Appl. Entomol. Zoo!. 39 (3): 417-425 (2004) http://odokon.ac.affrc.go.jp/
Biological studies on three Micromus species in Japan (Neuroptera: Hemerobiidae) to evaluate their potential as biological control agents against aphids: 1. Thermal effects on development and reproduction
Takahiko SATO* and Hajimu TAKADA Laboratory of Applied Entomology, Graduate School of Agriculture, Kyoto Prefectural University; Kyoto 606-8522, Japan
(Received 13 January 2004; Accepted 9 March 2004)
Abstract We investigated the developmental period, survival rates during the larval and pupal stages, adult longevity, and fecun dity of Micromus numerosus, M. angulatus and M. linearis at five constant temperature conditions (10, 15, 20, 25 and 30°C), under a 15L-9D photoregime with Aphis craccivora as prey. The lower thermal thresholds and thermal con stants for total development were estimated, respectively, at 7.7°C and 343 degree-days (DD) forM. numerosus, 9.0°C and 297 DD forM. angulatus, and 5.2°C and 447 DD forM. linearis. M. linearis eggs did not hatch at 30°C. At 20°C, the mean total number of eggs laid by a female was 544 in M. numerosus, 399 in M. angulatus, and 614 in M. linearis. The mean longevity of female adult in days was 55 in M. numerosus, 46 in M. angulatus, and 46 in M. linearis. From these results, we evaluated suitable temperature ranges as approximately 20°C forM. numerosus, 15-25°C forM. an gulatus, and 10-25°C forM. linearis.
Key words: Brown lacewing; Micromus; development; reproduction; temperature
as biological control agents for pest aphids in Eu INTRODUCTION rope (van Lenteren et al., 1997). In 2001, C. Brown lacewings (Neuroptera: Hemerobiidae) carnea was registered as a pesticide for pest aphids feed on small soft-bodied arthropods, such as in Japan. However, no hemerobiids have been used aphids, scale insects, spider mites and so on (New, in inoculation and inundation biological control 1975). Thus, brown lacewings have been used as (Eilenberg et al., 2001), so far as we are aware. natural enemies of these pests in classical biologi Among the Hemerobiidae, Micromus and Hemero cal control (Eilenberg et al., 2001 ). Micromus bius species appear promising as biological control timidus Hagen was introduced from Australia to agents against pest aphids, because of their wide the Hawaiian Islands in 1919 for control of various range of prey and habitat (New, 1988). aphids, particularly on sugar cane and corn plants M. numerosus Navas, M. angulatus (Stephens), (Williams, 1927). Brown lacewings were released and M. linearis (Hagen) are common species in and later recovered in the field. Hemerobius nitidu Japan. M. numerosus was recorded from Japan and lus Fabricius and H. stigma Stephens were intro China (Monserrat, 1993). Nakahara (1954) exam duced from Europe to Canada as biological control ined its development under natural conditions, and agents against the balsam woolly aphid, Adelges Kawashima (1958) reported its life history. M. nu piceae (Ratzeburg), during the 1930s (Smith and merosus larvae feed on the brown citrus aphid, Tox Cappel, 1957). However, neither species was re optera citricidus (Kirkaldy), mainly in citrus covered (Garland, 1978), possibly because they did groves (Nakao, 1962). M. angulatus is widely dis not adapt to the climate of Canada. tributed in the Holarctic region (Monserrat, 1993). In another neuropteran family, Chrysopidae, The development and fecundity of the European Chrysoperla carnea (Stephens) and C. rufilabris populations of this species have been investigated (Burmeister) have already been used commercially (Miermont and Canard, 1975; Honek and Ko-
*To whom correspondence should be addressed at: E-mail: [email protected] DOI: 10.1303/aez.2004.417
417 ------~~~~~======~ •
418 T. SATO and H. T AKADA
courek, 1988; Stelzl and Hassan, 1992). M. linearis method. We calculated the lower thermal threshold, is widely distributed from Sri Lanka to Japan t, and thermal constant, K, for the development (Monserrat, 1993), and it is a predator of T. citri from oviposition to adult emergence. The former cidus in Japanese citrus groves (Nakao, 1962). was estimated by extrapolating the regression lines In the present study, we investigated the develop through the x axis (temperature). The latter was de ment, survival rate, adult longevity, and fecundity rived from a reciprocal of the slope of the regres of M. numerosus, M. angulatus, and M. linearis sion line. under a long-day condition at five constant temper Reproduction. A conspecific pair of newly atures ranging from 10 to 30°C and evaluated their emerged adults that had been reared under the potential as biological control agents against pest same temperature and photoperiodic conditions aphids in inoculation and inundation biological was placed in a plastic cup with abundant A. crac control. civora on a leaf of V. faba, a piece of cotton (3 X 5 em), and a piece of moist cotton ball. Each pair was reared under the same conditions as in the MATERIALS AND METHODS immature stages, and the number of eggs laid was Stock culture. The laboratory cultures of M. nu recorded daily until death of the female. If neces merosus and M. angulatus were each established sary, aphids were added to the cup, and the cotton from one female adult that was collected at the Shi was changed daily during the oviposition period. mogamo Branch of the University Farm of Kyoto Statistical analysis. Tukey-type multiple com Prefectural University, Shimogamo, Kyoto in May parison test (Zar, 1999) was conducted for compar 1996. A laboratory culture of M. linearis was es ing the survival rates and sex ratios between the tablished from two female adults that were col five temperatures. In other experiments, the lected on cucumber plants in a plastic greenhouse Kruskal-Wallis test was first conducted to test for in Kamigamo, Kyoto, in May and June 1997. The differences in the data among temperature treat three stock cultures were kept in plastic cages ments and among species. When a significant dif (20X20X30cm) at 18°C under a 15h light: 9h ference (p<0.05) was detected by the test, a com dark (15L-9D) photoregime. The cowpea aphid, parison between temperatures or between species Aphis craccivora Koch, on broad bean, Vicia faba in each combination was performed using Mann L. var. minor, was provided as prey for the stock Whitney's U-test by the Bonferroni method. cultures of the three Micromus species. As females prefer to lay eggs on cotton (Sato, T., unpublished RESULTS data), a piece of cotton (5X8 em) was attached to the ceiling as an oviposition substrate, and was Development changed every 24 h. The larval period consisted of three stadia in all Development. Eggs laid on the cotton in the three Micromus species. The pupa emerged form stock culture within 24 h were placed in a plastic the cocoon after cutting its way out with its cup (5.5 em diam., 3 em high) kept at a constant mandibles and then transformed to an adult. temperature of 10, 15, 20, 25 or 30°C, under a Table 1 shows the mean duration of each devel 15L-9D photoregime. Just after hatching, larvae opmental stage at each temperature. The total de were individually placed in separate plastic cups velopmental period of all three species increased with abundant A. craccivora on a leaf of V. faba with decreasing temperature within the tempera and a piece of moist cotton ball. They were ob ture range tested. The free-living larval period was served daily and their developmental stage and sur approximately one third of the total developmental vival were recorded. period (from oviposition to adult emergence) in The influence of temperature on development each species at all five temperatures. was expressed by regressing the reciprocals of the The lower thermal thresholds and thermal con number of days for development (developmental stants for total development of the brown rates) of the various stages against temperature and lacewings were estimated respectively, at 7. 7°C calculating the regression coefficients. Linear re and 343 degree-days (DD) for M. numerosus, gression lines were generated by the least-squares 9.0°C and 297 DD forM. angulatus, and 5.2°C and •
Table 1. Mean (±SD) developmental period (days) of three Micromus species at different temperatures under a 15L-9D photoregime. Number of individuals are shown in parentheses.
Species From hatching to cocoon formation From cocoon formation to adult emergence From Temperature Egg oviposition to ti eq First stadium Second studium Third studium Total Prepupa Pupa Total adult emergence ~ ('J) 0 "0 M. numerosus s ('J) 10 24.1 ::'::1.0 (11) a - 35.1 ::'::5.2 (11) a 16.0::':: 1.6 (5) a a 15 9.8::'::1.4 (60) b 5.8::'::1.6 (51) a 5.6::':: 1.2 (43) a 5.9::'::2.3 (41) a 17.3::'::4.1 (41) b 8.6::':: 1.2 (28) b 16.2::'::1.7 (21) a 25.0::'::2.0 (21) a 49.4::'::3.1 (21) a ::l "'0.. 20 5.8::'::0.4 (51) c 3.1::'::0.3(43)b 2.4::':: 1.1 (40) b 2.9::'::0.6 (40) b 8.3::':: 1.3 (40) c 4.8::':: 1.0 (37) c 8.1 ::'::0.6 (35) b 12.9::':: 1.3 (35) b 26.9::'::2.4 (35) b 1;;' 25 4.0::'::0 (42) d 2.3::'::0.5 (26) c 1.7::'::0.7 (21) c 2.6::':: 1.0 (18) be 6.6::'::1.1 (18)d 3.1 ::'::0.3 (12) d 5.8::'::0.4 (10) c 8.9::'::0.3 (10) c 19.2::'::0.8 (10) c "0 0"' 30 3.0::'::0 (20) e 1.4::'::0.5 (17) d 1.2::'::0.4 (14) c 2.2::'::0.4 (9) c 4.8::'::0.7 (9) e 2.8::'::0.4 (5) d 5.0::'::0 (3) c 8.0::'::0 (3) c 15.7::'::0.6 (3) c 0.. $:::= M. angulatus ~ s· 10 25.1::'::0.9 (24) a - 29.0::'::3.0 (12) a 20.0::'::6.9 (3) a ::l 15 13.3::'::0.5 (23) b 8.5::'::1.5 (21) a 5.7::':: 1.0 (17) a 6.5::':: 1.9 (17) a 20.5::'::2.2 (17) b 8.4::':: 1.6 (15) ab 15.2::':: 1.0 (9) a 23.2::'::0.8 (9) a 57.7::':: 1.4 (9) a ....,0 >-l 20 6.4::'::0.5 (26) c 2.2::'::0.4 (9) b 3.6::'::0.5 (7) b 3.3 ::'::0.5 (7) b 8.5::'::0.6 (21) c 4.8::'::0.7 (20) c 6.9::'::0.7(17)b 11.7::'::0.9(17)b 26.2::'::1.6(17)b P" @ 25 4.0::'::0 (28) d 2.3::'::0.5 (21) b 1.8::'::0.5 (18) c 1.6::'::0.5 (18) c 5.7::'::0.6 (18) d 2.1 ::'::0.3 (14) d 4.5::'::0.5 (13) c 6.6::'::0.5 (13) c 16.3::'::0.8 (13) c ('J) ::I: 30 3.2::'::0.4 (26) e 2.1 ::'::0.6 (19) b 1.2::'::0.6 (17) d 1. 7::'::0.6 (19) c 5.0::'::0.9 (19) e 2.2::'::0.5 (18) d 4.0::'::0 (13) d 6.1 ::'::0.3 (13) d 14.0::'::0.0 (13) d ('J) M.linearis s ('J) 10 20.9::':: 1.1 (56) a 24.2::':: 1.9 (29) a ::':: ::':: 0 14.3 1.8 (26) a 25.1 1.8 (22) a 39.4::'::2.7 (22) a 83.7::'::3.2 (22) a g:"' 15 10.0::'::0 (27) b 6.9::':: 1.0 (8) a 4.0::':: 1.0 (3) a 4.7::'::0.6 (3) a 18.1 ::'::2.7 (20) b 10.0 ::'::1.2 (20) b 19.5::':: 1.4 (20) b 29.5::':: 1.9 (20) b 57.5::'::3.5 (20) b 5.: til 20 6.0::'::0 (62) c 3.5::'::0.7 (34) b 2.5::'::0.8 (42) b 3.5::'::0.7 (45) b 10.0::':: 1.5 ( 46) c 4.3::'::0.8 (45) c 8.0::'::0.6 (44) c 12.3::'::0.6 (44) c 27.8::'::1.8 (44) c 25 5.1 ::'::0.3 ( 45) d 2.1 ::'::0.3 (17) c 2.0::'::0 (17) c 3.0::'::0.8 (20) c 7.6::':: 1.2 (28) d 3.0::'::0.6 (24) d 5.4::'::0.5 (20) d 8.5 ::'::0.6 (20) d 20.8 ::'::1.2 (20) d
Means in the column of each species followed by the same letter were not significantly different at 5% level by Mann-Whitney's U-test using the Bonferroni method.
\0-"'"
1l •
420 T. SATO and H. T AKADA
447 DD forM. linearis (Fig. 1). adult emergence was significantly higher at 20°C (62.7%) than at any other temperature examined Survival rate (Tukey-type multiple comparison test, p<0.05). In Table 2 shows the survival rates in the larval and M angulatus, the survival rate was highest (65.4%) pupal stages of the three Micromus species. None at 20°C, but did not significantly differ with the of the 100 eggs of M linearis hatched at 30°C. In temperature from 15 to 30°C (Tukey-type multiple M. numerosus, the survival rate from hatching to comparison test, p>0.05). In M. linearis, it was significantly higher at 15 and 20°C (74.1 and 1/y 71.1 %, respectively) than at 10 or 25°C. At 10°C, M. numerosus and M. angulatus larvae preyed on • 0.08 ~ M. numerosus 1/y=0.003x-O.D23. 11'=0.994 (P=0.0029) // aphids and developed, but did not pupate. --~- M. angulatus 1/y=0.004x-o.03e. R'=O.a1e
5 15 20 25 30 Oviposition period, adult longevity, and fecun Temperature ('t) dity Fig. 1. Relationship between temperature and develop In M. numerosus, the proportion of females mental rate during larval and pupal stages of three Micromus ovipositing (percentage of females laying fertile species under a 15L-9D photoregime. eggs to females examined) was significantly lower
Table 2. Survival rate during larval and pupal stages, and sex ratio of three Micromus species at different temperatures under a 15L-9D photoregime. Number of individuals are shown in parentheses.
Number Survival rate (%) Species of Sex ratio Temperature individuals From hatching From cocoon formation From hatching (%females) (OC) examined to cocoon formation to adult emergence to adult emergence
M. numerosus 10 30 36.7 c 0 c 0 c 15 60 68.3 ab 41.5b 28.3 b 52.9 (17) a 20 51 78.4 a 80.0 a 62.7 a 46.9 (32) a 25 42 47.6 be 40.0b 19.0 b 62.5 (8) a 30 18 50.0 be 33.4 be 16.7 be M. angulatus 10 24 50.0 a 0 b 0 b 15 23 73.9 a 52.9 a 39.1 a 55.6 (9) a 20 26 80.8 a 81.0 a 65.4 a 58.8 (17) a I 25 28 64.3 a 72.2 a 46.4 a 61.5 (13) a 30 22 86.4 a 68.4 a 59.1 a 69.2 (13) a ! ~ M. linearis il 10 37 78.4 a 75.9 be 59.5 b 54.5 (22) a II 15 27 74.1 a 100 a 74.1 a 50.0 (20) a 20 62 74.2 a 95.7 ab 71.0 ab 47.7 (44) a 25 45 62.2 a 71.4 c 44.4 b 60.0 (20) a
Values in the column of each species followed by the same letter were not significantly different at 5% level (Tukey-type multi ple comparison test). l It ------·· ------•
Table 3. Reproductive traits of three Micromus species at different temperatures under a 15L-9D photoregime. Number of individuals are shown in parentheses.
Species Percentage of Adult longevity (days)b Preoviposition Oviposition period Postoviposition Temperature females Total number of period (days )b (days)b period (days)b eggs laidb tj eq ovipositing• Female Male ~ (\) 0 >-cj M. numerosus (\)s 15 89 (9) ab 18.0:±:6.4 (8) a 43.5:±: 14.7 (8) a 13.6:±: 18.3 (8) a 78.6±20.8 (9) a 69.3:±:30.5 (7) a 9.7±13.7 (8) b g 20 100(15)a 8.4:±:2.9 (14) b 47.4:±:25.3 (14) ab 1.0:±: 1.9 (14) b 54.8:±:25.5 (14) a 57.1 :±:21.6 (15) a 544.1±543.0(14)a ::l "'0. 25 60 (5) ab 6.3 :±:1.2 (3) ab 9.7:±:5.1 (3) b 0.3 :±:0.6 (3) ab 11.0:±:8.8 (5) b 35.0:±:4.2 (2) a 181.0±269.4 (3) ab ~ 30 33 (3) b 3 (1) 6 (1) 1 (1) 13.0:±:5.2 (3) b >-cj 9 (I) .... M. angulatus 0.0 $::= 15 90(10)a 18.9:±:5.8 (8) a 43.4:±: 13.6 (8) a 11.1 :±:10.1 (8) a 97.1 ±29.3 (7) a 53.0±41.0 (2) ab 84.6:±: 116.3 (7) a ~ s· 20 90(10)a 6.7:±:3.5 (9) b 35.9:±: 18.5 (9) ab 7.9:±: 14.5 (9) a 45.8±21.6 (10) b 86.4:±: 14.3 (7) a 398.9:±:422.1 (9) a ::l 25 100 (8) a 4.8:±: 1.6 (8) b 22.0:±: 11.2 (8) a 2.1 :±:1. 7 (8) a 28.9±9.5 (8) b 31.8:±:24.9 (4) ab 223.2:±:249.0 (8) a ....,0 ...., 30 86 (7) a 4.7:±: 1.6 (6) b 13.7:±:8.2 (6) b 1.3 :±:1.2 (6) a 18.0±9.0 (7) b 23.8:±: 16.9 (4) b 12.8:±: 10.2 (6) b P" @ M linearis (\) 10 92 (12) a 18.1:±:4.7 (10) a 88.9±26.1 (10) a ::r: 4.4:±:2.8 (10) a 111.4±24.3 (10) a 144.8:±:70.6 (9) a 559.9:±:243.7 (10) a (\) 15 lOO(lO)a 10.5±2.5 (10) b 64.4:±: 17.7 (10) a 2.5:±:3.1 (10) ab 77.4:±:17.1 (10) b 73.7:±:12.2 (9) a 515.1±266.5 (10) a s(\) .... 20 91 (21) a 5.7:±:2.2 (18) c 39.4:±: 16.8 (18) b 2.8:±:7.6 (18) b 45.5:±:21.1 (20) c 49.4:±:29.9 (18) b 614.2:±:361.8 (18) a 0 g: 25 80(10)a 5.8:±: 1.3 (5) c 15.6±2.1 (5) b 2.6±3.0 (5) ab 21.7:±: 11.8 (7) c 17.9:±: 10.5 (8) c 186.6±56.2 (5) a 0.: 00
a Values in the column of each species followed by the same letter were not significantly different at 5% level (Tukey-type multiple comparison test). b Means ( ±SD) in the column of each species followed by the same letter were not significantly different at 5% level by Mann-Whitney's U-test using the Bonferroni method.
.j:>. N 422 T. SATO and H. T AKADA
1oo.----..,..---, 50 1
~---- 40
50 :b ~ "0 ~
0 0 50 100 I '5 ~ ... -~ 1 rv>r····················' 50 100 50 :I ~ • r/) 25"C 30"C :I 40 40 z 10 10 ~~~-,~~--~o o~r-+-.-.-.-.-,-,-~~ 0 50 100 0 50 100 Days after adult emergence Fig. 2. Survival rate and mean number of eggs laid daily by surviving females of M. numerosus at different temperatures under a 15L-9D photoregime. 50 20"C 40 30 30 50 20 20 10 10 IJJJJJJJj...L..,----,--;,----,,-,.....-l 0 0 0 50 100 50 100 Days after adult emergence Fig. 3. Surival rate and mean number of eggs laid daily by surviving females of M. angulatus at different temperatures under a 15L-9D photoregime. at 30°C than at 20°C (Table 3, Tukey-type multiple temperature range tested (Table 3). M. numerosus comparison test, p<0.05). In M. angulatus and M. and M. angulatus laid a large number of eggs at linearis, it did not significantly differ with the tem both 20 and 25°C (Table 3). M. numerosus laid few perature examined (Tukey-type multiple compari eggs at 15 and 30°C (Fig. 2 and Table 3), and the son test, p>0.05). number of eggs was not significantly different be The preoviposition period, oviposition period, tween 15 and 25°C (Mann-Whitney's U-test by the postoviposition period, and adult longevity in Bonferroni method, p>0.05). The total number of creased with the decrease in temperature within the eggs laid by M. angulatus did not significantly dif- • Development and Reproduction of Three Hemerobiids 423 50 M. linearis 1O"C 40 30 z. 20 ~ "0 2 10 ]! cu ~ 0 ... 0 50 100 150 200 D 0 1 .8 -~100~ 1501 50 II) •. E • .-a.-. I L.. ,\..., 20"C z:J 40 " -- 40 30 30 20 20 10 0 0 0 50 100 0 50 Days after adult emergence Fig. 4. Survival rate and mean number of eggs laid daily by surviving females of M. linearis at different temperatures under a 15L-9D photoregime. fer with the temperature from 15 to 25°C (Mann angulatus. This value was similar to that for the Whitney's U-test by the Bonferroni method, same species in the present study (9.0°C). p>0.05). M linearis laid many eggs at 10°C, and The lower thermal threshold for development of the total number of eggs laid by M. linearis did not the common green lacewing, Chrysoperla carnea, differ with the temperature from 10 to 25°C (Fig. 4 was 9.5°C in a New York population, 9.8°C in an and Table 3, Kruskal-Wallis test, p>0.05). The Alaskan population, and 10.5°C in a Mexican pop total number of eggs laid did not significantly dif ulation (Tauber and Tauber, 1982). That of other fer among the three species either at 20 or 25°C, North-Central American green lacewings ranged but at l5°C M. linearis laid significantly more eggs from 9 to 13°C (Tauber et al., 1987; Albuquerque than the other two species (Table 3, Mann-Whit et al., 1994; Lopez-Arroyo et al., 1999). Aphi ney's U-test by the Bonferroni method, p<0.05). dophagous coccinellids, Coccinella septempunc tata L. and Hippodamia septemmaculata (DeGeer) had a lower thermal threshold of 10.2°C and 9.6°C DISCUSSION (Honek and Kocourek, 1988), respectively. Thus, Brown lacewings have been reported to have an brown lacewings can generally develop under extremely low lower thermal threshold for develop lower thermal conditions than other aphid preda ment, for example, Hemerobius pacificus Banks tors. (California population), 0.4°C for egg, 4.1 oc for The reproductive capacity of brown lacewings is larva, 0.6°C for pupa (Neuenschwander, 1975); very high, for example, the mean total number of Micromus tasmaniae (Walker) (Australian popula eggs laid was 715 in H. pacificus (Neuenschwan tion), -2.9°C from egg to adult (Samson and der, 1976), 933 in Micromus posticus (Walker) Blood, 1979); M tasmaniae (New Zealand popula (Miller and Cave, 1987), and 569 in M subanticus tion), 5.8°C from egg to adult (Syrett and Penman, (Walker) (Selhime and Kanavel, 1968). European 1981). Neuenschwander (1975) considered that the M. angulatus laid 252 eggs at 24-26°C (Stelzl and extremely low lower thermal threshold might be a Hassan, 1992), similar to the value of the present characteristic of Hemerobiidae. Honek and Ko study (223 eggs), although some females of a courek (1988) reported that the highest lower ther French population laid 1,500--2,000 eggs (Mier mal threshold among the brown lacewings so far mont and Canard, 1975). In the present study, the reported was 9.2°C in a Czech population of M. maximum number of eggs laid by one female was 424 T. SATO and H. TAKADA 1,201 in M. angulatus, 1,527 in M numerosus, and South America. Bioi. Contro/4: 8-13. 1,099 in M linearis. The number of eggs laid var Eilenberg, J., A. Hajek and C. Lomer (2001) Suggestions for ied greatly in all three species even under suitable unifying the terminology in biological control. BioCon tro/46: 387-400. temperatures. Garland, J. A. (1978) Reinterpretation of information on ex We evaluated suitable temperature for the activ otic brown lacewings (Neuroptera: Hemerobiidae) used ity of the three Micromus species from the results in a biocontrol programme in Canada. Manitoba Ento of survival rates for the larval and pupal stages, mol. 12: 25-28. lower thermal threshold for development, and total Honek, A. and F. Kocourek (1988) Thermal requirements for development of aphidophagous Coccinellidae number of eggs laid. The lower thermal threshold (Coleoptera), Chrysopidae, Hemerobidae (Neuroptera), for development of M. numerosus was 7.7°C. In and Syrphidae (Diptera): some general trends. Oecolo this species, the survival rate was significantly gia 76: 455-460. higher at 20°C than at any other temperature tested, Kawashima, K. (1958) Bionomics and earlier stages of some and the total number of eggs laid was high at both Japanese Neuroptera Eumicromus numerosus (Navas) 20 and 25°C. Thus, we evaluated the suitable tem (Hemerobiidae). Mushi (Fukuoka) 32: 43-47. Lopez-Arroyo, J. 1., C. A. Tauber and M. J. Tauber (1999) perature of M. numerosus as approximately 20°C. Comparative life histories of the predators Ceraeochrysa The lower thermal threshold for development of cincta, C. cubana and C. smithi (Neuroptera: Chrysopi M. angulatus was 9°C. The survival rate of this dae). Ann. Entomol. Soc. Am. 92:208-217. species did not significantly differ among tempera Miermont, Y. and M. Canard (1975) Biologie du predateur tures from 15 to 30°C. Females laid a large number aphidiphage Eumicromus angulatus (Neur.: Hemerobi idae): Etudes au laboratoire et observations dans le sud of eggs at 15, 20 and 25°C. Thus, we evaluated the ouest de Ia France. Entomophaga 20: 179-191. suitable temperature range of M. angulatus as Miller, G. L. and R. D. Cave (1987) Bionomics of Micromus 15-25°C. Unlike the other two species, M. linearis posticus (Walker) (Neuroptera: Hemerobiidae) with de could not develop at 30°C, and the lower thermal scriptions of the immature stages. Proc. Entomol. Soc. threshold for development (5.2°C) was lower in M Wash. 89: 776-789. linearis than in the other two species. The survival Monserrat, V. J. (1993) New data on some species of the genus Micromus Rambur, 1842 (Insecta: Neuroptera: rate from hatching to cocoon formation and total Hemerobiidae ). Ann. Mus. Civ. St. Nat. "G. Doria" 89: number of eggs laid did not significantly differ 477-516. among the temperatures examined. Thus, we evalu Nakahara, W (1954) Early stages of some Japanese Hemero ated the suitable temperature range of M. linearis biidae, including two new species. Kontyu (Tokyo) 21: as 10-25°C. 41-55. Nakao, S. (1962) A list of insects collected in a citrus grove The present results suggest that these three near Fukuoka City (Ecological studies on the insect com species are useful biological control agents when munity of citrus groves, IV). Kontyu (Tokyo) 30: 50-71 applied under suitable environmental conditions. (in Japanese with English summary). Particularly, M. linearis can prey on aphids, de Neuenschwander, P. (1975) Influence of temperature and hu velop and reproduce even at 10°C, a temperature at midity on the immature stages of Hemerobius pactficus. which most other aphid predators are inactive. The Environ. Entomol. 4: 215-220. Neuenschwander, P. (1976) Biology of the adult Hemerobius characteristic of activity at a low temperature pacificus. Environ. Entomol. 5: 96-100. should be useful for biological control early in the New, T. R. (1975) The biology of Chrysopidae and Hemero season, before aphid population sizes grow large biidae (Neuroptera), with reference to their usage as bio (New, 1988). control agents: a review. Trans. R. Entomol. Soc. Land. 127: 115-140. ACKNOWLEDGEMENTS New, T. R. ( 1988) Neuroptera. In Aphids Their Biology, Nat ural Enemies and Control. Vol. B. (A. K. Minks and P. We thank Dr. S. Tsukaguchi for identification of the three Harrewijn eds.). Elsevier, Amsterdam, pp. 249-258. 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Tauber (1982) Evolution of seasonal Zar, J. H. (1999) Biostatistical Analysis. 4th ed. Prentice adaptations and life history traits in Chrysopa: response Hall, Upper Saddle River, New Jersey, pp. 563-565. Bibliography of the Neuropterida Bibliography of the Neuropterida Reference number (r#): 12793 Reference Citation: Sato, T.; Takada, H. 2004 [2004.??.??]. Biological studies on three Micromus species in Japan (Neuroptera: Hemerobiidae) to evaluate their potential as biological control agents against aphids: 1. Thermal effects on development and reproduction. Applied Entomology and Zoology 39:417-425. Copyrights: Any/all applicable copyrights reside with, and are reserved by, the publisher(s), the author(s) and/or other entities as allowed by law. No copyrights belong to the Bibliography of the Neuropterida. Notes: File: File produced for the Bibliography of the Neuropterida (BotN) component of the Lacewing Digital Library (LDL) Project, 2015.