked because of close biological similarities between My data suggest inquilines incur a relatively high host and parasite: discovering further such examples risk of exposure to predators and to dessication, the will require careful taxonomic and ecological investi- latter of which is a constant threat to gall-dwelling gation. insects experiencing arid conditions during the growing season (Price et al. 1987, Morris et al. 1999). The Acknowledgments same temporal “window of opportunity” for invasion and exploitation of established galls imposes an in- I thank M. Marchetti for critical comments during prep- creased likelihood of encountering natural enemies aration of the manuscript. P. Ullman assisted with Fig. 1. The (Stone and Scho¨nrogge 2003). However, under ex- staffs of the Bidwell Environmental Institute, Blodgett For- perimental conditions, inquilines experienced a sig- est, and Deep Canyon Research Stations provided access to niÞcantly reduced rate of attack by a specialist pred- aphid populations. This work was supported by the California ator and survived dessication signiÞcantly longer than State University, Chico Department of Biological Sciences, the Trinity University Department of Biology, a National did foundresses. It is not yet clear what factors lend Institute of Health Postdoctoral Fellowship at the Center for inquilines greater immunity to predators and to evap- Insect Science, University of Arizona, and a UC Berkeley orative demand, but their distinctive morphology may Research Assistantship. All experiments performed comply be important in this regard (Fig. 1): compared with with the current laws of the United States. foundresses, adult inquilines are densely pubescent and exhibit signiÞcant sclerotization. The distinct morphogenetic patterns of inquilines References Cited may provide further clues about their ecological role Abbot, P., J. H. Withgott, and N. Moran. 2001. Genetic con- with foundresses. In aphid species in which usurpation ßict and conditional altruism in social aphid colonies. or defense of galls occurs, specialized morphology for Proc. Natl. Acad. Sci. U.S.A. 98: 12068Ð12071. combat is most pronounced in the Þrst instar (Aoki Akimoto, S. 1988. The evolution of gall parasitism accom- 1977, Aoki and Makino 1982). Greater sclerotization panied by a host shift in the gall aphid, Eriosoma yangi would likewise be expected in Þrst-instar inquilines if (Homoptera: Aphidoidea). Biol. J. Linn. Soc. 35: 297Ð312. Akimoto, S. 1989. 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Aoki, S. 1977. Colophina clematis (Homoptera, Pemphigi- degree of differences in sclerotization between inqui- dae), an aphid species with “soldiers.” Kontyuˆ . 45: 276Ð lines and foundresses remains to be quantiÞed. 282. Neither the details of the mechanism by which T. Aoki, S. 1982. Soldiers and altruistic dispersal in aphids, pp. coweni induces galls nor the events by which the 154Ð158. In M. D. Breed, C. D. Michener, and H. E. Evans ability to induce galls was lost in the ancestral T. (eds.), The biology of social insects. In Proceedings, 9th inquilina are known. As obligate invaders of galls, Congress of the International Union for the Study of inquilines may lack the appropriate probing behaviors Social Insects, Westview Press, Boulder, CO. or chemical or genetically mediated factors necessary Aoki, S., and S. Makino. 1982. Gall usurpation and lethal to stimulate a gall. 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