Host quality of different aphid species for rearing Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)

BIOLOGICAL CONTROL

Host quality of different aphid species for rearing Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)

RJ Silva; FJ Cividanes; EC Pedroso; SRD Sala

Depto Fitossanidade, FCAV/UNESP, Jaboticabal, SP, Brasil

^{Correspondence}

ABSTRACT

This study aimed to evaluate the quality of the aphid Myzus persicae (Sulzer), Lipaphis erysimi (Kaltenbach) and Brevicoryne brassicae (L.) as hosts for the parasitoid Diaeretiella rapae (McIntosh). Parasitization by D. rapae was higher on M. persicae than on L. erysimi and B. brassicae. The time of development of D. rapae from egg to mummy or egg to adult male or female were shorter on M. persicae than on L. erysimi and B. brassicae. Moreover, D. rapae showed no significant differences in the emergence rate, sex ratio and longevity when reared on the three aphid species. Myzus persicae was the largest aphid host, with B. brassicae and L. erysimi being of intermediate and of small size, respectively. Diaeretiella rapae reared on M. persicae was larger than when reared on L. erysimi and B. brassicae, and females of D. rapae were significantly larger than males on M. persicae, but males of D. rapae were larger than females when reared on L. erysimi. No difference in size was detected between males and females in parasitoids reared on B. brassicae. Among the aphid species studied, M. persicae was found to be the most suitable to D. rapae.

Keywords: Brassicaceae, glicosinolate, Myzus persicae, Lipaphis erysimi, Brevicoryne brassicae

Introduction

Aphidiinae endoparasitoids (Braconidae) are the most widely used natural enemies in biological control programs against aphids. In Brazil, studies on aphidiine parasitoids for aphid control were focused on Aphidius colemani Viereck a biocontrol agent of Aphis gossypii Glover and Myzus persicae (Sulzer) (Sampaio et al 2001a,b), Lysiphlebus testaceipes (Cresson) (Silva et al 2008a,b) and Praon volucre (Haliday) (De Conti et al 2008). It is noteworthy that the country has scarce information about the use of the aphidiine parasitoid Diaeretiella rapae (McIntosh) in aphid control. This species is considered a specialist on aphids associated with crucifers (Blande et al 2004), being reported in Brazil as the main parasitoid of Brevicoryne brassicae (L.), Lipaphis erysimi (Kaltenbach) and M. persicae (Sousa & Bueno 1992, Mussury & Fernandes 2002, Resende et al 2006). Diaeretiella rapae also occurs associated with other species of aphids in different crops and it is distributed in several states in Brazil (Starý et al 2007).

To assess host suitability and to accept a host for oviposition, aphidiine parasitoids use a number of host-derived cues, such as shape, color, odor, taste and movements (Mackauer et al 1996, Blande et al 2007). Nutritional and physiological characteristics of the host directly affect development, mortality, longevity and fecundity of natural enemies such as parasitoids (Roitberg et al 2001). Because immature stages of hymenopteran parasitoids rely on the nutrients present in host insects (Mackauer & Sequeira 1992), parasitoid females oviposit on a particular host when it presents nutritional and physiological requirements for the development of their offspring. Also, larvae of the parasitoids rely on their mother's ability to access the host quality to ensure their development (Mackauer et al 1996).

Several studies have demonstrated the importance of glucosinolates (GS) from crucifers as indicators of the quality of the host plant to herbivorous insects (Moyes et al 2000, Gols et al 2008). These compounds also play a role in the plant defense against insect herbivores (Rask et al 2000) and can indirectly affect predators and parasitoids, causing a cascade effect (Francis et al 2001, Goals et al 2009). Recently, it has been investigated the use of chemical signals from glucosinolates by parasitoids to locate their hosts, habitats and to evaluate host quality (Blande et al 2004, 2007, 2008).

Generalist herbivores produce enzymes that can detoxify a wide range of substrates (Krieger et al 1971), whereas specialists evolved an enzymatic system able to detoxify defensive plant compounds (Ratzka et al 2002). Thus, generalist herbivores are usually more sensitive to high levels of specific allelochemicals as compared to specialists (Giamoustaris & Mithen 1995). Specialists feeding on brassicaceous plants are adapted to glucosinolates-containing plants, and they can detoxify, excrete, or even sequester these harmful metabolites (Ratzka et al 2002, Wittstock et al 2004).

The high potential of D. rapae as a biological control agent against aphids in various crops, including crucifers, has been already indicated (Lara et al 1999, Mussury & Fernandes 2002, Vaz et al 2004). But for the establishment of a successful biological control program of aphids through the use of parasitoids, several bioecological aspects of the selected natural enemy, such as, the suitability of host species that are candidates to host for parasitoid mass rearing are required. As little is known on D. rapae in Brazil, this study aimed to evaluate the host suitability of three aphid species that feed on Brassica oleraceae plants, the generalist M. persicae and the specialists L. erysimi and B. brassicae, to D. rapae.

Material and Methods

Rearing the aphid hosts

Myzus persicae, L. erysimi and B. brassicae were collected from Brassicaceae plants in the region of Jaboticabal (21º15'22"S, 48º18'58"W), state of São Paulo. Aphids were reared on Brassica oleracea var. acephala cultivar Georgia in 500 ml pots in wooden framed cages (45 x 50 x 70 cm) coverage by cheesecloth, and maintained in a greenhouse. Adult females from the stock colonies were used to obtain nymphs for the experiments.

Rearing the parasitoid D. rapae

Aphid mummies of M. persicae, L. erysimi and B. brassicae were collected in Brassicaceae plants at the same localities as the aphids. The mummies were individualized in glass tubes (80 x 19 mm) and kept at 25 ± 1ºC, 60 ± 10% RH and 12h photophase. Adults of D. rapae were sexed and released inside wooden cages (described earlier) containing potted plants of B. oleracea var. acephala cultivar Georgia individually infested with M. persicae, L. erysimi or B. brassicae. Stock colonies of D. rapae were maintained on each aphid host species studied. Honey was offered daily as a food source for adult parasitoids.

Quality of M. persicae, L. erysimi and B. brassicae as hosts of D. rapae

Experiments were conducted in a climate chamber at 25 ± 1ºC, 60 ± 10% RH and 12h photophase. Fifteen, 0-24h-old, mated, naive females of D. rapae were individually released in Petri dishes (5 cm in diameter) containing 20, 3 d-old nymphs of either M. persicae, B. brassicae or L. erysimi for parasitization. Aphids were offered on a kale leaf disc on a layer of a 1% agar-water solution. Parasitoid females were allowed to parasitize for 60 min afterwards, females were removed and the aphid nymphs were maintained inside the chambers for the complete development of parasitoids.

The development time from egg to mummy and from egg to adult parasitoid was determined. The mummified aphids were counted and individualized in glass tubes (80 x 19 mm) to assess parasitization, emergence, and sex ratio. The longevity of D. rapae was evaluated from 15 males and 15 females randomly selected. They were fed daily with honey and water deposited on the walls of the rearing glass tubes.

Host and parasitoid sizes were determined based on the length of their hind tibia, as tibia length is considered an appropriate indicator of the size of aphids (Nicol & Mackauer 1999, Van Emden & Kifle 2002) and aphidiine parasitoids (Nicol & Mackauer 1999). Host and parasitoid sizes were also used as indicators of the suitability of each aphid species as a host to D. rapae.

Second-instars of M. persicae, L. erysimi and B. brassicae were kept in Petri dishes (15 cm in diameter) containing a kale leaf disc laid on top of a layer of a 1% agar-water solution. From a single colony of each aphid species, 15 nymphs were collected and they right posterior tibiae were removed. Other 60 to 80 nymphs were offer to a newly-emerged, mated female of D. rapae. for 60 min. Parasitized nymphs were maintained at constant temperature and RH (described earlier) until mummification, when they were transferred to separate glass tubes (80 x 19 mm) for parasitoid emergence. Fifteen males and 15 females of parasitoid adults obtained from each particular host were randomly collected for the removal and measurement of the right hind tibia.

The tibiae of both nymphs and parasitoids were mounted between a glass slide and a coverslip in 70% ethanol and immediately measured with micrometers adapted to a microscope.

Data analysis

The experiments were conducted in a completely randomized design using a 2 × 3 factorial design (2 sexes × 3 hosts). All variables (parasitization, development periods, percentage of adult emergence, sex ratio, longevity and size) were analyzed by ANOVA followed by a Tukey test at 5% significance level, using the softwares SAS v.9.0. and AgroEstat v.1.0.

Results and Discussion

The parasitization of the aphid species studied by D. rapae ranged from 42.5% to 66.5%, and was significantly higher on M. persicae than on L. erysimi and B. brassicae (F = 4.91, P < 0.05) (Table 1). Generally, the highest percentage of parasitism may be an indication of host quality. Aphids with better quality provide better conditions for aphidiine females to lay a large amount of eggs (Silva et al 2008a). This can also be characterized by the largest number of stings with ovipositor made by the female parasitoid at the time of laying the eggs (Sampaio et al 2001a). However, host acceptance does not necessarily correlates with host quality, as demonstrated for other aphidiine species (Chau & Mackauer 2001, Henry et al 2005, Sampaio et al 2008). The developmental time is also an indication of host quality, and development from egg to mummy (F = 28.13, P < 0.0001), from egg to adult-male (F = 12.04, P < 0.0001) and egg to adult-female (F = 3.74, P < 0.0001) of D. rapae were consistently shorter in M. persicae than in L. erysimi and in B. brassicae (Table 1).

The percentage of parasitism and the development time of D. rapae on B. brassicae (Table 1) were similar to those obtained by Bayhan et al (2007) (40.2% and 11.6 d, respectively), but our data on M. persicae and L. erysimi contradict those obtained by Blande et al (2004), that reported a higher parasitism rate of D. rapae on L. erysimi than on M. persicae. This controversy may be related to the genetic variation among populations of D. rapae and their hosts from different geographic regions (Antolin et al 2006, Baer et al 2004). Another possible explanation is the use of different host plants (Bayhan et al 2007), as Blande et al (2004) reared M. persicae and L. erysimi on turnip, Brassica rapa var rapifera cv Tokyo Cross. The differential effect of host plants on host and parasitoid fitness may also be related to their glucosinolate composition, as the glucosinolates produced by Brassicaceae are hydrolyzed by the enzyme myrosinase under herbivore attack, leading to the production of isothiocyanates, thiocyanates and nitriles, which play a defensive role against herbivory (Rask et al 2000, Fahey et al 2002, Halkier & Gershenzon 2006). It is noteworthy that the profile of glucosinolates in Brassica varies significantly among and within populations (Moyes et al 2000, Newton et al 2009). Glucosinolates are known to affect the performance of insect herbivores and the third trophic level depending on their degree of specialization (Gols et al 2008).

Specialist crucifer-feeding aphids, such as L. erysimi and B. brassicae, can synthesize the enzyme myrosinase (MacGibbon & Beuzenberg 1978, Jones et al 2001), which is compartmentalized into microbodies within muscles in the thorax and head of aphids (Bridges et al 2002). Therefore, L. erysimi and B. brassicae have developed the ability to sequester, accumulate and hydrolyze glucosinolates, avoiding their toxic effects, utilizing them to their own benefit as chemical defenses against natural enemies (Husebye et al 2005). On the other hand, the generalist aphid M. persicae can only tolerate the negative effects of glucosinolates, which are quickly eliminated through the gut and excreted with the honeydew (Weber et al 1986). These strategies to handle glucosinolates from the host plant may explain the better performance of D. rapae when reared on M. persicae as opposed to L. erysimi and B. brassicae, suggesting a possible influence of glucosinolates in the immature stages of parasitoids.

Male and female of D. rapae had similar development time from egg to adult regardless the host aphid species (M. persicae - F = 0.20, P > 0.05; L. erysimi - F = 0.00, P > 0.05; B. brassicae - F = 0.01, P > 0.05) (Table 1). There were no significant differences in immature survivalship (F = 2.33, P > 0.05), sex ratio (F = 0.12, P > 0.05) and adult longevity (males - F = 1.30, P > 0.05; females - F = 0.74, P > 0.05) of D. rapae among the three host aphid species (Table 1). Also, the development time and longevity of males and females of D. rapae did not differ one from another in each host species (M. persicae - F = 0.01, P > 0.05; L. erysimi - F = 2.51, P > 0.05; B. brassicae - F = 1.89, P > 0.05) (Table 1).

The host size was positively correlated with the parasitoid size, as observed for other aphidiine parasitoids (Sampaio et al 2008, Silva et al 2008b, De Conti et al 2008). Myzus persicae was the largest aphid (0.454 mm), followed by B. brassicae (0.327 mm) and L. erysimi (0.296 mm) (F = 154.16, P < 0.0001) (Table 2), as observed elsewhere (Sampaio et al 2008). Myzus persicae yielded the largest adults of D. rapae, with males as large as 0.546 mm (F = 12.87, P < 0.0001) and females as large as 0.582 mm (F = 23.00 P < 0.0001), as given by their tibial length. Parasitoids obtained in here were much larger than those reported by Blande et al (2004) by rearing D. rapae on the same host aphid species (males = 0.49 mm; females = 0.51 mm).

Males and females of D. rapae showed no significant differences in their tibial length when reared on B. brassicae (F = 0.51, P > 0.05) (Table 2). However, males reared from L. erysimi were larger than females (F = 8.09, P < 0.01), while females reared from M. persicae were larger than males (F = 10.19, P < 0.01) (Table 2). The fact that the smallest aphid host L. erysimi yielded larger males than females differs from the pattern observed in aphidiine parasitoid species, in which females are generally larger than males (Sequeira & Mackauer 1993, Mackauer 1996). Female aphidiine parasitoids can obtain and accumulate more resources per unit time than males, achieving, thus, larger sizes in smaller hosts (Sampaio et al 2008). In this study the opposite was observed, as males of D. rapae were more successful than females to allocate resources, reaching larger sizes in the smaller host L. erysimi (Table 2). Size variation between males and females of aphidiine parasitoids are usually more conspicuous when these parasitoids are reared in smaller hosts and tends to decrease as the host size increases (Sequeira & Mackauer 1993, Mackauer 1996, Sampaio et al 2008). This finding was not observed in this study because males and females of D. rapae showed a significant difference in size when reared on the largest and smallest hosts (Table 2).

Diaeretiella rapae reared on M. persicae showed a higher percentage of parasitism, the shortest period of development and a larger size. Generally, larger hosts are preferred and provide better quality for aphidiine parasitoids, leading to the development of larger individuals, which have a competitive advantage over those that developed in smaller hosts (Cloutier et al 2000, Chau & Mackauer 2001). However, host size may not necessarily correlate with host quality for parasitoid development. Certain biological traits of parasitoids, as their reproductive capacity and longevity, are not directly related to host size, but with the ability of larvae to obtain the available resources from the host (Sequeira & Mackauer 1992, 1994).

Our data on D. rapae showed that the host aphid species M. persicae, L. erysimi and B. brassicae were nutritionally and physiologically suitable for parasitoid development, but M. persicae was considered the best host among the species tested (larger adults, higher parasitization capacity, shorter development time).

It should be emphasized the need for new studies to clarify the influence of glucosinolates on D. rapae biology. The available information refers to the indirect effects of these compounds as chemical signals, mainly in the foraging behavior of D. rapae female. Our data suggest that glucosinolates can act not only indirectly on the parasitoid, but also directly, increasing the defense mechanisms of crucifer-feeding specialists aphids through bioaccumulation, or influencing the quality of aphids to parasitoids.

Acknowledgments

To Dr Marcelo Teixeira Tavares (UFES - Vitória/ES) for identifying the parasitoid species, Dr. Carlos Roberto Sousa Silva (UFSCar - São Carlos/SP) for the identifying the aphids, to Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for providing a PhD scholarship to the first author (Proc.: 2007/05467-3) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for to the second author (Proc.: 304930/2009-1).

Received 01 December 2010 and accepted 11 April 2011

Edited by Madelaine Venzon – EPAMIG

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Publication Dates

• Publication in this collection
  14 Sept 2011
• Date of issue
  Aug 2011

History

• Accepted
  11 Apr 2011
• Received
  01 Dec 2010