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Functional response of adult Cheyletus malaccensis (Acari: Cheyletidae) to different developmental stages of Aleuroglyphus ovatus (Acari: Acaridae)
Journal of Stored Products Research 84 (2019) 101525
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Functional response of adult Cheyletus malaccensis (Acari: Cheyletidae) to different developmental stages of Aleuroglyphus ovatus (Acari: Acaridae) Peipei Zhu, Yuxiang Fan, Weifen Mo, Tianrong Xin, Bin Xia, Zhiwen Zou* School of Life Science, Nanchang University, Nanchang, 330031, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 July 2019 Received in revised form 25 September 2019 Accepted 6 October 2019 Available online xxx
Cheyletus malaccensis is an important natural enemy of stored pests. In the study, the functional response of C. malaccensis against Aleuroglyphus ovatus was investigated under five constant temperatures of 16, 20, 24, 28 and 32 C. The results showed that the functional response of adult C. malaccensis to different stages of A. ovatus was conformed to Holling II. Under the temperature between 16 and 32 C, C. malaccensis females consumed more larvae and nymphs, followed by male and females of A. ovatus. While male C. malaccensis merely consumed larvae and nymphs of prey. Adult C. malaccensis ate few eggs of A. ovatus. The daily consumption and instantaneous attack rate (a/Th) increased with the temperature increasing from 16 C to 32 C while the peak was at 28 C. The maximum daily consumption for larva and a/Th of female C. malaccensis are 135.1 and 110.7, respectively. Cheyletus malaccensis showed positive preference to larvae and nymphs, while negative preference to adults and eggs of A. ovatus. Because of the competition and interference among predators, the predation efficiency decreased with the density of predator increasing, and the interference coefficient (m) was 0.485 at 28 C. These results could be helpful to provide theoretical basis and practical instructions for the biological control of A. ovatus by C. malaccensis. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Functional response Cheyletus malaccensis Aleuroglyphus ovatus Preference Interference
1. Introduction Mites of the genus Cheyletus, associated with stored grains and stored-product pests (Hughes, 1976; Yousef et al., 1982), are frequently used for biological control agents (Pek ar; Hubert, 2008; Cebolla et al., 2009; Palyvos and Emmanouel, 2011). Cheyletus malaccensis Oudemansis a generalist predator that preys on storedproduct pests, such as Acarus siro Linnaeus, Aleuroglyphus ovatus Troupeau, Caloglyphus redickorzevi Zachvatkin, Lepidoglyphus destructor Schrank, Tyrophagus putrescentiae Schrank, Caloglyphus rodriguezi Samsinak, Rhizoglyphus echinopus Fumouze and Robin, (Yousef et al., 1982; Cebolla et al., 2009; Al-Shammery, 2014). It is known to prey also on other pests, Musca domestica Linnaeus, Lepidocyrtinus incertus Handschin, Ephestia kuehniella Zeller (Yousef et al., 1982; Athanassiou and Palyvos, 2006). It was reported that 90% reduction of A. siro was achieved by releasing three r; Hubert, 2008). Cheyletus malaccensis C. malaccensis at 25 C (Peka
* Corresponding author. E-mail address: [email protected] (Z. Zou). https://doi.org/10.1016/j.jspr.2019.101525 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
is the genius predatory mite. For one thing, it is a generalist predr and ator so that it can well control not only the stored pest (Peka Hubert, 2008; Cebolla et al., 2009) but also the field pest Megoura japonica Matsumura (Hemiptera: Aphididae) (Yin et al., 2019). Cheyletus malaccensis is the most common parthenogenetic predatory mite, and it can reproduce at temperatures between 17.5 and 35 C, and develop in the range between 11.6 and 37.8 C. The immature stages of C. malaccensis varied from 11.3 to 13.8 days and the total 169.7 eggs were laid when feeding on T. putrescentiae at 30 C. Therefore, high fertility, fast multiply, tolerance to wide temperature range and parthenogenesis are beneficial for production in biological control (Zdarkova, 1979; Yousef et al., 1982; Palyvos and Emmanouel, 2011; Hubert et al., 2016). Aleuroglyphus ovatus, a major storage pest mite, damages stored products and causes great economic loss for its fast growth and high fertility. It can transform from egg to adult only 13 days and produce more than 236 eggs in total on artificial diets (our unpublished data). It infests a wide range of stored products, such as stored bran, wheat, chicken meal, dried fish products and traditional Chinese medicine (Geary et al., 2000; Li et al., 2003). In addition, it endangers human health with infection dermatitis,
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allergic rhinitis, asthma, respiratory diseases, pulmonary acariasis and urinary acariasis (Fernandez-Caldas et al., 1993; Li, 2000; Valdivieso et al., 2006). In contrast to greenhouses, orchards or fields, biological control is absent in storages (Luk as et al., 2007). The traditional methods to manage storage pest mites were chemical and physical measures (Norris, 1958; Thind and Dunn, 2002). As a safe and effective way, biological control of A. ovatus needs more attention. Functional response is an important behavioral response to reveal different aspects of prey-predator interactions (Jafari and Goldasteh, 2009) and assess the predation efficacy of predators. Though the functional responses of different predatory mites have been conducted, the functional response of C. malaccensis to A. ovatus has never been reported. The aim of the study is to assess the functional response of C. malaccensis to different stages of A. ovatus under different temperatures, effects of interference among predators on functional response and prey stage preference, which is important to find an effective agent on controlling this pest mite.
2007; Wu et al., 2016): A ¼ QP-m Where A is the mean consumption for a single predator, P is the number of predator, m is the interference coefficient, Q is the max consumption when P ¼ 1. 2.4. Preference of C. malaccensis to A. ovatus A 24 h starved female predator and equal numbers of each stage (egg, larva, nymph, male adult and female adult) preys (total 100 mites) were transferred into the jelly box (25 ml) with cover. After 24 h, the numbers of prey consumed for each stage were recorded. Ten groups were used as replicates. When there were different stages of prey, it was common to calculate the preference of the predator to different preys by the equation (Zhou and Chen, 1987; Wu et al., 2016): Qi ¼(1 þ Ci) /(1-Ci)Fi,
2. Materials and methods 2.1. Mite colony A. ovatus collected from a flourmill nearby Nanchang University were maintained on wheat bran in a climatic chamber (RXZ-260B; Ningbo Dongnan Instrument, China) at 28 C, 85% relative humidity and dark. They were reared more than five years. The predatory mites, C. malaccensis collected from the same place were mass cultured in plastic bottles filled with A. ovatus and wheat bran in the same condition.
in which Qi is the predation rate of the predator against the i-th stage prey, Fi is the proportion of the i-th stage prey, Ci refers to the preference of predator for the i-th prey. When Ci ¼ 0, it means the predator shows no preference for the i-th prey; 0 < Ci < 1, the predator shows positive preference for the i-th prey; 1
2.2. Functional response 3. Results The functional responses of adult C. malaccensis to different stages of A. ovatus were investigated at 16, 20, 24, 28 and 32 C (Yin et al., 2019). Each predator for experiment was starved for 24 h to standardize the hunger degree (Dehkordi and Sahragard, 2013). Various densities and different stages of A. ovatus were transferred into the rearing cell which consisted of a slide on a lid of the film cartridge. Then one pretreated predator was put into the cell. After 24 h, the number of prey consumed was recorded. The densities of egg, adult female and male of A. ovatus were 3, 6, 9, 12 and 15,while larvae and nymphs were 20, 25, 30, 35 and 40. Each experiment was repeated at least 12 times. Holling disc equation (Holling, 1959) was used to describe the functional response of adult C. malaccensis to different stages of A. ovatus:
3.1. Functional response The functional response of adult C. malaccensis against different stages of A. ovatus at different temperatures displayed Holling II (Fig. 1). With the density increasing of prey, the consumption first went up then reaching the plateau (Fig. 2). Female C. malaccensis almost caught and ate all stages of A. ovatus, but barely eggs (less than 3 eggs at the highest initial prey density of 15 of A. ovatus in 24 h). By contrast, male predators merely consumed larvae and nymphs (Table 1), and hardly consumed adults and eggs of A. ovatus. Under any temperatures, adult female C. malaccensis consumed the most larvae followed by nymphs, males and females
Na ¼ aN/ (1 þ aThN) in which a is attack rate, N is the number of preys offered, Na is the number of preys consumed, Th is handling time, a/Th is the instantaneous attack rate. 2.3. Effects of predator interference on functional response Different densities (1, 3, 5, 7 and 9) of female C. malaccensis were released into 50 male adults of A. ovatus in a rearing unit. Then the unit was placed to the climatic chamber. The temperature was also set from 16 to 32 C. After 24-h exposure, the number of eaten A. ovatus was recorded. More than 12 replications were done. In evaluating influence of interference among predators, the following relationships are frequently used (Watt, 1959; Xia et al.,
Fig. 1. The consumed numbers of female C. malaccensis to various densities female A. ovatus at different temperatures.
P. Zhu et al. / Journal of Stored Products Research 84 (2019) 101525
Fig. 2. The interference among adult females of Cheyletus malaccensis varying with densities of preys under different temperatures.
of A. ovatus. The highest daily consumption of females, males, nymphs, larvae of A. ovatus at 28 C was 7.3, 18.2, 84.0 and 135.1, respectively (Table 1). At other temperatures, female C. malaccensis also consumed more immature stage than adults of prey. And its consumption of larvae was about twice than nymph, as well as that of males was far more than females. The maximum predation ability of male C. malaccensis on nymphs and larvae were 40.1 and
3
59.8 at 28 C, which was less than half of female. The consumption of male C. malaccensis against larvae was higher than nymph at any temperatures (Table 2). The predation efficiency of C. malaccensis increased with the temperature increasing, which reached its peak at 28 C. So the value of a, a/Th, the max daily consumption were increased with the temperature rising while Th was decreased. Their value however, it was at 28 C that C. malaccensis shown the peak (a ¼ 0.819, a/ Th ¼ 110.67, Th ¼ 0.007, max daily consumption ¼ 135.13). At 24 C, the C. malaccensis consumed almost as many preys as when at 32 C. The female C. malaccensis consumed the 111 larvae and 55 nymphs at 24 C, while 111 larvae and 58 nymphs at 32 C. The male consumed 71 larvae and 41 nymphs at 24 C, 75 larvae and 43 nymphs at 32 C. Besides, when temperature was between 24 C and 32 C, C. malaccensis consumed much more preys than 16 C and 20 C. When at low temperature (16 C), C. malaccensis moved slowly and the Th was longer. The predation ability was poorer than it at high temperature (32 C). The results indicated that low temperature did greater harm to the predation activity of C. malaccensis than high temperature. The results implied that C. malaccensis had the different degree ability to control various stages of A. ovatus. And it was more efficient to control the population at the young stages, with females doing better than males.
Table 1 Functional response parameters of female C.malaccensis to different stages of A. ovatus in 24 h. Temperature( C)
prey stage
a
Th
a/Th
Max consumption
Na
16
female male nymph larva female male nymph larva female male nymph larva female male nymph larva female male nymph larva
0.493 0.566 0.554 0.587 0.464 0.558 0.584 0.743 0.487 0.893 0.681 0.668 0.863 0.619 0.678 0.819 0.638 0.536 0.739 0.769
0.297 0.162 0.02 0.01 0.317 0.137 0.017 0.01 0.268 0.117 0.018 0.009 0.137 0.055 0.012 0.007 0.228 0.147 0.017 0.009
1.66 3.494 27.156 56.44 1.464 4.073 34.353 72.136 1.817 7.632 38.267 74.222 6.299 11.255 56.975 110.676 2.798 3.646 43.471 85.444
3.37 6.173 49.02 96.154 3.155 7.29 58.824 97.087 3.731 8.54 55.556 111.111 7.299 18.182 84.034 135.135 4.386 6.803 58.824 111.111
Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na
20
24
28
32
R2 ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.493N/(1 0.566N/(1 0.554N/(1 0.587N/(1 0.464N/(1 0.558N/(1 0.584N/(1 0.743N/(1 0.487N/(1 0.893N/(1 0.681N/(1 0.668N/(1 0.863N/(1 0.619N/(1 0.678N/(1 0.819N/(1 0.638N/(1 0.536N/(1 0.739N/(1 0.769N/(1
þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ
0.146N) 0.092N) 0.011N) 0.006N) 0.147N) 0.076N) 0.009N) 0.007N) 0.131N) 0.104N) 0.012N) 0.006N) 0.118N) 0.034N) 0.008N) 0.006N) 0.145N) 0.079N) 0.013N) 0.007N)
0.921** 0.923** 0.917** 0.933** 0.932** 0.964** 0.939** 0.985** 0.796* 0.980** 0.940** 0.967** 0.874** 0.993** 0.935** 0.961** 0.990** 0.975** 0.984** 0.999**
1)*p < 0.05, **p < 0.01. 2)Max consumption means the number of the max daily consumption for A. ovatus.
Table 2 Functional response parameters of male C. malaccensis to different stages of A. ovatus in 24 h. Temperature( C)
prey stage
a
Th
a/Th
Max consumption
Na
16
nymph larva nymph larva nymph larva nymph larva nymph larva
0.583 0.691 0.636 0.749 0.856 0.737 0.814 0.778 0.593 0.679
0.026 0.024 0.027 0.015 0.024 0.014 0.020 0.013 0.023 0.013
22.423 28.792 23.556 49.933 35.667 52.643 40.099 59.846 25.783 51.053
38.462 41.667 37.037 66.667 41.667 71.429 49.261 78.125 43.478 75.188
Na Na Na Na Na Na Na Na Na Na
20 24 28 32
1)*p < 0.05, **p < 0.01. 2)Max consumption means the number of the max daily consumption for A. ovatus.
R2 ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.583N/(1 0.691N/(1 0.636N/(1 0.749N/(1 0.856N/(1 0.737N/(1 0.814N/(1 0.778N/(1 0.593N/(1 0.679N/(1
þ þ þ þ þ þ þ þ þ þ
0.015N) 0.017N) 0.017N) 0.011N) 0.021N) 0.010N) 0.016N) 0.010N) 0.014N) 0.009N)
0.839** 0.983** 0.975** 0.990** 0.848** 0.995** 0.964** 0.791* 0.739** 0.909**
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P. Zhu et al. / Journal of Stored Products Research 84 (2019) 101525
3.2. Effects of predator interference on functional response The interference among adult female C. malaccensis under different temperatures was shown in Table 3. Due to the interference and competition among predators, the total amount of consumed preys increased, while the mean consumption decreased with the density of predator increasing at the same temperature (Fig. 2). It indicated that the predator interference decreased the predation efficiency. As was shown, the estimation of attack rate (Q) without competition and interference coefficient (m) increased with the temperature increasing, reaching the peak at 28 C. Cheyletus malaccensis at higher temperatures had higher m value, such as 24, 28 and 32 C, than at low ones, and there were insignificant difference among treatments at higher temperatures. At low temperature 16 C, both predators and preys moved slowly so that the interference coefficient was the least. 3.3. Preference of C. malaccensis on A. ovatus When all different stages of prey were equal number, the consumption of female C. malaccensis was significantly different (F4, 45 ¼ 475.9, P ¼ 0.000). The number of larvae consumed was significantly higher than nymphs, eggs and adults. The preference of C. malaccensis was significantly different (F4, 45 ¼ 318.25, P ¼ 0.000). The preference (Ci) against egg, larva, nymph, male and female adult of A. ovatus were 0.532, 0.412, 0.243, 0.349 and 0.755 respectively (Table 4). Cheyletus malaccensis showed positive preference to larva and nymph of A. ovatus, while negative preference to egg and adult of A. ovatus. The results indicated that C. malaccensis was a good biological control agent to against the nymph and larva of A. ovatus. 4. Discussion The functional response of C. malaccensis to A. ovatus is type II functional response. This response was common in many predators (Holling, 1959) and noticed in Cheyletus eruditus Schrank (Xia et al., 2007) and Neoseiulus barkeri Hughes preying on A. ovatus (Li et al., 2008), N. californicus on Tetranychus urticae Koch (Ahn et al., 2010). Nevertheless, nymphs and adults of Euseius concordis Chant displayed a type III functional response when preying on immature stages and females of Mononychellus tanajoa Bondar (Costa et al., 2014). Furthermore, the functional response of predators against different stages of prey may show different types. Stethorus tridens Gordon presented type III functional response when feeding on eggs and larvae of Tetranychus bastosi Tuttle, while, type II functional response against nymphs and adults (Costa et al., 2017). These indicated that the functional response of a predator may shift between type II and type III (Ganjisaffar and Perring, 2015). It’s reported that the functional response can be influenced by abiotic (including ambient temperature, humidity and arena) and biotic factors, like prey characteristics, predator age and body size (Kalinoski and DeLong, 2016; Uiterwaal et al., 2017).
Table 3 The interference among female C. malaccensis under different temperature. T/ C 16 20 24 28 32
predator density 1e9 1e9 1e9 1e9 1e9
Mean consumptions 4.0e1.78 5.5e2.56 6.5e2.44 8.5e3.0 7.0e2.67
R2 R2
A 0.318
A ¼ 4.320P A ¼ 5.553P0.336 A ¼ 6.106P0.435 A ¼ 8.596P0.485 A ¼ 7.226P0.463
1)*p < 0.05, **p < 0.01. 2)Mean consumption refers to the average number of prey consumed.
0.822** 0.955** 0.961** 0.996** 0.980**
Egg consumption of natural enemies is very important for pest control. Many predators prefer to prey eggs. E. concordis consumed more eggs than larvae, nymphs or adults of M. tanajoa (Costa et al., 2014). Galendromus flumenis Chant consumed significantly more eggs than other stages of Oligonychus pratensis Banks (Ganjisaffar and Perring, 2015), which was similar with Amblyseius largoensis Muma preyed on Raoiella indica Hirst and Euseius hibisci Chant ~ a, 2012). against T. urticae eggs (Badii et al., 2004; Carrillo and Pen However, the female Kampimodromus aberrans Oudemans had lower consumption rate to T. urticae eggs than its larvae (Kasap and Atlihan, 2011), which was in accordance with the present study that C. malaccensis adults consumed few A. ovatus eggs (adult predators generally didn’t eat egg, with few taking less than 3). Similarly, immature stages of C. malaccensis more favored larvae than eggs of T. putrescentiae (Yousef et al., 1982). The lower consumption on eggs might be that eggs provided lower nutritional benefits to certain predators (Ganjisaffar and Perring, 2015). Food consumption of predator decreased with growth of prey. E. hibisci cleared only about 8, 7, 4.6, 0.7 and 0.3% of the initial number of T. urticae eggs, larvae, protonymphs, deutonymphs and adults, respectively (Badii et al., 2004). Galendromus flumenis ate the most eggs and least deutonymphs of O. pratensis (Ganjisaffar and Perring, 2015). In present study, C. malaccensis preyed on more larvae and nymphs than adults. The greater consumption for young stages prey and less for adult ages might be the factors that prey defense mechanisms and the nutritional value (Badii et al., 2004). The preference for prey early stages was important for pest management thus the population would be controlled at young stage. It will be better to control stored pests to combine C. malaccensis with an effective egg predator Blattisocius keegani Fox that fed on eggs of Cryptolestes, Tribolium, Trogoderma, Oryzaephilus, and the mites Glycyphagus domesticus De Geer, Aeroglyphus robustus Banks (Barker, 1967). The predation efficacy of female C. malaccensis was higher than male adults. Similar finding was observed in N. barkeri preying upon A. ovatus (Li et al., 2008), C. eruditus on A. ovatus (Xia et al., 2007). It might be that the greater female C. malaccensis body size can account for its larger food consumption than male. Even Brose (2010) suggested that larger predators covered more ground and encountered more prey. The reason might be female need more energy and nutrients to maintain produce eggs. The functional response of C. malaccensis was affected by temperature. Generally consumption rate increased with increasing temperature. The handling time of N. californicus to T. urticae declined significantly with temperature increasing from15 C to 35 C (Ahn et al., 2010). Phytoseiulus persimilis was increasingly efficient against T. urticae with the temperature going up (Hoque et al., 2010). It could be that mites, as ectotherm animals, moved slowly in colder temperatures, and the metabolic processes increased when warming, rendering faster movement and contacts of predator and prey (Kalinoski and DeLong, 2016). Cheyletus malaccensis devoured more A. ovatus at higher temperature (24e32 C), but reached the peak at 28 C. Similarly, at five constant temperatures (16, 20, 24, 28 and 32 C), N. barkeri was most effective against A. ovatus at 28 C (Li et al., 2008). The P. persimilis foraged more preys as the temperature increased from 15 C to 25 C, but the number of prey consumed then decreased at 30 C (Skirvin and Fenlon, 2003). The reason may be different predators and preys can bear different temperatures. It indicated that it was feasible to control A. ovatus in stored products and commercially produce acarophagous C. malaccensis by A. ovatus between 24 and 32 C. Because of interference and competition among predators, maybe not each individual predatory mite could make full use of their control potential. It might cause the waste of the predatory mites if too much predators were released into the population of
P. Zhu et al. / Journal of Stored Products Research 84 (2019) 101525
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Table 4 Preference of adult female C. malaccensis to different stages of A. ovatus (Mean ± SE.). stages
Prey offered
Fi
Prey consumed
Qi(%)
Ci
Egg Larva Nymph Male Female
20 20 20 20 20
20% 20% 20% 20% 20%
1.7 ± 0.458b 13.2 ± 1.077e 9.0 ± 0.894d 2.7 ± 0.640c 0.8 ± 0.400a
6.22 ± 1.733b 48.18 ± 3.462e 32.91 ± 1.428d 9.79 ± 1.997c 2.89 ± 1.449a
0.532 ± 0.107b 0.412 ± 0.031e 0.243 ± 0.021d 0.349 ± 0.089a 0.755 ± 0.123c
1)Prey offered means the number of prey offered. 2)Prey consumed means the number of prey consumed. 3)Values with different letters within a column are statistically different (comparison of 95% CI).
pests. The degree of control would be poor if too little predators were released into pests. It might be helpful to give instructions on how many predators would be released. Moreover, C. malaccensis might be contaminated by the bacteria carried by its prey, which would affect its fitness and reproduction and have a negative impact on biological performance. Therefore, these effects must be taken into consideration in practical application. Declaration of competing interest We all authors declare that: (i) no support, financial or otherwise, has been received from any organization that may have an interest in the submitted work; and (ii) there are no other relationships or activities that could appear to have influenced the submitted work. Acknowledgement The research was funded by the National Natural Science Foundation of China (31860601, 31760621), Natural Science Foundation of Jiangxi Province (20161BBF60066, 20172BCB22004, 20161ACB20003, 20181BAB204005), funds from Jiangxi Food and Drug Administration (2017YX19), and the Graduate Innovation Foundation of Nanchang University, China (CX2018100). We would like to thank Dr. Alexandra G Duffy (Brigham Young University, USA) for her support and comments on writing. References Ahn, J.J., Kim, K.W., Lee, J.H., 2010. Functional response of Neoseiulus californicus (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae) on strawberry leaves. J. Appl. Entomol. 134 (2), 98e104. Al-Shammery, K.A., 2014. Influence of feeding on three stored product pests on rearing of the predatory mite Cheyletus malaccensis (Acari: Cheyletidae) in Hail, Saudi Arabia. Life Sci. J. 11 (5), 260e266. Athanassiou, C.G., Palyvos, N.E., 2006. Laboratory evaluation of two diatomaceous earth formulations against Blattisocius keegani Fox (Mesostigmata, Ascidae) and Cheyletus malaccensis oudemans (Prostigmata, Cheyletidae). Biol. Control 38 (3), 350e355. Badii, M.H., Hern andez-Ortiz, E., Flores, A.E., Landeros, J., 2004. Prey stage preference and functional response of Euseius hibisci to Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Exp. Appl. Acarol. 34 (3e4), 263. Barker, P.S., 1967. Bionomics of Blattisocius keegani (Fox) (Acarina - Ascidae) a predator on eggs of pests of stored grains. Can. J. Zool. 45, 1093e1099. Brose, U., 2010. Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct. Ecol. 24 (1), 28e34. ~ a, J.E., 2012. Prey-stage preferences and functional and numerical Carrillo, D., Pen responses of Amblyseius largoensis (Acari: Phytoseiidae) to Raoiella indica (Acari: Tenuipalpidae). Exp. Appl. Acarol. 57 (3e4), 361e372. Cebolla, R., Pek ar, S., Hubert, J., 2009. Prey range of the predatory mite Cheyletus malaccensis (Acari: Cheyletidae) and its efficacy in the control of seven storedproduct pests. Biol. Control 50 (1), 1e6. ^go, A.S., Pedro-Neto, M., Sarmento, R.A., 2014. FuncCosta, E.C., Teodoro, A.V., Re tional response of Euseius concordis to densities of different developmental stages of the cassava green mite. Exp. Appl. Acarol. 64 (3), 277e286. Costa, J.F., Matos, C.H.C., Oliveira, C.R.F.D., Silva, T.G.F.D., Neto, I.F.A.L., 2017. Functional and numerical responses of Stethorus tridens Gordon (Coleoptera: Coccinellidae) preying on Tetranychus bastosi Tuttle, baker & sales (Acari: Tetranychidae) on physic nut (Jatropha curcas). Biol. Control 111, 1e5. Dehkordi, S.D., Sahragard, A., 2013. Functional response of Hippodamia variegata
(Coleoptera: Coccinellidae) to different densities of Aphis gossypii (Hemiptera: aphididae) in an open patch design. J. Agric. Sci. Technol. 15 (4), 651e659. ndez-Caldas, E., Baena-Cagnani, C.E., Lo pez, M., Patin ~ o, C., Neffen, H.E., Ferna nchez-Medina, M., Naspitz, C.K., 1993. Cutaneous sensitivity to six mite Sa species in asthmatic patients from five Latin American countries. J. Invest. Allerg. Clin. 3 (5), 245e249. Geary, M.J., Knihinicki, D.K., Halliday, R.B., Russell, R.C., 2000. Contact dermatitis associated with the brown-legged mite, Aleuroglyphus ovatus (Troupeau) (Acari: Acaridae), in Australia. Aust. J. Entomol. 39 (4), 351e352. Ganjisaffar, F., Perring, T.M., 2015. Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis. Biol. Control 82, 40e45. Holling, C.S., 1959. Some characteristics of simple type of predation and parasitism. Can. Entomol. 91 (7), 385e398. Hoque, M.F., Islam, M.W., Khalequzzaman, M., 2010. Functional response of Phytoseiulus persimilis Athias-Henriot to Tetranychus urticae Koch: effects of prey life stages and temperature. Univ. J. Zool. 29 (1), 1e8. Hubert, J., Stejskal, V., Nesvorna, M., Aulicky, R., Kopecky, J., Erban, T., 2016. Differences in the bacterial community of laboratory and wild populations of the predatory mite Cheyletus eruditus (Acarina: Cheyletidae) and bacteria transmission from its prey Acarus siro (Acari: Acaridae). J. Econ. Entomol. 109 (3), 1450e1457. Hughes, A.M., 1976. The mites of stored food and houses. Tech. Bull. Minist. Agric. Fish. Food. 9, 1e400. Jafari, R.E.Z.A., Goldasteh, S.H.I.L.A., 2009. Functional response of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae) on Aphis fabae (Scopoli) (Homoptera: aphididae) in laboratory conditions. Acta Entomol. Serb. 14, 93e100. Kalinoski, R.M., DeLong, J.P., 2016. Beyond body mass: how prey traits improve predictions of functional response parameters. Oecologia 180 (2), 543e550. Kasap, I., Atlihan, R., 2011. Consumption rate and functional response of the predaceous mite Kampimodromus aberrans to two-spotted spider mite Tetranychus urticae in the laboratory. Exp. Appl. Acarol. 53 (3), 253e261. Li, C.P., 2000. An epidemiological survey of pulmonary acariasis in different occupations. China Occup. Med. 27, 23e25. Li, C.P., Cui, Y.B., Wang, J., Yang, Q.G., Tian, Y., 2003. Acaroid mite, intestinal and urinary acariasis. World J. Gastroenterol. 9 (4), 874. Li, P.X., Xia, B., Shu, C., Zhong, L., Li, A.H., 2008. Predation of Amblyseius barkeri on Aleuroglyphus ovatus. Plant Prot. 34 (3), 65e68. a rkov Luk as, J., Stejskal, V., Jarosík, V., Hubert, J., Zd’ a, E., 2007. Differential natural performance of four Cheyletus predatory mite species in Czech grain stores. J. Stored Prod. Res. 43 (1), 97e102. Norris, J.D., 1958. Observations on the control of mite infestations in stored wheat by Cheyletus spp. (Acarina, Cheyletidae). Ann. Appl. Biol. 46 (3), 411e422. Palyvos, N.E., Emmanouel, N.G., 2011. Reproduction, survival, and life table parameters of the predatory mite Cheyletus malaccensis (Acari: Cheyletidae) at various constant temperatures. Exp. Appl. Acarol. 54 (2), 139e150. Pek ar, S., Hubert, J., 2008. Assessing biological control of Acarus siro by Cheyletus malaccensis under laboratory conditions: effect of temperatures and prey density. J. Stored Prod. Res. 44 (4), 335e340. Skirvin, D.J., Fenlon, J.S., 2003. The effect of temperature on the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae). Exp. Appl. Acarol. 31 (1e2), 37e49. Thind, B.B., Dunn, J.A., 2002. A laboratory evaluation of a regulated airflow through wheat at four combinations of temperature and humidity on the productivity of three species of stored product mites. Exp. Appl. Acarol. 27 (1e2), 89e102. Uiterwaal, S.F., Mares, C., DeLong, J.P., 2017. Body size, body size ratio, and prey type influence the functional response of damselfly nymphs. Oecologia 185 (3), 339e346. ~a n, M., Ferna ndez-Caldas, E., 2006. Sensitization and Valdivieso, R., Iraola, V., Estupin exposure to house dust and storage mites in high-altitude areas of Ecuador. Ann. Allergy Asthma Immunol. 97 (4), 532e538. Watt, K.E.F., 1959. A mathematical model for the effect of densities of attacked and attacking species on the number attacked. Can. Entomol. 91 (3), 129e144. Wu, P.X., Ouyang, H.Y., Xu, J., He, J., Zhang, R., Zhang, R.Z., 2016. Predation of Poratrioza sinica Yang Li by the adults of Coccinella septempunctata. J. Appl. Ecol. 27 (11), 3712e3718. Xia, B., Luo, D.M., Zou, Z.W., Xu, R., Zhu, Z.M., 2007. Predation of Cheyletus eruditus on Aleuroglyphus ovatus. Chin. Bull. Entomol. 44, 549e552. Yin, J.D., Li, Y.H., Li, X.E., Mo, W.F., Zhang, C., Wang, J., Xin, T.R., Zou, Z.W., Xia, B.,
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2019. Predation of Cheyletus malaccensis (Acari: Cheyletidae) on Megoura japonica (Hemiptera: aphididae) under five different temperatures. Int. J. Acarol 45 (3), 176e180. Yousef, A.A., Zaher, M.A., Kandil, M.M., 1982. Effect of prey and temperature on the development and biology of Cheyletus malaccensis Oudemans (Acari,
Cheyletidae). J. Appl. Entomol. 93 (1e5), 39e42. Zdarkova, E., 1979. Cheyletid fauna associated with stored products in Czechoslovakia. J. Stored Prod. Res. 15, 11e16. Zhou, J.Z., Chen, C.M., 1987. Quantitative measurement of selectivity of predator for prey. Acta Ecol. Sin. 7 (1), 50e56.
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Functional response of adult Cheyletus malaccensis (Acari: Cheyletidae) to different developmental stages of Aleuroglyphus ovatus (Acari: Acaridae) Peipei Zhu, Yuxiang Fan, Weifen Mo, Tianrong Xin, Bin Xia, Zhiwen Zou* School of Life Science, Nanchang University, Nanchang, 330031, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 July 2019 Received in revised form 25 September 2019 Accepted 6 October 2019 Available online xxx
Cheyletus malaccensis is an important natural enemy of stored pests. In the study, the functional response of C. malaccensis against Aleuroglyphus ovatus was investigated under five constant temperatures of 16, 20, 24, 28 and 32 C. The results showed that the functional response of adult C. malaccensis to different stages of A. ovatus was conformed to Holling II. Under the temperature between 16 and 32 C, C. malaccensis females consumed more larvae and nymphs, followed by male and females of A. ovatus. While male C. malaccensis merely consumed larvae and nymphs of prey. Adult C. malaccensis ate few eggs of A. ovatus. The daily consumption and instantaneous attack rate (a/Th) increased with the temperature increasing from 16 C to 32 C while the peak was at 28 C. The maximum daily consumption for larva and a/Th of female C. malaccensis are 135.1 and 110.7, respectively. Cheyletus malaccensis showed positive preference to larvae and nymphs, while negative preference to adults and eggs of A. ovatus. Because of the competition and interference among predators, the predation efficiency decreased with the density of predator increasing, and the interference coefficient (m) was 0.485 at 28 C. These results could be helpful to provide theoretical basis and practical instructions for the biological control of A. ovatus by C. malaccensis. © 2019 Elsevier Ltd. All rights reserved.
Keywords: Functional response Cheyletus malaccensis Aleuroglyphus ovatus Preference Interference
1. Introduction Mites of the genus Cheyletus, associated with stored grains and stored-product pests (Hughes, 1976; Yousef et al., 1982), are frequently used for biological control agents (Pek ar; Hubert, 2008; Cebolla et al., 2009; Palyvos and Emmanouel, 2011). Cheyletus malaccensis Oudemansis a generalist predator that preys on storedproduct pests, such as Acarus siro Linnaeus, Aleuroglyphus ovatus Troupeau, Caloglyphus redickorzevi Zachvatkin, Lepidoglyphus destructor Schrank, Tyrophagus putrescentiae Schrank, Caloglyphus rodriguezi Samsinak, Rhizoglyphus echinopus Fumouze and Robin, (Yousef et al., 1982; Cebolla et al., 2009; Al-Shammery, 2014). It is known to prey also on other pests, Musca domestica Linnaeus, Lepidocyrtinus incertus Handschin, Ephestia kuehniella Zeller (Yousef et al., 1982; Athanassiou and Palyvos, 2006). It was reported that 90% reduction of A. siro was achieved by releasing three r; Hubert, 2008). Cheyletus malaccensis C. malaccensis at 25 C (Peka
* Corresponding author. E-mail address: [email protected] (Z. Zou). https://doi.org/10.1016/j.jspr.2019.101525 0022-474X/© 2019 Elsevier Ltd. All rights reserved.
is the genius predatory mite. For one thing, it is a generalist predr and ator so that it can well control not only the stored pest (Peka Hubert, 2008; Cebolla et al., 2009) but also the field pest Megoura japonica Matsumura (Hemiptera: Aphididae) (Yin et al., 2019). Cheyletus malaccensis is the most common parthenogenetic predatory mite, and it can reproduce at temperatures between 17.5 and 35 C, and develop in the range between 11.6 and 37.8 C. The immature stages of C. malaccensis varied from 11.3 to 13.8 days and the total 169.7 eggs were laid when feeding on T. putrescentiae at 30 C. Therefore, high fertility, fast multiply, tolerance to wide temperature range and parthenogenesis are beneficial for production in biological control (Zdarkova, 1979; Yousef et al., 1982; Palyvos and Emmanouel, 2011; Hubert et al., 2016). Aleuroglyphus ovatus, a major storage pest mite, damages stored products and causes great economic loss for its fast growth and high fertility. It can transform from egg to adult only 13 days and produce more than 236 eggs in total on artificial diets (our unpublished data). It infests a wide range of stored products, such as stored bran, wheat, chicken meal, dried fish products and traditional Chinese medicine (Geary et al., 2000; Li et al., 2003). In addition, it endangers human health with infection dermatitis,
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allergic rhinitis, asthma, respiratory diseases, pulmonary acariasis and urinary acariasis (Fernandez-Caldas et al., 1993; Li, 2000; Valdivieso et al., 2006). In contrast to greenhouses, orchards or fields, biological control is absent in storages (Luk as et al., 2007). The traditional methods to manage storage pest mites were chemical and physical measures (Norris, 1958; Thind and Dunn, 2002). As a safe and effective way, biological control of A. ovatus needs more attention. Functional response is an important behavioral response to reveal different aspects of prey-predator interactions (Jafari and Goldasteh, 2009) and assess the predation efficacy of predators. Though the functional responses of different predatory mites have been conducted, the functional response of C. malaccensis to A. ovatus has never been reported. The aim of the study is to assess the functional response of C. malaccensis to different stages of A. ovatus under different temperatures, effects of interference among predators on functional response and prey stage preference, which is important to find an effective agent on controlling this pest mite.
2007; Wu et al., 2016): A ¼ QP-m Where A is the mean consumption for a single predator, P is the number of predator, m is the interference coefficient, Q is the max consumption when P ¼ 1. 2.4. Preference of C. malaccensis to A. ovatus A 24 h starved female predator and equal numbers of each stage (egg, larva, nymph, male adult and female adult) preys (total 100 mites) were transferred into the jelly box (25 ml) with cover. After 24 h, the numbers of prey consumed for each stage were recorded. Ten groups were used as replicates. When there were different stages of prey, it was common to calculate the preference of the predator to different preys by the equation (Zhou and Chen, 1987; Wu et al., 2016): Qi ¼(1 þ Ci) /(1-Ci)Fi,
2. Materials and methods 2.1. Mite colony A. ovatus collected from a flourmill nearby Nanchang University were maintained on wheat bran in a climatic chamber (RXZ-260B; Ningbo Dongnan Instrument, China) at 28 C, 85% relative humidity and dark. They were reared more than five years. The predatory mites, C. malaccensis collected from the same place were mass cultured in plastic bottles filled with A. ovatus and wheat bran in the same condition.
in which Qi is the predation rate of the predator against the i-th stage prey, Fi is the proportion of the i-th stage prey, Ci refers to the preference of predator for the i-th prey. When Ci ¼ 0, it means the predator shows no preference for the i-th prey; 0 < Ci < 1, the predator shows positive preference for the i-th prey; 1
2.2. Functional response 3. Results The functional responses of adult C. malaccensis to different stages of A. ovatus were investigated at 16, 20, 24, 28 and 32 C (Yin et al., 2019). Each predator for experiment was starved for 24 h to standardize the hunger degree (Dehkordi and Sahragard, 2013). Various densities and different stages of A. ovatus were transferred into the rearing cell which consisted of a slide on a lid of the film cartridge. Then one pretreated predator was put into the cell. After 24 h, the number of prey consumed was recorded. The densities of egg, adult female and male of A. ovatus were 3, 6, 9, 12 and 15,while larvae and nymphs were 20, 25, 30, 35 and 40. Each experiment was repeated at least 12 times. Holling disc equation (Holling, 1959) was used to describe the functional response of adult C. malaccensis to different stages of A. ovatus:
3.1. Functional response The functional response of adult C. malaccensis against different stages of A. ovatus at different temperatures displayed Holling II (Fig. 1). With the density increasing of prey, the consumption first went up then reaching the plateau (Fig. 2). Female C. malaccensis almost caught and ate all stages of A. ovatus, but barely eggs (less than 3 eggs at the highest initial prey density of 15 of A. ovatus in 24 h). By contrast, male predators merely consumed larvae and nymphs (Table 1), and hardly consumed adults and eggs of A. ovatus. Under any temperatures, adult female C. malaccensis consumed the most larvae followed by nymphs, males and females
Na ¼ aN/ (1 þ aThN) in which a is attack rate, N is the number of preys offered, Na is the number of preys consumed, Th is handling time, a/Th is the instantaneous attack rate. 2.3. Effects of predator interference on functional response Different densities (1, 3, 5, 7 and 9) of female C. malaccensis were released into 50 male adults of A. ovatus in a rearing unit. Then the unit was placed to the climatic chamber. The temperature was also set from 16 to 32 C. After 24-h exposure, the number of eaten A. ovatus was recorded. More than 12 replications were done. In evaluating influence of interference among predators, the following relationships are frequently used (Watt, 1959; Xia et al.,
Fig. 1. The consumed numbers of female C. malaccensis to various densities female A. ovatus at different temperatures.
P. Zhu et al. / Journal of Stored Products Research 84 (2019) 101525
Fig. 2. The interference among adult females of Cheyletus malaccensis varying with densities of preys under different temperatures.
of A. ovatus. The highest daily consumption of females, males, nymphs, larvae of A. ovatus at 28 C was 7.3, 18.2, 84.0 and 135.1, respectively (Table 1). At other temperatures, female C. malaccensis also consumed more immature stage than adults of prey. And its consumption of larvae was about twice than nymph, as well as that of males was far more than females. The maximum predation ability of male C. malaccensis on nymphs and larvae were 40.1 and
3
59.8 at 28 C, which was less than half of female. The consumption of male C. malaccensis against larvae was higher than nymph at any temperatures (Table 2). The predation efficiency of C. malaccensis increased with the temperature increasing, which reached its peak at 28 C. So the value of a, a/Th, the max daily consumption were increased with the temperature rising while Th was decreased. Their value however, it was at 28 C that C. malaccensis shown the peak (a ¼ 0.819, a/ Th ¼ 110.67, Th ¼ 0.007, max daily consumption ¼ 135.13). At 24 C, the C. malaccensis consumed almost as many preys as when at 32 C. The female C. malaccensis consumed the 111 larvae and 55 nymphs at 24 C, while 111 larvae and 58 nymphs at 32 C. The male consumed 71 larvae and 41 nymphs at 24 C, 75 larvae and 43 nymphs at 32 C. Besides, when temperature was between 24 C and 32 C, C. malaccensis consumed much more preys than 16 C and 20 C. When at low temperature (16 C), C. malaccensis moved slowly and the Th was longer. The predation ability was poorer than it at high temperature (32 C). The results indicated that low temperature did greater harm to the predation activity of C. malaccensis than high temperature. The results implied that C. malaccensis had the different degree ability to control various stages of A. ovatus. And it was more efficient to control the population at the young stages, with females doing better than males.
Table 1 Functional response parameters of female C.malaccensis to different stages of A. ovatus in 24 h. Temperature( C)
prey stage
a
Th
a/Th
Max consumption
Na
16
female male nymph larva female male nymph larva female male nymph larva female male nymph larva female male nymph larva
0.493 0.566 0.554 0.587 0.464 0.558 0.584 0.743 0.487 0.893 0.681 0.668 0.863 0.619 0.678 0.819 0.638 0.536 0.739 0.769
0.297 0.162 0.02 0.01 0.317 0.137 0.017 0.01 0.268 0.117 0.018 0.009 0.137 0.055 0.012 0.007 0.228 0.147 0.017 0.009
1.66 3.494 27.156 56.44 1.464 4.073 34.353 72.136 1.817 7.632 38.267 74.222 6.299 11.255 56.975 110.676 2.798 3.646 43.471 85.444
3.37 6.173 49.02 96.154 3.155 7.29 58.824 97.087 3.731 8.54 55.556 111.111 7.299 18.182 84.034 135.135 4.386 6.803 58.824 111.111
Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na Na
20
24
28
32
R2 ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.493N/(1 0.566N/(1 0.554N/(1 0.587N/(1 0.464N/(1 0.558N/(1 0.584N/(1 0.743N/(1 0.487N/(1 0.893N/(1 0.681N/(1 0.668N/(1 0.863N/(1 0.619N/(1 0.678N/(1 0.819N/(1 0.638N/(1 0.536N/(1 0.739N/(1 0.769N/(1
þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ þ
0.146N) 0.092N) 0.011N) 0.006N) 0.147N) 0.076N) 0.009N) 0.007N) 0.131N) 0.104N) 0.012N) 0.006N) 0.118N) 0.034N) 0.008N) 0.006N) 0.145N) 0.079N) 0.013N) 0.007N)
0.921** 0.923** 0.917** 0.933** 0.932** 0.964** 0.939** 0.985** 0.796* 0.980** 0.940** 0.967** 0.874** 0.993** 0.935** 0.961** 0.990** 0.975** 0.984** 0.999**
1)*p < 0.05, **p < 0.01. 2)Max consumption means the number of the max daily consumption for A. ovatus.
Table 2 Functional response parameters of male C. malaccensis to different stages of A. ovatus in 24 h. Temperature( C)
prey stage
a
Th
a/Th
Max consumption
Na
16
nymph larva nymph larva nymph larva nymph larva nymph larva
0.583 0.691 0.636 0.749 0.856 0.737 0.814 0.778 0.593 0.679
0.026 0.024 0.027 0.015 0.024 0.014 0.020 0.013 0.023 0.013
22.423 28.792 23.556 49.933 35.667 52.643 40.099 59.846 25.783 51.053
38.462 41.667 37.037 66.667 41.667 71.429 49.261 78.125 43.478 75.188
Na Na Na Na Na Na Na Na Na Na
20 24 28 32
1)*p < 0.05, **p < 0.01. 2)Max consumption means the number of the max daily consumption for A. ovatus.
R2 ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
0.583N/(1 0.691N/(1 0.636N/(1 0.749N/(1 0.856N/(1 0.737N/(1 0.814N/(1 0.778N/(1 0.593N/(1 0.679N/(1
þ þ þ þ þ þ þ þ þ þ
0.015N) 0.017N) 0.017N) 0.011N) 0.021N) 0.010N) 0.016N) 0.010N) 0.014N) 0.009N)
0.839** 0.983** 0.975** 0.990** 0.848** 0.995** 0.964** 0.791* 0.739** 0.909**
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3.2. Effects of predator interference on functional response The interference among adult female C. malaccensis under different temperatures was shown in Table 3. Due to the interference and competition among predators, the total amount of consumed preys increased, while the mean consumption decreased with the density of predator increasing at the same temperature (Fig. 2). It indicated that the predator interference decreased the predation efficiency. As was shown, the estimation of attack rate (Q) without competition and interference coefficient (m) increased with the temperature increasing, reaching the peak at 28 C. Cheyletus malaccensis at higher temperatures had higher m value, such as 24, 28 and 32 C, than at low ones, and there were insignificant difference among treatments at higher temperatures. At low temperature 16 C, both predators and preys moved slowly so that the interference coefficient was the least. 3.3. Preference of C. malaccensis on A. ovatus When all different stages of prey were equal number, the consumption of female C. malaccensis was significantly different (F4, 45 ¼ 475.9, P ¼ 0.000). The number of larvae consumed was significantly higher than nymphs, eggs and adults. The preference of C. malaccensis was significantly different (F4, 45 ¼ 318.25, P ¼ 0.000). The preference (Ci) against egg, larva, nymph, male and female adult of A. ovatus were 0.532, 0.412, 0.243, 0.349 and 0.755 respectively (Table 4). Cheyletus malaccensis showed positive preference to larva and nymph of A. ovatus, while negative preference to egg and adult of A. ovatus. The results indicated that C. malaccensis was a good biological control agent to against the nymph and larva of A. ovatus. 4. Discussion The functional response of C. malaccensis to A. ovatus is type II functional response. This response was common in many predators (Holling, 1959) and noticed in Cheyletus eruditus Schrank (Xia et al., 2007) and Neoseiulus barkeri Hughes preying on A. ovatus (Li et al., 2008), N. californicus on Tetranychus urticae Koch (Ahn et al., 2010). Nevertheless, nymphs and adults of Euseius concordis Chant displayed a type III functional response when preying on immature stages and females of Mononychellus tanajoa Bondar (Costa et al., 2014). Furthermore, the functional response of predators against different stages of prey may show different types. Stethorus tridens Gordon presented type III functional response when feeding on eggs and larvae of Tetranychus bastosi Tuttle, while, type II functional response against nymphs and adults (Costa et al., 2017). These indicated that the functional response of a predator may shift between type II and type III (Ganjisaffar and Perring, 2015). It’s reported that the functional response can be influenced by abiotic (including ambient temperature, humidity and arena) and biotic factors, like prey characteristics, predator age and body size (Kalinoski and DeLong, 2016; Uiterwaal et al., 2017).
Table 3 The interference among female C. malaccensis under different temperature. T/ C 16 20 24 28 32
predator density 1e9 1e9 1e9 1e9 1e9
Mean consumptions 4.0e1.78 5.5e2.56 6.5e2.44 8.5e3.0 7.0e2.67
R2 R2
A 0.318
A ¼ 4.320P A ¼ 5.553P0.336 A ¼ 6.106P0.435 A ¼ 8.596P0.485 A ¼ 7.226P0.463
1)*p < 0.05, **p < 0.01. 2)Mean consumption refers to the average number of prey consumed.
0.822** 0.955** 0.961** 0.996** 0.980**
Egg consumption of natural enemies is very important for pest control. Many predators prefer to prey eggs. E. concordis consumed more eggs than larvae, nymphs or adults of M. tanajoa (Costa et al., 2014). Galendromus flumenis Chant consumed significantly more eggs than other stages of Oligonychus pratensis Banks (Ganjisaffar and Perring, 2015), which was similar with Amblyseius largoensis Muma preyed on Raoiella indica Hirst and Euseius hibisci Chant ~ a, 2012). against T. urticae eggs (Badii et al., 2004; Carrillo and Pen However, the female Kampimodromus aberrans Oudemans had lower consumption rate to T. urticae eggs than its larvae (Kasap and Atlihan, 2011), which was in accordance with the present study that C. malaccensis adults consumed few A. ovatus eggs (adult predators generally didn’t eat egg, with few taking less than 3). Similarly, immature stages of C. malaccensis more favored larvae than eggs of T. putrescentiae (Yousef et al., 1982). The lower consumption on eggs might be that eggs provided lower nutritional benefits to certain predators (Ganjisaffar and Perring, 2015). Food consumption of predator decreased with growth of prey. E. hibisci cleared only about 8, 7, 4.6, 0.7 and 0.3% of the initial number of T. urticae eggs, larvae, protonymphs, deutonymphs and adults, respectively (Badii et al., 2004). Galendromus flumenis ate the most eggs and least deutonymphs of O. pratensis (Ganjisaffar and Perring, 2015). In present study, C. malaccensis preyed on more larvae and nymphs than adults. The greater consumption for young stages prey and less for adult ages might be the factors that prey defense mechanisms and the nutritional value (Badii et al., 2004). The preference for prey early stages was important for pest management thus the population would be controlled at young stage. It will be better to control stored pests to combine C. malaccensis with an effective egg predator Blattisocius keegani Fox that fed on eggs of Cryptolestes, Tribolium, Trogoderma, Oryzaephilus, and the mites Glycyphagus domesticus De Geer, Aeroglyphus robustus Banks (Barker, 1967). The predation efficacy of female C. malaccensis was higher than male adults. Similar finding was observed in N. barkeri preying upon A. ovatus (Li et al., 2008), C. eruditus on A. ovatus (Xia et al., 2007). It might be that the greater female C. malaccensis body size can account for its larger food consumption than male. Even Brose (2010) suggested that larger predators covered more ground and encountered more prey. The reason might be female need more energy and nutrients to maintain produce eggs. The functional response of C. malaccensis was affected by temperature. Generally consumption rate increased with increasing temperature. The handling time of N. californicus to T. urticae declined significantly with temperature increasing from15 C to 35 C (Ahn et al., 2010). Phytoseiulus persimilis was increasingly efficient against T. urticae with the temperature going up (Hoque et al., 2010). It could be that mites, as ectotherm animals, moved slowly in colder temperatures, and the metabolic processes increased when warming, rendering faster movement and contacts of predator and prey (Kalinoski and DeLong, 2016). Cheyletus malaccensis devoured more A. ovatus at higher temperature (24e32 C), but reached the peak at 28 C. Similarly, at five constant temperatures (16, 20, 24, 28 and 32 C), N. barkeri was most effective against A. ovatus at 28 C (Li et al., 2008). The P. persimilis foraged more preys as the temperature increased from 15 C to 25 C, but the number of prey consumed then decreased at 30 C (Skirvin and Fenlon, 2003). The reason may be different predators and preys can bear different temperatures. It indicated that it was feasible to control A. ovatus in stored products and commercially produce acarophagous C. malaccensis by A. ovatus between 24 and 32 C. Because of interference and competition among predators, maybe not each individual predatory mite could make full use of their control potential. It might cause the waste of the predatory mites if too much predators were released into the population of
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Table 4 Preference of adult female C. malaccensis to different stages of A. ovatus (Mean ± SE.). stages
Prey offered
Fi
Prey consumed
Qi(%)
Ci
Egg Larva Nymph Male Female
20 20 20 20 20
20% 20% 20% 20% 20%
1.7 ± 0.458b 13.2 ± 1.077e 9.0 ± 0.894d 2.7 ± 0.640c 0.8 ± 0.400a
6.22 ± 1.733b 48.18 ± 3.462e 32.91 ± 1.428d 9.79 ± 1.997c 2.89 ± 1.449a
0.532 ± 0.107b 0.412 ± 0.031e 0.243 ± 0.021d 0.349 ± 0.089a 0.755 ± 0.123c
1)Prey offered means the number of prey offered. 2)Prey consumed means the number of prey consumed. 3)Values with different letters within a column are statistically different (comparison of 95% CI).
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