AE  Vol.4 No.2 , April 2016
Food Preference of Pecky Rice Bugs Is Influenced by Experience
ABSTRACT
This study investigated whether prior experience influences the plant food preference of Trigonotylus caelestialium and Stenotus rubrovittatus which cause pecky rice grain, by using rice plants and 2 poaceous weeds. In a choice experiment between Digitaria ciliaris and the rice plants, both T. caelestialium and S. rubrovittatus adults that were reared on D. ciliaris plants showed significant initial preference for D. ciliaris over rice. In a choice experiment between Echinochloa crus-galli var. aristata and rice plants, T. caelestialium adults reared on E. crus-galli var. aristata strongly preferred E. crus-galli var. aristata over rice throughout the experiment. However, at and after 24 h, T. caelestialium adults reared on rice showed no food preference, although T. caelestialium initially preferred E. crus-galli var. aristata. In contrast, S. rubrovittatus adults reared on rice showed no preference between E. crus-galli var. aristata and rice. However, S. rubrovittatus reared on E. crus-galli var. aristata initially preferred E. crus-galli var. aristata to rice, with this preference waning with time. The same results were obtained for both sexes. Although the effect of experience differed with food source and the species of mirid bug, prior experience initially had a noticeable effect, which disappeared with time (1 d).

Received 14 March 2016; accepted 15 April 2016; published 19 April 2016

1. Introduction

The rice leaf bug, Trigonotylus caelestialium (Kirkaldy), and the sorghum plant bug, Stenotus rubrovittatus (Matsumura) are major rice pests in Japan. Although the nymphs of these bugs grow well on hulled rice, rice plant leaves are not suitable food for their growth. Thus, adults are assumed to cause damage to rice grains when they move to rice plants at the heading stage after growing on other poaceous plants, along with nymphs that emerge from eggs deposited by the adults on rice. Therefore, it is important to identify host plants that are suitable for nymph growth. Field sampling and observations have identified Italian ryegrass, Lolium multiflorum; annual bluegrass, Poa annua; and southern crabgrass, Digitaria ciliaris as important food sources for rice bugs [5] - [7] . Laboratory tests have shown that nymphs grow well on P. annua, Alopecurus aequalis, Poasphondylodes, Hordeum murinum, Dactylis glomerata, Agrostis clavata subsp. matsumurae, L. multiflorum [8] , Poa pratensis, and Digitaria violascens [9] . These plants may facilitate the development of rice bugs. Alternatively, the relative preference of rice bugs between host plants and rice plants may contribute to the occurrence of pecky rice, because rice grain damage is caused by rice bugs that move from poaceous weeds to rice plants.

It has been reported that rice leaf bugs and sorghum plant bugs are attracted to plants at specific developmental stages [10] [11] . Furthermore, rice leaf bugs prefer flowering poaceous weeds over rice plants before heading, whereas they show equal preference for flowering poaceous weeds and rice plants at the heading stage [12] . Therefore, the increase in bug populations in rice paddies after heading [5] [6] [13] is attributable to an increase in their relative preference for rice plants over other host plants. Differences in the relative preference may affect bug movement between plants. Thus, in addition to the increased effects of poaceous weeds, the relative difference in bug preference between weeds and rice plants must be considered when evaluating how plants affect the occurrence of pecky rice. Moreover, if rice bugs develop a preference for rice plants after experiencing poaceous weeds, these weeds may have a pronounced effect on the incidence of pecky rice.

To study whether bug development on poaceous weeds influences their preference for rice plants, the relative preference between poaceous weeds and rice plants was investigated for T. caelestialium and S. rubrovittatus adults that had had prior experience on different plants. In this study, Digitaria ciliaris and Echinochloa crus- galli var. aristata were used as poaceous weeds because the ears of these plants emerge during the same season as those of rice plants, and because rice bugs grow relatively better on these plants than on other poaceous weeds that are present during the season [8] .

2. Materials and Methods

2.1. Insects

Trigonotylus caelestialium and Stenotus rubrovittatus were collected from fields at the Hokuriku Research Center, National Agricultural Research Center, Niigata Prefecture, Japan. These insects had been reared on young wheat seedlings under laboratory conditions (16:8 L:D photoperiod, 25˚C) for several years as described previously [14] - [16] .

2.2. Plants

Digitaria ciliaris and Echinochloa crus-galli var. aristata that were growing wild, and rice, Oryza sativa, that was cultivated in the paddy fields, were collected from the fields at the Hokuriku Research Center. The flowering stages of these plants were used for tests.

2.3. Experience Treatment

Within 24 h of emergence, 50 - 150 T. caelestialium or S. rubrovittatus adults were released in a plastic rearing cage (34 × 25 × 34 cm). Digitaria ciliaris, E. crus-galli var. aristata, and rice with flowering ears were placed in conical flasks (100 ml) filled with water. Each plant was made available to the adults for 4 d. The plants were renewed daily or every other day. This treatment was conducted under laboratory conditions (16:8 L:D photoperiod, 25˚C).

2.4. Choice Preference Test

One ear each of D. ciliaris, E. crus-galli var. aristata, and rice was placed in sample tubes filled with water. Two tubes with D. ciliaris and rice or E. crus-galli var. aristata and rice were placed diagonally at the corner of a plastic rearing cage (34 × 25 × 34 cm). Ten adults reared on these plants as described above were released in a plastic cup (top diameter: 8 cm, bottom diameter: 6 cm, height: 4 cm). The plastic cup was placed at the center of the plastic rearing cage and then the cap was removed to allow the adults to disperse. Adults reared on D. ciliaris were released in D. ciliaris vs. rice cages. Those on E. crus-galli var. aristata were released in E. crus- galli var. aristata vs. rice cages. Those on rice were released in D. ciliaris vs. rice cages or E. crus-galli var. aristata vs. rice cages. The number of adults on the plants was counted at 3, 6, 24, 27, and 30 h after starting the test. The test was conducted separately for males and females to prevent interaction between the sexes from influencing food preference. Twelve cages (i.e., 120 individuals) were used for each test, except for T. caelestialium males reared on E. crus-galli var. aristata (7 cages). These tests were conducted under rearing conditions (16:8 L:D photoperiod, 25˚C).

2.5. Statistical Analysis

The numbers of adults on rice plants and other poaceous plants were compared at each time point using binomial test. The ratios of the adults present on the plant species on which they had been reared versus those present on the plant species on which they had not been reared were compared between rice and each poaceous species at each time point using Fisher’s exact test. For example, at 3 h, the total number of T. caelestialium females reared on D. ciliaris that were present on D. ciliaris and rice was 64 and 25 individuals, respectively (Figure 1(a)). At the same time period, the total number of T. caelestialium females reared on rice that were present on D. ciliaris and rice was 44 and 41 individuals, respectively (Figure 1(b)). These two ratios (64/25 and 44/41) were then compared statistically by Fisher’s exact test. If these ratios were significantly different, prior food experience probably influenced bug preference.

Figure 1. Proportion of adult rice bug females on Digitaria ciliaris versus those on rice plants. Choice preference tests between D. ciliaris and rice were conducted with a: Trigonotylus caelestialium reared on D. ciliaris, b: T. caelestialium reared on rice, c: Stenotus rubrovittatus reared on D. ciliaris, and d: S. rubrovittatus reared on rice. The adults were counted at 3, 6, 24, 27, and 30 h. The numbers in parentheses represent the number of adults on plants. : P values comparing the number of adults on D. ciliaris and that on rice at each time point using binomial test. : P values comparing the proportion of adults present on D. ciliaris and rice (i.e., the plants used for rearing) at the same time points using Fisher’s exact test. Asterisk (*) represents p < 0.05.

3. Results

3.1. Choice Preference Test between Digitaria ciliaris and Rice

3.1.1. Trigonotylus caelestialium

After rearing of females on D. ciliaris, a significantly higher number of females was found on D. ciliaris than on rice at 3, 6, 24, and 27 h (number of individuals on D. ciliaris/rice = 64/25, 77/20, 64/29, and 54/34 respectively) (binomial test, p < 0.05; Figure 1(a)); however, after 30 h, there was no significant difference in the number of females on D. ciliaris and rice (number of individuals on D. ciliaris/rice = 47/34) (binomial test, p > 0.05; Figure 1(a)). In contrast, after rearing of females on rice, the number of females present on rice was not significantly different between D. ciliaris and rice (number of individuals on D. ciliaris/rice at 3, 6, 24, 27, and 30 h = 44/41, 46/52, 42/46, 46/47, and 48/40 respectively) (binomial test, p > 0.05; Figure 1(b)). The ratio of females present on the two tested plants used for rearing (D. ciliaris and rice) was significantly different at 3, 6, and 24 h (Fisher’s exact test, p < 0.05; Figure 1(a) and Figure 1(b)), whereas no significant difference was observed at 27 and 30 h (Fisher’s exact test, p > 0.05; Figure 1(a) and Figure 1(b)).

After rearing of males on D. ciliaris, a significantly higher number of adult males was present on D. ciliaris than on rice at 3, 6, and 27 h (number of individuals on D. ciliaris/rice = 46/27, 64/15, and 42/22 respectively) (binomial test, p < 0.05; Figure 2(a)), with no significant difference in male ratios at all other time points (number of individuals on D. ciliaris/rice at 24 and 30 h = 35/27 and 38/25 respectively) (binomial test, p > 0.05; Figure 2(a)). However, the number of males reared on rice was not significantly different between D. ciliaris and rice at all of the time points (number of individuals on D. ciliaris/rice at 3, 6, 24, 27, and 30 h = 39/37, 34/39, 24/26, 28/25, and 29/27 respectively) (binomial test, p > 0.05; Figure 2(b)). The ratio of males present on the two tested plants used for rearing (D. ciliaris and rice) was significantly different at 6 h (Fisher’s exact test, p < 0.05; Figure 2(a) and Figure 2(b)), but not at any of the other time points (Fisher’s exact test, p> 0.05; Figure 2(a) and Figure 2(b)).

Figure 2. Proportion of adult rice bug males on Digitaria ciliaris versus those on rice plants. Choice preference tests between D. ciliaris and rice were conducted with (a): Trigonotylus caelestialium reared on D. ciliaris; (b): T. caelestialium reared on rice; (c): Stenotus rubrovittatus reared on D. ciliaris, and (d): S. rubrovittatus reared on rice. The adults were counted at 3, 6, 24, 27, and 30 h. The numbers in parentheses represent the number of adults on plants. : P values comparing the number of adults on D. ciliaris and that on rice at each time point using binomial test. : P values comparing the proportion of adults present on D. ciliaris and rice (i.e., the plants used for rearing) at the same time points using Fisher’s exact test. Asterisk (*) represents p < 0.05.

3.1.2. Stenotus rubrovittatus

After rearing of females on D. ciliaris, a significantly higher number of females was present on D. ciliaris versus rice at all of the time points (number of individuals on D. ciliaris/rice at 3, 6, 24, 27, and 30 h = 54/34, 66/33, 81/34, 86/27, and 80/29 respectively) (binomial test, p < 0.05; Figure 1(c)). After rearing of females on rice, there was no significant difference in the number of adult females on rice and D. ciliaris at 3 and 6 h (number of individuals on D. ciliaris/rice = 35/44 and 48/49 respectively) (binomial test, p > 0.05; Figure 1(d)); however, a significantly higher number of females was present on D. ciliaris than on rice at 24 h and later (number of individuals on D. ciliaris/rice at 24, 27, and 30 h = 70/43, 74/42, and 77/36 respectively) (binomial test, p < 0.05; Figure 1(d). The ratio of females present on the two tested plants used for rearing (D. ciliaris and rice) was significantly different at 3, 6, and 27 h (Fisher’s exact test, p < 0.05; Figure 1(c) and Figure 1(d)), but not at 24 and 30 h (Fisher’s exact test, p > 0.05; Figure 1(c) and Figure 1(d)).

After rearing of males on D. ciliaris, a significantly higher number of males was present on D. ciliaris than on rice at all of the time points (number of individuals on D. ciliaris/rice at 3, 6, 24, 27, and 30 h = 67/25, 74/20, 54/15, 72/12, and 70/16 respectively) (binomial test, p < 0.05; Figure 2(c)). After rearing of males on rice, no significant difference in the number of males was detected between D. ciliaris and rice at 3 h (number of individuals on D. ciliaris/rice = 50/38) (binomial test, p > 0.05; Figure 2(d)); however, a significantly higher number of males was present on D. ciliaris at 6 h and after (number of individuals on D. ciliaris/rice at 6, 24, 27, and 30 h = 61/34, 50/25, 56/33, and 64/28 respectively) (binomial test, p < 0.05; Figure 2(d)). The ratio of males present on the two plants used for rearing (D. ciliaris and rice) was significantly different at 3, 6, and 27 h (Fisher’s exact test, p < 0.05; Figure 2(c) and Figure 2(d)), but not at 24 and 30 h (Fisher’s exact test, p > 0.05; Figure 2(c) and Figure 2(d)).

3.2. Choice Preference Test between E. crus-galli var. aristata and Rice

3.2.1. Trigonotylus caelestialium

After rearing of females on E. crus-galli var. aristata, a significantly higher number of females was present on E. crus-galli var. aristatathan on rice at all of the time points (number of individuals on E. crus-galli var. aristata/rice at 3, 6, 24, 27, and 30 h = 71/8, 58/8, 47/8, 41/1, and 42/10 respectively) (binomial test, p < 0.05; Figure 3(a)). In contrast, after rearing of females on rice, a significantly higher number of females was present on E. crus-galli var. aristata than on rice at 3 and 6 h (number of individuals on E. crus-galli var. aristata/rice = 73/16 and 74/23 respectively) (binomial test, p < 0.05; Figure 3(b)), with no significant difference being documented at 24 h and after (number of individuals on E. crus-galli var. aristata/rice at 24, 27, and 30 h = 49/34, 38/33, and 30/34 respectively) (binomial test, p > 0.05; Figure 3(b)). The ratio of females present on the plants used for rearing (E. crus-galli var. aristata and rice) was significantly different at 24 - 30 h (Fisher’s exact test, p < 0.05; Figure 3(a) and Figure 3(b)), but not at 3 and 6 h (Fisher’s exact test, p > 0.05; Figure 3(a) and Figure 3(b)).

After rearing of males on E. crus-galli var. aristata, a significantly higher number of males was present on E. crus-gallivar. aristata than on rice at 3 - 27 h (number of individuals on E. crus-gallivar. aristata/rice at 3, 6, 24, and 27 h = 28/8, 30/6, 17/1, and 21/4 respectively) (binomial test, p < 0.05; Figure 4(a)), whereas there was no significant difference at 30 h (number of individuals on E. crus-galli var. aristata/rice = 16/3) (binomial test, p > 0.05; Figure 4(a)). In contrast, after rearing of males on rice, a significantly higher number of males was present on E. crus-galli var. aristata than on rice at 3 and 6 h (number of individuals on E. crus-galli var. aristata/rice = 60/15 and 58/12 respectively) (binomial test, p < 0.05; Figure 4(b)), whereas no significant difference was detected at 24 h or later (number of individuals on E. crus-galli var. aristata/rice at 24, 27, and 30 h = 40/24, 37/21, and 39/17 respectively) (binomial test, p > 0.05; Figure 4(b)). The ratio of males present on the plants used for rearing (E. crus-galli var. aristata or rice) was significantly different at 24 h (Fisher’s exact test, p < 0.05; Figure 4(a) and Figure 4(b)), but not at any other time point (Fisher’s exact test, p > 0.05; Figure 4(a) and Figure 4(b)).

3.2.2. Stenotus rubrovittatus

After rearing of females on E. crus-galli var. aristata, a significantly higher number of females was present on E. crus-galli var. aristata than on rice at 3 and 6 h (number of individuals on E. crus-galli var. aristata/rice = 60/13 and 70/17 respectively) (binomial test, p < 0.05; Figure 3(c)), whereas there was no significant difference at 24 h or later (number of individuals on E. crus-galli var. aristata/rice at 24, 27, and 30 h = 46/60, 43/57, and 47/50

(a) (b)(c) (d)

Figure 3. Proportion of adult rice bug females on Echinochloa crus-galli var. aristata versus those on rice plants. Choice preference tests between E. crus-galli var. aristata and rice were conducted with (a): Trigonotylus caelestialium reared on E. crus-galli var. aristata; (b): T. caelestialium reared on rice; (c): Stenotus rubrovittatus reared on E. crus-galli var. aristata, and (d): S. rubrovittatus reared on rice. The adults were counted at 3, 6, 24, 27, and 30 h. : P values comparing the number of adults on E. crus-galli var. aristata and that on rice at each time point using binomial test. The numbers in parentheses represent the number of adults on plants. : P values comparing the proportion of adults present on E. crus-galli var. aristata and rice (i.e., plants used for rearing) at the same time points using Fisher’s exact test. Asterisk (*) represents p < 0.05.

respectively) (binomial test, p > 0.05; Figure 3(c)). In contrast, after rearing of females on rice, a slightly higher number of females was present on E. crus-galli var. aristata than on rice at 3 h (number of individuals on E. crus-galli var. aristata/rice = 57/33) (binomial test, p < 0.05; Figure 3(d)), whereas no significant difference in the number of females was observed at 6 h or later (number of individuals on E. crus-galli var. aristata/rice at 6, 24, 27, and 30 h = 57/41, 64/46, 61/45, and 60/43 respectively) (binomial test, p > 0.05; Figure 3(d)). The ratio of females present on the plants used for rearing (E. crus-galli var. aristata and rice) was significantly different at 3, 6, and 24 h (Fisher’s exact test, p < 0.05; Figure 3(c) and Figure 3(d)), but not at 27 h or later (Fisher’s exact test, p > 0.05; Figure 3(c) and Figure 3(d)).

After rearing males on E. crus-galli var. aristata, a significantly higher number of males was present on E. crus-galli var. aristata than on rice at 3 and 6 h (number of individuals on E. crus-galli var. aristata/rice = 76/15 and 74/13 respectively) (binomial test, p < 0.05; Figure 4(c)), whereas no significant difference was detected at 24 h or later (number of individuals on E. crus-galli var. aristata/rice at 24, 27, and 30 h = 38/29, 46/24, and 42/34 respectively) (binomial test, p > 0.05; Figure 4(c)). In contrast, after rearing of males on rice, there was no significant difference in the number of males present on E. crus-galli var. aristataor rice at any of the time points (number of individuals on E. crus-galli var. aristata/rice at 3, 6, 24, 27, and 30 h = 40/35, 55/42, 30/38, 30/48, and 31/47 respectively) (binomial test, p > 0.05; Figure 4(d)). The ratio of males present on the plants used for rearing (E. crus-galli var. aristata and rice) was significantly different at 3, 6, and 27 h (Fisher’s exact test, p < 0.05; Figure 4(c) and Figure 4(d)), but not at 24 and 30 h (Fisher’s exact test, p > 0.05; Figure 4(c) and Figure 4(d)).

(a) (b)(c) (d)

Figure 4. Proportion of adult rice bug males on Echinochloa crus-galli var. aristata versus those on rice plants. Choice preference tests between E. crus-galli var. aristata and rice were conducted with (a): Trigonotylus caelestialium reared on E. crus-galli var. aristata; (b): T. caelestialium reared on rice; (c): Stenotus rubrovittatus reared on E. crus-galli var. aristata, and (d): S. rubrovittatus reared on rice. The adults were counted at 3, 6, 24, 27, and 30 h. : P values comparing the number of adults on E. crus-galli var. aristata and that on rice at each time point using binomial test. The numbers in parentheses represent the number of adults on plants. : P values comparing the proportion of adults present on E. crus-galli var. aristata and rice (i.e., plants used for rearing) at the same time points using Fisher’s exact test. Asterisk (*) represents p < 0.05.

4. Discussion

The ratio of the number of S. rubrovittatus adults on D. ciliaris versus rice and E. crus-galli var. aristata versus rice increased with time, possibly because S. rubrovittatus had a stronger preference for D. ciliaris than for E. crus-galli var. aristata. In comparison, the ratio of T. caelestialium adult numbers on D. ciliaris versus rice decreased with time, whereas it remained consistently higher for E. crus-galli var. aristata versus rice, possibly because T. caelestialium has a stronger preference for E. crus-galli var. aristata than for D. ciliaris. If prior experience affects preference, after rearing of T. caelestialium adults on rice, more individuals would be expected to prefer rice over E. crus-galli var. aristata initially, and then this preference would subsequently decrease. However, the opposite results were obtained. It is possible that the quality of plants in the flasks deteriorated with time. Nevertheless, preference should be influenced by prior experience, because significantly different adult ratios were obtained between the two weeds and rice, depending on the plants used for rearing. Because T. caelestialium had a strong preference for E. crus-galli var. aristata, adults reared on E. crus-galli var. aristata might have retained this preference, even when the test plants deteriorated. In contrast, T. caelestialium adults reared on rice might have selected E. crus-galli var. aristata when the plants were in good condition, switching to rice plants when E. crus-galli var. aristata deteriorated.

Prior experience influenced plant preference behavior of T. caelestialium and S. rubrovittatus. However, the effect of experience disappeared after just 1 d. Experience during specific periods (egg-young larvae) has been shown to influence adult oviposition in a parasitic wasp [17] . In contrast, oviposition by Drosophila melanogaster is influenced by odor exposure immediately before testing, with this effect being enhanced by the length of the exposure period [18] . Thus, 4 d might have been a too short duration for the rice bugs to have gained sufficient experience in this study. Alternatively, 1 d of experience might be sufficient, and rice bugs might experience and adjust to other plants (i.e., the non-rearing plant) during the tests. Thus, further study is required to understand the relationship between the length of experience and the strength of the effect of experience.

It remains unclear what regulates the relationship between preference and prior experience. Both rice bug species are attracted by odors released from host plants [10] - [12] [19] . Attraction behavior is altered by olfactory learning in several phytophagous insects [20] - [24] . Therefore, these bugs may be influenced by learning plant odors. However, because the current experiment was conducted in a narrow cage, plant selection by the bugs was probably not caused by their attraction to volatile compounds; rather, they probably remained on the plant following direct contact or sucking (feeding).

Trigonotylus caelestialium and S. rubrovittatus females release sex attractants to attract males [25] - [28] . However, it remains unclear how attractants influence the behavior of bugs in narrow cages; thus, the males and females are separated in the selection test to avoid any interaction between sexes. The results showed that both sexes exhibited the same preference trends; thus, differences between the sexes were not considered in this study.

In the current study, adult bugs tended to select plants that they had previously experienced. If the effect of experience in nymphs is sustained to the adult stage, adults may select the same plant species as that on which the nymphs grew. Therefore, if these two rice bug species developed on weeds, they would probably select the same plant species as adults. However, if the weeds deteriorate and disappear, the bugs may transfer and adjust to rice plants in a relatively short period. The results of this study showed that the influence of prior experience declined with time, leading to a situation where the adult ratio on rice plants versus weeds became equal. Thus, these ratios indicate innate preference. Consequently, even though rice bugs grow on weeds, they are expected to adjust to rice plants with time, and spread over rice paddies.

Acknowledgements

I am grateful to Dr. H. Higuchi, Ryukoku University, and Dr. A. Takahashi, NARO Tohoku Agricultural Research Center, for their support and suggestions.

Cite this paper
Nagasawa, A. (2016) Food Preference of Pecky Rice Bugs Is Influenced by Experience. Advances in Entomology, 4, 104-113. doi: 10.4236/ae.2016.42012.
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