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Acta zoológica mexicana

versión On-line ISSN 2448-8445versión impresa ISSN 0065-1737

Acta Zool. Mex vol.34  Xalapa  2018  Epub 12-Nov-2018

http://dx.doi.org/10.21829/azm.2018.3412127 

Notas científicas

Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae), a small but voracious predator of Diaphorina citri Kuwayama (Hemiptera: Liviidae)

Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae), pequeño pero voraz depredador de Diaphorina citri Kuwayama (Hemiptera: Liviidae)

Takumasa Kondo1  * 

Angela María Arcila1 

Laura Isabel Colorado1 

Yenifer Campos-Patiño1 

Paola Sotelo-Cardona1 

1 Corporación Colombiana de Investigación Agropecuaria AGROSAVIA, Centro de Investigación Palmira, Diagonal a la intersección Cra. 36A con Cll. 23, Palmira, Valle del Cauca, Colombia.

Abstract

The effect of predation by the little fire ant Wasmannia auropuntacta (Roger) (Hymenoptera: Formicidae) on Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) kept under experimental conditions for the breeding of the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) was evaluated. An experiment was carried out using cages with capacity for 9 plants of Murraya paniculata (L.) Jack (Rutaceae) infested with an average of 600 nymphs of D. citri and 100 adults of T. radiata per cage. Three cages were exposed to ants and one had no ant exposure (Control). In each cage, the numbers of healthy and parasitized nymphs and the numbers of adults of D. citri and T. radiata were counted every 2 days for 15 days. Exposure to predation by W. auropunctata significantly affected the number of nymphs that reached the adult stage as well as the number of nymphs parasitized by T. radiata (Fisher's exact test). In the ant-exposed cages, about 3% of the nymphs survived to the adult stage in contrast to 18% in the control cage. Likewise, the action of the parasitoid was affected, with 24% of nymphs parasitized in the ant-exposed cages in contrast to 66% in the control cage. Wasmannia auropunctata has a great potential as a natural enemy of this psyllid pest in citrus nurseries. The ant also consumes T. radiata by consuming parasitized nymphs of D. citri and this predation may negatively impact the control of D. citri by the parasitoid.

Resumen

Se evaluó el efecto de depredación de Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae) sobre ninfas de Diaphorina citri Kuwayama (Hemiptera: Liviidae) mantenidas en condiciones experimentales para la cría de Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). Se realizó un ensayo empleando jaulas con capacidad para 9 plantas de Murraya paniculata (L.) Jack (Rutaceae) infestadas con un promedio de 600 ninfas de D. citri y 100 adultos de T. radiata por jaula. Tres jaulas fueron expuestas a las hormigas y una sin exposición (Control). En cada jaula se contabilizó el número de ninfas sanas y parasitadas y el número de adultos de D. citri y T. radiata, cada 2 días durante 15 días. La exposición a la depredación por W. auropunctata afectó de forma significativa el número de ninfas que alcanzaron el estado adulto y el número de ninfas parasitadas por T. radiata (prueba exacta de Fisher). En las jaulas expuestas, cerca del 3% de las ninfas sobrevivieron al estado adulto en contraste con 18% en la jaula control. De igual manera se vio afectada la acción del parasitoide, con un 24% de ninfas parasitadas en las jaulas expuestas en contraste con 66% en la jaula control. Wasmannia auropunctata tiene gran potencial como controlador de esta plaga en viveros de cítricos. La hormiga también consume T. radiata de forma indirecta al consumir ninfas de D. citri parasitadas.

Many ant species have been reported as predators of Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) (e.g., Michaud, 2004), although predation by ants has not been directly observed. In an ant exclusion experiment conducted in Florida (USA), Navarrete et al. (2013) reported that the presence of the ants Pheidole megacephala Fabricius, 1793, Brachymyrmex patagonicus Mayr, 1868, and Solenopsis invicta Buren, 1972, correlated positively with high rates of parasitization by the wasp Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). In that study, Navarrete et al. (2013) did not observe any aggressive behavior of the ants towards D. citri nymphs, and the number of nymphs of D. citri showed no statistical difference between ant-tended and not ant-tended nymphs, suggesting that ants do not feed on D. citri. In a glass house where D. citri is mass reared together with its natural enemy T. radiata, the little fire ant, Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae), was observed feeding on nymphs (Fig. 1a) and just emerged adults (Fig. 1b) of D. citri and causing serious losses to the breeding stock. This is one of the few studies where predation of D. citri by ants has been verified.

Photos by L. Colorado.

Figure 1 Wasmannia auropunctata, a predator of Diaphorina citri; a) a worker of W. auropuntata feeding on a nymph of D. citri, b) two workers of W. auropuntata feeding on a newly-emerged adult of D. citri

Location: The breeding stock of D. citri is located in a glass house of the Corporación Colombiana de Investigación Agropecuaria [Colombian Corporation for Agricultural Research] (Agrosavia), Palmira Research Center, in the municipality of Palmira, department of Valle del Cauca, Colombia, 03°31′17″N, 76°18′25″W, ca. 1,000 m asl. The experiment was conducted during April 11-22, 2016. After an initial heavy attack of W. auropunctata on a mass-rearing facility of D. citri, follow-up observations were made in order to verify the reduction of psyllid individuals from the breeding cages by this predatory ant.

Experimental unit. Four cages (70 cm × 70 cm × 70 cm) with a capacity of 9 plants of Murraya paniculata (L.) Jack (Rutaceae), each infested with an average of 600 nymphs of D. citri were used in the experiment. Three of the four cages were exposed to the ants and one served as a control (without exposure to W. auropunctata). The number of nymphs (healthy and parasitized) and adults of D. citri and adults of T. radiata were counted every 2 days for 15 days. Healthy and parasitized nymphs that disappeared in the following count were assumed to have been eaten by the ants.

Data Analysis. Fisher´s exact test was run using PAST 3.16 (Hammer et al., 2001), to analyze contingency tables in order to assess the association between the presence of W. auropunctata and the survival of D. citri to adult stage, the number of D. citri nymphs parasitized by T. radiata, and the survival of T. radiata to adult stage.

During the observation period, all the cages showed a decrease in the number of healthy nymphs and adults of D. citri (Fig. 2). The cages that were exposed to W. auropunctata had a lower survival of D. citri individuals with a mean of 2.78% +/- 2.08% compared to the control cage (no exposure to W. auropunctata) 18.3% (Fig. 3). The D. citri population in the control cage decreased until the 8th day and remained around 20% of the initial population until the end of the experiment. The cages that were exposed to W. auropunctata showed a steady decrease in D. citri numbers, with an average of 1% of the original population remaining at the end of the experiment (Fig. 2).

Figure 2 Percentage of surviving individuals of D. citri (nymphs and adults) in the experimental cages as recorded from day 1 to 15. The psyllids in the cages in the predation treatment were exposed to Wasmannia auropunctata. The percentage of surviving individuals was calculated as follows ((hn + Dc)/hn1)*100; hn: number of healthy D. citri nymphs, Dc: number of D. citri adults, hn0: Initial number of healthy D. citri nymphs. Error bars represent the standard deviation, not calculated for control treatment (n=1). 

Figure 3 Average survival of D. citri and T. radiata in cages exposed to W. auropunctata (predation) and control cages (not exposed). Error bars represent the standard deviation, not calculated for control treatment (n=1). 

Fisher´s exact test confirmed that exposure to predation by W. auropunctata was significantly associated with the number of D. citri nymphs that were able to reach the adult stage (DF= 1, χ2 = 179.35, p=6.7057 E-41). In other words, cages exposed to W. auropunctata had a lower survival percentage of D. citri. The same pattern was observed with the survival of T. radiata to adult stage (Fig. 3); and a significant association also was detected between the two variables (DF= 1, χ2 = 279.16, p = 1.1451 E-62).

The number of D. citri nymphs parasitized by T. radiata was also affected by the exposure to the little fire ant (Fig. 4). The proportion of parasitized nymphs in the control cage (65.8%) was almost three times higher than in the ant-exposed cages (23.9% +/-12.9%). A significant association was found between the two variables (DF= 1, χ2 = 203.7, p =3.2549 E-46).

Figure 4 Average percentage of D. citri nymphs parasitized by T. radiata in cages exposed to W. auropunctata (predation) and control cages (not exposed). Error bars represent the standard deviation, not calculated for control treatment (n=1). 

Although the little fire ant is an effective predator of D. citri nymphs, it also has a negative effect on the psyllid's parasitoid T. radiata, both directly by consuming parasitized D. citri nymphs and indirectly by preventing the wasps from parasitizing D. citri, however, the exact mechanism by which W. auropunctata interferes with the parasitoid T. radiata cannot be inferred from these results. Nevertheless, the negative effect of predation by these ants on T. radiata should be considered in biological control programs of D. citri by the parasitoid wasp.

Kondo et al. (2017) presented a list of 101 species of arthropods (arachnids and insects), distributed in nine orders and 26 families worldwide, reported to be natural enemies of D. citri. The majority of the natural enemies of D. citri recorded in the literature are ladybirds (Coleoptera: Coccinellidae) with 39 species (38.6%), followed by the lacewings (Neuroptera: Chrysopidae) with 13 species (12.9%) and syrphid flies with 8 species (7.9%). With the addition of W. auropunctata the number of arthropod natural enemies of D. citri worldwide is increased to 102 species. Among the many species of ants recorded as natural enemies of D. citri, there is only some evidence of predation by the species, Dorymyrmex bureni (Trager, 1988) and Pseudomyrmex gracilis (Fabricius, 1804) (Michaud, 2004). With this record, the number of confirmed predatory ants of D. citri is increased to three species.

Acknowledgements

Thanks to the Colombian Ministry of Agriculture and Rural Development (MADR) for funding the project “Evaluation of entomopathogens and chemical products for the control of Diaphorina citri Kuwayama (Hemiptera: Liviidae) and biological studies of D. citri and its main natural enemy Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae)”, convention tv16. Many thanks for the critical review of the manuscript to anonymous reviewers.

Literature cited

Hammer, Ø., Harper, D. A. T., Ryan, P. D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1), 9 pp. Available at: http://palaeo-electronica.org/2001_1/past/issue1_01.htmLinks ]

Kondo, T., G. González, F., Guzmán-Sarmiento, Y. C. (2017) Enemigos naturales de Diaphorina citri. Pp. 23−32. In: T. Kondo (Ed). Protocolo de cría y liberación de Tamarixia radiata Waterston (Hymenoptera: Eulophidae). Corporación Colombiana de Investigación Agropecuaria (CORPOICA). Mosquera, Colombia. [ Links ]

Michaud, J. P. (2004) Natural mortality of Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biological Control, 29, 260−269. [ Links ]

Navarrete, B., McAuslane, H., Deyrup, M., Peña J. E. (2013) Ants (Hymenoptera: Formicidae) associated with Diaphorina citri (Hemiptera: Liviidae) and their role in its biological control. Florida Entomologist, 96, 590−597. [ Links ]

Received: February 21, 2018; Accepted: May 28, 2018

* Corresponsal author: <tkondo@corpoica.org.co>

Editor responsable: Arturo Bonet

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