Bulletin of Entomological Research (2006) 96, 637–645 DOI: 10.1079/BER2006467 Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles W.O.C. Symondson1 *, S. Cesarini1, P.W. Dodd1, G.L. Harper1y, M.W. Bruford1, D.M. Glen2·, C.W. Wiltshire3 and J.D. Harwood1z 1Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK: 2IACR-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol, BS41 9AF, UK: 3Arion Ecology, The Brambles, Stinchcombe Hill, Dursley, Gloucestershire, GL11 6AQ, UK Abstract Environment-friendly farming techniques seek to increase invertebrate biodi- versity in part with the intention of encouraging greater numbers of predators that will help to control crop pests. However, in theory, this effect may be negated if the availability of a greater abundance and diversity of alternative prey diverts predators away from feeding on pests. The hypothesis that access to alternative prey can lead to reduced pest suppression under semi-field conditions was tested. Alternative prey type and diversity were manipulated in 70 mesocosms over 7+ weeks in the presence of the carabid Pterostichus melanarius (Illiger), a known predator of slugs, and reproducing populations of the slug Deroceras reticulatum (Mu¨ ller). Significantly fewer slugs survived where no alternative prey were provided. Maximum slug numbers and biomass were found in treatments containing either carabids plus a high diversity of alternative prey (many species of earthworm and three of Diptera larvae) or a single additional prey (blowfly larvae, Calliphora vomitoria Linnaeus). In these treatments slug numbers and biomass were as high as in plots lacking predators. The effects of alternative prey were taxon-specific. Alternative prey strongly affected carabid fitness in terms of biomass and egg load. The fittest predators (those with access to high alternative prey diversity or C. vomitoria larvae) reduced slug numbers the least. The mean individual slug weights were greater in treatments with alternative prey than where no alternative prey were provided to the carabids. These results suggest that pests may survive and reproduce more rapidly in patches where predators have access to alternative prey. *Fax: +44 (0)29 20 874 305 E-mail: [email protected] ·Honorary Professor of Cardiff University and independent consultant at Styloma Research and Consulting, Phoebe, The Lippiatt, Cheddar, BS27 3QP, UK yPresent address: School of Applied Sciences, University of Glamorgan, Pontypridd, Mid-Glamorgan, CF37 1DL, UK zPresent address: Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY 40546-0091, USA 638 W.O.C. Symondson et al. Keywords: Carabidae, Deroceras reticulatum, diet, generalist predators, predator fitness, Pterostichus melanarius, slugs Introduction Prey diversity has been shown to have a powerful effect on predator nutrition, reproduction and survival. Green- Alternative prey help to sustain and retain generalist stone (1979) suggested that predators seek to diversify their predators within crops when target pests are absent or at low diets in order to balance their amino acid requirements and, density. This dietary flexibility of generalists can, in theory, more recently, Mayntz et al. (2005) demonstrated that give them a significant advantage over specialist natural invertebrate predators are capable of selective foraging in enemies, allowing them to be present within a crop early order to balance their intake of proteins and lipids. Other in the year before the pests arrive in any significant numbers studies have shown the benefits of a mixed diet, either to (Murdoch et al., 1985; Chiverton, 1987; Chang & Karieva, balance dietary needs or to avoid prey toxins that affect 1999; Harwood et al., 2004). Certain agricultural practices can predator fitness (e.g. Toft & Wise, 1999; Oelberman & Scheu, encourage greater numbers of alternative prey during this 2002; Fisker & Toft, 2004). Importantly, however, beneficial/ early period, allowing predators to reach high densities detrimental effects of a mixed diet are taxon-specific. J.D. by the time the crop needs to be protected from immigrating Harwood, S.W. Phillips, K.D. Sunderland, D.M. Glen, M.W. or rapidly reproducing pests (Settle et al., 1996). Such Bruford, G.L. Harper, and W.O.C. Symondson (unpublished systems depend upon temporal separation between periods data) have demonstrated that both linyphiid spiders and of maximum alternative prey availability and periods of carabid beetles benefit from a diverse diet; for example pest abundance. In many circumstances this is probably not carabids fed a more diverse diet weighed more, laid more achievable and practices such as conservation tillage eggs, continued to lay eggs for longer and the eggs (minimal tillage systems including direct drilling that are developed and hatched more rapidly. Carabids and spiders designed to conserve the soil (Ko¨ller, 2003)) are now fed on pests only (slugs or aphids) were the least fit. There is employed, in part, to maximize biodiversity (Kladivko, some evidence that these effects translate to the field where 2001), in the hope that this will foster a larger and more carabids in more complex habitats, with more diverse prey, diverse predator community that will go on to control the were larger and contained more eggs (Bommarco, 1998, pests. Empirical studies have shown that this is often an 1999). Clearly, prey diversity, if exploitable by the predator, effective strategy for increasing predator numbers (Stinner & improves predator fitness and between years this may lead House, 1990), but the effects of mechanical operations to increased predator numbers, even of univoltine species (cultivation, harvesting) on predators and their prey can be such as carabid beetles. The predators may go on to limit complex and taxon-specific (El Titi, 2003; Holland & growth in pest numbers, although where the pests form a Reynolds, 2003; Holland, 2004; Thorbek & Bilde, 2004). The substantial proportion of the total available prey, suppres- additional predators in minimal or no-tillage systems may sion may lead to subsequent limitation of predator densities sometimes go on to increase predation pressure on pests, but through loosely-coupled feedback mechanisms (Symondson in other instances predator numbers, pest numbers and crop et al., 2002b). However, in the medium term (within a year) damage may all increase (Stinner & House, 1990), a problem univoltine carabids do not have time to respond numerically that has been particularly noted with slugs (Kendall et al., to prey abundance and diversity. For flightless species such 1995; Symondson et al., 1996; Glen & Symondson, 2003). as the ground beetle Pterostichus melanarius (Illiger) field A theoretical problem with the conservation tillage scenario boundaries have been shown to be effective barriers to is that alternative prey may divert predators away from movements (Thomas et al., 1998), preventing significant feeding on target pests (Halaj & Wise, 2002; Symondson aggregative responses to prey, although within-field aggre- et al., 2002a; Koss & Snyder, 2005; Rypstra & Marshall, 2005), gation to pest density can take place (Bohan et al., 2000; and the more numerous and diverse the community of Winder et al., 2005a,b). Thus, P. melanarius responses to alternative prey, the more likely it would be that prey dietary components and prey diversity will be restricted to choice would favour one or more of these alternative prey the prey available in the fields in which they are sampled, species rather than the target pests. This may happen and the fitness of those predators will depend upon the through simple substitution (non-pest for pest) or through abundance and diversity of available food resources. Within switching behaviour as relative densities of prey species year, therefore, reproductive numerical responses will not change (Holt & Lawton, 1994). Food web theory suggests have time to operate, and spatial numerical responses will be that, within a more diverse system, many of those alternative limited, restricting responses by the predators to alternative prey will be other predators, and that predation on each prey to functional responses. If this is correct, then the other potentially decreases the ability of the predator presence of alternative prey is likely to lead to reduced community as a whole to limit herbivore (pest) numbers predation on the target prey (slugs) (Harmon & Andow, (Polis et al., 1989; McCann et al., 1998; Finke & Denno, 2004). 2004). And so the question remains, what happens when The carabid P. melanarius is a highly generalist predator farming systems encourage a numerous and diverse fauna eating a wide variety of prey (Sunderland, 1975, 2002; within a crop coincident with periods when pest density is Symondson et al., 2000). However, Symondson et al. (1996) likely to be high? May the goals of encouraging alternative found, using anti-slug antibodies and enzyme linked prey and biodiversity, and seeking biocontrol of pests, immunosorbent assays, that over 80% of P. melanarius sometimes conflict? May not the fittest predators, replete captured in the field in one year contained slug proteins in with alternative prey, be the least effective at controlling their guts, clearly demonstrating that slugs are a signifi- pests? cant prey item. These carabids have now been shown, in Alternative prey reduce