Functional response of Neoseiulus californicus (Acari: Phytoseiidae) on different stages of development of Oligonychus punicae (Acari: Tetranychidae).

O. García-Ángel1; Y. M. Ochoa-Fuentes1; E. Cerna-Chavez1; L. A. Aguirre-Uribe1; R. J. Flores-Canales2; J. L. Landeros-Flores1*

1. Universidad Autónoma Agraria Antonio Narro, Calzada Antonio Narro # 1923. C.P. 25315. Buenavista, Saltillo; Coahuila, México., Universidad Autónoma Agraria Antonio Narro, Universidad Autónoma Agraria Antonio Narro,

<postal-code>25315</postal-code>
<city>Saltillo</city>
<state>Coahuila</state>
, Mexico , 2. Universidad Autónoma de Nayarit, Unidad Académica de Agricultura, Carretera Tepic-Compostela Km 9, C.P. 63780 Xalisco, Nayarit, México., Universidad Autónoma de Nayarit, Universidad Autónoma de Nayarit, Unidad Académica de Agricultura,
<postal-code>63780</postal-code>
<city>Xalisco</city>
<state>Nayarit</state>
, Mexico

Correspondence: *. Corresponding Author: Jerónimo, Landeros-Flores. Universidad Autónoma Agraria Antonio Narro, Calzada Antonio Narro # 1923. C.P. 25315. Buenavista, Saltillo; Coahuila, Mexico. Phone: +52(844) 100 2647 E-mail: E-mail:


Abstract

The functional response of Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) was studied at different densities and developmental stages of avocado mite Oligonychus punicae (Hirst) (Acari: Tetranychidae), under laboratory conditions on Hass avocado leaf discs. Results showed a Type II functional response in all assessed stages. Maximum consumption of N. californicus on O. punicae at a density of 64 offered preys, was 15.13, 26.93, 13.07 eggs, larvae and nymphs respectively; as well as 7.40 adults at a density of 32 prey mites. These results show that N. californicus tends to eat more larvae than eggs and nymphs; and even a lower numbers of adults.

Received: 2017 December 19; Accepted: 2018 April 18

revbio. 2020 Mar 23; 5(spe1): e422
doi: 10.15741/revbio.05.nesp.e422

Keywords: Key words: Avocado Brown Mite, Biological Control, Predator.

Introduction

Oligonychus punicae (Hirst) is considered one of the main mites affecting avocado crops in Mexico. Its presence damages the epidermis of leaves and distorts the ratio between chlorophyll and photosynthates, leading to reddish or tanned lesions (Dorantes et al., 2004; Equihua et al., 2007; Dreistadt, 2008). When feeding on avocado leaves, this mite limits itself mainly to the upper side, close to the central vein; although it can also move to the underside when the population levels become high (Ochoa et al., 1991; Dorantes et al., 2004) for a long time, partially defoliating the trees. This type of damage can occur at densities of 300 mites per leaf, although under draught conditions, 70 adult females per leaf can cause the same damage, (Peña and Wysoki, 2008) In this plague mite the chemical control is the most used method for its management (Soto, 2013). However, an alternative for its control can be through the use of predatory mites belonging to the family Phytoseiidae, (Zhang, 2003). A highly infested orchard trees may have defoliation, general weakening, and, consequently, growth retardation with poorly developed and scarce fruits, it occurs all year round, but with greater severity in spring and autumn (Coria and Ayala, 2010). In Mexico occurs practically in all the orchards where it is often the presence of trees highly defoliated by this mite, although little is known about the economic losses of this species. The most popular management method for this pest mite is chemical control (Soto, 2013); in Mexico this species is controlled with applications of sulfur, petroleum oils and light mineral oil, in addition to Abamectin; Azadirachtin and Lambda cyhalothrin (Coria and Ayala, 2010). However, repeated use can cause resistance problems, as well has health and ecological, which forces to search after new control options (Lemus-Soriano and Romero-García, 2015) how the use of natural enemies (biological control). Predating mites from Phytoseiidae family offer an alternate control (Zhang, 2003). A predator must be evaluated according to its adaptation to environmental searching capacity, functional and numerical response, and spatio-temporal synchronization with the prey (Huffaker et al., 1971). The functional response of a predator is a key factor in the population dynamics of predator-prey systems (Schenk and Bacher, 2002). In this regard, one of the most widely used mite species in biological control programs is Neoseiulus californicus (McGregor), classified as a generalist predator of spider mites and one of the main biological control agents used to protect different greenhouse and open-field crops (Gotoh et al., 2006; Marafeli et al., 2011; Singh, 2016). N. californicus is not only widely distributed, but it is also reared and released in several countries of the world, (Canlas et al., 2006; McMurtry et al., 2013; Barbosa and de Moraes, 2015). Among its benefits, N. californicus eats some types of insects such as trips, besides feeding on mites, and can even survive feeding on pollen when the primary prey is not available (Castagnoli and Simoni, 1999; Sazo et al., 2006). This mite is considered a Type II predator; a category that includes selective predators of tetraniquid mites, which are more frequently associated to species that form dense spider webs, as it is the case of Oligonychus y Tetranychus. Nevertheless, this predator can also behave like a Type III predator (Croft et al., 1998; Croft et al., 2004; McMurtry et al., 2013; Rezaie et al., 2017). Therefore, this research work focused in determining the efficiency of Neoseiulus californicus through its functional response over Oligonychus punicae in Hass avocado leaves and with the results obtained it will be possible to demonstrate that it is a natural enemy that can be considered in the management of this pest.

Material and Methods

The research work was conducted in a bioclimatic chamber of the Parasitology department at “Universidad Autónoma Agraria Antonio Narro”, Saltillo, Coahuila, Mexico, (25°21′13″N 101°01′56″W). A mother colony of Oligonychus punicae was reared, using mites from Hass avocado trees planted in Tepic, Nayarit, Mexico, the mites were reproduced under controlled conditions, at a temperature of 26 ± 2 ºC; relative humidity of 70 ± 10 % and a light-darkness photoperiod: 12:12h L: D. The commercially available predator Neoseiulus californicus was obtained from Spical® (Koppert Mexico, S.A. DE C.V.) and was reproduced on bean leaves infested with Tetranychus urticae (Koch) (Acari: Tetranychidae). Functional response experiments were developed in the bioclimatic chamber under the same developmental conditions than the mother colony, following the methodology of Brodeur and Cloutier (1992), using leaf-discs in agar, with some modifications. The experimental unit was an avocado leaf disc of 3 centimeters in diameter, placed on top of a solidified agar layer (nearly 20 mL), within a plastic container of 30 mL capacity, a water film was poured on the agar layer and the contour of the leaf disc. The containers were sealed with a semi-air tight cap with a whole in the middle, and were covered with thin cloth to avoid excessive moisture. In the predation study of N. californicus over O. punicae eggs, 10 to 20 pregnant avocado brown mite females were left for 24 hours on the avocado leaf discs. After removing the females, the number of eggs was adjusted to 1, 2, 4, 8, 16, 32 and 64 per every leaf disc. The same method previously described was followed for the next stages of development, except the eggs, which were kept until hatching, allowing them to reach the life stages that were going to be assessed (larvae, nymphs and adult females); 24 hours after emerging from the corresponding stage, an adult female of N. californicus was introduced per every preying density, with 15 replicates per density. The predation rate was recorded within 24 hours, in order to determine the type of functional response (curve’s shape), through logistic regression analysis, adjusting a polynomial equation of the ratio of eaten preys (Na /No ) vs the number of preys offered (No):

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Where:

Na =
number of eaten preys,
No =
number of offered preys.
P0 ,P 1 , P2 , y P3 =
parameters to be estimated

If P1 > 0 and P2 <0, it means that the ratio of eaten preys positively depends on density and therefore we have a Type III functional response. If P1 <0, the ratio of eaten preys decreases with the initial number of offered preys, showing a Type II functional response (Juliano, 2001). After learning the type of functional response, the parameters of such functional response were estimated: Time of handling (Th ) and attack capacity () according to Holling’s Type II functional response (1966).

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Where:

Na =
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a’ =
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No =
Prey density,
T =
Total available time (24 h in this experiment) and
Th =
Time of handling.

Procedure PROC NLIN de SAS/STAT (SAS, 2008) was used to estimate the parameters.

Results and Discussion

There are several models of functional response with slight variants. Within these models, Rogers (1972) proposed a model known as “random Predator equation”, with very similar characteristics but also allows the prey to deplete. Although models usually behave the same way. (Badii and Chacón, 2014) In this study the results were analyzed by Holling’s Model II (1966) simply because it is the most frequently used. The percentage of preys eaten in all the stages of development of O. punicae decreased, with an increase in the density of offered preys (Figure 1). This means that there is a reverse dependency of the initial density.


[Figure ID: f1] Figure 1.

Functional response lines of Neoseiulus californicus over different stages and densities of Oligonychus punicae.


The logistic regression analysis of all the prey stages yielded a significant linear parameter P1 <0 and a positive quadratic coefficient (P2) of the ratio of preys eaten at every density, versus the initial preying density (Table 1). This shows a Type II functional response.

Table 1.

Results of the logistic regression analysis on the ratio of preys eaten by Neoseiulus californicus (Na /No) vs the number of offered preys (No) of Oligonychus punicae.


Stage Parameters
Intercept (P0) Linear (P1) Quadratic (P2)
Egg 2.3039* -0.1196 0.000688
(1.9591, 2.6487) ( -0.1402, -0.0990) (0.000536, 0.000840)
Larva 3.4647 -0.0601 ---
(3.0220, 3.9074) ( -0.0683, -0.0519) ---
Nymph 2.7255 -0.1789 0.00182
(2.2535, 3.1974) ( -0.2167, -0.1410) (0.00130, 0.00235)
Adult 3.1391 -0.3925 0.0081
( 2.4911, 3.7872) (-0.4871, -0.2979) ( 0.00559, 0.0106)

TFN1* indicate statistically significant differences of p<0.05, Values between parenthesis show a 95 % confidence interval, both based on Wald (SAS, 2008).


This type of response coincides with the results reported by Doker et al., (2016), Gotoh et al., (2004) and Song et al., (2016), who mentioned that N. californicus shows a Type II functional response over eggs and immature subjects of Tetranychus urticae and Tetranychus kanzawai. Similarly, Xiao and Fadamiro (2010) said that N. californicus showed a Type II functional response over nymphs of Panonychus citri. With regards to the attack rate coefficients (a’) and the time of handling (Th), an a’ of 0.9192, 1.4429, 1.1179, 1.15 and a Th of 0.0521, 0.0244, 0.0638, 0.1152 were estimated for eggs, larvae, nymphs and adults respectively (Table 2). Ahn et al., (2010) reported a maximum number of T. urticae preys eaten by N. californicus adult females, accounting for 17.14, 15.14 and 11.81 eggs, larvae and nymphs respectively; with an a’ of 0.0697, 0.0678, 0.0662 and a Th of 1.4002, 1.5855, 2.0331, for the same stages of development during 24 hours at 25 °C. Xiao et al., (2013) reported a maximum number of 26.6 eggs eaten a day, with an a’ of 0.49 and a Th of 1.7328 for the same prey.

Table 2.

Specimens of Oligonychus punicae eaten by Neoseiulus californicus on avocado leaves and parameters of functional response Type II.


Initial Density
(No)
Eggs Larvae Nymphs Adults
Na ± SD Ho Na ± SD Ho Na ± SD Ho Na ± SD Ho
1 1 ± 0 0.9 1 ± 0 1.4 1 ± 0 1.1 1 ± 0 1.1
2 2 ± 0 1.8 2 ± 0 2.9 2 ± 0 2.2 2 ± 0 2.3
4 3.67± 0.62 3.6 4 ± 0 5.7 3.73 ± 0.59 4.4 3.40 ± 1.12 4.5
8 6.13 ± 1.55 7.2 7.80 ± 0.56 11.4 5.80 ± 1.65 8.7 4.20 ± 1.37 8.8
16 7.80 ± 2.01 14.3 14.46 ±1.68 22.6 8.13 ± 3.27 17.1 5.40 ± 1.24 16.9
32 10.47 ± 2.97 27.6 24.93 ± 5.03 44.1 10.67 ± 2.99 32.7 7.40 ± 1.72 31.3
64 15.13 ± 3.27 52.2 26.93 ± 8.7 84.4 13.07 ± 3.26 60.1
0.9192 1.4429 1.1179 1.15
Th 0.0521 0.0244 0.0638 0.1152
X2 0.342 1.479 0.035 1.901

TFN2Na=attacked and observed preys; SD=Standard deviation; Ho= Expected Holling; a’=Rate of attack, Th =Time of handling; X2=Chi-square test.


In this research work we recorded an average consumption of O. punicae by N. californicus at a density of 64 offered preys of 15.13, 26.93, 13.07 eggs, larvae and nymphs respectively; as well as 7.40 adults at a density of 32 prey mites. Hereinabove results show that N. californicus tends to eat more larvae, followed by eggs, nymphs and lower numbers of female adults. In this sense, Sabelis (1985) and Xiao et al., (2013) mentioned that phytoseiid mites often prefer to feed on immature stages and eggs. On the other hand, Xiao and Fadamiro (2010), reported that N. californicus prefers nymphs over the eggs of P. citri; while Song et al., (2016) and Rezaie et al., (2017) expressed that N. californicus showed higher predation rate on T. urticae active stages than on the eggs. In the case of phytoseiids generalists, Blackwood et al., (2001), mention that spider larvae can be consumed more than eggs by nutritional benefits, as well as manipulation time, they observed that the females of several species of generalists often tried to unsuccessfully drill eggs before attacking the larvae. A possible explanation for this observation would be that these species of generalists may have less effective mouthparts in the chorion perforation of the egg. Flechtmann & Mc-Murtry (1992), found important cheliceral differences between the species of Phytoseiidae that feed mainly on mites and pollen.

Conclusion

In this research N. californicus consumed all the states of development of O. punicae. in addition, is a generalist predator can eat other types of dams and even pollen grains and survive in the absence of the plague or in low populations, this predator can be used as a tool in the efficient management of this pest.


fn1Cite this paper: García-Ángel, O., Ochoa-Fuentes, Y. M., Cerna-Chavez, E., Aguirre-Uribe, L. A., Flores-Canales, R. J., Landeros-Flores, J. L. (2018). Functional response of Neoseiulus californicus (Acari: Phytoseiidae) on different stages of development of Oligonychus punicae (Acari: Tetranychidae). Revista Bio Ciencias 5(nesp), e422. doi: https://doi.org/10.15741/revbio.05.nesp.e422

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Revista Bio Ciencias, Año 11, vol. 7,  Enero 2020. Sistema de Publicación Continua editada por la Universidad Autónoma de Nayarit. Ciudad de la Cultura “Amado Nervo”,  Col. Centro,  C.P.: 63000, Tepic, Nayarit, México. Teléfono: (01) 311 211 8800, ext. 8922. E-mail: revistabiociencias@gmail.com, revistabiociencias@yahoo.com.mx, http://revistabiociencias.uan.mx. Editor responsable: Dr. Manuel Iván Girón Pérez. No. de Reserva de derechos al uso exclusivo 04-2010-101509412600-203, ISSN 2007-3380, ambos otorgados por el Instituto Nacional de Derechos de Autor. Responsable de la última actualización de este número Dr. Manuel Iván Girón Pérez. Secretaria de Investigación y Posgrado, edificio Centro Multidisciplinario de Investigación Científica (CEMIC) 03 de la Universidad Autónoma de Nayarit. La opinión expresada en los artículos firmados es responsabilidad del autor. Se autoriza la reproducción total o parcial de los contenidos e imágenes, siempre y cuando se cite la fuente y no sea con fines de lucro.

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