Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae)

Biological Control 43 (2007) 163–170 www.elsevier.com/locate/ybcon

Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae) M.L. Pappas a, G.D. Broufas b, D.S. Koveos a

a,*

Aristotle University of Thessaloniki, School of Agriculture, Laboratory of Applied Zoology and Parasitology, 541 24 Thessaloniki, Greece b Department of Agricultural Development, Democritus University of Thrace, Pantazidou 193, 68 200 Orestiada, Greece Received 19 January 2007; accepted 14 July 2007 Available online 6 August 2007

Abstract The effects of different prey species on preimaginal development and survival, as well as on adult longevity and fecundity of the predatory lacewing Dichochrysa prasina Burmeister were studied under laboratory conditions. The prey species tested were the aphids Aphis fabae Scopoli, Aphis nerii Boyer de Fonscolombe, Aphis pomi De Geer, Hyalopterous pruni Geoffroy, Macrosiphum rosae (L.) and Myzus persicae (Sulzer), the ‘‘two spotted spider mite’’ Tetranychus urticae Koch, the ‘‘moth’’ Ephestia kuehniella (Zeller) and the ‘‘beetles’’ Tribolium confusum Duval and Tenebrio molitor (L.). Eggs of E. kuehniella and nymphs of M. persicae were the most favorable among the tested prey, resulting in high survival and short developmental time of preimaginal stages as well as in increased adult longevity and fecundity of D. prasina. Larvae of T. molitor were less favorable, resulting in a decrease of adult longevity and fecundity of D. prasina. Among the other prey studied, nymphs of A. fabae, A. pomi, H. pruni and M. rosae, nymphs and adults of T. urticae, and larvae of T. confusum were the least favorable for development, whereas nymphs of A. nerii did not allow the completion of larval development of D. prasina. These results could be useful for mass-rearing of D. prasina and for understanding its population dynamics in the field in relation to the availability of certain prey species.  2007 Elsevier Inc. All rights reserved. Keywords: Lacewings; Dichochrysa prasina; Aphis fabae; Aphis nerii; Aphis pomi; Hyalopterous pruni; Macrosiphum rosae; Myzus persicae; Tetranychus urticae; Ephestia kuehniella; Tribolium confusum; Tenebrio molitor; Prey; Development; Demography

1. Introduction Lacewings of the family Chrysopidae are polyphagous predators and important biological control agents of aphids and other soft-bodied phytophagous insects. Certain chrysopid species mainly of the genus Chrysoperla have been successfully mass-reared and used in biological control programs either in greenhouses or in the field (New, 1988). Several other chrysopids, such as Dichochrysa spp. could also have an important role as biocontrol agents in agroecosystems either through conservation of indigenous populations or through inundative and augmentative *

Corresponding author. Fax: +30 2310998845. E-mail address: [email protected] (D.S. Koveos).

1049-9644/$ - see front matter  2007 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2007.07.006

releases (Daane, 2001). Approximately 122 Dichochrysa species have been described with a world-wide distribution (Aspo¨ck et al., 1980; Brooks and Barnard, 1990; Dong et al., 2004). They have been found in diverse habitats such as field crops, fruit orchards, vegetables, forests and meadows (Greve, 1984; New, 1984; Se´me´ria, 1984; Zeleny´, 1984; Duelli, 2001; Szentkira´lyi, 2001a, b). Dichochrysa larvae are trash-carriers and prey upon soft-bodied arthropods, whereas the adults feed mainly on honeydew and pollen (Principi and Canard, 1984; Bozsik, 1992, 2000; Canard, 2001). The lacewing Dichochrysa prasina (Burmeister) is a widely distributed and abundant species recorded at Palearctic, Oriental and African regions (Se´me´ria, 1984; Dong et al., 2004). In Europe D. prasina has been found in a

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M.L. Pappas et al. / Biological Control 43 (2007) 163–170

variety of diverse habitats including coniferous forests, fruit orchards, field crops, vegetables and ornamental plants (Principi, 1956; Se´me´ria, 1984; Zeleny´, 1984). In Greece, D. prasina is one of the most abundant indigenous chrysopid species in orchards, vegetables and field crops (Canard and Laude´ho, 1977; Santas, 1984; Souliotis and Broumas, 1994; Thierry et al., 2005). The nutritional ecology, prey preference and food requirements for development and reproduction of D. prasina have not been studied. A number of stored-food insect species have been used as prey for rearing predatory insects mainly because they are easily reared in the laboratory. The eggs of the moth Ephestia kuehniella (Zeller) are one of the most frequently used prey for mass-rearing chrysopids such as Chrysoperla species because it ensures rapid growth and development, high fecundity and survival (Lo´pez-Arroyo et al., 1999b; Tauber et al., 2000). The eggs and young larvae of other stored-food insects such as Tribolium castaneum (Herbst) and Tenebrio molitor (L.) have also been used for rearing chrysopid and pentatomid species, respectively (Hydorn and Whitcomb, 1979; Kubota and Shiga, 1995; Zanuncio et al., 1996; Vivan et al., 2003; Legaspi and Legaspi, 2004). Larvae of D. prasina can feed on eggs of certain Lepidoptera pests (Babrikova, 1979). However, the suitability of Lepidoptera eggs to sustain development and reproduction of D. prasina has not been evaluated. Larvae of D. prasina are polyphagous predators that feed on a variety of prey species including aphids, mites and eggs of Lepidoptera (Babrikova, 1979). The relative suitability for D. prasina of different types of prey either encountered in the field or offered for mass-rearing purposes has not been studied. We assessed three types of prey (E. kuehniella eggs and young larvae of Tribolium confusum and T. molitor) for rearing larvae under laboratory conditions and tested their effects on survival, development and reproduction of D. prasina. In addition, we evaluated the suitability as prey of six different aphid species and a phytophagous mite that coexist with D. prasina in the field. The adults of D. prasina are known to feed on honeydew and pollen (Bozsik 1992, 2000). Therefore, we tested the effect of different prey species during larval development on the female longevity and fecundity. The results may be useful either for laboratory mass-rearing of D. prasina or for understanding its population dynamics in the field in relation to the availability of different prey species.

cae (Sulzer) nymphs and adults offered daily as prey. The stock colony was maintained in a climatic room at 25 ± 1 C and a photoperiod of 16:8 LD. First-generation offspring of the field-collected adults were used in the experiments. Voucher specimens have been deposited at the National Museum of Natural History in Sofia (Bulgaria) and at the personal collection of Prof. A. Bozsik (University of Debrecen, Hungary). 2.2. Prey species In the experiments preimaginal developmental rate and survival, adult longevity and fecundity of D. prasina were determined when larvae preyed upon various insect and mite species. Nymphs of six aphid species namely Aphis fabae Scopoli, Aphis nerii Boyer de Fonscolombe, Aphis pomi De Geer, Hyalopterous pruni Geoffroy, Macrosiphum rosae (L.) and M. persicae (Sulzer) and nymphs and adults of the ‘‘two spotted spider mite’’ Tetranychus urticae Koch which are commonly found with D. prasina in the field and could be potential prey species were tested in the experiments. In addition, eggs of the ‘‘moth’’ E. kuehniella (Zeller) and larvae of the ‘‘beetles’’ T. confusum Duval and T. molitor (L.) known stored-food insects were also tested. Nymphs of A. fabae and M. persicae used in the experiments were collected from laboratory colonies which were maintained in an insectary on potted broad bean (Vicia faba L., cv. Negreta) and radish plants (Raphanus sativus L., cv. Saxa), respectively, at 25 ± 1 C and a photoperiod of 16:8 LD. Nymphs of the other aphid species were collected from field on infested host plants grown on the University Campus. More specifically, A. nerii nymphs were collected from oleander plants (Nerium oleander L.), A. pomi from apple trees (Malus communis L. cv. Golden Delicious) and M. rosae from roses (Rosa spp.). In addition, T. urticae individuals were collected from a laboratory colony which has been maintained for several years on detached bean leaves (Phaseolus vulgaris L., cv. Processor), as described by Veerman and Koveos (1989). Larvae of T. confusum and T. molitor were collected from laboratory colonies maintained on wheat flour and bran, respectively. Eggs of E. kuehniella were UV-sterilized and purchased from Biotop (Valbonne, France). 2.3. Effect of prey species on immature development and survival

2. Materials and methods 2.1. Stock colony of D. prasina Our stock colony of D. prasina was established with adults collected with a hand net from cotton fields in the area of Alexandrea, Northern Greece. Adults were maintained in cylindrical plastic cages (20 · 15 cm) and had access to water and a liquid diet consisting of 1:1:1:1 water, yeast hydrolysate, sugar and honey. Larvae were reared in plastic boxes (7 · 14 · 9.5 cm) with plenty of Myzus persi-

For the experiments eggs of D. prasina were collected from the stock colony daily for three to five consecutive days and maintained each in an eppendorf tube at 25 ± 1 C and 16:8 LD. Every 2 h the eggs were inspected and newly hatched larvae were transferred individually with the help of a fine hair brush into a plastic Petri dish (5.5 cm in diameter). In order to ensure proper ventilation inside the Petri dish, a hole 1.5 cm in diameter was opened through the lid and covered by thin gauze. A constant surplus of each prey was placed daily in each Petri dish. Specifically, more than

M.L. Pappas et al. / Biological Control 43 (2007) 163–170

200 spider mites of various developmental stages or approximately 120 third and fourth instar aphid nymphs were offered daily to each chrysopid larva throughout larval development. Considering the non-prey species, a constant surplus of E. kuehniella frozen eggs (0.5 g) or four second instar mechanically injured larvae of T. confusum or T. molitor were offered daily to each lacewing larva. Every 12 h larval developmental stage and survival were recorded. All the experiments were carried out at 25 ± 1 C and a photoperiod of 16:8 LD. For each treatment (prey species tested) 50–80 newly hatched lacewing larvae were tested but only those that completed their development were included in data analysis (Table 1). In the case of T. confusum, two groups of 80 newly hatched D. prasina larvae with one week interval period (i.e. a total of 160 individuals) were tested. In further data analysis each larva of D. prasina has been considered as one replicate. 2.4. Effects of larval prey species on adult longevity and fecundity Females and males fed throughout their larval development on different prey species were transferred in pairs on the day of emergence and maintained in cylindrical plastic cages (volume 350 ml) where they had continuous access to water and a liquid diet as described above for the stock colony. The number of eggs laid by each female and female survival was recorded daily. Males that died were replaced with young ones. Egg hatchability was estimated in a similar way with that described by Lo´pez-Arroyo et al., (1999a). Due to the large number of treatments and exper-

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imental pairs, once a week during the first thirty days of the oviposition period (a total of three sampling dates), 15 randomly chosen eggs laid by each female were collected and transferred individually in plastic Petri dishes. Subsequently, eggs were maintained under the same temperature and photoperiodic conditions with the parental females. Daily eggs were inspected and the number of newly hatched larvae was recorded. The percentages of egg hatching at each sampling date were estimated for eggs laid by all tested females. 2.5. Data analysis Analysis of variance (ANOVA) was used to compare the effect of prey species on developmental time of D. prasina. Log transformation of data was used to minimize variances, and means were compared using Student–Newman–Keuls test (P = 0.05) with the procedure of SPSS 12 V (SPSS, 2005). Within each treatment the t-test was used to compare total developmental times in females and males. The chi-square test was used for all possible pair-wise comparisons of survival percentages for different prey species (P = 0.05). The type-I error was corrected using the Bonferroni method (Sokal and Rohlf, 1995). Analysis of variance (ANOVA) was used to compare longevity and fecundity of females as well as egg hatchability in the different treatments. Means were compared using Student–Newman–Keuls test (P = 0.005) (SPSS, 2005). Before analysis of variance data were subjected to log or arcsin (in the case of egg hatchability) transformation to minimize variances between different treatments.

Table 1 Mean developmental time (±SE) (days) of preimaginal developmental stages of D. prasina when fed on different prey at 25 C and 16:8 LD Prey

na

Developmental time (days) 1st instar

2nd instar

3rd instar

Prepupa

Pupa

Overall

9.0 ± 0.3a 10.8 ± 0.4c 7.6 ± 0.2b 7.7 ± 0.3b 7.8 ± 0.4b 9.1 ± 0.4a 7.7 ± 0.2b 7.2 ± 0.5b 9.4 ± 0.4a

32.1 ± 0.5a 31.1 ± 0.5a 33.6 ± 0.6ab 35.8 ± 0.7bc 37.0 ± 0.8cd 39.5 ± 1.2d 38.9 ± 0.7d 50.3 ± 0.9e 48.9 ± 0.9e

Females M. persicae E. kuehniella T. molitor H. pruni M. rosae A. fabae A. pomi T. urticae T. confusum

18 16 16 17 15 16 19 20 20

5.4 ± 0.2a 6.0 ± 0.2bc 4.6 ± 0.1g 6.4 ± 0.3cd 5.5 ± 0.3ab 7.1 ± 0.2de 6.7 ± 0.2cd 9.4 ± 0.5f 7.6 ± 0.2e

5.9 ± 0.3a 4.7 ± 0.2d 7.2 ± 0.2b 8.9 ± 0.4c 8.8 ± 0.6c 7.5 ± 0.3b 6.1 ± 0.3a 7.5 ± 0.3b 9.1 ± 0.3c

7.6 ± 0.4a 6.3 ± 0.3f 9.3 ± 0.5bd 8.4 ± 0.4ab 10.3 ± 0.7bd 9.9 ± 0.5bd 8.2 ± 0.4ab 12.3 ± 0.7e 10.8 ± 0.4de

4.5 ± 0.2a 3.4 ± 0.1e 4.9 ± 0.3ab 4.3 ± 0.2a 4.5 ± 0.2a 5.4 ± 0.3bc 4.6 ± 0.2a 8.0 ± 0.4d 5.9 ± 0.3c

Males M. persicae E. kuehniella T. molitor H. pruni M. rosae A. fabae A. pomi T. urticae T. confusum

20 20 18 18 15 14 16 17 19

4.9 ± 0.2a 4.8 ± 0.2a 4.3 ± 0.1a 7.6 ± 0.5b 6.5 ± 0.4b 7.1 ± 0.3b 6.6 ± 0.2b 7.4 ± 0.2b 7.2 ± 0.2b

6.6 ± 0.3a 4.6 ± 0.1d 6.7 ± 0.2a 7.3 ± 0.2ab 7.1 ± 0.3ab 6.4 ± 0.4a 6.1 ± 0.4a 8.0 ± 0.4bc 8.7 ± 0.4c

5.9 ± 0.5a 5.6 ± 0.2a 6.3 ± 0.4a 8.6 ± 0.5b 8.4 ± 0.9b 9.4 ± 0.8b 8.3 ± 0.7b 9.1 ± 0.5b 8.7 ± 0.4b

5.1 ± 0.2ab 4.2 ± 0.2d 5.5 ± 0.2b 4.4 ± 0.1ad 4.5 ± 0.2ad 5.4 ± 0.2b 4.2 ± 0.2d 8.2 ± 0.4c 5.0 ± 0.2ab

8.1 ± 0.4abc 7.1 ± 0.2a 7.3 ± 0.2a 7.7 ± 0.2ab 8.1 ± 0.2abc 9.3 ± 0.3c 7.1 ± 0.3a 6.1 ± 0.5d 8.7 ± 0.3bc

Means within a column followed by the same letter are not significantly different at P = 0.05 by Student–Newman–Keuls test. a Number of individuals tested.

30.8 ± 0.9a 26.4 ± 0.4b 30.3 ± 0.4a 35.5 ± 0.9cd 34.7 ± 1.3c 37.5 ± 1.2d 37.9 ± 1.1d 44.5 ± 0.6e 44.5 ± 1.0e

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2.6. Demographic parameters

(F = 123.79; df = 8, 296; P < 0.001) and the sex (F = 53,28; df = 1, 296; P < 0.001). Since none of the tested chrysopid larvae completed their development when fed on A. nerii, this treatment was not included in data analysis. As shown in Table 1 the different prey species tested significantly affected the duration of each preimaginal developmental stage and the mean total developmental time both in females (1st instar larva F = 30.653; df = 8, 148; P < 0.001; 2nd instar larva F = 19.960; df = 8, 148; P < 0.001; 3rd instar larva F = 15.494; df = 8, 148; P < 0.001; prepupa F = 29.850; df = 8, 148; P < 0.001; pupa F = 10.415; df = 8, 148; P < 0.001; total immature development F = 75.915; df = 8, 148; P < 0.001) and males (1st instar larva F = 26.437, df = 8, 148; P < 0.001; 2nd instar larva F = 16.147; df = 8, 148; P < 0.001; 3rd instar larva F = 9.676; df = 8, 148; P < 0.001; prepupa F = 22.708; df = 8, 148; P < 0.001; pupa F = 10.193; df = 8, 148; P < 0.001; total immature development F = 55.801; df = 8, 148; P < 0.001). For both females and males the mean larval developmental period was significantly shorter when they were reared on E. kuehniella eggs, M. persicae nymphs and T. molitor larvae than on the other prey species tested (Table 1). The mean larval developmental time did not differ significantly between females and males when fed on each of the different aphids tested (0.23 6 t 6 1.53; 33 6 df 6 36; 0.138 6 P 6 0.821). However, the total preimaginal developmental time was shorter in males than in females when chrysopid larvae were fed on T. urticae individuals (t = 4.97; df = 35; P < 0.001), T. confusum larvae (t = 3.26; df = 37; P < 0.005), T. molitor larvae (t = 4.59; df = 32; P < 0.001) and E. kuehniella eggs (t = 7.481; df = 34; P < 0.001). As shown in Table 2, the percentage of individuals that completed the egg to adult development was significantly affected by prey species (v2 = 76.2; df = 8). It was high when the lacewings fed on nymphs of M. persicae, eggs of E. kuehniella or young larvae of T. molitor, intermediate when fed on nymphs of the other four aphid species and on nymphs of T. urticae and low when fed on larvae of T. confusum.

Life and fertility table parameters were estimated by combining data from preimaginal development, adult survival, and reproduction experiments, as described by Wang and Tsai (2001). The intrinsic rate of population increase was estimated by iteratively solving the equation given by Birch (1948): n X

erx lx mx ¼ 1

x¼0

where x is the mean age class, mx the mean number of female progeny per female of age x and lx the probability of survival to age x. A trial number of values for r were substituted into equation until rm value for which the sum on the left side of the equation approximates unity. In data analysis we assumed a 1:1 sex ratio and this assumption is justified since our rearing experiment yielded approximately equal numbers of males and females (0.013 < v2 < 0.223, v21,0.05 = 3.84; P > 0.05). The Jacknife procedure was used to estimate a standard error for the rm values at different treatments (Meyer et al., 1986). The rm values were compared by Student–Newman– Keuls test (Sokal and Rohlf, 1995) as described by Broufas and Koveos (2001). Further data analysis was used to calculate the net reproductive rate (R0 = Rlxmx, number of female offspring produced per female), mean generation time (T = lnR0/rm, in days), doubling time (DT = ln2/rm, number of days required for the population to double its numbers) and finite rate for increase (k = erm, number of times the population will multiply itself per unit of time) (Birch, 1948; Southwood, 1978). 3. Results 3.1. Effect of prey species on immature development and survival Two-way analysis of variance revealed that total developmental time was significantly affected by the prey species

Table 2 Preimaginal survival, mean female adult longevity (days) (±SE) and mean total fecundity (eggs/female) (±SE) of D. prasina fed on different prey, at 25C and 16:8 LD

M. persicae E. kuehniella T. molitor H. pruni M. rosae A. fabae A. pomi T. urticae T. confusum a b c d

na

Preimaginal survivalb

Numberc of females

Longevity

Fecundity

50 50 50 80 80 80 80 80 160

76.0 72.0 68.0 43.8 37.5 37.5 43.8 46.3 24.4

18 16 16 17 15 16 19 20 20

51.56 ± 2.85ab 54.00 ± 3.89ab 38.50 ± 1.17b 54.35 ± 4.18ab 50.53 ± 4.21ab 44.88 ± 3.01ab 56.32 ± 2.57a 45.10 ± 3.11ab 39.50 ± 1.92b

377.89 ± 30.97ad 521.56 ± 40.64b 191.75 ± 13.22c 318.06 ± 47.26ac 253.93 ± 31.23c 205.31 ± 39.73ac 269.58 ± 38.63c 200.45 ± 23.84c 198.20 ± 24.89c

Initial number of newly hatched larvae tested. 100· (total number of emerging adults/initial number of newly hatched larvae tested). Number of females tested. Means within a column followed by the same letter are not significantly different at P = 0.05 by Student–Newman–Keuls test.

M.L. Pappas et al. / Biological Control 43 (2007) 163–170 20 16 12 8 4 0

0

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

20 16 12 8 4 0

0

1.0 M. persicae 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

0

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

0

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

0

1.0 20 0.8 16 H. pruni 0.6 12 0.4 8 0.2 4 0.0 0 10 20 30 40 50 60 70 80 90 0

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

0

1.0 20 0.8 16 0.6 12 0.4 8 0.2 4 0.0 0 10 20 30 40 50 60 70 80 90 0

20 16 12 8 4 0

A. fabae

mx

20 16 12 8 4 0 20 16 12 8 4 0

M. rosae

A. pomi

T. urticae

20 16 12 8 4 0

T. confusum

lx

20 16 12 8 4 0

E. kuehniella

1.0 0.8 0.6 0.4 0.2 0.0 10 20 30 40 50 60 70 80 90

167

species. The effect of prey species was even more pronounced on fecundity which varied from approximately 192 eggs per female when the larvae were fed on T. molitor larvae to 521 eggs when fed on E. kuehniella eggs. The age-specific oviposition rates and survival of D. prasina when larvae were fed on different prey species are shown in Fig. 1. Egg hatchability was high and ranged from approximately 81–90% without significant differences between the treatments (F = 1.824; df = 8, 18; P = 0.138). Based on these data we estimated the demographic parameters of D. prasina on different prey species that are shown in Table 3. High rm values were recorded when larvae were fed on E. kuehniella eggs, M. persicae nymphs and T. molitor larvae. These three species could be considered as prey of high suitability. Lower rm values were found on A. fabae, A. pomi and T. urticae. The lowest rm value was recorded when T. confusum larvae were offered as prey which resulted in high larval mortality of D. prasina although the few surviving females laid a substantial number of eggs (Table 2).

T. molitor

0

4. Discussion

Adult age (days) Fig. 1. Age-specific oviposition rates (mx, mean number of eggs laid per day per female) (solid line) and survival (lx) (dotted line) of D. prasina females fed on different prey species during their larval development at 25 C and 16:8 LD.

3.2. Effect of prey species on adult longevity and fecundity As shown in Table 2, both mean female adult longevity (F = 3.116; df = 8, 148; P < 0.05) and fecundity (F = 5.328; df = 8, 148; P < 0.001) were significantly affected by the prey species offered to larvae. Female adult longevity ranged from approximately 40–56 d, depending on the prey

Chrysopid larvae can prey on a variety of soft-bodied arthropods such as coccids, leafhoppers, whiteflies, psyllids, thrips, psocids, tetranychid and eriophyid mites, eggs and young larvae of certain species of Lepidoptera and less commonly on eggs and larvae of certain species of Coleoptera, Diptera and Neuroptera (Principi and Canard, 1984; New, 1988; Miller et al., 2004). Some species of the above mentioned orders could be optimal for development and reproduction of chrysopid species and, therefore, result in high larval developmental rates and increased preimaginal survival and adult longevity (Principi and Canard, 1984). The larvae of D. prasina could be considered as polyphagous, since they prey upon a great variety of aphid species such as M. persicae, M. rosae, Myzus cerasi (F.), A. pomi,

Table 3 Demographic parameters of D. prasina fed on different prey at 25C and 16:8 LD Prey

na

rm

95% CIc

E. kuehniella M. persicae T. molitor M. rosae H. pruni A. fabae A. pomi T. urticae T. confusum

16 18 16 15 17 16 19 20 20

0.09826ab 0.08111b 0.07872b 0.06938c 0.06836c 0.05820d 0.05581de 0.05407e 0.04583f

0.09724 0.07870 0.07624 0.06615 0.06685 0.05548 0.05331 0.05292 0.04365

0.09927 0.08351 0.08120 0.07260 0.06987 0.06091 0.05831 0.05523 0.04801

T

R0

k

DT

63.2 61.3 55.1 64.5 65.8 65.2 66.4 75.4 70.9

165.4 136.6 56.44 44.4 68.6 40.8 64.3 50.3 24.8

1.10 1.08 1.08 1.07 1.07 1.06 1.06 1.05 1.04

7.05 8.54 8.80 9.99 10.14 11.91 12.42 12.81 15.13

rm, intrinsic rate of natural increase (d1). R0, net reproductive rate (female offspring per female). T, mean generation time (d). k, finite capacity for increase (d1). DT, doubling time (d). a Number of individuals tested. b Means within a column followed by the same letter are not significantly different at P = 0.05 by Student–Newman–Keuls test. c 95% confidence intervals.

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A. fabae and on eggs of lepidopteran pests (Babrikova, 1979). In certain other lacewing species, it has been found that the species of larval prey could substantially affect preimaginal development and survival as well as fecundity and longevity of adults (Principi and Canard, 1984; McEwen et al., 1993; Zheng et al., 1993; Canard and Volkovich, 2001). In the present study, it was shown that most larval diets had a strong influence not only on preimaginal development but also on the female longevity and fecundity. In addition, except for T. molitor larvae, those diets that subserved rapid preimaginal development and high percentages of survival resulted in better reproductive performance for D. prasina as well. Our results show that among the prey species potentially encountered in the field and tested in the experiments nymphs of M. persicae were proven to be the most favorable for development and reproduction of D. prasina resulting in high immature survival rate, short larval developmental time and increased adult longevity and fecundity. The nymphs of M. rosae, H. pruni, A. fabae and A. pomi resulted in intermediate to low survival and reduced oviposition rates, whereas A. nerii did not allow the completion of larval development. In the present study, the experimental larvae of D. prasina were the first offspring of a parental generation reared on M. persicae. Therefore, we cannot exclude the possibility that the highest suitability of M. persicae in relation to the other tested aphid species could be due to an adoption and/or preference that developed by the predator during the first generation, as it has also been reported for Chrysopa quadripunctata Burmeister (Albuquerque et al., 1997). However, similarly to our results a considerable variation has been found in the relative suitability of several aphid species when tested as prey for lacewing larvae. Great variation in pupal weight and developmental rate has been recorded for Chrysopa perla when fed on various aphid species (Principi and Canard, 1984). Development and reproduction of Chrysoperla rufilabris (Burmeister) and Chrysoperla carnea (Stephens) was favored when fed as immatures on M. persicae and Aphis gossypii Glover whereas Lipaphis erysimi (Kaltenbach) was of low nutritional value for both species (Chen and Liu, 2001; Liu and Chen, 2001). Development and reproduction of another chrysopid species Nineta flava (Scopoli) was also favored when larvae preyed upon the aphids M. persicae and Acyrtosiphon pisum (Harris) or on Microlophium evansi (Theobald) (Principi and Canard, 1984). By contrast, high juvenile mortality has been reported in C. perla and C. carnea when young larvae fed on A. fabae (Principi and Canard, 1984; Ehler et al., 1997; Chen and Liu, 2001). Increased first instar mortality and cocoon-spinning failure were recorded when C. rufilabris larvae preyed upon Tetranychus gloveri Banks and T. castaneum larvae or on Drosophila melanogaster Meigen adults (Hydorn and Whitcomb, 1979). Our experiments have shown that T. urticae and T. confusum are less suitable prey species that result in a low developmental rate and reproduction of D. prasina. In

northern Greece, predation of D. prasina on T. urticae may considerably affect its population dynamics throughout the summer when high field temperatures and low relative humidity cause an abrupt decline of aphid population. Therefore, we may assume that the active presence of D. prasina during summer when population density of its main aphid prey species is low could be due mainly to the availability of alternative non-aphid prey species such as T. urticae, lepidopteran eggs and coleopteran larvae, or other food sources such as extrafloral nectar (Lo´pezArroyo et al., 1999a; Daane, 2001; Limburg and Rosenheim, 2001). Among the aphid species tested A. nerii did not allow the completion of development of young larvae of D. prasina. This may be due to the accumulation of plant-derived toxic cardenolides into the heamolymph that may make this prey species unpalatable or toxic as concluded by Rothschild et al. (1970). However, we cannot exclude the possibility that other factors such as handling time and/ or prey preference may have affected the survival of D. prasina larvae fed on A. nerii. The different aphid species used were collected from different host plants. Therefore, we cannot exclude the possibility that tri-trophic interactions between aphids and host plants may also have affected the survival, development and predation efficiency of D. prasina. According to Giles et al. (2000), C. rufilabris larvae fed on pea aphids reared on alfalfa developed faster than when those aphids were reared on faba beans. Furthermore, whiteflies reared on poinsettia or Lima bean were nutritionally inadequate for the development of C. rufilabris (Legaspi et al., 1994). In our study, observations under a stereomicroscope of young larvae of D. prasina feeding on A. nerii revealed that in most of them the mouthparts or even the whole head were covered with a sticky liquid material that may be a defensive secretion emitted from the aphid cornicles. It is known that, tri-trophic relations that include A. nerii as prey species are really complex mainly because of the interactions between aphid behavior and host–plant developmental stage (Principi and Canard, 1984 and references therein). Eggs of E. kuehniella were the most suitable among the prey species tested favoring rapid immature development, high survival rate and increased fecundity and longevity of D. prasina. Similar results have also been reported for Chrysoperla externa (Hagen) and three species of the genus Cereochrysa (Albuquerque et al., 1994; Lo´pez-Arroyo et al., 1999b). The differences reported in the present study between the moth eggs and M. persicae may indicate that eggs are more nutritious and/or that chrysopid larvae expended more energy in handling the aphids. The water content in the body of aphid species is high and therefore may not affect their relative suitability as prey for aphidophagous predators such as coccinellids or chrysopids (Tauber et al., 1991; Hodek and Honeˇk, 1996). However, other prey such as the eggs of Lepidoptera may have lower water content than aphids (Michaud and Grant, 2005). In addition, the rates of water loss may differ

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among different prey species. Therefore, differences in water content among the non aphid-prey species may have affected their suitability for D. prasina. Young larvae of T. molitor resulted in reduced fecundity and longevity of D. prasina. However, supplementing T. molitor larvae with another food or prey species might be worth trying in the mass-rearing of D. prasina. Mixed diets of prey species (e.g. aphid species) and other non-prey food (e.g. nectar or pollen) have been reported to favor development and survival of several predatory insects including lacewings (Legaspi et al., 1994; Hauge et al., 1998; Nielsen et al., 2002; Patt et al., 2003). In conclusion, our results show that D. prasina could successfully complete development and reproduce on a number of prey species. Furthermore, adults of D. prasina survived and reproduced on a liquid diet and, therefore, can be easily reared in the laboratory. Among the prey species tested E. kuehniella eggs were the most suitable for development and reproduction and could be used for mass-rearing of D. prasina. In our experiments we offered to D. prasina a surplus of single prey species. The quantity of prey consumed by the larvae was not determined and could be different depending on the prey species. Further experiments with identical levels of consumption are needed to evaluate the effects of quantity of prey if any. In the field D. prasina could possibly encounter simultaneously more than one prey species or other alternative food. Therefore, further experiments are required in order to clarify the suitability of different potential food sources and their combinations as well as the level of their availability on the predator’s food preference and performance. Acknowledgments We thank Professor A. Bozsik (University of Debrecen, Hungary) and Professor A. Popov (National Museum of Natural History, Bulgaria) for the identification of the lacewings and for providing useful literature. Many thanks are also due to Prof. Emeritus M.E. Tzanakakis (Aristotle University of Thessaloniki) and two anonymous reviewers for their valuable comments on an earlier version of the manuscript. This study was funded by a scholarship to the senior author by the Greek State Scholarship Foundation. References Albuquerque, G.S., Tauber, C.A., Tauber, M.J., 1994. Chrysoperla externa (Neuroptera: Chrysopidae): life history and potential for biological control in Central and South America. Biol. Control 4, 8–13. Albuquerque, G.S., Tauber, M.J., Tauber, C.A., 1997. Life-history adaptations and reproductive costs associated with specialization in predacious insects. J. Anim. Ecol. 66, 307–317. Aspo¨ck, H., Aspo¨ck, U., Ho¨lzel, H., 1980. Die Neuropteren Europas. Eine ¨ kologie und Chozusammenfassende Darstellung der Systematik, O rologie der Neuropteroidea (Megaloptera, Raphidioptera, Planipennia). Goecke & Evers, Krefeld. Babrikova, T., 1979. Bioecological studies on the green deer fly (Chrysopa prasina Burmeister). Gradinarska Lozarska Nauka 16, 12–18 (in Bulgarian).

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