Effect of bran moisture content and initial population

Systematic & Applied Acarology 20(5): 497–506 (2015) http://dx.doi.org/10.11158/saa.20.5.6

ISSN 1362-1971 (print) ISSN 2056-6069 (online)

Article

Effect of bran moisture content and initial population density on mass production of Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) YA-YING LI1, YAN ZHANG1, QIN HU1, LEI LIU1, XUE-NONG XU2, HUAI LIU1* & JIN-JUN WANG1 1

Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, P. R. China 2 Key Laboratory of Integrated Pest Management in crops, Ministry of Agriculture, Institute of Plant Protection, CAAS, Beijing 100193, P. R. China *Corresponding Author: [email protected]

Abstract The mold mite, Tyrophagus putrescentiae (Schrank), is an alternative prey for the predatory mites used in biological control. In order to maximize the food supply and maintain the population of predators, it is very important to understand the effects of bran moisture content (BMC) and initial population density (IPD) on mass production of T. putrescentiae. In the current study, the population increase of T. putrescentiae under six BMCs and five IPDs were evaluated at optimal temperature and humidity with suitable photoperiod conditions. The results showed that the population growth rates of T. putrescentiae were significantly higher with higher BMC. The population increased by 8, 32, 72, 304 times within five weeks under different BMC which was 8.3%, 10%, 15%, 20%, respectively. Unfortunately, when BMC reached to 25%, there was a great amount of mildew growing other than the mites. In the case of IPD, about 10000 adult mites per 100 g bran resulted in the largest final population of T. putrescentiae. However, either lower or higher IPD led to a smaller final population. It was also concluded that population growth rate decreased while the initial density was increasing, ranging from 1,055, 601, 397, 266, 109 times under initial density of ~5,000, 10,000, 15,000, 20,000, 25,000 adult mites per 100 g bran, respectively. Besides, we also described a method in detail for the effective isolation and counting of mites from bran. We found that population growth grew to maximum (over 50,000 mites / bran per gram) under BMC of 20%, IPD of ~50 adults / bran per gram, temperature of 28±1 °C, 80±5% R.H. and photoperiod of all darkness, which could be the best condition for mass production of T. putrescentiae. Our results provide basic biological information for the mass rearing of the mold mite, which will maintain stable and controllable food source for the predatory mites. Key words: mold mite, population increase, counting method, group behavior, mass rearing

Introduction The mold mite, Tyrophagus putrescentiae (Schrank), is one of the most significant mites infesting stored products because of its wide host range and cosmopolitan occurrence (Hughes 1976). It is well known that this mite could infest plenty of stored products heavily (Cunnington 1976; Hughes 1976; Brazis et al. 2008). Moreover, under favorable conditions they could be very abundant in a lot of stored foods with high fat and protein contents (Sánchez-Ramos & Castañera 2005). It has been reported that this mite could be an etiological agent of allergic illness to affect both dogs and human (Bravo et al. 1999; Mueller et al. 2005) and disseminate quite a number of toxigenic fungi (Hubert et al. 2004; Canfield & Wrennt 2010). At present, most work has been dealing with direct and © Systematic & Applied Acarology Society

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indirect damage control of the mite. However, the pest mite, T. putrescentiae (Li et al. 2000), together with some other mold mites such as T. casei (Rasmy et al. 1987), Acarus farris (Ramakers & Van Lieburg 1982), A. siro (Gillespie 1989)), was turned into treasure of artificial propagation of predatory mites, one of the most important commercial production of natural enemies, which have been successfully used as biological control agents against some small sap-sucking pests, including spider mites, thrips and whiteflies (Zhang 2003; Xu et al. 2006; McMurtry et al. 2013; Xu et al. 2013). Because of their high fecundity and low culturing costs, they were used as the alternative prey of some high-efficiency predatory mites, such as Amblyseius cucumeris (Ramakers & Van Lieburg 1982; Rasmy. et al. 1987; Li et al. 2000), A. gossipi (Rasmy et al. 1987), Neoseiulus barkeri and Agistemus exsertus (Rasmy et al. 1987). Generally, there are two lines to achieve the large-scale production of predatory mites; one is “banker plant-prey mite-predatory mite” (Helle & Sabelis 1985), and the other is “wheat bran-mold mite-predatory mite” (Rasmy et al. 1987; Xu et al. 2013). The latter is much more extensively used owing to its low investment and high output. Wheat bran is mostly used for feeding due to its high nutritional potential with low costs (Hemery et al. 2009) and its fluffy characteristic which is propitious to movements of mites (Zhang et al. 2007). In order to obtain enough food supply and accurately control population of predatory mites, it is necessary to make it clear that how and when one can have largest population of mold mite. In general, humidity is a considerable factor affecting dispersal and outbreak of the mites (Auger et al. 1999). In other words, bran moisture content (BMC) which is closely related to humidity is the key factor influencing the population of mold mites. Besides, the population density (PD) is another important factor affecting hexapodous growth by competitive and cooperative mechanism (Berryman et al. 2002). Changing densities in nature further contributes to the differences in the density and diversity (DeMott 1989). It is known that initial population density (IPD) is a specific PD describing the inoculation concentration for rearing (Gower & Buckland 1978), but there has no systematic investigations of the effects of IPDs on the growth of insects and mites. Previous reports have indicated that the mold mites as well as the predatory mites would survive and develop under ambient temperature of 20 to 30 °C and 75 to 95% R.H. (Sánchez-Ramos & Castañera 2005; Xia et al. 2012; Wang et al. 2014). Under these circumstances, it is likely to occur that the mite intra-specifically compete for both food and space. Especially in monospecific communities like mass rearing, intraspecific completion may act to regulate population density (Hooper et al. 2003). Therefore, it is also essential to know that when we need to add diet and nutrition for the mass rearing to regulate mite population. The aim of the present study was to evaluate the population increase of the prey mites regarding to mass rearing possibilities under different environmental conditions. Here, as a first step of investigations and assessments, we describe a detailed method which is simple, cheap and convenient for effective isolation and quick counting of the mites from bran. Specifically, we focused on the comparison of population growth of the mite under various bran moisture content starting with different initial population densities. Such knowledge will constitute a basis for further research on the mass rearing and large-scale releasing of predatory mites in pest control of orchards and greenhouses.

Materials and methods Mite source The acaroid mite, Tyrophagus putrescentiae (Schrank) was initially introduced from the Key Laboratory of Integrated Pest Management in Crops, Institute of Plant Protection, Chinese Academy of Agricultural Science. Mites were maintained on wheat bran in cylindrical plastic cages (6.5cm in 498

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diameter × 3.5cm in depth) at constant temperature 28 ± 1 °C, 80 ± 5% R.H. and complete darkness (Sánchez-Ramos & Castañera 2005; Xia et al. 2012). The cylindrical plastic cages with mites were kept in a RXZ-260B environmental chamber (Ningbo Jiangnan Instrument Factory, Ningbo), connected with an YC-D202 humidifier (Beijing Yadu Science and Technology Co. Ltd., Beijing). Bran was weighed by Electronic Balance FA2204A (Shanghai Jingtian Electronic Instrument Co. Ltd., Shanghai). Mite samples were counted under a SMZ168-TL stereo microscope (Motic China Group Co. Ltd., Shenzhen) and a BX51 light microscope (Olympus Corporation, Tokyo). Each rearing cage (6.5cm in diameter × 3.5cm in depth) was covered with a plastic lid with a 5 cm diameter hole in the center sealed with screen net for ventilation. Mite carrier for weighing was rectangular pieces of paper (5 cm in length × 5 cm in width) pasted in double side tape (4 cm in length × 1 cm in width). Mite containers for measuring total volume were bottomless cylindrical tubes made of plastic injector (1ml volume) divided into 0.05 ml, 0.10 ml, 0.15 ml, 0.20 ml, and 0.25 ml volume, respectively. Counting method Previously, 50, 100, 300, 500 of adults of T. putrescentiae were introduced on the mite carrier for weighting with the help of a thin camel hair brush. The net weight of mites was recorded by an electronic balance. Each treatment was replicated six times. Respectively 0.05 ml, 0.10 ml, 0.15 ml, 0.20 ml, and 0.25 ml volume of adults of mites were measured by the mite containers mentioned before, then moved to Petri dishes (3.5 cm in diameter) filled with 95% ethanol to kill the mites adequately. Besides, the alcoholic solution within dead mites was transferred into 0.25% agar solution at temperature of 30 °C to dilute 20 to 40 times. After the agar solution with mites was shaken firmly for three to five times, the 0.5ml dilute solution measured by a pipette (Eppendorf Research plus 100 - 1000 μl, Eppendorf Vertrieb Deutschland GmbH, Hamburg, Germany) was transferred into Petri dishes (3.5 cm in diameter) to be counted using a stereo microscope. This experiment was replicated nine times. Population increase of T. putrescentiae Bran was sterilized by heat steam sterilization, and oven-dried 72 h by electric thermostatic antique drying box, as well as weighted 100 g adding in double distilled water to cylindrical plastic cages (12 cm in diameter, 14 cm in depth, having a 8 cm in diameter hole in the center sealed with screen net to allow air flow), constituting bran of water content of 10%, 15%, 20%, 25%, and 30%, respectively, whereas bran was dried in the air after sterilizing, whose moisture content was measured to be 8.33%. Each 100 g of bran was introduced in 0.05 ml adults (~5000 adults) of T. putrescentiae. The cages were placed in environmental chambers at constant temperature 28 ± 1 °C, 80 ± 5% R.H. and complete darkness. The amount of T. putrescentiae was recorded at 7, 14, 21, 28, and 35 days after adult mites were introduced. Every time the mite amount was recorded, the cylindrical plastic cages were shaken up for a few seconds to make mite distribute as uniformly as possible. Each replication of treatments was carried out using five point sampling method from top to bottom with each sample 1 g weight. Samples were filtered with two stainless steel sieves (mesh diameter of sieve-1 is 0.50 mm, and that of sieve-2 is 0.05 mm; Qingda Wire Mesh Co., Ltd., Chongqing, China) by running tap water, where bran pulp was kept on sieve-1 and mite was kept on sieve-2. After that mites on the sieve-2 were transferred into 0.25% agar solution to dilute 0 to 400 times to count. At last the bran was added up to 100 g weight after sampling. Each treatment was replicated nine times. As to the IPD experiment, it was conducted in a similar way as described above. Every 100 g of 20% moisture content bran was introduced 0.05 ml, 0.10 ml, 0.15 ml, 0.20 ml, and 0.25 ml adults of T. putrescentiae, respectively, in the cylindrical plastic cages. The experiment was conducted nine replications. 2015

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Data analysis Data were analyzed using SPSS 16.0 statistical analysis software (SPSS, Chicago, IL, USA). For weight and volume experiments, a repeated measure analysis of variance (ANOVA) was conducted with a linear regression equation. Factors were treatments (weights or volumes) and time period (repeated measure), and block (replications) was considered as a random effect. For these two experiments, one-way ANOVA was performed, followed by Tukey-Kramer Honestly Significant Difference (HSD) comparison and Dunnett’s T3 multiple comparison test, respectively. When necessary, data obtained from brain moisture and initial density experiments were first transformed with log10(x) to meet the conditions of parametric statistics. Analysis of these data were performed using ANOVA followed by the Tamhane’s T2 multiple comparison test.

Results Relationship between quantity and weight or volume of adult mites The linear regression between the gross weight and number of the mites was y1 = 5.540×10-3 x1 + 0.172 (r = 0.928, P < 0.05), where y1 is the gross weight of mites and x1 is the number of mites. The gross weight was significantly correlated with the number (Fig. 1; F = 136, df = 23, P < 0.05). The mean gross weight of adult mites at different quantities (50, 100, 300, and 500 adult mites, respectively) was approximately 0.35, 0.80, 1.92 and 2.88 mg, respectively (Fig. 1). Linear regression revealed a significant positive relationship between quantities and total volume of adult mites: y2 = 101.209 x2 + 221.333 (r = 0.963, P < 0.05), where y2 is the number of mites and x2 is the total volume of mites. The mean number of adult mites at different volumes (0.05, 0.10, 0.15, 0.20, and 0.25 ml, respectively) was estimated to be 5,267, 10,737, 15,373, 19,395 and 26,240, respectively (Fig. 2; F = 554, df = 44, P < 0.05).

FIGURE 1. Relationship between number and weight of mass T. putrescentiae adults. Each point represents the mean ± SE of six treatment replications. The linear regression is y1 = 5.540×10-3 x1 + 0.172 (r = 0.928, P < 0.05), where y1 is the gross weight of mites and x1 is the number of mites.

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FIGURE 2. Relationship between volume and number of mass T. putrescentiae adults. Each point represents the mean ± SE of nine treatment replications. The linear regression is y2 = 101.209 x2 + 221.333 (r = 0.963, P < 0.05), where y2 is the number of mites and x2 is the total volume of mites.

Population increase of T. putrescentiae at different bran moistures The population increase of the mites reared in bran with different moistures were investigated. The mite population estimated by sample-counting was recorded after the adult mites were introduced (Fig. 3; F = 33, df = 270, P < 0.05). The population density of mites varied significantly

FIGURE 3. Effect of bran moisture content on population of mites (transformed as logarithm value). The number of treatment replications was nine; analysis of variance indicated significant differences at P < 0.05 by Tamhane’s T2 multiple comparison test. 2015

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with the moisture. Among six treatments, the mite populations under bran moisture of 25% and 30% mostly died, while those under other moisture levels increased significantly in the first three weeks and remained stable in the two weeks afterwards. Besides, the mite population under a higher moisture level was significantly larger than that in a lower one at the same developmental period. The population reached the peak at the third or fourth week after the adult mites were introduced. Mites in 20% BMC had the largest population which was about 2,653,333 per hundred gram bran on the fourth week after the adult mites’ introduction. The population increased by 8, 32, 72, and 304 times within five weeks under respective BMC 8.3%, 10%, 15%, and 20%. Population increase of T. putrescentiae at different initial densities Mites were separated from bran, and counted to show the population increase in different IPDs, which was recorded at intervals of every seven days (Fig. 4; F = 100, df = 225, P < 0.05). Mites with different initial densities about 50, 100, 150, 200, and 250 adults per gram of bran (exact mean value was 53, 107, 154, 194, and 262 adults) were introduced to the cylindrical plastic cages, respectively (Fig. 2). Within the first week, there was a little decrease in the population of mite starting with different IPD rather than increase, except the group starting with 250 adults (Fig. 4). The populations of all five mite groups increased dramatically in the second week, and reached the plateau stage in the third week. However, population with the highest initial density reached a peak which was significantly lower than the other groups in the third week. In addition, we calculated the population densities along with the time for the tested mite groups staring with different initial population densities. The results were similar to our population growth data. As the results indicated, the highest population density of each mite group appeared in the third or fourth week after adult mites transferred, which was similar to the results of moisture experiments.

FIGURE 4. Effect of initial population density on population of mites (transformed as logarithm value). IPD1: the initial density was ~52.6 adults / bran per gram; IPD2: the initial density was ~107.4 adults / bran per gram; IPD3: the initial density was ~153.7 adults / bran per gram; IPD4: the initial density was ~194.0 adults / bran per gram; IPD5: the initial density was ~262.4 adults / bran per gram. The number of treatment replications was nine; analysis of variance indicated significant differences at P < 0.05 by Tamhane’s T2 multiple comparison test. 502

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Discussion To accurately assess the mite amount and density, scientific sampling, isolating and counting method were essential. There were three alternative methods for mites isolating, altering the specific gravity of the extracting solution (Sasa et al. 1961; Ree et al. 1997), filtering mites with a sieve by flushing of running water (Shamiyeh et al. 1971; Natuhara 1989), and utilizing biological characteristics of mites (Shamiyeh et al. 1971; Wharton 1976). However, transferring thousands of mites into different replications was also an arduous task to complete. So the regression equations were built to fit the relationship between the amount and the weight or volume for this mite. As expected, the regression was linear, and goodness of fit test indicated its high reliability (χ2 = 0.86). Based on our observation and operation, measuring a certain volume of the adult mites was an effective and reliable way to estimate the amount of mites, which significantly reduced the working capacity and shortened the operating time from the counting experiments. Previous studies have shown that a reduction in resources or an increase in density has negative effects on somatic growth and juvenile development (Postma et al. 1994; Péry et al. 2002). Here, a comparison of the population increase under different BMCs and IPDs depending on the approach and method used. We obtained a statistically significant difference between the bran moisture contents. Obviously it was more propitious to population growth of the mold mite when the bran moisture content is higher. Unfortunately, humid tropical condition is much more propitious to the development of mould and fungi. It was supported by our moisture experiments results that when the moisture was more than 20%, the humid tropical condition turned to develop the population of fungi, especially Aspergillus fungi, instead of T. putrescentiae. When population increase of different IPD were compared, it indicated to be better that density gradient should be 100 adults per unit. Despite densities of ~100 and 200 adults per unit, we observed that mites of high IPD (~250 adults / unit) colonized in five days, as well as mites of medium IPD (~150 adults / unit) and low IPD (~50 adults / unit) cost nine days to colonize successfully. Nevertheless insect and mite colonies were complex systems where the interactions of many individuals led to colony-level collective behaviors. Although mites of high IPD colonized and developed earlier, the largest population was significantly lower than that of medium or low IPD, showing that density effects were more pronounced at lower densities (Hooper et al. 2003). This is probably related to its food availability and feeding behavior, which in turn may depend directly or indirectly on population density (Vranken et al. 1988; Hooper et al. 2003). In some insect systems, the actions of individuals combine to produce emergent group behaviors, which are often adaptive (Dornhaus et al. 2012). According to our observation, there was an interesting group behavior occurring during later period of all the experiments and laboratory rearing. The populations of T. putrescentiae reached the peak in three or four weeks, and remained stable for about two weeks. However, the population dropped very quickly to naught in several days. We accounted this as scarcity of diet and nutrition at the beginning and added enough bran and dusty yeast into the rearing containers when the population began to drop (Ye & Zhang 2014). In spite of this, the population still could not be maintained anymore. Similar group behaviors like decisionmaking and foraging patterns were studied in ants and honeybees (Detrain & Deneubourg 2008). The mechanism of massive dying behavior of this mite remains unknown and definitely needs further investigation in the future. In order to maintain large amount of predatory mites, many species of stored products mites have been successfully reared as their food resource in the laboratory (Hughes 1976). In the current study, we found that the population of this mite species starting with IPD of ~50 adults / unit could reach the peak (over 50,000 mites / unit) three weeks later with 20% BMC, under temperature of 28

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± 1 °C, 80 ± 5% R.H. and photoperiod of all darkness. In actual mass productions, new bran and additional diet like dusty yeast should be generally provided every three or four weeks. On one hand, the mold mite population increase we had obtained could help us assess quantity of mites in the rearing containers, pursuantly adjust the ratio of predatory and prey to obtain more predatory mites during mass rearing. On the other hand, quantitative assessment resulted from population increase could help control mites amount in packages used for releasing, to avoid the occurrence that predatory mites stay in packages rather than prey pest mites when amount of alternative mites is overabundant, or that predatory mites die of starvation when lacking of prey. Our results will help both in the mass rearing the prey and predatory mites, and in the design of more realistic biological control study that incorporate the effects of density dependence.

Acknowledgements This research was supported in part by the Special Fund for Agro-scientific Research in the public interest from the Ministry of Agriculture, China (200903032) and the Innovation Fund for Graduate Students of Chongqing (CYB2015056).

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