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Testing the Enemy Release Hypothesis on tall-statured grasses in South Africa, using Arundo donax, Phragmites australis, and Phragmites mauritianus as models

Published online by Cambridge University Press:  17 August 2018

K. Canavan ,
I.D. Paterson ,
M.P. Hill  and
T.L. Dudley
K. Canavan*
Affiliation:
Department of Zoology and Entomology, Centre for Biological Control, Rhodes University, PO Box 94 Grahamstown, South Africa
I.D. Paterson
Affiliation:
Department of Zoology and Entomology, Centre for Biological Control, Rhodes University, PO Box 94 Grahamstown, South Africa
M.P. Hill
Affiliation:
Department of Zoology and Entomology, Centre for Biological Control, Rhodes University, PO Box 94 Grahamstown, South Africa
T.L. Dudley
Affiliation:
Marine Science Institute, University of California, Santa Barbara, CA 93106-6150, USA
*
*Author for correspondence Phone: +27 46 603 8763 Fax: +2746 622 8959 E-mail: [email protected]
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Abstract

The Enemy Release Hypothesis (ERH) predicts that introduced plant species can escape herbivory and therefore have a competitive advantage over native plants, which are exposed to both generalist and specialist natural enemies. In this study, the ERH was explored using the invasive alien species, Arundo donax and two native tall-statured grasses, the cosmopolitan Phragmites australis and African endemic Phragmites mauritianus in South Africa. It was predicted that A. donax would have reduced species richness of herbivores compared with the native Phragmites spp., that it would be devoid of specialist herbivores and would thus be experiencing enemy escape in the adventive range. The herbivore assemblages were determined from both field surveys and a literature review. The assumptions of the ERH were for the most part not met; 13 herbivores were found on A. donax compared with 17 on P. australis and 20 on P. mauritianus. Arundo donax had two specialist herbivores from its native range, and shared native herbivores with Phragmites spp. Although A. donax had reduced species richness and diversity compared with that found in the native distribution, it has partially re-acquired a herbivore assemblage which is similar to that found on analogous native species. This suggests that enemy release may not fully explain the invasive success of A. donax in South Africa.

Keywords

Enemy Release Hypothesistall-statured grassespre-introductory surveybiological controlTetramesa romana
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 3 , June 2019 , pp. 287 - 299
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Copyright
Copyright © Cambridge University Press 2018 

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References

Allen, W.J., Young, R.E., Bhattarai, G.P., Croy, J.R., Lambert, A.M., Meyerson, L.A. & Cronin, J.T. (2015) Multitrophic enemy escape of invasive Phragmites australis and its introduced herbivores in North America. Biological Invasions 17(12), 3419–3432.Google Scholar
Andrew, N.R. & Hughes, L. (2005) Herbivore damage along a latitudinal gradient: relative impacts of different feeding guilds. Oikos 108(1), 176–182.Google Scholar
Assefa, Y., Conlong, D.E., Van den Berg, J. & Le Rü, B.P. (2008) The wider distribution of Eldana saccharina (Lepidoptera: Pyralidae) in South Africa and its potential risk to maize production. Proceedings of the Annual Congress – South African Sugar Technologists’ Association 81, 290–297.Google Scholar
Bell, G.P. (1997) Ecology and management of Arundo donax, and approaches to riparian habitat restoration in southern California. pp. 103–113 in Brock, J., Wade, M., Pyšek, P., Green, D. (Eds) Plant Invasions: Studies From North America and Europe. Leiden, The Netherlands, Backhuys Publishers.Google Scholar
Blackman, R.L. (2007) Aphids on the world's herbaceous plants and shrubs. Vol. 1: host lists and keys; Vol. 2: the aphids. Entomologia Experimentalis et Applicata 125(3), 325–325.Google Scholar
Blackman, R.L. & Eastop, V.F. (2008) Aphids on the World's Herbaceous Plants and Shrubs. London, John Wiley & Sons.Google Scholar
Blossey, B. (2014) Identification, Development, and Release of Insect Biocontrol Agents for the Management of Phragmites Australis. Publication CR-14-2. The US Army Engineer Research and Development Center (ERDC), Department of Natural Resources, New York, Cornell University.Google Scholar
Canavan, K., Paterson, I.D., Lambertini, C. & Hill, M.P. (2018) Expansive reed populations – alien invasion or disturbed wetlands? AoB Plants 10, doi: doi.org/10.1093/aobpla/ply014.Google Scholar
Casagrande, R.A., Häfliger, P., Hinz, H.L., Tewksbury, L. & Blossey, B. (2018) Grasses as appropriate targets in weed biocontrol: is the common reed, Phragmites australis, an anomaly? BioControl 63, 1–13.Google Scholar
Chao, A., Colwell, R.K., Lin, C.W. & Gotelli, N.J. (2009) Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90(4), 1125–1133.Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. & MacIsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters 7(8), 721–733.Google Scholar
Colwell, R.K. (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. Users Guide and application published at httppurloclcorgestimates, Version 7., User's Guide and application. Available online at http://purl.oclc.org/estimates.Google Scholar
Cripps, M.G., Schwarzländer, M., McKenney, J.L., Hinz, H.L. & Price, W.J. (2006) Biogeographical comparison of the arthropod herbivore communities associated with Lepidium draba in its native, expanded and introduced ranges. Journal of Biogeography 33, 2107–2119.Google Scholar
Cronin, J.T., Bhattarai, G.P., Allen, W.J. & Meyerson, L.A. (2015) Biogeography of a plant invasion: plant–herbivore interactions. Ecology 96(4), 1115–1127.Google Scholar
Dudley, T.L. & Lambert, A.M. (2007) Biological Control of Invasive Giant Reed (Arundo donax), Completion Report, U.S. California, Fish & Wildlife Service/Santa Clara River Trustee Council.Google Scholar
Dudley, T.L., Lambert, A.M. & Kirk, A. (2006) Augmentation biological control of Arundo donax. pp. 141–144 in Hoddle, M.S. & Johnson, M.W. (Eds) California Conference on Biological Control V. California, Marine Science Institute.Google Scholar
Dudley, T. L., Lambert, A. M., Kirk, A. & Tamagawa, Y. (2008) Herbivores associated with Arundo donax. in California. pp. 138–145 in Julien, M. (Ed.) Proceedings of the XII International Symposium on Biological Control of Weeds. La Grand Motte, France, CABI.Google Scholar
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: a study in coevolution. Evolution 18(4), 586–608.Google Scholar
Fish, L., Mashau, A., Moeaha, M. & Nembudani, M. (2015) Identification Guide to Southern African Grasses. An Identification Manual with Keys, Descriptions and Distributions. Pretoria, South African National Biodiversity Institute.Google Scholar
Gautam, R.D., Suroshe, S. & Mahapatro, G.K. (2009) Unique record of chloropid pest in rice (Oryza sativa). Indian Journal of Agricultural Sciences 79, 841–843.Google Scholar
Frenzel, M. & Brandl, R. (2003) Diversity and abundance patterns of phytophagous insect communities on alien and native host plants in the Brassicaceae. Ecography 26(6), 723–730.Google Scholar
Getu, E., Overholt, W.A. & Kairu, E. (2001) Distribution and species composition of stemborers and their natural enemies in maize and sorghum in Ethiopia. International Journal of Tropical Insect Science 21(4), 353–359.Google Scholar
Goolsby, J.A. & Moran, P. (2009) Host range of Tetramesa romana Walker (Hymenoptera: Eurytomidae), a potential biological control of giant reed, Arundo donax L. in North America. Biological Control 49(2), 160–168.Google Scholar
Goolsby, J.A., Kirk, A.A., Moran, P.J., Racelis, A.E., Adamczyk, J.J., Cortés, E., Marcos García, M.Á., Martinez Jimenez, M., Summy, K.R., Ciomperlik, M.A. & Sands, D.P. (2011) Establishment of the armored scale, Rhizaspidiotus donacis, a biological control agent of Arundo donax. Southwestern Entomologist 36(3), 373–374.Google Scholar
Häfliger, P., Schwarzlaender, M. & Blossey, B. (2005) Biology of Platycephala planifrons (Diptera: Chloropidae) and its potential effectiveness as biological control agent for invasive Phragmites australis in North America. Biological control 34(3), 302–311.Google Scholar
Henderson, L. (2001) Alien Weeds and Invasive Plants. A Complete Guide to Declared Weeds and Invaders in South Africa. Pretoria, Agricultural Research Council, Plant Protection Research Institute.Google Scholar
Hill, M.O. (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54(2), 427–432.Google Scholar
Hoffmann, J.H. & Moran, V.C. (1991) Biological control of Sesbania punicea (Fabaceae) in South Africa. Agriculture, Ecosystems & Environment 37(1), 157–173.Google Scholar
Jost, L. (2007) Partitioning diversity into independent alpha and beta components. Ecology 88(10), 2427–2439.Google Scholar
Keane, R.M. & Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17(4), 164–170.Google Scholar
Lake, J.C. & Leishman, M.R. (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biological Conservation 117(2), 215–226.Google Scholar
Lambert, A.M. & Casagrande, R.A. (2006) Distribution of native and exotic Phragmites australis in Rhode Island. Northeastern Naturalist 13(4), 551–560.Google Scholar
Lambert, A.M., Dudley, T.L. & Saltonstall, K. (2010) Ecology and impacts of the large-statured invasive grasses Arundo donax and Phragmites australis in North America. Invasive Plant Science and Management 3(4), 489–494.Google Scholar
Le Rü, B.P., Ong'amo, G.O., Moyal, P., Ngala, L., Musyoka, B., Abdullah, Z., Cugala, D., Defabachew, B., Haile, T.A., Matama, T.K. & Lada, V.Y. (2006 a) Diversity of lepidopteran stem borers on monocotyledonous plants in eastern Africa and the islands of Madagascar and Zanzibar revisited. Bulletin of Entomological Research 96, 555–563.Google Scholar
Le Rü, B.P., Ong'amo, G.O., Moyal, P., Muchugu, E., Ngala, L., Musyoka, B., Abdullah, Z., Matama-Kauma, T., Lada, V.Y., Pallangyo, B. & Omwega, C.O. (2006 b) Geographic distribution and host plant ranges of East African noctuid stem borers. International Journal of Entomology 42(3–4), 353–361.Google Scholar
Liu, H. & Stiling, P. (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biological Invasions 8(7), 1535–1545.Google Scholar
McClay, A.S. (1988) The potential of Larinus planus (Coleoptera: Curculionidae), an accidentally-introduced insect in North America, for biological control of Cirsium arvense. pp. 173–179 in Proceedings of the Seventh International Symposium on Biological Control of Weeds, 6 March – 11 March 1988. Istituto Sperimentale per la Patologia Vegetale Ministerio dell'Agricoltura e delle Foreste, Rome.Google Scholar
McClay, A.S. & Balciunas, J.K. (2005) The role of pre-release efficacy assessment in selecting classical biological control agents for weeds – applying the Anna Karenina principle. Biological Control 35(3), 197–207.Google Scholar
Menhinick, E.F. (1964) A comparison of some species-individuals diversity indices applied to samples of field insects. Ecology 45(4), 859–861.Google Scholar
Meyrick, E. (1912) New South African Microlepidoptera. Annals of the South African Museum 10(3), 349–379.Google Scholar
Mitchell, C.E., Agrawal, A.A., Bever, J.D., Gilbert, G.S., Hufbauer, R.A., Klironomos, J.N., Maron, J.L., Morris, W.F., Parker, I.M., Power, A.G. & Seabloom, E.W. (2006) Biotic interactions and plant invasions. Ecology Letters 9(6), 726–740.Google Scholar
Mlynarek, J.J., Moffat, C.E., Edwards, S., Einfeldt, A.L., Heustis, A., Johns, R., MacDonnell, M., Pureswaran, D.S., Quiring, D.T., Shibel, Z. & Heard, S.B. (2017) Enemy escape: a general phenomenon in a fragmented literature? FACETS 2(2), 1015–1044.Google Scholar
Moeletsi, M.E., Walker, S. & Landman, W.A. (2011) ENSO and implications on rainfall characteristics with reference to maize production in the Free State Province of South Africa. Physics and Chemistry of the Earth, Parts A/B/C 36(14), 715–726.Google Scholar
Moolman, J., Van den Berg, J., Conlong, D., Cugala, D., Siebert, S. & Le Rü, B. (2014) Species diversity and distribution of lepidopteran stem borers in South Africa and Mozambique. Journal of Applied Entomology 138(1–2), 52–66.Google Scholar
Moran, P.J., Vacek, A.T., Racelis, A.E., Pratt, P.D. & Goolsby, J.A. (2017) Impact of the arundo wasp, Tetramesa romana (Hymenoptera: Eurytomidae), on biomass of the invasive weed, Arundo donax (Poaceae: Arundinoideae), and on revegetation of riparian habitat along the Rio Grande in Texas. Biocontrol Science and Technology 27(1), 96–114.Google Scholar
Moyal, P., Le Rü, B., Conlong, D., Cugala, D., Defabachew, B., Matama-Kauma, T., Pallangyo, B. & Van den Berg, J. (2010) Systematics and molecular phylogeny of two African stem borer genera, Sciomesa Tams & Bowden and Carelis Bowden (Lepidoptera: Noctuidae). Bulletin of Entomological Research 100(6), 641–659.Google Scholar
Mukherjee, A., Jones, J.W., Cuda, J.P., Kiker, G. & Overholt, W.A. (2012) Effect of simulated herbivory on growth of the invasive weed Hygrophila polysperma: experimental and predictive approaches. Biological Control 60(3), 271–279.Google Scholar
Nartshuk, E.P. (2014) Grass-fly larvae (Diptera, Chloropidae): diversity, habitats, and feeding specializations. Entomological Review 94(4), 514–525.Google Scholar
Ndemah, R., Schulthess, F., Le Rü, B. & Bame, I. (2007) Lepidopteran cereal stemborers and associated natural enemies on maize and wild grass hosts in Cameroon. Journal of Applied Entomology 131(9–10), 658–668.Google Scholar
Ong'amo, G.O., Rü, B.P.L., Dupas, S., Moyal, P., Muchugu, E., Calatayud, P.A. & Silvain, J.F. (2006) The role of wild host plants in the abundance of lepidopteran stem borers along altitudinal gradient in Kenya. International Journal of Entomology 42(3–4), 363–370.Google Scholar
Ong'amo, G.O., Le Gall, P., Ndemah, R. & Le Rü, B.P. (2014) Diversity and host range of lepidopteran stemborer species in Cameroon. African Entomology 22(3), 625.Google Scholar
Onyango, F.O. (1994) Continuous rearing of the maize stem borer Busseola fusca on an artificial diet. Entomologia Experimentalis et Applicata 73(2), 139–144.Google Scholar
Orians, C.M. & Ward, D. (2010) Evolution of plant defenses in nonindigenous environments. Annual Review of Entomology 55, 439–459.Google Scholar
Peet, R.K. (1974) The measurement of species diversity. Annual Review of Ecology and Systematics 5, 285–307.Google Scholar
Prinsloo, G.L. & Uys, V.M. (2015) Cereals and sugarcane. pp. 88–156 in Prinsloo, G.L. & Uys, V.M. (Eds) Insects of Cultivated Plants and Natural Pastures of Southern Africa. Cape Town, The Entomological Society of Southern Africa.Google Scholar
Prior, K.M., Powell, T.H., Joseph, A.L. & Hellmann, J.J. (2015) Insights from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects. Biological Invasions 17(5), 1283–1297.Google Scholar
Purvis, A. & Hector, A. (2000) Getting the measure of biodiversity. Nature 405(6783), 212.Google Scholar
Quiring, D., Flaherty, L., Johns, R. & Morrison, A. (2006) Variable effects of plant module size on abundance and performance of galling insects. pp. 189–197 in Ozaki, K., Yukawa, J., Ohgushi, T. & Price, P.W. (Eds) Galling Arthropods and Their Associates. Tokyo: Japan, Springer.Google Scholar
Reddy, K.V.S. (1987) Sorghum stem borers in Eastern Africa. pp. 33–40 in International Workshop on Sorghum Stem Borers. Hyderabad: India, International Crops Research Institute for the Semi-Arid Tropics Centre.Google Scholar
Rutherford, M.C., Mucina, L. & Powrie, L.W. (2006) Biomes and bioregions of Southern Africa. pp. 30–51 in The Vegetation of South Africa, Lesotho and Swaziland. Pretoria, South African National Biodiversity Institute.Google Scholar
Saltonstall, K. (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences 99(4), 2445–2449.Google Scholar
Schwarzländer, M. & Häfliger, P. (2000) Shoot flies, gall midges, and shoot and rhizome mining moths associated with common reed in Europe and their potential for biological control. in Proceedings of the Xth International Symposium on Biological Control of Weeds. Montana State University, Bozeman, Montana.Google Scholar
Skuhravá, M. & Skuhravý, V. (1992) Biology of gall midges on common reed in Czechoslovakia. pp. 196–207 in Shorthouse, J.D. & Rohfritsch, O. (Eds) Biology of Insect-Induced Galls. New York, Oxford, Oxford University Press.Google Scholar
Slater, J.A. (1976) Monocots and chinch bugs: a study of host plant relationships in the Lygaeid subfamily Blissinae (Hemiptera: Lygaeidae). Biotropica 8, 143–165.Google Scholar
Slater, J.A. & Wilcox, D.B. (1973) The chinch bugs, or Blissinae of South Africa (Hemiptera: Lygaeidae). Memoirs of the Entomological Society of Southern Africa 12, 135.Google Scholar
Spellerberg, I.F. & Fedor, P.J. (2003) A tribute to claude shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the ‘Shannon–Wiener’ index. Global Ecology and Biogeography 12(3), 177–179.Google Scholar
Spencer, D.F., Tan, W. & Whitehand, L.C. (2010) Variation in Arundo donax stem and leaf strength: implications for herbivory. Aquatic Botany 93(2), 75–82.Google Scholar
Tarin, D., Pepper, A.E., Goolsby, J.A., Moran, P.J., Arquieta, A.C., Kirk, A.E. & Manhart, J.R. (2013) Microsatellites uncover multiple introductions of clonal giant reed (Arundo donax). Invasive Plant Science Management 6, 328–338.Google Scholar
Tewksbury, L., Casagrande, R., Blossey, B., Häfliger, P. & Schwarzländer, M. (2002) Potential for biological control of Phragmites australis in North America. Biological Control 23(2), 191–212.Google Scholar
Tracy, J.L. & DeLoach, C.J. (1998) Suitability of classical biological control for giant reed (Arundo donax) in the United States. pp. 73–109 in Bell, C.E. (Ed.) Arundo and Saltcedar Management Workshop Proceedings. California, University of California Cooperative Extension.Google Scholar
Tscharntke, T. (2008) Changes in shoot growth of Phragmites australis caused by the gall maker Giraudiella inclusa (Diptera: Cecidomyiidae). Oikos 54(3), 370–377.Google Scholar
van den Berg, J. & Rebe, M. (2001) Developing habitat management systems for gramineous stemborers in South Africa. Insect Science and its Application 21(4), 381–388.Google Scholar
van der Toorn, J. & Mook, J.H. (1982) The influence of environmental factors and management on stands of Phragmites australis. I. Effects of burning, frost and insect damage on shoot density and shoot size. Journal of Applied Ecology 19, 477–499.Google Scholar
van Lenteren, J.C., Babendreier, D., Bigler, F., Burgio, G., Hokkanen, H.M.T., Kuske, S., Loomans, A.J.M., Menzler-Hokkanen, I., Van Rijn, P.C.J., Thomas, M.B. & Tommasini, M.G. (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. Biocontrol 48(1), 3–38.Google Scholar
van Wilgen, B.W., Nel, J.L. & Rouget, M. (2007) Invasive alien plants and South African rivers: a proposed approach to the prioritization of control operations. Freshwater Biology 52, 711–723.Google Scholar
Vári, L., Martin, K. & Kroon, D.M. (2002) Classification and Checklist of the species of Lepidoptera Recorded in Southern Africa. Pretoria, Simple Solutions.Google Scholar
Weyl, P.S.R. (2015)Friend or foe?: Resolving the status of the submerged macrophyte Myriophyllum spicatum L. (Haloragaceae) in southern Africa. PhD Thesis, Rhodes University.Google Scholar
Whittaker, R.H. (1972) Evolution and measurement of species diversity. Taxon 21(2), 213–251.Google Scholar
World Weather Online (2016) Yearly Weather Summary. Available online at http://www.worldweatheronline.com (accessed 27 January 2016).Google Scholar
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