Abstract
The structure of the community of insect herbivores in a plant can be determined by plant traits and also by interactions with consumers. We studied the herbivores associated with the tropical plant Andira nitida (Fabaceae), aiming to understand the temporal co-occurrence of herbivore insects from different guilds. We monitored and quantified the temporal sequence of appearance and leaf consumption of three herbivore guilds (leaf miners, gall-formers and chewers) at weekly intervals for 23 weeks (between September 2021 and March 2022), testing whether functional leaf traits (leaf area, leaf dry matter content, specific leaf area and leaf age) influence herbivory incidence and intensity. Leaves of A. nitida showed simultaneous damage by miners, chewers and six gall species. We found a temporal sequence in the establishment of leaf herbivores and a preference for young leaves. However, null model analysis indicated independent patterns of association between herbivores, and there was no evidence of co-occurrence or repulsion between herbivores or herbivore guilds. We found that leaf age is a determinant functional trait for the occurrence of all guilds and types of herbivores in A. nitida. However most of the physical characteristics of the leaf did not show a clear effect on the herbivore community. We showed that interactions among herbivores partially explained the organization of herbivorous insects in A. nitida and that patterns of occurrence depend more on the life history of herbivores than on aspects associated with plant functional traits. We suggest that there is differential leaf use by herbivores in time, which leads to the formation of different pairs of co-occurring herbivores.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data that based this study will be available upon reasonable request.
References
Aide TM (1993) Patterns of leaf development and herbivory in a tropical understory community. Ecology 74:455–466. https://doi.org/10.2307/1939307
Almende BV, Thieurmel B, Robert T (2019) VisNetwork: Network Visualization using ‘vis.js’ Library. R package version 2.0.9. Available from: https://CRAN.R-project.org/ package = visNetwork. Accessed on: 27 Aug. 2022
Araujo DSD, Pereira OJ, Peixo AL (2008) Native fields at the Linhares Forest Reserve, Espírito Santo, Brazil. In: Thomas W.W. (Ed) The Atlantic Coastal Forest of northeastern Brazil. Memoirs of The New York Botanical Garden, The New York Botanical Garden Press; Bronx, USA, pp 371–394
Barber NA, Marquis RJ (2011) Leaf quality, predators, and stochastic processes in the assembly of a diverse herbivore community. Ecology 92:699–708. https://doi.org/10.1890/10-0125.1
Barreto JR, Berenguer E, Ferreira J, Joly CA, Malhi Y, Seixas MMM, Barlow J (2021) Assessing invertebrate herbivory in human-modified tropical forest canopies. Ecol Evol 11:4012–4022. https://doi.org/10.1002/ece3.7295
Barton KE, Edwards KF, Koricheva J (2019) Shifts in woody plant defence syndromes during leaf development. Funct Ecol 33(11):2095–2104. https://doi.org/10.1111/1365-2435.13435
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67: 1–48. https://doi.org/10.48550/arXiv.1406.5823
Becerra JX (2007) The impact of herbivore-plant coevolution on plant community structure. Proc Natl Acad Sci 104:7483–7488. https://doi.org/10.1073/pnas.060825310
Bird G, Kaczvinsky C, Wilson AE, Hardy NB (2019) When do herbivorous insects compete? A phylogenetic meta-analysis. Ecol Lett 22:875–883. https://doi.org/10.1111/ele.13245
Blumenthal DM, Mueller KE, Kray JA, Ocheltree TW, Augustine DJ, Wilcox KR (2020) Traits link drought resistance with herbivore defence and plant economics in semi-arid grasslands: the central roles of phenology and leaf dry matter content. J Ecol 108(6):2336–2351. https://doi.org/10.1111/1365-2745.1345
Brunissen L, Cherqui A, Pelletier Y, Vincent C, Giordanengo P (2009) Host‐plant mediated interactions between two aphid species. Entomol Exp Appl 132:30–38
Caldwell E, Read J, Sanson GD (2016) Which leaf mechanical traits correlate with insect herbivory among feeding guilds? Ann Bot 117:349–361. https://doi.org/10.1093/aob/mcv178
Carneiro MAA, Branco CS, Braga CE, Almada ED, Costa M, Maia VC, Fernandes GW (2009) Are gall midge species (Diptera, Cecidomyiidae ) hostplant specialists? Revista Brasileira De Entomologia 53:365–378. https://doi.org/10.1590/S0085-56262009000300010
Chase JM, Leibold MA (2009) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago, USA, p 221
Cody ML, MacArthur RH, Diamond JM (1975) Ecology and evolution of communities. Harvard University Press, Cambridge, UK, p 560
Coley PD (1980) Effects of leaf age and plant life history patterns on herbivory. Nature 284:545–546. https://doi.org/10.1038/284545a0
Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335. https://doi.org/10.1146/annurev.ecolsys.27.1.305
Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228. https://doi.org/10.1111/j.2006.0030-1299.14928.x
Cornelissen TG, Fernandes GW (2001a) Patterns of attack by herbivores on the tropical shrub Bauhinia brevipes (Leguminosae): Vigour or chance? European Journal of Entomology 98:37–40. https://doi.org/10.14411/eje.2001.006
Cornelissen TG, Fernandes GW (2001b) Defence, growth and nutrient allocation in the tropical shrub Bauhinia brevipes (Leguminosae). Austral Ecol 26(3):246–253. https://doi.org/10.1046/j.1442-9993.2001.01109.x
Cornelissen T, Stiling P (2008) Clumped distribution of oak leaf miners between and within plants. Basic Appl Ecol 9:67–77. https://doi.org/10.1016/j.baae.2006.08.007
Cornelissen T, Guimarães CDC, Viana JPR, Silva B (2013) Interspecific competition influences the organization of a diverse sessile insect community. Acta Oecologica 52:15–18. https://doi.org/10.1016/j.actao.2013.07.001
Costa EC, Martini VC, Souza-Silva A, Lemos-Filho JP, Oliveira DC, Isaias RM (2021) How galling herbivores share a single super-host plant during their phenological cycle: the case of Mimosa gemmulata Barneby (Fabaceae). Trop Ecol 63:1–14. https://doi.org/10.1007/s42965-021-00182-1
Csardi G, Tamas N (2006) The igraph software package for complex network research. InterJournal Complex Systems. http://igraph.org. Accessed 26 out 2022
Csóka G, Stone G, Melika G (2017) Non-native gall-inducing insects on forest trees: a global review. Biol Invasions 19:3161–3181. https://doi.org/10.1007/s10530-017-1466-5
Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012
Demétrio CGB, Hinde J, Moral RA (2014) Models for overdispersed data in entomology. In: Ferreira C, Godoy W (eds) Ecological Modelling Applied to Entomology. Entomology in Focus, vol 1. Springer Cham. pp 219–259. https://doi.org/10.1007/978-3-319-06877-0_9
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331. https://doi.org/10.1146/annurev.en.40.010195.001501
Descombes P, Marchon J, Pradervand JN, Bilat J, Guisan A, Rasmann S, Pellissier L (2017) Community-level plant palatability increases with elevation as insect herbivore abundance declines. J Ecol 105:142–151. https://doi.org/10.1111/1365-2745.12664
Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard University Press, Cambridge, MA, USA, pp 342–444
Ellwood MDF, Manica A, Foster WA (2009) Stochastic and deterministic processes jointly structure tropical arthropod communities. Ecol Lett 12:277–284. https://doi.org/10.1111/j.1461-0248.2009.01284.x
Erb M, Robert CA, Hibbard BE, Turlings TC (2010) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15. https://doi.org/10.1111/j.1365-2745.2010.01757.x
Fagundes M, Xavier RCF, Faria ML, Lopes LGO, Cuevas-Reyes P, Reis-Junior R (2018) Plant phenological asynchrony and. community structure of gall-inducing insects associated with a tropical tree species. Ecol Evol 8:10687–10697. https://doi.org/10.1002/ece3.4477
Fagundes M, Santos ÉMS, Duarte K, Santos L, Vieira J, Oliveira C, Silva PS (2020) Diversity of gall-inducing insects associated with a superhost plant species plant architecture, resource availability and interspecific interactions. Biodivers J Biol Divers 21:1182–1189. https://doi.org/10.13057/biodiv/d210344
Farias RP, da Costa LEN, de Arruda ECP, de Oliveira AFM, Cornelissen T, Mehltreter K (2021) Interactions of gall-formers and leaf-chewers on a tropical tree fern: evidence for non-repulsion and co-occurrence between insect guilds. Plant Biol 23:1037–1043. https://doi.org/10.1111/plb.13298
Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76:161–167. https://doi.org/10.1007/BF00379948
Fernandes GW, Coelho MS, Santos JC (2014) Neotropical insect galls: status of knowledge and perspectives. In: Santos JC, Fernandes GW (eds) Neotropical Insect Galls. Springer, Netherlands, New York, USA, pp 1–14
Gaytán Á, Moreira X, Castagneyrol B, Van Halder I, De Frenne P et al (2022) The co-existence of multiple oak leaf flushes contributes to the large within-tree variation in chemistry, insect attack and pathogen infection. New Phytol 235(4):1615–1628. https://doi.org/10.1111/nph.18209
Godinho DP, Janssen A, Li D, Cruz C, Magalhães S (2020) The distribution of herbivores between leaves matches their performance only in the absence of competitors. Ecol Evol 10:8405–8415. https://doi.org/10.1002/ece3.6547
Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
Gotelli NJ, Ellison AM (2013) EcoSimR 1.00. Available at: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html. Accessed 15 Jun 2022
Gotelli NJ, Hart EM, Ellison AM (2015) EcoSimR: Null model analysis for ecological data. R package version 0.1.0. https://rdrr.io/cran/EcoSimR/. Accessed 15 Jun 2022
Griffith DM, Veech JA, Mars CJ (2016) Cooccur: probabilistic species co-occurrence analysis in R. J Stat Softw 69:1–17
Harris MO, Pitzschke A (2020) Plants make galls to accommodate foreigners: some are friends, most are foes. New Phytol 225:1852–1872. https://doi.org/10.1111/nph.16340
Hayward A, Stone GN (2005) Oak gall wasp communities: evolution and ecology. Basic Appl Ecol 6:435–443. https://doi.org/10.1111/nph.16340
Hespenheide HA (1991) Bionomics of leaf-mining insects. Annu Rev Entomol 36:535–560. https://doi.org/10.1146/annurev.en.36.010191.002535
Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton, NJ
Isaias RMDS, Carneiro RGS, Oliveira DC, Santos JC (2013) Illustrated and. annotated check list of Brazilian gall morphotypes. Neotropical Entomol 42:230–239. https://doi.org/10.1007/s13744-013-0115-7
Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994. https://doi.org/10.1111/j.1461-0248.2007.01093.x
Karban R, Baldwin IT (2007) Induced responses to herbivory. University of Chicago Press
Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960. https://doi.org/10.1111/j.1461-0248.2009.01354.x
Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015a) Global patterns in background losses of woody plant foliage in insects. Glob Ecol Biogeogr 24:1126–1135. https://doi.org/10.1111/geb.12347
Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015b) Background losses of woody plant foliage in insects show variable relationships with plant functional traits across the globe. J Ecol 103:1519–1528. https://doi.org/10.1111/1365-2745.12471
Kraft NJ, Adler PB, Godoy O, James EC, Fuller S, Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599. https://doi.org/10.1111/1365-2435.12345
Kurzfeld-Zexer L, Inbar M (2021) Gall-forming aphids are protected (and benefit) from defoliating caterpillars: the role of plant-mediated mechanisms. BMC Ecol Evol 21(1):1–11. https://doi.org/10.1186/s12862-021-01861-2
Leibold MA, Mikkelson GM (2002) Coherence, species turnover, and boundary clumping: elements of meta-community structure. Oikos 97:237–250. https://doi.org/10.1034/j.1600-0706.2002.970210.x
Leite GLD, Soares MA, Veloso RVS, Silva LF, Guanabens PFS, Munhoz EJM, Zanuncio JC (2022) Free-feeding organisms and galling insects (Hymenoptera) interactions on Caryocar brasiliense (Malpighiales:Caryocaraceae) trees, a savanna plant from Brazil. Brazilian J Biol 84:1–6. https://doi.org/10.1590/1519-6984.257975
Lewinsohn TM, Inácio Prado P, Jordano P, Bascompte J, Olesen JM (2006) Structure in plant–animal interaction assemblages. Oikos 113:174–184. https://doi.org/10.1111/j.0030-1299.2006.14583.x
Li Y, Meijer D, Dicke M, Gols R (2018) Oviposition preference of three lepidopteran species is not affected by previous aphid infestation in wild cabbage. Entomol Exp Appl 166(5):402–411. https://doi.org/10.1111/eea.12663
Lopez-Vaamonde C, Kirichenko N, Ohshima I (2021). Collecting, rearing, and preserving leaf-mining insects. In: Santos JC, Fernandes GW. (eds) Measuring Arthropod Biodiversity. Springer, Cham. pp 439–466. https://doi.org/10.1007/978-3-030-53226-0_17
Martins SS, Biondi D (1990) Preliminary remarks by “Angel im” (Andira nitida Mart. ex Benth) for use in urban afforestation. Acta Botanica Brasilica 4:137–144. https://doi.org/10.1590/S0102-33061990000300013
McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98(5):985–992. https://doi.org/10.1111/j.1365-2745.2010.01693.x
McKenzie SW, Vanbergen AJ, Hails RS, Jones TH, Johnson SN (2013) Reciprocal feeding facilitation between above-and below-ground herbivores. Biol Let 9:20130341. https://doi.org/10.1098/rsbl.2013.0341
Mendes GM, Silveira FAO, Oliveira C, Dáttilo W, Guevara R, Ruiz-Guerra B, Boaventura MG, Sershen RS, Phartyal SS et al (2021) How much leaf area do insects eat? A data set of insect herbivory sampled globally with a standardized protocol. Ecology 102:03301. https://doi.org/10.1002/ecy.3301
Moles AT, Westoby M (2000) Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos 90:517–524. https://doi.org/10.1034/j.1600-0706.2000.900310.x
Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6:e18840.
Muiruri EW, Barantal S, Iason GR, Salminen JP, Perez-Fernandez E, Koricheva J (2019) Forest diversity effects on insect herbivores: do leaf traits matter? New Phytol 221:2250–2260. https://doi.org/10.1111/nph.15558
Nardi C, Rech C, Oliveira JRF, Peñaflor MFGV, Santos F, Bento JMS (2023) Preference-performance hypothesis and host oviposition selection of Diabrotica speciosa: aboveground female avoids belowground conspecific larvae in maize. Arthropod-Plant Interactions. https://doi.org/10.1007/s11829-023-09972-x
Njovu HK, Peters MK, Schellenberger D, Brandl R, Kleyer M, Steffan-Dewenter I (2019) Leaf traits mediate changes in invertebrate herbivory along broad environmental gradients on Mt. Kilimanjaro. Tanzania J Animal Ecol 88:1777–1788. https://doi.org/10.1111/1365-2656.13058
Novotny V, Miller SE, Baje L, Balagawi S, Basset Y, Cizek L, Weiblen GD (2010) Guild-specific patterns of species richness and host specialization in plant–herbivore food webs from a tropical forest. J Animal Ecol 79:1193–1203. https://doi.org/10.1111/j.1365-2656.2010.01728.x
Oliveira EF, Pallini A, Janssen A (2019) Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores. Insect Sci 26:108–118. https://doi.org/10.1111/1744-7917.12499
Oliveira ANS, Amorim CMF, Lemos RPL (2020) As riquezas das áreas protegidas no território alagoano. Instituto do Meio Ambiente-Mineradora Vale Verde, Maceió, BR
Pascual-Alvarado E, Cuevas-Reyes P, Quesada M, Oyama K (2008) Interactions between galling insects and. leaf-feeding insects: the role of plant phenolic compounds and. their possible interference with herbivores. J Trop Ecol 24:329–336. https://doi.org/10.1017/S0266467408005038
Peeters PJ (2002) Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biol J Lin Soc 77:43–65. https://doi.org/10.1046/j.1095-8312.2002.00091.x
Pennington RT (2003) Monograph of Andira (Leguminosae-Papilionoideae). Syst Bot Monographs 64:1–143. https://doi.org/10.2307/25027903
Pérez- Harguindeguy N, Díaz S, Vendramini F, Cornelissen JH, Gurvich DE, Cabid M (2003) Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecol 28:642–650. https://doi.org/10.1046/j.1442-9993.2003.01321.x
Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust Bot 61:167–234. https://doi.org/10.1071/BT12225_CO
Price PW (2002) Resource-driven terrestrial interaction webs. Ecol Res 17:241–247. https://doi.org/10.1046/j.1440-1703.2002.00483.x
R Core Team (2022) R: A language and. environment for statistics computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org. Accessed 13 june 2022
Raghu S, Brown B, Purcell MF (2012) Searching for the signal of competition in plant-mediated interactions among coexisting gall insects on broad-leaved paperbark. Arthropod-Plant Interact 6(1):83–91. https://doi.org/10.1007/s11829-011-9162-3
Ramos LF, Solar RR, Santos HT, Fagundes M (2019) Variation in community structure of gall-inducing insects associated with a tropical plant supports the hypothesis of competition in stressful habitats. Ecol Evol 9:13919–13930. https://doi.org/10.1002/ece3.5827
Ribeiro SP, Basset Y (2007) Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography 30:663–672. https://doi.org/10.1111/j.2007.0906-7590.05083.x
Ruiz-Guerra B, Garcia A, Velázquez-Rosas N, Ângulo D, Guevara R (2021) Plant-functional traits drive insect herbivory in a tropical rainforest tree community. Perspect Plant Ecol Evol Syst 48:125587. https://doi.org/10.1016/j.ppees.2020.125587
Ruiz-Guerra B, Velázquez-Rosas N, Díaz-Castelazo C, Guevara R (2020) Functional plant traits and plant-herbivore interactions. In: Núñez-Farfán J., Valverde P.L. (Eds) Evolutionary Ecology of Plant-Herbivore Interaction. Springer Nature; Switzerland: 91–207. https://doi.org/10.1007/978-3-030-46012-9_10
Santos JC, Maldonado-López Y, Venâncio H, Almeida WR, Felicio DT, Cintra FCF, Cuevas-Reyes P (2021) Interspecific competition drives gall-inducing insect species distribution on leaves of Matayba guianensis Aubl. (Sapindaceae). Ecol Entomol 46:1059–1071. https://doi.org/10.1111/een.13042
Satoh T, Yoshida T, Koyama S, Yamagami A, Takata M, Doi H, Hata Y (2016) Resource partitioning based on body size contributions I’m the species diversity of wood-boring beetles and arboreal nesting ants. Insect Conserv Divers 9:4–12. https://doi.org/10.1111/icad.12136
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089
Schultz BB (1992) Insect herbivores as potential causes of mortality and adaptation in gall forming insects. Oecologia 90:297–299. https://doi.org/10.1007/BF00317190
Silva EAM, Urso-Guimarães MV (2021) New records and expansion of the geographic distribution of gall inducers of the family Cecidomyiidae (Diptera) associated to Andira Lam (Fabaceae) species in Brazil. Revista Brasileira De Entomol 65:1–12. https://doi.org/10.1590/1806-9665-RBENT-2021-0071
Silva DB, Jiménez A, Urbaneja A, Pérez-Hedo M, Bento JM (2021) Changes in plant responses induced by an arthropod influence the colonization behavior of a subsequent herbivore. Pest Manag Sci 77:4168–4180. https://doi.org/10.1002/ps.6454
Sinclair RJ, Hughes L (2010) Leaf miners: the hidden herbivores. Austral Ecol 35:300–313. https://doi.org/10.1111/j.1442-9993.2009.02039.x
Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522. https://doi.org/10.1016/S0169-5347(03)00247-7
Strong DR, Lawton JH, Southwood SR (1984) Insects on plants: community patterns and mechanisms. Harvard University Press, London, UK, p 313
Van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55. https://doi.org/10.1146/annurev.ento.52.110405.091418
Van Dijk LJ, Ehrlén J, Tack AJ (2020) The timing and asymmetry of plant–pathogen–insect interactions. Proc R Soc B 287(1935):20201303. https://doi.org/10.1098/rspb.2020.1303
Veech JA (2013) The probabilistic model for analyzing species co-occurrence. Global Ecol Biogeogr 22:252–260. https://doi.org/10.1111/j.1466-8238.2012.00789.x
Venner S, Pélisson PF, Bel-Venner MC, Débias F, Rajon E, Menu F (2011) Coexistence of insect species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments. PLoS ONE 6(3):e18039. https://doi.org/10.1371/journal.pone.0018039
Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896. https://doi.org/10.1890/04-0313
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.216637
Wei T, Simko V (2021) R package 'corrplot': Visualization of a Correlation Matrix. (Version 0.92), https://github.com/taiyun/corrplot>
Yamasaki M, Kikuzawa K (2003) Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata. Oecologia 137:226–232. https://doi.org/10.1007/s00442-003-1337-x
Yukawa J (2000) Synchronization of gallers with host plant phenology. Popul Ecol 42:105–113. https://doi.org/10.1007/PL00011989
Yukawa J, Akimoto K (2006) Influence of synchronization between adult emergence and. host plant phenology on the population density of Pseudasphondylia neolitseae (Diptera:Cecidomyiidae) inducing leaf gals on Neolitsea sericea (Lauraceae). Popul Ecol 48:13–21. https://doi.org/10.1007/s10144-005-0233-0
Acknowledgements
We would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial Support. We would also like to thank Tenilson de Assis, Willames Santos, Amanda Souza and Dalton Souza for their support and aid during fieldwork.
Funding
This study was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) through fellowship to SS, Luziene. KRB is a fellowship recipient of Programa de Educação Tutorial (PET/SESu/MEC). TC acknowledges funding from CNPq.
Author information
Authors and Affiliations
Contributions
Conceptualization: LS, GRD, KRB and TC. Data curation: LS. Formal analysis: LS and GRD. Methodology: LS, GRD, KRB, TC. Writing—Original Draft: LS. Writing—Review & editing: LS, GRD, KRB, and TC.
Corresponding author
Ethics declarations
Conflict of interest
The authors report no existing competing interests.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Handling Editor: Bastien Castagneyrol.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Seixas, L., Demetrio, G.R., Barão, K.R. et al. Temporal co-occurrence of leaf herbivory by chewers, leaf miners and gall-formers on a tropical tree: Do leaf traits matter?. Arthropod-Plant Interactions (2024). https://doi.org/10.1007/s11829-024-10053-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11829-024-10053-w