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Interactions Between Ghost Ants and Invasive 1474 Florida Entomologist 97(4) December 2014 INTERACTIONS BETWEEN GHOST ANTS AND INVASIVE MEALYBUGS: THE CASE OF TAPINOMA MELANOCEPHALUM (HYMENOPTERA: FORMICIDAE) AND PHENACOCCUS SOLENOPSIS (HEMIPTERA: PSEUDOCOCCIDAE) 1,2, 2 2 2 2 A. M. ZHOU *, G. W. LIANG , L. ZENG , Y. Y. LU AND Y. J. XU 1Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, People’s Republic of China 2Red Imported Fire Ant Research Center, South China Agricultural University, Guangzhou 510642, China *Corresponding author; E-mail: [email protected] ABSTRACT Mutualism between ants and honeydew-producing hemipterans is a common phenomenon in ecosystems, and interactions between ants and hemipterans have been extensively studied. The invasive solenopsis mealybug, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococ- cidae), and the ghost ant, Tapinoma melanocephalum (F.) (Hymenoptera: Formicidae), are widely distributed in China. Previous studies showed that the ghost ant can promote the fitness of the invasive mealybug when natural enemies of the mealybug are excluded. In this study, we investigated the interactions between the ghost ant and the invasive solenopsis mealybug when the mealybug’s natural enemies were included. Our results indicated that the honeydew produced by mealybugs facilitated colony growth of the ghost ant significantly more than by allowing them to feed on the mealworm, Tenebrio molitor L. (Coleoptera: Tenebrioni- dae). Tending by the ghost ant increased mealybug survival on the plants when six-spotted zigzag lady beetle larvae, Cheilomenes sexmaculata (Fabricius) (Coleoptera: Coccinellidae), were present. Both lady beetle adults and the mealybug parasitoid, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), showed strong avoidance responses to ghost ants. The fe- cundity of lady beetle adults and the hatching rate of their eggs were significantly reduced by ghost ants. Also ghost ant tending appeared to negatively affect parasitoid performance. The number of mummified mealybugs onHibiscus rosa-sinensis L. (Malvales: Malvaceae) in the presence of ghost ants was significantly less than the number without ants. Key Words: Aenasius bambawalei, ant-mealybug mutualism, colony growth, Cheilomenes sexmaculata, parasitoid, predator RESUMEN El mutualismo entre hormigas y hemípteros que producen mielcilla es un fenómeno común en los ecosistemas, y las interacciones entre las hormigas y hemípteros han sido ampliamen- te estudiados. La cochinilla invasiva solenopsis, Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), y la hormiga fantasma, Tapinoma melanocephalum (F.) (Hymenoptera: Formicidae), estan ampliamente distribuidas en China. Estudios anteriores mostraron que la hormiga fantasma puede promover el desempeño de la cochinilla invasiva cuando se ex- cluyen los enemigos naturales de la cochinilla. En este estudio, hemos investigado las inte- racciones entre la hormiga fantasma y la cochinilla solenopsis invasiva cuando se incluyeron los enemigos naturales de la cochinilla. Nuestros resultados indican que la mielcilla produ- cida por cochinillas facilitó un crecimiento de las colonias de la hormiga fantasma mas sig- nificativo que permitiendoles alimentarse sobre el gusano de la harina,Tenebrio molitor L. (Coleoptera: Tenebrionidae). El cuidado de las cochinillas por la hormiga fantasma aumento la sobrevivencia de las cochinillas en las plantas cuando las larvas del coccinelido con seis manchas zigzag, Cheilomenes sexmaculata (Fabricius) (Coleoptera: Coccinellidae), estuvie- ron presentes. Tanto los adultos de escarabajos cocinelidos y el parasitoide de la cochinilla, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), mostraron fuertes respuestas de evitación a las hormigas fantasmas. La fecundidad de los adultos del cocinelido y la tasa de eclosión de los huevos se redujeron significativamente por las hormigas fantasmas. También el cuido de las cochinillas por la hormiga fantasma parecía afectar negativamente el des- empeño del parasitoide. El número de las cochinillas momificados en Hibiscus rosa-sinensis L. (Malvales: Malvaceae) en presencia de hormigas fantasma fue significativamente menor que el número sin hormigas. Palabras Clave: Aenasius bambawalei, mutualismo hormiga-cochinilla, crecimiento de colo- nias, Cheilomenes sexmaculata, parasitoides, depredadores Zhou et al.: Interactions between a Ghost Ant and the Solenopsis Mealybug 1475 Interactions between ants and hemipterans both (Zhou et al. 2012a; Zhou et al. 2012b; Zhou et are common and ecologically important (Höll- al. 2013). In China, the distribution of T. melano- dobler 1990; Stadler & Dixon 2005; Styrsky & cephalum is more extensive than that of fire ants, Eubanks 2007). Ants and hemipterans are of- and interactions between T. melanocephalum and ten abundant species that often live in the same mealybugs may produce more profound ecological habitats (Stadler & Dixon 2005); and interactions consequences. However, few studies have investi- commonly occur between them (Helms & Vinson gated the effects of tending by T. melanocephalum 2002; Brightwell & Silverman 2010). Ant-tending on P. solenopsis and its natural enemies. Also, we can promote hemipteran colonies because ant wanted to clarify clear how the T. melanocephalum species protect them from their natural enemies ghost ant benefits from the honeydew produced by (Daane et al. 2007; Powell & Silverman 2010). In P. solenopsis. In this study, we conducted a series of exchange for tending the hemipterans, the ants experiments to examine the effects of P. solenopsis receive large amounts of honeydew in a consum- honeydew on the growth of T. melanocephalum col- er-resource mutualism (Holland et al. 2005). He- onies and the effects of T. melanocephalum -tend- mipteran honeydew contains sugar and various ing on the survival of the mealybugs and their amino acids (Yao & Akimoto 2002; Helms & Vin- natural enemies. son 2008) that can be essential for the ant colony’s growth and survival. MATERIALS AND METHODS The ghost ant, Tapinoma melanocephalum, (F.) (Hymenoptera: Formicidae) is a worldwide Cotton Plants invasive species, whose native range is unknown but is believed to be Africa or Asia (Wheeler Cotton plants (Gossypium spp.; Malvales: Mal- 1910). Ghost ant populations and infestations are vaceae were cultivated in greenhouses in plastic reported in many areas of the United States, as flowerpots (18 cm diam × 17 cm height). Each well as in Canada, Puerto Rico, and the Carib- plant was approximately 25-30 cm in height and bean Islands (Smith & Whitman 1992). Tapino- had 15-20 true leaves. ma melanocephalum forms polygynous colonies that contain huge numbers of workers. Ghost Insects ants show a preference for sweets, sugar, cakes, and syrups. Ghost ant workers frequently tend Colonies of P. solenopsis were collected from a honeydew-producing insects and scavenge for suburb of Guangzhou and fed on cotton. First in- dead insects in fields (Smith 1965). The ghost ant star mealybugs were inoculated on cotton and the is highly adaptable in its nesting habits and has colony was raised for several generations. Cotton been present in China for a long time. plants with established mealybug colonies were The mealybug, Phenacoccus solenopsis, Tins- used for subsequent experiments. Mealybug colo- ley (Hemiptera: Pseudococcidae) is native to the nies were reared in the laboratory at 27 ± 2 °C US (Fuchs et al. 1991) and has spread through- and 60–70% RH and 16:8 h L:D. Twenty colonies out the world including Central America, South of T. melanocephalum ghost ants were collected America, and Africa. It caused serious damage to from the campus of South China Agricultural cotton (Gossypium spp.; Malvales: Malvaceae) in University. Colonies were separated from the soil India and Pakistan in 2005 (Nagrare et al. 2009). by dripping water into plastic boxes containing Currently, it is an important invasive species in soil and ants until the ants floated to the surface south China (Lu et al. 2008), where it is frequent- (Jouvenaz et al. 1977). One T. melanocephalum ly found on Hibiscus rosa-sinensis L. (Malvales: sub-colony (approximately 1.0 g fresh weight of Malvaceae) and cotton. ants) from each colony was weighed out by a mi- Zhou et al. (2012a) showed that tending by crobalance (Sartorius, BS, 224S). Each sub-colony Solenopsis invicta Buren (Hymenoptera: Formi- included one queen, adult workers, pupae, larvae, cidae), had positive impacts on the fitness ofP. and eggs. Each sub-colony was placed in a 9-cm solenopsis mealybug colonies under laboratory plastic Petri dish, which served as an artificial conditions when enemies are absent. However, nest. T. melanocephalum sub-colonies were main- few studies have attempted to determine whether tained with distilled water plus a 10% honey solu- the T. melanocephalum ghost ant also have posi- tion, which was distributed through tubes (1.5 cm tive impacts when enemies are present. Previous diam × 12 cm length) plugged with cotton. studies showed that the invasive fire ant,S. in- The natural enemies of mealybugs, including victa established a close relationship with P. sole- the predatory larvae of the six-spotted zigzag lady nopsis in south China (Zhou et al. 2012a). Fire ants beetle Cheilomenes sexmaculata (F.), (Coleoptera: frequently protect mealybugs from their natural Coccinellidae), and the parasitoid, Aenasius bam- enemies, and honeydew produced by P. solenop- bawalei Hayat
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