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Do Differences in Food Web Structure Between Organic and Conventional Farms Affect the Ecosystem Service of Pest Control?

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Do Differences in Food Web Structure Between Organic and Conventional Farms Affect the Ecosystem Service of Pest Control? Ecology Letters, (2009) 12: 229–238 doi: 10.1111/j.1461-0248.2008.01279.x LETTER Do differences in food web structure between organic and conventional farms affect the ecosystem service of pest control? Abstract Sarina Macfadyen,1 Rachel While many studies have demonstrated that organic farms support greater levels of Gibson,1 Andrew Polaszek,2 biodiversity, it is not known whether this translates into better provision of ecosystem Rebecca J. Morris,1,3 Paul services. Here we use a food-web approach to analyse the community structure and 4 5 G. Craze, Robert Planque´ , function at the whole-farm scale. Quantitative food webs from 10 replicate pairs of William O.C. Symondson6 and 1 organic and conventional farms showed that organic farms have significantly more Jane Memmott * species at three trophic levels (plant, herbivore and parasitoid) and significantly different 1School of Biological Sciences, network structure. Herbivores on organic farms were attacked by more parasitoid species University of Bristol, Woodland on organic farms than on conventional farms. However, differences in network structure Road, Bristol BS6 7EU, UK 2Department of Entomology, did not translate into differences in robustness to simulated species loss and we found no Natural History Museum, difference in percentage parasitism (natural pest control) across a variety of host species. London SW7 5BD, UK Furthermore, a manipulative field experiment demonstrated that the higher species 3Department of Zoology, richness of parasitoids on the organic farms did not increase mortality of a novel University of Oxford, South herbivore used to bioassay ecosystem service. The explanation for these differences is Parks Road, Oxford OX1 3PS, UK likely to include inherent differences in management strategies and landscape structure 4Biology and Environmental between the two farming systems. Science, University of Sussex, Brighton BN1 9QG, UK Keywords 5 Department of Mathematics, Agro-ecology, biodiversity, networks, parasitoid diversity, species interactions. VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands 6Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3US, UK *Correspondence: E-mail: [email protected] Current address: CSIRO Entomology, Black Mountain, GPO Box 1700, Canberra, ACT 2601, Australia Ecology Letters (2009) 12: 229–238 a large pool of species is necessary to maintain the INTRODUCTION functioning of ecosystems, especially in intensive agricul- The extent to which biodiversity can be lost before it affects tural landscapes (Loreau et al. 2001; Tscharntke et al. 2005). the provision of ecosystem services is unclear. Services such For example, for insect pollinators, maintaining a diversity as natural pest control are the result of the complex network of species is essential for sustaining plant pollination of interactions among species in a community. These services because of yearly variations in community compo- services provide substantial, if not invaluable economic sition (Kremen et al. 2002). For the service of natural pest benefits to humans particularly in food production (Losey & control the situation is more complex. Snyder et al. (2006) Vaughan 2006; Klein et al. 2007). Many studies suggest that found that a greater number of predator species increased Ó 2008 Blackwell Publishing Ltd/CNRS 230 S. Macfadyen et al. Letter aphid suppression, but in contrast Rodriguez & Hawkins changes to community structure, species interactions and (2000) found that species-rich parasitoid communities did ecosystem function (Tylianakis et al. 2007). Furthermore, not result in higher parasitism rates than species-poor these descriptors tell us little about the functioning of an communities. Rather it seems that at least in some host– ecosystem or the provision of essential services (Kremen parasitoid communities, one or a few species drive the 2005; Tscharntke et al. 2005). Ecological networks such as dynamics of the system with additional species contributing food webs provide a powerful tool for examining complex little to pest control (Hawkins 1994). communities of species that interact across trophic levels Governments worldwide are investing heavily in and are essential for revealing the functional components schemes that aim to reverse the trend of declining of biodiversity (McCann 2007). Here, our aim is to use a biodiversity in intensive agricultural landscapes (Benton food-web approach to characterize both community et al. 2002; Carvell et al. 2007; Whittingham 2007). Wide- structure and function on replicate organic and conven- scale conversion to organic farming has been suggested as tional farms, with networks described at the scale of entire one means for reversing the process of agricultural farms. Biodiversity studies in agro-ecosystems have usually intensification, and is thought to lead to increased diversity been carried out at the field scale (e.g. Pocock & Jennings of up to 30% for some taxa (Bengtsson et al. 2005; Hole 2008; Firbank et al. 2003). However, such field-scale et al. 2005). Organic farms generally have specific crop comparisons may be inappropriate if there are emergent rotations, greater areas of semi-natural vegetation (Gibson properties at the whole-farm scale (Vandermeer 1997). et al. 2007) and do not use synthetic pesticides (Lampkin Quantifying the interactions between species at the 1999). Pest control on organic farms relies largely on community level is a unique approach and reflects our cultural practices and naturally occurring predators and aim to study the community function as well as commu- parasitoids to control insect pest outbreaks. If organic nity structure. Our objectives are fourfold: (1) to use food farms support higher levels of biodiversity, they may be webs from replicated farms to determine whether organic better protected against the effects of invasion by alien farms are more species rich than conventional farms at species (including novel pest species) through biotic three trophic levels sampled at the scale of whole farms. resistance. There is evidence that as species richness Given that previous studies have demonstrated that increases, resistance to invasion increases (Kennedy et al. organic farms support greater levels of biodiversity 2002). Consequently organic farms that have higher (Bengtsson et al. 2005; Hole et al. 2005), we predict that biodiversity (in the form of more species of predators, our organic farms will have higher species richness at all parasitoids and pathogens) may be better protected against three trophic levels in comparison with our conventional novel pests in comparison with their conventional coun- farms. (2) To determine whether the two farming systems terparts. However, ecological theory indicates that organic have a different network structure. Here our predictions farms may be more vulnerable to extinction cascades. are twofold: first, that as a consequence of their higher Connectance is a measure of network complexity and is species richness, the organic farms will have lower calculated as the number of realized links divided by all connectance than conventional farms; second, given that potential links in the network. General relationships organic farms are expected to provide greater levels of between connectance and the number of species in a natural pest control, we predict that more parasitoid network are still unclear (Martinez 1993; Murtaugh & species will attack each herbivore species. (3) To use a field Kollath 1997). However, Dunne et al. (2002) demonstrated experiment to test whether organic farms provide a more that in ecological networks, robustness to simulated species effective ecosystem service of natural pest control. We loss increases with network connectance. Networks with predict that the higher species richness of parasitoids on high connectance seem to delay the onset of the threshold the organic farms provides biotic resistance (e.g. Kennedy past, which they display extreme sensitivity to the removal et al. 2002) to the invasion of alien herbivores and thereby of species (Dunne et al. 2002). In general, as insect- the establishment of novel pests. (4) To test the robustness dominated networks become more species rich (assuming of organic and conventional farms to species loss. Here we a similar composition of generalist to specialist consumers), predict that the lower connectance on the organic farms connectance decreases in an exponential curve (Schoenly will lead to the networks being less robust to species loss et al. 1991), suggesting that organic farms that support (Dunne et al. 2002). greater levels of biodiversity may be less robust to species loss in comparison to their conventional counterparts. MATERIALS AND METHODS Traditionally descriptors such as species richness, species abundance and diversity indices have been used to assess Ten pairs of organic and conventional farms were chosen in the anthropogenic impact on natural communities. How- south-west England. Organic farms had been certified as ever, these descriptors may fail to detect important organic for an average of 7.3 years (range 3–12 years) at the Ó 2008 Blackwell Publishing Ltd/CNRS Letter Provision of ecosystem services from farm food webs 231 start of the study. All were mixed farms, with arable crops, than c. 2.5 m) was visually inspected, sweep netted, and if pasture and livestock and had similar soil types. Organic tall enough, beaten over a beating tray and all leaf-mining farms
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