An investigation into why coccidoxenoides peregrinus (timberlake) (hymenoptera:encyrtidae) is an ineffective biological control agent in Queensland citrus

Ceballo, Flor Angel Aquino. (2002). An investigation into why coccidoxenoides peregrinus (timberlake) (hymenoptera:encyrtidae) is an ineffective biological control agent in Queensland citrus PhD Thesis, School of Biological Sciences, The University of Queensland.

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Author Ceballo, Flor Angel Aquino.
Thesis Title An investigation into why coccidoxenoides peregrinus (timberlake) (hymenoptera:encyrtidae) is an ineffective biological control agent in Queensland citrus
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2002
Thesis type PhD Thesis
Supervisor A/Prof Gimme Walter
Total pages 167
Language eng
Subjects L
770404 Control of pests and exotic species
270504 Invertebrate Biology
Formatted abstract Coccidoxenoides peregrinus is an encyrtid primary parasitoid of the citrus mealybug, Planococcus citri, a serious pest of citrus and many other orchard crops and ornamental plants across all zoogeographical regions. The parasitoid has been used in biological control programs but has had variable success. In citrus-growing areas of southeast Queensland, where this study was based, the level of parasitism achieved is high when C. peregrinus invades mass rearing facilities, but its performance in the field against the mealybug is very poor. I therefore designed a series of surveys, data analyses and experiments to investigate the discrepancy in its performance.

I first assessed the species composition of citrus-infesting mealybugs and their natural enemies in southeast Queensland orchards (Chapter 2). More than 650 fruits and twigs were sampled from citrus trees and nearby plants in Mundubbera, Nambour and Brisbane. Planococcus citri accounted for virtually all mealybugs collected and most were recorded at Mundubbera in December and January. Ten species of hymenopteran parasitoids were recovered, but overall parasitism was never higher than 3%. The pteromalid Ophelosia sp. and four Encyrtidae (Anagyrus sp., Coccidoxenoides peregrinus, Leptomastix dactylopii and Leptomastidea abnormis) were the most common species and are primary parasitoids of mealybugs. A hyperparasitic signiphorid, Chartocerus sp., was also present, as were males of unidentified encyrtid species whose host relationships remain indeterminate.

The field survey thus demonstrated that C. peregrinus is not abundant in the two southeast Queensland citrus-growing localities, even though the host mealybugs were present at pest densities. This suggests that climatic variables may be influencing the occurrence of C. peregrinus in the surveyed region. I therefore used the climate-matching program CLIMEX to check whether the climate in Mundubbera and Nambour is predicted to be suitable for this species (Chapter 3). After several iterative rounds of matching by CLIMEX, Mundubbera and Nambour were predicted to be favourable for the population growth and persistence of C. peregrinus. The prediction is consistent with the observed distribution of the species, but is inconsistent with its recorded abundance and poor biocontrol performance in these areas. The outcomes from the climate matching exercise were then used to develop tests of why C. peregrinus performs so poorly as a biological control agent in southeast Queensland citrus.

The biological properties of C. peregrinus that are, in theory, relevant to its performance as a biocontrol agent were quantified (Chapter 4). I assessed and quantified the ovipositional activity and lifetime productivity of the species under laboratory conditions, and its primary mode of reproduction was re-evaluated. Coccidoxenoides peregrinus is confirmed to be almost entirely thelytokous, with males sporadically produced at very low frequency (n = 1250, about 0.012%). The females have a high reproductive potential, and deposit an average of 239 (± 34.3, n = 10 females) eggs during their lifetime, after a short pre-ovipositional period (12 h on average; n = 10). Females have a full complement of eggs within a short time after emergence and they start to oviposit as soon as hosts are encountered, but for only a relatively brief period. Consequently, a protracted lifetime is needed to ensure that maximum fecundity is achieved; an abundance of hosts, on its own, is insufficient. Although C. peregrinus attacks all stages of its host, it does not do so at the same rate. Whether the wasps have a choice of larval stage, or no choice, they deposit most eggs into second instars (L2 = 50% n = 165 arenas), and most of these develop successfully (90%) into adults. Only a few are deposited into each of the other mealybug instars (LI = 5% n = 165 arenas and L3 = 46% n = arenas), which consequently had few individuals developing successfully (only about 5% of the deposited eggs, in each instar). Parasitoid eggs deposited into reproducing mealybugs (L4) did not persist and were presumed encapsulated.

To complement the study of whether southeast Queensland conditions are suitable for C. peregrinus wasps to persist in the field, the influence of temperature, saturation deficit and adult nutrition on parasitoid survival and reproductive performance was assessed in the laboratory (Chapter 5). Exposing the wasps to various combinations of temperature and saturation deficits revealed that adult C. peregrinus has low tolerance for high saturation deficit and that such conditions also reduced their reproductive output. Nectar from the plants Alpinia zerumbet and Datura Candida proved to be good adult food sources as indicated by their enhanced survival rate and reproductive output achieved on this diet. Their performance on Alpinia nectar matched that of honey-fed wasps and was much higher (survival increased by six times and reproductive performance by nine times) than wasps provided with water but no food.

Coccidoxenoides peregrinus achieves only low levels of parasitism in the field in southeast Queensland citrus, despite its relatively high fecundity. I investigated two possible causes of such low levels of parasitism. They could result from poor survival of the adults in the field, because of adverse environmental conditions, or they could result from inaccuracies in the measurement of parasitism (Chapter 6). Adult survival under natural conditions was therefore assessed to determine whether providing food could enhance survival rate in the field. Adults of C. peregrinus that were held without food, but in contact with leaves within citrus canopies, did not survive more than a day. By contrast, those provided with a food source lived much longer for about 5 days. Nectar from two plant species, A. zerumbet and D. Candida, again proved to be good sources of food for the adult wasps and were comparable with honey in this regard. Survival was, however, lower than that achieved in the laboratory, by about 29%. The low levels of parasitism (0.6%) achieved by C. peregrinus is southeast Queensland citrus (as compared to 49% in Rio Grande (Texas) and 38 % in Bangalore (India)) thus appears to be a consequence of the short adult life and the negative effects of a harsh environment. Provision of a suitable food source (e.g. nectar) could well enhance survival levels of the wasps, and could increase the level of parasitism achieved in the field.

Behavioural observations were conducted to test whether C. peregrinus induces behavioural changes in Pl. citri, and thus causes them to move away from their feeding site and hide before mummification. If they move away like this, they would be missed when sampling is conducted in the usual way, and unrealistically low measures of parasitism would be recorded. Parasitised mealybugs, regardless of instar, undergo changes to their behaviour as indicated by high levels of movement (quantified as the number of mealybugs walking in a given amount of time). Unparasitised mealybug control do not show this change, which clearly demonstrates that parasitism was responsible for their behavioural change. All parasitised mealybugs were highly active between 7 - 14 days after exposure and eventually underwent physical changes as well. The body of parasitised mealybugs becomes cylindrical and the legs become rigid and immobile, which is the typical appearance of the mummy. All mealybugs that eventually became mummified fell from the host lemon fruit (presumably because of their impaired locomotion), were caught on the sticky traps and were mummified there. The usual site of mummification could not therefore, be established. Fruits with sentinel mealybug hosts were placed in the field to test if movement of parasitised hosts affected the measurement of parasitism rates. Fruits were returned to the laboratory before most of the parasitised bugs started moving. Rates of parasitism were still as low as those recorded previously in the field.

The results obtained are discussed in relation to the differential performance of C. peregrinus as a biological control agent in southeast Queensland citrus. I also make some suggestions for further research that may enhance our understanding of this parasitoid in the field, and help to develop conservation measures that enhance its performance as a biocontrol agent. 
Keyword Citrus -- Diseases and Pests -- Control
Mealybugs -- Control

Document type: Thesis
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