Herbivory-induced mortality increases with radial growth in an invasive riparian phreatophyte.

BACKGROUND AND AIMS Under equal conditions, plants that allocate a larger proportion of resources to growth must do so at the expense of investing fewer resources to storage. The critical balance between growth and storage leads to the hypothesis that in high-resource environments, plants that express high growth rates are more susceptible to episodic disturbance than plants that express lower growth rates. METHODS This hypothesis was tested by measuring the radial growth, basal area increment (BAI) and carbon isotope ratios (δ(13)C) in tree-ring α-cellulose of 62 mature tamarisk trees (Tamarix spp.) occurring at three sites in the western USA (n = 31 live and 31 killed trees across all sites, respectively). All of the trees had been subjected to periods of complete foliage loss by episodic herbivory over three or more consecutive growing seasons by the tamarisk leaf beetle (Diorhabda carinulata), resulting in approx. 50 % mortality at each site. KEY RESULTS Mean annual BAI (measured from annual ring widths) in the 10 years prior to the onset of herbivory was on average 45 % higher in killed trees compared with live trees (P < 0·0001). Killed trees that had higher growth rates also expressed higher (less negative) δ(13)C ratios compared with live trees. In fact, at one site near Moab, UT, the mean annual BAI was 100 % higher in killed trees despite having about a 0·5 ‰ higher δ(13)C relative to live trees (P = 0·0008). Patterns of δ(13)C suggest that the intrinsic water-use efficiency was higher in killed than surviving trees, possibly as a consequence of lower whole-canopy stomatal conductance relative to live trees. CONCLUSIONS The results show that a likely trade-off occurs between radial growth and survival from foliage herbivory in Tamarix spp. that currently dominates riparian areas throughout the western USA and northern Mexico. Thus, herbivory by D. carinulata may reduce the overall net primary productivity of surviving Tamarix trees and may result in a reduction in genetic variability in this dominant invasive tree species if these allocation patterns are adaptive.

[1]  P. Dennison,et al.  Detection of Tamarisk Defoliation by the Northern Tamarisk Beetle Based on Multitemporal Landsat 5 Thematic Mapper Imagery , 2012 .

[2]  D. Woodruff,et al.  Carbon dynamics in trees: feast or famine? , 2012, Tree physiology.

[3]  P. Dalin,et al.  Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.) , 2012, Evolutionary applications.

[4]  N. McDowell,et al.  Associations between growth, wood anatomy, carbon isotope discrimination and mortality in a Quercus robur forest. , 2011, Tree physiology.

[5]  C. D’Antonio,et al.  Early impacts of biological control on canopy cover and water use of the invasive saltcedar tree (Tamarix spp.) in western Nevada, USA , 2011, Oecologia.

[6]  J. Ehleringer,et al.  Tamarisk biocontrol in the western United States: ecological and societal implications , 2010 .

[7]  J. Ehleringer,et al.  Sap flux-scaled transpiration by tamarisk (Tamarix spp.) before, during and after episodic defoliation by the saltcedar leaf beetle (Diorhabda carinulata) , 2010 .

[8]  Nate G. McDowell,et al.  Growth, carbon‐isotope discrimination, and drought‐associated mortality across a Pinus ponderosa elevational transect , 2010 .

[9]  C. Bigler,et al.  Increased early growth rates decrease longevities of conifers in subalpine forests , 2009 .

[10]  N. McDowell,et al.  Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? , 2008, The New phytologist.

[11]  G. Nigh,et al.  Growth patterns prior to mortality of mature Abies lasiocarpa in old-growth subalpine forests of southern British Columbia , 2008 .

[12]  Christof Bigler,et al.  Drought induces lagged tree mortality in a subalpine forest in the Rocky Mountains , 2007 .

[13]  J. Kiniry,et al.  Defoliation by introduced Diorhabda elongata leaf beetles (Coleoptera: Chrysomelidae) reduces carbohydrate reserves and regrowth of Tamarix (Tamaricaceae) , 2007 .

[14]  M. Stitt,et al.  Coordination of carbon supply and plant growth. , 2007, Plant, cell & environment.

[15]  J. Sperry,et al.  Scaling of angiosperm xylem structure with safety and efficiency. , 2006, Tree physiology.

[16]  Christof Bigler,et al.  Drought as an Inciting Mortality Factor in Scots Pine Stands of the Valais, Switzerland , 2006, Ecosystems.

[17]  M. Berenbaum,et al.  Elevated CO2 reduces leaf damage by insect herbivores in a forest community. , 2005, The New phytologist.

[18]  P. Shafroth,et al.  Dominance of non-native riparian trees in western USA , 2005, Biological Invasions.

[19]  J. Sperry,et al.  Inter‐vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade‐off in xylem transport , 2005 .

[20]  T. Kitzberger,et al.  Factors predisposing episodic drought‐induced tree mortality in Nothofagus– site, climatic sensitivity and growth trends , 2004 .

[21]  C. Bigler,et al.  Growth patterns as indicators of impending tree death in silver fir , 2004 .

[22]  P. Coley,et al.  Herbivores Promote Habitat Specialization by Trees in Amazonian Forests , 2004, Science.

[23]  Andreas Richter,et al.  Non‐structural carbon compounds in temperate forest trees , 2003 .

[24]  C. Körner Carbon limitation in trees , 2003 .

[25]  M. Dobbertin,et al.  Tree‐life history prior to death: two fungal root pathogens affect tree‐ring growth differently , 2002 .

[26]  T. Whitham,et al.  FAST-GROWING JUVENILE PINYONS SUFFER GREATER HERBIVORY WHEN MATURE , 2002 .

[27]  J. Gaskin,et al.  Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  N. Cobb,et al.  TREE-RING VARIATION IN PINYON PREDICTS LIKELIHOOD OF DEATH FOLLOWING SEVERE DROUGHT , 2000 .

[29]  H. Fritts,et al.  Tree Rings and Climate. , 1978 .

[30]  P. Feeny SEASONAL CHANGES IN OAK LEAF TANNINS AND NUTRIENTS AS A CAUSE OF SPRING FEEDING BY WINTER MOTH CATERPILLARS , 1970 .

[31]  T. Dudley Progress and Pitfalls in the Biological Control of Saltcedar (Tamarix Spp.) in North America , 2005 .

[32]  J. Nash Hydrogeochemical studies of historical mining areas in the Humboldt River basin and adjacent areas, northern Nevada , 2005 .

[33]  B. Pedersen,et al.  THE ROLE OF STRESS IN THE MORTALITY OF MIDWESTERN OAKS AS INDICATED BY GROWTH PRIOR TO DEATH , 1998 .

[34]  O. Kovalev Co-evolution of the tamarisks (Tamaricaceae) and pest arthropods (Insecta; Arachnida: Acarina), with special reference to biological control prospects. , 1995 .

[35]  S. Leavitt,et al.  Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis , 1993 .

[36]  Peter Kareiva,et al.  Plant defense, herbivory, and climate change. , 1993 .

[37]  J. Ehleringer 12 – 13C/12C Fractionation and Its Utility in Terrestrial Plant Studies , 1991 .

[38]  F. Stuart Chapin,et al.  The Ecology and Economics of Storage in Plants , 1990 .

[39]  T. Swetnam,et al.  Dendroecology: A Tool for Evaluating Variations in Past and Present Forest Environments , 1989 .

[40]  A. Tyree,et al.  Vulnerability of Xylem to Cavitation and Embolism , 1989 .

[41]  J. Seemann,et al.  The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. , 1989 .

[42]  H. Mooney,et al.  Resource Limitation in Plants-An Economic Analogy , 1985 .