Appl. Entomol. Zool. 43 (2): 259–264 (2008) http://odokon.org/
Developmental Parameters and Photoperiodism in Trigonotylus tenuis (Reuter) (Heteroptera: Miridae)
Yoshinori SHINTANI*,† and Hiroya HIGUCHI National Agriculture and Food Research Organization, National Agricultural Research Center, Hokuriku Research Center; Joetsu, Niigata 943–0193, Japan (Received 12 July 2007; Accepted 25 December 2007)
Abstract Developmental parameters and photoperiodism in Trigonotylus tenuis (Reuter) (Heteroptera: Miridae) were examined using wheat seedlings as food. The thermal threshold and effective cumulative temperature were 12.5°C and 91.9 day-degrees in the egg stage, 12.7°C and 155.8 day-degrees in the nymphal stage, and 11.7°C and 49.7 day-degrees in the preoviposition stage. Mean longevity of female and male adults at 25°C was 18.4 and 22.8 days, respectively, and a female adult laid 203 eggs on average. A temperature-dependent long-day photoperiodic response was observed in the maternal induction of egg diapause. At 17.5, 20 and 22.5°C, females showed a clear response to the photoperiod with a critical daylength of around 12.5 h/day; females reared under short-day conditions laid diapause eggs whereas those reared under long-day conditions laid nondiapause eggs. At higher temperatures (25, 27.5 and 30°C), however, females responded little to the photoperiod, irrespective of which they laid a high percentage of nondiapause eggs. Based on comparisons with T. caelestialium, a species closely related to T. tenuis, this photoperiodism is considered to be an adaptation to southern climates.
Key words: Trigonotylus tenuis; developmental parameter; maternal effect; photoperiodism; egg diapause
Higuchi and Takahashi, 2005) and photoperiodic INTRODUCTION and thermal induction of diapause (Okuyama, Bugs of various families in Heteroptera suck 1982; Kudô and Kurihara, 1989; Higuchi and young rice grains and this results in pecky rice at Takahashi, 2005) have been examined. harvest. Such bugs are called ‘pecky rice bugs’ and Another species in the genus Trigonotylus, damage from pecky rice bugs has been increasing, T. tenuis had not been recorded on the mainland especially in northern Japan, the major source of until it was recently found in southwestern Japan in rice in the country (Shiraishi, 2001; Higuchi and Okayama, Hiroshima and Nagasaki Prefectures Takahashi, 2003). The rice leaf bug Trigonotylus (Sato and Yasunaga, 1999a,b). This species is con- caelestialium, not recognized as an important sidered to be of southern origin because it is pecky rice bug except in Hokkaido, has recently widely distributed in tropical and temperate zones been expanding colonized areas in northern Hon- (Schuh, 1995). T. tenuis has never been recorded in shu, severely damaging rice crops in the Tohoku northern Japan, but in southwestern Japan, accord- and Hokuriku districts (Higuchi and Takahashi, ing to reliable records, T. tenuis and T. caelestial- 2003; Watanabe and Higuchi, 2006). In this ium coexist (Sato and Yasunaga, 1999b). It is very species, fundamental life history characteristics, likely that due to their similar appearance, T. cae- i.e., overwintering status (Higuchi and Takahashi, lestialium and T. tenuis have been confused, and 2002), seasonal occurrence of egg diapause thus, the records of insects treated as T. caelestial- (Okuyama, 1982; Kudô and Kurihara, 1988; ium, especially in southwestern Japan, are partially
*To whom correspondence should be addressed at: E-mail: [email protected] † Present address: Laboratory of Horticultural Entomology, Minami Kyushu University, Minami-Takanabe 11609, Takanabe, Miyazaki 884–0003, Japan DOI: 10.1303/aez.2008.259
259 260 Y. SHINTANI and H. HIGUCHI unreliable (Sato and Yasunaga, 1999b; Yasunaga et bated or reared from egg to adult stages at various al., 2001). In southern Kyushu, T. caelestialium is temperatures (17.5, 20, 22.5, 25, 27.5 and 30°C) considered to be uncommon because only T. tenuis under 16L : 8D. Adult insects from the mass-rear- has been collected in Miyazaki Prefecture (Shin- ing culture were reared at one of these tempera- tani, unpublished). Yasunaga et al. (2001) strongly tures. Laid eggs were collected, placed on wet filter doubted past records from the Nansei Islands, paper in Petri dishes (9 cm diameter), and incu- located south of Kyushu. This information suggests bated at the same temperatures. Hatching nymphs that T. caelestialium is adapted to northern cli- were transferred to plastic cups (12 cm diameter, mates. 12 cm height) and reared successively at the same It is likely that T. tenuis is also a pecky rice bug temperatures. The nymphs were provided with because of its similarity in food habituation to wheat seedlings washed free of soil and checked other pecky rice bugs. Except for its morphology for adult emergence every day. Some of the (Sato and Yasunaga, 1999a,b), however, little is nymphs were examined for the number of molts at known about the fundamental characteristics of 25°C. Adults were paired in a glass tube (17.5 cm this species. In the present study, the thermal high and 2.5 cm thick) on the day of emergence. threshold and effective cumulative temperature Two wheat seedlings (about 5 cm tall) were placed were determined, and fecundity and photoperi- upright in a wet sponge fixed at the bottom of the odism were examined in T. tenuis. Here, the eco- glass tube. The upper end of the glass tube was logical significance of photoperiodism in T. tenuis closed with a piece of nylon mesh. The wheat is discussed based on comparisons with T. caeles- seedlings were changed every day and leaf sheaths tialium. were checked for eggs. The collected eggs were kept at the same temperatures and hatching was checked every day. Thermal threshold was deter- MATERIALS AND METHODS mined using a formula proposed by Ikemoto and Insects. About 200 adults of T. tenuis were col- Takai (2000); DT k tD, where D indicates the lected from Poaceae grasses by sweeping an insect duration of development; T, temperature; t, the net near rice paddy fields in Izumi-Sano City estimated thermal threshold; and k, the effective (34.4°N, 135.3°E), Osaka on August 31, 2002. Ac- cumulative temperature. cording to Sato and Yasunaga (1999a), the collec- Adult longevity and fecundity. To examine tion site in the present study is located near the longevity and fecundity, newly emerged adults in northernmost limits of the species in Japan. The in- the mass-rearing culture were paired in glass tubes sects collected were brought to the laboratory and on the day of emergence. Twenty pairs were made mass-reared under 16L : 8D (16 h of light and 8 h and reared with two wheat seedlings. The seedlings of dark) at 25°C following the method for mass- were changed every day and the leaf sheaths were rearing of T. caelestialium reported by Higuchi and checked for eggs. The number of eggs laid was Takahashi (2000). Briefly, the insects were placed recorded until death. If the female died first, only in acryl amide cages (34 cm 25 cm 34 cm) with the male was reared thereafter, whereas if the male wheat seedlings about 5 cm tall as food. The wheat died first, another male was placed in the glass tube was grown from seed in Petri dishes (9 cm diame- as a new partner. The dates of emergence and death ter) with soil at 25°C for four or five days, before of adults were recorded. being put into the cages. They also served as Photoperiodism. Eggs were removed from the oviposition sites for adult insects and were changed mass-rearing culture and placed on wet filter paper every seven to ten days. When insects were needed in a Petri dish under 16L : 8D at 25°C. Hatching for experiments, adult insects or leaf sheaths inside nymphs were reared in plastic cups under various which eggs were laid were taken out randomly photoperiodic conditions at 17.5, 20, 22.5, 25, 27.5 from the mass-rearing culture. and 30°C. Adults that emerged under these condi- Determination of developmental parameters. tions were paired in glass tubes on the day of emer- To determine the thermal threshold and effective gence (day 0), and laid eggs were collected every cumulative temperature for embryonic, nymphal day until day 6 at 25 to 30°C, until day 8 at 20 and and preoviposition development, insects were incu- 22.5°C, and until day 20 at 17.5°C. The eggs were Life History Characteristics in T. tenuis 261 incubated under 16L : 8D at 25°C and diapause 203 35 (mean S.D.). attributes were determined. The percentage of dia- pause eggs in each condition was obtained as the Photoperiodism average data for individual pairs. Unfertilized eggs No significant difference in the nymphal or pre- were excluded from analysis. oviposition period was observed among insects reared under various photoperiods (ANOVA, p 0.05). Namely, the development of neither the RESULTS nymphal nor preoviposition stage was controlled Developmental parameters Table 1 shows the egg, nymphal and preoviposi- Table2. Estimated developmental threshold and effective a tion periods in T. tenuis. The mean egg period at cumulative temperature in T. tenuis 30, 27.5, 25, 22.5 and 20°C was 5.4, 6.2, 7.1, 9.0 Effective Developmental and 12.5 days, respectively. Nymphs underwent cumulative Correlation Stage threshold five instars and the mean nymphal period at 30, temperature coefficient, r2 (°C) 27.5, 25, 22.5, 20 and 17.5°C was 9.2, 10.8, 12.4, (day-degrees) 15.5, 21.2 and 33.0 days, respectively. The mean preoviposition period at 30, 27.5, 25, 22.5 and Egg 12.5 91.9 0.9951 Nymph 12.7 155.8 0.9991 20°C was 2.9, 3.2, 3.5, 4.4 and 6.2 days, respec- Preoviposition 11.7 49.7 0.9703 tively. From these data, the thermal threshold and effective cumulative temperature for each stage a Values were calculated from data in Table 1. were calculated as 12.5°C and 91.9 day-degrees for the egg stage, 12.7°C and 155.8 day-degrees for the nymphal stage, and 11.7°C and 49.7 day- degrees for the preoviposition stage (Table 2).
Adult longevity and fecundity Figure 1A shows survival curves for adult T. tenuis at 25°C. Longevity varied from 8 to 27 days in females and 6 to 37 days in males with mean values ( S.D.) of 18.4 5.0 and 22.8 8.0 days, respectively. The time course of oviposition at 25°C is shown in Fig. 1B. Oviposition started on day 3 after the emergence of adults in most females and oviposition reached a maximal level of activity from days 5 to 7. During this period, more than 10 eggs were laid daily; thereafter, the activity gradu- ally decreased. The overall number of eggs reached
Table1.Developmental time of T. tenuis in days (mean S.D.) at different constant temperaturesa
Temperature Preoviposition Egg Nymph (°C) period
30 5.4 0.3 (25) 9.2 0.6 (22) 2.9 0.6 (19) Fig. 1. A. Survival curves of adults of T. tenuis under 27.5 6.2 0.4 (26) 10.8 0.9 (23) 3.2 0.6 (16) 16L : 8D at 25°C. Data for females ( ) and males ( ) are 25 7.1 0.6 (26) 12.4 1.1 (24) 3.5 0.9 (21) shown separately. Sample size was 20 for each sex. B. Change 22.5 9.0 0.7 (25) 15.5 1.2 (19) 4.4 1.2 (17) in oviposition activity with age in T. tenuis. Adults were reared 20 12.5 1.0 (25) 21.2 1.8 (21) 6.2 1.4 (15) under 16L : 8D at 25°C and eggs were collected every day. Num- 17.5 — 33.0 3.4 (16) — ber of eggs laid per female per day ( ) and percentage of females laying eggs ( ) are shown. Both values were calculated a Numbers in parentheses indicate sample size. based on the number of females that survived until that day. 262 Y. SHINTANI and H. HIGUCHI by the photoperiod. For example, the mean nymphal period under various photoperiodic conditions at 20°C was 21 to 22 days and 20 to 21 days in females and males, respectively, and the mean pre- oviposition period under various photoperiodic conditions at 20°C was about 6 days. In the embry- onic stage, however, two types of development were observed; some eggs hatched on days 6 to 8 at 25°C but others did not hatch for some months when kept at the same temperature. Both types of eggs were banana-shaped and green when laid, and thus, it was impossible to distinguish them early in embryonic development. However, their appear- ance differed from day 3; the non-hatching eggs Fig. 2. Photoperiodic response of T. tenuis at various tem- were colored violet near the operculum and green peratures. Insects were reared from hatching under various at the other end, with a gradual change in color in combinations of temperature and photoperiod, and the dia- the middle, and this appearance did not change for pause attributes of the eggs laid were examined. Each plot in- at least a few months, whereas the hatching eggs dicates the average percentage of diapause eggs laid by an in- continued development, with their appearance dividual female. Sample size was 8 to 21 for each plot. changing daily. It has been observed in T. caeles- tialium that in eggs laid by adults reared under 12L : 12D, diapause occurred in most if not all of short-day conditions, embryonic development the eggs. Under 12.5L : 11.5D, diapause occurred ceases at an early stage (Okuyama, 1982; Kudô in 33, 47 and 70% of the eggs at 22.5, 20 and and Kurihara, 1988). Okuyama (1982) confirmed 17.5°C, respectively. that such eggs hatch after chilling for a few months and considered the phenomenon to be diapause. DISCUSSION Also in T. tenuis, it was found that non-hatching eggs exposed to chilling at 5ºC for two months As an adaptation to seasonally changing envi- hatched after being returned to 25°C (Shintani, ronments, many insects enter diapause by respond- unpublished). Thus, it was concluded that non- ing to seasonal cues such as temperature and pho- hatching eggs were diapause eggs. Differences toperiod (Tauber et al., 1986; Danks, 1987). In the between diapause and nondiapause eggs appeared present study, it was shown that T. tenuis enters di- three days after oviposition, but because the col- apause early in the egg stage by responding to tem- lected eggs were kept under the same conditions perature and photoperiod in parental generation. In (25°C and 16L : 8D), this diapause was considered many insects that have facultative egg diapause, to be induced maternally. whether an egg enters diapause or not depends on Figure 2 shows the incidence of diapause under the environmental conditions experienced by its various photoperiods and temperatures. At 30°C, parental generation (Danks, 1987; Mousseau and diapause did not occur under any of the photoperi- Dingle, 1991). In the silkworm Bombyx mori, for odic conditions. At 27.5 and 25°C, diapause did example, egg diapause is induced or avoided by the not occur under any photoperiod from 13L : 11D to temperature and photoperiod experienced by eggs 16L : 8D; however, under 12L : 12D at 27.5°C, dia- and young larvae of the preceding generation pause occurred in 6% of the eggs, and under (Kogure, 1933). In the band-legged ground cricket 11L : 13D and 12L : 12D at 25°C, it occurred in 18 Dianemobius nigrofasciatus, egg diapause is con- and 2% of the eggs, respectively. At 22.5, 20 and trolled by parental photoperiod and temperature, 17.5°C, however, a clear long-day photoperiodic although egg temperature also has an important response was observed with a critical daylength of effect on diapause induction (Fukumoto et al., around 12.5 h/day: under a photoperiod of 2006). Also in T. caelestialium, the species closely 13L : 11D or longer, diapuse occurred in few if any related to T. tenuis, egg diapause is maternally of the eggs, whereas under 11L : 13D and induced early in the embryonic stage (Okuyama, Life History Characteristics in T. tenuis 263
1982; Kudô and Kurihara, 1989). In T. tenuis, be- to lay diapause eggs in the same season every year, cause a high percentage of diapause eggs are laid and the temperature-dependent photoperiodism under short-day conditions and diapause eggs do may not be fully functional in Osaka. not hatch for long periods unless they experience In the subtropics, however, this temperature- chilling, this species is considered to overwinter in dependent photoperiodism may function to modu- the egg stage in diapause as does T. caelestialium late the timing of diapause. In Amami City (28.4° (Higuchi and Takahashi, 2002). N, 129.5°E), Amami Island (in the Nansei Islands), In the majority of insects examined, photoperi- for example, a daylength of 12.5 h/day occurs odic responses are thermally modified and interac- around the 14th of October. The average tempera- tion between photoperiod and temperature is ex- ture for the 11 days between October 9th and 19th pressed in thermal alternation of the critical in the last 10 years has been 24.2°C (e.g., Japan daylength. In long-day insects, long daylengths and Meteorological Agency, 1997). The highest aver- high temperatures function together to prevent dia- age temperature was 25.7°C in 2005 and the lowest pause, and short daylengths and low temperatures was 21.4°C in 1997. If autumn temperature is function together to promote diapause. This leads higher, as in 2005, diapause is avoided even under to shorter critical daylengths with higher tempera- short daylengths and more generations are pro- tures. Among insect species, however, a wide vari- duced, and if the autumn temperature is lower, as in ation is found in the degree to which critical 1997, diapause is induced. daylength shifts with temperature, but such mecha- The optimal range for the photoperiodism of nisms generally have a role in modulating the tim- T. tenuis (17.5 to 22.5°C) seems remarkably differ- ing of diapause to synchronize with yearly variable ent from that of T. caelestialium. Okuyama (1982) seasonal changes in the environment (Beck, 1980; examined the photoperiodism of T. caelestialium Tauber et al., 1986; Saunders, 2002). The long-day collected in Asahikawa City (43.8°N, 142.3°E), photoperiodic response found in T. tenuis is also Hokkaido at 23–25°C, and discovered that they thermally modified, but the interaction between responded clearly to the photoperiod with a critical photoperiod and temperature is different in that daylength of between 13 and 14 h/day. Kudô and temperature up to 22.5°C does not alter the critical Kurihara (1989) also showed that T. caelestialium daylength of around 12.5 h/day, and higher temper- collected in Morioka City (39.7°N, 141.2°E), Iwate atures produce almost no diapause under any pho- Prefecture clearly responded to the photoperiod at toperiod. In other long-day insects, temperature 25°C. Higuchi and Takahashi (2005) demonstrated does not alter critical daylength to any great de- that T. caelestialium collected in Joetsu City gree, but it has an important effect on whether the (37.1°N, 138.2°E), Niigata Prefecture responded to insects respond to the photoperiod at all. For exam- the photoperiod at 25°C but found that the re- ple, in a flesh fly Sarcophaga argyrostoma, which sponse was less clear at 22°C because diapause oc- enters pupal diapause when larvae are reared under curred in a substantial proportion of the eggs laid short-day conditions, all photoperiods at 25°C pro- under 14L : 10D and 15L : 9D. Another geographic duce almost no diapause (Saunders, 1971). In the population collected in Azuchi Town (35.1°N, case of T. tenuis, the critical daylength of the pho- 136.1°E), Shiga Prefecture also showed a long-day toperiodic response is about 12.5 h/day, and this photoperiodic response at 25°C with a critical occurs around the 10th of October at the collection daylength of around 13.5 h/day (Shintani, unpub- site when one hour is added as civil twilight. lished). These findings indicate that the optimal According to meteorological data (e.g., Japan Me- temperature for photoperiodism in T. caelestialium teorological Agency, 1997), the average tempera- is 25°C or higher and this species starts to lay dia- ture in Kumatori Town (34.4°N, 135.4°E), Osaka, pause eggs in early autumn. T. caelestialium has a for the 11 days between October 5th and 15th from multivoltine life cycle and the number of genera- 1997 to 2006, was 19.5°C. The highest average tions per year varies geographically from two to temperature was 21.5°C in 1999 and the lowest five depending on climatic conditions (Okuyama, was 17.5°C in 1997. In this season, temperatures as 1982; Yasunaga et al., 2001; Higuchi and Taka- high as 25°C are only reached for a few hours at a hashi, 2003). T. tenuis undoubtedly has a multivol- time. Therefore, it is considered that T. tenuis starts tine life cycle because field-collected adults laid 264 Y. SHINTANI and H. HIGUCHI nondiapause eggs, and subsequent generations tion of line-fitting methods with both variables subject to were reared in the laboratory. The thermal thresh- error. Environ. Entomol. 29: 671–682. old and effective cumulative temperature of each Japan Meteorological Agency (1997) Monthly Report of the Japan Meteorological Agency, Meteorological Observa- stage and adult longevity in T. tenuis determined in tions for January–Decenber 1997. The Japan Meteoro- the present study are comparable to those in T. cae- logical Agency, Tokyo (on CD-ROM). lestialium (Takahashi and Higuchi, 2001) and, thus, Kogure, M. (1933) The influence of light and temperature on the time required for one generation is not so dif- certain characteristics of the silkworm, Bombyx mori. ferent. In part of the Kinki district, which is located Journal of the Department of Agriculture, Kyushu Imper- ial University 4: 1–93. in the central area of Honshu Island, the two Kudô, S. and M. Kurihara (1988) Seasonal occurrence of species coexist at some sites (N. Hozumi, personal egg diapause in the rice leaf bug, Trigonotylus caelestial- communication). At such sites, it is considered that ium Kirkaldy (Heteroptera: Miridae). Appl. Entomol. autumnal prevalence differs clearly between the Zool. 23: 365–366. two species. Apparently, T. caelestialium is of Kudô, S. and M. Kurihara (1989) Effects of maternal age on northern origin and has a tendency to prepare for induction of egg diapause in the rice leaf bug, Trigonoty- lus caelestialium Kirkaldy (Heteroptera: Miridae). Jpn. winter earlier in the season by laying diapause eggs J. Entomol. 57: 440–447. when the temperature is relatively high, but Mousseau, T. A. and H. Dingle (1991) Maternal effects in T. tenuis produces more generations late into au- insect life histories. Annu. Rev. Entomol. 36: 511–534. tumn. The difference in the optimal temperature Okuyama, S. (1982) Role of day-length in the oviposition of range and critical daylength for photoperiodism dormant eggs by the rice leaf bug, Trigonotylus caeles- tialium Kirkaldy, and condition for release from the dor- likely comes from the difference in origin. mancy. Annu. Rep. Plant Prot. North Japan 33: 89–92 ACKNOWLEDGEMENTS (in Japanese). Sato, T. and T. Yasunaga (1999a) Taxonomy of the genus We thank the two anonymous referees for invaluable com- Trigonotylus Fieber from Japan (Heteroptera, Miridae). ments. Rostria 48: 11–19. Sato, T. and T. Yasunaga (1999b) Taxonomy and identifica- REFERENCES tion of three Japanese species of the plant bug Genus Beck, S. D. (1980) Insect Photoperiodism. 2nd ed. Acade- Trigonotylus. Plant Prot. 53: 265–267 (in Japanese). mic Press, New York. 397pp. Saunders, D. S. (1971) The temperature-compensated pho- Danks, H. V. (1987) Insect Dormancy: An Ecological Per- toperiodic clock “programming” development and pupal spective. Biological Survey of Canada, Ottawa. 439 pp. diapause in the flesh-fly, Sarcophaga argyrostoma. J. Fukumoto, E., H. Numata and S. Shiga (2006) Effects of Insect Physiol. 17: 801–812. temperature of adults and eggs on the induction of em- Saunders, D. S. (2002) Insect Clocks. 3rd ed. Elsevier, bryonic diapause in the band-legged ground cricket, Di- Amsterdam. 576 pp. anemobius nigrofasciatus. Physiol. Entomol. 31: 211– Schuh, R. T. (1995) Plant Bugs of the World (Insecta: Het- 217. eroptera: Miridae): Systematic Catalog, Distribution, Higuchi, H. and A. Takahashi (2000) Method for rearing the Host List and Bibliography.New York Entomological rice leaf bug, Trigonotylus caelestialium (Kirkaldy) (Het- Society, New York. xii 1329 pp. eroptera: Miridae) with wheat seedlings. Proc. Assoc. Shiraishi, M. (2001) Occurrence situation of rice bugs caus- Pl. Prot. Hokuriku 48: 23–25 (in Japanese). ing the pecky rice in 2001. Plant Prot. 55: 445–446 (in Higuchi, H. and A. Takahashi (2002) Lack of evidence for Japanese). nymphal and adult hibernation in Joetsu population of the Takahashi, A. and H. Higuchi (2001) Effect of temperature rice leaf bug, Trigonotylus caelestialium (Kirkaldy) (Het- on the development of rice leaf bug, Trigonotylus caeles- eroptera: Miridae). Jpn. J. Appl. Entomol. Zool. 46: 41– tialium (Kirkaldy) (Heteroptera: Miridae). Proc. Assoc. 43 (in Japanese with English summary). Pl. Prot. Hokuriku 49: 19–22 (in Japanese). Higuchi, H. and A. Takahashi (2003) [Problems on pecky Tauber, M. J., C. A. Tauber and S. Masaki (1986) Seasonal rice bugs.] Agriculture and Horticulture 78: 756–761 Adaptations of Insects. Oxford University Press, New (in Japanese). York. 411 pp. Higuchi, H. and A. Takahashi (2005) Seasonal changes in Watanabe, T. and H. Higuchi (2006) Recent occurrence and egg diapause induction and effects of photoperiod and problem of rice bugs. Plant Prot. 60: 201–203 (in Japa- temperature on egg diapause in the rice leaf bug, nese). Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miri- Yasunaga, T., M. Takai, T. Kawasawa and Y. Nakatani (2001) dae). Jpn. J. Appl. Entomol. Zool. 49: 113–118 (in A Field Guide to Japanese Bugs II. Terrestrial Het- Japanese with English summary). eropterans (T. Yasunaga, M. Takai and T. Kawasawa Ikemoto, T. and K. Takai (2000) A new linearized formula eds.). Zenkoku Noson Kyoiku Kyokai, Tokyo. 350 pp. for the law of total effective temperature and the evalua- (in Japanese).