Predatory behavior of Pseudodorus clavatus (Diptera, Syrphidae) on aphids tended by ants

Predatory behavior of Pseudodorus clavatus (Diptera, Syrphidae) on aphids tended by ants

Alexandra Bächtold^I; Kleber Del-Claro^II

^IFaculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo. Avenida Bandeirantes, 3900, Monte Alegre, 14040–901 Ribeirão Preto-SP, Brasil. [e-mail]

^IIInstituto de Biologia, Universidade Federal de Uberlândia. Campus Umuarama, CP. 593, 38400–920 Uberlândia-MG, Brasil. [e-mail]

ABSTRACT

Predatory behavior of Pseudodorus clavatus (Diptera, Syrphidae) on aphids tended by ants. In this study, we examined the interactions between myrmecophilous aphids, their ant-guards and a predatory syrphid species, Pseudodorus clavatus (F.). Larvae of this predator were found in the colonies of three aphid species: Aphis gossypii, A. spiraecola and Toxoptera sp., which were tended by eight ant species, especially Camponotus. Hoverfly larvae managed to infiltrate the aphid colonies and consume nymphs. Predator larvae exhibited inconspicuous movements and were not detected by ants which were commonly observed touching and antennating the larvae they come into contact. These results suggest that behavioral and chemical cues are involved in the infiltration and on the successful predation of syrphids upon aphids.

Keywords: Cerrado; myrmecophilous aphids; predation; syrphid.

Ants are well known for their mutualistic associations with trophobiont insects, especially hemipterans. These interactions are beneficial for both species involved, as ants receive honeydew and in turn, protect the trophobiont herbivore against predators and parasitoids (Del-Claro & Oliveira 2000; Stadler & Dixon 2008). In the case of aphids, ants protect them from a wide range of natural enemies including coccinelids, lacewings, midges, spiders, parasitoids and hoverflies (see in Almohamad et al. 2008). Hoverflies (Diptera, Syrphidae) are mostly aphidophagous (Gilbert et al. 1994) and good models in studies of top-down forces (Dziock 2005). Although aphid-hoverfly interactions have been addressed in many studies, especially concerning oviposition patterns and biological control (Sadeghi & Gilbert 2000; Almohamad et al. 2009; Bergh & Short 2008), little is known about the relationships between myrmecophilous aphids, their associated tending ants and predatory hoverflies (Renault et al. 2005). The hoverfly Pseudodorus clavatus (Fabricius, 1794) is widespread in South America and is an important natural enemy of several aphids (Auad 2003). This species was recently observed in Struthanthus polyanthus Martius (Loranthaceae), in aphid colonies tended by ants. In this context, the aim of this study was to examine the interaction among P. clavatus, aphid species and tending ants, as well to detail the predatory behavior of this hoverfly on myrmecophilous aphids in a neotropical savanna. The Cerrado biome is a global hotspot which supports high levels of diversity of fauna and flora, but so far little is still known about the underlying mechanisms controlling and affecting insect-plant and insect-insect interactions (Del-Claro & Torezan-Silingardi 2009). In the present study we then examined i) possible antagonistic interactions between P. clavatus and ants (attack or predation); and ii) whether hoverflies showed defenses against ant contact or attack.

Fieldwork was conducted in September 2012 in a cerrado savanna reserve in Uberlandia, Brazil (400 ha; 18°59'S, 48°18'W). In the cerrado, S. polyanthus is a generalist hemiparasitic plant, occurring in association with several hosts (e.g., Kielmeyera coriacea Martius, Pouteria ramiûora (Martius) Radlkofer and Styrax ferrugineus Nees et Martius) (Arruda et al. 2006). We initially search the aphids in 70 individuals of S. polyanthus, but these insects were found in 16 plants only (22.85%). These 16 individuals of S. polyanthus were then tagged and observations of hoverfly-aphid-ant interactions were performed on three occasions: September 10, 18 and 28. Aphid aggregations were defined as colonies per inflorescence (sensu Yao & Akimoto 2009). The observations of hoverfly-aphid-ant interactions were performed in 15 min weekly sessions for each plant (sensu Völk 1995). Observations were performed ad libitum in the morning (08:00h to 12:00h) of sunny days. In order to investigate the aphid-ant-hoverfly interactions, in each observation session we carefully examined the behavior of each species involved, especially hoverflies. We were particularly interested in determining whether i) syrphids attack aphids tended by ants and ii) ants would notice presence of syrphids and attack them. At the end of the study, insects (ants, aphids and hoverflies) were collected for identification.

Pseudodorus clavatus was found in colonies of three aphid species: Aphis gossypii Glover, 1877, A. spiraecola Patch, 1914 and Toxoptera sp. All these aphid species were attended by ants. Pseudodorus clavatus was found in 92.3% (n = 12) of ant-aphid associations (Table I). No overlap among ant species in a given aphid colony was observed. Camponotus was the most diverse (four species) and frequent ant genus in S. polyanthus (in 12 of 16 plants with aphids). For instance, C. crassus was present in 50% of plants with aphids (n = 8), whereas Brachymyrmex sp. was observed in only 6% of plants with aphids (n = 1). When aphid colonies were small (< 10 nymphs), tending ants usually abandoned the aphids for a while to forage on the plant. On these occasions, P. clavatus larvae were observed to move towards aphids, infiltrate the colonies (n = 6 observations) and prey upon unattended nymphs. Only nymphs were attended by ants regardless of aphid colony size, small or large. Three from six observations resulted in predation. When aphid colonies were large (> 20 nymphs), ants tended aphids for longer periods. In these cases, infiltrated hoverfly larvae remained motionless (n = 10 observations), but ants were commonly observed antennating their bodies. Antennation on larvae of P. clavatus was performed by C. blandus (n = 4 observations), C. crassus (n = 4), C. trapeziceps (n = 1) and Crematogaster bruchi (n = 1) (see C. crassus in Fig. 1). Nymphs attacked by P. clavatus remained immobile and no reaction was observed from the neighboring nymphs in the colony. Ants were also not observed to interrupt the feeding activity of hoverflies. The predatory behavior of P. clavatus towards aphids was recorded in the following associations: A. gossypii tended by C. blandus (n = 1 record); Toxoptera sp. tended by C. crassus (n = 1); A. spiraecola tended by C. blandus (n = 1). For the other hoverfly-aphid-ant associations (Table I), aphids were not observed to be preyed upon by P. clavatus. Among all the syrphids observed (n = 16) co-occurring with aphids, 62.5% (n = 10 larvae) of them were antennated by ants whenever they approached the aphid colonies. These larvae were infiltrated in colonies of the three aphid species: six larvae associated with A. spiraecola, three with A. gossypii and one with Toxoptera sp.

Some aphid predators can forage in myrmecophilous aphid colonies without being attacked, presumably because they use specific behavior and chemical camouflage (e.g.Völkl 1995; Del-Claro & Oliveira 2000). Syrphus ribesii (Linnaeus, 1758) is an example of hoverfly that presents chemical camouflage similar to its aphid prey (Lohmann et al. 2006). In our study, we recorded P. clavatus infiltrating and preying on myrmecophilous aphids tended by aggressive ant-guards. The hoverfly exhibited similar behavior to the aphidophagous coccinellid Platynaspis luteorubra (Goeze, 1777) (Völkl 1995). Larvae of both species present inconspicuous movements on ant presence that may help to prevent visual detection by ants. Although chemical analyses are necessary to confirm the chemical camouflage by larvae of P. clavatus, we suggest that chemical cues are probably involved in predatory behavior of this hoverfly since its larvae were not attacked by ants which were commonly observed antennating their bodies. According to Sadeghi and Gilbert (2000), studies concerning the adap–tations of syrphids to aphid defenses, especially myr–me–cophilous species, are fundamental for a better understanding of the evolution of Syrphidae. In this sense, our study contributes with information about the behavior of a common aphidopha–gous syrphid and its myrmecophilous preys, and consequently can aid the implementation of biological control strategies, since many aphids are crop pests.

ACKNOWLEDGEMENTS

We are grateful to the Clube de Caça e Pesca Itororó de Uberlândia for permission to work in their cerrado areas, and to Estevão Alves-Silva for valuable comments on the manuscript. We also thank Alexander Machado Auad for syrphid identification, Marcus Vinícius Sampaio for aphid identification and Denise Lange for ant identification. This study was supported by Fapesp (A. Bächtold) and CNPq (K. Del-Claro).

Received 10 July 2013

Accepted 20 September 2013

Associate Editor: Gustavo Graciolli

• Almohamad, R., Verheggen, F.J., Francis, F., Hance, T. & Haubruge, E. 2008. Discrimination of parasitized aphids by a hoverfly predator: Effect on larval performance, foraging and oviposition behavior. Entomologia Experimentalis et Applicata 128: 7380.
• Almohamad, R., Verheggen, F.J. & Haubruge, E. 2009. Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review. Biotechnology, Agronomy, Society and Environment 13: 467481.
• Arruda, R., Carvalho, L.N., Del-Claro, K. 2006. Host specificity of Brazilian mistletoe, Struthanthus aff. polyanthus (Loranthaceae), in cerrado tropical savanna. Flora 201: 127134.
• Auad, A.M. 2003. Aspectos biológicos dos estágios imaturos de Pseudodorus clavatus (Fabricius) (Diptera: Syrphidae) alimentados com Schizaphis graminum (Rondani) (Hemiptera: Aphididae) em diferentes temperaturas. Neotropical Entomology 32: 475480.
• Bergh, J.C. & Short, B.D. 2008. Ecological and life-history notes on syrphid predators of woolly apple aphid in Virginia, with emphasis on Heringia calcarata BioControl 53: 773786.
• Del-Claro, K. & Oliveira, P.S. 2000. Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124: 156165.
• Del-Claro, K. & Torezan-Silingardi, H.M. 2009. Insect-plant interactions: new pathways to a better comprehension of ecological communities in Neotropical savannas. Neotropical Entomology 38: 159164.
• Dziock, F. 2005. Evolution of prey specialization in aphidophagous syrphids of the genera Melanostoma and Platycheirus (Diptera: Syrphidae). 1. Body size, development and prey traits. European Journal of Entomology 102: 413421.
• Gilbert, F., Rotheray, G., Emerson, P. & Zafar, R. 1994. The evolution of feeding strategies, p. 323343. In: Eggleton, P. & Vane-Wright, R.I. (eds). Phylogenetics and Ecology Linnaean Society Symposium Series 17, London, Academic Press, 376 p.
• Lohman, D.J., Liao, Q. & Pierce, N.E. 2006. Convergence of chemical mimicry in a guild of aphid predators. Ecological Entomology 31: 4151.
• Renault, C.K., Buffa, L.M. & Delfino, M.A. 2005. An aphid-ant interaction: effects on different trophic levels. Ecological Research 20: 7174
• Sadeghi, H. & Gilbert, F. 2000. Aphid suitability and its relationship to oviposition preference in predatory hoverflies. Journal of Animal Ecology 69: 771784.
• Stadler, B. & Dixon, A.F.G. 2008. Mutualism: ants and their insect partners Cambridge, Cambridge University Press, viii+219 p.
• Völkl, W. 1995. Behavioral and morphological adaptations of the coccinellid Platynaspis luteorubra for exploiting ant-attended resources (Coleoptera: Coccinellidae). Journal of Insect Behavior 8: 653670.
• Yao, I. & Akimoto, S.I. 2009. Seasonal changes in the genetic structure of an aphid-ant mutualism as revealed using microsatellite analysis of the aphid Tuberculatus quercicola and the ant Formica yessensis Journal of Insect Science 9: 118.

Publication Dates

• Publication in this collection
  03 Dec 2013
• Date of issue
  Dec 2013

History

• Received
  10 July 2013
• Accepted
  20 Sept 2013