Density effect and intraspecific competition in a leaf-mining moth on bamboo leaves

Abstract

When confined to a single leaf, the larvae of most leafminers should suffer intense intraspecific competition. The survival and performance of individuals are expected to decline with increasing larval density within a leaf, showing a negative density-dependent effect. The maximum density of an Elachista Treitschke (Lepidoptera: Elachistidae) miner on Indocalamus tessellatus (Munro) Keng f. (Poaceae: Bambusoideae) under natural conditions can be greater than 40 per leaf, making this a good system for studying intraspecific competition and density effects. We counted the number of leaves with different mine densities in the field and found a clumped distribution of leafminer larvae among host leaves. The emergence rates of pupae (and last-instar larvae), adults and parasitoids were inversely correlated with larval density. Pupal weight and adult weight also showed negative relationships with larval density. However, pairwise tests showed that there might be no differences in pupal or adult weight at larval densities of 1–10 mines per leaf, indicating that density-dependent effects are more obvious at densities greater than 10 mines per leaf. Intraspecific competition could lead to stable density and consistent body size in surviving individual insects, which would help maintain a sustainable population size. The density threshold could be an indicator of the balance between intraspecific competitive detriments and conspecific aggregation benefits; however, the validity of the threshold density hypothesis requires further testing and confirmation.

Keywords

Leafminer / Density-dependent / Distribution pattern / Sustainable population / Threshold density

References

[1] Aparicio ML, Fenoglio MS, Videla M. Leafminer egg distribution at decreasing leaf availability levels: do females avoid intraspecific competition?. Entomol Exp Appl, 2015, 156: 170-177.

[2] Auerbach M, Simberloff D. Oviposition site preference and larval mortality in a leaf-mining moth. Ecol Entomol, 1989, 14: 131-140.

[3] Auerbach MJ, Conner EF, Mopper S, Connor EF, Mopper S. Cappuccino N, Price PW. Minor miners and major miners: population dynamics of leaf-mining insects. Population dynamics: new approaches and synthesis, 1995, San Diego: Academic Press Inc 83 110

[4] Awmack CS, Leather SR. Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol, 2002, 47: 817-844.

[5] Ayabe Y, Shibata E. Spatial distributions of the leafminer Ophiomyia maura (Diptera: Agromyzidae) in host plant Aster ageratoides. Insect Sci, 2008, 15: 343-348.

[6] Bai H, Xu J, Dai X. Three new species, two newly recorded species and one newly recorded genus of Lithocolletinae (Lepidoptera: Gracillariidae) from China. Zootaxa, 2015, 4032: 229-235.

[7] Bai H, Xu J, Dai X. Two new and one newly recorded species of Gracillariidae from China (Lepidoptera). Zookeys, 2016, 559: 139-150.

[8] Bawin T, De Backer L, Dujeu D, Legrand P, Megido R, Francis F, Verheggen F. Infestation level influences oviposition site selection in the tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae). Insects, 2014, 5: 877-884.

[9] Bultman TL, Faeth SH. Patterns of intra- and interspecific association in leaf-mining insects on three oak host species. Ecol Entomol, 1985, 10: 121-129.

[10] Bultman TL, Faeth SH. Experimental evidence for intraspecific competition in a leapidopteran leaf miner. Ecology, 1986, 67: 442-448.

[11] Bultman TL, Faeth SH. Effect of within-leaf density and leaf size on pupal weight of a leaf-miner, Cameraria (Lepidoptera: Gracillariidae). Southwest Nat, 1986, 31: 201-206.

[12] Bultman TL, Faeth SH. Leaf size selection by leaf-mining insects on Quercus emoryi (Fagaceae). Oikos, 1986, 46: 311-316.

[13] Chen Y, Zhao J. Density-dependent effect of the experimental population of vegetable leafminer Liriomyza sativae (Diptera: Agromyzidae). J Fujian Agric Univ, 1998, 27: 78-81.

[14] Connor EF, Beck MW. Density-related mortality in Cameraria hamadryadella (Lepidoptera: Gracillariidae) at epidemic and endemic densities. Oikos, 1993, 66: 515-525.

[15] Connor EF, Cargain MJ. Density-related foraging behavior in Closterocerus tricinctus, a parasitoid of the leaf-mining moth, Cameraria hamadryadella. Ecol Entomol, 1994, 19: 327-334.

[16] Cornelissen T, Stiling P. Clumped distribution of oak leaf miners between and within plants. Basic Appl Ecol, 2008, 9: 67-77.

[17] D’Costa L, Koricheva J, Straw N, Simmonds MSJJ. Oviposition patterns and larval damage by the invasive horse-chestnut leaf miner Cameraria ohridella on different species of Aesculus. Ecol Entomol, 2013, 38: 456-462.

[18] Dai X, Xu J, Ding X. Circular distribution pattern of plant modulars and endophagous herbivory within tree crowns: the impact of roadside light conditions. J Insect Sci, 2013, 13: 141.

[19] Dai X, Xu J, Cai L. Effects of roads on Castanopsis carlesii seedlings and their leaf herbivory in a subtropical forest in China. J Insect Sci, 2014, 14: 17.

[20] Digweed SC. Oviposition preference and larval performance in the exotic birch-leafmining sawfly Profenusa thomsoni. Entomol Exp Appl, 2006, 120: 41-49.

[21] Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci, 2003, 14: 927-930.

[22] Doak P, Wagner D. The role of interference competition in a sustained population outbreak of the aspen leaf miner in Alaska. Basic Appl Ecol, 2015, 16: 434-442.

[23] Dohse LA, McNeil JN. An intraspecific competition model for the leafminer Agromyza frontella Rondani. Can Entomol, 1988, 120: 779-786.

[24] Eber S. Bottom-up density regulation in the holly leaf-miner Phytomyza ilicis. J Anim Ecol, 2004, 73: 948-958.

[25] Ermolaev I, Izhboldina N. The effect of population density of the lime leafminer Phyllonorycter issikii Kumata (Lepidoptera, Gracillariidae) on the ratio of intrapopulation forms. Entomol Rev, 2013, 93: 95-104.

[26] Faeth SH. Aggregation of a leafminer, Cameraria sp. nov. (Davis): consequences and causes. J Anim Ecol, 1990, 59: 569-586.

[27] Faeth SH (1991) Novel aspects of host tree resistance to leafminers. In: Baranchikov YN, Mattson WJ, Hain FP, Payne TL (eds) Forest insects guilds: patterns of interaction with host trees. USDA Forest Service, General Technical Report NE-153, pp 219–239

[28] Faeth SH, Simberloff D. Population regulation of a leaf-mining insect, Cameraria sp. nov., at increased field densities. Ecology, 1981, 62: 620-624.

[29] Faria CA, Torres JB, Fernandes AMV, Farias AMI. Parasitism of Tuta absoluta in tomato plants by Trichogramma pretiosum Riley in response to host density and plant structures. Ciênc Rural, 2008, 38: 1504-1509.

[30] Fisher N, Ubaidillah R, Reina P, Salle J La (2005) Liriomyza parasitoids in Southeast Asia. http://www.ento.csiro.au/science/Liriomyza_ver3/key/Liriomyza_Parasitoids_Key/Media/Html/home.html. Accessed 21 Mar 2017

[31] Freeman BE, Smith DC. Variation of density-dependence with spatial scale in the leaf-mining fly Liriomyza commelinae (Diptera: Agromyzidae). Ecol Entomol, 1990, 15: 265-274.

[32] Gripenberg S, Roslin T. Host plants as islands: resource quality and spatial setting as determinants of insect distribution. Ann Zool Fenn, 2005, 42: 335-345.

[33] Gripenberg S, Roslin T. Neither the devil nor the deep blue sea: larval mortality factors fail to explain the abundance and distribution of Tischeria ekebladella. Ecol Entomol, 2008, 33: 346-356.

[34] Gripenberg S, Morriën E, Cudmore A, Salminen JP, Roslin T. Resource selection by female moths in a heterogeneous environment: what is a poor girl to do?. J Anim Ecol, 2007, 76: 854-865.

[35] Hammer Ø, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron, 2001, 4: 1-9.

[36] Hao Y, Wang K, Zhang L, Lei Z, Luo H, Lian Z, Zhou G. Density-dependent effect of Liriomyza trifolii at immature stage and interspecific competition with Liriomyza sativae. Sci Agric Sin, 2014, 47: 4269-4279.

[37] Hespenheide HA. Bionomics of leaf-mining insects. Annu Rev Entomol, 1991, 36: 535-560.

[38] Hovemeyer K. Population studies of Cheilosia fasciata (Diptera: Syrphidae), a leaf miner of Allium ursinum. Ecol Entomol, 1992, 17: 331-337.

[39] Ishino MN, De Sibio PR, Rossi MN. Leaf trait variation on Erythroxylum tortuosum (Erythroxylaceae) and its relationship with oviposition preference and stress by a host-specific leaf miner. Austral Ecol, 2011, 36: 203-211.

[40] Johne AB, Weissbecker B, Schütz S. Volatile emissions from Aesculus hippocastanum induced by mining of larval stages of Cameraria ohridella influence oviposition by conspecific females. J Chem Ecol, 2006, 32: 2303-2319.

[41] Kagata H, Ohgushi T. Preference and performance linkage of a leaf-mining moth on different Salicaceae species. Popul Ecol, 2001, 43: 141-147.

[42] Kagata H, Ohgushi T. Oviposition stimuli for host plant recognition and clutch size determination in a leaf-mining moth. Ecol Entomol, 2002, 27: 622-625.

[43] Kaila L, Sugisima K. Elachistine moths of Australia (Lepidoptera: Gelechioidea: Elachistidae), 2011, Collingwood: CSIRO Publishing

[44] Kato M. Alternation of bottom-up and top-down regulation in a natural population of an agromyzid leafminer, Chromatomyia suikazurae. Oecologia, 1994, 97: 9-16.

[45] Kohandani F, Le Goff GJ, Hance T. Does insect mother know under what conditions it will make their offspring live?. Insect Sci, 2016, 24: 1-25.

[46] Kozlov M. Density fluctuations of the leafminer Phyllonorycter strigulatella (Lepidoptera: Gracillariidae) in the impact zone of a power plant. Environ Pollut, 2003, 121: 1-10.

[47] Low C. Grouping increases visual detection risk by specialist parasitoids. Behav Ecol, 2008, 19: 532-538.

[48] Low C, Wood SN, Nisbet RM. The effects of group size, leaf size, and density on the performance of a leaf-mining moth. J Anim Ecol, 2009, 78: 152-160.

[49] Marquardt K. Biologie und Ökologie der Minierfliegen (Dipt., Agromyzidae) an Lonicera und Symphoricarpos (Caprifoliaceae). J Appl Entomol, 1985, 100: 244-255.

[50] Meyer D, Zeileis A, Hornik K (2017) vcd: visualizing categorical data. R package version 1.4-4

[51] Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schäffer AA. Database indexing for production MegaBLAST searches. Bioinformatics, 2008, 24: 1757-1764.

[52] Murai M. Studies on the interference among larvae of the citrus leaf miner, Phyllocnistis citrella Stainton (lepidoptera: Phyllocnistidae). Res Popul Ecol, 1974, 16: 80-111.

[53] Nufio CR, Papaj DR. Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl, 2001, 99: 273-293.

[54] Oatman ER. Intraspecific competition studies of the melon leaf miner, Liriomyza pictella (Thomson) (Diptera: Agromyzidae). Ann Entomol Soc Am, 1960, 53: 130-131.

[55] Parrella MP. Intraspecific competition among larvae of Liriomyza trifolii (Diptera: Agromyzidae): effects on colony production. Environ Entomol, 1983, 12: 1412-1414.

[56] Petitt FL, Wietlisbach DO. Intraspecific competition among same-aged larvae of Liriomyza sativae (Diptera: Agromyzidae) in lima bean primary leaves. Environ Entomol, 1992, 21: 136-140.

[57] Potter DA. Population regulation of the native holly leafminer, Phytomyza ilicicola Loew (Diptera: Agromyzidae), on American holly. Oecologia, 1985, 66: 499-505.

[58] Potter DA, Gordon FC. Parasites associated with the native holly leafminer, Phytomyza illicicola (Diptera: Agromyzidae), on American holly in Kentucky. J Kansas Entomol Soc, 1985, 58: 727-730.

[59] Preszler RW, Price PW. A test of plant-vigor, plant-stress, and plant-genotype effects on leaf-miner oviposition and performance. Oikos, 1995, 74: 485-492.

[60] Quiring DT, McNeil JN. Exploitation and interference intraspecific larval competition in the dipteran leaf miner, Agromyza frontella (Rondani). Can J Zool, 1984, 62: 421-427.

[61] R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

[62] RStudio Team. RStudio: integrated development for R, 2016, Boston: RStudio Inc.

[63] Sato H. Differential resource utilization and co-occurrence of leaf miners on oak (Quercus dentata). Ecol Entomol, 1991, 16: 105-113.

[64] Scheirs J, De Bruyn L, Verhagen R. Optimization of adult performance determines host choice in a grass miner. Proc Biol Sci, 2000, 267: 2065-2069.

[65] Scheirs J, De Bruyn L, Verhagen R, De Bruyn L, Verhagen R. Host nutritive quality and host plant choice in two grass miners: primary roles for primary compounds?. J Chem Ecol, 2003, 29: 1373-1389.

[66] Stiling PD, Brodbeck BV, Strong DR. Intraspecific competition in Hydrellia valida (Diptera: Ephydridae), a leaf miner of Spartina alterniflora. Ecology, 1984, 65: 660-662.

[67] Sugimoto T. On competition among larvae in experimental population of a leaf mining fly, Phytomyza ranunculi Schrank (Diptera: Agromyzidae). Appl Entomol Zool, 1971, 6: 97-104.

[68] Sugisima K, Kaila L. Japanese Elachista mining on the leaf of woody Poaceae (Lepidoptera: Elachistidae s. str.). Entomol Fenn, 2005, 16: 83-102.

[69] Sugiura S, Yamazaki K, Yamaura Y. Intraspecific competition as a selective pressure on the choice of oviposition site in a phytophagous insect. Biol J Linn Soc, 2007, 92: 641-650.

[70] Tack AJM, Ovaskainen O, Harrison PJ, Roslin T. Competition as a structuring force in leaf miner communities. Oikos, 2009, 118: 809-818.

[71] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol, 2013, 30: 2725-2729.

[72] Tuomi J, Niemelä P, Mannila R. Leaves as islands: interactions of Scolioneura betuleti (Hymenoptera) miners in birch leaves. Oikos, 1981, 37: 146-152.

[73] Valladares G, Lawton JH. Host-plant selection in the holly leaf-miner: does mother know best?. J Anim Ecol, 1991, 60: 227-240.

[74] Videla M, Valladares GR, Salvo A. Choosing between good and better: optimal oviposition drives host plant selection when parents and offspring agree on best resources. Oecologia, 2012, 169: 743-751.

[75] Wu ZY, Raven PH, Hong DY. Flora of China. Vol. 22: Poaceae, 2006, Beijing: Science Press.

[76] Zhang Z, Schwartz S, Wagner L, Miller W. A greedy algorithm for aligning DNA sequences. J Comput Biol, 2000, 7: 203-214.