Ants indirectly interfere with mealybug management by preventing parasitic wasps from effectively parasitizing their mealybug hosts.

Honeydew excreted by mealybugs constitutes a large part of the ants’ diet, although honeydew is not all that ants feed on. They are also efficient predators, attacking many agricultural pests, especially soft-bodied insects, such as larvae of moths and fruit flies which are found in the soil. Ants perform important ecological functions such as pollination, nutrient recycling and soil improvement.

It is therefore important to first determine whether they occur at damaging levels before applying control measures, which may be unnecessary and expensive. Current Integrated Production of Wine (IPW) approved control measures include the use of direct chemical stem barriers with registered chemicals. These are, however, not effective against certain ant species which nest in the vine canopy, and can therefore only be used against soil-nesting species. An improvement on the original 25% action threshold was investigated and it was determined that a threshold of 20% is a more accurate measure for initiating control action (Addison & Addison, 2010). From this study, we also concluded that ants significantly reduce biological control of the vine mealybug by the parasitoids Coccidoxenoides perminutus and Anagyrus sp. In the laboratory we found significant differences in ant aggression between species and ant-tolerance between parasitoids.

Wynboer – November 2011 – Development of new ant control methods in vineyards, with focus on integration with biological control of vine mealybug

Wynboer - November 2011 - Development of new ant control methods in vineyards, with focus on integration with biological control of vine mealybug

The cocktail ant, Crematogaster peringueyi and the Argentine ant Linepithema humile showed the most disruption, and the parasitoid C. perminutus (currently being commercially produced as a biological control agent) showed a high degree of ant tolerance. In the field trials, these differences were not as profound due to many factors coming into play in vineyards that cannot be accounted for in a laboratory (Addison & Mgocheki, 2010).

The following is a report on our latest research results, which focused on the development of bait toxicants for use in vineyards against both soil- and vine-nesting ant species. Target ants of this study included the Argentine ant common pugnacious ant (Anoplolepis custodiens) and cocktail ant. Furthermore, we discuss the toxicity of various common vineyard chemicals on two important mealybug parasitoids C perminutus and Anagyrus sp. Life table studies recently conducted on Anagyrus sp. (near) pseudococci provide important temperature thresholds within which the latter is effective to manage mealybugs in the absence of ants. These results contribute to improving vine mealybug management.

DEVELOPMENT OF LOW TOXICITY BAITS AGAINST VINEYARD ANTS
Field bait preference (Nyamukondiwa & Addison 2011a) and bait acceptance experiments, aimed at determining bait repellence and palatability, respectively, were carried out during spring, summer and autumn in three vineyards infested with the Argentine ant, the common pugnacious ant and the cocktail ant. Five toxicants were tested (Table 1). Gourmet ant bait is scientifically formulated to mimic honeydew and contains a patented attractant, UNI-TRACT™, which enhances feeding in a number of ant species, including the Argentine ant. All bait toxicants were dissolved in 25 % sugar solution, resulting in the concentrations outlined in Table 1.
Laboratory bait efficacy assessments using Gourmet ant bait, boric acid and spinosad were conducted at concentrations of 0.25, 0.5, 1, 2 and 4 times field dose, while fipronil was assessed at 0.015625, 0.03125, 0.0625, 0.125 and 0.25 times the field dose. Foraging activity and food preference experiments were carried out in vineyards (Nyamukondiwa & Addison 2011b) to determine at which density toxic baits should be placed in the field to still be effective and attractive against each ant species. The results are summarized below:

Gourmet ant bait was significantly more preferred and accepted by all ant species than all other baits (Nyamukondiwa & Addison 2011.
Boric acid (2%), gourmet ant bait (2%) and fipronil (1.0 x 10-5%) exhibited delayed toxicity for Argentine ant and cocktail ant, while spinosad (0.01%) showed delayed action for Argentine ant (see Nyamukondiwa, 2008). Common pugnacious ants were not tested in the efficacy trials due to logistic constraints. Delayed toxic action is important for controlling ants, as killing ants immediately on contact will not affect the whole colony, only foraging workers. Baits that demonstrate delayed toxicity will also stand a chance of being transferred to other colony members, such as the queen, and therefore affect the whole nest.
The foraging distance of the Argentine ant was higher compared to pugnacious ant or cocktail ant, supporting the supercolony theory of the Argentine ant (ants of this species do not display any aggression towards each other and so are able to form extensive shared nests). The practical implication for this is that placing bait stations every 9m (i.e. approximately 81 baits/ha) will potentially affect 80% of the Argentine ant population, but only 30% of pugnacious ants and 20% of cocktail ants (Nyamukondiwa & Addison 2011b).
Food preference trials showed that the Argentine ant and the cocktail ant prefer sugary foods, while the pugnacious ant significantly preferred protein (tuna). However, all three ant species showed a distinct preference for wet foods, as opposed to dry ones (Nyamukondiwa & Addison 2011b).

DETERMINING THE EFFECT OF COMMON VINEYARD PESTICIDES ON THE PARASITIC WASP OF THE VINE MEALYBUG
For biological control of vine mealybug to be effective, it is important to determine what effect synthetic pesticides have on the parasitic wasps currently produced commercially for augmentative releases. Twenty-four hour pesticide bioassays with parasitoids were conducted using common pesticides used in vineyards (Table 2).

In one bioassay, parasitoids were exposed continuously to pesticide residues over 24 hours and dose response data were analyzed. In a second bioassay, field rate pesticides were applied topically to parasitized mealybugs (mummies). Mortality and longevity of adult parasitoids that emerged from mummies were assessed. The results are summarized as follows (see Mgocheki & Addison, 2009):

Fipronil and -cypermethrin residues were the most toxic pesticides of those tested for Anagyrus sp. and C. perminutus. Mortality of C. perminutus was significantly higher than that of Anagyrus sp.
The adult stage of the parasitoids is more vulnerable to pesticide residues as opposed to the protected juvenile stage. Low mortality was recorded for all these pesticides for parasitoids emerging from mummies. Therefore, the mummy case was an effective barrier to pesticides.
Buprofezin, mancozeb and the insecticidal soap were not toxic to parasitoids in both bioassays.

A third bioassay determined the sublethal effects of imidachloprid (Confidor 350SC) as serial dilutions, using parasitoids which parasitized vine mealybugs having fed on treated vines. It was found that both Anagyrus sp. and C. perminutus were equally susceptible to this systemic pesticide. Survival of C. perminutus F1 generation was significantly reduced by imidachloprid whereas that of Anagyrus sp. was not.

IMPORTANCE OF LIFE TABLE STUDIES ON ANAGYRUS SP NR. PSEUDOCOCCI
To compliment previous work by Walton & Pringle (2005) on C. perminutus, life tables where conducted on the predominant Anagyrus sp. present in Western Cape vineyards, Anagyrus sp nr. pseudococci. This information is vital in directing mealybug management towards biological control, with low reliance on pesticides. The life table study was conducted at constant temperatures, 11, 17, 22, 27, 30, 32 and 34C, at a humidity of approximately 53% and day light regime of 16L:8D (Wohlfarter & Addison, 2011). Maximum values for the intrinsic rates of increase and net reproduction rate of A. sp. nr. pseudococci were 4.305 and 152.7 respectively, obtained at 27C (Wohlfarter & Addison, 2011). The lower temperature threshold of development (T0), upper lethal limit (TL) beyond which no development will occur and optimum temperature threshold (Topt), were estimated at 16.32C, 35.66C and 30.75C, respectively (Wohlfarter & Addison, 2011). Given these developmental parameters, we can conclude that A. sp. nr. pseudococci is well adapted to outperform its host, the vine mealybug, at higher temperatures and can also provide better parasitism than its counterpart C. perminutus. The commercial rearing of A. sp. nr. pseudococci should therefore be seriously considered, to provide growers with a range of biological control agents against vine mealybug.

CONCLUSION AND RECOMMENDATIONS
We conclude that ants indeed significantly reduce biological control of the vine mealybug by the two parasitoids discussed here and that special attention should be given to cocktail and Argentine ant infestations, which could impact more on biological control of vine mealybug than the pugnacious ant.

Control measures should be applied once 20% of vine stems (cordons, 30 cm on either side of the main stem) are infested with ants. This figure should be determined by using the standard monitoring system developed for vineyards (de Villiers et al, 2006). This action threshold can be used for either of the ant species monitored during this study.
Results from earlier research show that the best control measure to use are chemical stem barriers, applied only to the main stem using a knapsack spray pump (Addison, 2002). Consult your area technical representative for options on chemical products and dosages.
For biological control of the vine mealybug, C. perminutus can be used as an augmentative release agent, as it was found to be relatively ant-resistant and is commercially available. However, if either biological control agent is used in combination with chemical stem barriers against ants, biological control could be substantially improved. Since the chemical treatment is localized on the main vine stem, this should not affect biological control agents negatively, but will assist in reducing ant pressure from the ground.
Whilst Anagyrus sp. was found to be less ant resistant than C. perminutus, it showed higher tolerance to common vineyard pesticides. The wider temperature thresholds of A. sp. nr. pseudococci and especially its ability to control vine mealybug at higher temperatures than C. perminutus, increase the importance of combined releases, as they could, in theory, greatly improve biological control of vine mealybug. The debate about multi-species releases has been extensively reviewed (Hokkanen, 1985) and also found by more recent research to be potentially very beneficial (Bokonon-Ganta et al., 1996), as long as no competition for resources is experienced (Amaresekare et al., 2010). It appears that the characteristics of C. perminutus and Anagyrus sp. are such that they would not compete for P. ficus hosts as they probably utilize different life stages, and that they would therefore complement each other in a multi-species release. This will have to be fully established on local populations, as no information is available on the Anagyrus sp. found in South African vineyards, before more specific recommendations can be made.
Preliminary studies on low toxicity baits indicate that these could be a good alternative to chemical stem treatments. Full scale field trials need to be conducted and a practical and inexpensive bait station will need to be designed for this method to become commercially available.
AUTHORS
Pia Addison, Nyembezi Mgocheki, Casper Nyamukondiwa: Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland, 7602.

Martin Wohlfarter: Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland, 7602. Entomon Technologies (Pty) Ltd, P.O. Box 12669, Die Boord, 7613

ACKNOWLEGEMENT
We thank FruitGro Science, Winetech and THRIP for funding; the producers of the wine farms for assistance in providing us with trial sites; Dr KL Pringle for assisting with statistical analyses (not indicated to any great extent in this publication); Mr L Williams, S Arnolds, P. Mudavanhu, Ms JY de Waal and Ms E Apinda-Legnuou for technical assistance.

REFERENCES
ADDISON, P. 2002. Chemical stem barriers for the control of ants (Hymenoptera: Formicidae) in vineyards. South African Journal of Enology and Viticulture 23 (1): 1 8.

ADDISON, P. & MGOCHECKI, N. 2010. Improving ant management in vineyards: How damaging are they and when should they be controlled South African Fruit Journal 9 (2): 30 31.

AMARASEKARE, K., MANNION, CM. & EPSKY, ND. 2010. Host instar susceptibility and selection and interspecific competition of three introduced parasitoids of the mealybug Paracoccus marginatus (Hemiptera: Pseudococcidae). Environmental Entomology 39: 1506 1512.

BOKONON-GANTA, AH., VAN ALPHEN, JJM. & NEUENSCHWANDER, P. 1996. Competition between Granusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition. Entomologia experimentalis et Applicata 79: 179 185.

DE VILLIERS M, WALTON VM, PRINGLE KL & ADDISON P. 2006. Monitoring system for pests of vines. Stellenbosch University, Department of Conservation Ecology & Entomology, Faculty of AgriSciences pp 1-2.

HOKKANEN, HMT. 1985. Success in classical biological control. CRC Critical Reviews in Plant Sciences 3: 35 72.

MGOCHEKI, N & ADDISON, P. 2009. Effect of contact pesticides on vine mealybug parasitoids, Anagyrus sp. near pseudococci (Girault) and Coccidoxenoides perminutus (Timberlake) (Hymenoptera: Encyrtidae). South African Journal of Enology and Viticulture 30: 110 116.

NYAMUKONDIWA, C. 2008. Assessment of toxic baits for the control of ants (Hymenoptera: Formicidae) in South African vineyards. MSc thesis, Stellenbosch University.

NYAMUKONDIWA, C. & ADDISON, P. 2011a.Preference of foraging ants (Hymenoptera: Formicidae) for bait toxicants in South African vineyards. Crop Protection 30: 1034-1038.

NYAMUKONDIWA, C. & ADDISON, P. 2011b. Food preference and foraging activity of ants (Hymenoptera: Formicidae) in South African vineyards: recommendations for low toxicity baits field applications. Crop Protection In review.

WALTON, V.M. & PRINGLE, K.L. 2005. Developmental biology of vine mealybug, Planococcus ficus (Signoret) (Homoptera: Pseudococcidae), and is parasitoid Coccidoxenoides perminutus (Timberlake) (Hymenoptera: Encyrtidae), African Entomology, 13 (1): 143-147.

WOHLFARTER M. & ADDISON P, 2011, A life table study of Anagyrus sp. (near) pseudococci (Girault) (Hymenoptera: Encyrtidae) on its host, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae), submitted for publication African Entomology.

This article originates from research funded by Winetech and the final reports of project 230048 (Assessment of toxic baits for the control of ants in vineyards), project US E A03 (Life table studies on Anagyrus pseudococci, an important parasitoid of the key wine and table pest, vine mealybug) and project US E A04 (Determing the effect of field-sprayed pesticides on the important vine mealybug parasitoid, Anagyrus pseudococci) can be downloaded from http://www.sawislibrary.co.za/dbtextimages/AddisonP5.pdf, http://www.sawislibrary.co.za/dbtextimages/AddisonP6.pdf and http://www.sawislibrary.co.za/dbtextimages/Addsionp4.pdf

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