Deborah K. Letourneau and Jae C. Choe.
Homopteran attendance by wasps and ants: the stochastic nature of interactions.
Psyche 94:81-92, 1987.

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HOMOPTERAN ATTENDANCE BY WASPS AND ANTS: THE STOCHASTIC NATURE OF INTERACTIONS
BY DEBORAH K. LETOURNEAU~ AND JAE C. CHOE~ Associations of Hymenoptera with Homoptera have intrigued ecologists and evolutionary biologists as model systems of mutual- ism. The extensive body of literature, however, tends to be skewed to the interactions between ants and homopteran trophobionts in the Aphidae or Coccoidea (e.g., Kloft et al. 1965, Nixon 1951, Way 1963, Wilson 1971). In the following account we document a web of multispecies interactions within and between trophic levels, in- volving a species of wasp, several species of ants, and two species of Hornoptera. This account is unique in the literature on Hymenoptera-Homoptera associations because it (1) addresses observable interference between hymenopteran attendants, (2) reports behavioral preference by homopterans for certain hymenop- teran attendants, and (3) describes an interaction between a polis- tine wasp and an aetalionid planthopper. In addition, this study has general implications about the quality of diffuse and multiple asso- ciations between Homoptera and their honeydew foragers. Ten aggregations of feeding Aconophora ferruginea Fowler (Homoptera: Mernbracidae) and four of Aetalion reticulaturn (L.) (Hornoptera: Aetalionidae) were located in the tropical wet forest along the Quebrada Camaronal at La Sirena, Parque Nacional de Corcovado, Osa Peninsula, Costa Rica. Both species of Homoptera are common in Costa Rica, ranging from Mexico and from Costa Rica to Brazil, respectively, and possessing wide ranges of host plants (Ballou 1935, 1936, Wood 1984). They are generally sessile, mating and depositing egg masses at the feeding site (Wood 1984). 'Board of Environmental Studies, 407 Kerr Hall, University of California, Santa Cruz, California 95064.
2The Biological Laboratories, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Mass. 02138 Manuscript received by the editor February 3, 1987. Pachc Ìö4:BI-(1 (1987). hup Yipsychc einclub orgÌö4f94-08i.htni



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82 Psyche [VOL 94
Parachartergus fraternus (Gribodo) (Hymenoptera: Vespidae), a major diurnal attendant, occurs from Costa Rica to Argentina and commonly nests on trees and saplings (Fig. la) near streams or swamps (Richards 1978). Six species of formicine and one species of myrmicine ants were also recorded among the hymenopteran attendants.
Behavioral observations were made during 15-1 8 August 1984 for approximately 18 hours in daylight, six at dawn or dusk, and three at night. Parachartergus fraternus attendants were marked to determine if the same individuals returned to the same groups of Homoptera. An extended anal tube of aetalionids allowed inspec- tion of honeydew delivery to individual attendants. We noted the size class of droplets, and recorded the number of droplets per feeding bout and length of feeding bout for three major attendants. Common attendant Hymenoptera and Homoptera were collected for identification, and voucher specimens were deposited at the Museum of Comparative Zoology, Harvard University. Two aggregations of A. ferruginea and two of A. reticulatum were tended by P. fraternus during daylight hours (Fig. 1 b, c). Of 14 homopteran aggregations, 13 were visited by two or more species of ants. These ant species included Camponotus abdominalis (F.), C. novogranadensis Mayr, C. sexguttatus (F.), C. simillimus (F. Sm.), two unidentified Camponotus spp., Zacryptocerus porrasi (Wheeler), and a few other unidentified occasional species. One male-female pair of A. reticulatum was not tended during our observation period. All homopteran aggregations except one were feeding on Piper auritum Kunth, a common plant of forest edges and disturbed sites in moist regions from Mexico to Columbia (Burger 1971). One aggregation of A. reticulatum was found on balsa, Ochroma lagopus Swartz var. bicolor (Rowlee) Standl. & Steyermark.
The most explicit forms of ownership behavior (sensu Brown 1976) were displayed by P. fraternus, which tended throughout the daylight hours. During our observation period, the same individual wasps returned to the same homopteran aggregations shortly after dawn and remained there until dusk except for several short (less than 10 minutes each) breaks. The wasps constantly antennated and



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19871 Leiourneau & Choe- Wasps and ants 83 3




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84 Psyche [vo~. 94
actively herded the homopterans. Whenever an aetalionid moved away from the feeding group, the wasp quickly flew over the aetali- onid and assumed a stiff posture with stilt legs and elevated wings (N = 12). The wasp sometimes buzzed its wings and the aetalionid soon returned to its own group. The same type of behavior was observed in the wasp when attending membracid nymphs. Parachartergus fraternus responded to any approaching animals, including ants, conspecific wasps, anole lizards, and even humans. The typical display involved a combination of the following behaviors: positioning antennae low to the dorsum, extending wings laterally, buzzing wings, chasing, making stinging movements, or biting. These activities appeared to be successful in preventing most ants from soliciting honeydew from the homopterans. On one occa- sion, a wasp flew at an approaching myrmicine ant and actually knocked it off the branch. Workers of C. sexguttatus were observed frequently (on average once every 20 seconds during three six- minute periods) to descend the branch and petiole to a point approximately 5 cm from the wasp-tended homopteran aggrega- tion, but the mere presence of P. fraternus seemed to deter the ants from approaching closer. Unlike P. fraternus, most attendant ant species did not actively interfere with other approaching ants. One exception was C. abdominalis, the major nocturnal attendant, which pursued and disrupted any approaching ant of a different species.
Ants tended in groups of two or three, whereas P. fraternus always tended alone. P. fraternus also tended much larger groups of A. reticulaturn (19 and 25 individuals) than did ants (1 and 3 indi- viduals). For smaller membracids, however, there was no such trend; ants managed to tend groups of four to 24 individuals, while P. fraternus tended 12 and 13 nymphs. In wasp-tended aggrega- tions, when a wasp was momentarily absent, ants were often quick to move in and collect honeydew. Upon the return of the wasp, however, ants always retreated.
A specialized anal tube of A. reticulaturn enabled us to assess honeydew delivery. In response to vigorous antennation on the dor- sal tip of the abdomen by wasps or ants, aetalionids protruded the anal tube and secreted droplets of honeydew often at a high rate. We counted up to 34 consecutive droplets taken from an adult aetalio- nid during a single feeding bout by P. fraternus. Aetalionid



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19871 Letourneau & Choe- Wasps and ants 85 nymphs also produced honeydew, but presented droplets on the dorsal surface about 2 mm from the tip of the abdomen. It appeared that nymphs did not have fully developed tubes. Aetalion reticulatum appeared to discriminate between attend- ants. The mean number of droplets per feeding bout was signifi- cantly higher (Kruskal-Wallis test: p < 0.001) when P. fraternus was soliciting than when either C. abdominalis, the major nocturnal tender, or Z. porrasi were tending (Table 1). The size of droplets from the same adults was consistently larger (about twice in diame- ter) when P. fraternus was tending. Duration of feeding bouts, how- ever, did not differ (Table l). In the presence of P. fraternus, aetalionids commonly raised a pair of legs nearest an approaching ant, kicked at it, and prevented it from collecting honeydew. Thus A. reticulatum appeared to play an active role in selecting an attendant.
Associations of Hymenoptera with Homoptera cover the entire range of interaction categories including predation (e.g., Evans 1968, Hook 1981), parasitism, mutualism, commensalism, and behavioral combinations such as mutualism-predation (Pontin 1958) and parasitism-predation (Gerling 1966). It is well known that wasps and bees, like ants, depend upon homopterans as sources of carbohydrates (Evans and West Eberhard 1970, Spradbery 1973); however, the behaviors associated with honeydew collection in wasps and bees have not been reviewed.
Our literature survey and field study revealed that bees and wasps exhibit nearly as great a range of interactions as do ant associates. Honeydew foraging of bees and wasps involves various types of behavior ranging from little or no contact with Homoptera to dis- plays of active herding and guarding (Table 2). Unlike some ants (e.g., Maschwitz and Hanel 1985), however, no bees or wasps have been observed to move homopterans to favorable feeding sites. At least eight species of Trigona bees and ten species of polistine wasps are now known to tend and collect honeydew from various Homop- tera. It is interesting to note that all hymenopteran species known to collect honeydew directly from Homoptera are meliponine bees and polistine wasps. Other social hymenopterans such as honey bees, bumble bees, and vespine wasps have been observed only to obtain



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86 Psyche [vo~. 94
Table 1.
Honeydew excretion rates of Aetalion reticulatum when solicited by three species of Hymenoptera.
Soliciting Hymenoptera Drops per bout Length of bout (size, mm) N (mean å SD) (mean + SD, seconds) Formicidae
Z. porrasi 20 2.7 + 2.0 11.3 k 10.0
(3.5)
C. abdominalis 7 3.4k1.0 10.6 + 4.5
(6.0)
Vespidae
P. fraternus 22 8.6 k 6.5 13.1 k 8.9
(12.9)
honeydew by gleaning foliage near feeding homopterans. Further- more, all studies, except for Polistes fuscatus (Barrows 1979), have been reported from tropical areas. Distinct ownership behavior has been recorded from only a few species.
Our observations on two homopteran species and their complex of hymenopteran attendants, together with those of other workers, add several facts regarding the nature of mutualism between these two groups. First, the association between Homoptera and their hymenopteran attendants is highly stochastic and often involves a multispecies complex. Most studies have focussed on a single hyme- nopteran species (e.g., Fritz 1982, Messina 1981), but several workers (e.g., Addicott 1979, Bradley and Hinks 1968, Bristow 1984, O'Neill and Robinson 1977) have now investigated commu- nity aspects of the relationship. An individual Homoptera may host several species of Hymenoptera during its lifetime. For instance, A. reticulaturn has been observed to be tended by Trigona arnalthea and T. spinipes along with a variety of ant species in Brazil (Brown 1976, Castro 1975, Cockerel1 1920). Brown (1976) studied hymenop- teran attendance of A. reticulaturn on the Osa Peninsula, not far from our study site, and found a completely different complex of attendant species with die1 shifts. An attendant hymenopteran spe- cies may also associate with more than one species of Homoptera. Trigona arnalthea is known to tend A. reticulaturn and at least two species of membracids (Cockerel1 1920, Salt 1929, Schuster 1981). Our study also reports that P. fraternus readily associates with both A. reticulaturn and A. ferruginea. Elements of chance due to nest distribution and nutritional need of hymenopteran attendants, and



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19871 Letourneau & Choe- Wasps and ants 87 Table 2.
Activities of bees and wasps as honeydew foragers. Gleans honeydew from foliage near feeding homopterans Apidae
Apinae (Apini)
Apis mellifera
Bloc et al. 1984, Kunkel & Kloft 1977,
Prabucki 1972, Santas 1983
Bombinae
Bombus bifarius
Wagner & Cameron 1985
Vespidae
Vespinae
Vespa orientalis
Ikan & Ishay 1966
Vespula spp.
Duncan 1939, Evans & West Eberhard 1970
Obtains honeydew directly from feeding homopterans Apidae
Apinae (Meliponini)
Trigona amalthea
Trigonu cagafogo
Trigonal corvina
Trigona cupira
Trigona hyalinata branneri
Trigona spinipes*
Trigona tataira*
Trigona sp.
Vespidae
Polistinae
Polistes fuscatus*
Parachartergus apicalis
Parachartergus fraternus*
Parachartergus richardsi*
Mischocyttarus drewseni
Stelopolybia testacea
Pseudopolybia compressa
Pseudopolybia vespiceps
Polybia sp.
Cockerel1 1920, Salt 1929, Schuster 198 1 Miiller 1873, 1874
Jiron P. & Salas D. 1975
Silvestri 1902
Laroca & Sakakibara 1976
Castro 1975
Cortopassi-Laurino 1977
Wood 1984
Barrows 1979
Williams 1928, Wood 1984
This study
Schremmer 1978
Jeanne 1972
Jeanne 1972
Brown 1976, Wood 1984
Jeanne 1972
Jiron P. & Salas D. 1975
Belt 1874
Brachysastra sp.*
*Distinct ownership behavior has been observed. habitat heterogeneity may play a large role in determining the part- nership. Recently, Law and Koptur (1986) provided an elegant theoretical argument supporting the evolution of non-specificity in mutualistic interactions.




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88 Psyche [vo~. 94
Second hymenopteran attendants differ in tenacity of attendance. Components of these differences include fidelity and constancy of attendance, foraging strategy, and temporal activity pattern. Para- chartergus fraternus showed high fidelity during our observation period, i.e., the same individuals tended the same homopteran groups. Similar behavior is known for Polistes fuscatus (Barrows 1979). In general, wasps tend to forage as individuals (Barrows 1979, Schremmer 1978, and this study), whereas social bees, like ants, more often recruit (Cortopassi-Laurino 1977, Schuster 1981). Both wasps and bees remain with homopterans for long periods interrupted only by short forays to the nest. Honeydew foraging activities of wasps and bees are always diurnal (Schremmer 1978 and this study).
Third, hymenopteran attendants also differ in quality. It is now well established that hymenopteran attendance enhances the fitness of homopterans (Bristow 1984, Fritz 1982). However, the quality of hymenopteran services varies widely in terms of the effectiveness of sanitation, enhancement of growth rate, and defense. At least in a few studies with ants and aphids (Banks and Nixon 1958, El-Ziady 1960), rapid rate of honeydew excretion indicates an increased rate of assimilation of essential nutrients, higher growth rate, and higher fecundity in homopterans. In our study, sanitation was maintained by most attendants, but wasp attendance could potentially increase the fitness of homopterans through providing better defense and enhancing growth rates. Jiron P. and Salas D. (1975), on the other hand, report no evidence that the presence of bees and wasps deter scale predators but observe benefits due to site sanitation. Bombus bifarius may not enhance aphid growth rates, but its leaf-gleaning activities can disrupt potential enemies (Wagner and Cameron 1985).
Fourth, homopterans may show preference for certain attend- ants. Benefits to homopterans from hymenopteran attendants may not be equal and certain Homoptera-Hymenoptera associations may be favored (Addicott 1979, Bristow 1984, Messina 1981). In this study, we documented differential responses of A. reticulaturn to various hymenopteran attendants. In the presence of P. fraternus, aetalionids behaved defensively and provided little, if any, honey- dew to soliciting ants. Furthermore, under wasp solicitation, aetali- onids produced significantly larger quantities of honeydew. This



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19871 Letourneau & Choe- Wasps and ants 89 behavioral plasticity may be adaptive under conditions of variable tender quality. It may also play an important role in mediating competitive interactions within mutualistic systems. A web of multispecies interactions involving a planthopper, Aetalion reticulaturn, and a membracid, Aconophora ferruginea, and their hymenopteran attendants were studied in Costa Rica. A wasp, Parachartergus fraternus, tended both species of Homoptera diurnally and prevented other Hymenoptera from obtaining honey- dew. Carnponotus abdominalis, a major nocturnal attendant, also showed a similar degree of "owners hip" behavior. Other ant species, however, appeared to be opportunistic. Although associations were highly stochastic with regard to partnership, A. reticulaturn showed a clear preference for P. fraternus over ant attendants. It provided significantly more honeydew to P. fraternus and in the presence of P. fraternus it behaved antagonistically toward any ants. The litera- ture on associations of Homoptera with wasps and bees is also reviewed.
We thank the Servicio de Parques Nacionales of Costa Rica and the Organization for Tropical Studies (OTS) for making our study in Parque Nacional de Corcovado possible. We are grateful to R. R. Snelling for identifying the Hymenoptera and to T. K. Wood for identifying the Homoptera. P. H. Adler, C. B. Bristow, J. Carpen- ter, B. Holldobler, S. Koptur, D. L. Perlman, and E. 0. Wilson have provided important suggestions for improving earlier drafts. JCC was supported by the Richmond Fund of Harvard University. ADDICOTT, J. F. 1979. A multi-species aphid-ant association: density dependence and species-specific effects. Can. J. Zool. 57: 558-569. BALLOU, C. H.
1935. Insect notes from Costa Rica in 1934. Bull. Ins. Pest Surv. 15: 163-212.
BALLOU, C. H. 1936.
Insect notes from Costa Rica in 1935. Bull. Ins. Pest Surv. 16: 437-497.
BANKS, C. J. AND H. L. NIXON. 1958.
Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. J. Exp. Biol. 35: 703-7 1 1.




================================================================================

90 Psyche pol. 94
BARROWS, E. M. 1979. Polistes wasps (Hymenoptera: Vespidae) show interfer- ence competition with other insects for Kermes scale insects (Homoptera: Ker- mesidae) secretions. Proc. Entomol. Soc. Wash. 81: 570-575. BELT, T.
1874. The Naturalist in Nicaragua. John Murray, London. 403 pp. BLOC, A., P. THIEVENT, AND H. MONTAGNER. 1984. Etude preliminaire de la
dynamique des populations d'un puceron producteur de miellat: Cinarapectina- tae Nordl. (Hornoptera-Lachnidae) dans Le Doubs. relation avec la pluviome- trie. Apidologie 15: 11-22.
BRADLEY, G. A. AND J. D. HINKS.
1968.
Ants, aphids, and jack pine in Manitoba. Can. Entomol. 100: 40-50.
BRISTOW, C. M.
1984. Differential benefits from ant attendance to two species of Homoptera on New York ironweed. J. Anim. Ecol . 53: 715-726. BROWN, R. L. 1976. Behavioral observations on Aethalion reticulatum (Hem., Aethalionidae) and associated ants. Ins. Soc. 23: 99-107. BURGER, W. 1971. Flora Costaricencis. Fieldiana Botany 35: 1-227. CASTRO, P. R. C.
1975. Mutualism entre Trigona spinipes (Fabricius 1793) e Aethalion reticulatum (L. 1767) em Cajanus indicus Spreng. na presenca de Camponotus spp. Ciencia e Cultura 27: 537-539. COCKERELL, T. D. A. 1920.
Some tropical meliponid bees. Bull. Amer. Mus. Nat. Hist. 42: 459-468.
CORTOPASSI-LAURINO, M. 1977. Notas sobre associacoes de Trigona (Oxytri- gona) tataira (Aphidae, Meliponinae). Bolm. Zool. Univ. Sao Paulo 2: 183- 187. DUNCAN, C. D. 1939.
A contribution to the biology of North American vespine wasps. Stanford Univ. Pub. Biol. Sci. 8: 1-272. EL-ZIADY, S. 1960.
Further effects of Lasius niger L. on Aphis fabae Scopoli. Proc. Roy. Entomol. Soc. London (A) 35: 30-38. EVANS, H. E.
1968. Notes on some digger wasps that prey upon leafhoppers. Ann. Entomol. Soc. Amer. 61: 1343- 1344.
EVANS, H. E. AND M. J. WEST EBERHARD.
1970. The Wasps. Univ. of Michigan
Press, Ann Arbor, 265 pp.
FRITZ, R. S.
1982. An ant-treehopper mutualism: effects of Formica subsericea on the survival of Vanduzea arquata. Ecol. Entomol. 7: 267-276. GERLING, D.
1966.
Biological studies on Encarsia formosa. Ann. Entomol. Soc. Arner. 59: 142-143.
HOOK, A. 1981. Nesting biology of Tanyoprymnus moneduloides and Ammato- mus icarioides. Ann. Entomol. Soc. Amer. 74: 409-41 1. IKAN, R. AND J. ISHAY. 1966.
Larval wasp secretions and honeydew of the aphids, Chaitophorus populi, feeding on Populus euphratica as sources of sugars in the diet of the oriental hornet, Vespa orientalis F. Israel J. Zool. 15: 64-68. JEANNE, R. L.
1972. Social biology of the neotropical wasp Mischocyttarus drew- seni. Bull. Mus. Comp. Zool. 144: 63-150. JIRON P., L. F. AND S. SALAS D. 1975. Simbiosis entre "cochinillas de cola" (Coccoidea: Margarodidae) y otros insectos. I. Los componentes del sistema simbiotico en la tierra alta de Costa Rica. Brenesia 5: 67-71. KLOFT, W., A. MAURIZIO, AND W. KAESER. 1965. Das Waldhonigbuch. Ehren- wirth Verlag Munchen, Munchen.
KUNKEL, W. AND W. KLOFT.
1977.
Fortschritte auf dem Gebiet der Honigtau- Forschung. Apidologie 8: 369-39 1.




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! 9871 Letourneau & Choe- Wasps and ants 91 LAROCA, S. AND A. M. SAKAKIBARA. 1976. Mutualism entre Trigom hyalimia brunneri (Aphidae) e Aconophoruflavtpes (Membracidae). Rev. bras. Ent. 20: 71 -72.
LAW, R. AND S. KOPTUR.
1986.
On the evolution of non-specific mutualism. Biol. J. Linn. Soc. 27: 251-267.
MASCHWITZ, U. AND H. HANEL. 1985. The migrating herdsman Dtilichodems (Diabolus) cuspida~us: an ant with a novel mode of life. Behav. EGO!. Suciobiol. 17: 171-184.
MESSINA, F. J.
1981. Plant protection as a consequence of an ant-membracid mutualism: interactions on goldenrod (Solidago so.). Ecology 62; 1433-1440. M~LLER, H.
1873. Larvae of Membracix serving as milk-cattle to a Brazilian species of honey-bees. Nature 8: 201-202. MULLER, H.
1874. Larvae of Membracis serving as milk-cattle to a Brazilian species of bee. Nature 10: 31-32.
Nixon, G. E, J,
1951. The Association of Ants with Aphids and Coccids. Comm. Inst, Entomol,, London, 36 pp.
O'NEILL, M. C. AND A. G. ROBINSON.
1977. Ant-aphid association in the Prov- ince of Manitoba. Manitoba Entomol. 11: 74-88. FONTIN, A. J.
1958. A preliminary note on the eating of aphids by ants of the genus Lasius. Entomol. Man. Mag. 94: 9-1 1. PBABUCKI, J. 1972, The honeydew-secreting aphid Phyllaphis fugi L. (Homop-