José Carlos Franco

Novel Approaches for the Management of Mealybug Pests

Mealybugs (Hemiptera: Pseudococcidae) are small, soft-bodied plant sap-sucking insects that constitute the second largest family of scale insects (Hemiptera: Coccoidea), with more than 2,000 described species and ca. 290 genera (Ben-Dov 2006; Downie and Gullan 2004). Their common name is derived from the mealy wax secretion that usually covers their bodies (Kosztarab 1996). A recent phylogenetic study, based on analysis of nucleotide sequence data, supported the existence of three subfamilies Pseudococcinae, Phenacoccinae and Rhizoecinae (Downie and Gullan 2005). This estimate was recently revised in light of integrated molecular and morphological data, and only two subfamilies emerged: Pseudococcinae and Phenacoccinae (Hardy et al. 2008). Mealybugs are severe agricultural pests. According to Miller et al. (2002), 158 species of mealybugs are recognized as pests worldwide. These species most frequently originate from the Palearctic region (ca. 29%), followed by the Nearctic (17%), Neotropical (16%), Oriental (15%), Afrotropical (12%) and Australasian (11%) regions. Approximately 22% of the mealybug pests are polyphagous, 20% occur on grasses (e.g., sugar cane), 16% on citrus and tropical fruits, and 6% on coffee.

Management strategies of mealybug pests of citrus in mediterranean countries

Six mealybug species have been reported as citrus pests in the Mediterranean Basin: the citrus mealybugPlanococcus citri (Risso), the citriculus mealybugPseudococcus cryptus Hempel, the longtailed mealybugPseudococcus longispinus (Targioni-Tozzetti), the citrophilus mealybugPseudococcus calceolariae (Maskell), the obscure mealybugPseudococcus viburni (Signoret) and the spherical mealybugNipaecoccus viridis (Newstead). Some of these species,e.g. N. viridis, have recently been introduced into the region and are still spreading. Mealybugs are usually occasional or minor pests of citrus, but some species can reach key pest status. Mealybug management strategies in citrus have been based mostly on classical biological control and, to a lesser extent, on augmentative releases. However, chemical control is widely used, mainly because of the poor adaptation of the principal natural enemies to the climatic conditions of the Mediterranean. The application of pheromones is still restricted to monitoring the citrus mealybug, whose sex pheromone is commercially available. Mass trapping and mating disruption should be considered for possible use in IPM programs as an alternative method to supplementary chemical treatments. Enhancement of biological control through management of ant populations is another promising tactic for control of mealybugs. Strategies for managing mealybug pests of citrus, and possible levels of integration of different tactics according to the pest status, are discussed.

Effect of ground cover vegetation on the abundance and diversity of beneficial arthropods in citrus orchards

The effect of ground cover upon the communities of beneficial arthropods established in the canopy of lemon trees was investigated, by comparing three ground-cover management treatments applied: RV, resident vegetation; S, sowed selected species; and BS, bare soil by controlling weeds with herbicide. Over two consecutive years, arthropod communities in the tree canopy were sampled periodically by beating and suction techniques. Significantly higher numbers of beneficial arthropods were found in the RV and S treatments in comparison with bare soil. Spiders and parasitoid wasps were the two most common groups, representing, respectively, 70% and 19% of all catches in beating samples and 33% and 53% in suction samples. For the RV and S treatments, significant seasonal deviations from the bare soil treatment were observed using principal response curves. Similar seasonal patterns were observed over the two years. The RV and S treatments showed significant positive deviations from the BS treatment in late spring and summer, accounted for the higher numbers of parasitoid wasps, coccinelids and lacewings present. By contrast, the seasonal deviations observed for the spider community differed from those of the remaining arthropods. During late winter and early spring, the RV and S treatments presented a higher abundance of spiders in the tree canopy, in comparison with bare soil, whereas in the summer significantly more spiders were found in the bare soil treatment. Spider movements between tree canopy and ground vegetation layers may justify this result.

Kairomonal response of the parasitoid Anagyrus spec. nov. near pseudococci to the sex pheromone of the vine mealybug

The occurrence of a kairomonal response of the parasitoid Anagyrus spec. nov. near pseudococci (Hymenoptera: Encyrtidae) to (+)‐(1R,3R)‐cis‐2,2‐dimethyl‐3‐isopropenyl‐cyclobutanemethanol acetate (PcA, namely, planococcyl acetate) and (S)‐(+)‐lavandulyl senecioate (LS), the respective female sex pheromones of its hosts, the citrus mealybug, Planococcus citri (Risso) and the vine mealybug, Planococcus ficus (Signoret) (Homoptera: Pseudococcidae) was investigated. Attraction to the pheromones was tested by employing pheromone traps in field trials and by static air olfactometer bioassays in the laboratory. Female wasps showed a significant response to LS, in both field and olfactometer experiments. No significant response was registered to the sex pheromone of P. citri. Despite the similarity between the structures of LS and its analogue (S)‐(+)‐lavandulyl isovalerate (LI), no significant response to the latter compound was observed. It seems that differences between the structures of the carboxylate moiety of the respective molecules (LS and LI) markedly affect the kairomonal attractiveness to the parasitoid. The kairomonal response of Anagyrus spec. nov. near pseudococci was neither influenced by the host habitat nor by the host species on which it developed. This suggested innate behaviour of Anagyrus spec. nov. near pseudococci, possibly derived from evolutionary relationships between the parasitoid and P. ficus. The practical implications of the results are discussed.

Presence of the Eucalyptus gall wasp Ophelimus maskelli and its parasitoid Closterocerus chamaeleon in Portugal: First record, geographic distribution and host preference

The Eucalyptus gall wasp Ophelimus maskelli (Hymenoptera: Eulophidae) and its parasitoid Closterocerus chamaeleon (Hymenoptera: Eulophidae) were observed for the first time in Portugal, in 2006 and 2007, respectively. Data on the distribution of O. maskelli in Portugal, differences in the susceptibility of two host species, Eucalyptus globulus and Eucalyptus camaldulensis, and parasitism by C. chamaeleon are given.

Attraction of Planococcus ficus males to racemic and chiral pheromone baits: flight activity and bait longevity

The vine mealybug (VM), Planococcus ficus (Signoret), is a worldwide pest and affects mainly grapevine and figs. In Israel, (S)‐lavandulyl senecioate [(S)‐LS] and (S)‐lavandulyl isovalerate [(S)‐LI] were identified from VM reared for several generations on potato sprouts, when compared with the identification of only (S)‐LS from feral females. Racemic lavandulyl senecioate (LS) can be used for fieldwork because the unnatural enantiomer is benign and does not affect the activity of the pheromone. Lures loaded with 200 μg of LS remained active for 24 weeks but it is recommended to replace lures after 12 weeks to preserve constant and high attractiveness. Delta sticky traps, baited with 50 or 200 μg of LS were used to determine the daily flight pattern and the seasonal flight activity including vine plant infestation. A positive correlation between peak mealybug density and male capture was observed strengthening the usefulness of the pheromone traps for monitoring the pest. Addition of racemic or the two enantiomers of lavandulyl isovalerate (LI) to LS decreased the capture of VM males. The level of inhibition varied during 2003–2004. Both enantiomers of LI displayed the same antagonistic activity. Addition of (S)‐lavandulol to the pheromone resulted in shut‐down of the traps. Inhibition by the antipode, (R)‐lavandulol, was moderate indicating a certain degree of chiral discrimination.

A common mode of attraction of larvae and adults of insect predators to the sex pheromone of their prey (Hemiptera: Matsucoccidae)

The attraction of several adult predators, genera Elatophilus, Hemerobius and Sympherobius, to the sex pheromones of pine bast scales, Matsucoccus Cockerell, has already been demonstrated. Here, the hypothesis that the larvae of these predators are similarly attracted to the host prey sex pheromone is tested. The response of predators was tested in field trials using pine tree arenas baited with the sex pheromones of M. josephi Bodenheimer & Harpaz, M. feytaudi Ducasse and M. matsumurae Kuwana. Experiments were conducted in Israel in stands of Pinus halepensis infested by M. josephi and in Portugal in stands of P. pinaster infested by M. feytaudi, respectively. The selectivity of larvae for the three sex pheromones was tested in Petri dish arenas in the laboratory. In the field, the larval stages exhibited similar modes of attraction to those of the conspecific adults: Elatophilus hebraicus Pericart in Aleppo pine forest, E. crassicornis Reuter and Hemerobius stigma Stephens in the maritime pine forests. Laboratory choice tests confirmed the kairomonal selectivity of larvae. Both forest and laboratory tests demonstrated the response of a coccinellid of the genus Rhyzobius to the sex pheromones of M. feytaudi and M. matsumurae. A unique chemical communication system among several taxa of predators of Matsucoccus spp. was highlighted that may be attributed to their coevolution on a geological time scale.

Synthesis and structure-activity relationship of diene modified analogs of Matsucoccus sex pheromones

The biological activity of the Matsucoccus spp. sex pheromones and diene modified analogs has been tested in forests of Israel and Portugal in order to explore the structure-activity relationship of the pine bast scale pheromone/kairomone system. The response of the adult predatory bugs, Elatophilus hebraicus and E. crassicornis and of the brown lacewing, Hemerobius stigma is more selective than that of the conspecific Matsucoccus males. The removal of the terminal methyl group from the diene terminus of both pheromones 1 and 2 eliminates all kairomonal activity but retains moderate pheromonal activity. Addition of a methyl group to the diene terminus of pheromones 1 and 2 sustains full pheromonal and kairomonal activities of the Elatophilus spp. but eliminates entirely the kairomonal activity of H. stigma. Subtle designed alterations in the structure of the diene group, typical of all Matsucoccus pheromones, change the mode of the kairomonal activity markedly.

Can facultative parthenogenesis occur in biparental mealybug species

The existence of facultative parthenogenesis in mealybugs has been reported by different authors and questioned by others in relation to certain species. We tested the hypothesis of facultative parthenogenesis in relation to three mealybug species, Planococcus citri (Risso), Pseudococcus calceolariae (Maskell) and Pseudococcus viburni (Signoret). The results suggest that these mealybug species are obligate amphimictic.

Defense Response of Native and Alien Mealybugs (Hemiptera: Pseudococcidae) Against the Solitary Parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae)

The host behavioral and immune (encapsulation) defenses against the parasitoid Anagyrus sp. nr. pseudococci were compared for five mealybug species with different phylogenetic relationships and geographical origins: i) a Mediterranean native mealybug species, Planococcus ficus, with a long co-evolutionary history with the parasitoid; ii) three alien mealybugs species, Planococcus citri, Pseudococcus calceolariae and Pseudococcus viburni, with a more recent co-evolutionary history; and iii) a fourth alien mealybug species, Phenacoccus peruvianus, with no previous common history with the parasitoid. Three host defense behaviors were registered: abdominal flipping, reflex bleeding and walking away. The native host Pl. ficus and its congener Pl. citri exhibited the lowest probability of defense behavior (0.11 ± 0.01 and 0.09 ± 0.01 respectively), whereas the highest value was observed in P. viburni (0.31 ± 0.02). Intermediate levels of defense behavior were registered for Ps. calceolariae, and Ph. peruvianus. The probability of parasitoid encapsulation was lowest and highest for two alien host species, Ph. peruvianus (0.20 ± 0.07) and Ps. viburni (0.86 ± 0.05), respectively. The native host Pl. ficus, its congener Pl. citri and Ps. calceolariae showed intermediate values (0.43 ± 0.07, 0.52 ± 0.06, and 0.45 ± 0.09, respectively). The results are relevant with respect to biological control and to understand possible evolutionary processes involved in host range of A. sp. nr. pseudococci.