BIOLOGICAL CONTROL 4,8-13 (1994)

Chrysoperla extern a (: ): Life History and Potential for Biological Control in Central and South America

GILBERTO S. ALBUQUERQUE, CATHERINE A. TAUBER, AND MAURICE J. TAUBER

Department of Entomology, Comstock Hall, Cornel/University, Ithaca, New York 14853-0901

Received February 22, 1993; accepted August 9, 1993

Lizarraga, 1988) reflect the growing interest in this spe­ The predacious Chrysoperia externa (Hagen) cies, especially in Central and South America. has a number of traits that make it amenable to mass­ Every stage of biological control-from choosing an rearing and use as a biological control agent. Develop­ appropriate natural enemy, to its rearing, release, and mental and reproductive rates were relatively high and evaluation-requires prior knowledge of specific life his­ directly related to temperature between 15.6 and tory and behavioral traits. This holds true for both na­ 26. 7°C. Survival also was high throughout this tempera­ tive and exotic natural enemies. With this in mind, we ture range. Lower thermal thresholds for development examined facets of the life history of C. externa that are (t) of all immature stages fell between 11 and 12.5°C, directly relevant for developing mass-rearing tech­ and the K value for total development was 320 heat de­ niques and for predicting development and activity in gree-days above 11.8°C. At 21.1°C, oviposition aver­ the field. Our study investigated the influence oftemper­ aged 284 eggs during the first 30 days. Variability in ature and photoperiod on developmental time and sur­ diapause induction occurred within and among popula­ vival of C. externa; we also initiated studies on its repro­ tions: a proportion of the Chilean and the Brazilian pop­ ductive rate and diapause induction. Furthermore, to ulations went into diapause under a short daylength , evaluate C. externa's potential as a biological control whereas no diapause occurred in the Honduran popula­ agent, we compared its life history traits with those of a tion. Chrysoperia externa appears well suited as a bio­ commercially produced and widely used species, Chry­ logical control agent for use in pest management pro­ grams in tropical and temperate regions of Central and soperla carnea (Stephens). South America. 'c, 1994 Academic Press, Inc. MATERIALS AND METHODS KEY WORDS: externa; developmental time; survival; photoperiod; temperature; diapause; bio­ Rearing Methods logical control. All tests began with first-generation offspring of field-collected adults, unless otherwise mentioned. These adults came from three localities: Copan, Hon­ INTRODUCTION duras (14°52'N), Brasilia, DF, Brazil (15°45'S), and Ar­ ica, Tarapaca, Chile (18°30'S). Larvae were reared indi­ Chrysoperla externa (Hagen) (C. lanata) is a widely vidually in vials. Each larva had a constant surplus of distributed predator that commonly occurs in open Angoumois grain moth [Sitotroga cerealella (Olivier)] grassland habitats from the southeastern United States eggs and green peach aphids [Myzus persicae (Sulzer)]. and the Antilles to southern South America (Adams, After emergence, adults were paired in cages and pro­ 1963,1983; Tauber, 1974; Agnew et ai., 1981; Adams and vided with distilled water, a protein-carbohydrate food Penny, 1985). Its broad distribution and habitat prefer­ mixture (1:1:1:1 volumetric mixture ofWheast®, protein ence make it suitable for increased use in biological con­ hydrolysate of yeast, sugar, and honey), and cabbage trol in many countries and in a variety of cropping sys­ leaves infested with green peach aphids that produced tems, such as field and row crops and citrus orchards honeydew. To maintain high humidity inside the cages, (Olazo, 1987; Tauber and Tauber, unpublished). Recent their organdy tops were covered with a moistened cot­ studies of its life cycle and tolerance to insecticides (Ru ton pad and a plastic lid. et at., 1975; de Crouzel and Botto, 1977; Nunez, 1988; Thermal Influence on Development, Reproduction, and Ribeiro et al., 1988; Passaro et al., 1993) and progress in Survival the development of artificial diets and adult food supple­ We examined responses of C. externa to temperature ments (Botto and de Crouzel, 1979; Canedo and in a population from Honduras. On the day of oviposi-

8 1049-9644/94 $6,00 Copyright © 1994 by Academic Press, Inc. All rights of reproduction in any form reserved. LIFE HISTORY OF Chrysoperla externa 9 tion, eggs were transferred to individual vials and dis~ for fertility, i.e., number of females that laid fertile eggs tributed among five temperature conditions (15.6, 18.3, (within a period of 30 days). 21.1, 23.9, and 26.7°C), all at ±1 "C and LD 16:8. The tests began with 25 eggs/temperature condition. Daily RESULTS observations were made on the development of each im~ mature life stage, adult emergence, and reproduction. Thermal Influence on Development, Reproduction, and We refer to the prepupal stage as the period from the Survival spinning of the cocoon to the larval-pupal ecdysis, and The developmental time of all immature stages of C. the pupal stage as the period from the larval-pupal ec­ externa decreased with an increase in temperature (Ta­ dysis to the adult emergence. The preoviposition period ble 1). Total developmental time ranged from =22 days was recorded and the oviposition rate was noted daily at 26.7°C to =83 days at 15.6°C. Between 15.6 and for the first 10 days of oviposition. In addition, eggs 26.7°C, the rate of development (l/developmental time) from seven pairs of C. externa from our Honduran popu­ of each life stage, the total development, and the preovi­ lation were counted daily during the first 30 days after position period had a linear relationship with tempera­ emergence to obtain an estimate of fecundity at 21.1 "C ture (see Tables 1 and 2). No mortality occurred in the (LD 16:8). immature stages at any temperature. At the beginning The influence of temperature on C. externa's develop­ of reproduction, the oviposition rate also was directly ment was expressed by regressing the reciprocals of the related to temperature (between 18.3 and 26.7°C), and number of days for development (rates of development) most of the eggs were fertile. At 15.6°C, the oviposition of the various stages against temperature and calculat­ rate was low, and the eggs were infertile and mostly ing the regression coefficients. Linear regression lines unstalked (Table 2). At all temperature conditions, were generated with the least-squares method. A 0.01 adults cannibalized their eggs. level of significance was used in all regression tests for The theoretical threshold for development (t) for all linearity. We calculated t and K values for each stage, life stages of C. externa, including total development, for total development (oviposition to adult emergence), fell between 11 and 12.5°C (Table 1). However, the and for the preoviposition period. The lower thermal preoviposition period had a lower t value (=9°C) (Table threshold, t, was estimated by extrapolating the regres­ 2), falling below the low range obtained for other life sion lines through the x axis (temperature). The ther­ stages, The thermal requirements (K) for total develop­ mal constant, K, was derived by the equation K = (11 ment (oviposition to adult emergence) and preoviposi­ y)(x - t), where y mean developmental rate, and x tion period were 320.1 heat degree-days above 11.8°C temperature (OC). (Table 1) and 123.5 heat degree-days above 9.4°C (Ta­ ble 2), respectively. Diapause Induction Over the first 30 days of an adult female's life, ovipo­ sition at 21.1°C averaged 284.1 ± 8.7 eggs (range 251 to We attempted to induce diapause in C. externa by ex­ 310). There was no oviposition during the first 10 days. posing individuals from three widespread localities to a Subsequently the daily rate of oviposition increased rap­ variety of photoperiodic and thermal conditions, as fol­ idly, and it stabilized at about 16 eggs/day until the 30th lows: day, at which time the studies ended (Fig. 1).

(a) Copan, Honduras (second-generation offspring Diapause Induction of field-collected adults )-six combinations of two pho­ toperiods (LD 10:14 and LD 14:10) and three tempera­ Photoperiod influenced the incidence of reproductive ture conditions (constant 21.1 "C, 21.1 °C during the day diapause in the Chilean population; the percentage of and 18.3°C during the night, and a decrease from 21.1 °C oviposition was inversely related to daylength (Table 3). to 18.3°C at the pupal stage). Fertility was not evaluated in this population but the (b) Brasilia, Brazil-two regimens: short-day (LD eggs were stalked-an indication that they were fertile. 10:14) with 21.1 °C during the day and 18.3°C during the In contrast, the populations from Honduras and Brazil night and a long-day (LD 16:8) with a constant 23.9°C. that we studied showed a high percentage of oviposition (e) Arica, Chile-five constant daylengths ranging without diapause under all photoperiodic and tempera­ from LD 10:14 to 14:10, all at 23.9°C. ture conditions. Nevertheless, under a short daylength, symptoms of diapause occurred in three females and In all tests, adults were paired immediately after three males from Brazil. These adults developed the emergence and provided with distilled water and the plump, waxy appearance that is typical of diapause in protein-carbohydrate diet; sibling pairings were Chrysoperla, and oviposition was delayed for 51 to 63 avoided. Cages were checked daily for oviposition and, days postemergence. Fertility in these two populations except for the population from Chile, we also checked varied with the rearing conditions: relatively high fertil- 10 ALBUQUERQUE, TAUBER, AND TAUBER

TABLE 1 Stage-Specific Thermal Requirements for Development of C. externa from Honduras

Thermal requirements Developmental time (xNo. days ± SE) t (OC) K Stage 15.6° 18.3° 21.1 ° 23.9oa 26.7° (equation)

Egg 14.0 ± 0.1 9.2 ± 0.1 6.5 ± 0.1 5.0 ± 0.0 4.0 ± 0.0 1l.3 62.8 (25) (25) (25) (24) (25) (y = 0.016x - 0.180) 1st instar 11.1 ± 0.2 6.0 ± 0.1 4.8 ± 0.1 :3.4 ± 0.1 3.0 ± 0.0 11.1 46.1 (25) (25) (25) (24) (25) (y = 0.022x - 0.240) 2nd instar 8.9 ± 0.1 5.2 ± 0.1 3.5 ± 0.1 2.8 ± 0.1 2.0 ± 0.0 12.5 30.2 (25) (25) (25) (24) (25) (y = 0.033x - 00412) 3rd instar 12.5 ± 0.2 7.5 ± 0.2 5.2 ± 0.1 4.0 ± 0.1 3.2 ± 0.1 12.0 47.1 (25) (25) (25) (24) (25) (y = O.021x - 0.254) Prepupa 12.2 ± 0.1 7.1 ± 0.2 4.9 ± 0.1 3.3 ± 0.1 3.2 ± 0.1 11.9 43.7 (25) (25) (25) (24) (25) (y = O.023x - 0.274) Pupa 24.0 ± 0.1 1404 ± 0.2 9.8 ± 0.1 7.6 ± 0.1 6.1 ± 0.1 11.9 9004 (25) (25) (25) (24) (25) (y = O.Ol1x - 0.132) Total developmentb 82.6 ± 004 4904 ± 0.5 34.7 ± 0.2 26.1 ± 0.1 21.5 ± 0.1 11.8 320.1 (25) (25) (25) (24) (25) (y = 0.003x - 0.037) Survival (%)b 100 100 100 100 100

Note. Temperature ± 1°C; LD 16:8; number in parentheses = total number tested; initial number = 25/condition; t lower thermal threshold for development; K = thermal requirement for development, in heat degree-days. a One deformed individual excluded. b From oviposition to adult emergence.

ity occurred under a long daylength in combination with DISCUSSION a high or fluctuating temperature, whereas low fertility occurred especially under a short daylength and con­ To date, the classical approach, i.e., importation and stant temperature or under a regimen that included a release of exotic natural enemies, has dominated biologi­ decrease in temperature in the pupal stage. cal control efforts; however, the use of native natural enemies is beginning to receive increased attention. For example, a number of Chrysoperla species [e.g. C. car­ TABLE 2 nea, C. rufilabris (Burmeister), and C. comanche Influence of Temperature on Reproduction by C. externa (Banks)] are commercially reared and successfully used from Honduras

Rearing 25 temperature Preoviposition period Oviposition rate W- (OC) (x No. days ± SE)a (xNo. eggs ± SE)b en +I ~ 20 15.6 18.1 ± 1.1 ~ (10) 0 18.3 13.3 ± 1.3 8.3 ± O.n 0+ 15 (10) (10) en 21.1 12.6 ± 0.5 12.1 ± 1.1 ~ (!) (11) (11) LU 10 23.9 8.3 ± 0.8 24.0 ± 1.1 U. 0 (12) (12) a: ± LU 5 26.7 6.9 004 26.5 ± 1.2 a:J (11) (10) :2 :::> z Note. Temperature ± 1°C; LD 16:8; number in parentheses = total 0 0 10 20 30 number of pairs tested = number of ovipositing females. a Thermal requirements, i.e., t and K values, were 904 °C and 123.5 DAYS AFTER EMERGENCE heat degree-days, respectively, and the equation was y = 0.008x - 0.076. FIG. 1. Daily oviposition rate for C. externa from Copan, Hon· b Number of eggs per day at the oviposition plateau. duras during the first 30 days of adult female's life (LD 16:8, 21.1 ± " Very low numbers, all infertile. 1°C). LIFE HISTORY OF Chrysoperla externa 11

TABLE 3 Influence of Photoperiod and Temperature on Reproduction by C. externa from Three Localities (Temperature ± 1°C)

Condition Ovipositing Fertile Photoperiod Temperature No. pairs females females Locality (L:D) (OC) tested (%) ('!O)

Copan, Honduras 10:14 21.1 25 96.0 8.0 10:14 21.1 ..... 18.3" 25 92.0 4.0 10:14 21.1I18.3b 27 100.0 51.9 14:10 21.1 30 96.7 46.7 14:10 21.1 .... 18.3a 29 93.1 3.4 14:10 21.1118.3b 27 100.0 96.3 Brasilia, Brazil 10:14 21.1I18.3b 20 85.0 55.0 16:8 23.9 18 100.0 88.9 Arica, Chile 10:14 23.9 12 25.0 11:13 23.9 6 50.0 12:12 23.9 12 83.3 13:11 2:1.9 10 80.0 14:10 23.9 12 91.7

a Arrows indicate transfer of pupa from one temperature to another. b Fluctuating temperature: daytime temperature on left.

C Not tested.

in biological control where they occur naturally (see A second characteristic that makes C. externa a good New, 1975; Ridgway and Murphy, 1984; Tulisalo, 1984; candidate for mass rearing is its high reproductive po­ Breene et at., 1992). Each of these species has attributes tential (Table 2, Fig. 1). Although its preoviposition pe­ that are advantageous in mass-rearing and in specific riod is relatively long (=7 days at 26.7°C), fecundity agroecosystems (Nordlund and Morrison, 1992; Tauber under laboratory conditions approximates that of other and Tauber, 1993). Our current findings help increase Chrysoperla species, including a. carnea (see Duelli, the choices available to biological control and IPM 1984). Further investigations on the relationship be­ practitioners by providing comparative data on a rela­ tween the adults' traits (especially initiation of oviposi­ tively underused member of this group-a. externa. tion, lifetime fecundity, and survival) and temperature are necessary to establish a favorable temperature regi­ Mass Rearing men for maintaining C. externa during the adult stage. Chrysoperla externa shares another favorable charac­ Chrysoperla carnea is widely used in pest management teristic with other Chrysoperla species: adults are not programs in part because of its ease in commercial rear­ predacious and feed on honeydew and pollen (Tauber ing and the extensive knowledge of its biological traits. Our results lead us to suggest that C. externa also could be mass reared efficiently. First, immatures have excel­ TABLE 4 lent survival and short developmental time under a broad range of temperature conditions (Table 1). The A Comparison of Thermal Requirements [Heat-Degree number of heat-degree days (K) required for C. ex­ Days (K) above Threshold (t)] for Preimaginal Development of C. externa and Other Species and Geographic Populations terna's preimaginal development compares well with of Chrysoperla those for other Chrysoperla species, including various geographic populations of C. carnea (see Table 4). Such Species Locality, oN Lat. t (OC) K a comparison has limitations because various factors, such as the origin of the population, rearing procedures, C. externa Honduras, 14.5° 11.8 320.1 C. carnea Mexico, 30° 10.5 333.3a and food type, can influence the K value (see Umeya and C. carnea mohave California, 36.9 ° 10.2 358.3a Yamada, 1973; Campbell et at., 1974; Obrycki and C. carnea New York, 42.5° 9.5 376.7a Tauber, 1982; Tauber and Tauber, 1982; Tauber et at., C. carnea Alaska, 65° 9.8 300Aa 1987). However, the comparison makes clear that a. ex­ C. downesi New York, 42.5° 10.8 378.0a terna can develop as rapidly as C. carnea and conse­ C. downesi Montana, 46° 10.9 355.9a C. harrisii New York, 42.5° 12.0 b quently, its production rate can be high. Also, its produc­ 566.0

tion can be adjusted by modulating the temperature be­ a Tauber and Tauber, 1982. cause development is directly related to temperature. b Tauber and Tauber, 1974b. 12 ALBUQUERQUE, TAUBER, AND TAUBER and Tauber, 1974a; Adams and Penny, 1985). This trait chards, especially in Central and South America. This permits the use of artificial diets and reduces the cost of potential could be brought to fruition with some addi­ production (Hagen, 1987). On the other hand, our stud­ tional, well-focused research, e.g., development of eco­ ies showed that adult C. externa may cannibalize their nomical mass-rearing techniques and the analysis of eggs immediately after oviposition, regardless of temper­ certain attributes such as the host range, response of ature and food availability. From our results and those adults to supplementary food, and variability in pheno­ of Ru et al. (1975), it is clear that egg predation is not logical responses. restricted to hungry adults as suggested by Canard and Duelli (1984). Therefore, when mass rearing is planned ACKNOWLEDGMENTS for C. externa, methods to avoid or reduce egg cannibal­ ism by adults should be developed. We thank J. R. Ruberson for critically reading the manuscript; Storage constitutes another significant component of W. H. Whitcomb (Univ. of Florida) and Paul, Michael, and Agatha the mass production and distribution of natural ene­ Tauber for help in collecting specimens; and E. Fontes (EMBRAPA, mies, and a stable, predictable diapause can be a valu­ Brasilia, Brazil) for hospitality (M.J.T. and C.A.T.). We acknowledge able asset in this process (e.g., van Lenteren and Woets, the support of CNPq Fellowship 204347/89-0 from the Brazilian gov­ ernment (G.S.A.), NSF Grant BSR 88-17822 (M.J.T. and C.A.T.), 1988; Tauber et al., 1993). Our results demonstrate that and W-84 Regional Project (M.J.T. and C.A.T.). some geographic populations of C. externa undergo a reproductive diapause under certain photoperiodic and temperature conditions (Table 3). Such adults could be REFERENCES stored in a diapausing state and then brought into re­ production when necessary. However, our study demon­ Adams, P. A. 1963. of Hawaiian (Neuroptera: Chrysopidae). Proc. Hawaii. Entornol. Soc. 18, 221-223. strated within- and among-population variability in Adams, P. A. 1983. A new subspecies of Chrysoperla externa (Hagen) diapause induction; this variability should be character­ from Cocos Island, Costa Rica (Neuroptera: Chrysopidae). Bull. ized prior to the development of any storage program South. Calif. Acad. Sci. 82, 42-45. for C. externa, Adams, P. A., and Penny, N. D. 1985. Neuroptera of the Amazon basin. Part lla. Introduction and . Acta Arnazonica 15, Biological Traits in the Field 413-479. 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Bibliography of the Neuropterida

Bibliography of the Neuropterida Reference number (r#): 8154

Reference Citation: Albuquerque, G. S.; Tauber, C. A.; Tauber, M. J. 1994 [1994.??.??]. Chrysoperla externa (Neuroptera, Chrysopidae) -- life history and potential for biological control in central and South America. Biological Control 4:8-13.

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