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Article

Comparing the Life Table and Population Projection of Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae) Based on the Age-Stage, Two-Sex Life Table Theory

by
Jihye Park
1,†,
Md Munir Mostafiz
1,†,
Hwal-Su Hwang
1,
Duck-Oung Jung
2,3 and
Kyeong-Yeoll Lee
1,2,3,4,*
1
Division of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University, Daegu 41566, Korea
2
Sustainable Agriculture Research Center, Kyungpook National University, Gunwi 39061, Korea
3
Institute of Agricultural Science and Technology, Kyungpook National University, Daegu 41566, Korea
4
Quantum-Bio Research Center, Kyungpook National University, Gunwi 39061, Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2021, 11(6), 1062; https://doi.org/10.3390/agronomy11061062
Submission received: 30 April 2021 / Revised: 21 May 2021 / Accepted: 24 May 2021 / Published: 25 May 2021
(This article belongs to the Special Issue Integrated Pest Management and Biological Control in Commercial Orchards)
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Versions Notes

Abstract

:
Predatory soil-dwelling mites, Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) (Mesostigmata: Laelapidae), are essential biocontrol agents of small soil arthropod pests. To understand the population characteristics of these two predatory mites, we investigated their development, survival, and fecundity under laboratory conditions. We used Tyrophagus putrescentiae (Schrank) as a food source and analyzed the data using the age-stage, two-sex life table. The duration from egg to adult for G. aculeifer was longer than that for S. scimitus, but larval duration was similar between the two species. Notably, G. aculeifer laid 74.88 eggs/female in 24.50 days, but S. scimitus laid 28.46 eggs/female in 19.1 days. Several population parameters, such as the intrinsic rate of increase, finite rate of increase, net reproductive rate, and gross reproductive rate of G. aculeifer, were significantly higher than those of S. scimitus. Using the bootstrap technique with 100,000 samples, we demonstrated that the life tables constructed based on the 2.5th and 97.5th percentiles of finite rate of increase (λ) net reproductive rate (R0) may characterize the variability in the survival and fecundity curves, as well as predict population growth uncertainty. These data provide important information for the practical application of predatory soil mites to manage agricultural pests.

1. Introduction

Gaeolaelaps aculeifer (Canestrini) and Stratiolaelaps scimitus (Womersley) are predatory, soil-dwelling mites belonging to the family Laelapidae (Acari: Mesostigmata). Typically, these two species are generalist predators and are used effectively as biological control agents of various soil pests, such as thrips pupae, fly maggots, and bulb mites [1,2,3,4,5,6,7]. Moreover, these two predatory mites are beneficial for controlling mushroom flies during mushroom cultivation [3,8,9,10], and control poultry red mite, Dermanyssus gallinae (De Geer) [11,12]. Recent research has shown that G. aculeifer and S. scimitus are natural enemies of Varroa destructor (Anderson and Trueman), the honey bee ectoparasitic mite [13]. They prey on other small soil organisms, such as Collembola, mites, nematodes, and Enchytraeidae [14,15,16,17,18].
The best predators should survive prey scarcity [19], and their populations should be able to survive when the target pest population density is low due to their diverse host range [20]. Furthermore, this ability facilitates rearing on factitious preys, such as the mold mite Tyrophagus putrescentiae (Schrank) (Acari: Sarcoptiformes: Acaridae). T. putrescentiae is an important pest of stored products having a high fat or protein content [21]. T. putrescentiae is routinely used for experimental and commercial rearing of predatory mites [9,22]. Predators, on the other hand, face intense selection pressure for prey quality and density, oviposition-friendly habitats, and antagonist availability [23,24,25,26].
Predator fitness was evaluated using the life table tool. Two-sex life table techniques are now widely used to assess predators’ fitness on prey. Two-sex life table studies assist in understanding an organism’s ecology and fitness, because they take both sexes into account when constructing the population curve for future populations [27,28]. Furthermore, incorporating the life table into constructing a mass-rearing system improves the mass-rearing system’s efficiency [29,30]. Traditional female age-specific life tables [31,32,33,34] ignore stage differentiation in metamorphic species and the effects caused by the male component of a population. In contrast, the age-stage, two-sex life table [35] considers both sexes and precisely describes stage differentiation; therefore, it can properly describe the developmental duration, survival, reproduction, and population growth.
Several studies have been conducted during the past few decades on the effect of diet on the development, fecundity, and mortality of G. aculeifer and S. scimitus, such as mold mite, bulb mite, thrips, and sciarid fly [22,36,37,38,39,40,41]. To the best of our knowledge, no extensive data on the fitness of these two predators employing age-stage, two-sex life methods has ever been published. In this study, we determined the fitness traits and population parameters of G. aculeifer and S. scimitus reared on a single-species diet of T. putrescentiae. We also employed the age-stage, two-sex life table to examine these data, as well as population projection to show the dynamics of stage structure and population growth variability. By considering the importance of integrated pest management, the findings of this study could assist in maintaining the predation of G. aculeifer and S. scimitus on T. putrescentiae.

2. Materials and Methods

2.1. Insect Rearing

The laboratory populations of G. aculeifer and S. scimitus were reared separately following a simple mass-rearing method [42,43]. The two predatory mite species were maintained in two closed plastic boxes (including an inner and outer box) at 25 ± 1 °C, 90% ± 5% relative humidity (RH), and a photoperiod of 16:8 (L:D) h.
The mold mite, T. putrescentiae, was used as prey for both predatory mites. The prey mites were also reared with rice bran as a food source following the same double box system [43].
The two predatory mites were collected from the stock population and reared in Petri dishes (50 mm D × 15 mm H). Cutting a 13.20-mm hole in each lid and covering the hole with a nylon mesh (0.053 mm) allowed ventilation in the Petri dishes. Rice husks (1 cc) were provided as a shelter for the mites in each Petri dish. To maintain constant humidity, water-saturated cotton was placed daily on the hole of each Petri dish (Figure 1).

2.2. Life Table Study of G. aculeifer and S. scimitus

Life table studies were initiated using the egg stages of predatory mites. More than 100 pairs of G. aculeifer and S. scimitus adults were isolated from the mite culture and maintained in the Petri dishes to obtain the egg stages. After 24 h, each newly-laid egg was separated and collected into another Petri dish. Forty-eight G. aculeifer eggs and 41 S. scimitus eggs were used for the life table study. We supplied mixed life stages of T. putrescentiae daily to each Petri dish as prey. The predatory mites’ developmental stage and survival rate were monitored every day. Emerged male and female adults of G. aculeifer and S. scimitus were paired, and each pair was transferred to a new Petri dish with new rice husks and prey. Males from the mass-rearing colony were used to mate with females from the life table cohort, since there were more females than males. The mass-rearing colony’s males were omitted from the life table analysis, and daily oviposited eggs were recorded and discarded. The survival of each adult was recorded daily until the death of all individuals. These bioassays were conducted under laboratory conditions at the temperature and RH conditions described in Section 2.1.

2.3. Life Table Data Analysis

The population parameters, including the intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), mean generation time (T), age-stage-specific survival rate (sxj), age-specific survival rate (lx), age-specific fecundity (mx), adult preoviposition period (APOP) and the total preoviposition period (TPOP), reproductive days (Rd), age-specific maternity (lxmx), age-stage life expectancy (exj), and reproductive value (vxj), were calculated, according to the age-stage, two-sex life table approach [35,44,45,46] using TWOSEX-MSChart [47]. Population parameter variances and standard errors were calculated following the 100,000 random resampling bootstrap technique [48]. The differences in population parameters between G. aculeifer and S. scimitus were evaluated using a paired bootstrap test, based on the confidence intervals implemented in the TWOSEX-MSChart [46,47,49]. All graphs were generated using SigmaPlot v.12.5 (Systat Software Inc., San Jose, CA, USA, 2013).

2.4. Population Projection

The potential population growth of G. aculeifer and S. scimitus on T. putrescentiae was projected according to Chi [50] by incorporating the life table data into TIMING-MSChart [51]. The variability of population growth was projected as described by Huang et al. [49] using life tables representing the 2.5th and 97.5th percentiles, i.e., the 2500th and 97,500th sorted bootstrap results of the net reproductive rate (R0) and finite rate of increase (λ).

3. Results

3.1. Survival and Developmental Characteristics of G. aculeifer and S. scimitus

We observed that the two predatory mite species could complete development and produce offspring when fed on T. putrescentiae. Table 1 shows the developmental times of each stage, preadult duration, adult longevity, reproductive days, and fecundity of females for the two species. The mean developmental time of the egg stage for G. aculeifer and S. scimitus was 3.71 and 2.89 d, respectively (Table 1). The duration of the egg stage was significantly different between the two species (p < 0.0001). However, no significant differences were observed in the duration of larva (p = 0.2783), protonymph (p = 0.3577), and deutonymph (p = 0.6078) between G. aculeifer and S. scimitus. The preadult duration was significantly longer for G. aculeifer (11.51 d) than for S. scimitus (10.69 d). However, there were no significant differences in preadult survival rate (sa) between the two species. Female longevity was significantly higher (p = 0.0165) for G. aculeifer (80.31 d) than S. scimitus (69.71 d). However, there were no significant differences in male longevity between the two species (p = 0.1242) (Table 1). Significant differences were observed in APOP and TPOP between the two predatory mites. The maximum number of reproductive days was recorded for G. aculeifer (24.5 d), which was significantly higher than that for S. scimitus (19.12 d) (p = 0.0288). The fecundity of G. aculeifer (74.88 offspring/female) was also significantly higher than that of S. scimitus (28.46 offspring/female) (p = 0.0285).

3.2. Life Table of G. aculeifer and S. scimitus fed on T. putrescentiae

The age-stage survival rate (sxj) depicts the probability of whether a newly hatched individual would survive to age x and stage j (Figure 2). Due to differences in developmental rate among individuals, there was an obvious stage overlap during the developmental period (Figure 2). The female and male adults emerged at 8 and 10 d, respectively, for S. scimitus (Figure 2). In contrast, female and male adults appeared at 9 and 10 d, respectively, for G. aculeifer (Figure 2). The longer longevity of female adults compared to males could be observed in Figure 2.
Figure 3 shows the age-specific survival rate (lx), female age-specific fecundity (fx5) (the female adult being in the fifth life stage), age-specific fecundity (mx), and age-specific maternity (lxmx) for G. aculeifer and S. scimitus fed on T. putrescentiae. The lx curve of G. aculeifer was significantly decreased from age 50 d, whereas that of S. scimitus decreased from age 37 d (Figure 3). The parameter, fx5, is the mean number of fertilized eggs produced by the female adult at age x. The highest peak of fx5 was observed for G. aculeifer fed on T. putrescentiae at age 18 d (f18,5 = 4.8 eggs). Based on the curve, mx, the highest peaks occurred at age 18 d (with 3.04 offspring) for G. aculeifer, and at age 24 d (with 0.86 offspring) for S. scimitus (Figure 3). Based on both lx and mx, the maximum lxmx value of 3.04 offspring was recorded for G. aculeifer at age 18 d, whereas its value of 0.86 offspring was recorded for S. scimitus at age 24 d (Figure 3).
Life expectancy (exj) indicates the length of time an individual of age x and stage j is expected to survive. The curves of exj of the egg, larva, protonymph, deutonymph, and adult of G. aculeifer fed on T. putrescentiae were higher than those of S. scimitus (Figure 4). The life expectancy values of a newly-laid egg of G. aculeifer and S. scimitus were 67.33 and 60.34 d, respectively (Figure 4).
The reproductive value (νxj) indicates the expected contribution of an individual of age x and stage j to the future population. The reproductive value gradually increased with an increase in age and stage, whereas the reproductive value of the female stage dramatically increased when they began to oviposit. The highest reproductive values for G. aculeifer and S. scimitus fed on T. putrescentiae were recorded at age 17 d (v17,5 = 24.11 d−1) and 18 d (v18,5 = 8.61 d−1), respectively (Figure 5).

3.3. Population Parameters

Table 2 shows the population parameters of G. aculeifer and S. scimitus. The intrinsic rate of increase (r), finite rate of increase (λ), net reproductive rate (R0), and gross reproduction rate (GRR) of G. aculeifer fed on T. putrescentiae were 0.1733 d−1, 1.1893 d−1, 47.49 offspring, and 47.53 offspring, respectively. These parameters were significantly higher (p < 0.0001) than the values obtained for S. scimitus (0.1079 d−1, 1.1139 d−1, 18.97 offspring, and 22.03 offspring, respectively) (Table 2). In contrast, the mean generation time (T) obtained for G. aculeifer (22.27 d) was significantly shorter (p < 0.0001) than that for S. scimitus (27.29 d) (Table 2).

3.4. Population Projection

The growth capacities of G. aculeifer and S. scimitus were projected using life table data to demonstrate the increase in the pest population and stage structure during population growth on T. putrescentiae. The population growth and stage structure of G. aculeifer and S. scimitus fed on T. putrescentiae are depicted in Figure 6; the changes in the stage structure can be observed. The fastest population growth was observed for G. aculeifer fed on T. putrescentiae. Starting with 10 eggs, the population of G. aculeifer increased faster than that of S. scimitus fed on T. putrescentiae, which increased slowly (Figure 6). According to the simulation, after 30 d, the total number of eggs, larvae, protonymphs, deutonymphs, female, and male adults of G. aculeifer was 112, 18, 55, 68, 46, and 29, respectively (Figure 6).
Figure 7 shows the total population sizes of the original cohort and those based on the 2.5th and 97.5th bootstrap percentiles of the finite rate and net reproductive rate, which helps understand the variability of population growth. The population growth rates of G. aculeifer and S. scimitus on T. putrescentiae were different. This could be attributed to differences in developmental time, viability, and fertility among individuals (Figure 7). The total population size of G. aculeifer and S. scimitus reached 76.76 and 27.93 individuals on day 30 when fed on T. putrescentiae, respectively (Figure 7).

4. Discussion

This study has shown that G. aculeifer had higher fecundity, intrinsic rate of increase, finite rate of increase, and shorter mean generation time than S. scimitus when fed on T. putrescentiae. Preadult survival and reproduction rates of insects on a prey that are higher indicate that the prey is more suitable [52]. Although this prey mite species has been used commercially for rearing G. aculeifer and S. scimitus [9,22], we used the age-stage, two-sex life table technique to compare the fitness traits of these two predatory mite species that feed on T. putrescentiae. The predator–prey interaction, population development, survival, and reproduction can all be assessed using life table parameters [53,54].
In a predator–prey relationship, predator fitness is extremely important. It is affected by many factors, such as prey size and density [55,56], environmental factors, i.e., temperature, humidity [57,58], habitat complexity, and internal state of the predator [54,59]. Changes in the developmental rate, survival rate, fecundity, and reproductive age can all be attributed to these factors [60,61]. Our study showed that G. aculeifer and S. scimitus could complete their development and reproduction when fed on T. putrescentiae, but the fitness of these two species differed due to differences in survival, development, and fecundity. S. scimitus was found to be less suited to T. putrescentiae than G. aculeifer due to its prolonged TPOP and preadult length, as well as its lower fecundity and reproductive value. On the other hand, G. aculeifer is more suited and susceptible when fed on T. putrescentiae, because it has longer adult longevity, and life expectancy, higher fecundity, and population parameters (Table 1 and Table 2).
Preys have been found to have an impact on the survival and development of numerous insects in previous studies [26,52,62]. Ajvad et al. [41] reported that female and male longevity of G. aculeifer fed on sciarid larvae was 67.7 and 60.3 d, respectively. Kakimoto et al. [63] revealed that the longevity of Orius similis Zheng females and males was 27.2 d and 13.2 d, respectively, compared with that of Orius sauteri (23.8 d and 14.5 d, respectively) when fed with Ephestia kuehniella Zeller. In another study, Asgari et al. [52] reported that male adult longevity (14.46 d) of Amblyseius swirskii Athias-Henriot was shorter than female adult longevity (16.61 d) when fed on T. putrescentiae. The same trend was observed in this study, where the total longevity of female and male adults (80.31 d and 73.33, respectively) of G. aculeifer was increased when fed on T. putrescentiae. Alternatively, the total longevity of females and males of S. scimitus was lower (69.71 d and 64.25 d, respectively) than G. aculeifer. This could be due to the nutritional content or quality of the specific diet/prey, decreased food pressure throughout development, physical defense or response of the prey, more feeding resources [62,64,65], predator preference behavior toward laying eggs [66,67], and complete physiological reactions in the insect body under selection pressure [68].
The life parameters, particularly r and λ, represent the various population features such as the developmental rate, fecundity, survival rate, and the population growth rate together to evaluate the population fitness. This theory supported the present study and showed that G. aculeifer showed higher R0, r, λ, and GRR values when fed on T. putrescentiae under our test conditions.
A population projection based on the age-stage, two-sex life table can reveal the change in stage structure during population growth. Understanding stage structure is vital to pest management, because predatory mites’ dispersal and damage capability vary with stage. This study demonstrated that such a life table could provide a comprehensive description of predatory mite population’s fitness on a given prey. The predicted population growth through time according to the age-stage, two-sex life table data can be described using the stages, as shown in Figure 6. Due to the incapability of traditional female age-specific life tables [31,32,34], to describe the stage differentiation, it would not be possible to show the stage structure, as shown in Figure 6.
We also demonstrated the variability of population growth using computer projections based on the bootstrap percentile confidence intervals. It is the first study to use the life tables of G. aculeifer and S. scimitus to depict the population growth range that is lower and upper 2.5th and 97.5th percentile to the most appropriate level of range for simulation (Figure 7). The findings revealed that insect populations have a lot of fluctuation and that including the life table variability into population projections is critical.

5. Conclusions

In conclusion, our study’s life table parameters and population prediction analysis demonstrated that G. aculeifer has greater efficiency as a natural enemy than S. scimitus. The obtained results support Hwang et al.’s study [43] indicating that the G. aculeifer population increased to a higher density than that of S. scimitus using a simple mass-rearing method. We strongly promote the use of age-stage, two-sex life table in pest management programs at the age stage to anticipate population growth, stage structure, and possible damage by including stage-specific consumption rates in their control strategies.

Author Contributions

Conceptualization: J.P., M.M.M., and K.-Y.L.; methodology: J.P, M.M.M., H.-S.H., D.-O.J., and K.-Y.L.; software: M.M.M.; formal analysis: M.M.M.; investigation: K.-Y.L.; resources: K.-Y.L.; data curation: K.-Y.L.; writing—original draft preparation: J.P. and M.M.M.; writing—review and editing: M.M.M. and K.-Y.L.; supervision: K.-Y.L.; project administration: K.-Y.L.; funding acquisition: K.-Y.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by a research fund (PJ01336201) from the Rural Development Administration.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

There is no supplementary information to reveal; all information is contained in this manuscript.

Acknowledgments

We would like to thank Hsin Chi (Department of Entomology, National Chung Hsing University, Taichung 402, Taiwan) for his support and invaluable advice.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Walter, D.E.; Oliver, J.H. Geolaelaps oreithyiae, n. sp. (Acari, Laelapidae), a Thelytokous Predator of Arthropods and Nematodes, and a Discussion of Clonal Reproduction in the Mesostigmata. Acarologia 1990, 30, 293–303. [Google Scholar]
  2. Navarro-Campos, C.; Wäckers, F.L.; Pekas, A. Impact of Factitious Foods and Prey on the Oviposition of the Predatory Mites Gaeolaelaps Aculeifer and Stratiolaelaps Scimitus (Acari: Laelapidae). Exp. Appl. Acarol. 2016, 70, 69–78. [Google Scholar] [CrossRef] [PubMed]
  3. Chambers, R.J.; Wright, E.M.; Lind, R.J. Biological Control of Glasshouse Sciarid Flies (Bradysia spp.) with the Predatory Mite, Hypoaspis Miles on Cyclamen and Poinsettia. Biocontrol Sci. Technol. 1993, 3, 285–293. [Google Scholar] [CrossRef]
  4. Bennison, J.A.; Maulden, K.; Maher, H. Choice of Predatory Mites for Biological Control of Ground-Dwelling Stages of Western Flower Thrips Within a “Push-Pull” Strategy on Pot Chrysanthemum. IOBC. WPRS Bull. 2002, 25, 9–12. [Google Scholar]
  5. Walter, D.E.; Campbell, N.J.H. Exotic vs. Endemic Biocontrol Agents: Would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), Please Stand Up? Biol. Control 2003, 26, 253–269. [Google Scholar] [CrossRef]
  6. Freire, R.A.P.; de Moraes, G.J.; Silva, E.S.; Vaz, A.C.; de Campos Castilho, R. Biological Control of Bradysia Matogrossensis (Diptera: Sciaridae) in Mushroom Cultivation with Predatory Mites. Exp. Appl. Acarol. 2007, 42, 87–93. [Google Scholar] [CrossRef]
  7. Park, J.; Mostafiz, M.M.; Hwang, H.-S.; Jung, D.-O.; Lee, K.-Y. Comparison of the Predation Capacities of Two Soil-Dwelling Predatory Mites, Gaeolaelaps Aculeifer and Stratiolaelaps Scimitus (Acari: Laelapidae), on Three Thrips Species. J. Asia. Pac. Entomol. 2021, 24, 397–401. [Google Scholar] [CrossRef]
  8. Ali, O.; Dunne, R.; Brennan, P. Effectiveness of the Predatory Mite Hypoaspis Miles (Acari: Mesostigmata: Hypoaspidae) In Conjunction with Pesticides for Control of the Mushroom Fly Lycoriella solani (Diptera: Sciaridae). Exp. Appl. Acarol. 1999, 23, 65–77. [Google Scholar] [CrossRef]
  9. Cabrera, A.R.; Cloyd, R.A.; Zaborski, E.R. Development and Reproduction of Stratiolaelaps scimitus (Acari: Laelapidae) with Fungus Gnat Larvae (Diptera: Sciaridae), potworms (Oligochaeta: Enchytraeidae) or Sancassania aff. sphaerogaster (Acari: Acaridae) as the Sole Food Source. Exp. Appl. Acarol. 2005, 36, 71–81. [Google Scholar]
  10. Jeon, H.Y.; Kim, H.H.; Jung, J.A.; Kang, T.J.; Yang, C.Y. Damage Status of Poinsettia by the Fungus Gnat (Bradysia difformis) and Its Control with Predatory Mite (Hypoaspis aculeifer). Korean J. Hortic. Sci. Technol. 2007, 25, 468–473. [Google Scholar]
  11. Ali, W.; George, D.R.; Shiel, R.S.; Sparagano, O.A.E.; Guy, J.H. Laboratory Screening of Potential Predators of the Poultry Red Mite (Dermanyssus Gallinae) and Assessment of Hypoaspis Miles Performance under Varying Biotic and Abiotic Conditions. Vet. Parasitol. 2012, 187, 341–344. [Google Scholar] [CrossRef] [PubMed]
  12. Lesna, I.; Sabelis, M.W.; van Niekerk, T.G.C.M.; Komdeur, J. Laboratory Tests for Controlling Poultry Red Mites (Dermanyssus Gallinae) with Predatory Mites in Small ‘Laying Hen’ Cages. Exp. Appl. Acarol. 2012, 58, 371–383. [Google Scholar] [CrossRef] [Green Version]
  13. Rangel, J.; Ward, L. Evaluation of the Predatory Mite Stratiolaelaps Scimitus for the Biological Control of the Honey Bee Ectoparasitic Mite Varroa destructor. J. Apic. Res. 2018, 57, 425–432. [Google Scholar] [CrossRef]
  14. Kevan, D.K.M.; Sharma, G.D. Observations on the Biology of Hypoaspis Aculeifer (Canestrini 1884), Apparently New to North America (Acarina: Mesostigmata: Laelaptidae). Acarologia 1964, 6, 647–658. [Google Scholar]
  15. Ragusa, S.; Zedan, M.A.; Sciacchitano, M.A. The Effects of Food from Plant and Animal Sources on the Development and Egg Production of the Predaceous Mite Hypoaspis Aculeifer (Canestrini) (Parasitiformes, Dermanyssidae). Redia 1986, 69, 481–488. [Google Scholar]
  16. Sardar, M.A.; Murphy, P.W. Feeding Tests of Grassland Soil-Inhabiting Gamasine Predators. Acarologia 1987, 28, 117–121. [Google Scholar]
  17. Karg, W. Raubmilben als lndikatoren bei der Entwicklung eines Ökologisch Orientierten Pflanzenschutzes. Nachr. Dtsch. Pflanzenschutzd. 1995, 47, 149–156. (In Germany) [Google Scholar]
  18. Axelsen, J.A.; Holst, N.; Hamers, T.; Krogh, P.H. Simulations of the Predator-Prey Interactions in a Two Species Ecotoxicological Test System. Ecol. Modell. 1997, 101, 15–25. [Google Scholar] [CrossRef]
  19. Hiltunen, T.; Kaitala, V.; Laakso, J.; Becks, L. Evolutionary Contribution to Coexistence of Competitors in Microbial Food Webs. Proc. R. Soc. B Biol. Sci. 2017, 284, 20170415. [Google Scholar] [CrossRef] [Green Version]
  20. Sabelis, M.W.; Van Rijn, P.C. Predation by Insects and Mites. In Thrips as Crop Pests; Lewis, T., Ed.; CABI: Wallingford, Oxfordshire, UK, 2021; pp. 259–354. [Google Scholar]
  21. Malik, A.; Gulati, R.; Duhan, K.; Poonia, A. Tyrophagus Putrescentiae (Schrank) (Acari: Acaridae) as a Pest of Grains: A Review. J. Entomol. Zool. Stud. 2018, 6, 2543–2550. [Google Scholar]
  22. Enkegaard, A.; Sardar, M.A.; Brødsgaard, H.F. The Predatory Mite Hypoaspis Miles: Biological and Demographic Characteristics on Two Prey Species, the Mushroom Sciarid Fly, Lycoriella Solani, and the Mould Mite, Tyrophagus Putrescentiae. Entomol. Exp. Appl. 1997, 82, 135–146. [Google Scholar] [CrossRef]
  23. Saeed, R.; Razaq, M. Effect of Prey Resource on the Fitness of the Predator Chrysoperla Carnea (Neuroptera: Chrysopidae). Pak. J. Zool. 2015, 47, 103–109. [Google Scholar]
  24. Aragón-Sánchez, M.; Román-Fernández, L.R.; Martínez-García, H.; Aragón-García, A.; Pérez-Moreno, I.; Marco-Mancebón, V.S. Rate of Consumption, Biological Parameters, and Population Growth Capacity of Orius Laevigatus Fed on Spodoptera Exigua. BioControl 2018, 63, 785–794. [Google Scholar] [CrossRef]
  25. Amer, M.E.S.; Fu, Y.; Niu, L. Biological Aspects of Orius Similis Zheng Reared on Two Preys at Three Constant Temperatures. J. Agric. Sci. Technol. A 2018, 8, 350–363. [Google Scholar]
  26. Liu, P.; Jia, W.; Zheng, X.; Zhang, L.; Sangbaramou, R.; Tan, S.; Liu, Y.; Shi, W. Predation Functional Response and Life Table Parameters of Orius Sauteri (Hemiptera: Anthocoridae) Feeding on Megalurothrips Usitatus (Thysanoptera: Thripidae). Fla. Entomol. 2018, 101, 254–259. [Google Scholar] [CrossRef]
  27. Ali, S.; Li, S.; Jaleel, W.; Musa Khan, M.; Wang, J.; Zhou, X. Using a Two-Sex Life Table Tool to Calculate the Fitness of Orius Strigicollis as a Predator of Pectinophora Gossypiella. Insects 2020, 11, 275. [Google Scholar] [CrossRef]
  28. Chi, H.; You, M.; Atlıhan, R.; Smith, C.L.; Kavousi, A.; Özgökçe, M.S.; Güncan, A.; Tuan, S.-J.; Fu, J.-W.; Xu, Y.-Y.; et al. Age-Stage, Two-Sex Life Table: An Introduction to Theory, Data Analysis, and Application. Entomol. Gen. 2020, 103–124. [Google Scholar] [CrossRef]
  29. Chi, H.; Getz, W.M. Mass Rearing and Harvesting Based on an Age-Stage, Two-Sex Life Table: A Potato Tuberworm (Lepidoptera: Gelechiidae) Case Study. Environ. Entomol. 1988, 17, 18–25. [Google Scholar] [CrossRef]
  30. Li, X.; Feng, D.; Xue, Q.; Meng, T.; Ma, R.; Deng, A.; Chi, H.; Wu, Z.; Atlihan, R.; Men, L.; et al. Density-Dependent Demography and Mass-Rearing of Carposina Sasakii (Lepidoptera: Carposinidae) Incorporating Life Table Variability. J. Econ. Entomol. 2019, 112, 255–265. [Google Scholar] [CrossRef]
  31. Lewis, E.G. On the Generation and Growth of a Population. Sankhyā Indian J. Stat. 1942, 6, 93–96. [Google Scholar]
  32. Leslie, P.H. On the Use of Matrices in Certain Population Mathematics. Biometrika 1945, 33, 183–212. [Google Scholar] [CrossRef] [PubMed]
  33. Birch, L.C. The Intrinsic Rate of Natural Increase of an Insect Population. J. Anim. Ecol. 1948, 17, 15–26. [Google Scholar] [CrossRef]
  34. Carey, J.R. Applied Demography for Biologists: With Special Emphasis on Insects; Oxford University Press: Oxford, NY, USA, 1993; ISBN 978-0-19-506687-6. [Google Scholar]
  35. Chi, H.; Liu, H. Two New Methods for the Study of Insect Population Ecology. Bull. Inst. Zool. 1985, 24, 225–240. [Google Scholar]
  36. Barker, P.S. The Response of a Predator, Hypoaspis Aculeifer (Canestrini) (Acarina:Laelapidae), to Two Species of Prey. Can. J. Zool. 2011, 47, 343–345. [Google Scholar] [CrossRef]
  37. Lesna, I.; Sabelis, M.; Conijn, C. Biological Control of the Bulb Mite, Rhizoglyphus Robini, by the Predatory Mite, Hypoaspis Aculeifer, on Lilies: Predator-Prey Interactions at Various Spatial Scales. J. Appl. Ecol. 1996, 33, 369–376. [Google Scholar] [CrossRef]
  38. Conijn, C.G.M.; Lesna, I.; Altena, K. Biological Control of the Bulb Mite Rhizoglyphus Robini by the Predatory Mite Hypoaspis Aculeifer on Lilies: Implementation in Practice. Acta Hortic. 1997, 430, 619–624. [Google Scholar] [CrossRef]
  39. Ydergaard, S.; Enkegaard, A.; Brødsgaard, H.F. The Predatory Mite Hypoaspis Miles: Temperature Dependent Life Table Characteristics on a Diet of Sciarid Larvae, Bradysia Paupera and B. Tritici. Entomol. Exp. Appl. 1997, 85, 177–187. [Google Scholar] [CrossRef]
  40. Berndt, O.; Poehling, H.-M.; Meyhöfer, R. Predation Capacity of Two Predatory Laelapid Mites on Soil-Dwelling Thrips Stages. Entomol. Exp. Appl. 2004, 112, 107–115. [Google Scholar] [CrossRef]
  41. Ajvad, F.T.; Madadi, H.; Michaud, J.P.; Zafari, D.; Khanjani, M. Life Table of Gaeolaelaps Aculeifer (Acari: Laelapidae) Feeding on Larvae of Lycoriella Auripila (Diptera: Sciaridae) with Stage-Specific Estimates of Consumption. Biocontrol Sci. Technol. 2018, 28, 157–171. [Google Scholar] [CrossRef]
  42. Jung, D.-O.; Hwang, H.-S.; Kim, J.-W.; Lee, K.-Y. Development of the mass-rearing technique for a predatory mite Stratiolaelaps scimitus (Acari: Laelapidae) using the double box system. Korean J. Appl. Entomol. 2018, 57, 253–260. [Google Scholar]
  43. Hwang, H.-S.; Jung, D.-O.; Park, J.; Lee, K.-Y. Simple Mass-Rearing Technique of a Predatory Mite Gaeolaelaps Aculeifer (Canestrini) (Acari: Laelapidae). Entomol. Res. 2019, 49, 529–533. [Google Scholar] [CrossRef]
  44. Chi, H. Life-Table Analysis Incorporating Both Sexes and Variable Development Rates Among Individuals. Environ. Entomol. 1988, 17, 26–34. [Google Scholar] [CrossRef]
  45. Chi, H.; Su, H.-Y. Age-Stage, Two-Sex Life Tables of Aphidius Gifuensis (Ashmead) (Hymenoptera: Braconidae) and Its Host Myzus Persicae (Sulzer) (Homoptera: Aphididae) with Mathematical Proof of the Relationship between Female Fecundity and the Net Reproductive Rate. Environ. Entomol. 2006, 35, 10–21. [Google Scholar] [CrossRef]
  46. Huang, Y.-B.; Chi, H. Life Tables of Bactrocera cucurbitae (Diptera: Tephritidae): With an Invalidation of the Jackknife Technique. J. Appl. Entomol. 2013, 137, 327–339. [Google Scholar] [CrossRef]
  47. Chi, H. TWOSEX-MSChart: A Computer Program for the Age-Stage, Two-Sex Life Table Analysis; National Chung Hsing University: Taichung, Taiwan, 2021. [Google Scholar]
  48. Efron, B.; Tibshirani, R.J. Introduction to the Bootstrap, Monographs on Statistics and Applied Probability; Chapman and Hall/CRC: London, UK, 1994; ISBN 978-0-412-04231-7. [Google Scholar]
  49. Huang, H.-W.; Chi, H.; Smith, C.L. Linking Demography and Consumption of Henosepilachna Vigintioctopunctata (Coleoptera: Coccinellidae) Fed on Solanum Photeinocarpum (Solanales: Solanaceae): With a New Method to Project the Uncertainty of Population Growth and Consumption. J. Econ. Entomol. 2018, 111, 1–9. [Google Scholar] [CrossRef]
  50. Chi, H. Timing of Control Based on the Stage Structure of Pest Populations: A Simulation Approach. J. Econ. Entomol. 1990, 83, 1143–1150. [Google Scholar] [CrossRef]
  51. Chi, H. TIMING-Mschart: A Computer Program for the Population Projection Based on Age-Stage, Two-Sex Life Table; National Chung Hsing University: Taichung, Taiwan, 2021. [Google Scholar]
  52. Asgari, F.; Moayeri, H.R.S.; Kavousi, A.; Enkegaard, A.; Chi, H. Demography and Mass Rearing of Amblyseius Swirskii (Acari: Phytoseiidae) Fed on Two Species of Stored-Product Mites and Their Mixture. J. Econ. Entomol. 2020, 113, 2604–2612. [Google Scholar] [CrossRef]
  53. Hafeez, M.; Jan, S.; Nawaz, M.; Ali, E.; Ali, B.; Qasim, M.; Fernández-Grandon, G.M.; Shahid, M.; Wang, M. Sub-Lethal Effects of Lufenuron Exposure on Spotted Bollworm Earias Vittella (Fab): Key Biological Traits and Detoxification Enzymes Activity. Environ. Sci. Pollut. Res. 2019, 26, 14300–14312. [Google Scholar] [CrossRef]
  54. Jaleel, W.; Saeed, S.; Saeed, Q.; Naqqash, M.N.; Sial, M.U.; Aine, Q.U.; Yanyuan, L.; Rui, Z.; He, Y.; Lu, L. Effects of Three Different Cultivars of Cruciferous Plants on the Age-Stage, Two-Sex Life Table Traits of Plutella Xylostella (L.) (Lepidoptera: Plutellidae). Entomol. Res. 2019, 49, 151–157. [Google Scholar] [CrossRef]
  55. Aljetlawi, A.A.; Sparrevik, E.; Leonardsson, K. Prey–Predator Size-Dependent Functional Response: Derivation and Rescaling to the Real World. J. Anim. Ecol. 2004, 73, 239–252. [Google Scholar] [CrossRef]
  56. Kalinoski, R.M.; DeLong, J.P. Beyond Body Mass: How Prey Traits Improve Predictions of Functional Response Parameters. Oecologia 2016, 180, 543–550. [Google Scholar] [CrossRef] [PubMed]
  57. Barbosa, L.R.; Santos, F.; Soliman, E.P.; Rodrigues, A.P.; Wilcken, C.F.; Campos, J.M.; Zanuncio, A.J.V.; Zanuncio, J.C. Biological Parameters, Life Table and Thermal Requirements of Thaumastocoris Peregrinus (Heteroptera: Thaumastocoridae) at Different Temperatures. Sci. Rep. 2019, 9, 10174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Ramos Aguila, L.C.; Hussain, M.; Huang, W.; Lei, L.; Bamisile, B.S.; Wang, F.; Chi, H.; Wang, L. Temperature-Dependent Demography and Population Projection of Tamarixia Radiata (Hymenoptera: Eulophidea) Reared on Diaphorina Citri (Hemiptera: Liviidae). J. Econ. Entomol. 2020, 113, 55–63. [Google Scholar] [CrossRef] [PubMed]
  59. Tazerouni, Z.; Talebi, A.A.; Fathipour, Y.; Soufbaf, M. Age-Specific Functional Response of Aphidius Matricariae and Praon Volucre (Hymenoptera: Braconidae) on Myzus Persicae (Hemiptera: Aphididae). Neotrop. Entomol. 2016, 45, 642–651. [Google Scholar] [CrossRef]
  60. Hoffmann, A.A.; Sørensen, J.G.; Loeschcke, V. Adaptation of Drosophila to Temperature Extremes: Bringing Together Quantitative and Molecular Approaches. J. Therm. Biol. 2003, 28, 175–216. [Google Scholar] [CrossRef]
  61. Broufas, G.D.; Pappas, M.L.; Koveos, D.S. Effect of Relative Humidity on Longevity, Ovarian Maturation, and Egg Production in the Olive Fruit Fly (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 2009, 102, 70–75. [Google Scholar] [CrossRef] [Green Version]
  62. Zhang, S.-C.; Zhu, F.; Zheng, X.-L.; Lei, C.-L.; Zhou, X.-M. Survival and Developmental Characteristics of the Predatory Bug Orius Similis (Hemiptera: Anthocoridae) Fed on Tetranychus Cinnabarinus (Acari: Tetranychidae) at Three Constant Temperatures. Eur. J. Entomol. 2013, 109, 503–508. [Google Scholar] [CrossRef] [Green Version]
  63. Kakimoto, K.; Urano, S.; Noda, T.; Matuo, K.; Sakamaki, Y.; Tsuda, K.; Kusigemati, K. Comparison of the Reproductive Potential of Three Orius Species, O. Strigicollis, O. Sauteri, and O. Minutus (Heteroptera: Anthocoridae), Using Eggs of the Mediterranean Flour Moth as a Food Source. Appl. Entomol. Zool. 2005, 40, 247–255. [Google Scholar] [CrossRef]
  64. Yosoff, S.F.; Mohamed, M.T.M.; Parvez, A.; Ahmad, S.H.; Ghazali, F.M.; Hassan, H. Production System and Harvesting Stage Influence on Nitrate Content and Quality of Butterhead Lettuce. Bragantia 2015, 74, 322–330. [Google Scholar] [CrossRef] [Green Version]
  65. Bonte, M.; Clercq, P. De Influence of Predator Density, Diet and Living Substrate on Developmental Fitness of Orius Laevigatus. J. Appl. Entomol. 2011, 135, 343–350. [Google Scholar] [CrossRef]
  66. Kessler, A.; Baldwin, I.T. Manduca Quinquemaculata’s Optimization of Intra-Plant Oviposition to Predation, Food Quality, and Thermal Constraints. Ecology 2002, 83, 2346–2354. [Google Scholar] [CrossRef]
  67. Notter-Hausmann, C.; Dorn, S. Relationship between Behavior and Physiology on an Invasive Pest Species: Oviposition Site Selection and Temperature-Dependent Development of the Oriental Fruit Moth (Lepidoptera: Tortricidae). Environ. Entomol. 2010, 39, 561–569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Saeed, S.; Jaleel, W.; Naqqash, M.N.; Saeed, Q.; Zaka, S.M.; Sarwar, Z.M.; Ishtiaq, M.; Qayyum, M.A.; Sial, M.U.; Batool, M.; et al. Fitness Parameters of Plutella Xylostella (L.) (Lepidoptera; Plutellidae) at Four Constant Temperatures by Using Age-Stage, Two-Sex Life Tables. Saudi J. Biol. Sci. 2019, 26, 1661–1667. [Google Scholar] [CrossRef]
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Figure 1. Experimental setup for the life table study of the two predatory mite species under laboratory conditions.
Figure 1. Experimental setup for the life table study of the two predatory mite species under laboratory conditions.
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Figure 2. Age-stage-specific survival rate (sxj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
Figure 2. Age-stage-specific survival rate (sxj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
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Figure 3. Age-specific survival rate (lx), female age-specific fecundity (fx5), age-specific fecundity (mx), and age-specific maternity (lxmx) of G. aculeifer and S. scimitus fed on T. putrescentiae.
Figure 3. Age-specific survival rate (lx), female age-specific fecundity (fx5), age-specific fecundity (mx), and age-specific maternity (lxmx) of G. aculeifer and S. scimitus fed on T. putrescentiae.
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Figure 4. Age-stage-specific life expectancy (exj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
Figure 4. Age-stage-specific life expectancy (exj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
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Figure 5. Age-stage-specific reproductive value (vxj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
Figure 5. Age-stage-specific reproductive value (vxj) of G. aculeifer and S. scimitus fed on T. putrescentiae.
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Figure 6. Population growth and stage structure of G. aculeifer and S. scimitus fed on T. putrescentiae.
Figure 6. Population growth and stage structure of G. aculeifer and S. scimitus fed on T. putrescentiae.
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Figure 7. Population projection of G. aculeifer and S. scimitus using life tables of the original cohort; the cohorts were constructed based on the 2.5% and 97.5% percentiles of finite rate of increase (λ) and net reproductive rate (R0).
Figure 7. Population projection of G. aculeifer and S. scimitus using life tables of the original cohort; the cohorts were constructed based on the 2.5% and 97.5% percentiles of finite rate of increase (λ) and net reproductive rate (R0).
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Table
Table 1. Development time for the different life stages, total preadult duration, adult longevity, adult preoviposition period (APOP), total preoviposition period (TPOP), reproductive days, and fecundity of G. aculeifer and S. scimitus fed on T. putrescentiae.
Table 1. Development time for the different life stages, total preadult duration, adult longevity, adult preoviposition period (APOP), total preoviposition period (TPOP), reproductive days, and fecundity of G. aculeifer and S. scimitus fed on T. putrescentiae.
Developmental Time (days)
Biological ParametersGaeolaelaps aculeiferStratiolaelaps scimitusp
NMean ± SENMean ± SE
Egg (d)413.71 ± 0.11 a362.89 ± 0.096 b<0.0001
Larva (d)411.05 ± 0.034 a361.11 ± 0.053 a0.2783
Protonymph (d)413.32 ± 0.101 a363.06 ± 0.112 a0.3577
Deutonymph (d)413.44 ± 0.093 a363.64 ± 0.15 a0.6078
Preadult (d)4111.51 ± 0.18 a3610.69 ± 0.25 b0.0064
Adult longevity (d)4166.24 ± 2.20 a3657.19 ± 2.61 b0.0072
Female adult 2680.31 ± 2.75 a2469.71 ± 3.08 b0.0165
Male adult 1573.33 ± 3.55 a1264.25 ± 4.78 a0.1242
Total longevity (d)4177.76 ± 2.21 a3667.89 ± 2.61 b0.0035
APOP (d)263.23 ± 0.19 a246.04 ± 0.47 b0.0035
TPOP (d)2614.88 ± 0.34 a2416.42 ± 0.60 b0.0285
Oviposition days (d)2624.50 ± 0.73 a2419.12 ± 1.29 b0.0288
Fecundity (offspring/individual)2674.88 ± 2.25 a2428.46 ± 2.00 b0.0285
Fecundity (eggs/day)263.06 ± 0.07 a241.49 ± 0.04 b<0.0001
Standard errors (SEs) were estimated using 100,000 bootstraps. Mean values followed by the same letters in rows are not significantly different between the two species as assessed using the paired bootstrap test at the 5% significance level.
Table
Table 2. Population parameter of G. aculeifer and S. scimitus fed on T. putrescentiae.
Table 2. Population parameter of G. aculeifer and S. scimitus fed on T. putrescentiae.
Population Parameters aBootstrap (Mean ± SE b,c)p
Gaeolaelaps aculeiferStratiolaelaps scimitus
r (d−1)0.1733 ± 0.0071 a0.1079 ± 0.0071 b<0.0001
λ (d−1)1.1893 ± 0.0084 a1.1139 ± 0.0068 b<0.0001
R0 (offspring/female)47.49 ± 5.80 a18.97 ± 2.59 b<0.0001
T (d)22.27 ± 0.44 a27.29 ± 0.83 b<0.0001
GRR (offspring/female)47.53 ± 5.81 a22.03 ± 3.12 b<0.0001
ar, intrinsic rate of increase; λ, finite rate of increase; R0, net reproductive rate; T, mean generation time (offspring/individual); GRR, gross reproduction rate. b Standard errors (SEs) were estimated using the bootstrap technique with 100,000 re-samplings. c Mean values followed by the same letters in rows are not significantly different between the two species as assessed using the paired bootstrap test at the 5% significance level.
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Park, J.; Mostafiz, M.M.; Hwang, H.-S.; Jung, D.-O.; Lee, K.-Y. Comparing the Life Table and Population Projection of Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae) Based on the Age-Stage, Two-Sex Life Table Theory. Agronomy 2021, 11, 1062. https://doi.org/10.3390/agronomy11061062

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Park J, Mostafiz MM, Hwang H-S, Jung D-O, Lee K-Y. Comparing the Life Table and Population Projection of Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae) Based on the Age-Stage, Two-Sex Life Table Theory. Agronomy. 2021; 11(6):1062. https://doi.org/10.3390/agronomy11061062

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Park, Jihye, Md Munir Mostafiz, Hwal-Su Hwang, Duck-Oung Jung, and Kyeong-Yeoll Lee. 2021. "Comparing the Life Table and Population Projection of Gaeolaelaps aculeifer and Stratiolaelaps scimitus (Acari: Laelapidae) Based on the Age-Stage, Two-Sex Life Table Theory" Agronomy 11, no. 6: 1062. https://doi.org/10.3390/agronomy11061062

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