Agriculture, Ecosystems and Environment 181 (2013) 206–212 Contents lists available at ScienceDirect Agriculture, Ecosystems and Environment jo urnal homepage: www.elsevier.com/locate/agee Detecting pest control services across spatial and temporal scales ∗ Rebecca Chaplin-Kramer , Perry de Valpine, Nicholas J. Mills, Claire Kremen Department of Environmental Science, Policy & Management, University of California, Berkeley, 130 Mulford Hall #3114, Berkeley, CA 94720, USA a r t i c l e i n f o a b s t r a c t Article history: Natural habitat may deliver ecosystem services to agriculture through the provision of natural enemies Received 14 May 2013 of agricultural pests. Natural or non-crop habitat has strongly positive effects on natural enemies in Received in revised form 2 October 2013 cropland, but the resulting impact on pests is not as well established. This study measured weekly natural Accepted 4 October 2013 enemy (syrphid fly larvae) and pest (cabbage aphid) abundances in Central California broccoli fields for three years. Abundance of syrphid fly larvae increased strongly with the proportion of natural habitat Keywords: surrounding the farm. As the density of syrphid fly larvae increased, weekly aphid population growth Biological control rates slowed, such that aphid densities just prior to harvest were lowest in farms with natural habitat. Brevicoryne brassicae These landscape-mediated impacts of syrphids on aphids were not evident when data were aggregated Ecosystem services into annual averages, a common metric in research on pest control services. We suggest that higher Landscape complexity Syrphidae temporal resolution of data for natural enemy and pest abundance can reveal top–down control that is Trophic ecology otherwise masked by seasonal and interannual variation in environmental factors. © 2013 Elsevier B.V. All rights reserved. 1. Introduction The challenge in detecting pest control services lies in differ- entiating the role of natural enemies from that of many other Natural enemies, the predators and parasitoids of agricul- variables that can influence pest distributions, such as climate, tural pests, provide a valuable ecosystem service to agriculture host plant presence, resource concentration and dispersal patterns through reduction or control of pest populations. Yet the magni- (Rusch et al., 2010), when all can vary across a landscape gradi- tude of top–down control operating in managed ecosystems and ent. Many studies investigating landscape effects on pest control the extent to which these dynamics are influenced by farm and take only a snapshot of pest and enemy densities at one point landscape characteristics is not always clear, hindering more accu- during the season, or combine multiple samples into one aver- rate assessments of the importance and value of trophic ecology age or cumulative measure, or limit their study period to one year in food production. Natural enemies may forage far beyond farm (Chaplin-Kramer et al., 2011b). When population growth is mea- boundaries and rely on nearby natural habitat. Understanding the sured, it is often between only two time periods during the season full picture of predator–prey relationships therefore requires a (Rand and Tscharntke, 2007; Roschewitz et al., 2005; Thies et al., landscape-scale perspective (Tscharntke et al., 2007). Despite a 2005, 2011). Such measurements may not provide the temporal well-established trend of natural enemy diversity and abundance resolution needed to document pest control that is actually occur- increasing in response to landscape-level habitat complexity, pest ring, which could account for the disconnect between the positive abundance does not show as strong or as consistent a response effects of landscape complexity on natural enemy communities (Chaplin-Kramer et al., 2011b). This apparent lack of a generaliz- and the absence of a concomitant effect on pest communities and able trend suggests either that top–down control is not operating in pest control (Tylianakis et al., 2006). Indeed, the few studies ana- these systems, or that the level of control that exists is undetectable lyzing multiple samples over a season and/or over multiple years by common sampling methods. Our study uses detailed analyses of have emphasized the importance of incorporating seasonal and pest and natural enemy densities across space and time to exam- interannual variation in their analyses (Dib et al., 2010; Menalled ine the relationship between natural habitat, trophic dynamics, and et al., 2003; Oberg et al., 2008; Östman et al., 2001; Prasifka et al., pest control services. 2004; Romeu-Dalmau et al., 2012; Schmidt and Tscharntke, 2005a). Therefore, it may be necessary to compare population growth tra- jectories rather than simply abundances, to elucidate the role of natural enemies in controlling pest populations that vary endoge- nously in space and time. ∗ Corresponding author. Present address: Natural Capital Project, Woods Institute Here, we investigate the role natural habitat plays in the pop- for the Environment, Stanford University, 371 Serra Mall, Stanford, CA 94305, USA. ulation dynamics of cabbage aphids (Brevicoryne brassicae) and Tel.: +1 831 331 6015. their syrphid predators (Diptera: Syrphidae) in broccoli (Brassica E-mail address: [email protected] (R. Chaplin-Kramer). 0167-8809/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.agee.2013.10.007 R. Chaplin-Kramer et al. / Agriculture, Ecosystems and Environment 181 (2013) 206–212 207 oleracea, var. italica cv. Gypsy). By analyzing weekly insect samples agriculture; residential; urban or industrial; water). The propor- taken over three years across a landscape gradient, we explore how tional area of natural habitat was then computed at a radius of 0.5, population densities of pests and predators change over time and 1, 1.5, 2, 2.5, and 3 km around the farm site using Hawth’s Tools space. Specifically, our goal was to determine the impact of land- (version 3.27, http://www.spatialecology.com). The proportion of scape complexity on: (1) syrphid communities, (2) aphid densities natural habitat was used as a metric of landscape complexity in sub- on the crops throughout the growing season and just prior to har- sequent analysis, with higher proportions of natural habitat around vest, and (3) suppression of aphid population growth by syrphids. the farm signifying greater landscape complexity. We suggest that this form of analysis is necessary to accurately quantify pest control services that may otherwise be masked by 2.1. Arthropod collection endogenous variation of pest population dynamics. Ten broccoli plants per week were collected at each field site starting four to seven weeks before harvest and continuing every 2. Materials and methods week until harvest. The variation in total weeks sampled occurred because the crops occasionally reached maturity more quickly or This research was conducted in California’s Central Coast region, slowly than the grower’s anticipated schedule. Further, different where nearly half of the broccoli produced in the US is grown. Cab- growers had different planting schedules, and as a result the first bage aphids are a major pest of broccoli and are prey for a number of week of sampling occurred anywhere between May and August natural enemies, including parasitic wasps (Diaeretiella rapae), lady across the study sites. The variable planting dates were unavoid- beetles (Coccinellidae), lacewing larvae (Chrysopidae), spiders, and able due to studying many different farms in different locations. a variety of other coleopteran and hemipteran predators. However, However, there was no significant correlation between sampling the larvae of flies in the family Syrphidae are the most abundant date and farm placement within the landscape gradient, and samp- aphid predator by far in this system (70% of all natural enemies ling date was included as a potential explanatory variable in the were syrphids, across all sites in all three years; unpublished data). analysis. It has been suggested that syrphids may in fact be the most effi- Individual plants and the insects they harbored were collected cient predators of the cabbage aphid (Van Emden, 1963). Adult every 5 m along a 50 m transect for a total of 10 plants per site. syrphid flies are extremely mobile, searching in many different Transects started from the edge of a field with no weeds or insec- habitats for nectar and pollen on which to feed, in order to obtain tary plantings wherever possible, to standardize edge effects in the energy necessary for reproduction (Almohamad et al., 2009; different-sized fields (Kremen et al., 2004). Entire plants were cut at Schneider, 1969). Syrphids also rely on perennial habitats for alter- the base and immediately placed in individual sealed plastic bags, nate (non-crop) prey for their larvae when crop aphid populations and each plant was washed over a sieve to remove and collect are low, shelter from strong wind that would otherwise prevent insects within 48 h of return to the lab. This collection technique their flying, and possibly overwintering habitat (Bugg et al., 2008). ensured that all syrphids inhabiting a plant were detected, as syr- Aphidophagous syrphid flies are therefore an excellent study taxon phid larvae are primarily nocturnal, hiding in the folds of leaves to use to explore the effects of landscape on pest control. during the day (Rotheray, 1986), and may therefore be underesti- The study was conducted on 24 organic