Reducing the impact of the two invasive pests, delottococcus aberiae (de lotto) (hemiptera pseudococcidae) and trioza erytreae (del guercio) (hemiptera: triozidae), by strengthening sustainability and biological control in mediterranean citrus

Resumen

Biological control is the base of the Integrated Pest Management (IPM) programs in Mediterranean citrus nowadays. The greatest risk for citrus is the appearance and emergence of exotic pests in the absence of indigenous natural enemies. Their establishment obligates growers to depend on the use of broad spectrum pesticides. This reversion to the use of pesticides jeopardizes current IPM programs implemented in Mediterranean citrus. This is the case of the two invasive citrus pests, Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) and Trioza erytreae (Del Guercio) (Hemiptera: Triozidae). Delottococcus aberiae was first detected in Europe in 2009. Native to Southern Africa, unlike other species of citrus mealybugs, it causes severe fruit size reduction and distortions that lead to significant economic losses. Since D. aberiae established itself, its management has relied on the repeated applications of broad spectrum insecticides due to the lack of effectiveness of the indigenous natural enemies and the absence of a reliable sampling procedure to determine the Economic Injury Levels (EIL) and the Environmental Economic Injury levels (EEIL). Consequently, in chapter 2, an efficient sampling protocol to assess mealybug population density as well as both EIL and EEIL were developed. Delottococcus aberiae tended to aggregate in all the organs of the tree and infested the fruits at the beginning of spring. The EIL and EEIL were calculated as 7.1% and 12.1% of occupied fruits, respectively. With these outcomes, we recommend sampling 275 fruits using a binomial sampling methodology or alternatively, 140 fruits with an enumerative method bimonthly between petal fall and July. Among natural enemies, parasitoids are the most used and effective biological control agents against mealybug pests. Unfortunately, a previous laboratory study demonstrated that indigenous parasitoids are ineffective to control D. aberiae because the mealybug encapsulates parasitoid eggs. In this context, in chapter 3 and 4 the role that other indigenous natural enemies of D. aberiae play in biological control was evaluated. In chapter 3, the predatory potential of the soil dwelling mite Gaeolaelaps (Hypoaspis) aculeifer (Canestrini) (Acari: Laelapidae) for D. aberiae was analysed. Even though predatory mites have been recorded as natural enemies of key pests that spend part of their life cycle in the soil, they have never been evaluated as mealybug predators that also inhabit the soil. Our results showed that under laboratory conditions G. aculeifer preyed on D. aberiae. Both predation rates and the proportion of G. aculeifer females that laid eggs were significantly higher when having preyed on mealybug nymphs than on eggs. In trials conducted under semi-field conditions, releases of G. aculeifer decreased D. aberiae density levels on potted citrus plants. Therefore, the presence of predatory mites should be promoted in conservation biological control strategies to reduce D. aberiae population densities when the mealybug migrates to the soil at the end of the winter and in spring. In chapter 4, we evaluated the impact of Cryptolaemus montrouzieri Mulsant (Coleoptera: Cocinellidae), one of the predators in the biological control of mealybugs most used worldwide to control D. aberiae in the field. Throughout the two years of our field study, C. montrouzieri and D. aberiae had two main synchronised population peaks per year: early spring and summer. However, in spite of this synchrony, C. montrouzieri did not prevent fruit damage. In addition, D. aberiae population growth rates were not correlated with C. montrouzieri density. Nevertheless, when two consecutive years were analysed, the increase of D. aberiae in the second year was negatively correlated with the density of C. montrouzieri in summer of the previous year. According to our results, C. montrouzieri was not able to prevent fruit damage produced by the mealybug. However, it could become a valuable addition to the natural enemy guild when combined with other natural enemies and rational control measures. Even more serious than the presence of the mealybug, it is the expansion of the African citrus psyllid Trioza erytreae in the Iberian Peninsula. This psyllid is the vector of the most devastating citrus disease in the world: the Huanglongbing (HLB) or citrus greening. In Europe, T. erytreae was first recorded in the islands of Madeira (Portugal) in 1994 and in the Canary Islands (Spain) in 2002. Until then, it had remained restricted to non-continental areas. In 2014 it was first detected in mainland Europe: north-western Spain and northern Portugal. In these regions the current contingency plans have not been successful and T. erytreae is now spreading quickly towards the south. At present, HLB has not been detected in Europe, but the establishment of the vector is normally followed by the arrival of the bacteria. Therefore, the implementation of an efficient and sustainable pest management program is needed. In this context, classical biological control seems to be the most feasible measure for preventing T. erytreae to spread further into the Mediterranean citrus growing areas. In chapter 5, the parasitoid complex of T. erytreae in South Africa was disentangled with both morphological and molecular characterization. Our results showed that the parasitoid complex of T. erytreae included three species of primary parasitoids: Tamarixia dryi (Waterston) (Hymenoptera: Encyrtidae), Psyllaephagus pulvinatus (Waterston) (Hymenoptera: Encyrtidae) and one new species from the genus Tamarixia. Among them, T. dryi was the most abundant species even though its relative abundance differed between sampling locations. The secondary sex ratio (males/females) of T. dryi and Tamarixia sp. became female biased when T. erytreae nymphs were larger than 0.6 and 1.2 mm2, respectively. Primary parasitoids were attacked by three species of hyperparasitoids: Aphidencyrtus cassatus Annecke (Hymenoptera: Encyrtidae), Marietta javensis (Howard) (Hymenoptera: Aphelinidae) and a species of the genus Aphanogmus. Aphidencyrtus cassatus was the most abundant hyperparasitoid which emerged from large nymphs. Both A. cassatus and T. dryi adult females showed similar longevity. In light of these results, the introduction of the parasitoid T. dryi into Europe will be the most promising biological control strategy to slow down T. erytreae spread.