Functional Ecology 2012, 26, 628–636 doi: 10.1111/j.1365-2435.2012.01986.x A petiole-galling insect herbivore decelerates leaf lamina litter decomposition rates Christopher J. Frost†,1,2,3,4, Jennifer M. Dean1,4, Erica C. Smyers4, Mark C. Mescher1,4, John E. Carlson1,2,3,5, Consuelo M. De Moraes1,4 and John F. Tooker*,1,4 1Center for Chemical Ecology, Pennsylvania State University, University Park, Pennsylvania 16802, USA; 2School of Forest Resources, Pennsylvania State University, University Park, Pennsylvania 16802, USA; 3Schatz Center for Tree Molecular Genetics, Pennsylvania State University, University Park, Pennsylvania 16802, USA; 4Department of Entomol- ogy, Pennsylvania State University, University Park, Pennsylvania 16802, USA; and 5Department of Bioenergy Science and Technology (WCU), Chonnam National University, 333 Yongbongro, Buk-gu, Gwangju 500-757, Korea Summary 1. Herbivore-mediated changes in leaf-litter chemistry are often considered responsible for alter- ing litter decomposition rates, but such chemical changes often co-occur with other factors such as physical alteration of leaf material that also influence decomposition rates. We attempted to disentangle these effects using the poplar petiole gall moth (Ectoedemia populella Brusk), which forms galls on petioles at the base of the leaf lamina but does not alter leaf morphology. Thus, differences in leaf decomposition rates between galled and ungalled leaves should be explained by gall-mediated changes in leaf chemistry. 2. Petiole galling decelerated leaf lamina litter decomposition in two Populus host species, but in temporally distinct ways. In Populus granidentata, galling decelerated decomposition by 7% after 4 months. After 12 and 18 months, Populus tremuloides litter decomposition rates were 12% and 17% lower, respectively, in lamina tissue whose petiole had been galled relative to ung- alled. On average, the petiole galler increased leaf lamina nitrogen concentrations by 17%, decreased tannin concentrations from 37% to 53% and decreased tannin-binding capacity by 11% and 37% in P. grandidentata and P. tremuloides, respectively. These changes would be expected to increase, rather than decrease, decomposition rates. 3. Unlike other insect herbivores guilds that have variable effects on litter decomposition in direction and magnitude, all gall insects studied to date have decelerated leaf-litter decomposi- tion. This consistent effect of galling on decomposition provides a framework for deciphering a fundamental aspect of insect herbivory on a critical ecosystem process. 4. We used a gall-inducing moth with a distinctive natural history to confirm the role of herbi- vore-mediated litter chemistry in leaf-litter decomposition dynamics. Moreover, we advance the hypothesis that gall-induced defensive manipulations that protect a host plant from injury by other herbivores lead to decelerated litter decomposition. Key-words: Ectoedemia, leaf chemistry, leaf-litter decomposition, plant–herbivore interactions, Populus litter quality as a substrate can have demonstrable effects Introduction on decomposition processes and thus terrestrial nutrient The process of decomposing dead plant material facilitates availability. As many plant species presumably increase the recycling of mineral nutrients and organic matter essen- their Darwinian fitness by altering foliar quality in response tial for biological activity in most terrestrial ecosystems to herbivores (Karban & Baldwin 1997), the potential for (Parton et al. 2007). Senesced leaf litter is an abundant, herbivores to indirectly influence litter quality – and thus ubiquitous example of such material, and variation in leaf- decomposition rates – has long been considered plausible (Choudhury 1988). While a number of studies have shown *Correspondence author. E-mail: [email protected] clear effects of herbivores on litter decomposition (Findlay †Present address. Warnell School of Forest Resources, University of et al. 1996; Belovsky & Slade 2000; Chapman et al. 2003; Georgia, Athens, Georgia 30601, USA. Schweitzer et al. 2005b; Chapman, Schweitzer & Whitham Ó 2012 The Authors. Functional Ecology Ó 2012 British Ecological Society Galling effects on leaf-litter decomposition 629 2006; Crutsinger et al. 2008; Frost & Hunter 2008; Kurokawa (P. betae) or by radically altering leaf growth patterns & Nakashizuka 2008), constructing a more detailed theoret- (R. solidaginis) (Fig. S1, Supporting information). As a ical framework has been difficult because herbivory can result, these systems have shown clearly that gall insects have accelerate or decelerate decomposition depending in part on ecosystem-level effects, but neither system necessarily disen- whether secondary metabolites are repressed or augmented, tangles chemical and morphological factors influencing litter what type of physical damage occurs, the type of herbivory decomposition. suffered or the ecosystem in which the decomposition is Here, we describe how herbivory by larvae of the poplar measured. Moreover, determining the importance of her- petiole gall moth (Ectoedemia populella Busck.) influences bivory-induced changes in leaf chemistry for decomposition leaf-litter chemistry and decomposition in two species of Pop- rates is often complicated by the co-occurrence of other ulus. Ectoedemia are monotrysian, nepticulid moths that herbivore-related factors that can also alter litter decompo- include some of the smallest known lepidopterans; adults of sition. For example, herbivory may induce changes in leaf- E. populella have c. 6-mm wingspans (Wilkinson & Scoble drop phenology that results in herbivore-affected litter 1979). The family consists primarily of leaf miners; only a few entering the detrital system in a different condition than Ectoedemia species consume bark, buds, or – in the case of undamaged litter (Chapman et al. 2003). Of equal impor- E. populella – induce galls (Wilkinson & Scoble 1979). Leaf- tance, most foliar herbivores physically damage leaf tissue mining Ectoedemia trace at least to the mid-Cretaceous era during feeding, and such damage can alter access to the lit- 97 million years ago (Labandeira et al. 1994); gall-inducing ter substrate (Findlay et al. 1996; Cornelissen et al. 1999; Ectoedemia on Populus trace to the Miocene era, some 5– Pe´rez-Harguindeguy et al. 2000; Ostertag, Scatena & Silver 17 million years ago (Madler 1936). Importantly, E. populella 2003). Insect herbivore species that influence host-plant form galls at the junction of the petiole and the lamina caus- chemistry but only minimally alter other aspects of a host ing no observable morphological difference in the lamina tis- plant, such as some species of gall insects, offer an ideal sue itself (Fig. S2, Supporting information). Moreover, the opportunity to explore the effects of herbivore-induced leaf phenology of the moth is offset with its hosts such that the chemistry on leaf-litter decomposition apart from other adults emerge and oviposit in May after leaves of their hosts co-occurring effects. have fully expanded foliage (Wilkinson & Scoble 1979). Thus, Gall-inducing insects are herbivores that force their host E. populella galls have limited or no influence on lamina plants to produce a tumour-like growth that provides the growth and development, although they may influence lam- insect with food and shelter, usually at the expense of plant ina quality. Larvae emerge and pupate in October and over- growth and ⁄ or reproduction. These insects have evolved inti- winter in the soil, so larvae do not reside in decomposing mate relationships with their host plants and an unparalleled galled leaf litter. Little else is known about the ecology of ability to influence host-plant morphology and physiology E. populella, including the direct effects of the gall on leaf (Larson 1998; Stone & Schonrogge 2003). Gall insects com- lamina metabolite profiles associated with the galled petiole. monly modify host-plant chemistry, often altering concentra- However, there are at least two reasons to hypothesize that tions of plant secondary metabolites for their own purposes E. populella will influence decomposition possibly by altering (Weis & Abrahamson 1986; Nyman & Julkunen-Tiitto 2000; laminar chemistry. First, the gall envelopes the petiole, forc- Tooker, Koenig & Hanks 2002; Allison & Schultz 2005). For ing all assimilates and other transported materials through example, high concentrations of secondary metabolites such vasculature that has been altered by the gall. Second, E. pop- as phenolics tend to be localized in gall exteriors, where they ulella deposits its frass inside the gall in a tight packet that presumably provide protection against natural enemies, while remains in the gall after leaf senescence; frass, which is nutri- the inner nutritive tissue on which the gall insect feeds is lar- ent rich, is known to influence ecosystem processes in other gely or entirely devoid of such potentially toxic compounds systems (Frost & Hunter 2007; Madritch, Donaldson & (Nyman & Julkunen-Tiitto 2000; Allison & Schultz 2005). Lindroth 2007). Moreover, gall insects also variably influence the chemistry of Throughout its range, E. populella forms galls on big- plant tissue that is not part of the gall itself, although investi- toothed aspen (Populus grandidentata) and quaking aspen gations thus far have been confined to neighbouring tissues (Populus tremuloides) (Wilkinson & Scoble 1979). This (Tooker et al. 2008; Cooper & Rieske 2009); such systemic makes the Populus ⁄ Ectoedemia system