Possible Mutualism between Females of the Subsocial Membracid Polyglypta dispar (Homoptera) Author(s): William G. Eberhard Source: Behavioral Ecology and Sociobiology, Vol. 19, No. 6 (1986), pp. 447-453 Published by: Springer Stable URL: http://www.jstor.org/stable/4599982 . Accessed: 07/09/2011 09:37

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http://www.jstor.org Behavioral Ecology Behav Ecol Sociobiol (1986) 19:447-453 and Sociobiology

<0 Springer-Verlag1986

Possible mutualism between females of the subsocial membracid Polyglypta dispar (Homoptera)

William G. Eberhard Smithsonian Tropical Research Institute and Escuela de Biologia, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica

Received April 18, 1986 / Accepted August 28, 1986

Summary. Female Polyglypta dispar membracids Study site and methods facultatively guard egg masses or oviposit into Polyglypta dispar (Fowler) is a large membracidfound on the masses guarded by other females. Defending weedy shrubs Montanoa hibiscifolia,and Verbesinaturbacensis females repel at least some enemies of both eggs (both Compositae). Observations were made on the principal and nymphs. Eggs of guarding females may be par- host, M. hibiscifolia,during the latter part of the rainy season tially protected from parasitism by the presence from 13 July to 19 October, 1982 near San Antonio de Escazu, Costa Rica (1350 m elevation). Eggs, nymphs, and attending of additional eggs laid by other females. Females females were checked daily or every other day during most sometimes desert egg masses or groups of nymphs, of this period, usually in the morning. Four differentM. hibisci- and undefended masses are sometimes adopted by folia plants within a 10 m radius were surveyed regularly, and other females. Some individuals remain on or near three others sporadically. M. hibiscifoliais a weedy perennial that is common in disturbed habitats in the Central Valley the plant where they grew up, and littermates of Costa Rica. It usually sheds some leaves and flowers early sometimes oviposit into the same egg mass. Some in the dry season, and vegetative growth is concentrated in copulating pairs are littermates, while others are the wet season, but plants generally have some green leaves not. Females with larger numbers of mature and year-round.Many plants near the study site and also at another nearly mature eggs in their ovaries are less likely site 12 km away with many M. hibiscifoliaplants lacked mem- bracids. Membracidswere individuallymarked with fast drying to defend egg masses, and females desert smaller model airplanepaint. groups of nymphs more often. Newly molted adults were captured in vials, marked, and returned to the same leaf. Rechecking showed that this treat- ment did not cause the adult to abandon the leaf when marking was done in the first 3 days of an adult's life. The accounts below of newly moulted adult behavior are of individuals marked in the first three days of adult life. Introduction Dissections of ovaries of freshly killed and newly thawed females that were killed by freezing were performed in saline Subsocial behavior (postovipositional parental be- solution on a glass slide. Large, partially translucent eggs havior that promotes the survival, growth or devel- >1 mm long were classified as "mature or nearly mature". Some of these were found in the oviducts, and others in the opment of offspring) has evolved many times in lower parts of ovarioles. In one female that had been oviposit- a wide variety of , and is particularly com- ing when collected, some of the translucenteggs in the oviduct mon in the homopteran family Membracidae (re- were covered by a thin whitish membrane. Other eggs, termed views by Eickwort 1981; Tallamy and Wood 1986). " developingeggs ", were pearly white in appearanceand ranged interactions between subsocial from 0.1 to <9 mm long. Developing eggs occurred only in Cooperative par- the ovarioles. The amount of fat on the female's body wall ents are much less widespread taxonomically, be- was estimated visually. Spermathecaeof known virgins were ing frequent only in the Hymenoptera (Wilson all flat and clear white in color; the other spermathecalforms 1971). This paper reports on possible cooperation (ovoid, spherical, ovoids in various states of collapse) all had in a subsocial membracid in which females guard dark material inside, and were taken to indicate that insemina- tion had occurred. eggs and nymphs. Some females oviposit in the Egg masses from which all membracidsand parasites had egg masses of others, and both females may benefit emerged were teased apart egg by egg. A brownish membrane as a result. on the otherwisewhite inner surface of the egg and an irregular 448

"chewed" emergal hole instead of the clean split at the egg's on the periphery (P<0.01 with Chi Squared Test) tip left by membracidnymphs were used as indicators of para- (average rates of parasitism were 34?16% and sitism (eggs containing wasp pupae had this membrane). Eggs 38+19% in the center and the while from which neithermembracids nor parasiteshad emergedwere periphery, classified as undeveloped. Observationsof the minute parasitic average rates of undeveloped eggs were 14 + 11 and wasps were made in the field using a magnifying lens mounted 20+16% respectively). on a headband magnifiergiving a 10 x magnification. Defense against some large predators of There is some uncertaintyregarding species classifications nymphs was more effective; I saw females success- in the Polyglypta. Metcalf and Wade grouped the form in this study with others under the name P. costata (T.K. Wood, fully chase off three coccinellid beetles which personalcommunication), but I have followed the older classifi- preyed on nymphs. They did not respond however cation of Fowler because some of the different morphological to syrphid larvae attacking their nymphs, perhaps forms of Metcalf and Wade's " costata " consistentlyoccur sym- because no alarm pheromone was released (Nault patrically but are associated with different plant species (Eber- et al. 1974). Defensive behavior was dangerous, as hard, in preparation),and the male genitalia are slightly differ- ent. I saw defending females succumb to attacks by All averages are followed by + 1 standarddeviation. a reduviid bug and a salticid . Two other predators attacked nymphs (an adult staphylinid beetle, and a larval chrysopid (Neuroptera)), and Results at least four other species preyed on unguarded eggs (three mirid bugs and an unknown predator 1. Guardingbehavior which ate large chunks out of egg masses - perhaps Most egg masses and many groups of nymphs were a katydid?). accompanied by an adult female. Guarding did not There were apparently 5 nymphal instars. Av- preclude feeding, as some brooding females were erage estimated durations of first through fourth seen with the proboscis inserted into the central instars in the field were, respectively, 5, 4, 6 and vein of the leaf. These sites may not be ideal feed- 8 days. These data are only approximate since indi- ing sites, however, as most solitary males and fe- vidual nymphs were not marked. Nymphs, like males not associated with offspring were seen on adults, fed on the lower surfaces of leaves. They younger leaves. Females near egg masses or groups tended to cluster with other nymphs. The usual of nymphs gave several apparently defensive re- presence of an egg mass near groups of younger sponses when other insects or large objects ap- nymphs and the relative uniformity of sizes of proached. In contrast to nonguarding females, a nymphs within most groups suggested that many female with eggs was unlikely to move away even aggregations were composed of individuals that when prodded and pinched with forceps. Often a had hatched from the same mass. There were occa- defending female responded by buzzing her wings, sional mismatches of nymphal sizes within an ag- giving strong lateral kicks at the object with a hind gregation or abrupt increases in the numbers of leg, or sidling toward the object, and swinging the larger instar nymphs in a group from one day to posterior end of her pronotum laterally, on occa- the next, however, indicating that some groups had sion hitting it. members that came from different egg masses. Females interacting with the small egg parasite Nymphs sometimes moved to other leaves, but Gonatocerus sp. shuddered their bodies, shuffled adult females showed no signs of guiding the their feet, and sometimes turned 1800. They seemed nymphs' movements as do other membracids(Tal- unable, however, to keep track of the wasp, and lamy and Wood 1986). in general the defense seldom resulted in the wasp leaving the egg mass. Rates of parasitism of eggs 2. Desertions and adoptions were higher in one study area (average 26.3% in 4375 eggs from 14 masses) then another about Females deserted eggs and nymphs after varying 1 km away (< 5% in each of 7 masses). lengths of time (Table 1). Offspring were never Rates of parasitism in different regions of egg guarded until the nymphs became adults. Since in masses were probably not uniform. Each egg mass large masses the oldest nymphs were often at least was divided into central and peripheral areas using two moults ahead of the youngest, many nymphs the maximum width of the mass (w) as a reference: were abandoned at younger ages than those in Ta- all eggs within w/3 of the edge were classed as ble 1. peripheral. When rates of membracid emergence The greater the number of nymphs in a mass in the central portions of large masses (.x=358 + the longer it was guarded (r=0.50, P<0.01 for 241 eggs each) were compared with those on the oldest nymphal stage abandoned versus number periphery, 14 of 16 were higher in the center than of nymphs in 28 masses). The average numbers 449 of nymphs present in these masses deserted at the Table 1. Frequencies(in %) with which 53 females abandoned first, second, third, fourth and fifth instar were, their offspring at different stages of development respectively, 28, 35, 56, 80, and 82. Egg masses Stage of development Approximatenumber Frequency laid later in the season tended to be abandoned of days the female earlier (r= -0.52, P<0.01 for oldest nymphal guarded stage abandoned versus number of days from start of the study). The partial correlation of abandon- Before eggs hatched < 18 36 ment with number of nymphs when the effect of Oldest nymphs 1st instar 18-23 15 Oldest nymphs 2nd instar 23-27 9 date was held constant was 0.44 (P = 0.01), indicat- Oldest nymphs 3rd instar 27-33 7 ing that both date and number of nymphs had Oldest nymphs 4th instar 33-41 19 significant and independent effects on time of Oldest nymphs 5th instar >41 11 abandonment. At the end of the rainy season females aban- doned eggs more frequently. For instance only 2 an aggregation of young adults. Copulation of 21 masses laid between 24 June and 17 August seemed to be particularlycommon 1-2 weeks after were abandoned before any nymphs hatched (ovi- the first adults of a group appeared, and one fe- position date was estimated by subtracting 18 days male copulated 13 days after being marked as a from the date of first hatching), while 19 of 33 newly molted adult. In four cases known litter- laid between 17 August and 15 October were aban- mates were found copulating, indicating that some doned before the first nymph hatched (p <0.001 inbreeding may occur (since more than one female with Chi Squared); modal abandonment stages can oviposit in a given egg mass, this is not proof during the first and second periods were fourth of inbreeding). Three other copulations involved instar and eggs respectively. marked individuals that matured in different Six of 32 egg masses that were left undefended clutches. Remating occurs at least occasionally, when females deserted them or when I collected since one female copulated two days after she laid the female were subsequently adopted by other fe- eggs, and three other females were found in aggre- males (dates of adoption ranged from 13 August gations after having previously attended egg to 14 October). One of the six adopting females masses (all females collected attending eggs and had been observed ovipositing into the mass sever- later dissected had mated - see below). al days earlier, but the others had not been asso- Aggregations usually formed on the leaf where ciated with the egg masses previously. The lengths the nymphs had matured. When one aggregation of time females defended adopted masses varied of marked adults was disbanded by causing the between 4 and 25 days. The sample was too small members to fly away, many of the same individuals to check whether adoptive females defended short- were reaggregated on the same leaf the next day. er lengths of time. In three other cases one female I could not discern why particularleaves were cho- replaced another and guarded a mass for at least sen for assembly sites. 5 days. The takeovers were not observed, and it is possible that the first females left before the re- placements arrived. 4. Ovipositionand interactionsbetween ovipositing females Eggs were 3. Aggregation of adults and copulation always laid into the lower side of a cen- tral vein of a leaf, often in the second pair of ex- Young adults remained in the vicinity of other panded leaves from the tip of the branch. Most group members for up to 1-2 weeks after the last of the oval egg was inside the leaf, with a small moult, and mating occurred in and near these ag- but variable fraction of one end free. Up to 6 para- gregations. Aggregations of new adults often also sitic wasps were seen near an ovipositing female, contained older males (judged by their harder cuti- and more than half of the more than twenty fe- cle) and four older females that had earlier been males observed ovipositing had at least one wasp marked while associated with other egg masses nearby. Once an egg was laid it apparently swelled, were also found in aggregations. Courtship was as the pair of "lines " near the tip, which were common in these aggregations. Males climbed parallel and nearly touching in newer eggs, later onto the backs of females, and females with diverged to form a rough circle. Close examination mounted males often walked away from the aggre- of eggs in the field permitted approximate determi- gation onto nearby leaves. I found about 20 copu- nation of their ages. lating pairs, in all but a few cases on leaves near The sizes of egg masses varied widely. Masses 450 collected with defending females (and which, as eggs (in all cases more than the respective guarding shown below probably would have in many cases female), in 13 of 14 cases the average length of received additional eggs) had 41-228 eggs (x= the visitor's developing eggs was larger than that 144+65, n=12); deserted masses from which all of the eggs of the guard (P<0.01 with one tailed insects had emerged ranged from 64 to 619 eggs Chi Squared Test). The numbers of developing (x = 259 + 159, n = 13) (P < 0.01 Mann Whitney U- eggs in different size categories also differed, with Test). Females sometimes added eggs over a period visitors having relatively more large (>0.67 mm of several days; one female was observed oviposit- long) eggs (P<0.001 with Chi Squared Test). In ing into a mass that she had been guarding contin- sum, visitors showed a weak tendency to have uously for the previous eight days. more mature and nearly mature eggs, and a It was common for more than one female to stronger trend to have larger developing eggs. oviposit into one egg mass. Sixty-two masses fol- lowed in the field averaged 2.8+2 females/mass; 5. Role switchingand migration 21 had only one female associated with them, while the maximum at one mass was 9. These are under- Of 113 marked females that were found associated estimates since some masses were not found until with an egg mass, 61 % were not resighted at differ- several days after they were initiated, and inspec- ent sites, while 21, 12, 3, 1, and 2% were resighted tions were usually made only once or twice/day. at 1, 2, 3, 4, and 5 other sites respectively. Individ- Some guarding females gave clear signs of at- ual females were not limited to either the visitor tempting to prevent an approaching visitor from or the guard role. Of 40 females for which succes- ovipositing (a female's intention to oviposit was sive roles were determined, 20 performed both indicated by her lowered, ventrally directed ovi- guarding and visiting, 18 visited only, and 2 only positor, a position seen only in association with defended (visiting was defined as <5 days seen oviposition). Guards kicked at visitors, pushed on or near a given mass with other females present, them with their pronota, swung the posterior part or not >1 consecutive day alone on the mass). of the pronotum sideways to hit them, and even The female with the longest recorded history (86 in one case apparently attempted to pry the visitor days and a probable minimum lifetime of at least off the leaf by backing under her with the rear 100 days) defended two successive clutches until tip of the pronotum. Such defensive behavior was the nymphs in each attained the fourth instar; then seen on 15 occasions but never caused the other starting two days later she spent three days in an female to leave without ovipositing. Sooner or later aggregation of new adults, then briefly visited three the guarding female stepped aside (remaining on other masses during the next 15 days, ovipositing the same leaf) and allowed the other to oviposit in each one; finally she took over guarding a sixth in her egg mass. In other cases guarding females mass from another female, abandoning this mass stepped aside without any sign of aggression to- when the nymphs began to hatch. ward visitors. One such case involved littermates, Rainy season populations of P. disparare prob- but two others involved individuals from different ably relatively philopatric. Eight females marked egg masses. Not enough pairs of known origins as newly moulted adults later guarded or were as- were observed to determine whether related indi- sociated with the same egg mass as probable litter- viduals were less likely to fight. Visiting females mates that were marked in the same aggregation. nearly always oviposited only into relatively young Females found with an egg mass on a given M. egg masses and usually at the edges of the masses; hibiscifolia plant were more likely to be resighted on one exceptional occasion a female oviposited on the same plant after finishing with that mass into one end of a large egg mass while nymphs than were other females (P <0.01 with Chi hatched from the other end. SquaredTest for each of the three plants with suffi- In 17 cases the guard-visitor status was clearly cient data). Resightings of females originally seen determined for each of a pair of females (all fe- with or without eggs on the largest plant were less males were collected after the "visitor" had left likely to occur on other plants than were those the egg mass), and the membracids were dissected. of females originally found on the other plants Comparing numbers of mature and nearly mature (P<0.001 with Chi Squared Test). Most individ- eggs, in two cases the females had similar numbers, uals at the site 75 m from the study site were in- in l Ithe guard had fewer eggs, and in 4 the visitor fested with a red mite which was rare at the study had fewer (P <0.08 with one-tailed Chi Square site (< 5 of 132 individually marked females). Test). Discounting the three cases in which the visi- On the other hand, dispersal from maternal tor had many (>25) mature and nearly mature plants does occur, as 39% of 163 resightings in- 451

Table 2. Results of dissections of ovaries of 63 females

Female's activity Number Average number Average length Amount of body fat (max. 6, min. 1) when dissected mature and nearly 5 largest developing mature eggs eggs in I ovary 1 2 3 4 5 6

Collected Mating 22 2.5 + 6.5 2.7+1.7 7 9 2 3 1 0 Defending egg mass Young eggs 21 9.9 + 7.6 4.2+1.7 0 2 3 5 8 2 Older eggs 6 0.5+0.9 0.6+0.6 0 0 1 0 1 3 Defending nymphs 10 0.8 +1.4 1.9 +0.8 0 4 3 0 0 3 Aggregationsofnewadults 4 0 0.5+0.1 4 0 0 0 0 0

volved females which had moved to a different M. mature" eggs that were apparently degenerating, hibiscifolia plant. One female that matured on one suggesting that egg resorption may be at least par- plant was found >75 m away on an egg mass tially responsible for the reduction in numbers of along with an unmarked female. Only 40% of the mature and nearly mature eggs carried by females 207 females marked as newly matured adults were guarding older masses. Most females found copu- seen after they left the aggregation of new adults lating (18 of 22) had no mature or nearly mature (94% of these females were resighted near an egg eggs and were probably young females that had mass). Rates of disappearanceof guarding females not yet oviposited, but the other four had an aver- were so low that it seems likely that most females age of 13.8 such eggs. The six copulating females that disappeared from aggregations had migrated that were 9-12 days old showed striking intraovary rather than died. differencesin the sizes of developing eggs in differ- The overall pattern of movement seems to be ent ovarioles. The average coefficient of variation that many individuals probably move little or not in egg length was 26%, and in three females the at all, but that some do move relatively long dis- largest developing egg in the ovary was more than tances. This is in accord with the impression that twice as long as the smallest. Thus eggs developed the distribution of P. dispar on M. hibiscifolia asynchronously even before females began to ovi- plants was highly clumped. posit.

6. Ovary contents Discussion Each of a female's two ovaries usually had 14 or 15 ovarioles (x=14.8, range 11 to 17), and the The comparatively ineffective defense of eggs by maximum number of mature or nearly mature eggs P. disparagainst parasitic wasps may have contrib- in each ovariole was 3, giving a maximum capacity uted to the tendency for females of this species of about 90 eggs per female; the most found in to lay their eggs in other females' egg masses. In a single individual was 70. species with effective defense such as Ennya paci- Females from aggregations of new adults and fica (Eberhard, in preparation) and in subsocial those collected while mating near such aggrega- species of other groups (e.g. Eberhard 1973; da tions had larger fat bodies and fewer mature or Souza Dias 1975, 1976) it is clear that oversized nearly mature eggs than those collected while egg masses would be harder to defend. The ineffec- guarding eggs or nymphs (Table 2) (P <0.01 com- tive defense of P. dispar even on small masses re- paring >4 fat bodies with <4 using Chi Squared duces the premium on keeping egg mass size down, Test, and P<0.01 comparing egg numbers with and thus reduces the disadvantage of adding eggs Mann Whitney U-Test). Females found with to already large masses. young egg masses had more mature and nearly Another factor probably associated with the mature eggs than those with older eggs and with of sharing egg masses in this group is nymphs (P<0.001 Mann Whitney U-Test), and the apparent tendency for females not to mature averages of their five largest developing eggs were and lay their entire complement of eggs at once. also larger (P<0.001 Mann Whitney U-Test). Two If only a few eggs are ready at once, the benefits females on young masses had "mature or nearly of guarding them will be smaller. Asynchrony in 452 egg maturation occurs even during the develop- later resighted. Those that were resighted had not ment of a female's first eggs, and females can un- disappearedlater (in terms of nymphal stages) than doubtedly start off their reproductivelives as either those that were not resighted (P>0.1 with Chi visitors or guarders. The presence of mature or Squared Test). The reason for the females' reduced nearly mature eggs in the ovaries of females guard- tendency to guard eggs and nymphs near the end ing egg masses, and the observation of a female of the rainy season is not clear. ovipositing into a mass she had been guarding sug- Oviposition by visitor females may benefit gest that females frequently add eggs to their own guarding females, since later eggs were generally masses. Addition of eggs to a defended mass must laid at the sides and ends of egg masses. Thus the usually occur only during the first few days after original eggs (probably usually those of the guard- a mass is initiated, since the nymphs from smaller ing female) became more centrally placed, and masses usually did not vary in age by more than probably less subject to parasitism by wasps. The one instar. Resorption of unlaid eggs may also oc- guarding female's nymphs may also be less likely cur occasionally, and females guarding older eggs to be singled out by predators such as syrphids and nymphs had very low numbers of ovarian when in larger groups. Thus the interactions be- eggs. tween females near egg masses may be mutualistic. Guarding is a reproductively costly behavior. The line between mutualism and parasitism is fine, Guarding females often experience a several week however, and if a guarding female's expected re- interruption of oviposition, even though they feed productive output is even slightly decreased by the as they guard. Guarding behavior is probably also visitor, the visitor is more appropriately termed costly to females both in terms of exposure to some a parasite. The visiting behavior of P. disparclosely predators and in terms of the energy expended in resembles "egg dumping" that occurs in the lace defensive behavior (Tallamy and Denno 1982). bugs Gargaphiasolani (Tallamy 1985), G. tiliae and Visitor females would seem to be at an advantage G. irridescens(D.W. Tallamy, personal communi- because they do not incur these costs. cation), and probably some other membracids Nevertheless most females do guard at least (T.K. Wood, personal communication). some of their eggs, and many guard their nymphs. It is not clear why guarding females often re- Advantages from defending probably result from sisted the attempts of other females to oviposit; several factors. Defense was relatively effective the additional cost of defending a few more eggs against some enemies of both eggs and nymphs. and nymphs would seem to be so small that the Independent lines of evidence also imply that since cost of aggression would not be compensated; and only limited local female movement occurs, closely as just noted, guarding females may actually bene- related females sometimes guard each others eggs. fit from being visited. The likelihood that a visiting Presumablythe probability of high genetic rela- female was genetically related to the guarding fe- tedness also contributes to the tendency for females male would make such defense even less advanta- to adopt abandoned egg masses. Abandoned egg geous (Hamilton 1964). The lace bug masses have a sharply reduced probability of es- solani very seldom attempts to repel visiting fe- caping , so adoption could confer rela- males in what may be very similar situations (Tal- tively large benefits to the original females, making lamy 1985). It is possible that the defending mem- the cost/benefit relation for the adopter more fa- bracid female mistakenly reacted to visiting fe- vorable (West Eberhard 1975). It seems unlikely males as if they were predators. Another possibility that this behavior is explained by previously depos- is that the defending female's resistence was com- ited eggs somehow mechanically facilitating fur- municatory rather than aggressive, indicating her ther oviposition, as the leaves are quite soft and readiness to remain with the egg mass (probably ovipositing females appeared to have little trouble associated with the relative readiness of other eggs inserting their ovipositors. In fact oviposition in in her ovaries); in groups of close relatives, appro- adopted masses may increase the risk of parasit- priate behavior based on accurate assessment of ism, since one mass had a wasp near it when a both females' projected output of eggs in the near membracid arrived to adopt it, and two other de- future would increase both females' inclusive fit- serted masses had parasitic wasps lingering in the ness. vicinity. All females eventually deserted their offspring. It Acknowledgements.T.K. Wood identified the membracids, is unlikely that many desertions were due to M.E. Schauff the wasp, and J. Gomez Laurito the plants. M.J. the female's death, since of 32 females that de- West-Eberhardand W. Wicslo made helpful comments on the fended a mass until nymphs hatched, 47% were manuscript, T.K. Wood supplied useful information, and the 453

Vicerrectoriade Investigaci6nof the Universidadde Costa Rica Social insects, vol. II. Academic, New York, pp 199- provided financial support. I thank all for their help. 280 Hamilton WD (1964) The genetic evolution of social behavior, I and II. J Theor Biol 7:1-52 Nault LR, Wood TK, Goff AM (1974) Treehopper(Membraci- References dae) alarm peromones. Nature 249:387-388 Tallamy DW (1985) "Egg dumping" in lace bugs (Gargaphia Da Souza Dias BF (1975) Comportamentopre-social de Sinfi- solani, : ). Behav Ecol Sociobiol tas do Brasil Central I. Themosolfersii (Klug) (Hymenop- 17:357-362 tera, Argiidae). Studia Entomol 18:401-432 Tallamy DW, Denno RF (1982) Life history trade-offs in Gar- Da Souza Dias BF (1976) Comportamentopre-social de Sinfi- gaphia solani (Hemiptera: Tingidae): the cost of reproduc- tas do Brasil Central II. Dielocerusdiasi Smith (Hymenop- tion. Ecol 63:616-620 tera, Argiidae). Studia Entomol 19:461-501 Tallamy DW, Wood TK (1986) Convergencepatterns in subso- EberhardWG (1973) The natural history of a subsocial penta- cial insects. Ann Rev Entomol 31:369-390 tomid bug and two scelionid wasps: strategy and counter- West Eberhard MJ (1975) The evolution of social behavior strategy in a host and its parasites. Smithson Contrib Zool by kin selection. Quart Rev Biol 50:1-33 205:1-39 Wilson EO (1971) The societies. Harvard University Eickwort GW (1981) Presocial insects. In: Hermann HR (ed) Press, Cambridge,pp 548