Appl. Entomol. Zool. 36 (3): 361–366 (2001)
Effects of three aphid species (Homoptera: Aphididae) on development, survival and predation of Chrysoperla carnea (Neuroptera: Chrysopidae)
Tong-Xian Liu* and Tian-Ye Chen Vegetable IPM Laboratory, Texas Agricultural Experiment Station, Texas A&M University, Weslaco, TX 78596–8399, U.S.A. (Received 19 October 2000; Accepted 16 February 2001)
Abstract The effects of three aphid species (fourth instars only), Aphis gossypii Glover; Myzus persicae (Sulzer) and Lipaphis erysimi (Kaltenbach), on immature development, survival and predation of the common green lacewing, Chrysoperla carnea (Stephens), were determined in the laboratory. Survival rates of C. carnea from first stadium to adult emer- gence were significantly different among larvae fed different aphid species. When larvae were fed A. gossypii and M. persicae, 94.4 3.3% (mean SE) and 87.6 5.1% of individuals developed to adults, respectively; whereas only 14.9 3.4% of individuals developed to adults when fed L. erysimi. The developmental durations of C. carnea larvae were also significantly different among larvae fed the three aphid species. The developmental duration from first sta- dium to adult emergence was shortest when larvae were fed A. gossypii (19.8 0.4 d), followed by M. persicae (22.8 0.2 d), and then L. erysimi (25.5 0.4 d). The total number of fourth stadium aphids consumed by C. carnea larvae differed significantly among individuals fed different aphid species. Chrysoperla carnea consumed more A. gossypii (292.4) and M. persicae (272.6) than L. erysimi (146.4). Although total numbers of aphids consumed by the three C. carnea larval stadia differed significantly, the proportions of aphids consumed by each larval stadium to the total number of aphids consumed were similar, 3.9–7.1% by the first stadium, 12.0–16.8% by the second stadium, and 78.1–83.9% by the third stadium.
Key words: Predation, aphids, lacewings, biological control, vegetables
dramatic effects such as apparent toxicity of certain INTRODUCTION aphid species by causing high mortality, to more The common green lacewing, Chrysoperla subtle effects such as an increase in developmental carnea (Stephens), has been recorded as an effec- time, or a decrease in larval survival rate (Canard tive predator of aphids, including Aphis gossypii and Principi, 1984). Several species of aphids, Glover (Burke and Martin, 1956; Yuksel and Goc- Aphis sambuci L. (Bansch, 1964), A. nerii Boyer men, 1992; Balasubramani and Swamiappan, 1994; (Hafez and Abd-el-Hamid, 1965), Megoura viciae Zaki et al., 1999) and Myzus persicae (Sulzer) Backton (Canard, 1970), A. fabae Scopoli (Canard (Ridgway and Kinzer, 1974; Tulisalo and Tuovi- and Principi, 1984; Sengonca et al., 1987; Osman nen, 1975; Hassan, 1978; Zohdy, 1982; Hesselein and Selman, 1993), were recorded as unsuitable et al., 1993). It occurs in various agroecosystems, prey for chrysopids. including vegetables (Hoffmann and Frodsham, Cotton aphid, A. gossypii, green peach aphid, M. 1993). Chrysoperla carnea is by far the most inten- persicae, and turnip aphid, L. erysimi, are three of sively studied species of chrysopids because of its the most common and important aphid species on abundance and broad habitat range (Tauber et al., various vegetable crops in south Texas and other 2000), and it has been mass-reared and marketed states (Cartwright et al., 1987; Yue and Liu, 2000). commercially in North America and Europe (Wang High densities of aphids may stunt or kill plants in and Nordlund, 1994; Daane et al., 1998; Tauber et early stages of growth, and later on, their contami- al., 2000). nation reduces the market value of the crops Larval prey quality has considerable influence (Kennedy and Abou-Ghadir, 1979). In addition, ef- on the biology and behavior of chrysopids (Canard fective aphid control has diminished because of in- and Principi, 1984). These influences range from secticide resistance in naturally occurring popula-
* To whom correspondence should be addressed at: E-mail: [email protected]
361 362 T.-X. Liu and T.-Y. Chen tions. Although aphid control may be reestablished newly hatched larvae were individually transferred through the application of alternate or new aphici- to clear plastic petri dishes (5.5 cm in diameter, 1.5 dal compounds, biological control using preda- cm in depth) with a fine brush. A leaf disk (≈8.0 ceous lacewings is deemed desirable. cm in diameter) of either cabbage (‘Royal Van- Although C. carnea larvae are general predators, tage’) for L. erysimi or cotton (‘Stoneville 454’) for they are best known as aphid predators; their prey A. gossypii or a leaf (≈30–40 cm2) of pepper includes A. gossypii and M. persicae on vegetables (‘Jupiter’) for M. persicae was placed in each petri (Burke and Martin, 1956; Carnard and Principi, dish. A filter paper (5 cm in diameter) was placed 1984; Balasubramani and Swamiappan, 1994), but on the bottom, and a few drops of water were L. erysimi has not been recorded as prey of C. added for moisture. Only the fourth stadium aphids carnea. These three aphid species may present on were used in all experiments because the adult some vegetables at the same time in south Texas, aphids would produce neonate aphids during the but often only one or two aphid species are present. 24-h period which may be consumed by the C. Therefore, the ability of C. carnea to complete de- carnea larvae. The lacewing larvae were provided velopment and reproduce when feeding on one, a predetermined number of the appropriate aphid two or three aphid species on vegetable, particu- species daily. The numbers of fourth stadium larly L. erysimi, is critical to their sustained exis- aphids provided varied with larval stadium and tence in the vegetable ecosystem. aphid species, and ranged from a minimum of 10 The objective of this study was to determine if aphids for newly hatched larvae to a maximum of C. carnea when fed exclusively on one of the three 80 aphids for third instars. Each lacewing larva aphid species, L. erysimi, A. gossypii or M. persi- was examined daily for development and survival, cae, common on vegetables in the Lower Rio the remaining aphids were removed and counted, Grande valley (LRGV) of Texas, can successfully and the larva was supplied with fresh aphids. complete development, and if there are differences Data analysis. Prey consumption, percentage in the time required to complete development, and survival, and development duration of C. carnea in survival to adulthood. were analyzed using the general linear model (PROC GLM), and the means were distinguished using the least significant difference test (LSD) MATERIALS AND METHODS after a significant F-test at p 0.05 (SAS Institute, Aphids. Lipaphis erysimi and A. gossypii were 1996). collected from cabbage (Brassica oleraceae L.) and pepper (Capsicum annuum L.), respectively, at RESULTS the Research Farm of Texas Agricultural Experi- ment Station, Texas A&M University at Weslaco, Development Texas. Myzus persicae were collected from Chi- The durations of immature stages of C. carnea nese cabbage (Brassica sinensis L.) in McAllen, fed on A. gossypii, M. persicae and L. erysimi are Texas. All aphids were maintained in an insectary shown in Table 1 and Fig. 1. The developmental held at 25 2°C, 50–60% relative humidity, and a durations of the different larval stages varied sig- photoperiod of 16 : 8 (L : D) h, L. erysimi on cab- nificantly when the larvae fed on different aphid bage, A. gossypii on cotton, and M. persicae on species (F 3.74–18.46; df 2, 60–91; p 0.0294– pepper. 0.0001). Chrysoperla carnea larvae had the longest Lacewings. Chrysoperla carnea eggs were ob- developmental duration when the fed on L. erysimi, tained from Gardens Alive, Lawrenceburg, IN. and the shortest when fed on A. gossypii. However, Upon arrival, they were maintained in a growth the relative speed of development of larvae fed on chamber at 25 2°C, 55–60% RH, and a photope- M. persicae varied among stadia: the first stadium riod of 16 : 8 (L : D) h. Newly hatched larvae were developed as slowly as those fed on L. erysimi; the used in the experiments. second stadium developed as quickly as those fed Development, survival and predation. The ex- on A. gossypii; whereas the third instars developed periment was replicated four times, and 20 C. slower than those fed on A. gossypii but faster than carnea larvae were used in each replicate. The those fed on L. erysimi. The duration of C. carnea Predation of Chrysoperla carnea on Aphids 363
Table 1. Effects of three aphid species on C. carnea: development and survival from first stadium to adult emergence, and prey consumption by the three larval stadia
Development Survival Prey consumption Prey species (D SE)a (% SE) (Aphids/larva SE)
Aphis gossypii 19.8 0.4 c 94.4 3.3 a 292.4 18.6 a Myzus persicae 22.8 0.2 b 87.1 5.1 a 272.6 13.8 a Lipaphis erysimi 25.5 0.4 a 14.9 3.4 b 146.4 14.7 b F 25.71 119.44 25.09 p 0.0001 0.0001 0.0001 df 2, 60 2, 79 2, 94 Fig. 2. Accumulated percentage survival of C. carnea fed on three aphid species in the laboratory. a Means ( SE) followed by the same letter did not differ significantly at p 0.05 (LSD, SAS Institute, 1996).
Fig. 3. Numbers of aphids consumed by each of the three Fig. 1. Developmental durations of each immature sta- larval stadia of C. carnea fed on three aphid species in the lab- dium of C. carnea fed on three aphid species in the laboratory. oratory. development from first stadium to adult eclosion individuals that reached the third stadium pupated was longest (25.5 0.4 d) when the larvae fed on L. successfully and 94.4 3.3% of the pupae eclosed erysimi; intermediate (22.8 0.2 d) when the larvae to adults. When larvae were fed M. persicae, fed on M. persicae, and shortest (19.8 0.4 d) when 93.3 3.9% of the first instars successfully molted the larvae fed on A. gossypii (F 25.71; df 2, 60; and pupated, and 93.7 3.6% of the pupae eclosed p 0.0001). to adults. In contrast, when larvae were fed L. erysimi, only 82.6 7.4% of the first instars molted Survival to the second stadium, 89.5 5.4% of the second Percentages of survival of immature stages of C. instars molted to the third stadium, 80.8 6.9% of carnea are shown in Table 1 and Fig. 2. The per- the third instars pupated, and 25.0 3.2% of the centage of immatures surviving from the first sta- pupae eclosed to adults. dium to the adult stage differed significantly among larvae fed different aphid species (F Prey consumption 119.4; df 2, 9; p 0.0001). When fed on A. The quantities of A. gossypii, M. persicae and L. gossypii and M. persicae, 94.4 3.3% and 87.4 erysimi consumed by C. carnea are shown in Table 5.1% of the larvae developed to adults, respec- 1 and Fig. 3. The number of aphids consumed by tively, compared with only 14.9 3.4% of those fed first instars differed significantly among the three L. erysimi. When larvae were fed A. gossypii, all aphid species (F 5.49; df 2, 97; p 0.0055). The 364 T.-X. Liu and T.-Y. Chen
first instars consumed more A. gossypii (14.9 1.3) reduced to as low as 14.9% when larvae fed on L. than M. persicae (10.7 0.8) or L. erysimi (10.4 erysimi, compared with 94.4% and 87.4% when 1.0) with no difference between the two latter the larvae fed on A. gossypii and M. persicae, re- aphid species. The numbers of aphids consumed by spectively. Although C. carnea larvae could accept second instars varied greatly among the three aphid L. erysimi as prey, a low survival rate (75.0%) oc- species. Each larva consumed an average of curred during the cocoon stage and during imagi- 49.1 4.4 A. gossypii (maximum), 32.7 2.9 M. nal ecdysis. persicae (intermediate) and 21.1 2.9 L. erysimi Host plants on which the aphids fed might affect (minimum). The third instars consumed as many A. the quality of the aphids, which in turn, may affect gossypii (228.3 18.7) as M. persicae (228.8 the development, survival and predation of C. 12.7), but fewer L. erysimi (115.4 12.6) (F carnea. Legaspi et al. (1996) measured the effect 18.71; df 2, 94; p 0.0001). Compared with the of host plants on the body weight, developmental total numbers of aphids consumed per larva of first duration and survival of C. rufilabris, and found to third instars, C. carnea consumed about equal that lacewings fed silverleaf whitefly, Bemisia ar- numbers of A. gossypii (292.4 18.6) and M. persi- gentifolii Bellows & Perring, reared on cucumber cae (272.6 13.8), but remarkably fewer L. erysimi (Cucumis sativus L.) and cantaloupes (Cucumis (146.4 14.7) (F 25.09; df 2, 94; p 0.0001). melo L.) developed more rapidly, showed increased Although the number of aphids consumed by each survival, and weighed more as newly-emerged of the three C. carnea larval stadia differed signifi- adults, compared with those reared on poinsettia cantly, the proportion of aphids consumed by each (Euphorbia pulcherrima Willd.) and lima bean larval stadium to the total number of aphids con- (Phaseolus limensis L.). Balasubramani and sumed by all larval stadia was similar, 3.9–7.1% by Swamiappan (1998) found that the larvae of C. the first stadium, 12.0–16.8% by the second sta- carnea, a congeneric species of C. rufilabris, that dium, and 78.1–83.9% by the third stadium. fed on A. gossypii developed faster on cowpea and groundnuts than on other host plants. It appears that L. erysimi reared on cabbage might be nutri- DISCUSSION tionally inadequate for C. carnea, or the cabbage The results of this study indicate that the three plants may even have an accumulative toxic effect aphid species significantly affected the develop- on the predators. In addition, the presence of a thin ment and survival of C. carnea, as well as the num- white waxy powder on L. erysimi’s body may affect ber of aphids consumed by the larvae. In our study, prey preference, development and survival of C. the development time of C. carnea larvae was carnea larvae. Some aphid species may be toxic to shortest when fed on A. gossypii, intermediate on natural enemies. For example, the cardiac glyco- M. persicae, and longest on L. erysimi. Hydorn and sides present in the orleander aphid, A. nerii, is Whitcomb (1979) found that C. rufilabris highly toxic to predators, including C. carnea (Burmeister) fed on Drosophila melanogaster (Rothschild et al., 1970). Meigen adults resulted in full-grown larvae, but The quantity of prey consumed by C. carnea de- failure to spin cocoons. Canard and Principi (1984) pends on the prey species, size and the stage of- reported that first stadium Chrysopa perla (L.) had fered. Information in the literature can not be eas- a low survival rate when they fed on A. fabaei. ily compared because the aphid species, stages and Osman and Selman (1993) also found that M. per- the host plants on which the aphids were reared sicae and Acyrthosiphon pisum (Harris) were more were different. In general, the numbers of aphids suitable to C. carnea, whereas A. fabae caused consumed in this study are comparable to those re- higher larval mortality, smaller cocoons, and lower ported previously. C. carnea fed on as few as 208 fecundity than M. persicae. Similarly, Sengonca et A. gossypii (Burke and Martin, 1956) (reported as al. (1987) found that when C. carnea larvae fed on C. plorabunda Fitch) to as many as 419 (Balasub- A. fabae, adult mortality was high. As found in this ramani and Swamiappan, 1994) and 487 (Afzal study, A. gossypii and M. persicae did not cause and Khan, 1978), and as few as 128 female apter- significant reduction in C. carnea larval survival. ous M. persicae to as many as 386 nymphs (Hafez In contrast, larval survival rates were significantly and Abd-el-Hamid, 1965). Predation of Chrysoperla carnea on Aphids 365
In conclusion, C. carnea has great potential as a havior. In Biology of Chrysopidae (M. Canard, Y. Seme- predator of A. gossypii and M. persicae. However, ria and T. R. New eds.). Dr W. Junk Publishers, The due to the severe effects of L. erysimi on larval and Hague, pp. 57–149. Cartwright, B., J. V. Edelson and C. Chambers (1987) Com- pupal survival of C. carnea and the limited con- posite action thresholds for the control of lepidopterous sumption, it should not be considered as an effec- pests on fresh-market cabbage in the Lower Rio Grande tive biological agent for this species of aphid on Valley of Texas. J. Econ. Entomol. 80: 175–181. cabbage. The ability of C. carnea to successfully Daane, K. M., K. S. Hagen and N. J. Mills (1998) Predaceous complete development on these three aphid species insects for insects and mite control. In Mass-Reared Nat- ural Enemies: Application, Regulation, and Needs (R. L. common in the LRGV agroecosystem suggests the Ridgway, M. P. Hoffmann, M. N. Inscoe and C. S. Glenis- potential for the chrysopid to survive when one or ter eds.). Thomas Say Publ. Entomol., Entomol. Soc. more aphid species are absent. Besides aphids, C. Am., Lanham, MO, pp. 61–115. carnea also attacks lepidopterous eggs and other Hafez, M. and A. Abd-el-Hamid (1965) On the feeding habits soft bodied-prey (Alrouechdi and Voegelé, 1981). of the aphid lion Chrysopa vulgaris Schn. Agric. Res. While the ability to survive on a broad range of Rev. Cairo 43: 37–46. Hassan, S. A. (1978) Releases of Chrysopa carnea Step. to prey is insufficient to ensure that the chrysopid can control Myzus persicae (Sulzer) on eggplant in small establish and continue to suppress these aphids and greenhouse plots. Zeitschrift Pflanzenkrankheiten und other prey, it is a desirable characteristic for suc- Pflanzenschutz 85: 118–123. cessful exploitation of this ecosystem. Hesselein, C., K. Robb, J. Newman, R. Evans and M. P. Par- rella (1993) Demonstration/integrated pest management ACKNOWLEDGEMENTS program for potted chrysanthemums in California. Bull. OILB/SROP 16: 71–76. We would like to thank J. C. Legaspi (Texas Agricultural Hoffmann, M. P. and A. C. Frodsham (1993) Natural Enemies Experiment Station, Weslaco) and J. V. French (Citrus Center, of Vegetable Insect Pests. A Cornell Coop. Ext. Publ., Texas A & M University Kingsville, Weslaco) for review of Cornell Univ., Ithaca, NY. 63 pp. this manuscript. This paper was approved for publication by Hydorn, S. B. and W. H. Whitcomb (1979) Effects of larval the Center Director of Texas Agricultural Research and Exten- dits on Chrysopa rufilabris. Fla. Entomol. 62: 293–298. sion Center at Weslaco, and the Head of the Department of Kennedy, G. G. and M. F. Abou-Ghadir (1979) Bionomics of Entomology, Texas A&M University, College Station. the turnip aphid on two turnip cultivars. J. Econ. Entomol. REFERENCES 72: 754–757. Legaspi, J. C., D. A. Nordlund and B. C. Legaspi, Jr. (1996) Afzal, M. and M. R. Khan (1978) Life history and feeding be- Tri-trophic interactions and predation rates in Chrysop- havior of green lacewing Chrysopa carnea Steph. (Neu- erla spp. attacking the silverleaf whitefly. Southwest. En- roptera: Chrysopidae). Pakist. J. Zool. 10: 83–90. tomol. 21: 33–42. Alrouechdi, K. and J. Voegelé (1981) Prédation des tri- Osman, M. Z. and B. J. Selman (1993) Suitability of different chogrammes par les chrysopides. Agronmie 1: 187–189. aphid species to the predator Chrysoperla carnea Balasubramani, V. and M. Swamiappan (1994) Development Stephens (Neuroptera: Chrysopidae). Univ. J. Zool., Ra- and feeding potential of the green lacewing Chrysoperla jshahi Univ. 12: 101–105. carnea Steph. (Neur. Chrysopoidae) on different insect Ridgway, R. L. and R. E. Kinzer (1974) Chrysopids as preda- pests of cotton. Anzeiger Schadlingskunde Pflanzenschutz tors of crop pests. Entomophaga 7: 45–51. Umweltschutz 67: 165–167. Rothschild, M., J. von Euw and T. Reichstein (1970) Cardiac Balasubramani, V. and M. Swamiappan (1998) Suitability of glycosides in the orleander aphid Aphis nerii (Ho- groundnut aphid Aphis craccivora Koch for rearing green moptera: Aphididae). J. Insect Physiol. 16: 1141–1145. lacewing Chrysoperla carnea Stephens. Intern. Arachis SAS Institute (1996) SAS/STAT User Guide, Version 6.03. Newsletters 18: 30–31. Cary, NC. Bansch, R. (1964) Verleichende Untersuchungen zur Biologie Sengonca, C., S. Gerlach and G. Melzer (1987) Effect of feed- und zum beute fangverhalten aphidivorer Coccinelliden, ing with different prey on Chrysoperla carnea (Stephens) Chrysopidan und Syrphiden. Zool. Jb., Syst. Okol. Geogr. (Neuroptera: Chrysopidae). Zeitschrift Pflanzenkrankhei- Tiere 91: 271–340. ten Pflanzenschutz 94: 197–205. Burke, H. R. and D. F. Martin (1956) The biology of three Tauber, M. J., C. A. Tauber, K. M. Daane and K. S. Hagen chrysopid predators of the cotton aphid. J. Econ. (2000) Commercialization of predators: recent lessons Entomol. 49: 698–700. from green lacewings (Neuroptera: Chrysopidae: Canard, M. (1970) The bearing of the nutritive value of vari- Chrysoperla). Am. Entomol. 46: 26–38. ous aphids (Homoptera, Aphididae) on the potential rate Tulisalo, U. and T. Tuovinen (1975) The green lacewing, of increase of Chrysopa perla (L.) (Neuroptera, Chrysop- Chrysopa carnea Steph. (Neuroptera, Chrysopidae), used idae). Ann. Zool. Ecol. Anim. 3: 345–355. to control the green peach aphid, Myzus persicae Sulz., Canard, M. and M. M. Principi (1984) Life histories and be- and the potato aphid, Macrosiphum euphorbiae Thomas 366 T.-X. Liu and T.-Y. Chen
(Homoptera, Aphididae), on greenhouse green peppers. dae) as a predator on cotton aphid Aphis gossypii Glov. Ann. Entomol. Fennici 41: 94–102. (Homoptera, Aphididae). In Proc. Second Turkish Nat. Wang, R. and D. A. Nordlund (1994) Use of Chrysopela spp. Congr. Entomol., Ege Univ., Izmir, Turkey, pp. 209–216. (Neuroptera: Chrysopidae) in augmentative release pro- Zaki, F. N., M. F. El-Shaarawy and N. A. Farag (1999) Release grammes for control of arthropod pests. Biocontrol News of two predators and two parasitoids to control aphids and Inf. 15: 51–57. whiteflies. Anzeiger Schadlingskunde Pflanzenschutz Um- Yue, B. and T.-X. Liu (2000) Host selection, development, sur- weltschutz 72: 19–20. vival and reproduction of turnip aphid (Homoptera: Aphi- Zohdy, N. Z. M. (1982) Suitability of Myzus persicae for the didae) on green and red cabbage varieties. J. Econ. Ento- development of Chrysopa carnea as affected by changing mol. 93: 1308–1314. prey food. Res. Bull., Fac. Agric., Ain Shams Univ. 1810: Yuksel, S. and H. Gocmen (1992) The effectiveness of 1–13. Chrysoperla carnea (Stephens) (Neuroptera, Chrysopi-