BIOLOGICAL CONTROL 4,8-13 (1994) Chrysoperla extern a (Neuroptera: Chrysopidae): 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 insect 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: Chrysoperla 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.