Abstract
Historical, niche-based, and stochastic processes have been proposed as the mechanisms that drive community assembly. In plant–herbivore systems, these processes can correspond to phylogeny, leaf traits, and the distribution of host plants, respectively. Although patterns of herbivore assemblages among plant species have been repeatedly examined, the effects of these factors among co-occurring congeneric host plant species have rarely been studied. Our aim was to reveal the process of community assembly for herbivores by investigating the effects of phylogeny, leaf traits, and the altitudinal distribution of closely related host plants of the genus Acer. We sampled leaf functional traits for 30 Acer species in Japan. Using a newly constructed phylogeny, we determined that three of the six measured leaf traits (leaf thickness, C/N ratio, and condensed tannin content) showed a phylogenetic signal. In a field study, we sampled herbivore communities on 14 Acer species within an elevation gradient and examined relationships between herbivore assemblages and host plants. We found that herbivore assemblages were significantly correlated with phylogeny, leaf traits, phylogenetic signals, and the altitudinal distribution of host plants. Our results indicate that the interaction between historical and current ecological processes shapes herbivore community assemblages.
Similar content being viewed by others
References
Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:165–184
Ackerly DD (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci USA 17:19699–19706
Ackerly DD, Donoghue MJ (1998) Leaf size, sapling allometry, and Corner’s rules: phylogeny and correlated evolution in maples (Acer). Am Nat 152:767–791
Adler PB, HilleRisLambers J, Levine JM (2007) A niche for neutrality. Ecol Lett 10:95–104
Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432
Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149
Agrawal AA, Fishbein M, Halitschke R, Hastings AP, Rabosky DL, Rasmann S (2009) Evidence for adaptive radiation from a phylogenetic study of plant defenses. Proc Natl Acad Sci USA 106:18067–18072
Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552
Asmussen E, Peutzfeldt A, Heitmann T (1999) Stiffness, elastic limit, and strength of newer types of endodontic posts. J Dent 27:275–278
Barber NA, Marquis RJ (2011) Leaf quality, predators, and stochastic processes in the assembly of a diverse herbivore community. Ecology 92:699–708
Becerra JX (1997) Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256
Becerra JX (2007) The impact of herbivore–plant coevolution on plant community structure. Proc Natl Acad Sci USA 104:7483–7488
Beck J, Khen CV (2007) Beta-diversity of geometrid moths from northern Borneo: effects of habitat, time and space. J Anim Ecol 76:230–237
Bergvall UA, Leimar O (2005) Plant secondary compounds and the frequency of food types affect food choice by mammalian herbivores. Ecology 86:2450–2460
Broadhurst RB, Jones WT (1978) Analysis of condensed tannins using acidified vanillin. J Sci Food Agric 29:788–794
Cavender-Bares J, Hozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715
Chase JM (2003) Experimental evidence for alternative stable equilibria in a benthic pond food web. Ecol Lett 6:733–741
Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci USA 104:17430–17434
Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago
Chase JM, Biro EG, Ryberg WA, Smith KG (2009) Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecol Lett 12:1210–1218
Cornell HV, Washburn JO (1979) Evolution of the richness-area correlation for cynipid gall wasps on oak trees: a comparison of two geographic areas. Evolution 33:257–274
Craine JM (2009) Resource strategies of wild plants. Princeton University Press, New Jersey
Darrow K, Bowers MD (1997) Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem Syst Ecol 25:1–11
Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard University Press, Cambridge, pp 342–444
Emerson BC, Gillespie RG (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol Evol 23:619–630
Fay MF, Cameron KM, Prance GT, Lledó MD, Chase MW (1997) Familial relationships of Rhabdodendron (Rhabdodendraceae): plastid rbcL sequences indicate a caryophyllid placement. Kew Bull 52:923–932
Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens MHM, Sääksjärvi I, Schultz JC, Coley PD (2006) The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:150–162
Graham CH, Fine PVA (2008) Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecol Lett 11:1265–1277
Hanski I (1999) Metapopulation ecology. Oxford University Press, New York
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Huelsenbeck JP, Ronquist F (2001) MrBayes, Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Jackson BG, Peltzer DA, Wardle DA (2013) Are functional traits and litter decomposability coordinated across leaves, twigs and wood? A test using temperate rainforest tree species. Oikos 122:1131–1142
Jombart T, Balloux F, Dray S (2010) Adephylo: new tools for investigating the phylogenetic signal in biological traits. Bioinformatics 26:1907–1909
Jordan WC, Courtney MW, Neigel JE (1996) Low levels of intraspecific genetic variation at a rapidly evolving chloroplast DNA locus in North American duckweeds (Lemnaceae). Am J Bot 83:430–439
Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298
Kocyan A, Zhang L-B, Schaefer H, Renner SS (2007) A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Mol Phylogenet Evol 44:553–577
Kumata T, Kobayashi S, Hirowatari T (2013) Gracillaria (in Japanese). In: Nasu Y, Hirowatari T, Kisida Y (eds) The standard of moths in Japan. IV. Gakken Education, Tokyo, pp 91–155
Kurokawa H, Peltzer DA, Wardle DA (2010) Plant traits, leaf palatability and litter decomposability for co-occurring woody species differing in invasion status and nitrogen fixation ability. Funct Ecol 24:513–523
Kursar TA, Coley PD (2003) Convergence in defense syndromes of young leaves in tropical rainforests. Biochem Syst Ecol 31:929–949
Kursar TA, Dexterc KG, Lokvama J, Penningtond RT, Richardsond JE, Webera MG, Murakamia ET, Draked C, McGregord R, Coley PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci USA 106:18073–18078
Lavoie B, Oberhauser KS (2004) Compensatory feeding in Danaus plexippus (Lepidoptera:Nymphalidae) in response to variation in host plant quality. Environ Entom 33:1062–1069
Lei TT, Lechowicz MJ (1990) Shade adaptation and shade tolerance in saplings of three Acer species from eastern North America. Oecologia 84:224–228
Lei TT, Lechowicz MJ (1997) The photosynthetic response of eight species of Acer to simulated light regimes from the centre and edges of gaps. Funct Ecol 11:16–23
Losos JB (1996) Ecological and evolutionary determinant of the species-area relation in Caribbean anoline lizards. Philos Trans R Soc B 351:847–854
Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
Milla R, Reich PB (2011) Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude. Ann Bot 107:455–465
Murakami M, Hirao T, Ichie T (2007) Comparison of lepidopteran larval communities among tree species in a temperate deciduous forest, Japan. Ecol Entomol 32:613–620
Novotny V, Weiblen GD (2005) From communities to continents: beta diversity of herbivorous insects. Ann Zool Fenn 42:463–475
Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, Drozd P (2002) Low host specificity of herbivorous insects in a tropical forest. Nature 416:841–844
Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118
Novotny V, Miller SE, Baje L, Balagawi S, Basset Y, Cizek L, Craft KJ, Dem F, Drew RAI, Hulcr J, Leps J, Lewis O, Pokon R, Stewart AJA, Weiblen GD (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J Anim Ecol 79:1193–1203
Ødegaard F, Diserud OH, Ostbye K (2005) The importance of plant relatedness for host utilization among phytophagous insects. Ecol Lett 8:612–617
Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package. R package version 2.0-2. http://CRAN.R-project.org/package=vegan
Olmstead RG, Michaels HJ, Scott KM, Palmer JD (1992) Monophyly of the Asteridae and identification of their major lineages inferred from DNA sequences of rbcL. Ann Mo Bot Gard 79:249–265
Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelis-sen JHC, Diaz S, Dominy NJ, Elgart A, Enrico L, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Prez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE Jr, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312
Pavoine S, Ollier S, Pontier D, Chessel D (2008) Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theor Popul Biol 73:79–91
Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Natl Acad Sci USA 106:18097–18102
Pearse IS, Hipp AL (2012) Global patterns of leaf defenses in oak species. Evolution 66:2272–2286
Preszler RW, Boecklen WJ (1996) The influence of elevation on tri-trophic interactions: opposing gradients of top-down and bottom-up effects on a leaf-mining moth. Ecoscience 3:75–80
Price ML, Butler LG (1977) Rapid visual estimation and spectro-photometric determination of tannin content of sorghum grain. J Agric Food Chem 25:1268–1273
Rasmann S, Agrawal AA (2011) Evolution of specialization: a phylogenetic study of host range in the red milkweed beetle (Tetraopes tetraophthalmus). Am Nat 177:728–737
Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167
Ricklefs RE (2004) A comprehensive framework for global patterns in biodiversity. Ecol Lett 7:1–15
Rominger AJ, Miller TEX, Collins SL (2009) Relative contributions of neutral and niche-based processes to the structure of a desert grassland grasshopper community. Oecologia 161:791–800
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. (www.r-project.org)
Samuels CL, Drake JA (1997) Divergent perspectives on community convergence. Trends Ecol Evol 12:427–432
Sax DR, Gaines SD, Brown JH (2002) Species invasions exceed extinctions on islands worldwide: a comparative study of plants and birds. Am Nat 160:766–783
Silva DM, Batalha MA (2010) Defense syndromes against herbivory in a cerrado plant community. Plant Ecol 212:181–193
Sipe TW, Bazzaz FA (1994) Gap partitioning among maples (Acer) in central New England: shoot architecture and photosynthesis. Ecology 75:2318–2332
Sipe TW, Bazzaz FA (1995) Gap partitioning among maples (Acer) in central New England: survival and growth. Ecology 76:1587–1602
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tanaka H (1995) Seed demography of three co-occurring Acer species in a Japanese temperate deciduous forest. J Veg Sci 6:887–896
The University of Tokyo Chichibu Forest, Graduate School of Agricultural and Life Sciences, The University of Tokyo (2012) In: The 10th Education and Research Plan of The University of Tokyo Chichibu Forest (2011–2020) (in Japanese)
Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton
Tuomisto H, Ruokolainen K (2006) Analyzing or explaining beta-diversity? Understanding the targets of different methods of analysis. Ecology 87:2697–2708
van Jaarsveld AS, Freitag S, Chown SL, Muller C, Koch S, Hull H, Bellamy C, Kruger M, Endrody-Younga S, Mansell MW, Scholtz CH (1998) Biodiversity assessment and conservation strategies. Science 279:2106–2108
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Webster B, Bruce T, Pickett J, Hardie J (2010) Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim Behav 79:451–457
Weiblen GD, Webb CO, Novotny V, Basset Y, Miller SE (2006) Phylogenetic dispersion of host use in a tropical insect herbivore community. Ecology 87:S62–S75
Yonekura K, Kajita T (2003) BG Plants YList: an online service of Japanese plant names, including a nomenclature index (in Japanese). <http://bean.bio.chiba-u.jp/bgplants/ylist_main.html> Accessed 20 Oct 2013
Zehnder CB, Stodola KW, Joyce BL, Egetter D, Cooper RJ, Hunter MD (2009) Elevational and seasonal variation in the foliar quality and arthropod community of Acer pensylvanicum. Environ Entomol 38:1161–1167
Acknowledgments
We thank K. Watanabe, S. Saito, J. Saihanna, Y. Okamura and Y. Igarashi for their help in the field and laboratory and N. Kamata and technical staff of the University Forests in Chichibu, the University of Tokyo for their kind support. We also thank Nippon Shinyaku and the garden shop of Tsukasa Maples for providing specimens for the DNA extractions. This work was supported by a Grant-in-Aid for Scientific Research from the Japanese Society for the Promotion of Science to M. M. (no. 24310170).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jennifer Thaler.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nakadai, R., Murakami, M. & Hirao, T. Effects of phylogeny, leaf traits, and the altitudinal distribution of host plants on herbivore assemblages on congeneric Acer species. Oecologia 175, 1237–1245 (2014). https://doi.org/10.1007/s00442-014-2964-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-2964-0