The genetic diversity, relationships, and potential for biological control of the lobate lac scale, Paratachardina pseudolobata Kondo & Gullan (Hemiptera: Coccoidea: Kerriidae)

The lobate lac scale Paratachardina pseudolobata Kondo & Gullan (Kerriidae) is a polyphagous pest of woody plants in Florida (U.S.A.) the Bahamas, Christmas Island (Australia) and it has been reported from Cuba. Its recent appearance as a pest in these places indicates that this scale is introduced; however, its native range is unknown. Until 2006, this pest species was identified mistakenly as Paratachardina lobata (Chamberlin) [now P. silvestri (Mahdihassan)], which is native to India and Sri Lanka. Quarantine laboratory acceptance trials with Indian P. silvestri parasitoids indicated a strong immune response from P. pseudolobata. Gregarious development of encyrtid wasps was the only observed parasitism, but parasitization levels were below 3%. Identification of the native range of P. pseudolobata would facilitate the search for natural enemies better adapted to the scale. Sequence data from the D2–D3 region of the nuclear large subunit ribosomal RNA gene (LSU rRNA, 28S) and the mitochondrial gene cytochrome oxidase I (COI) distinguished P. pseudolobata from the morphologically similar species P. silvestri and P. mahdihassani Kondo & Gullan, and showed P. pseudolobata to be more closely related to these Indotropical species than to an Australian species of Paratachardina Balachowsky. Paratachardina pseudolobata was genetically uniform throughout its exotic range, consistent with a single geographic origin, although lack of variation in these genes is not unusual for scale insects. Molecular identification of morphologically similar Paratachardina species was possible using the D2–D3 region of 28S, despite its length variation, suggesting that this gene region might be suitable as a non-COI barcoding gene for scale insects.     

Confirmation of the existence of alloparasitoids in nature – host relationships of an Australian Coccophagus species that parasitizes mealy bugs

Heteronomous hyperparasitoids are parasitic wasps with sex‐related host relationships that are unique to a group of genera in the chalcidoid family Aphelinidae. Females are primary parasitoids of various sedentary bugs (mainly, scale insects, mealy bugs, and whiteflies). Males, in contrast, are hyperparasitic, and they frequently develop at the expense of female conspecifics. Alloparasitoids constitute a special category of heteronomous hyperparasitoids, for their males never develop through female conspecifics. The existence of alloparasitic host relationships and the utility of the category ‘alloparasitoid’ have both been questioned. Here, we present results that confirm the existence of the alloparasitic way of life among heteronomous aphelinids. We investigated an undescribed species of Coccophagus (Hymenoptera: Aphelinidae), an Australian parasitoid that attacks the introduced lantana mealy bug, Phenacoccus parvus Morrison (Homoptera: Pseudococcidae), in Queensland. A year‐long field survey regularly returned large numbers of female Coccophagus spec. near gurneyi individuals from P. parvus (total n = 4212), but only few males (n = 11). Males emerged from samples only when the encyrtid parasitoid Anagyrus diversicornis (Howard) (Hymenoptera: Encyrtidae) was present in samples in relatively high numbers. Laboratory oviposition tests confirmed that A. diversicornis is a male host and showed that males do not develop at the expense of conspecific females. Other studies show that males are attracted in numbers to virgin females held in cages above mealy bug‐infested Lantana montevidensis (Spreng.) Briq. (Verbenaceae) in the field, demonstrating that they are common in the population as a whole. This confirms that the males need hosts other than conspecific females and that their usual hosts are present outside of the lantana/P. parvus system. The implications of these results for developing a realistic classification of heteronomous host relationships are discussed.     

Host searching behavior and potential of an aquatic ichneumonid pupal parasitoid of rice caseworm (Parapoynx stagnalis) in an upland rice paddy agro-ecosystem of the Western Ghats,India

Parapoynx stagnalis (Zeller) (=Nymphula depunctalis (Guenée), is a sporadic rice paddy pest of south and southeast Asian rice paddy fields, and widely known as rice caseworm. A recent outbreak of the pest was observed in the upland rice paddy agro-ecosystem of the central Western Ghats, India. No potential natural enemies of this pest have so far been reported, mainly due to the semi-aquatic behavior of the larvae and pupae. However, an undescribed aquatic ichneumonid wasp species (belonging to a genus near Litochila) is reported as a potentially useful early stage pupal parasitoid of this pest in our study. The host searching behavior and potential of the parasitoid wasp was studied in detail using both field and laboratory experiments. The adult female wasps usually dive into the water in search of the host pupae, remaining under water for a maximum of 90.2s, while searching for rice caseworm pupae. In field and laboratory experiments, we found 73% of the parasitized pupae of P. stagnalis kept under water yielded adult parasitic wasps. However, no parasitoids emerged from parasitized host pupae maintained in dry terrariums. Sex ratio was 2.8:1. The present discovery of the semi-aquatic parasitoid wasp could aid in better management of the rice caseworm population in rice paddy fields.     

Role of Coccophagus sp. in the suppression of the soft green scale Coccus viridis (Green) (Hompoptera: Coccidae) on sapota

The soft green scale Coccus viridis (Green) (Homoptera: Coccidae) has become a major pest of sapota, Manilkara achras (Mill.) Forberg in India. A field study was conducted on the population dynamics of soft green scale Coccus viridis (Green) for 2 years (2004–2006) on sapota at the Indian Institute of Horticultural Research (IIHR) farm, Bangalore, India. The population of green scale declined from 30.72 per leaf in May 2004 to 1.62 per leaf in March 2006. Two coccinellid predators Chilocorus nigrita (Fab.) and Cryptolaemus montrouzieri (Muls.) and one aphelinid parasitoid Coccophagus sp. were recorded on C. viridis. Both the predators played a minor role in the population fluctuation of C. viridis. The parasitoid Coccophagus sp. was the dominant natural enemy observed throughout the study recording a mean of 10.24–94.67% parasitism. A significant positive correlation of the scale population with minimum temperature (r=0.54) and negative relationship with the parasitism by Coccophagus sp. (r=0.81) was recorded. Multiple regression analysis revealed that 75.7% of the variation present in the green scale population could be predicted by abiotic factors and parasitism by Coccophagus sp. Further, step-wise regression procedure employed to arrive at a multiple regression model showed that about 65.60% of the scale population could be predicted by one factor namely, parasitism by Coccophagus sp. These results showed that parasitism by Coccophagus sp. played a major role in regulating the population of the soft green scale infesting sapota.     

New distribution and host records of chalcidoid parasitoids (Hymenoptera: Chalcidoidea) of scale insects (Hemiptera: Coccoidea) in Espírito Santo,Brazil

Three species of chalcidoid parasitoids of scale insects are recorded for the first time in Brazil: Adelencyrtus moderatus, Homalopoda sp., and Diglyphomorpha sp.; and new parasitoid–host associations are recorded between the chalcidoids Encarsia lounsburyi with Hemiberlesia palmae, Encarsia lounsburyi with Melanaspis smilacis, and Diglyphomorpha sp. with Dysmicoccus brevipes.     

Status of biological control by egg parasitoids of Diaprepes abbreviatus (Coleoptera: Curculionidae) in citrus in Florida and Puerto Rico

Eggs of Diaprepes abbreviatus (L.) were routinely monitored in citrus groves at ten locations in Florida during 1997 and 1998 to study egg parasitism. One citrus location was studied in Puerto Rico. No native parasitoids were recovered from 1,337 D. abbreviatus egg masses studied in Florida citrus. In contrast, an average of 35.5% (range 12.5 to 68.8%) parasitism of egg masses was reported in Puerto Rico. The parasitoids Aprostocetus gala, Horismenus spp, and Quadrastichus haitiensis were recovered from the eggs of D. abbreviatusfstudied in Puerto Rico. The Horismenus parasitoids were suspected hyperparasitoids. Releases of the parasitoid Ceratogramma etiennei from Guadeloupe were initiated during 1998 at each of the Florida research sites. By the end of 1998, C. etiennei had been recovered from D. abbreviatus eggs at two of nine locations in Florida citrus. The parasitoid was recovered from 1 of 34 egg masses at one of these locations during the month of September and from 3 of 34 egg masses at the other location during the month of November. Whether or not C. etiennei establishes itself at one or more locations in Florida remains to be seen.     

Transgenic GNA Expressing Potato Plants Augment the Beneficial Biocontrol of Lacanobia Oleracea (Lepidoptera: Noctuidae) by the parasitoid Eulophus Pennicornis (Hymenoptera; Eulophidae)

The effect of expressing the gene encoding snowdrop lectin (Galanthus nivalis agglutinin, GNA) in transgenic potato plants, on parasitism of the phytophagous insect pest Lacanobia oleracea by the gregarious ectoparasitoid Eulophus pennicornis, was investigated in glasshouse trials. Expression of GNA (approx. 1.0% total soluble protein) by transgenic plants significantly reduced the level of pest damage, thus confirming previous studies. Furthermore, the presence of the parasitoid significantly reduced the levels of damage incurred either by the transgenic or control plants when compared to those plants grown in the absence of the parasitoid. For the GNA expressing plants the presence of the parasitoid resulted in further reductions (ca. 21%) in the level of damage caused by the pest species. The ability of the wasp to parasitise and subsequently develop on the pest larvae was not altered by the presence of GNA in the diet of the host. E. pennicornis progeny that developed on L. oleracea reared on GNA expressing plants showed no significant alteration in fecundity when compared with wasps that had developed on hosts fed on control potato plants, although mean size and longevity of female parasitoids was significantly reduced. The number of F ₂ progeny produced by parasitoids derived from hosts fed on GNA-expressing plants was not significantly different to those produced by parasitoids from hosts fed control plants. Results from the present study demonstrate that the use of transgenic plants expressing insecticidal proteins can be compatible with the deployment of beneficial insects and that the two factors may interact in a positive manner.     

Within-plant vertical distributions of the scale insect Nipponaclerda biwakoensis and its five parasitoids that exhibit frequent successful multiparasitism on the common reed

Within‐shoot vertical distributions of the scale insect Nipponaclerda biwakoensis, five species of gregarious parasitoid wasps attacking the scale, and successful multiparasitism (emergence of multiple parasitoid species from a single host) by the parasitoids on the common reed were investigated. Each reed shoot collected was longer than 2.0 m, and was divided into pieces of 0.5 m each from the base of the shoot. The mean number of adult female scales per 0.5 m of shoot increased with height, but the mean rate of overall parasitism of the female scales decreased with height. The five parasitoids showed species‐specific within‐shoot distribution patterns, with respect to the rate of parasitism: Astymachus japonicus, Boucekiella depressa and Encyrtidae sp. 2 showed the greatest rates of parasitism at heights of 0–0.5, 0.5–1.0 and 1.0–1.5 m, respectively. The parasitism rate by Aprostocetus sp. was higher at the lower half of the shoots, whereas that by Encyrtidae sp. 1 was higher at the central positions. The distribution of the five parasitoids largely overlapped with each other at the level of scale aggregations. Nevertheless, successful multiparasitism occurred frequently only in several types of species combinations that involved two parasitoid species showing similar within‐shoot distribution patterns. The rate of successful multiparasitism by B. depressa with A. japonicus or Aprostocetus sp., and that by Encyrtidae sp. 2 with Encyrtidae sp. 1 was constantly high at different vertical positions on the shoots. This may be because B. depressa and Encyrtidae sp. 2 preferentially oviposit into scales previously parasitized by these other species.     

Parasitoids associated with the common pistachio psylla, Agonoscena pistaciae, in Iran

The parasitoids associated with the common pistachio psylla, Agonoscena pistaciae Burckhardt and Lauterer, were investigated at three pistachio plantations in Rafsanjan, Iran. Of the 6504 wasps emerging from mummified psyllids, 46% were the primary parasitoid Psyllaephagus pistaciae Ferrière, and the remaining 54% represented six species of hymenopterous hyperparasitoids, including Chartocerus kurdjumovi (Nikol’skaja), Marietta picta (André), Pachyneuron aphidis (Bouché), Pachyneuron muscarum (Linnaeus), Psyllaphycus diaphorinae (Hayat), and Syrphophagus aphidivorus (Mayr). Lysiphlebus fabarum Marshall, the parasitoid of Aphis gossypii Glover and Aphis craccivora Koch present on weeds, was found to be an alternative host for three major hyperparasitoids of A. pistaciae. The most abundant hyperparasitoid was S. aphidivorus, appearing during the growing season in all trial locations on psyllids and aphids in pistachio orchards. The weed-infesting aphids, along with their primary parasitoid, can act as a reservoir of A. pistaciae secondary parasitoids. Therefore, parasitized aphids allow populations of secondary parasitoids to increase and consequently to apply higher pressure on P. pistaciae. We detected that two primary parasitoid species, including P. pistaciae and L. fabarum, attacking different species of hosts interact indirectly through shared secondary parasitism. It is suggested that the community structure of A. pistaciae may be influenced by apparent competition, although more work is needed to provide firm evidence.     

Searching strategies and attack rates of parasitoids of the ash bark beetle (Leperisinus varius) and its relevance to biological control

Abstract.

• 1 Point estimates of parasitoid behaviour indicated that braconid parasitoids of the bark beetle, Leperisinus varius, spend 70% of their host searching time stationary on the bark surface, in sharp contrast to the chalcidoid parasitoids which spend 60–70% of their host searching time moving across the bark surface.
• 2 Aggressive encounters between searching parasitoids are common and the data suggest that they do not occur at random.
• 3 The chalcidoid parasitoids, Cheiropachus quadrum and Eurytoma morio, are more frequently involved in aggressive encounters than expected and can displace ovipositing individuals of other species.
• 4 Attack rates for the parasitoids were estimated to vary from two hosts per day for the braconid Coeloides filiformis to four hosts per day for E.morio, and net reproductive rates vaned from 6.3 for C.filiformis to 0.8 for Coeloides melanotus.
• 5 These data suggest that while all parasitoids of the scolytid can act as primary parasitoids, at least some of the chalcidoid parasitoids are facultative cleptoparasitoids and should be avoided in classical biological control introductions.

     

Where to sample? Ecological implications of sampling strata in determining abundance and impact of natural enemies of the coffee berry borer,Hypothenemus hampei

Several parasitoids of African origin have been introduced to coffee producing areas of the Americas and Asia as biological control agents of the coffee berry borer (CBB) Hypothenemus hampei (Coleoptera: Curculionidae). These parasitoids have become established in the field but their effect on the CBB has been limited. A two-year field study in Western Kenya has found Prorops nasuta (Hymenoptera: Bethylidae) to be the predominant parasitoid emerging from CBB-infested coffee berries collected on coffee trees or from the ground. P. nasuta comprises more than 75% of the total natural enemies collected. The density of P. nasuta was 90% higher in the berries collected from the ground than from the trees. Its hyperparasitoid, Aphanogmus sp. (Hymenoptera: Ceraphronidae), also emerged from both type of berries. Across the two seasons, the average P. nasuta density per berry was 18–35 times higher than that of Aphanogmus sp. Throughout the two years sampled, significantly higher numbers of P. nasuta and Aphanogmus sp. occurred between February and March, which coincides with the beginning of the rainy season. Higher numbers of live CBB females were recorded in berries collected from the trees. Nevertheless, mortality of adult CBB was considerably higher from January to March and started to decrease from April onwards. The possibly negative effects of cultural control practices in Latin America which include the removal of berries fallen to the ground on biological control of CBB are discussed, and the use of screened collection devices for these berries which would permit the release of parasitoids but prevent escape of the pest is proposed.     

Mutualistic ants and parasitoid communities associated with a facultative myrmecophilous lycaenid,Arhopala japonica,and the effects of ant attendance on the avoidance of parasitism

Herbivorous insects have evolved various defensive strategies to avoid their primary enemies, parasitoids. Many species of Lycaenidae (Lepidoptera) have food‐for‐protection mutualism with ants in their larval stages, where larvae produce nectar for ants and in return ants exclude parasitoids as well as predators. Myrmecophilous relationships are divided into two categories, obligate and facultative, by degrees of myrmecophily. Although parasitoids attacking obligate lycaenids always encounter lycaenid‐specific ant species, parasitoids that use facultative lycaenids are likely to encounter diverse ant species showing various defense systems. However, we know little about the parasitoid community of facultative lycaenid larvae. In this study, we investigated the mutualistic ant and parasitoid communities of a facultative myrmecophilous species, Arhopala japonica, in seven localities in Japan. The present field observation newly recorded four ant species attending A. japonica larvae, and combined with the previous data, the number of attending ant species reached 16, which is nearly the maximum number of reported attending ant species among myrmecophilous lycaenids. However, the present study revealed that almost all parasitized A. japonica larvae were attacked by a single braconid species, Cotesia sp. near inducta. We also assessed the efficiency of facultative ant defense against the parasitoid in the laboratory and revealed that oviposition by Cotesia sp. near inducta females was almost completely hindered when A. japonica larvae were attended by ants. This suggests that the dominant parasitoid does not have effective traits to overcome defensive behavior of ants and that the female wasps oviposit mainly in A. japonica larvae without intensive attendance.     

Female reproductive biology of Platygaster diplosisae (Hymenoptera: Platygastridae) and Aprostocetus procerae (Hymenoptera: Eulophidae), two parasitoids associated with the African Rice Gall Midge, Orseolia oryzivora (Diptera: Cecidomyiidae)

We investigated the female reproductive system of Platygaster diplosisae (Hymenoptera: Platygastridae) and Aprostocetus procerae (= Tetrastichus pachydiplosisae) (Hymenoptera: Eulophidae), two parasitoids associated with the African rice gall midge, Orseolia oryzivora (Diptera: Cecidomyiidae). Both optical and electron microscopy were used. The female reproductive system of P. diplosisae includes two large ovaries of the meristic polytrophic‐type, each composed of several tens of ovarioles. The system includes also a venomous gland that extends to a common oviduct. This gland had a filiform secretory portion, in which the epithelium was thin and surrounded a common evacuation canal. The secretory cells secrete into a large reservoir. Parasitism due to P. diplosisae is gregarious. The female reproductive system of A. procerae includes two ovaries of the meristic polytrophic‐type, and each ovary has a few ovarioles. Each ovariole includes one or two oocytes, which can be seen in the vitellarium. Two accessory glands, which extend to the oviduct, are also visible. The secretory epithelium of the accessory gland is made up of a dense network of secretory cells surrounded by muscle fibers. Females of A. procerae pierce the tissues of the gall and probably deposit one egg on or close to the pupa of the midge. Aprostocetus procerae is a solitary parasitoid of the midge. The two parasitoids exploit the same host at different developmental stages. These findings improve our knowledge of the reproductive biology of these two parasitoids associated with the African rice gall midge, an important pest in Africa.     

Ecological and morphological characteristics of endoparasitoids on Elcysma westwoodii (Vollenhoven) (Lepidoptera: Zygaenidae)

Six species of insect endoparasitoids were identified from Elcysma westwoodii, which is the most damaging lepidopteran pest of Prunus yedoensis. From Hymenoptera, two species were identified: a species in Braconidae and Charops striatus in Ichneumonidae. From Diptera, there were four species in Tachinidae: Compsilura concinnata, Exorista sp., Pales sp. and Tachinidae spp. The parasitic ratio was 4.86% (45 of 926 larvae). The hymenopterans were parasitic on 31 individuals of E. westwoodii (68.9%) and the dipterans were parasitic on 14 individuals (31.1%). It was found that parasitoids from the larvae of E. westwoodii were all either endoparasitoids or larval parasitoids. However, Exorista sp. of Tachinidae was found to be either a larval parasitoid or larval-pupal parasitoid. Additionally, all the identified parasitoids were solitary parasitoids, as only one parasite occurred in a larva of E. westwoodii. Because the larva of E. westwoodii eats and molts after it is parasitized, all the parasitoids were identified as koinobionts. There were no big differences in morphological characteristics and life histories between C. striatus and C. concinnata. However, for Exorista sp. and Pales sp., males took 3–5 days longer to emerge from their pupae and had remarkably longer body lengths than females.     

Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae)

Abstract.

• 1 In nature, interference among Anagrus delicatus (Hymenoptera: Mymaridae) parasitoids reduced the per-capita number of hosts parasitized. Interference increased with parasitoid density.
• 2 Anagrus delicatus did not avoid parasitizing hosts that had recently been parasitized by conspecific wasps. Evidence indicated that this superparasitism was largely a random process, increasing with the ratio of parasitized to unparasitized hosts.
• 3 Individual parasitoid efficiency, the number of hosts killed per wasp per unit time, decreased with increasing wasp density. This occurred whether wasps searched the patch together (simultaneously) or one by one (sequentially), and was the result of an increase in time spent superparasitizing hosts at higher wasp density. This is known as indirect mutual interference.
• 4 Increasing numbers of parasitoids together on the same patch caused a significant decline in the rate and per-capita number of hosts parasitized. However, there was not a correspondent decline in searching efficiency with increasing wasp density (i.e. no direct mutual interference).
• 5 These forms of parasitoid density dependence should contribute to the stability of the host—parasitoid interaction.

     

Description of Aprostocetus anoplophorae n. sp. (Hymenoptera: Eulophidae), a new egg parasitoid of the invasive pest Anoplophora chinensis (Förster) (Coleoptera: Cerambycidae)

Aprostocetus anoplophorae n. sp. (Hymenoptera: Eulophidae) is supposed to play a role as an egg parasitoid of the invasive pest, the Citrus Longhorned Beetle, Anoplophora chinensis (Förster). The studies of its morphology, and rDNA sequence data, strongly indicate that this taxon differs greatly from all described Aprostocetus species, and is new to science. This species is described and illustrated. Both its systematic placement and origin are discussed.     

Determination of the optimal parasitoid‐to‐host ratio for efficient mass‐rearing of the parasitoid,Sclerodermus pupariae (Hymenoptera: Bethylidae)

Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae) is used as a potential biocontrol agent for several buprestid and cerambycid larvae. This study aimed to enhance the efficiency of mass‐rearing of this parasitoid by investigating the fitness gain of this bethylid wasp, including the proportion of successful parasitism and development, brood size, sex ratio, proportion of winged female offspring, body size and longevity of female offspring, under eight different maternal parasitoid density treatments using Thyestilla gebleri Faldermann as host in the laboratory. The results indicated that the foundress densities did not affect the parasitism or emergence rate of this parasitoid. Brood size of the parasitoids increased significantly when the number of maternal wasps ranged from one to four. However, further increases in foundress number did not affect the parasitoid brood size. The sex ratios of S. pupariae were always female‐biased. The proportions of male in the progeny colonies were <10% throughout all experimental treatments. The percentage of winged female progeny was not significantly influenced by the density of adult maternal parasitoids. Body sizes of parasitoids significantly declined with increasing maternal parasitoid densities. Although the parasitoid body size reduced when maternal wasp number was higher, it could be compromised by the relatively higher number of female offspring produced. Further, more than 70% of the parasitoids remained alive when they were stored at 12°C for four months throughout the experiments. These findings suggest that exposure of four female wasps to a single host larva would result in the highest fitness of S. pupariae. Our findings might provide a new approach to enhance the efficiency of mass‐rearing of this bethylid wasp.     

A new species of Aprostocetus Westwood (Hymenoptera: Eulophidae), parasitizing mango leaf gall midge (Diptera: Cecidomyiidae), from India

A new species of Aprostocetus doonensis Singh sp. nov. is described from northern India. The new species is a parasitoid of mango leaf gall midge, Procontarinia mangiferae (Felt) (Diptera: Cecidomyiidae). Some observations on biology and parasitization rate are also given.