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Salinity driven interactions between plant growth and a biological control agent

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Abstract

Abiotic conditions can influence the effect that herbivores have on plant growth. Such biotic and abiotic interactions are of special interest in plant biological control programs because the goal of herbivore suppression of the target weed may not be reached in some abiotic settings. Additionally, target invasive plants typically occur across diverse landscapes raising the possibility that local adaptation to site-specific conditions leads to phenotypic variation that can affect herbivore responses. Here, we used Tamarix, an invasive plant, and its associated biological control agent, Diorhabda carinulata, to investigate how local variation in soil salinity and host plant origin influence interactions between the two taxa. To test if Tamarix was adapted to local conditions, we collected plants from sites with either low or high groundwater salinity, asexually propagated them through multiple generations, and then treated them with their home or reciprocal salinity levels. We found that plants accumulated the most biomass when grown at the salinities of their origin site. The biological control agent, D. carinulata preferred plants grown at source site salinity when given a choice against plants grown in the reciprocal salinity treatment. Although plants compensated for herbivory by regrowing foliage over three defoliation events and maintained similar leaf biomass through regrowth, they ultimately had a reduced basal area and 62% lower root biomass compared to the controls. Thus, herbivory caused a shift in plant allocation of resources from overall growth to compensation, reducing root and stem investment. Overall, D. carinulata caused a significantly greater reduction in total biomass in the high salinity plants than the low salinity ones when grown at their source salinity (averages of 63% and 32% respectively). Thus, the Tamarix biological control program may experience its greatest efficacy in high salinity areas where the impact of the agent is the greatest, likely due to increased water stress and reduced resources to enable regrowth.

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References

  • Albarracin MT, Stiling P (2006) Bottom-up and top-down effects on insect herbivores do not vary among sites of different salinity. Ecology 87:2673–2679

    Article  PubMed  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684

    Article  Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivourous insects. Annu Rev Entomol 47:817–844

    Article  CAS  PubMed  Google Scholar 

  • Barker HL, Holeski LM, Lindroth RL (2019) Independent and interactive effects of plant genotype and environment on plant traits and insect herbivore performance: a meta-analysis with Salicaceae. Funct Ecol 33:422–435

    Article  Google Scholar 

  • Bean DW, Dalin P, Dudley TL (2012) Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.). Evol Appl 5:511–523

    Article  PubMed  PubMed Central  Google Scholar 

  • Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892

    Article  Google Scholar 

  • Björkman C, Larsson S, Gref R (1991) Effects of nitrogen fertilization on pine needle chemistry and sawfly performance. Oecologia 86:202–209

    Article  PubMed  Google Scholar 

  • Bowdish TI, Stiling P (1998) The influence of salt and nitrogen on herbivore abundance: direct and indirect effects. Oecologia 113:400–405

    Article  PubMed  Google Scholar 

  • Capon SJ, Chambers LE, Mac Nally R, Naiman RJ, Davies P, Marshall N, Pittock J et al (2013) Riparian ecosystems in the 21st Century: hotspots for climate change adaptation? Ecosystems 16:359–381

    Article  Google Scholar 

  • Cox CS, McEvoy PB (1983) Effect of summer moisture stress on the capacity of tansy ragwort (Senecio jacobaea) to compensate for defoliation by cinnabar moth (Tyria jacobaeae). J Appl Ecol 20:225

    Article  Google Scholar 

  • Davidson J, Andrewartha HG (1948) The influence of rainfall, evaporation and atmospheric temperature on fluctuations in the size of a natural population of Thrips imaginis ( Thysanoptera ). J Anim Ecol 17:200–222

    Article  Google Scholar 

  • DeLoach CJ, Lewis PA, Herr JC, Carruthers RI, Tracy JL, Johnson J (2003) Host specificity of the leaf beetle, Diorhabda elongata deserticola (Coleoptera: Chrysomelidae) from Asia, a biological control agent for saltcedars (Tamarix: Tamaricaceae) in the Western United States. Biol Control 27:117–147

    Article  Google Scholar 

  • Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural Carbon in Woody Plants. Annu Rev Plant Biol 65:667–687

    Article  CAS  PubMed  Google Scholar 

  • Drus GM, Dudley TL, D’Antonio CM, Even TJ, Brooks ML, Matchett JR (2014) Synergistic interactions between leaf beetle herbivory and fire enhance tamarisk (Tamarix spp.) mortality. Biol Control 77:29–40

    Article  Google Scholar 

  • Dudley TL, Bean DW, Pattison RR, Caires A (2012) Selectivity of a biological control agent, Diorhabda carinulata Desbrochers, 1870 (Coleoptera: Chrysomelidae) for host species within the genus Tamarix Linneaus, 1753. Pan Pac Entomol 88:319–341

    Article  Google Scholar 

  • Erwin KL (2009) Wetlands and global climate change: The role of wetland restoration in a changing world. Wetlands Ecol Manage 17:71–84

    Article  Google Scholar 

  • Eyles A, Pinkard EA, Mohammed C (2009) Shifts in biomass and resource allocation patterns following defoliation in Eucalyptus globulus growing with varying water and nutrient supplies. Tree Physiol 29:753–764

    Article  CAS  PubMed  Google Scholar 

  • Friedman JM, Roelle JE, Gaskin JF, Pepper AE, Manhart JR (2008) Latitudinal variation in cold hardiness in introduced Tamarix and native Populus. Evol Appl 1:598–607

    Article  PubMed  PubMed Central  Google Scholar 

  • Fritz RS (1990) Effect of genetic and environmental variation on resistance of willow to sawflies. Oecologia 325–332

  • Gaffke AM, Sing SE, Dudley TL, Bean DW, Russak JA, Mafra-Neto A, Peterson RKD, Weaver DK (2019) Field demonstration of a semiochemical treatment that enhances Diorhabda carinulata biological control of Tamarix spp. Sci Rep 9:1–9

    Article  CAS  Google Scholar 

  • Glenn E, Tanner R, Mendez S, Kehret T, Moore D, Garcia J, Valdes C (1998) Growth rates, salt tolerance and water use characteristics of native and invasive riparian plants from the delta of the Colorado River, Mexico. J Arid Environ 40:281–294

    Article  Google Scholar 

  • González E, Shafroth PB, Lee SR, Ostoja SM, Brooks ML (2020a) Combined effects of biological control of an invasive shrub and fluvial processes on riparian vegetation dynamics. Biol Invasions 22:2339–2356

    Article  Google Scholar 

  • González E, Shafroth PB, Lee SR, Reed SC, Belnap J (2020b) Riparian plant communities remain stable in response to a second cycle of Tamarix Biocontrol defoliation. Wetlands 40:1863–1875

    Article  Google Scholar 

  • González E, Sher AA, Anderson RM, Bay RF, Bean DW, Bissonnete GJ, Cooper DJ et al (2017) Secondary invasions of noxious weeds associated with control of invasive Tamarix are frequent, idiosyncratic and persistent. Biol Cons 213:106–114

    Article  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058

    Article  Google Scholar 

  • Heard TA, Winterton SL (2000) Interactions between nutrient status and weevil herbivory in the biological control of water hyacinth. J Appl Ecol 37:117–127

    Article  Google Scholar 

  • Hemminga MA, Vansoelen J (1992) The performance of the leaf mining microlepidopteran Bucculatrix Maritima (Stt) on the salt marsh halophyte, Aster Tripolium (L), exposed to different salinity conditions. Oecologia 89:422–427

    Article  CAS  PubMed  Google Scholar 

  • Herms DA, Mattson WJ Jr (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hudgeons JL, Knutson AE, Heinz KM, DeLoach CJ, Dudley TL, Pattison RR, Kiniry JR (2007) Defoliation by introduced Diorhabda elongata leaf beetles (Coleoptera: Chrysomelidae) reduces carbohydrate reserves and regrowth of Tamarix (Tamaricaceae). Biol Control 43:213–221

    Article  Google Scholar 

  • Hultine KR, Dehn D, Bush SE, Acharya K, D’Antonio CM, Dudley TL, Healey J et al. (2021) Episodic defoliation rapidly reduces starch but not soluble sugars in an invasive shrub, Tamarix spp. Am J Bot In press.

  • Hultine KR, Dudley TL, Koepke DF, Bean DW, Glenn EP, Lambert AM (2015) Patterns of herbivory-induced mortality of a dominant non-native tree/shrub (Tamarix spp.) in a southwestern US watershed. Biol Invasions 17:1729–1742

    Article  Google Scholar 

  • Kennard D, Louden N, Gemoets D, Ortega S, González E, Bean D, Cunningham P et al (2016) Tamarix dieback and vegetation patterns following release of the northern tamarisk beetle ( Diorhabda carinulata ) in western Colorado. Biol Control 101:114–122

    Article  Google Scholar 

  • Keppel G (1991) Design and analysis: a researcher’s handbook, 3rd edn. Prentice-Hall Inc, Englewood Cliffs, NJ, US

    Google Scholar 

  • Lambers H, Stuart F, Chapin III, and Pons TL (2008) Plant Physiological Ecology. Soringer

  • Larsson S (1989) Stressful times for the plant stress: insect performance hypothesis. Oikos 56:277–283

    Article  Google Scholar 

  • Lee S-R, Jo Y-S, Park C-H, Friedman JM, Olson MS (2018) Population genomic analysis suggests strong influence of river network on spatial distribution of genetic variation in invasive saltcedar across the southwestern US. Mol Ecol 12:3218–3221

    Google Scholar 

  • Lewis PA, DeLoach CJ, Knutson AE, Tracy JL, Robbins TO (2003) Biology of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae), an Asian leaf beetle for biological control of saltcedars (Tamarix spp.) in the United States. Biol Control 27:101–116

    Article  Google Scholar 

  • Long R, Bush SE, Grady KC, Smith DS, Potts DL, D’Antonio CM, Dudley TL et al (2017) Can local adaptation explain varying patterns of herbivory tolerance in a recently introduced woody plant in North America? Conserv Physiol 5:1–13

    Article  Google Scholar 

  • Long RW (2020) Tradeoffs and Trait Variation in Tamarisk (Tamarix spp.) Across Environmental Gradients. University of California, Santa Barbara

  • Manion P (1981) Tree disease concepts. Prentice-Hall [ed.],. Englewood Cliffs, NJ

  • Manion PD (1991) Tree disease concepts, 2nd edn. Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Soc Nat 134:1–19

    Google Scholar 

  • Merritt DM, Shafroth PB (2012) Edaphic, salinity, and stand structural trends in chronosequences of native and non-native dominated riparian forests along the Colorado River, USA. Biol Invasions 14:2665–2685

    Article  Google Scholar 

  • Moon DC, Stiling P (2002) The effects of salinity and nutrients on a tritrophic salt- marsh system. Ecology 83:2465–2476

    Article  Google Scholar 

  • Moran PJ, DeLoach CJ, Dudley TL, Sanabria J (2009) Open field host selection and behavior by tamarisk beetles (Diorhabda spp.) (Coleoptera: Chrysomelidae) in biological control of exotic saltcedars (Tamarix spp.) and risks to non-target athel (T. aphylla) and native Frankenia spp. Biol Control 50:243–261

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nagler PL, Glenn EP, Didan K, Osterberg J, Jordan F, Cunningham J (2008) Wide-area estimates of stand structure and water use of tamarix spp. on the lower colorado river: implications for restoration and water management projects. Restor Ecol 16:136–145

    Article  Google Scholar 

  • Ohmart RD, Anderson BW, Hunter WC (1988) The ecology of the lower Colorado River from Davis dam to the Mexico-United States international boundary: a community profile. 296 pp

  • Pattison RR, C. M. D'Antonio, and T. L. Dudley. (2011) Biological control reduces growth, and alters water relations of the saltcedar tree (Tamarix spp.) in western Nevada, USA. J Arid Environ 75:346–352

    Article  Google Scholar 

  • Perry LG, Andersen DC, Reynolds LV, Nelson SM, Shafroth PB (2012) Vulnerability of riparian ecosystems to elevated CO 2 and climate change in arid and semiarid western North America. Glob Change Biol 18:821–842

    Article  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164

    Article  Google Scholar 

  • Renault, S., S. Wolfe, J. Markham, and G. Avila-Sakar. 2016. Increased resistance to a generalist herbivore in a salinity-stressed non-halophytic plant. AoB Plants 8: plw028.

  • Rossi AM, Stiling P (1998) The interactions of plant clone and abiotic factors on a gall-making midge. Oecologia 116:170–176

    Article  PubMed  Google Scholar 

  • Schile L, Mopper S (2006) The deleterious effects of salinity stress on leafminers. Ecol Entomol 31:345–351

    Article  Google Scholar 

  • Schulze ED, Robichaux RH, Grace J, Rundel PW, Ehleringer JR (1987) Plant water balance. Bioscience 37:30–37

    Article  Google Scholar 

  • Sexton JP, Mckay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660

    Article  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Stiling PD, Rossi AM (1996) Complex effects of genotype and environment on insect herbivores and their enemies. Ecology 77:2212–2218

    Article  Google Scholar 

  • Strauss SY (1990) The role of plant genotype, environment and gender in resistance to a specialist chrysomelid herbivore. Oecologia 84:111–116

    Article  PubMed  Google Scholar 

  • Trumble JT, Kolodney-Hirsch DM, Ting IP (1993) Plant Compensation for Anthropod Herbivory. Annreventomol 38:93–119

    Google Scholar 

  • Tyerman SD, Munns R, Fricke W, Arsova B, Barkla BJ, Bose J, Bramley H et al (2019) Energy costs of salinity tolerance in crop plants. New Phytol 221:25–29

    Article  PubMed  Google Scholar 

  • White T (1978) The importance of a relative shortage of food in animal ecology. Oecologia 86:71–86

    Article  Google Scholar 

  • Williams WI, Friedman JM, Gaskin JF, Norton AP (2014) Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol Appl 7:381–393

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the numerous undergrads from the Riparian InVasion Research Lab at the University of California, Santa Barbara for assistance with data collection and experiment execution. Notably, Catherine Patton for her assistance in the beetle preference trials and Eric Pelligrini for his help with the salinity trials. We thank the UCSB Tuesday night plant ecology and the members of the D’Antonio and Dudley labs for their helpful discussion on the manuscript. We would also like to thank our funding sources; the University of California, Santa Barbara Wooster Family Award to RWL, a grant from the US Department of Agriculture, National Institute of Food and Agriculture (Grant # 2015-67013-12138) awarded to KRH, TLD and CMD, and a grant awarded to TLD from California Environmental Protection Agency, Division of Pesticide Regulation. (Grant # 16-PML-G001).

Funding

Funding was provided by the University California Santa Barbara Wooster Family Award to RWL, a grant from the US Department of Agriculture, National Institute of Food and Agriculture (Grant # 2015–67013-12138) awarded to KRH, TLD and CMD, and a grant awarded to TLD from California Environmental Protection Agency, Division of Pesticide Regulation. (Grant # 16-PML-G001).

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RWL designed and implemented the experiment, RWL analyzed the data with suggestions from AML, RWL wrote the manuscript and CMD, TLD, KRH, and AML all provided substantial edits.

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Correspondence to Randall W. Long.

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Long, R.W., D’Antonio, C.M., Dudley, T.L. et al. Salinity driven interactions between plant growth and a biological control agent. Biol Invasions 23, 3161–3173 (2021). https://doi.org/10.1007/s10530-021-02556-x

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