Biochemical Systematics and Ecology 29 (2001) 995–1005

Communication between sagebrush and wild tobacco in the field

Richard Karban Department of Entomology, University of California, Davis, CA 95616 USA

Received 9 March 2001; accepted 19 April 2001

Abstract

Communication between plants has not been widely accepted by most ecologists. However, recent field experiments indicated that wild tobacco plants became more resistant to herbivores when grown in close proximity to clipped sagebrush neighbors. Tobacco plants grown within 15 cm of sagebrush that had been either manually clipped with scissors or damaged by herbivores experienced less naturally occurring folivory than tobacco plants with unclipped neighbors. These results were consistent over five field seasons and involved treatments that were randomly assigned and well replicated. Associated with lower levels of herbivory were increased activities of polyphenol oxidase in tobacco foliage near clipped sagebrush neighbors. Experiments that blocked either air or soil contact between sagebrush and tobacco indicated that the communication was airborne rather than soilborne. Alternative explanations involving altered microenvironmental conditions or avoidance of clipped sagebrush by herbivores were not supported. Much remains to be learned about the natural history of this phenomenon. Apparently the plants must be in close proximity for communication to occur. Preliminary results suggest that communication between sagebrush and other plants may also occur. The mech- anisms of communication as well as its ecological and evolutionary significance remain unknown. r 2001 Elsevier Science Ltd. All rights reserved.

Keywords: Communication; Herbivory; Induced resistance; Artemisia tridentata; Volatile cues

The notion of communication between plants has been the subject of considerable contention in the ecological literature. The hypothesis was proposed by David Rhoades (1983) to explain his field observations. He found that trees that had been damaged by caterpillars were poor hosts for subsequent caterpillars and surprisingly that the neighbors of damaged trees were poor hosts as well. He suggested that

E-mail address: [email protected] (R. Karban).

0305-1978/01/$ - see front matter r 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 3 0 5 - 1978(01)00046-1 996 R. Karban / Biochemical Systematics and Ecology 29 (2001) 995–1005 airborne communication between the damaged trees and their neighbors had caused the neighbors to increase their levels of resistance. This work was followed up by more controlled lab experiments that supported the interpretation that communica- tion could occur (Baldwin and Schultz, 1983; Bruin et al., 1992). Despite these reports, most ecologists remained skeptical of the notion, disregarding or dismissing it (see reviews by Fowler and Lawton, 1985; Bruin et al., 1995; Shonle and Bergelson, 1995; Karban and Baldwin, 1997). Several concerns led to this skepticism. First, it seemed unlikely that natural selection could favor plants that released information to unrelated neighbors: why should trees talk? Second, related to this, there has been confusion about the term ‘‘communication’’. I use the term without implying that either the plant that releases the cue or the plant that responds to it necessarily benefits by ‘‘communicating’’. Third, the early experiments had no true replication. All the replicates for each treatment were in one place; so effects caused by treatments could not be separated unambiguously from effects caused by place. Fourth, some of the results from these early experiments could be explained by alternative hypotheses that had not been tested. For example, an infectious disease could have caused Rhoades’ results (Myers and Williams, 1984; Fowler and Lawton, 1985). Fifth, workers who attempted to repeat some of the experiments that found evidence for communication were unable to get the result consistently (Myers and Williams, 1984; D. Rhoades, personal communication). Carefully controlled laboratory results indicated that airborne communication between plants was possible under some conditions. Tomato plants that were incubated with clipped branches of sagebrush in small, airtight containers increased production of proteinase inhibitors (Farmer and Ryan, 1990) and these chemicals have the potential to reduce herbivore performance (Broadway et al., 1986). Other experiments using plants in airtight containers supported and extended these results (e.g. Hildebrand et al., 1993; Shulaev et al., 1997). However, few ecologists are willing to extrapolate from results found in small airtight containers to field situations. One theoretical problem that some have had with the possibility of plant to plant communication seems easy to refute (Karban and Baldwin, 1997, p. 12). Although the factors that may favor damaged plants that release information to unrelated neighbors are unresolved, selection could favor neighbors that are responsive to cues released involuntarily by damaged plants. In essence, selection at the individual level may or may not favor ‘‘talkers’’ but could easily favor plants that are ‘‘good listeners’’ (Bruin et al., 1995). The problem then becomes an empirical oneFwhat is the evidence that this occurs in nature? A recent work suggests that communication between plants in the field may indeed be a real phenomenon for at least two systems: wild tobacco and European alder (Karban et al., 2000; Dolch and Tcharntke, 2000). Actually, this work is not that recent; both groups experienced editorial rejections attempting to publish these results years earlier. Here I will review the field evidence for communication between sagebrush and wild tobacco. Preston et al. (2001) discuss possible mechanisms of communication in this system. R. Karban / Biochemical Systematics and Ecology 29 (2001) 995–1005 997

1. The Sagebrush–Tobacco System

Sagebrush (Artemisia tridentata) is the most abundant, and defining, plant of the large North American biome, the Great Basin. In areas that have been grazed and where fires have been suppressed, sagebrush can make up over 90% of the woody vegetation. Wild tobacco (Nicotiana attenuata) is also restricted in distribution to the Great Basin where it grows in disturbed sitesFroadsides, seasonally dry washes, and recent burns. Wild tobacco is a native annual that often grows in close proximity to sagebrush and suffers relatively high rates of folivory (Wells 1959; Baldwin, 1999). The most common folivores at my study sites in eastern California are grasshoppers (six species in descending order of abundance: Cratypedes neglectus, Trimerotropis fontana, Conozoa sulcifrons, Cratypedes lateritius, Melanoplus sanguinipes and Cordillacris occipitalis) and noctuid cutworms (two common species: Peridroma saucia and Agrotis ypsilon). Several mammals are also common folivores including black-tailed jack rabbits (Lepus californicus), mountain cottontails (Sylvilagus nuttallii), and mule deer (Odocoileus hemionus). All of these generalist and mammal herbivores feed on both sagebrush and tobacco; sagebrush tends to be more preferred during the winter and spring when tobacco and other annual plants are seeds or small seedlings. Once tobacco and other annuals leaf out, the generalist herbivores shift their attention to the annuals.

2. Evidence for communication between sagebrush and tobacco

I assayed the levels of leaf herbivory for tobacco plants near clipped or unclipped sagebrush. Tobacco seedlings were transplanted immediately downwind (within 15 cm) of naturally occurring sagebrush plants. At this study site, glacial moraines constrain the wind to come consistently from the west. Half of the tobacco– sagebrush pairs had their sagebrush plants clipped with scissors. Sagebrush shoots were clipped once in the early summer when tobacco plants were at the rosette stage (prereproductive). In all cases less than 5% of the aboveground biomass of the sa