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Growth, Development and Consumption by Four Syrphid Species Associated with the Lettuce Aphid, Nasonovia Ribisnigri, in California ⇑ Julie V

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Growth, Development and Consumption by Four Syrphid Species Associated with the Lettuce Aphid, Nasonovia Ribisnigri, in California ⇑ Julie V Biological Control xxx (2011) xxx–xxx Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Growth, development and consumption by four syrphid species associated with the lettuce aphid, Nasonovia ribisnigri, in California ⇑ Julie V. Hopper , Erik H. Nelson, Kent M. Daane, Nicholas J. Mills Department of Environmental Science, Policy and Management, Mulford Hall, University of California, Berkeley, CA 94720-3114, USA article info abstract Article history: The lettuce aphid, Nasonovia ribisnigri Mosley, was accidentally introduced into California from Europe Received 1 November 2010 during the late 1990s and soon became an economic pest of Romaine lettuce along California’s central Accepted 25 March 2011 coast region. Indigenous syrphid larvae attack the lettuce aphid and are believed to be effective in the Available online xxxx management of this invasive pest, although there have been no studies on the capacity of the syrphid lar- vae to kill and consume lettuce aphids. We focused on four syrphid species commonly found in central Keywords: coast lettuce fields: Allograpta obliqua (Say), Eupeodes fumipennis (Thomson), Sphaerophoria sulphuripes Biological control (Thomson), and Toxomerus marginatus (Say). Laboratory feeding experiments were conducted to estimate Aphididae the development times of all juvenile stages, the daily growth rate of larvae, the number of third instar Syrphidae Predation potential aphids killed, the aphid biomass killed, and the aphid biomass consumed as measures of predator perfor- Lettuce mance. Results show that during larval development E. fumipennis killed the most third-instar aphids (507 aphids, 88 mg biomass killed) and reached the largest size, followed by A. obliqua (228 aphids, 39 mg killed), S. sulphuripes (194 aphids, 31 mg killed) and T. marginatus (132 aphids, 20 mg killed). Body size alone did not account for species differences in per-capita larval consumption rates. This information is discussed in relation to the predation potential of syrphids through the short cropping cycle of lettuce, and the choice of plant species to use for floral resource provisioning to enhance the activity of syrphids needed for effective management of lettuce aphids in California’s central coast fields. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction Syrphid larvae are an important group of aphid natural enemies (Brewer and Elliott, 2004; Freier et al., 2007; Haenke et al., 2009; The lettuce aphid, Nasonovia ribisnigri Mosley, was accidentally Tenhumberg and Poehling, 1995; Winder et al., 1994) and several introduced into California from Europe during the late 1990s and field studies have demonstrated a direct relationship between syr- has become an important pest of Romaine lettuce. Nasonovia ribis- phid egg and larvae densities and reductions in aphid densities in nigri can be difficult to control as it is characterized by rapid dis- agricultural crops (Freier et al., 2007; Smith et al., 2008; Tenhum- persal and colonization of the innermost leaves of the lettuce berg and Poehling, 1995). Syrphid flies are also commonly associ- head (Parker et al., 2002), which provide a refuge from many nat- ated with the lettuce aphid along the central coast of California ural enemy species. Although insecticide application(s) has been a (Smith and Chaney, 2007). However, many field-level conditions standard management practice for N. ribisnigri (Natwick et al., in the lettuce crop influence the level of aphid suppression pro- 2008), it has not always been effective due to poor accessibility vided by natural enemies. For example, if natural enemies fail to of aphids within the head of the lettuce and the development of colonize and suppress the aphid colonies early in the Romaine let- insecticide resistance (Parker et al., 2002). For these reasons, the tuce growth cycle, the plant growth can enclose the aphids, provid- potential to utilize natural enemies more effectively has become ing the pest some protection from natural enemies (Bugg et al., of increasing interest in the management of the lettuce aphid. In 2008). California, a number of indigenous natural enemy species have California’s organic lettuce growers have used floral resources found this invasive aphid to be a suitable new resource and, for this to increase numbers of syrphid larvae in their fields (Bugg et al., reason, have attracted attention for their potential role in lettuce 2008; Chaney, 1998; Smith et al., 2008). Whereas syrphid larvae aphid biological control. depend on the consumption of aphids for growth and survival, adult syrphids rely on aphid honeydew and/or floral nectar and pollen for energy and egg production (Smith et al., 2008). Floral re- sources are well known to be beneficial in attracting predators and ⇑ Corresponding author. Fax: +1 510 643 5438. parasitoids to agroecosystems (Gurr et al., 2004; Landis et al., E-mail address: [email protected] (J.V. Hopper). 2005; Robinson et al., 2008; Wackers and Van Rijn, 2005). Flower 1049-9644/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.03.017 Please cite this article in press as: Hopper, J.V., et al. Growth, development and consumption by four syrphid species associated with the lettuce aphid, Nasonovia ribisnigri, in California. Biological Control (2011), doi:10.1016/j.biocontrol.2011.03.017 2 J.V. Hopper et al. / Biological Control xxx (2011) xxx–xxx color, morphology, size, odor, nectar and pollen load, age, remnants We collected gravid female A. obliqua, E. fumipennis, S. sulphur- of previous visitors, or interactions with other pollinators or preda- ipes and T. marginatus from two locations in California: Hollister tors, can all influence which syrphid species visit a floral resource and Berkeley. Field-collected syrphid females were placed individ- (Ambrosino et al., 2006; Colley and Luna, 2000; Haslett, 1989; ually in clear polypropylene oviposition containers (947 ml Pro- Sutherland et al., 1999). The most common insectary plant cur- KalÒ) with a ventilated polypropylene lid (8.0 mm2 polyester rently used in lettuce fields is sweet alyssum (Lobularia maritima mesh). Each container was provisioned with diluted honey (L.) Desv.) (Smith and Chaney, 2007). (0.01% sorbic acid, 10% honey, 89.99% water) in a small cotton- The use of floral resources to enhance syrphid activity, through wool stoppered plastic cup (22.2 ml SOLOÒ, Highland Park, IL), conservation biological control, is based on the assumption that and a lettuce leaf with 10 N. ribisnigri of mixed instars that re- these natural enemies will respond at a sufficient level of abun- mained alive during the syrphid oviposition period (1–4 days). dance and per capita predation to suppress the aphid population Eggs from the oviposition cages were collected daily and used for and lessen crop damage. While it is known that insectary plantings observations on development, larval growth and consumption of do attract a greater abundance of adult syrphids in lettuce fields in the four syrphid species, using eggs from different females when- California (Smith et al., 2008), the species attracted vary consider- ever possible. Ovipositing female syrphids were subsequently fro- ably in size, and their per capita capacity for predation of the let- zen and used as vouchers to verify the identity of each species. tuce aphid remains unknown. The importance of per capita capacity for predation is well illustrated from a study of syrphid 2.2. Syrphid development, larval growth and consumption predators of Aphis fabae Scopoli in which different species varied considerably in their larval consumption rates (Sood et al., 2007). All life stages of each syrphid species were maintained at In addition, other studies have demonstrated a positive relation- 19.3 °C (±0.6 SD) and a 16:8 h L:D photoperiod approximating ship between larval body size and prey consumption for syrphid average mid summer conditions in Hollister lettuce fields. Newly species (Hagvar, 1974; Tinkeu and Hance, 1998). laid eggs were placed in separate plastic Petri dishes The goal of this study was to quantify the growth, development (3.5 Â 1.0 cm), provided with a fresh disk of lettuce (3.2 cm diam- and larval consumption rates of syrphid larvae under laboratory eter) and several aphids each day, and monitored every 24 h until conditions as an important step toward understanding the potential hatching. After hatching, larvae were left undisturbed for 24 h as of different syrphid species to control populations of N. ribisnigri in they were too fragile to be handled experimentally. Subsequently, lettuce fields in California. A variety of approaches can be used to individual larvae were provided with a fresh disk of lettuce, and a estimate the per capita larval consumption rates of predators, either new set of aphids each day until they completed their larval devel- in the laboratory or in the field (Mills, 1997, 2005), and both meth- opment. Sample sizes of individuals that completed development odology and choice of measurement variable (number or biomass of to pupation were 17 for A. obliqua, 15 for E. fumipennis, 11 for S. sul- prey killed or consumed) can influence the estimates obtained (La- phuripes, and 8 for T. marginatus. All individuals were checked daily tham and Mills, 2009). While it is often best to estimate the con- until adult emergence to provide estimates of development time sumption rate of predators through direct field observation for each life stage, and fresh weight was measured daily (Sartorius (Costamagna and Landis, 2007; Latham and Mills, 2010), this is less 1801 microbalance with an accuracy of ±0.1 mg) to estimate larval practical for syrphid larvae as they are commonly nocturnal in their growth rates. activity. Here, we focused on four of the more common syrphid spe- Larval consumption was monitored for syrphid larval ages of cies found in California’s central coast lettuce fields: Allograpta obli- days, 2, 3, 5, 7, and then every other day thereafter until pupation.
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