Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication.

Airborne communication between individuals, called "eavesdropping" in this paper, can cause plants to become more resistant to herbivores when a neighbor has been experimentally clipped. The ecological relevance of this result has been in question, since individuals may be too far apart for this interaction to affect many plants in natural populations. We investigated induced resistance to herbivory in sagebrush, Artemisia tridentata, caused by experimental clipping of the focal plant and its neighbors. We found no evidence for systemic induced resistance when one branch was clipped and another branch on the same plant was assayed for naturally occurring damage. In this experiment, air contact and plant age were not controlled. Previous work indicated that sagebrush received less damage when a neighboring upwind plant within 15 cm had been experimentally clipped. Here we found that pairs of sagebrush plants that were up to 60 cm apart were influenced by experimental clipping of a neighbor. Furthermore, we observed that most individuals had conspecific neighbors that were much closer than 60 cm. Air contact was essential for communication; treatments that reduced airflow between neighboring individuals, either because of wind direction or bagging, prevented induced resistance. Airflow was also necessary for systemic induced resistance among branches within an individual. Reports from the literature indicated that sagebrush is highly sectorial, as are many desert shrubs. Branches within a sagebrush plant do not freely exchange material via vascular connections and apparently cannot rely on an internal signaling pathway for coordinating induction of resistance to herbivores. Instead, they may use external, volatile cues. This hypothesis provides a proximal explanation for why sagebrush does not demonstrate systemic induced resistance without directed airflow, and why airborne communication between branches induces resistance.

[1]  I. Raskin,et al.  Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? , 1995, The Plant cell.

[2]  R. Karban Communication between sagebrush and wild tobacco in the field , 2001 .

[3]  J. Coleman,et al.  Control of systemically induced herbivore resistance by plant vascular architecture , 1993, Oecologia.

[4]  J. Wiens,et al.  Arthropod dynamics on sagebrush (Artemisia tridentata): effects of plant chemistry and avian predation , 1991 .

[5]  Ian T. Baldwin,et al.  Mechanism of damage-induced alkaloid production in wild tobacco , 1989, Journal of Chemical Ecology.

[6]  B. Casper,et al.  MORPHOGENETIC CONSTRAINTS ON PATTERNS OF CARBON DISTRIBUTION IN PLANTS , 1984 .

[7]  F. Schaller Enzymes of the biosynthesis of octadecanoid-derived signalling molecules. , 2001, Journal of experimental botany.

[8]  C. Orians Herbivores, Vascular Pathways, and Systemic Induction: Facts and Artifacts , 2005, Journal of Chemical Ecology.

[9]  M. Gordon,et al.  Assimilate movement dictates remote sites of wound-induced gene expression in poplar leaves. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Jay T. Lennon,et al.  Knowing when to draw the line: designing more informative ecological experiments , 2005 .

[11]  J. Thaler,et al.  Plant Vascular Architecture and Within-Plant Spatial Patterns in Resource Quality Following Herbivory , 2004, Journal of Chemical Ecology.

[12]  R. Karban,et al.  Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants , 2003 .

[13]  D. F. Rhoades Responses of Alder and Willow to Attack by Tent Caterpillars and Webworms: Evidence for Pheromonal Sensitivity of Willows , 1983 .

[14]  Thomas M. Hinckley,et al.  THE THEORY AND PRACTICE OF BRANCH AUTONOMY , 1991 .

[15]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

[16]  A. Hall Induced Responses to Herbivory. , 1999 .

[17]  Timo Vuorisalo,et al.  On plant sectoriality, or how to combine the benefits of autonomy and integration , 1996, Vegetatio.

[18]  M. Roberts,et al.  Signals Regulating Multiple Responses to Wounding and Herbivores , 2001 .

[19]  Y. Waisel,et al.  Patterns of Water Movement in Trees and Shrubs , 1972 .

[20]  J. Harper Population Biology of Plants , 1979 .

[21]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[22]  T. Tscharntke,et al.  Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours , 2000, Oecologia.

[23]  I. Baldwin,et al.  Constraints to Herbivore-Induced Systemic Responses: Bidirectional Signaling Along Orthostichies in Nicotiana attenuata , 2003, Journal of Chemical Ecology.

[24]  G. Laue,et al.  Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush , 2000, Oecologia.

[25]  E. Haukioja,et al.  Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator , 1985, Oecologia.

[26]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[27]  M. Roberts,et al.  Signals regulating multiple responses to wounding and herbivores. , 2001 .

[28]  G. Pearce,et al.  A Polypeptide from Tomato Leaves Induces Wound-Inducible Proteinase Inhibitor Proteins , 1991, Science.

[29]  R. Karban,et al.  THE SPECIFICITY OF EAVESDROPPING ON SAGEBRUSH BY OTHER PLANTS , 2004 .

[30]  G. Laue,et al.  Plant–Plant Signaling: Application of trans- or cis-Methyl Jasmonate Equivalent to Sagebrush Releases Does Not Elicit Direct Defenses in Native Tobacco , 2004, Journal of Chemical Ecology.

[31]  T. Tscharntke,et al.  Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa , 2001 .

[32]  C. Orians,et al.  Vascular Architecture Generates Fine Scale Variation in Systemic Induction of Proteinase Inhibitors in Tomato , 2000, Journal of Chemical Ecology.

[33]  M. Ardón,et al.  Vascular architecture and patchy nutrient availability generate within-plant heterogeneity in plant traits important to herbivores. , 2002, American journal of botany.

[34]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[35]  R. Karban,et al.  THE FITNESS CONSEQUENCES OF INTERSPECIFIC EAVESDROPPING BETWEEN PLANTS , 2002 .

[36]  M A Watson,et al.  Integrated physiological units in plants. , 1986, Trends in ecology & evolution.

[37]  G. Pickford The influence of continued heavy grazing and of promiscuous burning on spring-fall ranges in Utah. , 1932 .

[38]  C. W. Cook,et al.  Physiological responses of big sagebrush to different types of herbage removal. , 1960 .

[39]  C. Orians,et al.  Plants as resource mosaics: a functional model for predicting patterns of within‐plant resource heterogeneity to consumers based on vascular architecture and local environmental variability , 2001 .

[40]  J. Bruin,et al.  Chemical information transfer between plants: back to the future , 2001 .