The consequences of the prevalent loss of species have been thoroughly studied over the past decade. The effect of terrestrial plant species loss on primary productivity has certainly received most attention, with studies largely in agreement that a decline in plant species negatively affects ecosystem functioning at the plant level (reviewed, e.g. by Hooper et al. 2005; Balvanera et al. 2006). However, studies have rarely considered diversity loss in a multi-trophic context (Duffy et al. 2007; Thébault, Huber & Loreau 2007). For example, the loss of plant species is likely to have profound bottom–up effects via cascading secondary extinctions and subsequent loss of ecosystem function at higher trophic levels (Joshi et al. 2004; Kagata & Ohgushi 2006; Thébault & Loreau 2006; Thébault et al. 2007; Schmid et al. 2009).
In fact, a large number of hypotheses regarding multi-trophic consequences of plant diversity loss exist, but they are often contradictory and rarely reflected in empirical results even for herbivores, the first trophic level above plants. For example, the classical resource concentration hypothesis and the enemies’ hypothesis (Root 1973) predict high specialist herbivore loads at low plant diversity owing to a concentration of resources and a low efficiency of generalist predators. However, some studies have found exactly the opposite: weaker herbivory at low plant diversity (Prieur-Richard et al. 2002; Scherber et al. 2006), lower herbivore loads with increased host plant abundance (i.e. a resource dilution effect; Koricheva et al. 2000; Otway, Hector & Lawton 2005) and increased predator efficiency at low plant diversity (Aquilino, Cardinale & Ives 2005).
The higher the trophic level, the more complex are the predictions for plant diversity effects that have been proposed, especially because effects are often not direct but mediated by other trophic levels (Abrams et al. 1996; Siemann et al. 1998; Tscharntke & Hawkins 2002; Dyer & Letourneau 2003; Dyer & Stireman 2003; Balvanera et al. 2006; Schmid et al. 2009; Viketoft et al. 2009). For example, direct effects of plant diversity on higher trophic levels could include effects of plant architecture (Root 1973; Hochberg & Hawkins 1992; Brose 2003; Langellotto & Denno 2004; Vanbergen et al. 2007) or floral resources (e.g. Langellotto & Denno 2004; Araj et al. 2008). Indirect effects could be mediated by density, species richness or life-history traits (e.g. body size) of the species at lower trophic levels (Abrams et al. 1996; Knops et al. 1999; Bukovinszky et al. 2008).
Although plant species richness is often assumed to underlie food web change across habitats (e.g. Perner et al. 2003; Unsicker et al. 2006; Albrecht et al. 2007; Macfadyen et al. 2009) it is rarely explicitly manipulated. However, to disentangle effects of plant species loss and correlated factors on higher trophic levels, controlled experiments are necessary. Few such experiments have been conducted and the most rigorous ones have been lab experiments (e.g. Aquilino et al. 2005). Field experiments typically only consider one, rarely two, trophic levels above the primary producers (e.g. Siemann et al. 1998; Knops et al. 1999; Mulder et al. 1999; Koricheva et al. 2000; Symstad, Siemann & Haarstad 2000; Haddad et al. 2001, 2009; Prieur-Richard et al. 2002; Otway et al. 2005; Scherber et al. 2006) or focus on single or few plant species out of the entire community (e.g. Prieur-Richard et al. 2002). Furthermore, almost all field studies associate herbivores, predators, parasitoids and plant communities based on co-occurrences (e.g. Siemann et al. 1998; Knops et al. 1999; Koricheva et al. 2000; Haddad et al. 2001, 2009), rarely quantifying actual interactions between trophic levels. To address these shortcomings, this study examined quantified aphid–parasitoid food webs comprising three to four trophic levels above plants in a grassland field experiment that directly manipulated plant species richness (i.e. a random-loss scenario; Schmid & Hector 2004).
Aphids are attacked by primary parasitoid wasps that lay a single egg into their host’s body. The aphids continue to feed for a few days before dying and developing into hard-shelled ‘mummies’ in which the primary parasitoid larva eventually pupates. Two guilds of secondary parasitoid wasps attack primary parasitoids: hyperparasitoids lay their egg into the developing primary parasitoid larva inside the living aphid and delay their development until the primary parasitoid larva has killed the aphid host; they are koinobiont endoparasitoids. Mummy parasitoids, however, lay their egg onto the primary parasitoid larva inside the dead and mummified aphid; they are idiobiont ectoparasitoids (Godfray 1994). Because hyperparasitoid larvae have to deal with the primary parasitoid’s immune system, they are usually more specialized than mummy parasitoids (Müller et al. 1999; Bukovinszky et al. 2008). Mummy parasitoid larvae can furthermore feed on primary parasitoid larvae and hyperparasitoid larvae (facultative tertiary parasitism, Müller et al. 1999). Thus, mummy parasitoids represent a trophic level slightly above hyperparasitoids, that is, in our case a facultative fifth level in the community. With aphids being sedentary herbivores and all parasitoids being solitary (i.e. a single parasitoid developing from a single host), links between food web members can be established and fully quantified.
Aphid–parasitoid food webs are frequently used as ecological model systems for this reason (Müller et al. 1999), but also because they are important in an agricultural context (e.g. Schmidt et al. 2003; Brewer & Elliott 2004). Herbivory by aphids constitutes a central ecosystem function within the aphid–parasitoid community, albeit an unpopular one with farmers. Aphids can reduce crop yield considerably and aphid load, that is, in our case the number of aphids per biomass of the host plant, is typically positively correlated with the magnitude of plant damage (e.g. Larsson 2005). We therefore measured aphid load and used it as a proxy for aphid herbivory. Parasitism of aphids by parasitic wasps is another ecosystem function of the aphid–parasitoid community, but one that is promoted by farmers as biocontrol against aphids. These two important ecosystem functions could be affected by changes in plant diversity, either directly or indirectly via the density or richness of the involved organisms.
Here we report results from 47 quantified aphid–parasitoid food webs associated with experimental plant communities of varying plant species richness and test the following hypotheses: (i) the loss of plant species affects densities and species richness of all trophic levels; (ii) the loss of plant species has strong direct effects on lower trophic levels with indirect effects cascading up the food web; (iii) ecosystem functions at higher trophic levels, such as herbivory (herbivore load) and parasitism are affected by a loss of plant species.