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