The two-spotted spider mite, Tetranychus urticae Koch (Tetranychidae), is considered one of the most important species of pest-mites because it is cosmopolite and polyphagous. This species has been described as attacking over 1,100 plant species in 140 families of economic importance. On the other hand, Phytoseiulus macropilis (Banks) (Phytoseiidae) is a predatory mite of group I, specialist as predatory mite from the Tetranychus genus. Thus, the objective of this work was to evaluate predatory potential of P. macropilis in its different stages—nymphs, female and male adults—preying on T. urticae also in different stages—eggs, larvae, nymphs, and adults—and to know the functional and numerical responses in lab studies. Both the experiments were carried out on arenas made of Jack-bean leaflets’ discs [ Canavalia ensiformis (L.)—Fabaceae] with 3 cm in diameter over agar-water at 3% inside 5 cm in diameter uncapped Petri dishes. To know the predatory activity, forty T. urticae and one predatory mite were placed in each arena with the respective phases of the developmental life cycle to be evaluated. To know the potential of predation, the no killed mites were counted after 24 hours. To know the functional and numerical responses, immature T. urticae in densities of 1 to 300/arena were offered for P. macropilis. The results for the predatory potential showed that larvae and male adult of T. urticae were the most killed stages, and the female predatory mites were the one that consumed most prey. The functional response showed a positive and significant correlation, suggesting a type II functional response (convex), a cyrtoid curve rising at a decreasing rate to a plateau, where the consumption remains constant regardless of prey density.
The two-spotted spider mite, Tetranychus urticae Koch (Tetranychidae), is considered one of the most important species of mite pests because it is cosmopolite and polyphagous. This species has been described as attacking over 1,100 plant species in 140 families of economic value [
The mite Phytoseiulus macropilis (Banks) (Phytoseiidae) is a predatory mite belonging to the group I, specialist as predatory mite of mites from the Tetranychus genus [
It has been observed that P. macropilis with Neoseiulus californicus (McGregor) (Phytoseiidae) are the most abundant species in strawberry cultivation (Fragaria spp., Rosaceae) and in plants associated with this crop, in the state of Rio Grande do Sul, Brazil [
Two native species of phytoseiids from Brazil, Neoseiulus idaeus (Denmark and Muma) and P. macropilis, under experimental studies for the control of the two-spotted spider mite on strawberry, were able to significantly reduce the mite population when they were released in the initial stage of infestation, presenting a great potential to be used in biological control [
Other studies on P. macropilis in Brazil have been showing excellent results on the two-spotted spider mite biological control, in particular under protected growing conditions, an activity that is expanding, especially for floriculture and hydroponic vegetables, which are the crops that offer excellent conditions for the development of phytophagous mite [
Based on the facts mentioned previously, the objective of the present study was to evaluate the predatory potential of P. macropilis on eggs, larvae, nymphs, and adults of T. urticae and to know the functional and numerical responses of P. macropilis preying on T. urticae, both in bioassays under laboratory conditions.
The present study was performed under controlled conditions with temperature at 25˚C ± 1˚C, 70 ± 10% of RH and 14 hours of photophase in the Acarology Laboratory of the EPAMIG Sul―Research Center of Ecology Management of Pests and Plant Diseases―EcoCentro, Lavras, Minas Gerais, Brazil. The pest mite T. urticae and predatory mite P. macropilis were both obtained from the Federal Institute of Inconfidentes, Minas Gerais, Brazil.
For rearing the pest mite, T. urticae were placed on upper surface of the Jack-bean leaflets [Canavalia ensiformis L. (DC)―Fabaceae], weekly changed [
Uncapped Petri dishes (15 cm in diameter) were used, with a 1 cm thick foam maintained moist with distilled water and that covered the entire bottom surface of each dish with a Jack-bean leaflet placed on top of the foam and surrounded by strips of hydrophilic cotton wool that were also in contact with the damp foam in order to avoid mites from escaping and to better conserve the leaflet.
Rectangular arenas of black flexible PVC plastic sheets (26 × 22 cm) were used. These were put over StyrofoamTM of equal size and placed over water inside plastic trays (32 × 26.5 × 5.5 cm) [
The experiments of P. macropilis predatory potential on T. urticae under laboratory conditions were carried out on arenas made of Jack-bean leaflet discs with 3 cm in diameter over agar-water at 3% inside 5 cm in diameter uncapped Petri dishes. The dishes were covered with PVC film to avoid mites from escaping. Predatory mites, as well as pest mites, were obtained from maintenance laboratory rearing. The predatory mites were fasted for 24 hours before they were placed on the experimental arenas.
Experiments were carried out using all possible combinations among the stages of the predatory mite development life cycle―nymphs, adult male and adult female―and each stage of development life cycle of T. urticae―egg, larvae, nymphs, adult male and adult female―in other words, a factorial 3 × 5, with experimental design completely randomized. Forty T. urticae were placed on each arena in the respective stages to be studied, with 10 replications per treatment. After 24 hours of introducing the pest mites, killed, naturally dead and lives were counted.
Larvae of P. macropilis were not used in the tests because this stage is completed in less than a day. In addition, according to some researchers, mites in larval stage does not eat or eats very little [
Regarding the calculation of predatory capacity of P. macropilis, the data obtained were subjected to variance analysis and the means were compared with one another through the Tukey test at 5% significance, with the use of SigmaPlot software, version 9.01 [
Adult females of P. macropilis were confined for eight days on arenas of 3 cm in diameter made with Jack-bean leaflet discs inside uncapped Petri dishes of 5 cm in diameter, containing agar-water at 3%, as mentioned previously.
Pest mites, constituted only of immature stages of T. urticae, were placed on arena 3 cm in diameter, as already mentioned, in the following amounts: 1, 2, 5, 10, 20, 30, 35 (with seven replications), 45 (with four replications), 55 (with three replications), 70, 100, 125, 200, and 300 (with two replications). The variations in the replications occurred due to the large number of mite specimens that were necessary in the highest densities [
Immature stages―larvae and nymphs―of T. urticae were used as food for P. macropilis because, in general, these are the stages of the pest mite most preyed by phytoseiids [
The functional response of the P. macropilis predatory mite was found through the Holling model [
The cubic logistic regression model takes on a polynomial function as a linear predictor in order to describe the linear relation between Na/No and No and L0, L1, L2 and L3 as the representation of the intercept, linear, square, and cubic coefficients, respectively. The maximum likelihood method was used to estimate the coefficients. If L1 > 0 and L2 < 0, thus the ratio of prey consumed is supposedly a density that is positively dependent, configuring a Type III functional response. In contrast, if L1 < 0, the ratio of prey offered exhibits a monotonic decline with the initial number of prey offered, configuring a Type II functional response [
N a N o = exp ( L 0 + L 1 N o + L 2 N o 2 + L 2 N o 3 ) 1 + exp ( L 0 + L 1 N o + L 2 N o 2 + L 2 N o 3 ) Model (1)
Once the type of functional response has been defined, a model that relates the number of prey attacked by P. macropilis female mites as a function of the density of T. urticae can be considered.
Among the models of functional response, the Holling model is illustrated by Model (2) [
N a = a T N o 1 + a N o T h Model (2)
where a is the parameter associated with the predator attack rate, Th is the predator search time for the prey (handling time), T is the prey exposure time to the predator (in this case, it was 1 day) and No is the number or density of prey offered. Model (2) is non-linear in parameters and its parameters were estimated by the method of least squares [
The numerical response was evaluated based on a square regression model, illustrated by Model (3):
y = b 0 + b 1 N o + b 2 N o 2 Model (3)
in which b0, b1 and b2 are the model coefficients or parameters, No is the density of prey offered, and y is the predator mean daily oviposition. Parameters of Model (3) were estimated by the least squares method. Eventually, the weighted regression, considering the weight given by the reverse density of prey offered (1/No), was taken into account in order to stabilize the response variance in Model (3).
All statistical analyses were carried out with the assistance of the statistical software R [
Nymph stages, female and male adults of P. macropilis are able to preying on all stages of T. urticae. Larvae and adult males of T. urticae were the most preyed by all stages of the predatory mite, and the two-spotted spider mite adult female was the least preyed (
Adult females of P. macropilis were the most efficient in the predation, preying on approximately 65% of larvae, followed by adult males that consumed about 50% of the two-spotted spider mite larvae (
The estimated parameters by the logistic regression of the dead prey rate (Na/No) versus the number of prey offered (No) to P. macropilis females in a day, are shown in
Stages of Tetranychus urticae | Mean ± SE* of Tetranychus urticae killed by all stages of Phytoseiulus macropilis | ||
---|---|---|---|
Nymphs | Females | Males | |
Eggs | 8.7 ± 1.1 bB | 15.9 ± 1.7 bA | 12.3 ± 0.9 bcAB |
Larvae | 19.3 ± 1.2 aB | 26.3 ± 1.2 aA | 21.5 ± 1.8 aAB |
Nymphs | 9.8 ± 1.7 bB | 24.0 ± 1.5 aA | 15.2 ± 1.8 abB |
Adult males | 16.9 ± 1.1 aB | 25.6 ± 1.1 aA | 20.6 ± 1.4 aB |
Adult females | 3.3 ± 0.5 cAB | 5.4 ± 1.1 cA | 2.5 ± 0.4 dB |
*Mean ± SE (mean standard error) followed by the same lower case letter on the columns and the same capital letter on the rows do not differ among themselves by the Tukey test (P > 0.05).
Parameter* | Estimation | Standard error | Value P |
---|---|---|---|
L0 | −0.1754 | 0.05502 | 0.00143 |
L1 | −0.01216 | 0.00192 | <0.00001 |
L2 | 0.00002 | 0.000016 | 0.18620 |
L3 | −0.00000002 | 0.00000003 | 0.44465 |
*L0, L1, L2 and L3 = representation of the intercept, linear, square, and cubic coefficients, respectively.
number of prey offered, which configured a type II functional response (convex) according Holling models, a cyrtoid curve rising at a decreasing rate to a plateau, where the consumption remains constant regardless of prey density. This model presented a good fit to the data, which was indicated by the coefficient of determination value R2 (
The curve of the functional response of P. macropilis preying on T. urticae is shown in
The coefficients of P. macropilis female mites attack rate (a) and handling time (Th) on densities of the prey, T. urticae, estimated by the Holling equation [
The oviposition by P. macropilis females increased with the density of prey offered until it reached an approximate density of 162.5 T. urticae mites per arena 3 cm in diameter, with a maximum oviposition of 1.76 eggs/female/day, and after this density the female oviposition began to decrease (
The estimated parameters by the square regression model to the numerical response are represented in
Model | Parameter* | Estimation | Standard error | Value P | R2 |
---|---|---|---|---|---|
Holling 1959 | a | 0.7558 | 0.1935 | 0.0021 | 0.876 |
Th | 0.0362 | 0.0042 | <0.0001 | - | |
a/Th | 20.8710 | - | - | - | |
K = T/Th | 27.6160 | - | - | - |
*a = predator attack rate, Th = handling time (predator search time for the prey), and T = prey exposure time to the predator (in this case, it was 1 day) and, K = maximum predation rate.
Parameter* | Estimation | Standard error | Value P |
---|---|---|---|
L0 | 0.1696 | 0.05395 | 0.0093 |
L1 | 0.01945 | 0.00464 | 0.0015 |
L2 | −0.00006 | 0.00002 | 0.0234 |
*L0, L1 and L2 = representation of the intercept, linear, and square, coefficients, respectively.
A study of the biology of P. macropilis fed on Tetranychus tumidus Banks (Tetranychidae) showed that the nymphs and adults consumed more eggs and larvae than the other mite developmental stages; also that the female predatory mites was the one that consumed most prey, followed by males [
In the evaluation of P. macropilis predatory potential in the control of two-spotted spider mite, it was observed that the female predatory mite consumed all stages of the prey; however, the eggs stage was the most consumed and the adult female prey was the least consumed [
A study on the management of T. urticae in roses (Rosa spp., Rosaceae) growing in greenhouse and using Neoseiulus sp. predatory mite has demonstrated that females consume a larger number of larvae and nymphs under controlled conditions [
It is also known that the predation of T. urticae by N. californicus is low on leaves that present trichome such as in the tomato plant (Solanum lycopersicum L., Solanaceae). This low predation was related to trichomes present on tomato leaves, one of the attributes of the plant that must be considered as an essential component for biological control practices [
The present study shows that as well as in other studies cited previously, the P. macropilis adult predatory mites (females and males) consumed a larger number of preys than nymphs stage. However, those studies, in general, report a larger consumption of eggs, larvae, and nymphs, differing from the present study, in which larvae, males, and nymphs were the most consumed. This difference perhaps can be explained by the fact that none of the studies cited above evaluated the predation on T. urticae males. Also, the adult females of predatory mite consume more prey than the other stages of the predatory mite perhaps due to higher energy expenditure required for the oviposition [
The functional response is an important aspect in population dynamics, once it is an expression of the relation between the predator’s consumption and the prey’s density rate [
The type II functional response, found in the present study for P. macropilis, is the most commonly reported for phytoseiid predatory mites when the density of the prey is increased. This occurs when the attack rate (a) and the handling time (Th) do not have a relation with the prey densities [
The functional response has also been used to evaluate other parameters such as the effect of N. californicus long-term feeding [
The predatory mite handling time limits the response to the predatory activity. Nevertheless, an increase in the handling time (Th) leads a reduction of the maximum predation rate (K) [
The maximum predation estimation can be used to determine the ideal number of predatory mites that must be released in order to reduce the pest mite population. However, the predation rate under laboratory conditions might not be the same in the field situation [
Some researchers have studied the functional response of various predatory mites only with the prey eggs as food [
The results found in the present study, about increase of female oviposition with de increase of prey density, are similar to those found in a study on the effect of Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae) density in the functional and numerical response of Euseius alatus DeLeon and Iphiseiodes zuluagai Denmark and Muma [
The oviposition of P. macropilis decline when prey density is increased above 170 T. urticae/arena (
In a general way, another aspect that may be taken into account is the prey nutrition, which in high densities can also be impaired, since the food source (plant) is already decayed because of the intense attack due to the high density of pest mites present. Consequently, this will influence the predatory mite nutrition, especially that of the adult female [
The oviposition correlates with the preying on because phytoseiids allocate a great fraction of the ingested food for the egg production [
However, under natural conditions this prey consumption and oviposition values could be different, because another factor that needs to be considered is that, in general, phytoseiids females depend on the presence of males or at least once they have been mate in order to produce eggs [
In the present study, the maximum daily oviposition of P. macropilis was 1.76 eggs. This value may be considered low because the females were confined in arenas during eight days in the absence of the male, which was a necessary procedure to conduct the experiment to quantify only the adult female predatory activity alone.
The increase of the predatory mite oviposition in response to the increase in the prey density can contribute in the efficacy of biological control, allowing an increase in the predatory mites’ population. This is a favorable condition for P. macropilis because this mite, in general, is considered more efficient at high populations of the pest mites [
The obtained results allow concluding that all post-larval developmental stages of P. macropilis are efficient to kill all phases of T. urticae developmental cycle and with a type II functional response.
To the Conselho Nacional de Desenvolvimento Científico e Tecnológico―National Council for Scientific and Technological Development―CNPq for the financial support and the fellowships granted.
Souza-Pimentel, G.C., Reis, P.R., Liska, G.R. and Cirillo, M.Â. (2018) Predatory Potential of Phytoseiulus macropilis (Banks) Preying on Tetranychus urticae Koch (Acari: Phytoseiidae, Tetranychidae). Advances in Entomology, 6, 134-147. https://doi.org/10.4236/ae.2018.62010