Development, survival, and reproduction of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae) at different constant temperatures

Development, survival, and reproduction of the predatory mite Kampimodromus aberrans Oudemans were studied at constant temperatures in the range from 15 to 35 degrees C under laboratory conditions. Larval developmental rate for both males and females increased gradually from 15 to 35 degrees C and decreased at higher temperatures. Lactin's nonlinear model described with adequate accuracy the relationship between developmental rate and temperature. The model predicted that lower and upper threshold temperatures for preimaginal development ranged from 9.8 to 11.8 degrees C and from 37.2 to 39.8 degrees C, respectively. The intrinsic rate of population increase (rm) at the different temperatures ranged from 0.0442 to 0.1575, with the highest value recorded at 25 degrees C. At 33 degrees C a negative rm value was estimated. The rm values determined at different temperatures were fitted to Lactin's nonlinear model, and the lower and upper threshold and the optimal temperatures for population increase were 10.5, 32.4, and 27.6 degrees C, respectively. These data indicate that K. aberrans may be better adapted to intermediate temperatures around 27 degrees C and, therefore, could be a useful biocontrol agent of spider mites during spring and early summer when such temperatures are prevalent in northern Greece. The results could also be useful in developing a population model for K. aberrans under field conditions.     

A single nucleotide polymorphism in the acetylcholinesterase gene of the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae) is associated with chlorpyrifos resistance

The predatory mite Kampimodromus aberrans (Oudemans) (Acari: Phytoseiidae) is one of the most important biocontrol agents of herbivorous mites in European perennial crops. The use of pesticides, such as organophosphate insecticides (OPs), is a major threat to the success of biocontrol strategies based on predatory mites in these cropping systems. However, resistance to OPs in K. aberrans has recently been reported. The present study investigated the target site resistance mechanisms that are potentially involved in OP insensitivity. In the herbivorous mite Tetranychus urticae Koch (Acari: Tetranychidae), resistance to OPs is due to a modified and insensitive acetylcholinesterase (AChE; EC: 3.1.1.7) that bears amino acid substitution F331W (AChE Torpedo numbering). To determine whether the predators and prey have evolved analogous molecular mechanisms to withstand the same selective pressure, the AChE cDNA from a putative orthologous gene was cloned and sequenced from susceptible and resistant strains of K. aberrans. No synonymous mutation coding for a G119S substitution was determined to be strongly associated with the resistant phenotype instead of the alternative F331W. Because the same mutation in T. urticae AChE was not associated with comparable levels of chlorpyrifos resistance, the role of the G119S substitution in defining insensitive AChE in K. aberrans remains unclear. G119S AChE genotyping can be useful in ecological studies that trace the fate of resistant strains after field release or in marker-assisted selection of improved populations of K. aberrans to achieve multiple resistance phenotypes through gene pyramiding. The latent complexity of the target site resistance in K. aberrans vs. that of T. urticae is also discussed in the context of data from the genome project of the predatory mite Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae).     

Resistance to chlorpyriphos in the predatory mite Kampimodromus aberrans

The predatory mite Kampimodromus aberrans (Oudemans) is a key biocontrol agent in vineyards in Italy and Southern Europe. Its susceptibility to common pesticides (e.g., organophosphates) has been considered an important factor in preventing successful biocontrol of phytophagous mites. Nevertheless, populations of K. aberrans apparently resistant to organophosphates (OPs) have been reported to occur in Northern Italian vineyards. The resistance of K. aberrans to fungicides (e.g., mancozeb) has been demonstrated in the laboratory in France, but little is known about the toxicity of insecticides towards K. aberrans. Of these pesticides, the OP chlorpyriphos is extensively used in viticulture to control lepidopterans and homopterans. The present study investigated the dose–response effect of chlorpyriphos in four K. aberrans strains characterized by different levels of exposure to OP insecticides in the past: from never to frequently exposed. Resistance to chlorpyriphos is demonstrated for populations collected from vineyards and apple orchards. Resistance factors exceeded 145,000× for the three strains collected in vineyards and orchard. LC₅₀ values for resistant strains were 1.85–6.83 times higher than the recommended field dose of chlorpyriphos for vineyards and orchards (525 mg a.i./l).     

The predatory mite Typhlodromus pyri (Acari: Phytoseiidae) causes feeding scars on leaves and fruits of apple

Typhlodromus pyri Scheuten (Acari: Phytoseiidae) is the most important predator of Panonychus ulmi (Koch) (Acari: Tetranychidae) in orchards and vineyards. It was recently found that adult T. pyri females cause microscopic scars on apple leaves. The present laboratory experiments were carried out to confirm the production of scars on apple leaves and to assess if females cause scars on fruits as well. Scar production on apple leaves and/or fruits was investigated under various nutritional conditions: no food, pollen of Scots pine (Pinus sylvsestris L.) only, nymphs of P. ulmi only, and pollen + prey. Both on leaves and fruits, either offered alone or in combination, feeding scars were produced under all nutritional conditions, but mostly in the 'no food' treatment. The predators consumed significantly more P. ulmi nymphs when offered alone than when offered in combination with pollen. T. pyri laid eggs under all nutritional conditions, but mostly in the 'pollen + prey' treatment and least when no food was offered. T. pyri females caused scars on both leaves and fruits when offered simultaneously, but more on leaves than on fruits. The scars were also bigger on leaves than on fruits in all experiments. T. pyri survived and reproduced on plant material in the absence of other food sources. Whether the scars produced on leaves and fruits harm the quality of fruits or the yield of apple cannot be concluded from the present experiments.     

Life History of Kampimodromus aberrans as a predator of Phytoptus avellanae (Acari: Phytoseiidae, Phytoptidae)

The biology of Kampimodromus aberrans (Oudemans), a predator of the big bud mite, Phytoptus avellanae Nalepa, was studied under laboratory conditions. All experiments were conducted on hazelnut leaf discs in an incubator at 25 ± 1 °C, with 16:8 h L:D, at an average daily relative air humidity of 76%. Observations were made twice daily for the immature stages and daily for the adults to determine developmental time, survival and fecundity. The mean developmental time for females was 6.90 days and for males was 7.10 days, and mean adult longevity for females was 11.67 days. The mean total and daily egg production were 12.67 and 1.85 eggs, respectively. The net reproduction rate (R₀) was 7.09 females/female, intrinsic rate of increase (r_m) was 0.153 female/female/day and mean generation time (T₀) was 12.80 days. The mortality rate of immature stages was 0.66% and the sex ratio was 0.51 female.     

Rapid cold hardening in the predatory mite Euseius (Amblyseius) finlandicus (Acari: Phytoseiidae)

A rapid cold hardening response was studied in diapause and non-diapause females of the predatory mite Euseius finlandicus. When laboratory reared diapause and non-diapause females were transferred and maintained from the rearing temperature of 20 degrees C for 2 h to -11.5 degrees C and -10 degrees C, 10 to 20% survived respectively. However, conditioning of diapause females for 4 h at a range of temperatures from 0 to 10 degrees C before their exposure for 2 h to -11.5 degrees C, increased survival to approximately 90%. Similarly, conditioning of non-diapause females for 4 h at 5 degrees C before their exposure for 2 h to -10 degrees C increased survival to 90%. A similar rapid cold hardening response in both diapause and non-diapause females was also induced through gradual cooling of the mites, at a rate of approximately 0.4 degrees C per min. The rapid increase in cold tolerance after prior conditioning of the mites to low temperatures, was rapidly lost when they returned to a higher temperature of 20 degrees C. Rapid cold hardening extended the survival time of diapause and non-diapause females at sub-zero temperatures. The cost of rapid cold hardening in reproductive potential after diapause termination was negligible. In non-diapause females, however, the increase in cold tolerance gained through gradual cooling could not prevent cold shock injuries, as both fecundity and survival were reduced.     

Side-effects of three pesticides on the predatory mite, Phytoseiulus persimilis (Acari: Phytoseiidae)

Side-effects of three commonly used pesticides in Iran were evaluated on an introduced strain of the predatory mite. Phytoseiulus persimilis Athias-Henriot, reared for about 10 years without exposure to any pesticides. Application of pesticides was carried out either to detached bean leaves using a Potter tower at 1 mg wet deposit per cm2 or by a hand sprayer on bean plants until run off. According to an EPPO decision making scheme, pirimiphos-methyl was found to be harmful (E=90.8%) and heptenophos harmless (E=-3.7%) to the predatory mite in the residual initial toxicity tests. For determination of the hazard class of malathion a field test was found to be necessary (E=59.8%). Categories of 1, 2, 3 were determined for heptenophos, malathion and primiphos-methyl, respectively, using IOBC classification. Despite being harmful, it is possible to use pirimiphos-methyl 10 days before release of P. persimilis. Investigation of the contribution of both lethal and sub-lethal effects to total impact indicated the dominance of lethality in the case of pirimiphos-methyl, while malathion acted by both mechanisms. Heptenophos did not have negative effects on fecundity of P. persimilis but rather caused a higher rate of fecundity in comparison with the control. The mortality found in the heptenophos test was not significantly different from the control.     

Factors determining species displacement of related predatory mite species (Acari: Phytoseiidae)

Neoseiulus womersleyi (Acari: Phytoseiidae) used to be the dominant species in fruit-tree orchards throughout Japan, but starting in the 1990s, N. womersleyi began to be displaced by Neoseiulus californicus in central and southwestern Japan. The present study was conducted to examine factors explaining the displacement of N. womersleyi by N. californicus. First, we confirmed under laboratory conditions that N. californicus could exclude N. womersleyi if they initially coexisted in a 1:1 ratio. During a 2-h continuous observation period, none of the heterospecific pairs had copulated and after 5 days together with heterospecific males, none of the females had laid eggs. When these females were placed with conspecific males, normal numbers of offspring were produced. Moreover, conspecific matings were not substantially disturbed in the presence of heterospecific males or females. Total fecundity was significantly lower in N. womersleyi than in N. californicus, but their r _m values did not differ from each other. On the other hand, the frequency of intraguild predation by N. californicus on N. womersleyi was significantly higher than vice versa. From these results, we concluded that not reproductive interference nor differential female fecundity but asymmetrical intraguild predation seemed to explain the competitive exclusion of N. womersleyi by N. californicus.     

Biological studies of the Australian predatory mite Typhlodromalus lailae (Schicha) (Acari: Phytoseiidae)

Abstract The biology of the Australian phytoseiid mite Typhlodromalus lailae is described from material collected in Western Australia and New South Wales in 1994. At 25°C, when fed on cumbungi ( Typha sp.) pollen, the life cycle is completed in approximately 6 days, with an intrinsic rate of natural increase ( r _m ), of 0.38. Female−male pairs produced a mean total of 44.6 eggs within 22 days of oviposition, with 39% of these females living in excess of 29 days. Females that were deprived of males after first mating stopped laying eggs after 4−9 days, but if another male was added they resumed egg laying and produced close to a full complement of eggs (mean 42 eggs). At 25°C, fecundity on a diet of cumbungi pollen or thrips larvae (first-instar Frankliniella schutzei Trybom) was high, averaging 3.71 and 3.33 eggs per day, respectively, over a 3-day period. The sex ratio was approximately 1.5 females to 1 male. Consumption rate of thrips was also high, with an average of approximately seven first-instar or two second-instar F. schultzei larvae eaten per day. The species was also observed to feed on broad mite, Polyphagotarsonemus latus (Banks), and tomato russet mite, Aculops lycopersici (Massee). No diapause was observed under conditions of 25°C 8 h light and 10°C 16 h dark. Eggs were sensitive to low humidity, with 50% failing to hatch below 71.1% relative humidity. This species is of interest as a candidate biological control agent for thrips, broad mite and tomato russet mite in protected crops.     

Mating behavior of the predatory mite <Emphasis Type="Italic">Kampimodromus aberrans</Emphasis> (Acari: Phytoseiidae)

The mating behavior of the predatory mite Kampimodromus aberrans was studied in the laboratory at a constant temperature of 25± 1 °C and a photoperiod of 16:8 (L:D). Forty pairs of newly emerged virgin females and unmated males, were maintained separately on leaf discs and their mating behavior, was observed continuously under a stereomicroscope. The mean time until first contact of female and male individuals was approximately 8.2 min. After the first contact the male moved to the top of the female’s dorsum and subsequently underneath her in approximately 1.7 min and then the paired mites walked around on the leaf surface for approximately 7.5 min. Afterwards, the mites remained still in the mating position, i.e. the male beneath the female for an average period of 230.5 min. After mating, most of the females had one spermatophore in one of their spermathecae, whereas a few had one spermatophore in both spermathecae.     

The effects of prestarvation diet on starvation tolerance of the predatory mite Neoseiulus californicus (Acari: Phytoseiidae)

Understanding the factors affecting stress tolerance in phytoseiid mites is critical for their integration into biological control programs. In the present study, the effects of diet (varying in prey species, physiological status and phenotype) are examined on the future starvation tolerance of the predatory mite Neoseiulus californicus McGregor (Acari: Phytoseiidae). The predators are fed from egg to adulthood on diapausing or nondiapausing Tetranychus urticae, Tetranychus kanzawai (wild and albino strains) or the nondiapausing species Panonychus citri (wild and albino strains). Thereafter, 3‐day‐old mated adult females are held without food at 25 ± 1 °C and a relative humidity of 98 ± 2%. The survival of these starved females is observed daily until all females have died. The survival curves and mean survival times of N. californicus are found to vary among prey types and are significantly longer when the predator is fed with diapausing prey. This enhanced survival is consistent with high concentrations of glycogen and triacylglyceride in the body of the predator at the onset of starvation. The predators fed nondiapausing prey have shorter survival times, and the glycogen and triacylglyceride contents in their bodies are low or undetectable. The protein contents of the predator's body are similar after consuming different prey types, except for a high concentration when fed the albino strain of P. citri. Protein content is unlikely to play a direct role in starvation tolerance, although it may affect the response to varying glycogen and triacylglyceride levels. These findings indicate that nutritional value of prey has a strong impact on the starvation tolerance of N. californicus.     

Plantago asiatica groundcover supports Amblyseius tsugawai (Acari: Phytoseiidae) populations in apple orchards

Amblyseius tsugawai Ehara (Acari: Phytoseiidae) is a major predator of spider mites in orchards in Japan. To support populations in apple orchards in Akita Prefecture, northern Japan, we investigated whether it can use Plantago asiatica L. as a food resource. In laboratory tests, survival did not differ significantly between female adults given water only and those given a piece of P. asiatica leaf and water. However, A. tsugawai reproduces by feeding on P. asiatica pollen, and significantly more mites were reared on P. asiatica pollen than on tea pollen, which is commonly used for rearing phytoseiid mites. In orchards in 2013, female adults were observed on leaves of P. asiatica from late May; numbers peaked in mid-June and gradually decreased until late July. Most adults were found along veins on the hidden sides of the leaves. Female adults were also collected in Phyto traps attached to plants between late May and early August. Pollen production of P. asiatica peaked from mid-June to early July, when numbers of adults peaked on the plants. These results suggest that conservation of P. asiatica in apple orchards would sustain A. tsugawai populations.     

Molecular and morphological boundaries of the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae)

Neoseiulus californicus (McGregor) is a natural enemy of pest mites used worldwide in many crops. Its correct identification is thus essential to ensure biological control success. The present study aimed to characterize molecular and morphological intraspecific variations for assisting in the diagnosis of the species and to build baseline information about expected variations within a commercially important phytoseiid species. Morphological and molecular [12S rRNA, cytochrome b mitochondrial (mt)DNA, and internal transcribed spacer] analyses were carried out on fourteen populations collected worldwide and on one mass‐reared strain. The genetic distances between the specimens of N. californicus and another related species were high and no overlap was observed, sustaining the reliability of such molecular methods for assisting a specific diagnosis. Furthermore, the genetic distances between populations of N. californicus were very low and overlap between intra‐ and interpopulations distances was observed, except for two populations collected in France (Marsillargues and Midi‐Pyrénées). The high mitochondrial differentiation between these two latter populations and the others questions their specific status: do they belong to the species N. californicus or to another cryptic species? However, using nuclear DNA marker analyses, no distinct differences were observed. Furthermore, even if significant morphological differences were observed between the populations, these differences were very small and the standard errors within each population were very low. We thus concluded that all the populations studied belong to the species N. californicus, despite unexpected high mitochondrial variations. The present study thus displays the importance of an integrative taxonomic approach for avoiding misidentifications. A discussion on morphological and mtDNA variations in relation to diagnostic reliability is developped. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 393–406.     

Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israeli citrus orchards

The citrus rust mite (CRM), Phyllocoptruta oleivora (Acari: Eriophyidae) is a cosmopolitan key pest of citrus, inflicting severe economic damage if not controlled. In Israel, CRM damages all citrus cultivars. International regulation and increasing control failures of CRM led growers to seek sustainable biological control solutions such as acarine biological control agents. Laboratory studies conducted in Israel have indicated that the indigenous predator species Amblyseius swirskii, Iphiseius degenerans, Typhlodromus athiasae and Euseius scutalis (all Acari: Phytoseiidae) can potentially control CRM. Our general objective in the present study was to bridge the gap of knowledge between laboratory studies and the lack of control efficacy of these species in commercial orchards. Predator augmentation in the field showed that although predator populations increased immediately following releases they later decreased and did not affect CRM populations. When A. swirskii augmentation was combined with a series of maize pollen applications, A. swirskii populations were enhanced substantially and continuously but again CRM populations were not affected. Growth chamber studies with CRM-infested seedlings, with or without a maize pollen supplement, indicated that pollen provisioning led to population increase of E. scutalis and A. swirskii but only E. scutalis significantly lowered CRM populations. Control with E. scutalis was confirmed in the field on CRM infested seedlings with pollen provisioned by adjacent flowering Rhodes grass. While experiments in mature citrus orchard showed that pollen supplement usually increased predator populations they also indicated that other factors such as intraguild interactions and pesticide treatments should be taken into account when devising CRM biological control programs.     

Effect of temperature on life history of the predatory mite Amblyseius (Neoseiulus) californicus (Acari: Phytoseiidae)

Amblyseius (Neoseiulus) californicus is an indigenous mite in Japan that feeds on many spider mite species. We evaluated the development, survivorship and life-history parameters of A. californicus on a diet of eggs of Tetranychus urticae (red form). More than 97.3% of A. californicus eggs hatched and more than 81.6% of newly hatched larvae attained maturity at temperatures between 15 and 35 degrees C. Females oviposited at 37.5 degrees C, but no eggs hatched. At 40 degrees C, no females laid eggs. The lower threshold temperature from egg to oviposition was 10.3 degrees C and the thermal constant was 86.2 degree-days. Based on these data, the maximum number of generations that could complete development in a year under field conditions in Ibaraki, central Japan, would be between 21 and 28. At 25 degrees C, females laid a mean of 41.6 eggs during a mean oviposition period of 19.4 days. The intrinsic rates of natural increase (rm) were 0.173 at 20 degrees C, 0.274 at 25 degrees C and 0.340 at 30 degrees C.     

Cardinium is associated with reproductive incompatibility in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae)

Cardinium, a bacterium from the Bacteroidetes group, is associated with reproductive manipulations such as cytoplasmic incompatibility, parthenogenesis, and feminization in some arthropod species. We, and others, have shown that Cardinium, but not Wolbachia, is an endosymbiont in some populations of Metaseiulus occidentalis, a phytoseiid mite that is an important predator of spider mite pests of agricultural crops. However, the precise biological effects that Cardinium may have on M. occidentalis remain unclear. In this study we show, in two sets of crosses between different colonies of Cardinium-free (C-) M. occidentalis females and Cardinium-containing (C+) males, that fecundity was reduced in parental females, F1 progeny survival rates were reduced, and fewer female progeny were produced when compared to the reciprocal and control crosses. There were no differences in these attributes in the reciprocal and two control crosses. Cardinium was transmitted maternally but there was no observed paternal transmission. Finally, Cardinium did not cause asexual (thelytoky) reproduction in M. occidentalis. Thus, Cardinium is associated with nonreciprocal reproductive incompatibility in M. occidentalis and our results support the hypothesis that Cardinium is a reproductive parasite in this agriculturally important predator. Cardinium may therefore affect the evolution and ecology of M. occidentalis and biological control efforts using this mite.     

Cold-hardiness in the predatory miteAmblyseius potentillae (Acari: Phytoseiidae)

Cold-hardiness was studied in the predatory miteAmblyseius potentillae (Garman) by determining the mortality after exposure to –5°C. Predators reared under diapause-inducing conditions were more cold-resistant than mites that had been kept under long-day conditions. An acclimatization period at 4°C prior to exposure to sub-zero temperatures had a positive effect on the cold-hardiness of the predator, and was remarkable in diapausing mites.Lower temperatures during diapause induction had a positive effect on cold resistance in this predator; mites in which diapause was induced at 15°C were more cold-resistant than mites that had been subjected to short-day conditions at 18 and 20°C.A day/night temperature rhythm did not increase the cold-hardiness of the mite when grown under long-day conditions. Such a rhythm did increase the cold-hardiness of the diapausing predator when given a short acclimatization period, but this effect disappeared after longer acclimatization periods.