Love at first bite? Pre-release surveys reveal a novel association between a native weevil and the invasive Nymphaea mexicana Zuccarini (Nymphaeaceae) in South Africa

Authors

DOI:

https://doi.org/10.17159/2254-8854/2023/a14949

Keywords:

Biological control, enemy release hypothesis, invasive macrophytes, insect herbivores, Mexican waterlily, yellow waterlily

Abstract

Classical biological control aims to suppress alien invasive plant populations by introducing host-specific natural enemies from the native range. This relies on the assumption that invasive plant populations in the invaded range benefit from the release of natural enemies. Pre-release surveys in the invaded range are a useful way to determine if enemy release applies to a particular invasive alien plant, and to determine what other factors may contribute to the invasion. Similarly, pre-release surveys gather information that can be used to compare invaded sites before and after the release of biological control agents and may also identify whether natural enemies have been accidentally introduced into the country. Pre-release surveys were conducted in South Africa on the invasive Nymphaea mexicana Zuccarini (Nymphaeaceae) to gather such information about this species, for which a biological control programme is being developed. There was lower diversity and abundance of herbivores in the native range compared to South Africa, suggesting that N. mexicana does experience enemy release at most sites in South Africa. This support for the enemy release hypothesis justifies the investment in biological control for its management. However, a native weevil, Bagous longulus Gyllenhal (Coleoptera: Curculionidae), was found feeding and reproducing on N. mexicana at three sites, resulting in damage to the leaves and suggesting that a novel association has formed between these species. Bagous longulus may have potential to be distributed to sites of N. mexicana where it is not present, though further investigation is necessary to confirm if its host range is suitable for this to be a safe endeavour. With the exception of sites where B. longulus was present, leaf sizes were large and damage was low, and there is no evidence that any natural enemies have been accidentally introduced from the native range. Findings such as these emphasise the importance of conducting thorough surveys during the development of biological control programmes. 

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

American Public Health Association (APHA). 1998. Standard methods for the examination of water and wastewater. New York: APHA.

Blossey B, Notzold R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: A hypothesis. Journal of Ecology. 83:887–889. https://doi.org/10.2307/2261425

Branco M, Brockerhoff EG, Castagneyrol B, Orazio C, Jactel HE. 2015. Host range expansion of native insects to exotic trees increases with area of introduction and the presence of congeneric native trees. Journal of Applied Ecology. 52:69–77. https://doi.org/10.1111/1365-2664.12362

Canavan K, Paterson I, Hill MP. 2014. The herbivorous arthropods associated with the invasive alien plant, Arundo donax, and the native analogous plant, Phragmites australis, in the Free State Province, South Africa. African Entomology. 22:454–459. https://doi.org/10.4001/003.022.0204

Castagneyrol B, Jactel H, Brockerhoff EG, Perrette N, Larter M, Delzon S, Piou D. 2016. Host range expansion is density dependent. Oecologia. 182:779–788. https://doi.org/10.1007/s00442-016-3711-5

Cheng D, Vrieling K, Klinkhamer PGL. 2011. The effect of hybridization on secondary metabolites and herbivore resistance: Implications for the evolution of chemical diversity in plants. Phytochemistry Reviews. 10:107–117. https://doi.org/10.1007/s11101-010-9194-9

Coetzee JA, Hill MP. 2012. The role of eutrophication in the biological control of water hyacinth, Eichhornia crassipes, in South Africa. BioControl. 57:247–261. https://0-doi.org /10.1007/s10526-011-9426-y

Coetzee JA, Bownes A, Martin GD, Miller BE, Smith R, Weyl PSR, Hill MP. 2021. A review of the biocontrol programmes against aquatic weeds in South Africa. African Entomology. 29:935–964. https://doi.org/10.4001/003.029.0935

Coetzee J, Hill M, Byrne M, Bownes A. 2011. A review of the biological control programmes on Eichhornia crassipes (C. Mart.) Solms (Pontederiaceae), Salvinia molesta DS Mitch. (Salviniaceae), Pistia stratiotes L. (Araceae), Myriophyllum aquaticum (Vell.) Verdc. (Haloragac.). African Entomology. 19:451–468. https://doi.org/10.4001/003.019.0202

Colautti RI, Ricciardi A, Grigorovich IA, Macisaac HJ. 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters. 7:721–733. https://doi.org/10.1111/j.1461-0248.2004.00616.x

Colwell RK. 2006. EstimateS: statistical estimation of species richness and shared species from samples, version 8.0.

Creed RP, Sheldon SP. 1991. The potential for biological control of Eurasian watermilfoil (Myriophyllum spicatum): results of Brownington Pond, Vermont, study and multistate lake survey. Proceedings of the 25th Annual Meeting of the Aquatic Plant Control Research Program: 183–193. US Army Corps of Engineers.

Creed RP, Sheldon SP. 1993. The effect of feeding by a North American weevil, Euhrychiopsis lecontei, on Eurasian watermilfoil (Myriophyllum spicatum). Aquatic Botany. 45:245–256. https://doi.org/10.1016/0304-3770(93)90024-Q

De Lange WJ, van Wilgen BW. 2010. An economic assessment of the contribution of biological control to the management of invasive alien plants and to the protection of ecosystem services in South Africa. Biological Invasions. 12:4113–4124. https://doi.org/10.1007/s10530-010-9811-y

Diop O, Hill MP. 2009. Quantitative post-release evaluation of biological control of floating fern, Salvinia molesta D.S. Mitchell (Salviniaceae), with Cyrtobagous salviniae Calder and Sands (Coleoptera: Curculionidae) on the Senegal River and Senegal River Delta. African Entomology. 17:64–70.

Dudley TL, Lambert A, Kirk A. 2006. Augmentation biological control of Arundo donax. In: Hoddle MS, Johnson M, editors. Proceedings of the California Conference on Biological Control. Riverside, CA, USA; p. 141–145.

Dudley TL, Lambert AM, Kirk A, Tamagawa Y. 2008. Herbivores associated with Arundo donax in California. In: Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, Hinz HL, Rector BG, editors. Proceedings of the XII International Symposium on Biological Control of Weeds, 22-27 April 2007. La Grande Motte, France: CAB International; p. 138–145.

DWAF. 1996. South African Water Quality Guidelines: Aquatic Ecosystems. 2nd Edition. Pretoria: Department of Water Affairs and Forestry Scientific Research Publishing.

Fleming JP, Dibble ED. 2015. Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia. 746:23–37. https://doi.org/10.1007/s10750-014-2026-y

Fritz RS, Moulia C, Newcombe G. 1999. Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annual Review of Ecology and Systematics. 30:565–591. http://www.jstor.org/stable/221696

Fritz RS, Nichols-Orians C, Brunsfeld SJ. 1994. Interspecific hybridization of plants and resistance to herbivores: hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia. 97:106–117. https://doi.org/10.1007/BF00317914

González-Oreja JA, Garbisu C, Mendarte S, Ibarra A, Albizu I. 2010. Assessing the performance of nonparametric estimators of species richness in meadows. Biodiversity and Conservation. 19:1417–1436. https://doi.org/10.1007/s10531-009-9770-8

Gooden B, French K, Turner PJ, Downey PO. 2009. Impact threshold for an alien plant invader, Lantana camara L., on native plant communities. Biological Conservation. 142:2631–2641.

Hartig F. 2021. DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.4. https://CRAN.R-project.org/package=DHARMa

Herrick NJ, Kok LT. 2010. Classical biological control of weeds with Curculionidae. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 5:1–11. https://doi.org/10.1079/PAVSNNR20105028

Hierro JL, Maron JL, Callaway RM. 2005. A biogeographical approach to plant invasions: The importance of studying exotics in their introduced and native range. Journal of Ecology. 93:5–15. https://doi.org/10.1111/j.0022-0477.2004.00953.x

Hill MP, Coetzee J. 2017. The biological control of aquatic weeds in South Africa: Current status and future challenges. Bothalia. 47:1–12. https://doi.org/10.4102/abc.v47i2.2152

Hoffman JH. 2004. Biotypes, hybrids and biological control: lessons from cochineal insects on Opuntia weeds. XI International Symposium on Biological Control of Weeds. p. 283.

Jacob H, Briese DT. 2003. Improving the selection, testing and evaluation of weed biological control agents. In: Jacon HS, Briese DT, editors. Proceedings of the CRC for Australian Weed Management Biological Control of Weeds Symposium and Workshop. p. 87-98.

Jahner JP, Bonilla MM, Badik KJ, Shapiro AM, Forister ML. 2011. Use of exotic hosts by Lepidoptera: Widespread species colonize more novel hosts. Evolution. 65:2719–2724. https://doi.org/10.1111/j.1558-5646.2011.01310.x

Jakobs G, Weber E, Edwards PJ. 2004. Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Diversity and Distributions. 10:11–19. https://doi.org/10.1111/j.1472-4642.2004.00052.x

Joshi J, Vrieling K. 2005. The enemy release and EICA hypothesis revisited: Incorporating the fundamental difference between specialist and generalist herbivores. Ecology Letters. 8:704–714. https://doi.org//10.1111/j.1461-0248.2005.00769.x

Keane RM, Crawley MJ. 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution. 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0

Kent M. 2012. Vegetation Description and Analysis: A Practical Approach. 2nd Edition. University of Plymouth: John Wiley & Sons.

Martínez-Sanz C, Garciá-Criado F, Alaéz CF, Alaéz, MF. 2010. Assessment of richness estimation methods on macroinvertebrate communities of mountain ponds in Castilla y León (Spain). International Journal of Limnology. 46:101–110. https://doi.org/10.1051/limn/2010008

McFadyen REC. 2000. Successes in biological control of weeds. In: Spencer NR, editor. Proceedings of the X International Symposium on Biological Control of Weeds. Montana State University, Bozeman, Montana, USA. p. 3–14.

Memmott J, Fowler SV, Paynter Q, Sheppard AW, Syrett P. 2000. The invertebrate fauna on broom, Cytisus scoparius, in two native and two exotic habitats. Acta Oecologica. 21:213–222. https://doi.org/10.1016/S1146-609X(00)00124-7

Müller-Schärer H, Schaffner U. 2008. Classical biological control: Exploiting enemy escape to manage plant invasions. Biological Invasions. 10:859–874. https://doi.org/10.1007/s10530-008-9238-x

Newman RM, Biesboer DD. 2000. A decline of Eurasian Watermilfoil in Minnesota associated with the Milfoil Weevil, Euhrychiopsis lecontei. Journal of Aquatic Plant Management. 38:105–111.

Okamoto U, Shirahama S, Nasu S, Miyauchi H, Tokuda M. 2020. Host range expansion of a Polygonaceae-associated leaf beetle to an invasive aquatic plant Myriophyllum aquaticum (Haloragaceae). Arthropod-Plant Interactions. 14:491–497. https://doi.org/10.1007/s11829-020-09764-7

Ondrus MG. 1996. Laboratory Experiments in Environmental Chemistry. 2nd Edition. Winniperg, Canada: Wuerz Publishing Ltd.

Panetta FD, Gooden B. 2017. Managing for biodiversity: Impact and action thresholds for invasive plants in natural ecosystems. NeoBiota. 34:53–66. http://dx.doi.org/10.3897/neobiota.34.11821

Paynter Q, Downey PO, Sheppard AW. 2003. Age structure and growth of the woody legume weed Cytisus scoparius in native and exotic habitats: Implications for control. Journal of Applied Ecology. 40:470–480. https://doi.org/10.1046/j.1365-2664.2003.00817.x

Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L. 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist. 193:30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x

Prior KM, Adams DC, Klepzig KD, Hulcr J. 2018. When does invasive species removal lead to ecological recovery? Implications for management success. Biological Invasions. 20:267–283. https://doi.org/10.1007/s10530-017-1542-x

R Core Team. 2021. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Reid MK, Coetzee JA, Hill MP, Diaz R, Gettys LA, Cuda JP, Reid CS. 2020. Insect herbivores associated with Nymphaea mexicana (Nymphaeaceae) in southern United States: potential biological control agents for South Africa. Florida Entomologist. 103:54–63. https://doi.org/10.1653/024.103.0409

Reid MK, Naidu P, Paterson ID, Mangan R, Coetzee JA. 2021. Population genetics of invasive and native Nymphaea mexicana Zuccarini: Taking the first steps to initiate a biological control programme in South Africa. Aquatic Botany. 171:103372. https://doi.org/10.1016/j.aquabot.2021.103372

Roley SS, Newman RM. 2006. Developmental performance of the Milfoil Weevil, Euhrychiopsis lecontei (Coleoptera: Curculionidae), on Northern Watermilfoil, Eurasian Watermilfoil, and Hybrid (Northern X Eurasian) Watermilfoil. Environmental Entomology. 35:121–126. https://doi.org/10.1603/0046-225X-35.1.121

Sheppard AW, Heard TA, Briese DT. 2003. What is needed to improve the selection, testing and evaluation of weed biological control agents: workshop synthesis and recommendations. In: Jacob HS, Briese D, editors. Improving the Selection, Testing and Evaluation of Weed Biological Control Agents. p. 87–98.

Smith RA. 2010. Use of an aquatic weevil, Euhrychiopsis lecontei, as a biological control agent against Eurasian watermilfoil (Myriophyllum spicatum) in Michigan’s Les Cheneaux Islands. Les Cheneaux Watershed Council. http://lescheneauxwatershed.org/images/invasive-species/wvlproj_final_jan_2010.pdf

Sunny A, Diwakar S, Sharma GP. 2015. Native insects and invasive plants encounters. Arthropod-Plant Interactions. 9:323–331. https://doi.org/10.1007/s11829-015-9384-x

Thorstenson AL. 2011. Biological control of Eurasian watermilfoil (Myriophyllum spicatum) using the native milfoil weevil (Euhrychiopsis lecontei). MSc. Thesis. University of Wisconsin, Stevens Point, Wisconsin.

Urban AJ, Simelane DO, Retief E, Heystek F, Williams HE, Madire LG. 2011. The invasive ‘Lantana camara L.’ hybrid complex (Verbenaceae): a review of research into its identity and biological control in South Africa. African Entomology. 19:315–348. https://doi.org/10.1007/s11829-015-9384-x

Van Klinken RD, Fichera G, Cordo H. 2003. Targeting biological control across diverse landscapes: The release, establishment, and early success of two insects on mesquite (Prosopis spp.) insects in Australian rangelands. Biological Control. 26:8–20. https://doi.org/10.1016/S1049-9644(02)00107-X

Van Klinken RD, Raghu S. 2006. A scientific approach to agent selection. Australian Journal of Entomology. 45:253–258. https://doi.org/10.1111/j.1440-6055.2006.00547.x

Van Wilgen BW, Raghu S, Sheppard AW, Schaffner U. 2020. Quantifying the social and economic benefits of the biological control of invasive alien plants in natural ecosystems. Current Opinion in Insect Science. 38:1–5. https://doi.org/10.1016/j.cois.2019.12.004

Vasquez EC, Meyer GA. 2011. Relationships among leaf damage, natural enemy release, and abundance in exotic and native prairie plants. Biological Invasions. 13:621–633. https://doi.org/10.1007/s10530-010-9853-1

Whitham TG, Morrow PA, Potts BM. 1994. Plant hybrid zones as centers of biodiversity: the herbivore community of two endemic Tasmanian eucalypts. Oecologia. 97:481–490. https://doi.org/10.1007/BF00325886

Wickham H. 2016. Ggplot2: Elegant Graphics For Data Analysis. ISBN: 978-3-319-24277-4. New York: Springer-Verlag. https://ggplot2.tidyverse.org

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. Evolutionary Applications. 7:381–393. https://doi.org/10.1111/eva.12134

Wood SN. 2010. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society. 73:3–36. https://doi.org/10.1111/j.1467-9868.2010.00749.x

Downloads

Additional Files

Published

2023-05-18

How to Cite

1.
Reid M, Hill M, Coetzee J. Love at first bite? Pre-release surveys reveal a novel association between a native weevil and the invasive Nymphaea mexicana Zuccarini (Nymphaeaceae) in South Africa. Afr. Entomol. [Internet]. 2023 May 18 [cited 2024 May 27];31. Available from: https://www.africanentomology.com/article/view/14949

Issue

Section

Articles

Most read articles by the same author(s)