Interactions among Tamarix (Tamaricaceae), Opsius stactogalus (Cicadellidae), and Litter Fungi Limit Riparian Plant Establishment

Gibney M. Siemion¹, Lawrence E. Stevens^2*

¹Grand Canyon Wildlands Council, Inc., Flagstaff, USA.
²Museum of Northern Arizona, Flagstaff, USA.

DOI: 10.4236/ae.2015.32008                

Abstract

One of the most significant plant invasions in the U.S. has been that of the Old World genus Tamarix. While Tamarix spp. is widely studied, surprisingly little is known about more complex trophically-linked community mechanisms influencing under-canopy succession. We investigated multi- trophic interactions among Tamarix spp., nonnative host-specific Opsius stactogalus leafhopper distribution and honeydew production, and the Tamarix spp. canopy floor fungal assemblage. We quantified leafhopper abundance and honeydew throughfall, and tested under-canopy seed viability and seedling mortality across a 1600 m elevation gradient in the lower Colorado River basin in 2007. We conducted field and laboratory experiments in 2007-08 to test the effects of Tamarix spp. litter fungi, synthetic honeydew, and the combination of those variables on germination and seedling survivorship of three common, co-occurring phreatophyte (riparian groundwater-dependent plant) species. Tamarix spp. litter and honeydew treatments reduced understory seed viability and recruitment of two native, woody riparian species (Populus fremontii and Baccharis salicina), as well as Tamarix spp. Four major patterns were detected. 1) Litter fungi alone and synthetic honeydew alone reduced seed viability and seedling survivorship of all three species by two- to four-fold. 2) Synthetic honeydew + litter reduced Tamarix spp. and P. fremontii seed and seedling viability by up to 10-fold. 3) Synthetic honeydew concentration and seedling mortality were positively related among all three plant species. 4) B. salicina was less susceptible to all treatments than Tamarix spp. and P. fremontii. These results indicate that complex interactions among nonnative Tamarix spp., nonnative Opsius leafhopper honeydew production, and soil fungi may influence riparian phreatophyte recruitment and succession.

Keywords

Herbivore, Honeydew, Invasion Ecology, Multi-Trophic Interaction, Opsius stactogalus, Riparian, Tamarix

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Wilson, E.O. (1997) Strangers in Paradise. Island Press, Washington DC.
[2]	Gaskin, J. and Schaal, B. (2002) Hybrid Tamarix Widespread in U.S. Invasion and Undetected in Native Asian Range. Proceedings of the National Academy of Sciences of the United States of America, 99, 11256-11259. http://dx.doi.org/10.1073/pnas.132403299
[3]	Dewine, J. and Cooper, D. (2008) Canopy Shade and the Successional Replacement of Tamarisk by Native Box Elder. Journal of Applied Ecology, 45, 505-514. http://dx.doi.org/10.1111/j.1365-2664.2007.01440.x
[4]	Webb, R., Leake, A.S. and Turner, R.M. (2007) The Ribbon of Green: Change in Riparian Vegetation in the Southwestern United States. The University of Arizona Press, Tucson.
[5]	Robinson, T. (1965) Introduction, Spread and Aerial Extent of Saltcedar (Tamarix) in the Western States. United States Geological Survey Professional Paper 491-A. USA Geological Survey, Reston.
[6]	Carothers, S.W., Johnson, R.R. and Aitchison, S.W. (1974) Population Structure and Social Organization of Southwestern Riparian Birds. American Zoologist, 14, 97-108.
[7]	Mahoney, J. and Rood, S. (1998) Streamflow Requirements for Cottonwood Seedling Recruitment—An Integrative Model. Wetlands, 18, 634-645. http://dx.doi.org/10.1007/BF03161678
[8]	Grand Canyon Wildlands Council (2005) Glen and Grand Canyon Riparian Restoration Project: Final Report for Arizona Water Protection Fund. Contract # 99-075WPF, Phoenix.
[9]	Everitt, B. (1980) Ecology of Saltcedar—A Plea for Research. Environmental Geology, 3, 77-84. http://dx.doi.org/10.1007/BF02473474
[10]	Turner, R. and Karpiscak, M. (1980) Recent Vegetation Changes along the Colorado River between Glen Canyon Dam and Lake Mead, Arizona. USGS Professional Paper 1132.
[11]	Pataki, D., Bush, S.E., Gardner, P., Solomon, D.K. and Ehleringer, J.R. (2005) Ecohydrology in a Colorado River Riparian Forest: Implications for the Declines of Populus fremontii. Ecological Applications, 15, 1009-1018. http://dx.doi.org/10.1890/04-1272
[12]	Rood, S. and Mahoney, J. (1990) Collapse of Riparian Poplar Forests Downstream from Dams in Western Prairies: Probable Causes and Prospects for Mitigation. Environmental Management, 14, 451-464. http://dx.doi.org/10.1007/BF02394134
[13]	Hudgeons, J.L., Knutson, A.E., Heinz, K.M., DeLoach, C.J., Dudley, T.L., Pattison, R.R. and Kiniry, J.R. (2007) Defoliation by Introduced Diorhabda elongata Leaf Beetles (Coleoptera: Chrysomelidae) Reduces Carbohydrate Reserves and Regrowth of Tamarix (Tamaricaceae). Biological Control, 43, 213-221. http://dx.doi.org/10.1016/j.biocontrol.2007.07.012
[14]	Harding, L. (1930) The Biology of Opsius stactogalus Fieber (Homoptera: Cicadellidae). Journal of the Kansas Entomological Society, 3, 7-22.
[15]	Yard, H., Van Riper III, C., Brown, B.T. and Kearsley, M.J. (2004) Diets of Insectivorous Birds along the Colorado River in Grand Canyon, Arizona. The Condor, 106, 106-115. http://dx.doi.org/10.1650/7242
[16]	Wiesenborn, W. (2005) Biomass of Arthropod Trophic Levels on Tamarix ramosissima (Tamaricaceae) Branches. Environmental Entomology, 34, 656-663. http://dx.doi.org/10.1603/0046-225X-34.3.656
[17]	Stadler, B. and Michalzik, B. (1998) Linking Aphid Honeydew, Throughfall, and Forest Floor Solution Chemistry of Norway Spruce. Ecology Letters, 1, 13-16. http://dx.doi.org/10.1046/j.1461-0248.1998.00006.x
[18]	Stadler, B. and Müller, T. (1996) Aphid Honeydew and Its Effect on the Phyllosphere Microflora of Picea abies (L.) Karst. Oecologia, 108, 771-776. http://dx.doi.org/10.1007/BF00329054
[19]	Stevens, L. (1985) Aspects of Invertebrate Herbivore Community Dynamics on Tamarix chinensis and Salix exigua in the Grand Canyon. MS Thesis, Northern Arizona University, Flagstaff.
[20]	Levine, J., Vilà, M., D’Antonio, C.M., Dukes, J.S., Grigulis, K. and Lavorel, S. (2003) Mechanisms Underlying the Impacts of Exotic Plant Invasions. Proceedings of the Royal Society B: Biological Sciences, 270, 775-781. http://dx.doi.org/10.1098/rspb.2003.2327
[21]	Lesica, P. and DeLuca, T. (2004) Is Tamarix Allelopathic? Plant and Soil, 267, 357-365. http://dx.doi.org/10.1007/s11104-005-0153-y
[22]	Mawson, C. (1948) Honeydew on Lime Trees. Nature, 161, 176. http://dx.doi.org/10.1038/161176b0
[23]	Dighton, J. (1978) Effects of Synthetic Lime Aphid Honeydew on Populations of Soil Organisms. Soil Biology & Biochemistry, 10, 369-376. http://dx.doi.org/10.1016/0038-0717(78)90060-3
[24]	Dighton, J. (1978) In Vitro Experiments Simulating the Possible Fates of Aphid Honeydew Sugars in Soil. Soil Biology & Biochemistry, 10, 53-57. http://dx.doi.org/10.1016/0038-0717(78)90010-X
[25]	Grier, C. and Vogt, D. (1990) Effects of Aphid Honeydew on Soil Nitrogen Availability and Net Primary Production in an Alnus rubra Plantation in Western Washington. Oikos, 57, 114-118. http://dx.doi.org/10.2307/3565744
[26]	Dickson, L. and Whitham, T. (1996) Genetically-Based Plant Resistant Traits Affect Arthropods, Fungi, and Birds. Oecologia, 106, 400-406. http://dx.doi.org/10.1007/BF00334568
[27]	Batra, R.C., Sharma, D.R., Kumar, R. and Arora, P.K. (2002) Association of Citrus Whitefly Population with Sooty Mould. Indian Journal of Citriculture, 1, 171-175.
[28]	Dik, A. and van Pelt, J. (1993) Interaction between Phyllosphere Yeasts, Aphid Honeydew and Fungicide Effectiveness in Wheat under Field Conditions. Plant Pathology, 41, 661-675. http://dx.doi.org/10.1111/j.1365-3059.1992.tb02550.x
[29]	Hillocks, R. and Brettell, J. (1993) The Association between Honeydew and Growth of Cladosporium herbarum and Other Fungi on Cotton Lint. Tropical Science, 33, 121-129.
[30]	Beauchamp, V., Stromberg, J.C. and Stutz, J.C. (2005) Interactions between Tamarix ramosissima (Saltcedar), Populus fremontii (Cottonwood), and Mycorrhizal Fungi: Effects on Seedling Growth and Plant Species Coexistence. Plant and Soil, 275, 221-231. http://dx.doi.org/10.1007/s11104-005-1740-7
[31]	Elgersma, K. and Ehrenfeld, J. (2011) Linear and Non-Linear Impacts of a Nonnative Plant Invasion on Soil Microbial Community Structure and Function. Biological Invasions, 13, 757-768. http://dx.doi.org/10.1007/s10530-010-9866-9
[32]	National Weather Service Forecast Office (NWSFO) (2008) National Oceanic and Atmospheric Administration. http://www.weather.gov/climate/xmacis.php?wfo=psr
[33]	SAS Institute (2008) JMP Version 7.0.2. SAS Institute Inc., Cary.
[34]	Rice, W. (1989) Analyzing Tables of Statistical Tests. Evolution, 43, 223-225. http://dx.doi.org/10.2307/2409177
[35]	Hendrix, D., Wei, Y. and Leggett, J.E. (1992) Homopteran Honeydew Sugar Composition Is Determined by both the Insect and Plant Species. Comparative Biochemistry and Physiology Part B, 101, 23-27. http://dx.doi.org/10.1016/0305-0491(92)90153-I
[36]	Byrne, D., Hendrix, D.L. and Williams III, L.H. (2003) Presence of Trehalulose and Other Oligosaccharides in Hemipteran Honeydew, Particularly Aleyrodidae. Physiological Entomology, 28, 144-149. http://dx.doi.org/10.1046/j.1365-3032.2003.00310.x
[37]	Fischer, M. and Shingleton, A. (2001) Host Plant and Ants Influence the Honeydew Sugar Composition of Aphids. Functional Ecology, 15, 544-550. http://dx.doi.org/10.1046/j.0269-8463.2001.00550.x
[38]	Mortenson, S.G., Weisberg, P.J. and Stevens, L.E. (2011) The Influence of Floods and Precipitation History on Tamarix Establishment in Grand Canyon, Arizona: Consequences for Flow Regime Restoration. Biological Invasions, 14, 1061-1076.
[39]	Schafer, M. and Kotanen, P. (2004) Impacts of Naturally-Occurring Soil Fungi on Seeds of Meadow Plants. Plant Ecology, 175, 19-35.
[40]	Stevens, L.E. (1989) The Status of Ecological Research on Tamarisk (Tamaricaceae: Tamarix ramosissima) in Arizona. In: Kunzman, M.R., Johnson, R.R. and Bennett, P.S., Eds., Tamarisk Control in Southwestern United States, Cooperative National Park Resources Study Unit Special Report Number 9, Tucson, 99-105.
[41]	Reynolds, L. and Cooper, D. (2010) Environmental Tolerance of an Invasive Riparian Tree and Its Potential for Continued Spread in the Southwestern US. Journal of Vegetation Science, 21, 733-743.
[42]	Keane, R. and Crawley, M. (2002) Exotic Plant Invasions and the Enemy Release Hypothesis. Trends in Ecology and Evolution, 17, 164-170. http://dx.doi.org/10.1016/S0169-5347(02)02499-0
[43]	Abbott, K. and Green, P. (2007) Collapse of an Ant-Scale Mutualism in a Rainforest on Christmas Island. Oikos, 116, 1238-1246. http://dx.doi.org/10.1111/j.0030-1299.2007.15629.x
[44]	O’Dowd, D., Green, P.T. and Lake, P.S. (2003) Invasional “Meltdown” on an Oceanic Island. Ecology Letters, 6, 812-817. http://dx.doi.org/10.1046/j.1461-0248.2003.00512.x
[45]	Simberloff, D. and Von Holle, B. (1999) Positive Interactions of Nonindigenous Species: Invasional Meltdown? Biological Invasions, 1, 21-32. http://dx.doi.org/10.1023/A:1010086329619
[46]	Stromberg, J.C. (1998) Functional Equivalency of Saltcedar (Tamarix chinensis) and Fremont Cottonwood (Populus fremontii) along a Free-Flowing River. Wetlands, 18, 675-686. http://dx.doi.org/10.1007/BF03161682
[47]	Stevens, L. and Waring, G. (1985) The Effects of Prolonged Flooding on the Riparian Plant Community in Grand Canyon. In: Johnson, R.R., Ed., Riparian Ecosystems and Their Management: Reconciling Conflicting Uses, U.S. Forest Service, Tucson, General Technical Report RM-120, 81-86.
[48]	DeLoach, C., Carruthers, R.I., Lovich, J.E., Dudley, T.L. and Smith, S.D. (2000) Ecological Interactions in the Biological Control of Saltcedar (Tamarix spp.) in the United States: Toward a New Understanding. In: Spencer, N.R., Ed., Proceedings of the X International Symposium on Biological Control of Weeds, Montana State University Press, Bozeman, 819-873.
[49]	Shafroth, P., Friedman, J.M. and Ischinger, L.S. (1995) Effects of Salinity on Establishment of Populus fremontii (Cottonwood) and Tamarix ramosissima (Saltcedar) in Southwestern United States. Great Basin Naturalist, 55, 58-65.
[50]	Katz, G. and Shafroth, P. (2003) Biology, Ecology, and Management of Elaeagnus angustifolia L. (Russian olive) in Western North America. Wetlands, 23, 763-777. http://dx.doi.org/10.1672/0277-5212(2003)023[0763:BEAMOE]2.0.CO;2
[51]	Wiesenborn, W. (2003) Variation in Opsius stactogalus (Homoptera: Cicadellidae) Egg Density among Tamarix ramosissima (Tamaricaceae) Trees. Pan Pacific Entomologist, 79, 38-44.
[52]	Stevens, L.E., Burke, K.J., Spence, J.R., Pilkington, L. and Hughes, C. (2015) Colorado River Riparian Ecosystem Rehabilitation in Glen Canyon National Recreation Area, Arizona. In: Eleventh Biennial Symposium on Research on the Colorado Plateau, U.S. Geological Survey, Flagstaff, in Press.