Aphytis Melinus Research Articles

Florida red scale, Chrysomphalus aonidum (Linnaeus, 1758) (Hemiptera: Diaspididae) in Morocco, infesting citrus orchards and an avocado tree

AbstractA study was conducted on citrus and avocado trees in north‐western Morocco between February 2023 and April 2024 to detect scale insects (Hemiptera: Coccomorpha) and their associated natural enemies. A total of 55 orchards in seven provinces were studied. The Florida red scale, Chrysomphalus aonidum (Linnaeus, 1758) (Diaspididae) was found on leaves at two sites: a moderate infestation in one citrus orchard and one specimen on an avocado tree. This work is the first record of the scale insect on avocado in Morocco, and the first morphological description of C. aonidum from the country, based on 100 adult females mounted on microscope slides. Chrysomphalus aonidum is not causing economic damage in citrus or avocado orchards in Morocco. Two ectoparasitoid wasps (Aphytis melinus DeBach and Aphytis sp.; Hymenoptera: Aphelinidae), and three predatory beetles (Rhyzobius lophanthae Blaisdell, Chilocorus bipustulatus Linnaeus, and Clitostethus arcuatus Rosso; Coleoptera: Coccinellidae), were found associated with C. aonidum on citrus leaves.

Toxicity of insecticides to Aphytis melinus, 2011

Toxicity of insecticides to Aphytis melinus, 2011

Toxicity of insecticides to Aphytis melinus, 2014

Toxicity of insecticides to Aphytis melinus, 2014

Toxicity of insecticides to Aphytis melinus, 2016

Toxicity of insecticides to Aphytis melinus, 2016

Ecological relationship between Lepidosaphes beckii (Newman, 1869) (Homoptera Diaspididae) and its two parasitoids Aphytis melinus DeBach, 1959 and A. lepidosaphes Compere, 1955 (Hymenoptera Aphelinidae) on lemons orchads in two localities of Mitidja Algeria

Yasmina Agagna1, Khadidja Boudjemaa1, Narimene Oussalah1, Ibtissem Beloued1, Khaoula Aroua2 & Mohamed Biche

Biology of an Adventive Population of the Armored Scale Rhizaspidiotus donacis, a Biological Control Agent of Arundo donax in California

Simple SummaryThe invasive giant reed, Arundo donax, impacts river ecosystems world-wide. The plant-feeding scale insect Rhizapidiotus donacis is approved for biocontrol use in North America but a wild (adventive) population was found in southern California. We studied the adventive scale to document its distribution, life history, relatedness to European samples, risk to a native reed, and ability of a biocontrol wasp to develop within it. The adventive was found within a single watershed and is genetically closest to the Iberian scale population. Rhizaspidiotus donacis developed on some Phragmites reed types, but at lower densities than Arundo. It produces one generation each year with mobile juveniles from March through June. Aphytis melinus wasps showed similar interest in adventive R. donacis as their usual host with deposited eggs developing into a second generation. Rhizaspidiotus donacis appears limited in distribution by its life history, precluding broad biocontrol implementation through natural dispersal but allowing for targeted application. The genetic differentiation between imported biocontrol samples and adventive populations presents an opportunity for exploring benefits of hybrids and/or alternative genotypes where establishment has been difficult. While likely rare in the wild, spillover to vulnerable endemic Phragmites or deleterious parasitoid effects on scale populations warrants consideration when planning use of this agent.Arundo donax (giant reed) is invasive in Mediterranean, sub-, and tropical riparian systems worldwide. The armored scale Rhizaspidiotus donacis is approved for biocontrol in North America, but an adventive population was recently discovered in southern California. We documented this population’s distribution, phylogeny, phenology, potential host spillover to Phragmites spp., and potential for parasitism by a common biocontrol parasitoid of citrus scale. The adventive scale was found within a single watershed and is genetically closest to Iberian scale genotypes. Rhizaspidiotus donacis developed on Phragmites haplotypes but at much lower densities than Arundo. The adventive population is univoltine, producing crawlers from March-June. Aphytis melinus parasitoids exhibited sustained interest in R. donacis during choice and no-choice trials and oviposition resulted in a small second generation. Rhizaspidiotus donacis appears limited in distribution by its univoltinism and sessile adult females. This presents challenges for broad biocontrol implementation but allows for targeted application. The genetic differentiation between imported biocontrol samples and adventive populations presents an opportunity for exploring benefits of hybrids and/or alternative genotypes where establishment has been difficult. While unlikely to occur in situ, spillover to vulnerable endemic Phragmites or deleterious parasitoid effects on scale biocontrol agents warrants consideration when planning use of R. donacis.

Morphometric comparison between two populations of Aonidiella aurantii (Maskell) (Homoptera: Diaspididae) from Algeria and Turkey

The size of California red scale Aonidiella aurantii (Maskell, 1879) (Homoptera: Diaspididae) is the most reliable indicator in terms of host quality for Aphytis melinus (DeBach, 1959) (Hymenoptera: Aphelinidae) as well as for the efficiency of its biological control. Our study consisted in comparing the cover and body size of each scale developmental stage belonging to two different populations: one from Algeria and the other one from Turkey. The two scale populations were taken from lemon trees during 3 months. We compared measurements between the two localities and also between the plant organs. The larger individuals were those from Algeria. The same results were confirmed through the plant substrate on which scale was fixed: this size variation observed is mainly explained by climatic variations between the two countries and its repercussions on phenology and metabolism of the host plant. In addition, a higher parasitism rate was noticed in the Algerian scale population compared to that of Turkey.

Age-specific life tables of Aonidiellaaurantii (Maskell) (Hemiptera: Diaspididae) and its parasitoid Aphytismelinus DeBach (Hymenoptera: Aphelinidae)

Biological parameters of the California red scale (Aonidiella aurantii [Maskell] [Hemiptera: Diaspididae]) were determined under laboratory conditions at 3 different temperatures (20, 23, and 27 °C) on butternut squash (Cucurbita moschata Duchesne ex Lamarck) (Cucurbitaceae), while the biological parameters of its parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae) were conducted at 27 °C. The survival of A.a aurantii ranged between 80.0% and 88.3%. The highest mortality was recorded during the adult stage, with mortalities ranging between 12% and 20%. On C. moschata, the total development time was 93.1 ± 9.73, 81.8 ± 7.13, and 65.7 ± 6.37 days, while the adult longevity was 54.65 ± 0.71, 47.05 ± 0.97, and 39.35 ± 1.07 days at 20, 23, and 27 °C, respectively. The oviposition period of A. aurantii was 44.3 ± 0.51, 40.65 ± 0.41, and 34.5 ± 0.45 days at 20, 23, and 27 °C, respectively. Average fecundity was 73.25 ± 1.827, 109.7 ± 3.569, and 129.35 ± 4.564 individuals at 20, 23, and 27 °C, respectively. For A. melinus, adult longevity was 19.24 ± 0.73 days, and average fecundity 62.7 ± 2.81 eggs at 27 °C. The preoviposition period was 0.82 ± 0.05 days, oviposition period was 15.7 ± 0.52 days, and postoviposition period was 2.21 ± 0.09 days. The intrinsic rate of increase (rm) of A. melinus (0.188 ♀/♀/day) was significantly greater than that of A. aurantii (0.080) at 27 °C. These laboratory results demonstrated that A. melinus is an effective parasitoid for decreasing A. aurantii populations. Fecundity of A. aurantii and A. melinus was determined with the Enkegaard equation. The best-fit parameters of fecundity were calculated as a = 0.410, b = 0.099; a = 0.624, b = 0.098; a = 0.661, b = 0.091; a = 1.190, b = 0.179 for A. aurantii at 20, 23, and 27 °C, and A. melinus at 27 °C, respectively.

Evaluation of d-Limonene and β-Ocimene as Attractants of Aphytis melinus (Hymenoptera: Aphelinidae), a Parasitoid of Aonidiella aurantii (Hemiptera: Diaspididae) on Citrus spp.

The volatile organic compounds (VOCs) released from herbivore-infested plants can be used as chemical signals by parasitoids during host location. In this research, we investigated the VOC chemical signals for the parasitoid Aphytis melinus to discriminate between Aonidiella aurantii (California red scale)-infested fruit and non-infested fruit on three different citrus species. First, we identified the chemical stimuli emanating from non-infested and A. aurantii-infested citrus fruits via solid phase microextraction (SPME) and gas chromatography-mass spectrometry (GC-MS) analyses and identified 34 volatile organic compounds (VOCs). The GC-MS analysis showed qualitative and quantitative differences between VOCs emitted from non-infested and infested citrus fruit. Two VOCs, d-limonene and β-ocimene, were significantly increased in all infested fruit, regardless of the fruit species. The response of the female adult A. melinus to olfactory cues associated with A. aurantii infested fruit was evaluated using a Y-tube olfactometer. In two-choice behavioural assays, A. melinus females preferred infested citrus cues over non-infested fruit. Females showed positive chemotaxis toward these VOCs in all tested combinations involving two dosages of synthetic compounds, d-limonene and β-ocimene, except for d-limonene at a dosage of 10 μL/mL. The application of these VOCs may help to enhance the effectiveness of bio-control programs and parasitoid mass-rearing techniques.

Evolution of glandular structures on the scape of males in the genus Aphelinus Dalman (Hymenoptera, Aphelinidae)

The pores and associated glands on male antennae in species of Hymenoptera are involved in mate recognition and are diverse and widespread among taxa. However, nothing has been published about these structures in species ofAphelinus(Chalcidoidea: Aphelinidae), a genus of parasitoid wasps with a long history in biological control. Images from scanning electron microscopy (SEM) and transmission electron microscopy (TEM) ofAphelinus varipesrevealed pores on the ventral side of the male scape that were connected to glands. A survey of the scapes of male antennae in 16 species in six species complexes ofAphelinus, as well as two outgroup species,Aphytis melinusandCentrodorasp., showed that pores were present in all exceptCentrodorasp. The pores varied in several characters: the shape of the structures that carried them, pore size, elevation of the cuticle surrounding the structures, the extent of a carina delimiting the area around the structures, and the number and position of pores. The shape of the pore-bearing structures, the elevation of cuticle around these structures, and the extent of the carina around them map well onto a molecular phylogeny of theseAphelinusspecies. Combinations of pore characters are diagnostic of species complexes, and in some cases, species ofAphelinus.

Genome-wide analyses of single nucleotide polymorphisms reveal the consequences of traditional mass-rearing on genetic variation in Aphytis melinus (Hymenoptera: Aphelinidae): the danger of putting all eggs in one basket.

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) is a highly effective biocontrol agent of the California red scale Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae). It is commercially reared and used for augmentative releases within integrated pest management programs. However, mass rearing of biocontrol agents can result in population bottlenecks and high levels of inbreeding and/or adaptation to the factitious rearing conditions. Although these factors can all negatively impact field performance of biocontrol agents, few empirical studies have examined the genetic consequences of mass rearing. We used double-digest RAD sequencing (ddRADseq) to investigate the effect of traditional mass rearing on genetic variation among insectary colonies of A. melinus relative to wild populations in native (Pakistan) and introduced (California) ranges. Analyses of up to 9700 single nucleotide polymorphisms (SNPs) revealed that insectary populations had less genomic variation than introduced populations. This was evidenced by fewer private alleles, reduced heterozygosity, and greater missing data in the insectary populations. Further, California insectaries formed a distinct genomic cluster relative to the other samples, a surprising result given that the insectary colonies were putatively established at different times and from different source populations. These differences were evident across most data sets also after we filtered out contaminant DNA from the most common host species (Aspidiotus nerii Bouché and A. aurantii). We hypothesize that this pattern would only result if: (i) directional selection for 'captive' phenotypes produces convergent patterns of genomic variation across insectaries; or (ii) the California insectary colonies were all founded from a unifying source population and/or that the insectaries regularly exchange 'genetic' stocks. We show that RADseq is an effective method to investigate the effects of mass rearing on genetics of biocontrol agents. © 2019 Society of Chemical Industry.

Behavioural responses of the parasitoid Aphytis melinus to volatiles organic compounds (VOCs) from Aonidiella aurantii on its host fruit Tahitian lime fruit Citrus latifolia

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) is a parasitoid of Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae). However, the cues used by A. melinus for host location have not been extensively investigated. Many studies have shown that mating parasitoids are strongly attracted by specific volatiles from infested plants. This paper investigated the response of A. melinus to volatiles from Tahitian lime fruit infested with A. aurantii through two-choice olfactometer bioassays. First, we identified the chemicals emitting from non-infested and A. aurantii-infested lime fruit via gas chromatography-mass spectrometry analyses and solid phase microextraction and identified 26 volatile organic compounds (VOCs). Eighteen of these were increased by A. aurantii infestation, and one was decreased, whereas five compounds were produced exclusively from infested fruit. Innate positive chemotaxis of mating A. melinus females toward lime fruit and their VOCs was then tested in olfactometer assays. Compared to the control without fruit, female A. melinus showed significantly greater attraction to healthy and A. aurantii-infested lime fruit, while there were no significant differences in the attraction of the parasitoid between healthy fruit or fruit infested with the second and third instar of A. aurantii. Among the two synthetic compounds tested, d-limonene and β-ocimene elicited a strong attraction for parasitoids at tested dosages (15 μl/ml), indicating an intrinsic response to this compound as a short-range attractant. Results from this study suggest that A. melinus parasitoids mainly rely on olfactory cues in host habitat location and that d-limonene and β-ocimene are the major attractants in infested fruit volatiles. Practically, field applications of this volatile may play a significant role in attracting more A. melinus to enhance the efficiency of biological control of A. aurantii in the future.

Negative effect of global warming on biological control is mitigated by direct competition between sympatric parasitoids

Parasitoids are among the most important and successful groups of natural enemies used in the biological control of insect pests. In most systems, several parasitoid species can parasitize the same pest. The coexistence of parasitoids in agroecosystems and their efficacy as biological control agents may be disrupted by global warming. An increase of approximately 3 °C is predicted by the end of the twenty-first century in the Mediterranean basin (IPCC, 2014). In this context, we compared the present and future performance of two sympatric parasitoids of the genus Aphytis (Hymenoptera: Aphelinidae), which control the armoured scale Aonidiella aurantii (Hemiptera: Diaspididae) in Mediterranean citrus, either alone or in combination. The net reproductive rate (R0) of the introduced Aphytis melinus DeBach was higher than that of its competitor, the native Aphytis chrysomphali (Mercet), under current conditions. The two parasitoids responded differently to higher temperature and competition. The R0 of A. chrysomphali decreased by 50% when both parasitoids competed in the same patch, but was not affected by the temperature increase. The R0 of A. melinus decreased approximately 46% with the increase in temperature because the proportion of females was reduced. However, the presence of A. chrysomphali competing in the same patch mitigated the negative effect of the increase in temperature on A. melinus (R0 decreased by only 16%). Overall, our results suggest that global warming will have a negative effect on the biological control of A. aurantii and that this effect will be higher in areas, such as southern Spain, where A. melinus has displaced A. chrysomphali.

Effect of host instar on host discrimination of heterospecific‐parasitised hosts by sympatric parasitoids

1. Interspecific competition among hymenopteran parasitoids may shape their behavioural strategies for host resource exploitation. In order to reduce or prevent competition, many parasitoid species have evolved the ability to discriminate between unparasitised hosts and hosts parasitised by another parasitoid species (i.e. heterospecific host discrimination). However, discriminatory ability might be affected by host instar.2. This study reports the first results on whether host instar can influence the use of heterospecific‐parasitised hosts by sympatric parasitoids of the genus Aphytis (Hymenoptera: Aphelinidae).3. Aphytis melinus and Aphytis chrysomphali discriminated between unparasitised and heterospecific‐parasitised hosts when they found a third‐instar host (high quality), with a tendency to multi‐parasitise. However, this discrimination was not observed in the second instar (lower size).4. The behavioural strategies adopted towards multi‐parasitise third‐instar hosts varied between both species. Aphytis chrysomphali reduced its clutch size in heterospecific‐parasitised hosts, whereas A. melinus tended to probe them for longer than healthy hosts.5. Overall, our results highlight the importance of host instar in the study of intrinsic competition between parasitoids.

Overstinging by hymenopteran parasitoids causes mutilation and surplus killing of hosts

An appraisal of the regulatory role of natural enemies on target pests requires the identification of the mechanisms/traits that enhance the ability of an organism to control the density of its prey/host. After stinging herbivore hosts with their ovipositor, hymenopteran parasitoids tend to reject them without ovipositing or host-feeding. Termed pseudoparasitism, the frequency and consequences of this type of attack (hereafter oversting) have been largely disregarded in the hymenopteran parasitoid literature. We choose the parasitoids Aphytis melinus and A. chrysomphali and their common host Aonidiella aurantii as a model system to study this behavior. Using field and laboratory observations, we showed that overstinging is a common behavior in the wild. Under controlled conditions, overstinging occurred more frequently than host-feeding, a behavioral trait that is used to evaluate the potential of parasitoids as biological control agents. Oversting reduced the fecundity and survival of the herbivore host. When we compared between parasitoid species that attack the same host species, the virulence and frequency of this behavior depended on parasitoid species. These results demonstrate that overstinging should be incorporated in the models of host–parasitoid interactions to analyze population dynamics as well as in the future selection of parasitoids for biological control.

Does host quality dictate the outcome of interference competition between sympatric parasitoids? Effects on their coexistence

The suitability and quality of herbivorous insect hosts for hymenopteran parasitoids is dynamic, varying with host development. Generally, within a host species, large hosts (i.e. older instars) are considered of higher quality for parasitoid development. Studies of interspecific competition between parasitoids have considered the effect of host instar on indirect competition but its effect on interference competition remains unknown. Here, we report the first results on whether the quality of host instars might dictate the outcome of interference competition between sympatric parasitoids of the genus Aphytis (Hymenoptera: Aphelinidae) when they attack low-quality (second) and high-quality (third) instars of their common host Aonidiella aurantii (Hemiptera: Diaspididae). Oviposition behaviour (host acceptance and clutch size) in low- and high-quality host instars was similar for both Aphytis species in the absence of competition. When they found heterospecific parasitized hosts of high quality, Aphytis melinus laid more eggs and accepted significantly more hosts than Aphytis chrysomphali, whereas there were no significant differences in the low-quality instar. This result suggests that interference competition is mediated by host quality. However, the progeny proportion of both parasitoids in multiparasitized hosts (outcome of competition) was independent of host quality and A. melinus always emerged at higher rates. Therefore, the result of interference competition between these sympatric parasitoids was not affected by host quality and this competition will contribute to the displacement of the native A. chrysomphali by the introduced A. melinus, which has been observed in some areas of the Mediterranean basin.

Uniformity of petroleum-derived spray oils: lethal and sublethal effects on a herbivore pest and its parasitoid

Petroleum-derived spray oils (PDSO) are widely used and recommended in many integrate pest management programmes and in organic agriculture against several pests. However, there are numerous discrepancies in their efficacy against pests and, more interestingly, in their side effects on natural enemies. In the present study, we used the citrus key pest Aonidiella aurantii Maskell (Hemiptera: Diaspididae) and its main parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinedae) as models to evaluate both the lethal and sublethal effects of four commercial PDSO on different instars of the herbivore, as well as on the adult and immature stages of the parasitoid. The four PDSOs displayed similarly high mortalities against young instars of A. aurantii. However, most adult females survived all PDSO applications, and the fecundity of the surviving females was not altered. PDSOs were harmless to the parasitoid A. melinus because the survival (acute toxicity), longevity and fecundity of the surviving adults (sublethal effects) were not affected. Similarly, immature emergence was not affected by any of the four PDSOs after spraying the parasitized hosts. Overall, the results of the present study confirm the environmental-friendly profile of PDSOs against natural enemies and demonstrate a similar performance for PDSOs when they were correctly sprayed under the same conditions.

Evaluating the Performance and Preference of Aphytis melinus (Hymenoptera: Aphelinidae) on an Exotic Species, Acutaspis albopicta (Hemiptera: Diaspididae), and Aonidiella aurantii (Hemiptera: Diaspididae).

Acutaspis albopicta (Cockerell) is an exotic scale detected on imported ‘Hass’ avocados arriving in California from Mexico. An effort was made to understand how well this species might be biologically controlled by the parasitoid, Aphytis melinus DeBach. In no-choice trials, single life stages of A. albopicta and Aonidiella aurantii (Maskell) were exposed to one Ap. melinus female. Ap. melinus attacked and developed to adult on all A. albopicta life stages tested, which included early, middle, and late male and female second instars, and early, middle, and late female third instars. However, the proportion of scales attacked was relatively low (≤20%), as were the number of eggs laid on each scale stage. In six of seven comparisons of scale cover surface area between A. albopicta and Ao. aurantii that were similarly aged, Ao. aurantii was significantly larger. With intraspecific choice trials, females of Ap. melinus strongly preferred to parasitize the oldest and largest female scales in both single- and mixed-sex offerings. Younger, smaller scales were preferred for host feeding. Five comparisons of preference between A. albopicta and Ao. aurantii showed that Ap. melinus preferred 28- and 36-d-old Ao. aurantii females over similarly aged A. albopicta. However, Ap. melinus preferred 23-d-old males of A. albopicta. In three of five comparisons, Ao. aurantii was the preferred species to host feed on. More F1 females of Ap. melinus were recovered from both intraspecific choice trials compared with any stage in no-choice trials. Implications of incorporating Ap. melinus into biological control programs are discussed.

Diaspididae (Hemiptera: Coccoidea) of Important Species on Citrus Orchards in Antalya Province and Their Natural Enemies Population Fluctuations

In this study population fluctuations of important species of Diaspididae and their natural enemies were investigated in the mandarin, grapefruit, orange and lemon orchards of BATEM (West Mediterranean Agricultural Research Institute) in 2011-2012 years. As a result, Aonidiella aurantii (Maskell), Aonidiella citrina (Craw), Parlatoria pergandii Comstock species of scale insects were found. Natural enemies determined in the study were Chilocorus bipustulatus (L.) and Oenopiaconglobata (L.) (Coleoptera: Coccinellidae) as predators, and Aphytis melinus DeBach and Encarsia spp. (Hymenoptera: Aphelinidae) as parasitoids. In this study, population fluctuation of A. aurantii, A. citrina and P. pergandii, C. bipustulatus and O. conglobata, A. melinus and Encarsia spp. as their natural enemies,were investigated.

Effect of the California red scale Aonidiella aurantii sex pheromone on the natural parasitism by Aphytis spp. in Mediterranean citrus

Mating disruption has proved successful against California red scale (CRS), Aonidiella aurantii Maskell (Hemiptera: Diaspididae) in Mediterranean citrus. Although mating disruption does not affect negatively the parasitism by Aphytis melinus DeBach (Hymenoptera: Aphelinidae), a CRS parasitoid introduced to the Mediterranean, there is no information regarding its potential effect on the native Aphytis species. In the present study, the effect of CRS mating disruption on the field parasitism inflicted by Aphytis spp. has been assessed and compared to a mineral oil and a control treatment. In order to confirm the effectiveness of the mating disruption we also evaluated its effect on the captures of the CRS males and on fruit infestation. Moreover, the potential role of the CRS sex pheromone as kairomone for the Aphytis species was also evaluated by comparing captures of parasitoids on sticky traps with or without pheromone. Significantly lower CRS male captures and fruit damage were registered in the mating disruption respect to the control or oil treatments indicating that mating disruption was effective. In September, when compared to the control, parasitism by Aphytis spp. was significantly lower in the mating disruption and mineral oil treatments and crucially no Aphytis chrysomphali Mercet were registered in the mating disruption treatment. Finally, while the captures of both A. melinus and Aphytis lepidosaphes (Mercet) were not significantly different between traps with or without pheromone, A. chrysomphali captures were significantly higher in traps baited with CRS pheromone. These results suggest a possible kairomonal effect of the CRS pheromone on A. chrysomphali.