Suitability of two exotic mealybug species as prey to indigenous lacewing species

Biological Control 96 (2016) 93–100

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Suitability of two exotic mealybug species as prey to indigenous lacewing species Sibele J. Tapajós a, Rogério Lira a, Christian S.A. Silva-Torres a,⇑, Jorge B. Torres a, Rodrigo L.C.B. Coitinho b a b

Departamento de Agronomia-Entomologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, S/N, Dois Irmãos, 52171-900 Recife, PE, Brazil Instituto Agronômico de Pernambuco, Av. General San Martin, Bongi, 50761-000 Recife, PE, Brazil

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 Two indigenous lacewings were

tested against two exotic mealybugs species.  Lacewing larvae at 2nd- and 3rdinstar preyed successfully both mealybugs.  Mealybugs at 2nd-instar furnished development of all stages of both lacewings.  Predation rate when significant was always superior for Chrysoperla externa.

a r t i c l e

i n f o

Article history: Received 1 May 2015 Revised 23 January 2016 Accepted 9 February 2016 Available online 10 February 2016 Keywords: Biological control Predator-prey interaction Chrysopidae Pseudococcidae

a b s t r a c t Mealybugs (Hemiptera: Pseudococcidae) have spread throughout subtropical and tropical regions, causing severe losses to crop production that have prompted much interest in discovering effective biological agents against these pests. The Brazilian indigenous lacewing (Neuroptera: Chrysopidae) species Chrysoperla externa (Hagen) and Ceraeochrysa everes (Banks) were studied against two exotic mealybug species, Ferrisia dasylirii (Cockerell) and Pseudococcus jackbeardsleyi Gimpel & Miller. To assess the relative potential of these lacewing species as control agents against these two pests, we confined 1st-, 2nd-, and 3rd-instar lacewing larvae with 2nd- and 3rd-instar nymphs and adult female mealybugs to evaluate development, survival, reproduction and predation rate. Lacewing larvae at 2nd- and 3rd-instar preyed successfully on mealybugs of all ages, and second instar mealybug nymphs supported successful development of lacewing larvae irrespective of the predators’ age. However, 1st-instar lacewing larvae either failed to complete development or showed lower performance when fed only 3rd-instar or adult female of mealybugs of either species. Comparing the lacewing species, Ce. everes tended to produce more eggs, but showed delayed development and lower egg viability as compared to Ch. externa. Furthermore, in every case in which a significant difference in predation rate was detected, it was always superior for Ch. externa. Further studies to assess the establishment of these species and other lacewing species associated with these introduced mealybugs are reasonable to provide sustainable biological control. Ó 2016 Published by Elsevier Inc.

1. Introduction

⇑ Corresponding author. E-mail address: [email protected] (C.S.A. Silva-Torres). http://dx.doi.org/10.1016/j.biocontrol.2016.02.005 1049-9644/Ó 2016 Published by Elsevier Inc.

Mealybugs (Hemiptera: Pseudococcidae) are exclusively phytophagous, highly polyphagous, cosmopolitan insects infesting cultivated plants in many subtropical and tropical regions of the globe (Miller et al., 2002, 2012; Culik et al., 2006a,b; Silva-Torres et al.,

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2013). The introduction of mealybug species has been recorded in areas of Oceania, Africa, Asia, and in the Americas (Miller et al., 2002; Culik et al., 2006a,b; Silva-Torres et al., 2013; Mani et al., 2013). These exotic species have become problems for several reasons, such as lack of knowledge concerning efficient control practices such as registered insecticides, and the ample availability of cultivated host plants. The chemical control of mealybugs is restricted to broad-spectrum insecticides, especially organophosphates and neonicotinoids (Nagrare et al., 2011). However, several organophosphate insecticides registered to control mealybugs in Brazil and worldwide are facing removal from the market (EPA, 2012). Hence, a common reaction to the introduction of a new potential pest is to introduce natural enemies to counteract the problem (DeBach and Warner, 1969). However, when given enough time, indigenous natural enemies may establish associations with the exotic species in the new areas, helping with their control without the costs and risks created by a program of classical biological control (Hokkannen and Lynch, 2003; Colares et al., 2015). In general, mealybugs have become a very attractive target for biological control practitioners due to their high concentration and stability over time. Whereas other sucking pests such as aphids and psyllids produce erratic population peaks insufficient to stabilize a relationship with natural enemies, mealybugs usually have a sessile habit, staying and feeding for long periods on the same plant spot after establishment until death. This generates a clumped population distribution within plant (Silva-Torres et al., 2013; Oliveira et al., 2014a) and in the crop ecosystem (Beltrá et al., 2013). High reproductive potential results in availability of eggs and nymphs at different developmental stages (Oliveira et al., 2014a). Further, abundant honeydew attracts natural enemies such as adults of parasitoids, ladybird beetles, and lacewings that consume the honeydew as a food supplement. These conditions are favorable to the establishment and the persistence of a natural enemy population in the new habitat. Fact that many biological control programs have successfully used predators and parasites of mealybugs (Bokonon-Ganta and Neuenschwander, 1995; Kairo et al., 2000; Neuenschwander, 2001; Meyerdirk et al., 2004; Roltsch et al., 2006; Muniappan et al., 2006; Attia et al., 2007; Afifi et al., 2010; Solangi et al., 2012; Barbosa et al., 2014a,b). Lacewings (Neuroptera: Chrysopidae) are widely recognized as key predators of soft-bodied arthropods, especially aphids, psyllids, and mealybugs (Tauber et al., 2000; Senior and McEwen, 2001). Among predacious species used in biological control programs, lacewings provide good examples of successful mass production, commercial availability, and inundative releases to control pest species in protected (e.g. greenhouses) and field cropping systems (Principi and Canard, 1984; Tauber et al., 2000; Senior and McEwen, 2001). Furthermore, the use of Chrysoperla carnea (Stephens) has accounted for one third of all successful biological control programs in the world (Williamson and Smith, 1994; O’Neil et al., 1998), as well as Chrysoperla rufilabris (Burmeister) in North America (Tauber et al., 2000). Indigenous in Brazil, the lacewing species Ceraeochrysa everes (Banks) and Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) occur naturally in various crop ecosystems (Freitas, 2002; Santos et al., 2013), and like other lacewing species, they can be mass-produced using factitious prey in insectaries (Barbosa et al., 2002; Bortoli et al., 2006; Tavares et al., 2011). Up on that, recent studies have shown that indigenous natural enemies exhibit significant preadaptation against exotic species (Qureshi and Stansly, 2011; Colares et al., 2015). Thus, we hypothesized that indigenous lacewings would express good adaptation on exotic mealybugs and may contribute to their natural or applied biological control. Therefore, this work determined the development, reproduction and predation rate of two indigenous lacewing

species Ce. everes and Ch. externa upon two exotic mealybugs species recently introduced in Brazil, Ferrisia dasylirii (Cockerell) and Pseudococcus jackbeardsleyi Gimpel & Miller. 2. Material and methods 2.1. Mealybug species The mealybug species studied, F. dasylirii (=virgata) and P. jackbeardsleyi, originated from stock colonies maintained in the Biological Control Laboratory of the Universidade Federal Rural de Pernambuco (UFRPE). Dead specimens were sent to Dr. Penny Gullan (The Australian National University) for species confirmation and voucher species deposit. Nymphs and adults of both mealybug species were reared on pumpkin Cucurbita moschata var. ‘‘Jacarezinho” following the method described in Oliveira et al. (2014a,b). Adult females of both species exhibit roughly similar body size [F. dasylirii body length varies from 3.14 to 5.30 mm and 1.36 to 2.86 width (Gullan and Kaydan, 2012); while P. jackbeardsleyi average 3.2 mm body length by 1.8 mm width (Gimpel and Miller, 1996)]. 2.2. Lacewing rearing Eggs of Ce. everes were obtained from CRISOBIOL/LABEN (Biofábrica de Chrysopidae/Laboratório de Entomologia) of the ‘‘Instituto Agronômico de Pernambuco (IPA)”, Recife, PE; pupae of Ch. externa were obtained from the Biological Control Laboratory of the Universidade Federal de Lavras (UFLA), Lavras, MG. Adults, eggs, and larvae of both lacewing species were reared following the method described in Nordlund et al. (2001), with few adaptations. Stock colonies and all experiments conducted in this study were carried out at the Biological Control Laboratory of the UFRPE with regulated temperature, which averaged (mean ± SE) 24.9 ± 0.63 °C, 72.3 ± 8.1% RH and 13 h photophase. 2.3. Biology and predation of mealybugs by Ceraeochrysa everes and Chrysoperla externa Larvae of both lacewing species were reared using three prey types: 1) second instar F. dasylirii nymphs; 2) second instar P. jackbeardsleyi nymphs; and 3) a factitious prey, Anagasta kuehniella eggs, used as a standard control for comparisons. In every case, each newly hatched lacewing larva was confined in a plastic petri dish (5.5 cm diam) lined with filter paper and offered the different prey treatments separately. Based on preliminary consumption trials, lacewing larvae in the first, second, and third instars were fed with second instar mealybug nymphs at rates of 4, 7, and 50 nymphs per day, respectively. Each treatment was run with 50 replications each for the mealybug species and 40 replications for the A. kuehniella eggs, consisting of one lacewing larva per replication. Thus, the experiment was conducted considering predator as a main factor (two species) and prey as secondary factor (three types). In addition to the prey inside the petri dishes, a 1-cm long green stem taken from either a cotton plant or a hibiscus plant terminal was offered for F. dasylirii or P. jackbeardsleyi, respectively. The predator larvae were monitored daily to record molting dates, pupation date, mortality, adult emergence, and consumption of mealybug nymphs. Consumed mealybug nymphs were replaced daily; thus, the daily availability of prey was maintained constant throughout the experiment. Emerged lacewing adults were separated by gender at emergence day, and pairs of one male and one female were formed. These adults were kept in PVC cages (15 cm height, 10 cm

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diameter). Because adults of studied lacewing species are predatory only in the larval stage, adults from all treatments were fed with a similar diet consisting of a paste of honey and yeast (50%:50%) offered on the upper surface of adhesive tape fixed inside the cages. Moisture was provided using embedded cotton pads with distilled water placed inside small plastic tops at the bottom of the cage. Food and moisture were replaced every two days. Data on pre-oviposition period, number of eggs produced, egg viability, and longevity of females were obtained. Ten pairs (replications) were monitored for each one of the six treatments (2 lacewing species  3 prey species). The oviposition substrate paper was replaced daily, and numbers of eggs laid were recorded. Eggs were stored in 5-cm diameter petri dishes lined with filter paper. Larval eclosion rates were recorded twice a day to minimize losses due to cannibalism. Data on developmental time, survival, prey consumption, and adult reproductive parameters – age of the first oviposition, eggs produced per female, and egg hatching – were each submitted to a normality test (Kolmogorov-D: Normal test, Proc Univariate of SAS) and a variance homogeneity test (Bartlett’s test), and transformed into square root (x + 0.5) when needed to meet the assumptions for analysis of variance (ANOVA) (SAS Institute, 2002). The data were subjected to two-way ANOVA considering predator (two) as main factor and prey (three) as secondary factor. Significantly different means among prey items (df = 2) were separated using a Tukey’s high significant difference (HSD) test at 0.05 significance levels; mean values that differed between predators (df = 1) were separated using the Fisher’s test from ANOVA. 2.4. Predator-prey outcome at different developmental stages Because lacewing larvae encounter mealybugs of different developmental stages in the field, we confined single first, second and third instar larvae of Ce. everes and Ch. externa with third instar or adult female mealybugs. Mealybug nymphs at second instar lack a dense wax layer covering their body and had already been tested in the previous experiment. However, the third instar mealybugs used in this study produce a dense wax layer that may impair attack by lacewing larvae (Eisner and Silberglied, 1988). Thus, the experiment consisted of two predator species at three different larval instars as main factor (six) and two prey species (mealybugs) at two developmental stages (third instar nymph and adult female) as secondary factor (four), totaling 24 combinations of treatments with 40 predator larvae used per treatment (replications). The methods used for confining predator with prey and for prey exposure were similar to the methods for the previous experiment for each designed treatment. However, in this experiment the predator larvae used in the second and third instars were fed A. kuehniella eggs up to the moment of the experimental set-up. Further, during the experiment, each predator larva received prey at a rate of four mealybug nymphs or adult mealybug females per day. Prey consumed was replaced daily during the evaluation period. Daily evaluations included predation rate, predator mortality, molting events to pupation and adult stage, and adult body deformation at emergence day. The time required to complete the larval stage within each treatment, survival from treatment onset to adult emergence, duration of pupa stage, and predation rate were transformed into square root (x + 0.5), when needed to meet the assumptions of analysis of variance (ANOVA) (SAS Institute, 2002). For cases in which interaction results were null (i.e., when no predator completed development, causing unbalanced factorial design), the data were subjected to ANOVA considering each predator and its respective prey treatment separately, and significantly different means among prey stage (third instar or adult female) were separated using the Fisher’s test from ANOVA at 0.05 significance levels.

3. Results 3.1. Biology and predation of mealybugs by Ceraeochrysa everes and Chrysoperla externa Developmental time from first instar larva to adult emergence was significantly different for predator species (Fdf = 1, 214 = 669.51, P = 0.0001), prey types (Fdf = 1, 214 = 415.04, P < 0.0001), and for the interaction of predator species and prey types (Fdf = 2, 214 = 126.32, P < 0.0001). Larval development of Ch. externa was variable across mealybug species and A. kuehniella eggs (Fdf = 2, 55 = 105.77, P < 0.0001). Both lacewing species needed about twice as much time to fulfill larval development when fed second instar nymphs of P. jackbeardsleyi compared to their conspecifics that were fed eggs of A. kuehniella (Table 1). Likewise, Ce. everes also exhibited delayed development when fed mealybug F. dasylirii, followed by P. jackbeardsleyi (F2, 53 = 142.65, P < 0.0001). Comparing the predator species, longer developmental times were observed for Ce. everes fed A. kuehniella eggs or F. dasylirii second instar compared to Ch. externa; however, similar developmental times were found for both predators fed second instar P. jackbeardsleyi (Table 1). Duration from pupa to adult emergence was variable across predator species and prey types (Table 1). Between predators, Ch. externa exhibited shorter developmental duration compared to Ce. everes across all prey types (A. kuehniella: F1, 84 = 1627.37,

Table 1 Developmental time, reproduction and predation rate of Chrysoperla externa and Cereaochrysa everes fed Anagasta kuehniella eggs or second instar nymphs of Ferrisia dasylirii and Pseudococcus jackbeardsleyi. Characteristics

Anagasta kuehniella

Development of larvae (days) Ce. everes 14.1 ± 0.15 Ac Ch. externa 8.2 ± 0.16 Bc1

Ferrisia dasylirii

Pseudococcus jackbeardsleyi

21.4 ± 0.54 Aa 13.2 ± 0.54 Bb

16.4 ± 0.21 Ab 16.3 ± 0.43 Aa

Mean number of mealybug nymphs consumed Ce. everes – 380.6 ± 14.75 Aa Ch. externa – 272.3 ± 8.84 Ba

219.0 ± 3.62 Ab 213.6 ± 6.70 Ab

Development of pupae (days) Ce. everes 15.5 ± 0.09 Aa Ch. externa 9.9 ± 0.10 Bb

15.3 ± 0.10 Aa 11.5 ± 0.18 Ba

12.8 ± 0.14 Ab 11.6 ± 0.16 Ba

Development from neonate to adult (days) Ce. everes 29.5 ± 0.14 Ab 36.5 ± 0.35 Aa Ch. externa 17.9 ± 0.16 Bc 24.7 ± 0.42 Bb

29.3 ± 0.16 Ab 28.2 ± 0.41 Ba

Survival from neonate to adult (%) Ce. everes 100 ± 0.0 Aa Ch. externa 90.9 ± 4.15 Aa

48.8 ± 8.89 Bb 91.1 ± 3.51 Aa

80.0 ± 6.67 Aa 54.0 ± 7.33 Bb

Pre-oviposition period (days) Ce. everes 9.3 ± 0.21 Aa Ch. Externa 4.7 ± 0.17 Bab

10.9 ± 0.86 Aa 6.2 ± 0.42 Ba

11.0 ± 0.74 Aa 4.0 ± 0.42 Bb

725.1 ± 190.57 Ab

813.7 ± 207.47 Ab

629.0 ± 67.52 Ab

457.5 ± 78.12 Bc

3.3 ± 1.52 Bb 87.2 ± 2.84 Aab

0.5 ± 0.41 Bb 72.3 ± 7.14 Ab

84.0 ± 8.40 Aa 88.5 ± 5.88 Aa

78.8 ± 11.48 Aa 51.3 ± 7.49 Bb

Mean number of eggs per female Ce. everes 1629.4 ± 200.46 Aa Ch. Externa 1044.1 ± 81.81 Ba Egg viability (%) Ce. everes 72.6 ± 9.24 Aa Ch. Externa 91.8 ± 1.11 Aa Female longevity (days) Ce. everes 88.4 ± 10.05 Aa Ch. externa 83.7 ± 6.72 Aa

1 Means (±SEM) followed by uppercase letters within column do not differ between predators fed the same prey; while, means followed by lowercase letters within row do not differ for the same predator species comparing prey types (Tukey HSD, 0.05 significance level).

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P < 0.0001; F. dasylirii: F1, 63 = 276.57, P < 0.0001; and P. jackbeardsleyi: F1, 66 = 28.20, P = 0.0001). Pupae of Ch. externa developed faster when larvae were fed A. kuehniella eggs compared to larvae fed both mealybugs species (F2, 109 = 48.42, P < 0.0001). In addition, pupae of Ce. everes developed faster when larvae fed upon P. jackbeardsleyi (F2, 104 = 194.13, P < 0.0001) (Table 1). Developmental time from neonate larva to adult emergence was variable for both predator species and prey types (Table 1). Development of Ch. externa was faster compared to Ce. everes across all prey types (A. kuehniella: F1, 84 = 2882.14, P < 0.0001, F. dasylirii: F1, 63 = 411.20, P < 0.0001, and P. jackbeardsleyi: F1, 66 = 8.20, P = 0.0056). Prey type also delayed the development of Ce. everes (F2, 104 = 331.21, P < 0.0001) and Ch. externa (F2, 109 = 257.28, P < 0.0001) (Table 1). Among the prey types, Ch. externa fulfill development faster when fed A. kuehniella, followed by F. dasylirii, and P. jackbeardsleyi. Regarding the predators, Ce. everes achieved faster development from neonate larva to adult when fed F. dasylirii and similar time between P. jackbeardsleyi and A. kuehniella (Table 1). The survival from neonate larva to adult emergence also differed between predator species and prey types (Table 1). Lower survival was observed for Ch. externa and Ce. everes when fed P. jackbeardsleyi and F. dasylirii, respectively. However, both predator species exhibited survival rates of over 90% when fed A. kuehniella eggs. The length of time between adult emergence and first oviposition varied as a function of predator species (F1, 52 = 188.11, P < 0.0001), prey types (F1, 52 = 6.68, P = 0.0026) and the interaction of these factors (F2, 52 = 5.66, P = 0.0060). Females of Ch. externa initiated oviposition earlier than Ce. everes irrespective of the prey species they had consumed during the larval stage (A. kuehniella: F1, 17 = 286.13, P < 0.0001; F. dasylirii, F1, 18 = 27.69, P < 0.0001; P. jackbeardsleyi, F1, 17 = 76.50, P < 0.0001). The species Ch. externa delayed oviposition when fed F. dasylirii at larval stage compared to those fed P. jackbeardsleyi or A. kuehniella eggs (F2, 26 = 8.45, P = 0.0015). However, Ce. everes had similar pre-oviposition periods across all studied prey species (P = 0.1181) (Table 1). Similarly to results for the pre-oviposition period, the number of eggs produced per female varied as function of predator species (F1, 53 = 6.86, P < 0.0015) and prey types (F1, 53 = 12.35, P < 0.0001) as main factors, but not in the interaction of these factors (P = 0.2558). Between predators, Ce. everes produced more eggs per female than Ch. externa when reared on A. kuehniella eggs or P. jackbeardsleyi, but both lacewing species produced similar number of eggs after being fed F. dasylirii during larval stage. Furthermore, both predators produced more eggs when fed A. kuehniella eggs compared to both mealybugs used as prey (Table 1). Regarding the mealybugs as prey, Ch. externa produced more eggs when fed F. dasylirii compared to P. jackbeardsleyi, whereas Ceraeochrysa everes exhibited similar oviposition, regardless of which mealybug species it had received. Egg viability varied as a function of predator species (F1, 53 = 216.90, P < 0.0001), prey types (F2, 53 = 52.48, P < 0.0001) and of the interaction predator species and prey types (F1, 53 = 22.78, P < 0.0001). Egg viability was similar between predators, averaging over 72% when the lacewings were fed their standard prey, A. kuehniella eggs. On the other hand, lower egg viability for Ce. everes compared to Ch. externa was observed when they received mealybugs. Egg viability of Ch. externa was higher when fed A. kuehniella, followed by F. dasylirii, and similar to P. jackbeardsleyi (Table 1). Longevity of adult females varied as function of prey types (F2, 53 = 4.10, P = 0.0222), but not as function of predator species (P = 0.3347) or the interaction between predators and prey types (P = 0.1774). Females lived more than 78 days irrespective of prey types, except for females of Ch. externa fed P. jackbeardsleyi that lived on average 51.3 days (Table 1).

The predation rate varied as function of predator species (F1, 139 = 15.59, P < 0.0001) with Ce. everes consuming more prey than Ch. externa. Likewise, the predation rate varied as function of mealybug species (F1, 139 = 162.79, P < 0.0001) and the interaction of predator and mealybug species (F1, 139 = 34.55, P < 0.0001). Both lacewing species consumed more F. dasylirii mealybugs than P. jackbeardsleyi mealybugs (Table 1). Furthermore, the predator Ce. everes consumed more F. dasylirii than Ch. externa. Both predators consumed similar numbers of P. jackbeardsleyi (Table 1). 3.2. Predator-prey outcome at different developmental stages Among the 24 sets of treatment interacting predators and mealybug ages (Table 2), only four occasions we found significant statistical differences. Larvae of Ce. everes confined at first instar (F1, 32 = 22.47, P < 0.0001) and at second instar (F1, 51 = 13.17, P = 0.0007) completed their development more quickly when fed F. dasylirii compared to P. jackbeardsleyi, irrespective of mealybug age. Also, larvae of Ch. externa at second instar (F1, 48 = 27.89, P < 0.0001) and at third instar (F1, 55 = 20.54, P < 0.0001) fed third instar nymphs of F. dasylirii completed development faster than when fed P. jackbeardsleyi (Table 2). Larvae of both predator species at first instar had lower overall survival rates compared to older larvae when preying third instar and adult female mealybugs (Table 3). First instar larvae of Ce. everes did not complete their development feeding exclusively upon P. jackbeardsleyi females; while first instar larvae of Ch. externa exhibited low survival (3.3–6.6%) when preying upon third instar nymphs and adults females of P. jackbeardsleyi and F. dasylirii (Table 3). First instar lacewing larvae had higher survival when fed mealybug nymphs than when fed adult females. Likewise, except for larvae of Ch. externa at second instar that had been fed either mealybug species, more (70–96.7%) of the older predator larvae (confined at second and third instar) survived when fed mealybug nymphs than those fed mealybug adult females (Table 3). When they did survive, larvae of Ch. externa confined at first or second instar with females of F. dasylirii produced, respectively, 100% and 53% of adults with deformed wings, antennae, or legs. Larvae of both lacewing species consumed more third instar and adult females of P. jackbeardsleyi than of F. dasylirii, irrespective of the life stage at which these predators were confined with these mealybugs (Table 3). Furthermore, in every case in which a significant difference in predation rate was detected, it was always superior for Ch. externa. 4. Discussion The factitious prey used in this study, eggs of A. kuehniella, promoted satisfactory development, reproduction, and longevity of adult of both lacewings as expected and with values within those previously reported in the literature (Barbosa et al., 2002; Bortoli et al., 2006; Tavares et al., 2011). Thus, comparisons can be made regarding the potential performance of both predator species preying upon the mealybug species used in this study. Larvae of both predators exhibited variation on development, predation rate, and reproduction according to the mealybug species used as prey and when having these prey available at different developmental stages. Nevertheless, better performance was found when predator larvae fed upon younger waxless mealybug nymphs or when predator larvae were older, irrespective of the mealybug age. Therefore, depending on the age of the predator, both mealybug species can be considered ‘adequate’ prey for development of both lacewing species. The developmental duration of the predatory stage may be shortened when feeding on high quality prey (Torres et al., 2004;

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Table 2 Mean time (days) required by Ceraeochrysa everes and Chrysoperla externa to complete development of larval and pupal stages fed third instar nymphs or adult females of Ferrisia dasylirii and Pseudococcus jackbeardsleyi. Predator’s developmental stage

Predator species

Third instar prey

Adult female prey

Ferrisia dasylirii

Pseudococcus jackbeardsleyi

Ferrisia dasylirii

Pseudococcus jackbeardsleyi

Ce. everes Ch. externa

18.9 ± 0.43 Ab1 17.3 ± 0.96 B

24.5 ± 1.26 a –2

20.9 ± 0.85 –2

–2 –2

Second instar to pupa

Ce. everes Ch. externa

10.4 ± 0.28 Aa 9.6 ± 0.27 Ab

12.2 ± 0.33 Aa 12.0 ± 0.34 Aa

10.5 ± 0.38 Ab 10.2 ± 0.34 Aa

12.5 ± 0.40 Aa 9.8 ± 0.62 Ba

Third instar to pupa

Ce. everes Ch. externa

5.9 ± 0.22 Aa 5.9 ± 0.15 Ab

6.5 ± 0.30 Aa 7.4 ± 0.30 Aa

5.5 ± 0.17 Aa 4.6 ± 0.24 Aa

5.8 ± 0.27 Aa 5.3 ± 0.28 Aa

Ce. everes Ch. externa

13.7 ± 0.23 Aa 11.3 ± 0.33 B

14.4 ± 0.26 a –2

14. ± 0.16 –2

–2 –2

Second instar to pupa

Ce. everes Ch. externa

13.8 ± 0.09 Aa 10.4 ± 0.13 Ba

13.4 ± 0.12 Aa 11.4 ± 0.91 Ba

13.5 ± 0.41 Aa 10.3 ± 0.11 Ba

14.1 ± 0.16 Aa 10.8 ± 0.23 Ba

Third instar to pupa

Ce. everes Ch. externa

13.8 ± 0.14 Aa 10.1 ± 0.14 Ba

13.2 ± 0.08 Aa 10.4 ± 0.20 Ba

14.4 ± 0.14 Aa 10.4 ± 0.17 Ba

13.9 ± 0.10 Aa 10.3 ± 0.22 Ba

Larval stages First instar to pupae

Pupal stages First instar to pupae

1 Means (±SEM) followed by uppercase letters within column compare predator species fed same prey species of the same age; lowercase letters within the row compare the mealybug species of the same age as prey for the same predator species (Fisher’s test from ANOVA at 0.05 significance level). 2 Absence of values or less than two individuals completed the larval stage, not allowing statistical inferences.

Table 3 Predation rate and survival from larvae to adult (% of emergence) of Ceraeochrysa everes and Chrysoperla externa preying upon third instar nymphs or adult females of Ferrisia dasylirii and Pseudococcus jackbeardsleyi. Predator’s developmental stage

Predator species

Third instar prey

Adult female prey

Pseudococcus jackbeardsleyi

Ferrisia dasylirii

Pseudococcus jackbeardsleyi

Pseudococcus jackbeardsleyi

First instar to pupae

Ce. everes Ch. externa

39.9 ± 1.03 Ab1 (63.3)3 38.9 ± 1.36 A (30.0)

58.3 ± 2.90 a (56.7) –2 (3.3)

23.5 ± 1.13 (26.7) –2 (6.6)

–2 (0) –2 (3.3)

Second instar to pupa

Ce. everes Ch. externa

28.9 ± 1.11 Ab (93.3) 30.8 ± 0.90 Ab (70.0)

35.1 ± 0.85 Ba (96.7) 40.6 ± 1.40 Aa (93.3)

12.2 ± 0.50 Ab (93.3) 13.1 ± 0.57 Ab (56.7)

15.9 ± 0.74 Ba (76.7) 22.6 ± 0.85 Aa (56.7)

Third instar to pupa

Ce. everes Ch. externa

19.7 ± 1.05 Ba (96.7) 22.6 ± 0.55 Ab (93.3)

22.4 ± 1.21 Ba (96.7) 27.0 ± 1.12 Aa (93.3)

10.2 ± 0.51 Ab (90.0) 9.2 ± 0.47 Ab (86.7)

12.1 ± 0.75 Ba (86.7) 15.0 ± 0.43 Aa (90.0)

1 Means (±SEM) followed by uppercase letters within column compare predator species preying upon the same mealybug of the same age; while means followed by lowercase letters compare means within row for the same predator between mealybug species of the same age (Fisher’s test from ANOVA at 0.05 significance level). 2 Absence of values or less than two individuals completed the larval stage. 3 Values between brackets = viability [number of individuals completing larval stage/number of total individuals initiating the study) * 100].

Barbosa et al., 2014a). This concept agrees with our results for both lacewing species fed A. kuehniella eggs, prey commonly used in insectary production (Nordlund et al., 2001; Bortoli et al., 2006). However, when having first contact with new prey species such as the exotic mealybug species tested here, predators need some time to adapt to the new prey. This includes adaptation of attack behaviors – especially for the extra-oral digestion that predators such as lacewing larvae require to liquefy prey body contents prior to ingestion – and also to adapt their physiology to use all uptaken body content (Cohen, 1998; Grenier and De Clercq, 2003). Thus, one could expect improvement on the performance of both Ch. externa and Ce. everes after their populations have completed some generations using these mealybugs as prey. Among the 24 studied combinations of predator and prey (Tables 2 and 3), prey age had a major effect on the predator performance. In this study, second instar mealybug nymphs worked as the best prey age for these lacewings, regardless of the predators’ age. However, egg stage and first instar mealybug nymphs were not tested. The egg stage is completed during a few hours inside the female ovissac (Oliveira et al., 2014b), but the first instar nymphs (a.k.a. crawlers) are waxless, and thus their consumption rate will be likely high (Rashid et al., 2012; Khan et al., 2012; Hameed et al., 2013). Comparing the two lacewing species, the larvae of Ch. externa exhibited better performance (rapid development and high

survival) when preying upon F. dasylirii and rapid development and low survival when preying on P. jackbeardsleyi; meanwhile Ce. everes achieved higher survival from neonate to adult when fed P. jackbeardsleyi. These variations on the response between the lacewing species may be related to differences intrinsic in their biology and behavior and not solely from the new predator-prey associations. Albuquerque (2009) has suggested that larvae of trash-carrying lacewing species such as Ce. everes are less aggressive and exhibit slower development as compared to those larvae which do not carry trash such as Ch. externa. Our results for predation concurred when the prey was F. dasylirii. The daily predation rate (number of prey consumed/duration of larval stage) was nearly 20.6 and 17.8 nymphs of second instar for Ch. externa and Ce. everes, respectively. However, when the prey was P. jackbeardsleyi, the duration of larval stage and the predation rate of second instar nymphs were statistically equal for both studied predators. Prey effects on adult predator characteristics such as age of first oviposition and female longevity were undetectable for both lacewing species. On the other hand, the number of eggs produced and egg viability varied as function of predator species and prey types. The number of eggs laid per female was about twice as high when predators fed upon A. kuehniella eggs compared to those that fed upon mealybugs. Despite this difference associated with prey types, egg production by Ch. externa females that fed upon mealybugs exhibited fecundity superior when compared to results

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obtained in other studies with other wild prey species. Fecundity when using Aphis gossypii Glover (Hemiptera: Aphididae), Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), and Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), as prey were 428.5, 384.0, and 338.9 eggs, respectively (Macedo et al., 2010; Sattar et al., 2011). Likewise, species of Ceraeochrysa fed A. gossypii or Plutella xylostella L. (Lepidoptera: Plutellidae) produced, on average, 279 and 467.7 eggs, respectively (Almeida et al., 2009). Egg viability of Ce. everes preying on both mealybug species was low, ranging from 0.5 to 3.3%. Only two of 10 Ceraeochrysa everes females reared on F. dasylirii produced viable eggs; however, 87.1% of the eggs produced by these two females were viable. Likewise, only two out of 10 females fed P. jackbeardsleyi produced viable eggs, but in this case egg viability was much lower (6.6–12%). Based on these laboratory-based results, the maintenance of Ce. everes on P. jackbeardsleyi or F. dasylirii would appear to be compromised, especially when feeding exclusively on P. jackbeardsleyi. Under field conditions, however, larvae of Ce. everes may feed on various other prey types, mixing their diet and minimizing the single prey effect found here. In addition, under laboratory conditions there should be no problem raising this lacewing with factitious prey such as A. kuehniella eggs for a repeated release/ inundative program. Based on the characteristics of Ch. externa in the immature and adult stages, and its predation rate on both exotic mealybug species, this predator has some potential to control P. jackbeardsleyi or F. dasylirii in the field. Larvae of Ch. externa fed Planacoccus citri Risso (Hemiptera: Pseudococcidae) accomplish larval development in 14.29 days and viability of 13.3% (Bonani et al., 2009). Furthermore, larvae of Ceraeochrysa cubana Hagen (Neuroptera: Chrysopidae) fed Pinnaspis sp. (Coccoidea: Diaspididae) had, on average, larval duration of 20.5 days and viability of 31.6% (Santa-Cecília et al., 1997). Bortoli and Murata (2011) studied Ceraeochrysa paraguaia Navás (Neuroptera: Chrysopidae) fed Selenaspidus articulatus Morgan (Hemipetra: Diaspididae) and Orthezia praelonga Douglas (Hemipetra: Ortheziidae), concluding that only S. articulatus was a suitable prey with larval duration of 10.97 days and viability of 83.3%. Based on our results, first instar larvae of both lacewing species tested will require early stage mealybugs (or the presence of other food sources) to molt to the next instar. At the first instar stage, lacewing larvae may not be able to handle larger prey items like older mealybug nymphs and adults (Principi and Canard, 1984). According to Canard (2001), prey body size has a direct influence on predation rate of Chrysopidae; hence, younger larvae of small size relative to their prey are less able of attack. Studies by Lira and Batista (2006) and Barbosa et al. (2008) indicated that first instar larvae of Ch. externa had lower performance preying upon the larger green peach aphid Myzus persicae (Sulzer), despite the latter being a high quality and preferred prey species. Different prey instars also differ in their passive and active defenses. Despite having a soft body and low movement after reaching the second instar, mealybugs affixed to their host plant are not as defenseless as they might superficially appear. Third instar and adult female mealybugs (Pseudococcidae) secrete and cover the body with dense wax layer, which becomes a physical barrier against biotic and abiotic mortality factors (McKenzie, 1967; Eisner and Silberglied, 1988). Numerous examples illustrate the wax’s effectiveness. For instance, according to Rashid et al. (2012) and Hameed et al. (2013), Chrysoperla carnea Stephens had better performance preying upon first instar cotton mealybug Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae), presumably because at this early age, the mealybug nymphs lacked the waxy body coating of older nymphs, and, only older (third instar) lacewing larvae preyed with success upon the female adult mealybug. Further, Ch. carnea

larvae of all three larval stages preferred first instar nymphs relative to second and third instar P. solenopsis (Khan et al., 2012). Likewise, Eisner and Silberglied (1988) observed in the field that larvae of Cereaochrysa cincta (Schneider) fed preferentially on younger nymphs of Plotococcus eugeniae Miller & Denno rather than on older nymphs, which were covered with wax. These findings concur with our results regarding the waxless second instar nymphs being the most suitable prey for both predators irrespective of predator age, whereas third instar nymphs and adult females, which produce a dense wax layer, were a suitable prey only for older predator larvae. Moreover, evidence suggests that this wax functions as more than just a passive barrier. Gonçalves-Gervásio and Santa-Cecília (2001) reported that Chrysoperla externa struggle to feed on adult females of Dysmicoccus brevipes Cockerell (Hemipetra: Pseudococcidae). Barners (1975) observed that the wax secretion of P. citri tangled the sickle-shaped mandibles of Chrysopa zastrowi Esben-Peterson (Neuroptera: Chrysopidae) hindering the feeding behavior of the predator. In addition, mealybugs can produce defensive secretions through their ostiole that dry quickly in contact with the air; these cloak the feeding apparatus of predators, causing their death by starvation (Chandler and Watson, 1999). In fact, this deadly defense was observed for first instar lacewing larvae (and sometimes older larvae as well) preying upon third instar nymphs and adult females of F. dasylirii. When these secretions wrapped around the mandibles of older lacewing larvae and hindered their feeding, third instar lacewing larvae molted precociously into pupae that subsequently became malformed adults. Although different instars of the lacewing species in this laboratory-based study had different levels of success as predators upon mealybugs of varied developmental age, such variation does not automatically negate their potential value as a biological control agent. Mealybugs usually have high populations with overlapping generations; therefore, upon the same infested plant, predators encounter mealybugs of many ages and stages, including first and second instar waxless nymphs as suitable prey for sustaining younger lacewing larvae. A conservative conclusion would be that Ch. externa might serve as an indigenous predator species for both mealybug species, and Ce. everes could be mass-produced for periodic releases as needed against these two introduced agricultural pests. Results reported herein with indigenous lacewing species, those with lady beetles (Barbosa et al., 2014a,b), and the surveys registering various other predators and parasitoids attacking these mealybugs (Culik et al., 2006b; Giorgi et al., 2014), open opportunity to investigate potential practices to preserve them as natural biological control with the benefits of avoiding introduction of exotic natural enemies and of using to broad-spectrum insecticides usually required to control these pest species. Acknowledgments We thank professor Geraldo Carvalho (UFLA) for sending pupae of Chrysoperla externa to initiate our stock colony and to Dr. Penny Gullan (The Australian National University) for identifying the mealybug species. Special thanks to Dr. Janice Matthews and Robert Matthews (University of Georgia) for their comments and suggestions on the manuscript. This work was partially supported by the ‘‘Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE)” and by the ‘‘Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”. References Afifi, A.I., El Arnaouty, S.A., Attia, A.R., AbdAlla Ael, M., 2010. Biological control of citrus mealybug, Planococcus citri (Risso) using the coccinellid predator, Cryptolaemus montrouzieri Muls. Pak. J. Biol. Sci. 5, 216–222.

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