Comparison of the thermal performance between a population of the olive fruit fly and its co-adapted parasitoids

Long-term separation of a host from its native parasitoids may result in divergent thermal adaptation between host and parasitoid. The olive fruit fly, Bactrocera oleae (Rossi), most likely originated from Sub-Saharan Africa, but has since had a long invasion history in cultivated olives that spans geographical barriers and continents. This study compared three major thermal performance profiles (development, survival, and reproduction) across a wide range of temperatures (10–34 °C) among a Californian population of the olive fruit fly and two African parasitoids, Psyttalia lounsburyi (Silvestri) and Psyttalia humilis (Silvestri), believed to have co-adapted with the fruit fly in its native range. Temperature ranges for the development and survival were 10–30 °C for the fly, 10–28 °C for P. lounsburyi, and 14–32 °C for P. humilis. There was no difference in any thermal performance measured between two P. humilis populations (Kenya and Namibia) tested. The most suitable temperature ranges for reproduction were 22–30 °C for the fly, 18–32 °C for P. humilis, and 18–26 °C for P. lounsburyi. The results showed slight differences in the thermal profiles among olive fruit fly and both parasitoids species, with P. humilis being more heat tolerant whereas P. lounsburyi was less heat tolerant than the fruit fly. The results are discussed with respect to thermal co-adaptation and classical biological control of the olive fruit fly.     

Crop domestication relaxes both top-down and bottom-up effects on a specialist herbivore

Domestication of crop plants selects for numerous traits that often distinguish them dramatically from their wild progenitors. In some cases, these modifications lead to increased herbivory, by enhancing their attractiveness to herbivorous insects or reducing the efficiency of natural enemies, or both. This study investigated the effects of fruit enlargement on the olive (Olea europaea L.), the specialist olive fruit fly, Bactrocera oleae (Rossi), and its specialized larval parasitoids. Wild olive fruit are small (<2 mm pulp thickness) and the larval parasitoids associated with B. oleae have short ovipositors (<3 mm), while cultivated fruit are larger (4–8 mm pulp thickness). Female flies allocate more offspring to large than to small fruit within or across different-sized commercial cultivars, without reducing the fitness of their offspring. Fly larvae move deeper into the olive pulp with their increasing age and fruit size. In contrast, the specialist larval parasitoid, Psyttalia lounsburyi (Silvestri), more effectively parasitizes hosts in smaller than larger fruit. The inverse relationship between the performance of the fly and its co-evolved parasitoids on fruit of increasing sizes indicates that olive cultivation favors the success of the fly by providing a better food resource and more enemy-free space. These findings offer some explanation for the failure of the decades-old classical biological efforts to manage B. oleae using specialized larval parasitoids in the Mediterranean Basin and provide further evidence that crop domestication can alter host–parasitoid interactions.     

Mass‐rearing optimization of the parasitoid Psyttalia lounsburyi for biological control of the olive fruit fly

The olive fruit fly, Bactrocera oleae (Tephritidae), is a direct pest of olives that has invaded the Mediterranean Region and California. Psyttalia lounsburyi (Braconidae), a larval parasitoid from Africa, has been approved for release in the USA as a classical biological agent. However, it has been difficult to rear the parasitoid in the laboratory because it is multivoltine, and the host develops only in fresh olives, which are not available for most of the year. A method to rear the parasitoid on the factitious host, Mediterranean fruit fly (Ceratitis capitata) was developed, but it was not very efficient for producing large numbers of parasitoids needed for release. We developed a number of ways to improve the efficiency of rearing, including the frequency and duration of exposure for oviposition, optimizing the density of adult parasitoids, host age, as well as methods to quickly standardize the number of larvae exposed and to count emerging adult parasitoids. We significantly improved the number of progeny produced per female and the sex ratio of progeny. Thanks to these improvements, we produced in 2017 over 119,000 adults and shipped over 53,900 for release in California.     

Identification of 21 polymorphic microsatellites in the African parasitoid wasp, Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae)

We have developed 21 dinucleotide repeat microsatellite loci from African populations of Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae), a parasitoid wasp of the olive fruit fly, as part of a study assessing the role of introgression/hybridization in the success of a biological control introduction. We proposed suitable conditions for polymerase chain reaction multiplexing. All 21 loci were polymorphic with two to 21 alleles per locus within the Kenyan and South African populations tested. Most of them were successfully amplified in two other Psyttalia species.     

A survey of fruit-feeding insects and their parasitoids occurring on wild olives,Olea europaea ssp. cuspidata,in the Eastern Cape of South Africa

Fruits of wild olives, Olea europaea ssp. cuspidata (Wall. ex G. Don) Cif., were collected in the Eastern Cape, South Africa, during 2003–2005 to quantify levels of fruit-infesting pests and their parasitoids. Two species of Tephritidae, Bactrocera oleae (Rossi) and B. biguttula (Bezzi), were the most abundant insects recovered and were reared from most samples. Fruit infestation rates by the Bactrocera spp. were generally below 8% and over half of the infestations were under 1%. When parasitism occurred in samples with flies, levels ranged from 7 to 83%. Several species of opiine braconid wasps, Psyttalia concolor (Szépligeti), Psyttalia lounsburyi (Silvestri), and Utetes africanus (Szépligeti) and one braconine wasp, Bracon celer Szépligeti, were reared from fruits containing B. oleae and/or B. biguttula. Chalcidoid parasitoids and seed wasps included seven species of Eurytomidae (Eurytoma oleae, Eurytoma sp., and Sycophila sp.), Ormyridae (Ormyrus sp.), Torymidae (Megastigmus sp.), and Eupelmidae (Eupelmus afer and E. spermophilus). One species of moth, Palpita unionalis (Hübner) (Crambidae), was recovered in very low numbers and without parasitoids. The survey results indicate that fruit flies might not become economic pests of the nascent commercial olive industry in the Eastern Cape, and the small numbers present may be controlled to a considerable level by natural enemies.     

Effect of exposure time on mass‐rearing production of the olive fruit fly parasitoid,Psyttalia lounsburyi (Hymenoptera: Braconidae)

Classical biological control programmes rely on mass production of high‐quality beneficial insects for subsequent releases into the field. Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae) is a koinobiont larval–pupal endoparasitoid of tephritid flies that is being reared to support a classical biological control programme for olive fruit fly in California. The mass‐rearing system for a P. lounsburyi colony, initiated with insects originally collected in Kenya, was evaluated with the goal of increasing production, while at the same time reducing time requirements for rearing in a quarantine facility. We tested the effect of exposure time of a factitious host Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), on parasitization, adult production, superparasitism, and sex ratio of P. lounsburyi and survival of the host. Parasitization rates were highest (31%) at 3‐ and 4‐hr exposure times, while adult production (i.e., emergence of wasp progeny) was highest (16%) at the 2‐hr exposure time. Superparasitism over the course of the study was 1.5% and did not appear to be a factor affecting parasitoid production. The sex ratio of wasp progeny was male‐biased and did not vary significantly over different exposure times. The rate of stings on host larvae increased with exposure time and was consistent with decreases in pupal eclosion from larvae and emergence rate of adult flies. When compared to current rearing procedures, the 2‐hr exposure time resulted in an overall 2.8‐fold increase in P. lounsburyi production when standardized for time.     

Oviposition response and development of the egg-pupal parasitoid Fopius arisanus on Bactrocera oleae, a tephritid fruit fly pest of olive in the Mediterranean basin

To date, information is wanting with regard to the use of new exotic parasitoids against olive fruit fly, Bactrocera (=Dacus) oleae (Gmelin) (Diptera: Tephritidae), a serious pest of olives Olea europaea L., in the Mediterranean basin. We investigated the oviposition response and developmental biology on B. oleae of Fopius (=Biosteres) arisanus (Sonan) (=Opius oophilus Fullaway) (Hymenoptera: Braconidae), an egg-pupal parasitoid of tephritid fruit flies, never tested before as a potential parasitoid of this host. Our results showed that olive fruits infested with B. oleae eggs exerted a relevant attraction to gravid F. arisanus and represented a stimulus for oviposition. Nevertheless they were not as attractive to female parasitoids as the Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae), eggs infested papaya fruits (Carica papaya L.). In our experimental conditions, F. arisanus completed development in B. oleae within 33 ± 1.7 days (males) and 35 ± 1.6 (females). Increases in host egg to female parasitoid ratios of 1:1, 5:1, 10:1 and 20:1 corresponded with decreases in the percentage of B. oleae parasitisation and host killing but corresponded also with increases in absolute parasitisation. Our findings are discussed in light of possibilities of utilising F. arisanus for biological control of olive fruit fly.     

Prospects for improving biological control of olive fruit fly,Bactrocera oleae (Diptera: Tephritidae), with introduced parasitoids (Hymenoptera)

Olive fruit fly is a key pest of olive and consequently a serious threat to olive fruit and oil production throughout the Mediterranean region. With the establishment of Bactrocera oleae in California a decade ago, interest was renewed in classical (introduction) biological control of the pest. Here we discuss the prospects of identifying natural enemies of B. oleae in Africa and Asia that may help reduce B. oleae populations in California and elsewhere. Based on the current understanding of Bactrocera phylogenetics, early opinions that B. oleae originated in Africa or western Asia rather than the Mediterranean region or the Near East are taxonomically and ecologically supportable. Closely related to cultivated olive, the wild olive Olea europaea cuspidata is widely distributed in southern and eastern Africa, the Arabian Peninsula, and eastwards into Asia as far as southwestern China. Little is known regarding the biology and ecology of B. oleae in Africa and eastern Asia, especially in wild olives. While the diversity of parasitoids of B. oleae in the Mediterranean region is low and unspecialized, a diverse assemblage of parasitoids is known from B. oleae in Africa. Conversely, regions in Asia have remained largely unexplored for B. oleae and its natural enemies.     

Molecular characterization of <Emphasis Type="Italic">Psyttalia lounsburyi</Emphasis>, a candidate biocontrol agent of the olive fruit fly,and its <Emphasis Type="Italic">Wolbachia</Emphasis> symbionts as a pre-requisite for future intraspecific hybridization

Numerous arthropod species are genetically differentiated across their distribution area. Diversifying the geographical origins of a biocontrol agent species can be used to favour their perennial establishment by the sampling of pre-adapted genotypes and/or the production of new genotypes through hybridization. Hybridization can be nevertheless challenged by reproductive isolations induced by some common microbial endosymbionts. In this study, we aimed at characterizing (i) the genetic diversity of six populations of Psyttalia lounsburyi (Hymenoptera: Braconidae), a candidate biocontrol agent of the olive fruit fly Bactrocera oleae (Diptera: Tephritidae) and (ii) the diversity of their Wolbachia endosymbionts. Both mitochondrial and microsatellite markers evidence clustering between the South African population and several Kenyan/Namibian populations. The survey of the Wolbachia also distinguished two main variants with a spatial heterogeneity in the infection status. All these results are discussed in the context of the use of these P. lounsburyi populations for hybridization and further field releases.     

Female‐borne cues affecting Psyttalia concolor (Hymenoptera: Braconidae) male behavior during courtship and mating

Knowledge of the mechanisms that regulate courtship and mating behavior in Psyttalia concolor (Szépligeti)–a koinobiont endophagous solitary parasitoid of the olive fruit fly, Bactrocera oleae (Rossi), and of other fruit flies–is essential to its mass rearing and management. Augmentative releases of P. concolor for olive fruit fly control started in the Mediterranean areas in the 1950s and still continue with limited success. We determined the influence of visual and chemical cues on courtship and mating behavior of this braconid and the possible effect of the mating status of males and females in the perception of these cues. Our results suggest that integration of visual and chemical stimuli are fundamental for mate location and courtship. Indeed, the optimal response of the male was achieved when physical and chemical cues were simultaneously presented and vision and olfaction worked synergistically.     

Non-target host risk assessment of the idiobiont parasitoid Bracon celer (Hymenoptera: Braconidae) for biological control of olive fruit fly in California

Non-target risk posed by an African parasitoid, Bracon celer Szépligeti (Hymenoptera: Braconidae), was assessed for a classical biological control program against olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae: Dacinae), in California, USA. Behavioral and reproductive responses to non-target tephritid species were tested with beneficial (Chaetorellia succinea [Costa] and Parafreutreta regalis Munro) (Tephritidae: Tephritinae) and native (Rhagoletis fausta [Osten Sacken]) (Tephritidae: Trypetinae) fruit fly species in successive no-choice and choice experiments under close confinement in quarantine. Non-target host-plant substrates exposed to B. celer were yellow-starthistle flower heads containing C. succinea, Cape ivy stem galls containing P. regalis, and bitter-cherry fruit containing R. fausta. The parasitoid probed all three infested non-target plant substrates, but significantly less than olives infested with B. oleae. It produced offspring from P. regalis in Cape ivy stem galls, but appeared unable to penetrate yellow-starthistle flower heads with its ovipositor. Bracon celer killed some B. oleae and R. fausta larvae without parasitism. Reproduction on P. regalis indicates that B. celer has a broad physiological host range, which, combined with the parasitoid's acceptance of all three host-plant substrates, indicates a strong potential to negatively impact non-target species. Although physical and temporal barriers to host attack may reduce risk to most non-target tephritids by B. celer in California, the parasitoid should not be released due to its risk of harming the beneficial P. regalis. Release of P. regalis is still under consideration, however, and final risk assessment should depend on whether the fly proves useful for weed control.     

Psyttalia ponerophaga (Hymenoptera: Braconidae) as a potential biological control agent of olive fruit fly Bactrocera oleae (Diptera: Tephritidae) in California

The olive fruit fly, Bactrocera oleae (Rossi), is a newly invasive, significant threat to California's olive industry. As part of a classical biological control programme, Psyttalia ponerophaga (Silvestri) was imported to California from Pakistan and evaluated in quarantine. Biological parameters that would improve rearing and field-release protocols and permit comparisons to other olive fruit fly biological control agents were measured. Potential barriers to the successful establishment of P. ponerophaga, including the geographic origins of parasitoid and pest populations and constraints imposed by fruit size, were also evaluated as part of this investigation. Under insectary conditions, all larval stages except neonates were acceptable hosts. Provided a choice of host ages, the parasitoids' host-searching and oviposition preferences were a positive function of host age, with most offspring reared from hosts attacked as third instars. Immature developmental time was a negative function of tested temperatures, ranging from 25.5 to 12.4 days at 22 and 30 degrees C, respectively. Evaluation of adult longevity, at constant temperatures ranging from 15 to 34 degrees C, showed that P. ponerophaga had a broad tolerance of temperature, living from 3 to 34 days at 34 and 15 degrees C, respectively. Lifetime fecundity was 18.7 +/- 2.8 adult offspring per female, with most eggs deposited within 12 days after adult eclosion. Olive size affected parasitoid performance, with lower parasitism levels on hosts feeding in larger olives. The implications of these findings are discussed with respect to field manipulation and selection of parasitoid species for olive fruit fly biological control in California and worldwide.     

A kaolin‐based particle film for suppression of the olive fruit fly Bactrocera oleae Gmelin (Dip., Tephritidae) in olive groves

The efficacy of a kaolin‐based particle film formulation M‐99‐099 to control olive fruit fly, Bactrocera oleae Gmelin, field infestations was investigated in north‐western Syria. The results showed that fruit infestation levels were significantly reduced on kaolin‐treated trees compared with untreated trees. Kaolin particle film successfully suppressed B. oleae populations and provided season‐long insect control (>14 weeks) whereas the insecticide dimethoate failed to protect olives for as long a period after the last spray. Consistent with previous findings, the M‐99‐099 kaolin particle film proved to be a promising alternative method to synthetic insecticides and could be used to control B. oleae in olive groves.     

Distribution of Bactrocera oleae (Rossi, 1790) throughout the Iberian Peninsula based on a maximum entropy modelling approach

The Iberian Peninsula (Portugal and Spain) is a great production area of olives. The fruit production can be severely affected by the olive fruit fly, Bactrocera oleae (Rossi, 1790) (Diptera). Detailed geographical distribution maps of key pests, such as B. oleae, are essential for their integrated management. Although different sources reporting the occurrence of B. oleae are available for sub-regions of Portugal and Spain, the data available are dispersed and centralisation of this information considering the Iberian Peninsula as a faunistic geographical unit is currently lacking. In this work, we built two distribution maps of B. oleae throughout the Iberian Peninsula, one based on occurrence sites and another based on its bioclimatic habitat suitability. After modelling the bioclimatic suitability of B. oleae using a maximum entropy model, three potential distribution areas beyond the previously known occurrence range of the olive fruit fly were identified corresponding to the autonomous community of Galicia (Spain), the Spanish and Portuguese sides of the International Douro Natural Park, and the autonomous community of Castilla y León (Spain). Interestingly, each region houses nowadays autochthonous olive cultivars. The drivers that most contributed to the model were the precipitation of the coldest quarter and the precipitation of driest month which agrees with the B. oleae bioecology. Although our approach is not fully-comprehensive in terms of occurrence sites, we show how a maxent modelling approach can be useful to identify potential risk areas of B. oleae occurrence throughout a target geographical extent such as the Iberian Peninsula.     

Sugar concentration and timing of feeding affect feeding characteristics and survival of a parasitic wasp

The availability of food sources is important for parasitoid survival, especially for those that inhabit ecosystems where nectar and honeydew are spatially or temporally scarce. Therefore, the value of even a single meal can be crucial for survival. Psyttalia lounsburyi is a parasitoid, and biological control agent, of the olive fruit fly, Bactrocera oleae. In order to improve our understanding of the basic nutritional ecology of P. lounsburyi and its role in survival we evaluated the effect of a single sucrose meal on the longevity of female and male wasps. We measured the duration of feeding, volume ingested, sucrose consumption, energy content, and longevity of wasps provided with different concentrations of sucrose (0.5, 1, and 2 M) at different times after emergence (0, 1, 2 or 3 days after emergence). Our results showed that longevity was significantly influenced by sucrose concentration and timing of feeding. For females, feeding on sucrose increased the likelihood of survival to varying degrees, ranging from 32.3% to 95.4%, compared to water-only controls. The longest duration of feeding was observed for the highest sucrose concentrations and oldest wasps. The amount of sugar ingested and energy uptake increased, up to a point, as sugar concentration increased. Our results suggest that P. lounsburyi derived greatest benefit from the intermediate concentration (1 M) of sucrose provided 2 or 3 days after emergence. Our study emphasizes the importance of finding balance between increasing longevity and limiting the duration of feeding, and concomitant uptake of nutrients, that is fundamental for survival of the wasp in nature.     

Biosystematics of the Psyttalia concolor Species Complex (Hymenoptera: Braconidae: Opiinae): The Identity of Populations Attacking Ceratitis capitata (Diptera: Tephritidae) in Coffee in Kenya

The identity of a species of Psyttalia, a parasitoid of tephritid fruit flies in Kenya, was investigated. Individuals reared from coffee infested with Ceratitis capitata (Wiedemann) (Medfly) and two other tephritid species in Kenya were compared with individuals of Psyttalia concolor (Szépligeti) from a laboratory culture in Italy used in augmentative biological control of olive fly, Bactrocera oleae (Gmelin). Reciprocal crosses showed full compatibility, with production of viable female offspring. A preliminary morphometric analysis demonstrated that most individuals originating from Italy could be separated from most of those from Kenya based largely on differences in overall size.     

Relation of fruit color,elongation, hardness,and volume to the infestation of olive cultivars by the olive fruit fly,Bactrocera oleae

The susceptibility of olive cultivars to the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), has seldom been studied. This article examines factors associated with olive fruit fly infestation of 16 commonly planted Sicilian olive cultivars. Total infestation data were simultaneously correlated with categorical and quantitative factors using ordinal logistic regression. When all factors were included in the analysis, year, sampling date, cultivar, and fruit color were highly significant, but the quantitative factors fruit volume, fruit elongation, and fruit hardness were not. When the analysis was repeated excluding cultivar, all quantitative factors were significant, and elongation and volume were highly significant. Spherical, large, and hard fruit seemed to be preferred by B. oleae over fruit that are elongate, small, and soft. Therefore, fruit color, elongation, volume, and hardness provide useful information regarding the susceptibility of cultivars. In both organic and conventional olive cultivation, information about olive cultivar susceptibility to olive fruit fly will help orchard managers to produce quality oil and table olives while reducing treatments for olive fruit fly control.     

Evaluating potential sugar food sources from the olive grove agroecosystems for Prays oleae parasitoid Chelonus elaeaphilus

Chelonus elaeaphilus Silvestri (Hymenoptera: Braconidae) is a host-specific parasitoid of the olive moth, Prays oleae (Bernard), that can cause parasitism rates of up to 80% in Mediterranean olive groves. A laboratory study was carried out to assess the potential of sugars provided by wild plant species in olive grove agroecosystem to enhance the fitness of C. elaeaphilus. Insects were reared in a climate-controlled chamber at 25?±?2°C, 60?±?5% relative humidity (RH) with a photoperiod of 16:8 (L:D) h. Five naturally occurring wild plant nectar sugars (sucrose, fructose, glucose, maltose and mannose) were tested for their effect on insect longevity. The nectar sugar content of sucrose, fructose and glucose in 12 selected olive grove agroecosystem plant species was analysed and categorised on the basis of sugar ratios. Female insect longevity was increased when they were fed on both sucrose and glucose compared to either maltose or fructose, suggesting that sucrose-dominant nectars would bene?t this parasitoid. Sucrose was predominant in the nectar of five of the studied plant species (Silene gallica, Borago officinalis, Echium plantagineum, Lavandula stoechas and Lonicera hispânica). The results are discussed in terms of potential enhancement of the biological control of P. oleae.     

Brood size, sex ratio and egg load of Metaphycus lounsburyi (Hymenoptera: Encyrtidae) when parasitizing adult females of black scale Saissetia oleae (Hemiptera: Coccidae) in the field

Black scale Saissetia oleae (Olivier) (Hemiptera: Coccidae) is a widespread olive pest in California and Europe. Metaphycus lounsburyi (Howard) (Hymenoptera: Encyrtidae) is often one of its main parasitoids. Augmentative releases of M. lounsburyi have been proposed in those areas in which biological control is ineffective. In this paper, we study the relationship between black scale and M. lounsburyi in the field. According to our data, M. lounsburyi parasitizes mainly ovipositing females of black scale. Parasitism rates of ovipositing females reach high levels. In those scales, M. lounsburyi develops as a gregarious parasitoid, with an average of 13 and a maximum of 40 parasitoids developing per scale. The secondary sex ratio is female biased (proportion of males = 0.13) and appears to be brood size dependent. Metaphycus lounsburyi eggs are encyrtiform; however, its egg load is much higher than other Metaphycus that also parasitize black scale. The implications of these results on the behavioral ecology of M. lounsburyi and its use in biological control of black scale are discussed.     

Natural establishment of a parasitoid complex on Bactrocera latifrons (Diptera: Tephritidae) in Hawaii

Bactrocera latifrons (Hendel) (Diptera: Tephritidae) is the most recent of four tephritid fruit fly species accidentally introduced into Hawaii. Although parasitoids have been released against other tephritid fruit fly species and have shown partial success in Hawaii, no parasitoids were released until 2004 to suppress populations of B. latifrons. The present study was conducted to document the parasitoid complex that has naturally established against B. latifrons in Hawaii and to assess whether there is a need for improving the biological control of this species. Based on ripe turkeyberry (Solanum torvum Sw) fruit collections over three consecutive years B. latifrons was the dominant tephritid fruit fly infestating turkeyberry at all four sites surveyed, across three major islands in Hawaii. The overall percentage parasitism of B. latifrons ranged from a low of 0.8% (Hana, Maui) to a high of 8.8% (Kahaluu, Oahu). Five primary parasitoid species were recovered from individually held B. latifrons puparia: Fopius arisanus (Sonan), Psyttalia incisi (Silvestri), Diachasmimorpha longicaudata (Ashmead), D. tryoni (Cameron), and Tetrastichus giffardianus Silvestri. F. arisanus was the predominant parasitoid at three of the four sites. Low levels of parasitism suggest that there is a need to improve biological control of B. latifrons, to minimize chances of this species causing economic impacts on crop production in Hawaii. We discuss the possibility of improving biological control of B. latifrons through augmentative releases of F. arisanus or introduction and release of specific and efficient new parasitoid species.