Abstracts

Introduction

The social insects, including ants, bees, wasps and termites, play a part in multiple and important ecological interactions, arousing great scientific interest (Vilela et al. 2008VILELA, E.F., SANTOS, I.A., SCHOEREDER, J.H., SERRÃO, J.E., CAMPOS, L.A.O. & LINO-NETO, J. 2008. Insetos Sociais: da Biologia a Aplicação. Ed. UFV, Viçosa, 441p.). Some neotropical vespids are known to maintain associations with other insect and vertebrate taxa, like birds and bats (Jeanne 1970JEANNE, R.L. 1970. Note on a bat (Phylloderma stenops) preying upon the brood of a social wasp. J. Mamm. 51:624-625. http://dx.doi.org/10.2307/1378408
http://dx.doi.org/10.2307/1378408... , Richards 1971RICHARDS, O.W. 1971. The biology of social wasps (Hymenoptera: Vespidae). Biol. Rev. 46:483-528. http://dx.doi.org/10.1111/j.1469-185X.1971.tb01054.x
http://dx.doi.org/10.1111/j.1469-185X.19... , Wilson 1975WILSON, E.O. 1975. Sociobiology: The New Synthesis, Harvard University Press, Cambridge, 697p., Richards 1978RICHARDS, O.W. 1978. The social wasps of the Americas (excluding the Vespinae). British Museum of Natural History, London, 580p.). Because social wasps often defend their nests by inflicting painful stings or bites, some animals associate with them for protection against potential predators (Carpenter & Marques 2001CARPENTER, J.M. & MARQUES, O.M. 2001. Contribuição ao Estudo dos Vespídeos do Brasil. Universidade Federal da Bahia, Departamento de Fitotecnia. Série Publicações Digitais, v.3, 147p., CD-ROM.).

There are associations among different species of wasps, wherein a less bellicose species tends to be associated with a more aggressive one (Richards 1978RICHARDS, O.W. 1978. The social wasps of the Americas (excluding the Vespinae). British Museum of Natural History, London, 580p.). Polistes e Mischocyttarus, for example, are considered less aggressive, unlike the Polybia wasps (Richards 1978RICHARDS, O.W. 1978. The social wasps of the Americas (excluding the Vespinae). British Museum of Natural History, London, 580p.). In Central America, Polistes carnifex (Fabricius, 1775) has a habit of nesting with Polybia occidentalis (Oliver, 1791) and Mischocyttarus immarginatus Richards, 1940 nests in association with P. occidentalis and P. diguetana Buysson, 1905 (Corn 1972CORN, M.L. 1972. Notes on the biology of Polistes carnifex (Hymenoptera, Vespidae) in Costa Rica and Colombia. Psyche. 79:150-157. http://dx.doi.org/10.1155/1972/78756
http://dx.doi.org/10.1155/1972/78756... , Windsor 1972WINDSOR, D.M. 1972. Nesting association between two neotropical polybiine wasps (Hymenoptera, Vespidae). Biotropica 4:1-3. http://dx.doi.org/10.2307/2989638
http://dx.doi.org/10.2307/2989638... , Gorton 1978GORTON, R.E. 1978. Observations on the nesting behavior of Mischocyttarus immaginatus (Rich) (Vespidae: Hymenoptera) in a dry forest in Costa Rica. Insect. Soc. 25:197-204. http://dx.doi.org/10.1007/BF02224741
http://dx.doi.org/10.1007/BF02224741... , London & Jeanne 1997LONDON, K.B. & JEANNE, R.L. 1997. Site Selection by a Social Wasp in a Nesting Association (Hymenoptera: Vespidae). J. lnsect. Behav. 10:279-288. http://dx.doi.org/10.1007/BF02765560
http://dx.doi.org/10.1007/BF02765560... ). M. immarginatus was also observed in association with Synoeca, Brachygastra and Metapolybia (Starr 1988STARR, C.K. 1988. The nesting association of the wasps Mischocyttarus immarginatus and Polybia spp. in Costa Rica. Biotropica 20:171-173. http://dx.doi.org/10.2307/2388193
http://dx.doi.org/10.2307/2388193... ). Delabie (1990)DELABIE, J.H.C. 1990. The ant problems of Cocoa Farms in Brazil. In Applied Myrmecology: A World perspective. (R.K. Vander Meer, K. Jaffe & A. Cedeno, eds.). Westview Press, Boulder, p.556-569. reported that the aggressive wasps Polistes versicolor (Olivier, 1791) and Agelaia angulata (Fabricius, 1804) were associated with colonies of Azteca species.

Agelaia myrmecophila (Ducke, 1905) and some species of Mischocyttarus build their colonies associated with “ant plants” of the Boraginaceae and Melastomataceae families (Richards 1945RICHARDS, O.W. 1945. A revision of the genus Mischocyttarus Saussure (Hymenoptera, Vespidae). T. Roy. Ent. Soc. London 95:295-462. http://dx.doi.org/10.1111/j.1365-2311.1945.tb00264.x
http://dx.doi.org/10.1111/j.1365-2311.19... , Zikán 1949ZIKÁN, J.F. 1949. O gênero Mischocyttarus Saussure (Hymenoptera, Vespidae), com a descrição de 82 espécies novas. Boletin Parque Nacional do Itatiaia, 251p.). In the Peruvian Amazon, some species of Angiopolybia, Mischocyttarus, Polistes, Polybia and Pseudopolybia nest on “ant plants”, mostly of the genera Maieta and Tococa (Herre et al. 1986HERRE, E.A., WINDSOR, D.M. & FOSTER, R.B. 1986. Nesting associations of wasps and ants on Lowland Peruvian ant-plants. Psyche 93:321-330. http://dx.doi.org/10.1155/1986/94501
http://dx.doi.org/10.1155/1986/94501... ). Several ant species have been found associated with domatia of plant species of the genus Tococa (Melastomataceae) (Bizerril & Vieira 2002BIZERRIL, M.X.A. & VIEIRA, E.M. 2002. Azteca ants as antiherbivores agentes of Tococa formicaria (Melastomatacea) in Brasilian cerrado. Stud. Neotrop. Fauna Environ. 37:145-149. http://dx.doi.org/10.1076/snfe.37.2.145.8585
http://dx.doi.org/10.1076/snfe.37.2.145.... ). The ant Pheidole minutula Mayr, 1878 has an obligate association with Maieta, Cidemia and Tococa (Vasconcelos 1991VASCONCELOS, H. 1991. Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of its ant inhabitants: ant protection against insect herbivores. Oecologia 87:295-298. http://dx.doi.org/10.1007/BF00325269
http://dx.doi.org/10.1007/BF00325269... ). In return for refuge or food, the ants protect their host-plants against herbivores (Davidson & Mckey 1993DAVIDSON, D.W. & McKEY, D. 1993. The evolutionary ecology of symbiotic ant-plant relationship. J. Hym. Res. 2: 13-83., Cabrera & Jaffe 1994CABRERA, M & JAFFE, K. 1994. A trophic mutualism between the myrmecophytic Melastomataceae Tococa guianensis Aublet and an Azteca ant species. Ecotropicos 7:1-10., Bronstein 1998BRONSTEIN, J.L. 1998. The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150-161. http://dx.doi.org/10.1111/j.1744-7429.1998.tb00050.x
http://dx.doi.org/10.1111/j.1744-7429.19... , Vasconcelos & Davidson 2000VASCONCELOS, H. & DAVIDSON, D.W. 2000. Relation between plant size and associates in two Amazonian ant-plants. Biotropica 31:100-111., Alvarez et al. 2001ALVAREZ, G., ARMBRECHT, I., JIMENEZ, E., ARMBRECHT, H. & ULLOA-CHACON, P. 2001. Ant-plant association in two Tococa species from a primary rain forest of Colombian Choco (Hymenoptera: Formicidae). Sociobiology 38: 585-601., Michelangeli 2003MICHELANGELI, F.A. 2003. Ant protection against herbivory in tree species of Tococa (Melastomataceae) occupying different environments. Biotropica 35:181-188.).

Associations among wasps and birds occur in the Neotropics and are easily noticed, but little understood. Usually, these associations are considered commensalism, since the bird benefits, but there is no record of any advantage to wasps (Beier & Tungbani 2006BEIER, P. & TUNGBANI, A.I. 2006. Nesting with the wasp Ropalidia cincta increases nest success of red-cheeked cordonbleu (Uraeginthus bengalus) in Ghana. The Auk 123:1022-1037., Quinn & Ueta 2008QUINN, J.L. & UETA, M. 2008. Protective nesting associations in birds. Ibis 150:146-167. http://dx.doi.org/10.1111/j.1474-919X.2008.00823.x
http://dx.doi.org/10.1111/j.1474-919X.20... ). In Central America, birds commonly nesting in association with wasps build significantly more nests in trees containing Polybia colonies than in trees without this wasp (Joyce 1993JOYCE, F.J. 1993. Nesting success of Rufousnaped Wrens (Campylorhynchus rufi nucha) is greater near wasp nests. Behav. Ecol. Sociobiol. 32:71-77. http://dx.doi.org/10.1007/BF00164038
http://dx.doi.org/10.1007/BF00164038... ). In Southern Brazilian Amazon, nests of Galbula ruficauda Cuvier, 1816 have been found associated with some colonies of Polybia and Apoica (Fry 1972FRY, C.H. 1972. Convergence between jacamars and bee-eaters. Ibis 112:257-259. http://dx.doi.org/10.1111/j.1474-919X.1970.tb00098.x
http://dx.doi.org/10.1111/j.1474-919X.19... ). Campylorhynchus rufinucha (Lesson, 1838) and Uraeginthus bengalus (Linnaeus, 1766) birds have higher reproductive success when they are associated with nests of the social wasps Polybia rejecta (Fabricius 1798) and Ropalida cincta (Lepeletier, 1836), respectively (Joyce 1993JOYCE, F.J. 1993. Nesting success of Rufousnaped Wrens (Campylorhynchus rufi nucha) is greater near wasp nests. Behav. Ecol. Sociobiol. 32:71-77. http://dx.doi.org/10.1007/BF00164038
http://dx.doi.org/10.1007/BF00164038... , Beier & Tungbani 2006BEIER, P. & TUNGBANI, A.I. 2006. Nesting with the wasp Ropalidia cincta increases nest success of red-cheeked cordonbleu (Uraeginthus bengalus) in Ghana. The Auk 123:1022-1037.). In the Peruvian Amazon, nests of the bird Cacicus cela (Linnaeus, 1758) were recorded near social wasps colonies, which provide protection from mammals (primates), snakes and even other birds, decreasing the predation of C. cela eggs and youngs, thus increasing the reproductive success of this species (Robinson 1985ROBINSON, S.K. 1985. Coloniality in the Yellowrumped Cacique as a defense against nest predators. The Auk 102:506-519.).

Most such observations were reported over thirty years ago; since then, few similar studies have been published. The present study is the first to report associations between wasps, ants, and birds in the Central Amazon, with information about behavior, nest locations and photographs for active and abandoned colonies of Polybia rejecta, for one active colony of Synoeca virginea associated with ant nests of Azteca aff. chartifex, and one colony of Polybia rejecta associated with nests of Cacicus cela (Passeriformes: Icteridae).

Material and Methods

1. Study area

The associations were recorded in the Reserva Ducke, situated in the Central Brazilian Amazon. The reserve has a total area of approximately 100 km² of terra firme rainforest, and is located northeast of Manaus, Amazonas, Brazil, at km 26 on the Manaus-Itacoatiara Highway (02° 55′ to 03° 01′ S and 59° 53′ to 59° 59′ W) (Baccaro et al. 2008BACCARO, F.B., DRUCKER, D.P., DO VALE, J., OLIVEIRA, M.L., MAGALHÃES, C., LEPSCH-CUNHA, N. & MAGNUSSON, W.E. 2008. A Reserva Ducke. In Reserva Ducke, a biodiversidade amazônica através de uma grade (M.L. Oliveira, F.B. Baccaro, R. Braga-Neto & W.E. Magnusson, eds.). Editora INPA, 166p.). The climate is humid tropical, with annual relative humidity of about 80% and mean annual rainfall from 1750 to 2500 mm (Ribeiro & Adis 1984RIBEIRO, M.N.G. & ADIS, J. 1984. Local rainfall variability - a potential bias for bioecological studies in the Central Amazon. Acta Amazon. 14:159-174.). The mean annual temperature is 26 °C and there is a little thermal variation during the year (Marques Filho et al. 1981MARQUES FILHO, A.O., RIBEIRO, M.N.G., SANTOS, H.M. & SANTOS, J.M. 1981. Estudos climatológicos da Reserva Florestal Ducke - Manaus - AM. Precipitação. Acta Amazon. 11:759-768.).

2. Collecting technique

The observations were made within a PPBio (Brazilian Program for Biodiversity Research) grid of 5 × 5 km (02° 58′ 893″ S and 059° 57′ 677″ W), as well as along some trails and margins of creeks (igarapés) outside the grid and at camps borders and near the reserve headquarters: main headquarters (02° 55.100′ S and 059° 58.480′ W) and south headquarters (03° 00.460′ S / 059° 56.863′ W). In general, observations were performed by three collectors, from 8:00 AM to 4:00 PM, totaling about 120 hours and approximately 100 km of trails sampled over 16 days (eight days in August and eight in October 2010).

We collected some specimens from nests of wasps and ants, which were identified and deposited in the Zoological Collection of the National Institute for Research in the Amazon (INPA). Nests were photographed in situ using a Sony Cyber-shot DSC-H5 camera, and localities were georeferenced using a GPS.

Results and Discussion

1. Wasps associations with ants

We found five active and one abandoned colony of Polybia rejecta (Fabricius, 1798) and an active colony of Synoeca virginea (Fabricius, 1804), all associated with ant nests of Azteca aff. chartifex Forel, 1896. Two of the P. rejecta colonies were located at the reserve's main headquarters, one in the PPBio grid and three at the south headquarters. The S. virginea colony was at the south headquarters.

The five active colonies of P. rejecta were situated about 10-20 cm from Azteca nests (Figures 1a, b, 2a). Three were built in twigs and leaves of the tree andiroba (Carapa guianensis Aublet - Meliaceae), whereas two nests were built in leaves of the jambeiro (Eugenia malaccensis L. - Myrtaceae). The distance between the abandoned colony of P. rejecta and its adjacent Azteca nest (Figure 2b) was about 15 cm, both built in a unidentified vine.

The same association between P. rejecta nests and ant colonies of unidentified species in the genus Azteca was reported in Southern Brazilian Amazon (Richards 1978RICHARDS, O.W. 1978. The social wasps of the Americas (excluding the Vespinae). British Museum of Natural History, London, 580p.) and in the Mamirauá Sustainable Development Reserve, in Central Brazilian Amazon (Silveira et al. 2008SILVEIRA, O.T., DA COSTA NETO, S.V. & DA SILVEIRA, O.F.M. 2008. Social wasps of two wetland ecosystems in Brazilian Amazonia (Hymenoptera, Vespidae, Polistinae). Acta Amazon. 38:333-344. http://dx.doi.org/10.1590/S0044-59672008000200018
http://dx.doi.org/10.1590/S0044-59672008... ). In the former, two of ten wasp nests found were located in trees with ant colonies. Jeanne (1978)JEANNE, R.L. 1978. Intraspecific nesting associations in the Neotropical social wasps Polybia rejecta (Hymenoptera: Vespidae). Biotropica 10:234-235. http://dx.doi.org/10.2307/2387909
http://dx.doi.org/10.2307/2387909... found 47 nests of P. rejecta in Santarém, in Eastern Brazilian Amazon, mostly near other wasp nests and in some cases associated with Azteca ants.

In the active colonies of P. rejecta observed in this study, any disturbance caused by the collector resulted in aggressive behavior by the wasps. They would fly about 5 m around the colony, inflicting many stings on the collector. The ants, on the other hand, were aggressive only after their colony had been touched by the collector, at which time they quickly recruited large numbers and climbed on to whatever body part of the collector happened to be in contact with the colony, inflicting painful bites.

The colony of the wasp S. virginea was located about 10 cm from an Azteca aff. chartifex nest in an unidentified species of Myrtaceae, and there was a large concentration of ants on the wasp colony envelope (Figures 3a, b). This type of association has been recorded by Ducke (1910)DUCKE, A. 1910. Revision des guêpes sociales poligames d'Amerique. Ann. Hist-Nat. Mus. Natl. Hung. 8:449-544. and Richards (1978)RICHARDS, O.W. 1978. The social wasps of the Americas (excluding the Vespinae). British Museum of Natural History, London, 580p.. The wasps did not show aggressive behavior when their nest was disturbed by the collector; on the contrary, they sought refuge inside their nest. The same pattern was not observed for the Azteca ants, which responded aggressively just as in the cases mentioned above, biting the collector. While the wasps took refuge inside the nest, the ants remained defending the nest, walking in circles, seemingly looking for the cause of the disturbance.

We did not observe ants entering the nests of either wasp species; however, it was common to see them remaining on or near the envelope, usually moving in a circle around the nest surface but not reaching its interior. Furthermore, aggressive behavior was not observed between wasps and ants, which did not seem disturbed by each other's presence.

We hypothesize that one advantage of these associations is the protection given by the ants to the wasps, contributing to the wasps' reproductive success, since ants may repel the approach of predators to the colony. Richards & Richards (1951)RICHARDS, O.W. & RICHARDS, M.J. 1951. Observations on the social wasps of South America (Hymenoptera, Vespidae). T. Roy. Ent. Soc. London 102:1-169. http://dx.doi.org/10.1111/j.1365-2311.1951.tb01241.x
http://dx.doi.org/10.1111/j.1365-2311.19... reported that nesting in association with Azteca ants may be one of the few defense modes found in tropical wasps against attacks by predatory army-ants (Ecitoninae). According to Jeanne (1978)JEANNE, R.L. 1978. Intraspecific nesting associations in the Neotropical social wasps Polybia rejecta (Hymenoptera: Vespidae). Biotropica 10:234-235. http://dx.doi.org/10.2307/2387909
http://dx.doi.org/10.2307/2387909... nest aggregation is common in this kind of wasp. In the presence of ants, wasps receive protection against predators, especially birds and monkeys (Delabie 1990DELABIE, J.H.C. 1990. The ant problems of Cocoa Farms in Brazil. In Applied Myrmecology: A World perspective. (R.K. Vander Meer, K. Jaffe & A. Cedeno, eds.). Westview Press, Boulder, p.556-569.), when they build nests in trees near arboreal ants, particularly Azteca species (Bondar 1939BONDAR, G. 1939. Insetos daninhos e parasitas do cacau na Bahia. I. C. B. B Tecnico, Salvador, n.5, 112p.). Apparently, the wasps take advantage of the ants' tolerance, nesting near their colonies to obtain protection. Considering that no authors to date have proposed a benefit to the ants of the proximity to wasps, it appears that in this case the wasps receive the greater benefit from this association.

2. Wasps Association with birds

Associations among social wasps and birds are often found in nature (Dejean & Fotso 1995DEJEAN, A. & FOTSO, R.C. 1995. Nesting associations of small birds and Polybioides tabidus (Vespidae Epiponinae) in southern Cameroon. Ethol. Ecol. Evol. 7:11-25. http://dx.doi.org/10.1080/08927014.1995.9522967
http://dx.doi.org/10.1080/08927014.1995.... , Beier & Tungbani 2006BEIER, P. & TUNGBANI, A.I. 2006. Nesting with the wasp Ropalidia cincta increases nest success of red-cheeked cordonbleu (Uraeginthus bengalus) in Ghana. The Auk 123:1022-1037.). Much is known about the species of birds that nest near wasp colonies, but little is known about the wasps, which are rarely identified to species. Silveira et al. (2008)SILVEIRA, O.T., DA COSTA NETO, S.V. & DA SILVEIRA, O.F.M. 2008. Social wasps of two wetland ecosystems in Brazilian Amazonia (Hymenoptera, Vespidae, Polistinae). Acta Amazon. 38:333-344. http://dx.doi.org/10.1590/S0044-59672008000200018
http://dx.doi.org/10.1590/S0044-59672008... reported a nest colony of the bird Cacicus cela (Linnaeus, 1758), known as Yellow-rumped Cacique (Passeriformes: Icteridae) close to a Polybia rejecta wasp nest in the Mamirauá Sustainable Development Reserve, in Central Brazilian Amazon and Robinson (1985)ROBINSON, S.K. 1985. Coloniality in the Yellowrumped Cacique as a defense against nest predators. The Auk 102:506-519. reported nests of C. cela in the Peruvian Amazon associated with colonies of the social wasps Agelaia fuscipennis Cameron, 1901 and Chartergus chartarius (Oliver 1791). Robinson (1985)ROBINSON, S.K. 1985. Coloniality in the Yellowrumped Cacique as a defense against nest predators. The Auk 102:506-519. demonstrated that the wasps offer protection to the birds against predation by mammals (mainly primates), serpents and other bird species.

We observed one colony of Polybia rejecta associated with nesting colonies Cacicus cela, the yellow-rumped Cacique, (at the Ducke Reserve main headquarters) (Figures 4a, b). During the 16 days in which we frequented the locality, the wasps did not show any aggressive behavior toward the C. cela or their nests. Later, reserve guards reported that the birds remained there throughout the reproductive season, leaving only after the chicks fledged the nests. Quick field observations and the information reported in the literature suggest that the protection given to birds by wasps is not retributed by the birds, as in a case of commensalism, but more studies are needed, including experimental approaches to unveil the kind of association existing between these groups.

Acknowledgments

We sincerely thank Fernando B. Noll, Elisabeth Franklin, Sérgio H. Borges e Jorge P. Souza for their valuable suggestions on the manuscript; Jacques H.C. Delabie for help identifying the Azteca ants; Marcos Torres, Valdeana Linard, Lucas Marques de Camargos, Vítor Dias Tarli and Paulo da Silva Lopes for help in the field; two anonymous referees for their helpful suggestions; and Pedro Santos and Mario Cohn-Haft for help with the English version.

References

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