Arthropod associates of Kenyan buffelgrass (Cenchrus ciliaris): a field survey for biological control candidates of a globally important invasive grass
DOI:
https://doi.org/10.17159/2254-8854/2023/a16178Keywords:
biological control, grass, herbivore, introduced, gall midge, specialist, insect, invasive alien grassAbstract
Invasive species are the second largest contributor to biodiversity loss and drivers of ecosystem change. Buffelgrass is a C4, perennial grass native to Africa and Asia that was widely introduced across tropical and subtropical rangelands as livestock forage. Buffelgrass reduces native biodiversity and ecosystem stability in its introduced range when it escapes livestock pastures. Understanding the ecology of insects associated with buffelgrass in its native range may provide an understanding of invasion processes and biological control opportunities where buffelgrass has become an invasive challenge. Here, we present the results of a six-year survey of herbivorous arthropods of a native buffelgrass population from Kenya. Buffelgrass was examined for externally and internally feeding insects of vegetative and reproductive tissues. We also categorised buffelgrass detritivores and parasitoids that may use buffelgrass herbivores as hosts. The samples were photographed and Sanger sequenced to identify them to the lowest possible taxonomic ranking. We collected information on sample abundances, phenologies, tissues consumed, and putative diet breadths. We identified 25 morphospecies representing seven orders and 16 families. The putative host plant specialisation was as high as 67% for Diptera. Phenological variation in herbivore presence correlated with seasonal rainfall and provided a guide for when to conduct follow-up biological control agent searches. The most abundant herbivore was a gall midge (Diptera: Cecidomyiidae) that inhabits buffelgrass culms. Additional research should focus on bringing this species into containment where host choice trials can be conducted to determine if it is truly monophagous and assess its impact on buffelgrass growth.
Downloads
Metrics
References
Ahn PM, Geiger LC. 1987. Soils of Laikipia District. Nairobi: Ministry of Agriculture, National Agricultural Laboratories.
Alcala GC. 2005. Response of desert mule deer to habitat alterations in the lower Sonoran Desert. PhD Dissertation. University of Arizona, AZ, USA.
Barnes HF. 1956. Gall Midges of Economic Importance. Volume VII. Gall Midges of Cereal Crops. London: Crosby Lockwood & Son Ltd.
Bonzi SM. 1980. Wild host plants of rice gall midge Orseolia oryzae WM (Dipt. Cecidomyidae) in Upper Volta. WARDA Technical Newsletter. 2:5–6.
Brooks ML, D'antonio CM, Richardson DM, Grace JB, Keeley JE, DiTomaso JM, Hobbs RJ, Pellant M, Pyke D. 2004. Effects of invasive alien plants on fire regimes. BioScience. 54(7):677–688. https://doi.org/10.1641/0006-3568(2004)054[0677:EOIAPO]2.0.CO;2
Burquez-Montijo A, Miller ME, Martınez-Yrizar A. 2002. Mexican grasslands, thornscrub, and the transformation of the Sonoran Desert by invasive non-native buffelgrass (Pennisetum ciliare). In: Tellman B, editor. Invasive non-native species in the Sonoran region. Tucson.: University of Arizona Press and Arizona-Sonora Desert Museum p. 126–146.
Clarke PJ, Latz PK, Albrecht DE. 2005. Long‐term changes in semi‐arid vegetation: Invasion of an exotic perennial grass has larger effects than rainfall variability. Journal of Vegetation Science. 16:237–248. https://doi.org/ 10.1111/j.1654-1103.2005.tb02361.x
Carroll C, Merton L, Burger P. 2000. Impact of vegetative cover and slope on runoff, erosion, and water quality for field plots on a range of soil and spoil materials on central Queensland coal mines. Soil Research. 38:313–328. https://doi.org/10.1071/SR99052
Castellanos AE, Celaya‐Michel H, Rodríguez JC, Wilcox BP. 2016. Ecohydrological changes in semiarid ecosystems transformed from shrubland to buffelgrass savanna. Ecohydrology. 9:1663–1674. https://doi.org/10.1002/eco.1756
Caylor KK, Gitonga JG, Martins DJ. 2022. Mpala Research Centre Meteorological and Hydrological Dataset [Data File]. Mpala Research Centre, Laikipia, Kenya.
Cerling TE, Andanje SA, Blumenthal SA, Brown FH, Chritz KL, Harris JM, et al. 2015. Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma. Proceedings of the National Academy of Sciences. 112:11467–11472. https://doi.org/10.1073/pnas.1513075112
Cox JR, Martin-R MH, Ibarra F, Fourie JH, Rethman NFG, Wilcox DG. 1988. The influence of climate and soils on the distribution of four African grasses. Journal of Range Management. (41)2:127–139. https://doi.org/10.2307/3898948
Crego RD, Ogutu JO, Wells HB, Ojwang GO, Martins DJ, Leimgruber P, Stabach JA. 2020. Spatiotemporal dynamics of wild herbivore species richness and occupancy across a savannah rangeland: Implications for conservation. Biological Conservation. 242:108436. https://doi.org/10.1016/j.biocon.2020.108436
Crego RD, Wells HB, Ndung’u KS, Evans L, Njeri Nduguta R, Chege MA, et al. 2021. Moving through the mosaic: identifying critical linkage zones for large herbivores across a multiple‐use African landscape. Landscape Ecology. 36:1325-1340. https://doi.org/10.1007/s10980-021-01232-8
D’Antonio CMD, Vitousek PM. 1992. Biological invasions by exotic grasses, the grass/fire cycle, and global change Annual Review of Ecology and Systematics. 23:63–87. https://doi.org/10.1146/annurev.es.23.110192.000431
Denlinger DL. 1980. Seasonal and annual variation of insect abundance in the Nairobi National Park, Kenya. Biotropica:100–106. https://doi.org/10.2307/2387725
Harris KM, Dorchin N. 2012. The taxonomic status of Jean-Jacques Kieffer's type specimens of Afrotropical Cecidomyiidae (Diptera). African Invertebrates. (53)1:169–174. https://hdl.handle.net/10520/EJC121921
Dorchin N, Harris KM, Stireman III JO. 2019. Phylogeny of the gall midges (Diptera, Cecidomyiidae, Cecidomyiinae): Systematics, evolution of feeding modes and diversification rates. Molecular Phylogenetics and Evolution. 140:106602. https://doi.org/10.1016/j.ympev.2019.106602
Escobar Y, Guermache F, Bon MC, Kerdellant E, Petoux L, Desurmont GA. 2020. Biology, ecology, and impact of Cryptonevra nigritarsis Duda, a potential biological control agent against the giant reed Arundo donax. Biological Control. 147:104287. https://doi.org/10.1016/j.biocontrol.2020.104287
Farrell HL, Gornish ES. 2019. Pennisetum ciliare: a review of treatment efficacy, competitive traits, and restoration opportunities. Invasive Plant Science and Management. 12(4):203–213. https://doi.org/10.1017/inp.2019.28
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology. 3:294–299.
Franklin KA, Lyons K, Nagler PL, Lampkin D, Glenn EP, Molina-Freaner F, et al. 2006. Buffelgrass (Pennisetum ciliare) land conversion and productivity in the plains of Sonora, Mexico. Biological Conservation. 127:62–71. https://doi.org/10.1016/j.biocon.2005.07.018
Fulbright N, Fulbright TE. 1990. Germination of 2 legumes in leachate from introduced grasses. Rangeland Ecology and Management/Journal of Range Management Archives. 43:466–467. https://doi.org.10.2307/3899014
Gagné RJ, Jaschhof M. 2021. A catalog of the Cecidomyiidae (Diptera) of the world. 5th Edition. Washington, DC: United States Department of Agriculture & Entomological Society of Washington.
Goolsby JA, 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. https://doi.org/10.1016/j.biocontrol.2009.01.019
Goolsby JA, Moran PJ, Adamczyk JJ, Kirk AA, Jones WA, Marcos MA, Cortés E. 2009. Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (Poales: Poaceae) in North America. Biocontrol Science and Technology. 19:899–918. https://doi.org/10.1080/09583150903189099
Goolsby JA, Vacek AT, Salinas C, Racelis A, Moran PJ, Kirk AA. 2017. Host range of the European leaf sheath mining midge, Lasioptera donacis Coutin (Diptera: Cecidomyiidae), a biological control of giant reed, Arundo donax L. Biocontrol Science and Technology. 27:781–795. https://doi.org/10.1080/09583157.2017.1342222
Halvorson WAGP. 2003. Factsheet for: Penisetum ciliare (L.). In: Halvorson WAGP, editor. USGS Weeds in the West project: Status of Introduced Plants in Southern Arizona Parks. Tucson: U.S. Geological Survey, National Parks Service.
Hamilton WT, McGinty A, Ueckert DN, Hanselka CW, Lee MR. 2004. Brush management: past, present, future, Volume 7. College Station: Texas A and M University Press.
Hanselka CW. 1988. Buffelgrass — South Texas wonder grass. Rangelands. 10:279–281.
Harris KM, Williams CT, Okhidievbie O, Lasalle JE, Polaszek A. 1999. Description of a new species of Orseolia (Diptera: Cecidomyiidae) from Paspalum in West Africa, with notes on its parasitoids, ecology and relevance to natural biological control of the African rice gall midge, O. oryzivora. Bulletin of Entomological Research. 89:441–448. https://doi.org/10.1017/S0007485399000577
Harwood MR, Hacker JB, Mott JJ. 1999. Field evaluation of seven grasses for use in the revegetation of lands disturbed by coal mining in Central Queensland. Australian Journal of Experimental Agriculture. 39:307–316. https://doi.org/10.1071/EA98119
Havstad KM, Peters DP, Skaggs R, Brown J, Bestelmeyer B, Fredrickson E, Herrick J, Wright J. 2007. Ecological services to and from rangelands of the United States. Ecological Economics. 64:261–268. https://doi.org/10.1016/j.ecolecon.2007.08.005
Hawkins BA, Gagné RJ. 1989. Determinants of assemblage size for the parasitoids of Cecidomyiidae (Diptera). Oecologia. 81(1):75–88. https://doi.org/10.1007/ BF00377013
Hernández F, Guthery FS. 2012. Beef, brush, and bobwhites: quail management in cattle country. College Station: Texas A and M University Press.
Hinz HL, Müller-Schärer H. 2000. Influence of host condition on the performance of Rhopalomyia n. sp.(Diptera: Cecidomyiidae), a biological control agent for scentless chamomile, Tripleurospermum perforatum. Biological Control. 18:147–156. https://doi.org/10.1006/bcon.2000.0818
Impson FAC, Kleinjan CA, Hoffmann JH, Post JA. 2008. Dasineura rubiformis (Diptera: Cecidomyiidae), a new biological control agent for Acacia mearnsii in South Africa. South African Journal of Science. 104:247–249.
Johnson PJ, Torrez VC, Buhl PN. 2013. A new species of Platygaster Latreille (Hymenoptera: Platygastridae) parasitizing Chilophaga virgati Gagné (Diptera: Cecidomyiidae). Zootaxa. 3630:184–190. https://doi.org/10.11646/zootaxa.3630.1.8
Kasenene JM, Roininen H. 1999. Seasonality of insect herbivory on the leaves of Neoboutonia macrocalyx in the Kibale National Park, Uganda. African Journal of Ecology. 37:61–68. https://doi.org/10.1046/j.1365-2028.1999.00162.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
Kfir R, Overholt WA, Khan ZR, Polaszek A. 2002. Biology and management of economically important lepidopteran cereal stem borers in Africa. Annual review of entomology. 47:701–31. https://doi.org/10.1146/annurev.ento.47.091201.145254
Kolesik P, Sarfati MS, Brockerhoff EG, Kelly D. 2007. Description of Eucalyptodiplosis chionochloae sp. nov., a cecidomyiid feeding on inflorescences of Chionochloa (Poaceae) in New Zealand. New Zealand Journal of Zoology. 34:107–115. https://doi.org/10.1080/03014220709510069
Litt AR, Cord EE, Fulbright TE, Schuster GL. 2014. Effects of invasive plants on arthropods. Conservation Biology. 28:1532–1549. https://doi.org/10.1111/cobi.12350
LÓpez JMP, Johnson PJ, Gagné RJ, Boe A. 2015. A new species of Stenodiplosis (Diptera: Cecidomyiidae) on Spartina grasses (Poaceae) with notes on its biology and its parasitoid Tetrastichus bromi (Hymenoptera: Eulophidae). Zootaxa. 4057:115–124. https://doi.org/10.11646/zootaxa.4057.1.7
Lund HG. 2007. Accounting for the world's rangelands. Rangelands. 29:3–10. https://doi.org/10.2111/1551-501X(2007)29[3:AFTWR]2.0.CO;2
Marshall VM, Lewis MM, Ostendorf B. 2012. Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: a review. Journal of Arid Environments. 78:1–12. https://doi.org/10.1016/j.jaridenv.2011.11.005
Martins DJ. 2022. Grasses of East Africa. Cape Town: Struik Nature, Penguin Random House South Africa (Pty) Ltd.
McDonald CJ, McPherson GR. 2013. Creating hotter fires in the Sonoran Desert: Buffelgrass produces copious fuels and high fire temperatures. Fire Ecology. 9:26–39. https://doi.org/10.4996/fireecology.0902026
Moran PJ, Vacek AT, Racelis AE, Pratt PD, Goolsby JA. 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. https://doi.org/10.1080/09583157.2016.1258453
Morgan AR, Smith-Herron AJ, Cook JL. 2013. Rapid spread of Balclutha rubrostriata (Hemiptera: Cicadellidae) in Texas and southwestern Louisiana, USA with notes on its associated host plants. Florida Entomologist. 96:477–81. https://doi.org/10.1653/024.096.0213
Morrison CR, Rhodes AC, Bowman EA, Plowes RM, Sedio BE, Gilbert LE. 2023. Adding insult to injury: Light competition and allelochemical weapons interact to facilitate grass invasion. Ecosphere 14:e4438. https://doi.org/10.1002/ecs2.4438
Mound LA, Ng YF. 2009. An illustrated key to the genera of Thripinae (Thysanoptera) from Southeast Asia. Zootaxa. 2265:27–47. https://doi.org/10.11646/zootaxa.2265.1.2
Neiman EL, Manglitz GR. 1972. The Biology and Ecology of the Bromegrass Seed Midge in Nebraska. Nebraska Agricultural Experiment Station Research Bulletin. 252:1–23.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. 2020. Community ecology package. R package version 2.5.7. https://CRAN.R-project.org/package=vegan
Olff H, Ritchie ME, Prins HH. 2002. Global environmental controls of diversity in large herbivores. Nature. 415:901–904. https://doi.org/10.1038/415901a
Palmer CM. 2009. Buffel grass ('Cenchrus ciliaris' L.) is a host for the 'sugarcane whitefly' Neomaskellia bergii (Signoret) (Hemiptera: Aleyrodidae) in central Australia. The Australian Entomologist. 36:89–95.
Palmer CM, Mound LA. 2020. The diversity of thrips (Insecta: Thysanoptera) on buffel grass (Cenchrus ciliaris) is markedly lower than on native grasses in an urban landscape. Journal of Urban Ecology. 6:juaa024. https://doi.org.10.1093/jue/juaa024
Paynter Q, Fowler SV, Hugh Gourlay A, Groenteman R, Peterson PG, Smith L, Winks CJ. 2010. Predicting parasitoid accumulation on biological control agents of weeds. Journal of Applied Ecology. 47:575–582. https://doi.org/10.1111/j.1365-2664.2010.01810.x
Paterson ID, Vitorino MD, De Cristo SC, Martin GD, Hill MP. 2014. Prioritisation of potential agents for the biological control of the invasive alien weed, Pereskia aculeata (Cactaceae), in South Africa. Biocontrol Science and Technology. 24:407–425. https://doi.org/10.1080/09583157.2013.864382
Pinheiro F, Diniz IR, Coelho D, Bandeira MPS. 2002. Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology. 27:132–136. https://doi.org/10.1046/j.1442-9993.2002.01165.x
Price PW, Hunter MD. 2015. Population dynamics of an insect herbivore over 32 years are driven by precipitation and host-plant effects: testing model predictions. Environmental Entomology. 44:463–473. https://doi.org/10.1093/ee/nvv039
R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ratnasingham S, Hebert PD. 2007. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular ecology notes. 7(3):355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
Rector BG, Gagné RJ, Perilla López JM, Tonkel KC, Bon MC, Guermache F, Cristofaro M. 2021. Taxonomic description of Stenodiplosis tectori n. sp. (Diptera: Cecidomyiidae), a seed parasite of cheatgrass, Anisantha tectorum, based on morphological and mitochondrial DNA data. Insects. 12:755. https://doi.org/ 10.3390/insects12080755
Rhodes AC, Rutledge J, DuPont B, Plowes RM, Gilbert LE. 2021. Targeted grazing of an invasive grass improves outcomes for native plant communities and wildlife habitat. Rangeland Ecology and Management. 75:41–50. https://doi.org/ 10.1016/j.rama.2020.11.007
Rhodes AC, Plowes RM, Gilbert LE. 2023. Mitigating buffelgrass invasion through simulated targeted grazing: understanding restoration potential in a variable precipitation regime. Restoration Ecology. 31(6). https://doi.org/
1111/rec.13923
Sands D, Goolsby JA. 2011. The case for biological control of exotic African grasses in Australia and USA using introduced detritivores. In: Wu Y, Johnson T, Sing S, Raghu S, Wheeler G, Pratt P, et al. (eds). Proceedings of the XIII International Symposium on Biological Control of Weeds. Waikoloa, Hawaii, USA, 11–16 September 2011. p. 103–109.
Schwarzländer M, Hinz HL, Winston RL, Day MD. 2018. Biological control of weeds: an analysis of introductions, rates of establishment and estimates of success, worldwide. BioControl. 63:319–331. https://doi.org/10.1007/s10526-018-9890-8
Sinclair AR. 1975. The resource limitation of trophic levels in tropical grassland ecosystems. The Journal of Animal Ecology. 497–520. https://doi.org/ 10.2307/3608
Smyth A, Friedel M, O’Malley C. 2009. The influence of buffel grass (Cenchrus ciliaris) on biodiversity in an arid Australian landscape. The Rangeland Journal. 31:307–320. https://doi.org/10.1071/RJ08026
Sommers P, Davis A, Chesson P. 2022. Invasive buffel grass (Cenchrus ciliaris) increases water stress and reduces success of native perennial seedlings in southeastern Arizona. Biological Invasions. 24:1809–1826. https://doi.org/ 10.1007/s10530-022-02750-5
Stevens JM, Fehmi JS. 2011. Early establishment of a native grass reduces the competitive effect of a non‐native grass. Restoration Ecology. 19:399–406. https://doi.org/10.1111/j.1526-100X.2009.00565.x
Sutton GF, Canavan K, Day MD, Den Breeyen A, Goolsby JA, Cristofaro M, McConnachie A, Paterson IF. 2019. Grasses as suitable targets for classical weed biological control. BioControl. 64:605–622. https://doi.org/10.1007/s10526-019-09968-8
Sutton GF. 2020. Guy Sutton: Plotting species accumulation curves using ggplot. Retrieved from https://guysutton.netlify.app/posts/2020-10-29-automated-plotting-of-species-accumulation-curves-by-group/
Titcomb G, Allan BF, Ainsworth T, Henson L, Hedlund T, Pringle RM, et al. 2017. Interacting effects of wildlife loss and climate on ticks and tick-borne disease. Proceedings of the Royal Society B: Biological Sciences. 284:20170475. https://doi.org/10.1098/rspb.2017.0475
United States Department of Agriculture. 2010. Pennisetum ciliare (L.) Link Buffelgrass. Plants Profile. United States Department of Agriculture, Natural Resources Conservation Service.
Walker B, Weston EJ. 1990. Pasture development in Queensland–a success story. Tropical Grasslands. 24:257–268.
Whittaker RH, Gilbert LE, Connell JH. 1979. Analysis of two-phase pattern in a mesquite grassland, Texas. The Journal of Ecology. 67:935-952. https://doi.org/ 10.2307/2259222
Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.
Zeale MR, Butlin RK, Barker GL, Lees DC, Jones G. 2011. Taxon‐specific PCR for DNA barcoding arthropod prey in bat faeces. Molecular Ecology Resources. 11:236–244. https://doi.org/10.1111/j.1755-0998.2010.02920.x
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Colin Morrison, Robert Plowes, Ivy Ng’iru, Aaron Rhodes , Dino Martins , Lawrence Gilbert
This work is licensed under a Creative Commons Attribution 4.0 International License.
.png){kind=spacer}