Oecologia (2000) 125:504–511 DOI 10.1007/s004420000482 Rainer Dolch · Teja Tscharntke Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours Received: 2 November 1999 / Accepted: 27 June 2000 / Published online: 23 August 2000 © Springer-Verlag 2000 Abstract The effects of defoliation of alder (Alnus all changes after herbivory, “induced resistance” only glutinosa) on subsequent herbivory by alder leaf beetle changes that affect subsequent herbivory, and “induced (Agelastica alni) were studied in ten alder stands in defence” results in a fitness benefit to induced plants. northern Germany. At each site, one tree was manually Biochemical consequences of defoliation may affect defoliated (c. 20% of total foliage) to simulate herbivory. neighbouring plants (Tuomi et al. 1990), either by con- Subsequent damage by A. alni was assessed on ten alders nection via roots or mycorrhizae (Simard et al. 1997) or at each site on six different dates from May to September by reception of volatile substances such as terpenoids 1994. After defoliation, herbivory by A. alni increased (e.g. Dicke 1994). Volatiles implicated in signal transfer with distance from the defoliated tree. Laboratory exper- include ethylene and methyl jasmonate, which may acti- iments supported the field results. Not only leaf damage vate genes coding for plant resistance (Ecker and Davis in the field, but also the extent of leaf consumption in 1987; Farmer and Ryan 1990), and the latter has been laboratory feeding-preference tests and the number of shown to induce changes in the production of secondary eggs oviposited per leaf in another laboratory test were compounds (Shonle and Bergelson 1995). Such interplant positively correlated with distance from the defoliated communication may result in chemical changes in un- tree. Resistance was therefore induced not only in defoli- damaged plants adjacent to damaged ones, leading to ated alders, but also in their undamaged neighbours. lower susceptibility to herbivores of plants neighbouring Consequently, defoliation of alders may trigger inter- damaged conspecifics (Baldwin and Schultz 1983; plant resistance transfer, and therefore reduce herbivory Haukioja et al. 1985; Rhoades 1985). Evidence for this in whole alder stands. kind of interplant signal transfer – popularly referred to as “communication” – remains controversial (Bruin et al. Keywords Herbivory · Defoliation · Plant responses · 1995; Shonle and Bergelson 1995). Once harshly critici- Induced resistance · Talking trees sed by Fowler and Lawton (1985), the concept of inter- plant signal transfer and so-called “talking trees” has un- dergone a recent revival (e.g. Karban and Baldwin 1997). Introduction Here we present results from a field experiment using a bioassay in a natural setting involving black alders (Al- Plant responses following insect herbivory are known nus glutinosa) and alder leaf beetles (Agelastica alni). from a wide range of plants (Rosenthal and Janzen 1979; This system was chosen to study the consequences of Hedin 1983; Barbosa and Letourneau 1988; Schultz herbivory, since mass outbreaks of alder beetles and 1988; Haukioja 1990; Tallamy and Raupp 1991; Fritz complete defoliations of alders, triggering both rapid and and Simms 1992; Karban and Baldwin 1997). These in- delayed induced resistance, are well-known (Jeker 1981; duced responses may either be incidental physiological Baur et al. 1991; Seldal et al. 1994; R. Dolch and T. reactions (for instance to nutrient stress, Haukioja and Tscharntke, unpublished work). Neuvonen 1985) or purely defensive traits to prevent fur- This study addresses the following questions: ther insect damage (induced resistance). According to Karban and Baldwin (1997) “induced responses” means 1. How does manual defoliation affect herbivory of Agelastica alni on Alnus glutinosa? R. Dolch (✉) · T. Tscharntke 2. Does manual defoliation lead to induced resistance Agroecology, University of Göttingen, Waldweg 26, 37073 Göttingen, Germany in A. glutinosa? e-mail: [email protected] 3. Can resistance also be induced in non-defoliated Tel.: +49-551-392358, Fax: +49-551-398806 neighbours? 505 number of all leaves and the total number of leaves damaged by Materials and methods A. alni was counted for each of those alders, so that percentage of leaf area consumed could be calculated. We found that there was a We studied consequences of manual defoliation of alders (A. gluti- strong positive relationship between the percentage of total dam- nosa) for subsequent herbivory of the alder leaf beetle (Agelastica age and the estimated percentage of leaf damage on the lower alni; Coleoptera, Chrysomelidae) in the field. A. alni is a wide- branches (r2=0.675, n=100, P<0.001), and also between absolute spread univoltine specialist on alder and considered its most im- number and relative number (percentage) of damaged leaves portant herbivore. We examined 100 individuals of alder at ten (r2=0.908, n=10, P<0.001). This indicates that the estimated val- different sites (ten alders at each site) located near Göttingen in ues of leaf damage sufficiently reflect real damage levels. Leaf north-central Germany. Distances between the sites varied from damage caused by phytophagous arthropod species other than 300 to 3500 m. At all sites, alders were growing in rows along the A. alni (<5%) could be ignored as it was of minor importance bank on the same side of a creek at a similar distance (c. 1.5 m) (R. Dolch and T. Tscharntke, unpublished work). from the water. Individual alders can be regarded as genetic indi- We assessed stem diameter as a measure of tree age and related viduals, since the probability of alders growing along creeks to be it to subsequent leaf damage caused by A. alni. Distances between ramets of the same clone is almost zero (A. Bogenrieder and E. the defoliated tree and the non-defoliated trees at each site were Dister, personal communication). In order to standardize sampling also measured. By 1 week after manual defoliation, the ten defoli- and minimize possible effects of water or air currents, at each site ated alders had reflushed. Leaf flush of all 100 alders was assessed one randomly selected tree was chosen for defoliation. Nine alders in the field 7 and 37 days after defoliation as the percentage of to- located immediately downstream were not defoliated. Additional- tal leaf area accounted for by freshly flushed leaves on the three ly, we chose sites with trees whose diameters were distributed ran- lowest branches. domly (no relationship between position and diameter) and varied In the laboratory, oviposition and feeding preference tests were only slightly. carried out, using equal-aged leaves from each site (n=10 repli- Manual defoliation involved one randomly selected tree at cates). Six leaves from the manually defoliated tree, six from its each site in order to simulate damage by herbivory. Manual defoli- nearest neighbour and six from the farthest tree (all from the low- ation of trees is known to induce less resistance than herbivore est branches) were taken at each site. They were put into six petri damage (Haukioja and Neuvonen 1985; Hartley and Lawton dishes with one leaf of each tree per dish. Female beetles (six per 1987), but is useful for simulating herbivory. Damage was caused dish) could choose between those leaves for oviposition. In the by stripping 20% of the tree's leaves from the lower branches of feeding experiments, adult beetles (6 per dish) or larvae (12 per the canopy, up to a height of about 2.5 m. The majority of the dish) could choose between the leaves for consumption. leaves were crunched and torn, but care was taken not to affect In an additional feeding experiment (n=10 replicates) adult buds, damage to which might mask effects purely due to defolia- beetles and larvae had the choice between a young and an old leaf tion (e.g. Haukioja et al. 1990). Distance between the defoliated per petri dish. In all experiments, beetles were removed after 24 h alder and the farthest non-defoliated one averaged 10.8 m, and ac- and consumed leaf area was assessed using templates of known cordingly, average distance between the trees was 1 m. surface area. Manual defoliation took place in early May 1994, before adult beetles had colonized the alders. Resprouting occurred before the beetles started ovipositing. Oviposition usually takes place from May to June and larvae hatch after 9–15 days. After three larval stages, adults of the new generation emerge at the end of July, feed Results until September and begin hibernating in the ground near their host trees soon after. Damage pattern in the field Leaf damage by A. alni was estimated as percentage of total leaf area consumed on all trees at each of the ten sites (n=100 trees) at six dates between May and September 1994 (0, 7, 37, 52, Leaf damage was best explained by distance from the 81 and 133 days after manual defoliation). One site became inac- manually defoliated tree. Until 37 days after defoliation, cessible during the last two dates (81 and 133 days after defolia- distance and leaf damage were significantly positively tion), so that estimation of leaf damage was restricted to the re- maining 9 sites on these dates (n=90 trees). Results were also correlated in eight of ten alder stands (Table 1). When compared with estimated leaf damage at all ten sites before defoli- data from all sites were pooled, this correlation held until ation. 81 days after defoliation (Fig. 1). When regression was Since unconscious biases in the estimation of leaf damage performed without considering the manually defoliated might affect the detected pattern, we tested the fidelity of field es- timates for leaf damage. We first estimated the percentage of leaf trees, slopes of the graphs were lower and regression co- damage on ten randomly chosen alders that were not included in efficients were smaller, but there was almost no effect on our experiment.