Life table of Orius insidiosus (Hemiptera: Anthocoridae) feeding on Sitotroga cerealella (Lepidoptera: Gelechiidae) eggs

Tabla de vida de Orius insidiosus (Hemiptera: Anthocoridae) alimentado con huevos de Sitotroga cerealella (Leideoptera: Gelechiidae)

Jhon Alexander Avellaneda Nieto¹, Fernando Cantor Rincon¹, Daniel Rodríguez Caicedo¹

¹ Facultad de Ciencias Básicas y Aplicadas - Universidad Militar Nueva Granada. Cra. 11 No. 101- 80, Bogotá, Colombia. <control.biologico@unimilitar.edu.co>

Received: Received: June 2, 2015; Accepted: October 16, 2015

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Key words: Biological control, Pirate bugs, Stock colony, Sabana de Bogotá.

RESUMEN
To use a natural enemy to control an insect pest, it is important to determine the biological parameters of the native populations of the predator. The goal of this study was determinate the biological parameters of O. insidiosus fed on Sitotroga cerealella eggs. A batch of 225 O. insidiosus eggs were laid into bean pods. The bean pods were kept in glass jars, and the eggs and first instar nymphs were counted daily. All nymphs were extracted and individualized in Petri dishes. The presence/absence of exuvie was observed daily as a way to assess the emergence of adults from the nymphal stage. Seventeen adult couples were placed into Petri dishes with a segment of bean pod. The bean pod segments were extracted and replaced daily, counting the number of eggs present on the pods. The life cycle, survival percentage, sex ratio, male/female longevity, pre ovoposition, ovoposition and post ovoposition periods were determined. Finally, fertility life table parameters were estimated. The nymphal development time was 12.0 ± 0.22 days, with 80.47% ± 3.23 survival, while the total development time was 15.0 ± 0.23 days, with 66.67% ± 1.90 survival. Of the total adults that emerged, 30.95% ± 2.38 were females. The female sex ratio was 0.75, and the oviposition period was 0.86 ± 9.21 days with a total fertility of 60.29 ± 7.39 eggs. The data estimated from the fertility life table were: Ro: 28.26, rm: 0.14, T: 24.26, ?: 1.13 and DT: 5.01.

Palabras claves: Control biológico, Antocóridos, Pie de cría, Sabana de Bogotá.

The western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) is one of the most important agricultural pests worldwide (Kirk, 2003; Manners et al., 2013) due to its broad geographic range and high reproductive potential, allowing it to quickly produce large populations that can easily disperse over different crops (Castresana et al., 2008) in open field and greenhouse settings (Lewis, 1997).

The damage produced by this pest causes significant economic losses, depending on its level of attack, the control method employed and the suitability of such control method (Lewis, 1997). Different methods have been proposed for the control of F. occidentalis. The chemical method is widely used given its immediate effect on the pest population and its market availability. However, insecticides often do not generate the expected control because adults and immature stages have cryptic habits and can therefore feed and remain sheltered in the foliage, flower buds, developing fruits, and flower buds, which represent physical barriers against pesticides (Hansen et al., 2003; Helyer and Brobyn, 2008).

On the other hand, biological control is a promising alternative to pesticides for the future management of F. occidentalis (Fransen and Tolsma, 1992), biological control is a pest control method that is friendly to the environment, harmless to human health and an excellent alternative to pesticide use in integrated pest management (IPM) programs (Rojas and Perea, 2003). In addition to pathogens and parasitoids, natural predators are currently the most used resource for the regulation of populations method for the control of thrips F. occidentalis (Ramakers et al., 1989).

The need to identify potential predators to be used as bioinputs for the control of thrips F. occidentalis has led to the discovery of different biological control agents, including predatory mites from the genus Amblyseius (Berlese) (Acari: Phytoseiidae) and predatory minute pirate bugs from the genus Orius (Wolff, 1811) (Hemiptera: Anthocoridae). Several species belonging to the Anthocoridae family have proven highly effective as biological control agents used against various greenhouse and field crop pests, such as F. occidentalis (Funderburk et al., 2000).

In order to ensure that the predator species can adapt to the environmental zones where it will be used as a control agent, studies assessing the biological parameters of Orius insidiosus must be performed on natural populations that can be found spontaneously in grasslands or hedges located near areas where they could be released for the control of F. occidentalis.

The biological parameters of the predator are affected by the diet supplied during rearing, and several diets have been evaluated for raising different species of anthocorids. Kiman and Yeargan (1985) showed that O. insidiosus can survive on diets of pollen, vegetable juice and water. However, other studies have shown that anthocorids require animal prey to ensure effective reproduction and fertility (Zambrano, 2009). For this reason, many studies have evaluated the effect of diets based on the eggs, larvae and adults of different insects and have shown that lepidopteran eggs optimize the biological parameters of Orius sp. (Mendes et al., 2002; Saini et al., 2003; Zambrano, 2009; Sobhy et al., 2010).

Under this framework, the objective of this study was to set up a stock colony of O. insidiosus fed on Sitotroga cereallela (Olivier) (Lepidoptera: Gelechiidae) eggs and to use this stock colony to determine the survival curve, development time for different stages, sex ratio, longevity and fertility parameters of this species. These parameters could be important to optimize the rearing of O. insidiosus, this in order to use these parameters for the establishment a productive rearing for support possible integrated pest management.

MATERIALS AND METHODS

Experiments were conducted in a climate controlled room in the Biological Control Laboratory of the Militar Nueva Granada University (BCL UMNG) at 26 ± 1 °C, 65 ± 10% RH, and with a 12L: 12D photoperiod.

The rearing of O. insidiosus ]]> The O. insidiosus individuals used to establish stock colonies were collected on Red Clover (Trifolium pratense) in three areas of the Bogotá Savanna, Colombia: Cajicá (04°56'28.0"N and 74°00'34.9"W), Chía (04°51'52.39"N and 74°02'24.60"W), and Suba (04°44'53.3"N and 74°05'56.5"W). Each area was visited four times during a one month period. During each visit, the anthocorids were collected continuously for 1 hour by taking flower heads of T. pratense and shaking them rapidly on a plastic box about 3 times. The collected specimens were then aspirated.

The adults collected were transported in 50 mL plastic bottles to BCL UMNG, where they were kept in 500 cm3 cylindrical glass vials (7 cm diameter x 13 cm height) with 5 cm holes in the lids for ventilation. The vials were covered with a Swiss veil to prevent any individuals from escaping.

A piece of blotting paper was placed on the inner surface of each vial and was moistened three times per week to maintain the ambient moisture levels. Bean pods (Phaseolus vulgaris L. Var. Cerinza) were used as an oviposition substrate and were obtained directly from crops present in the UMNG greenhouses. Four pods were placed in each vial, and these were changed weekly. Anthocorids were fed three times per week ad libitum with Sitotroga cereallela eggs obtained from a breeding colony established at the BCL UMNG.

Embryonic development time and survival of O. insidiosus
A cohort of O. insidiosus eggs was obtained from the stock colony previously established. To achieve this, a population of nine females and 3 males was placed into a 500 cm³ cylindrical glass vial (7 cm diameter x 13 cm height), with bean pods (P. vulgaris) as the oviposition substrate. For this test, 13 replicates were employed. After 24 hours, the adults were removed from the vials, and the eggs were counted for each of the replicates.

Units of 500 cm3 cylindrical glass vials (7 cm diameter x 13 cm height) containing a group of P. vulgaris pods and 30 O. insidiosus eggs were assembled. Seven replicates were used for determining the time of development and the embryonic survival. The number of eggs and first instar nymphs present in each of the replicates was counted every 24 hours. This count was conducted until all nymphs had hatched and/or the individuals in the egg stage died. Nymphs were found daily, extracted from the experimental units and used for testing their development time and survival.

Development time, survival and sex ratio of O. insidiosus
The first instar nymphs obtained from the previous test were housed individually to avoid cannibalism and/or mutual interference, which have been reported for the genus Orius in the absence of food and/or when individuals are maintained at high densities (Meiracker, 1999). First instar nymphs were individually placed in 60 mL Petri dishes (5 cm diameter x 1.5 cm height) containing a blotting paper disk (5 cm diameter), which was moistened daily. Each Petri dish was covered with Stretch Wrap to prevent the nymphs from escaping. The nymphs were fed ad libitum with S. cerealella eggs three times per week.

The development time and apparent survival of the nymphs (given as the percentage of surviving individuals among individuals entering the developmental stage, as suggested by Sothwood and Henderson, 2000 were determined from daily observation. Experimental units were assessed with a stereoscope daily to determine the presence/absence of exuvie as an indicator of changes in the development stage. Also, the mortality and time span of each nymphal stage of development was assessed to measure the adult eclosion. Upon eclosion, adults were sexed by an observation of the abdominal region under the stereoscope and the pre imaging mortality (expressed as % of adults emerged), sex ratio (?/?) and percentage of females (?%) were determined.

Fecundity life table and longevity of O. insidiosus ]]> Petri dishes of 60 mL (5 cm diameter x 1.5 cm height) were used as the experimental units. A piece of cotton (1 cm³) was placed in each petri dish and moistened daily, and a P. vulgaris pod section (4 cm long) was used as the oviposition substrate. Sitotroga cerealella eggs were provided as food ad libitum every third day.

Virgin females and males no more than 24 hours old were paired. A total of 17 couples were placed individually in an experimental unit. Bean pod sections were replaced daily. Males were replaced when they were found dead.

Bean pods from each experimental unit were examined daily under a stereoscope to count the eggs laid. The pre oviposition period (age before the first oviposition), the oviposition period (the time elapsed from the first to the last egg oviposition), the post oviposition period (the time elapsed from the last egg oviposition to death), the total fecundity (the total number of eggs laid over the predator's lifetime), the daily fecundity (determined by dividing the total number of ovipositions by the oviposition period in days) and the longevity (the time elapsed from the first instar to death, or to adult eclosion) were registered for both males and females.

Calculations of life table parameters
Previously determined data on some biological parameters of O. insidiosus (longevity and fecundity) were used for the life table analysis, as described in Southwood y Henderson (2000). These parameters included age (x), age specific survival rate (lx), age specific fecundity (mx), total number of females born at a given age x (lx.mx), net reproductive rate (Ro), mean generation time (T), intrinsic rate of increase (rm), finite rate of increase (?), and doubling time (DT).

Population growth parameters (Ro, T, rm, ?, and DT) were calculated using the equations proposed by Southwood (1978):

RESULTS AND DISCUSSION

The embryonic development time of O. insidiosus lasted an average of 5.0 ± 0.22 days (Table 1); this value was about a day higher than the embryonic development time obtained by other authors such as Tommasini et al. (2004) who obtained an embryonic development time of 4.02 ± 0.02 days in the same temperature and relative humidity. These results were similar to those obtained by Santana (2009), who measured a period of embryonic development of 4.0 ± 0.05 days at 24 °C; in contrast, Meiracker (1999) measured an embryonic development time of 4.6 days at 25 °C. Differences in the measured embryonic development time between this and other studies may be due to genetic variability in the populations of predators used in each study, the rearing background from which the adults were extracted, the environmental conditions used in the study and the nutritional value of the food source, as suggested by Iranipour et al. (2009).

Importantly, the nutritional quality and temperature are likely the two factors with the greatest influence on the adults employed for oviposition. Our adults were fed with S. cerealella eggs, unlike the adults used in the tests performed by Meiracker (1999); Tommasini et al. (2004); and Santana (2009), who all used Ephestia kuehniella eggs instead (Lepidoptera: Cambridae) (Zeller, 1879). According to Pratissoli and Parra (2000), E. kuehniella eggs are more nutritious than S. cerealella eggs, which could explain why the embryonic development time obtained in this study was longer than that obtained by the other authors, as the temperatures used in this study were similar to those used in the other cited studies.

The lowest survival rate among the immature stages of O. insidiosus were observed in the egg stage, with a survival of 88.33 ± 3.09% (Table 2). When evaluating the survival rate of the egg stage of O. insidiosus, some individuals were found to be dehydrated during the hatching phase. This may be because the egg stage and the first instar are more susceptible to dehydration, given their small size (Schmidt et al., 1998). Indeed, having a smaller body size means having a greater surface area/volume ratio and, thus, a higher probability of surface water loss and subsequent dehydration.

Based on the above and considering that the development time obtained in this study for the egg stage was longer than for the other immature stages, we concluded that individuals in the egg stage had a lower chance of survival because they were more vulnerable to temperature changes and more likely to dehydrate. Richards and Schmidt (1996), who observed the highest hatching of O. insidiosus (100% RH), recommend mass rearing this predator in high humidity conditions to prevent egg dehydration.

Throughout the development of the nymphal stages of O. insidiosus, an increase in the time of each developmental stage were observed as individuals approached adulthood, resulting in values of 1.47 ± 0.10 days for the first instar stage to 2.58 ± 0.13 days for the fifth instar stage. The development time of the last nymphal stage was therefore the longest (Table 1).These results are consistent with the results obtained by Tommasini et al. (2004), who reported stage times of 2.0 ± 0.03 days for first instar and 3.6 ± 0.04 days for fifth instar, and by Brito et al. (2009), who reported stage times of 2.0 ± 0.05 days for first instar and 4.9 ± 0.12 days for fifth instar.

Consistently with Butler and O'Neil (2007), Brito et al. (2009), Santana (2009) and Tomassini et al. (2004), in the present study we found that the development time of the fifth instar is the longest. However, the time reported by these authors for this instar stage was longer than the time observed in our work. For instance, Butler and O'Neil (2007) obtained a development time for the fifth instar of 5.8 ± 0.34 days for nymphs fed with E. kuehniella eggs at 22 °C, 65 RH and with a 18L:6D photoperiod. The closest result to that obtained in this study was reported by Tommasini et al. (2004), who recorded a development of 3.6 ± 0.10 days for the fifth instar.

The total nymphal developmental time of O. insidiosus (from first instar to adult) was 12.0 ± 0.22 days (Table 1), which differs from the results of other authors, who have reported both higher and lower values, depending on the diet and the temperature used. For example, Santana (2009) reported a time of 35.5 ± 0.62 days and 9.7 ± 0.62 days at 16 °C and 28 °C, respectively, while Brito et al. (2009) reported values of 14.5 ± 0.13 days, 14.9 ± 0.72 days and 15.6 ± 0.10 days for the nymphal development time, when the nymphs were fed E. kuehniella eggs, Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) eggs and P. xylostella caterpillars, respectively.

The above results support the findings of Mendes et al. (2005), who reported that diet and temperature are the main factors influencing the nymphal development of O. insidiosus. Thus, these critical factors could modify the predator's behavior in field conditions. Therefore, it is important to assess whether this predator, when reared on Sitotroga cerealella, still prefers consuming thrips F. occidentalis over other prey in controlled and field conditions.

The total immature development time of O. insidiosus (from egg to adult) was 15.0 ± 0.23 days (Table 1), similar to that observed by Tommasini et al. (2004), who obtained a total time of 15.0 ± 0.10 days for O. insidiosus fed with E. kuehniella eggs and a time of 14.1 ± 0.07 days for O. insidiosus fed with F. occidentalis under the same temperature and relative humidity conditions used in the present study. In contrast, Brito et al. (2009) reported a total immature development time of 21.0 ± 0.13 days for O. insidiosus fed with A. kuehniella eggs under constant conditions (25 ± 1 °C, 70 ± 10% RH and a 12L:12D photoperiod). The values obtained by these authors are higher than those observed in this study, even though their temperature, relative humidity and photoperiod conditions were very similar.

Mendes et al. (2005) reported a survival rate of 68.01 ± 5.5 % for the total nymphal period, which was lower than that found in our study (80.47 ± 3.23%, Table 2). However, the value obtained in our study was very similar to that reported by Brito et al. (2009) (80.0 ± 0.80 %).

The total immature survival rate of O. insidiosus observed in this study (66.67 ± 1.90%, Table 2), was also very similar to that obtained by Brito et al. (2009), who evaluated the nymphal and egg survival rates in separate trials and reported survivals of 80.0 ± 0.80% and 80.4 ± 0.72%, respectively, for a total immature survival rate of 60.4%.

The survivorship curve of O. insidiosus obtained in this study showed that survival fell after the fourth day. Slightly over 50% of the individuals survived to day 25 after the first oviposition (the eighth day after adult emergence), and from this day onward the average survival rate steadily declined to 0% at day 42 (Figure 1).

Of the three types of survival curves used in the literature to describe different species, O. insidiosus development most closely follows a type II curve (Figure 1), meaning that a constant number of individuals died per unit time, such that a given individual has a constant probability of death over the course of its lifetime (Páramo et al., 1986).

Type II curves were obtained by Tommasini et al. (2004) for individuals fed with E. kuehniella eggs and F. occidentalis adults, but this author found that only 50% of individuals in the adult stage survived until day 48 after emergence. Furthermore, the survival rate was 0% at day 68, which differs from our results.

From the 30 eggs (n = 7) of O. insidiosus with which this test began, 16.29 ± 1.06 individuals (54.29%) reached adulthood. Of these, 30.95% were females and 23.33% were males, corresponding to a sex ratio (% of females) of 0.75 (Table 3). These values were lower than the results reported by other authors. Tommasini et al. (2004) observed a sex ratio of 1.08, while Argolo et al. (2002); and Santana (2009) observed a sex ratio of 0.5 in laboratory conditions. These differences were probably caused by differential mortality or a differential hatching rate in Shapiro et al. (2009).

Of the 17 couples used in the fecundity and longevity test, three did not show oviposition. Only females that oviposited were included in the results of the fecundity, daily fecundity, pre, post and oviposition periods. All females were included in the longevity assessment.

The pre oviposition period of O. insidiosus fed with eggs of S. cerealella was 3.07 ± 0.25 days (Table 4). This result obtained in this work are consistent with the result reported by Saini et al. (2003), who found a pre oviposition period of three days at both 25 °C and 30 °C for females fed the same diet used in this study. For females fed with E. kuheniella eggs, Brito et al. (2009) reported a pre oviposition period of 4.9 days, which is nearly two days longer than that observed in this study. Furthermore, Argolo et al. (2004) used the same diet and recorded a pre oviposition period of 3.3 days, while Meiracker (1994) recorded a pre oviposition period of 7.7 days for females raised under a 10L:14D photoperiod, suggesting that the pre oviposition period is affected by the diet photoperiod and temperature, as mentioned by Santana (2009).

The oviposition period was 9.21 ± 1.33 days (Table 4). This time was 3.6 and 4.8 times shorter than the periods reported by Santana (2009) and Mendes (2002), respectively, who instead used E. kuehniella eggs as a food source. These results may indicate that the food type greatly influences oviposition period. However, Brito et al. (2009) that also used E. kuehniella eggs but obtained an oviposition period of 2.3 ± 0.22 days, which was four times shorter than what we observed, suggesting that other, as yet unidentified factors, might also influence the oviposition period of O. insidiosus.

The daily fecundity of O. insidiosus obtained in the present study was 6.92 eggs/day (Table 4), was higher than that reported by Mendes (2002) and Santana (2009), 3.47 and 4.10 eggs/day, respectively. The marked differences between their and our measured fecundity may be related to female longevity, which was markedly lower in our study (12.47 days) than in the work of Santana and Mendes (40.5 and 56.25 days, respectively).

Based on the data obtained from the life table, we plotted the fertility curve (mx), which was unimodal but irregular. As shown, the fecundity reached a peak production of 8.24 eggs/(female/day) on the fourth day after adult emergence. A second peak of 6.57 eggs occurred eight days after adult emergence. Subsequently, the number of eggs dropped until oviposition stopped (Figure 1). This fertility curve was very similar to that obtained by Saini et al. (2003).

Female longevity in this study was 12.47 days, which was approximately two days longer than the value recorded for males (Table 4). Saini et al. (2003) reported longevities of 13.5 to 20.1 days for females of O. insidiosus fed with S. cerealella eggs, which are closer to the values obtained in our study. Such longevity values could also affect the total fertility reported by the same author (between 39.4 and 86.5 eggs/female at 25 °C with a different diet density), which were very similar to those obtained in this study (60.29 ± 7.39 eggs/female, Table 4). Moreover, their values were lower than those obtained by Mendes (2002); Tommasini et al. (2004) and Santana (2009), which were 195.3 ± 22.77, 144.3 ± 76.8 and 145.5 ± 15.37 eggs/female, respectively.

The differences between the male and female longevity observed in this study may be due to O. insidiosus males being more mobile in the rearing condition than the females (Shapiro et al. 2009). It is likely that their search for females for copulation requires greater energy expenditure, leading to a reduction in male longevity.

The fecundity life table parameters (Ro, T, rm, TD, and ?) of O. insidiosus obtained in this study are a valuable resource for evaluating the biological performance of the insects and the effects of both biotic and abiotic factors on their development (Vacari et al., 2007).

The net reproductive rate (Ro) obtained in this study (28.62) was higher than the net reproductive rates obtained by Brito et al. (2009), who reported rates of 2.40 and 6.61 for females fed with E. kuehniella and P. xylostella eggs, respectively. However, in a similar study, Tommasini et al. (2004) obtained values closer to those found in this study (17.9 and 30.1) when they fed the females with F. occidentalis adults and E. kuehniella eggs, respectively.

Bluter and O'Neil (2007) reported an intrinsic rate of increase (rm) of 0.094 for females fed with a mixed prey diet (1 individual of N. variabilis and 3 individuals of A. glycines), while Tommasini et al. (2004) instead reported a value of 0.101 for females fed with E. kuehniella eggs. These values of rm were different from those obtained in our study (0.14). This difference may be explained by the intrinsic rate of increase being strongly associated with the start time of the reproductive period. This means that individuals who begin to reproduce at an early age have a higher intrinsic rate of increase than those who begin to reproduce at a later age (Batista, 2006). This is consistent with differences in the reproductive period start times reported by Bluter and O'Neil (2007), Tommasini et al. (2004) and the values obtained in this study, which were 7.7, 3.7 and 3.07 days, respectively.

The doubling time (TD) required for the O. insidiosus population (TD) in this study was 5.01 days, which is nearly two days less than the doubling time reported by Brito et al. (2009) for females fed with E. kuehniella eggs. However, it was nearly two days longer than for females fed with P. xylostella, as reported by the same author.

Finally, the finite rate of increase (?) for O. insidiosus observed in this study was 1.13. Other studies have reported lower values for O. insidiosus females reared on different diets. For instance, Bortoli et al. (2008) reported a value of 1.09 using Aphis gossypii (Glover) (Hemiptera: Aphididae) adults on cotton cultivars as food, while the finite rates of increase observed by Brito et al. (2009) were 1.03 and 1.07 for females fed with E. kuehniella and P. xylostella eggs, respectively.

CONCLUSIONS

Based on the life table and life cycle parameters obtained in this work, we conclude that S. cerealella eggs are a viable alternative diet for rearing O. insidiosus under controlled conditions, although further studies are necessary to determine the factors other than diet that could affect longevity. A higher longevity would allow for an increase in the oviposition period and, therefore, the fecundity of individuals. It is also necessary to evaluate the functional response of O. insidiosus on thrips F. occidentalis to determine whether natural populations of anthocorids are a promising candidate for the control of thrips. This predator might be implemented in an improved integrated pest management program in the crops of the Bogotá Savanna.

ACKNOWLEDGMENTS

The authors are grateful to the Militar Nueva Granada University for providing financial support for this work. "Product derived of project CIAS 1177, funded by the Vice-rectory for Research of the Militar Nueva Granada University".

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