A highly resolved food web for insect seed predators in a species-rich tropical forest
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu dopisy
Grantová podpora
Royal Society
Smithsonian Tropical Research Institute
Carl Cedercreutz foundation
Frank Levinson Family Foundation
NE/J007463/1
Natural Environment Research Council
U.S. National Science Foundation
Academy of Finland
Rachadaphiseksomphot Fund
Graduate School
Chulalongkorn University
SENACYT
16-20825S
GACR
FY014
The Smithsonian barcoding initiative
FY015
The Smithsonian barcoding initiative
The John Fell OUP Research Fund
PubMed
31359570
PubMed Central
PMC6852488
DOI
10.1111/ele.13359
Knihovny.cz E-zdroje
- Klíčová slova
- Apparent competition, Barro Colorado Island, Janzen-Connell hypothesis, Panama, host specialisation, interaction network, plant traits, quantitative food web, seed predation,
- MeSH
- biodiverzita MeSH
- fylogeneze MeSH
- hmyz * MeSH
- lesy * MeSH
- potravní řetězec * MeSH
- semena rostlinná MeSH
- tropické klima * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- dopisy MeSH
- Geografické názvy
- Panama MeSH
The top-down and indirect effects of insects on plant communities depend on patterns of host use, which are often poorly documented, particularly in species-rich tropical forests. At Barro Colorado Island, Panama, we compiled the first food web quantifying trophic interactions between the majority of co-occurring woody plant species and their internally feeding insect seed predators. Our study is based on more than 200 000 fruits representing 478 plant species, associated with 369 insect species. Insect host-specificity was remarkably high: only 20% of seed predator species were associated with more than one plant species, while each tree species experienced seed predation from a median of two insect species. Phylogeny, but not plant traits, explained patterns of seed predator attack. These data suggest that seed predators are unlikely to mediate indirect interactions such as apparent competition between plant species, but are consistent with their proposed contribution to maintaining plant diversity via the Janzen-Connell mechanism.
Biodiversity Unit University of Turku Turku Finland
Biology Department University of San Diego San Diego CA USA
Department of Chemistry University of Turku Turku Finland
Department of Ecology Swedish University of Agricultural Sciences Uppsala Sweden
Department of Entomology Michigan State University East Lansing MI USA
Department of Zoology University of Oxford Oxford UK
Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
ForestGEO Smithsonian Tropical Research Institute Balboa Republic of Panama
Maestria de Entomologia Universidad de Panamá Panama Republic of Panama
National Museum of Natural History Smithsonian Institution Washington DC USA
School of Biological Sciences University of Reading Reading UK
Smithsonian Tropical Research Institute Balboa Republic of Panama
Zobrazit více v PubMed
Asner, G.P. & Martin, R.E. (2012). Contrasting leaf chemical traits in tropical lianas and trees: implications for future forest composition. Ecol. Lett., 15, 1001–1007. PubMed
Bagchi, R. , Gallery, R.E. , Gripenberg, S. , Gurr, S.J. , Narayan, L. , Addis, C.E. et al (2014). Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature, 506, 85–88. PubMed
Birch, A.N.E. , Fellows, L.E. , Evans, S.V. & Doherty, K. (1986). Para‐aminophenylalanine in vigna: possible taxonomic and ecological significance as a seed defence against bruchids. Phytochemistry, 25, 2745–2749.
Blomberg, S.P. , Garland, T. & Ives, A.R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717–745. PubMed
Blüthgen, N. , Menzel, F. & Blüthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecol., 6, 9. PubMed PMC
Boege, K. & Marquis, R.J. (2006). Plant quality and predation risk mediated by plant ontogeny: consequences for herbivores and plants. Oikos, 115, 559–572.
Boege, K. , Dirzo, R. , Siemens, D. & Brown, P. (2007). Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol. Lett., 10, 177–187. PubMed
Bradley, D.J. , Gilbert, G.S. & Martiny, J.B.H. (2008). Pathogens promote plant diversity through a compensatory response. Ecol. Lett., 11, 461–469. PubMed
Brown, P.D. , Tokuhisa, J.G. , Reichelt, M. & Gershenzon, J. (2003). Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana . Phytochemistry, 62, 471–481. PubMed
Burdon, J.J. , Thrall, P.H. & Ericson, A.L. (2006). The current and future dynamics of disease in plant communities. Annu. Rev. Phytopath., 44, 19–39. PubMed
Cárdenas, R.E. , Valencia, R. , Kraft, N.J. , Argoti, A. & Dangles, O. (2014). Plant traits predict inter‐ and intraspecific variation in susceptibility to herbivory in a hyperdiverse Neotropical rain forest tree community. J. Ecol., 102, 939–952.
Carmona, D. , Lajeunesse, M.J. & Johnson, M.T. (2011). Plant traits that predict resistance to herbivores. Funct. Ecol., 25, 358–367.
Coley, P.D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr., 53, 209–233.
Coley, P.D. , Bryant, J.P. & Chapin, F.S. (1985). Resource availability and plant antiherbivore defense. Science, 230, 895–899. PubMed
Condit, R. (1998). Tropical Forest Census Plots: Methods and Results from Barro Colorado Island, Panama and a Comparison with Other Plots. Springer‐Verlag, Berlin.
Condit, R. , Ashton, P.S. , Baker, P. , Bunyavejchewin, S. , Gunatilleke, S. , Gunatilleke, N. et al (2000). Spatial patterns in the distribution of tropical tree species. Science, 288, 1414–1418. PubMed
Connell, J.H. (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees In: Dynamics of Populations (eds. DenBoer P.J. & Gradwell, G.R.). PUDOC, Wageningen, pp. 298–312.
Crawley, M.J. (1989). Insect herbivores and plant‐population dynamics. Annu. Rev. Entomol., 34, 531–564.
Crawley, M.J. (2000). Seed predators and plant population dynamics In Seeds, 3rd Edition: The Ecology of Regeneration in Plant Communities (ed Gallagher R.S.). CAB International, Wallingford, Oxfordshire, pp. 167–182.
Croat, T.B. (1978). Flora of Barro Colorado Island. Stanford University Press, Stanford, CA.
Ctvrtecka, R. , Sam, K. , Brus, E. , Weiblen, G.D. & Novotny, V. (2014). Frugivorous weevils are too rare to cause Janzen‐Connell effects in New Guinea lowland rain forest. J. Trop. Ecol., 30, 521–535.
Cutler, D.R. , Edwards, T.C. , Beard, K.H. , Cutler, A. , Hess, K.T. , Gibson, J. et al (2007). Random forests for classification in ecology. Ecology, 88, 2783–2792. PubMed
Dormann, C.F. , Gruber, B. & Fründ, J. (2008). Introducing the bipartite package: analysing ecological networks.Rnews, 8.
Downey, H. , Lewis, O.T. , Bonsall, M.B. , Fernandez, D.C. & Gripenberg, S. (2018). Insect herbivory on seedlings of rainforest trees: effects of density and distance of conspecific and heterospecific neighbors. Ecol. Evol., 8, 12702–12711. PubMed PMC
Elton, C.S. (1975). Conservation and the low population density of invertebrates inside neotropical rain forest. Biol. Conserv., 7, 3–15.
Endara, M.‐J. , Coley, P.D. , Ghabash, G. , Nicholls, J.A. , Dexter, K.G. , Donoso, D.A. et al (2017). Coevolutionary arms race versus host defense chase in a tropical herbivore–plant system. Proc. Natl Acad. Sci. U. S. A., 114, E7499–E7505. PubMed PMC
Feeny, P.P. (1976). Plant apparency and chemical defense. Rec. Adv. Phytochem., 10, 1–40.
Fenner, M. & Thompson, K. (2005). The Ecology of Seeds. Cambridge University Press, Cambridge, UK.
Fenner, M. , Cresswell, J. , Hurley, R. & Baldwin, T. (2002). Relationship between capitulum size and pre‐dispersal seed predation by insect larvae in common Asteraceae. Oecologia, 130, 72–77. PubMed
Fritz, S.A. & Purvis, A. (2010). Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv. Biol., 24, 1042–1051. PubMed
Fritz, R.S. & Simms, E.L. (1992). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago, IL.
Futuyma, D.J. & Gould, F. (1979). Associations of plants and insects in deciduous forest. Ecol. Monogr., 49, 33–50.
Garzon‐Lopez, C.X. , Ballesteros‐Mejia, L. , Ordoñez, A. , Bohlman, S.A. , Olff, H. & Jansen, P.A. (2015). Indirect interactions among tropical tree species through shared rodent seed predators: a novel mechanism of tree species coexistence. Ecol. Lett., 18, 752–760. PubMed
Gilbert, G.S. & Webb, C.O. (2007). Phylogenetic signal in plant pathogen–host range. Proc. Natl Acad. Sci. U. S. A., 104, 4979–4983. PubMed PMC
Gilbert, G.S. , Magarey, R. , Suiter, K. & Webb, C.O. (2012). Evolutionary tools for phytosanitary risk analysis: phylogenetic signal as a predictor of host range of plant pests and pathogens. Evol. Appl., 5, 869–878. PubMed PMC
Gilbert, G.S. , Briggs, H.M. & Magarey, R. (2015). The impact of plant enemies shows a phylogenetic signal. PLoS ONE, 10, e0123758. PubMed PMC
Green, P.T. , Harms, K.E. & Connell, J.H. (2014). Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest. Proc. Natl Acad. Sci. U. S. A., 111, 18649–18654. PubMed PMC
Gripenberg, S. (2018). Do pre‐dispersal insect seed predators contribute to maintaining tropical forest plant diversity? Biotropica, 50, 839–845.
Gripenberg, S. , Rota, J. , Kim, J. , Wright, S.J. , Garwood, N.C. , Fricke, E.C. et al (2018). Seed polyphenols in a diverse tropical plant community. J. Ecol., 106, 87–100.
Hanski, I. (2001). Spatially realistic theory of metapopulation ecology. Naturwissenschaften, 88, 372–381. PubMed
Harms, K.E. , Wright, S.J. , Calderon, O. , Hernandez, A. & Herre, E.A. (2000). Pervasive density‐dependent recruitment enhances seedling diversity in a tropical forest. Nature, 404, 493–495. PubMed
Holt, R.D. (1977). Predation, apparent competition, and structure of prey communities. Theor. Popul. Biol., 12, 197–229. PubMed
Hubbell, S.P. , Foster, R.B. , O'Brien, S.T. , Harms, K. , Condit, R. , Wechsler, B. et al (1999). Light‐gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science, 283, 554–557. PubMed
Hubbell, S.P. , Condit, R. & Foster, R.B. (2005). Barro Colorado Forest Plot Census Data. http://ctfs.si.edu/webatlas/datasets/bci.
Janzen, D.H. (1968). Host plants as islands in evolutionary and contemporary time. Am. Nat., 102, 592–595.
Janzen, D.H. (1969). Seed‐eaters versus seed size, number, toxicity and dispersal. Evolution, 23, 1–27. PubMed
Janzen, D.H. (1970). Herbivores and number of tree species in tropical forests. Am. Nat., 104, 501–528.
Janzen, D.H. (1971). Seed predation by animals. Annu. Rev. Ecol. Syst., 2, 465–492.
Janzen, D.H. (1976). Why bamboos wait so long to flower. Ann. Rev. Ecol. Syst., 7, 347–391.
Janzen, D.H. (1980). Specificity of seed‐attacking beetles in a Costa Rican deciduous forest. J. Ecol., 68, 929–952.
Jones, F.A. & Comita, L.S. (2010). Density‐dependent pre‐dispersal seed predation and fruit set in a tropical tree. Oikos, 119, 1841–1847.
Kelly, D. (1994). The evolutionary ecology of mast seeding. Trends Ecol. Evol., 9, 465–470. PubMed
Kembel, S.W. , Cowan, P.D. , Helmus, M.R. , Cornwell, W.K. , Morlon, H. , Ackerly, D.D. et al (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464. PubMed
Kolb, A. , Ehrlén, J. & Eriksson, O. (2007). Ecological and evolutionary consequences of spatial and temporal variation in pre‐dispersal seed predation. Perspect. Plant Ecol. Evol. Syst., 9, 79–100.
Kress, W.J. , Erickson, D.L. , Jones, F.A. , Swenson, N.G. , Perez, R. , Sanjur, O. et al (2009). Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc. Natl Acad. Sci. U. S. A., 106, 18621–18626. PubMed PMC
Kuprewicz, E.K. & García‐Robledo, C. (2010). Mammal and insect predation of chemically and structurally defended Mucuna holtonii (Fabaceae) seeds in a Costa Rican rain forest. J. Trop. Ecol., 26, 263–269.
Landis, J.R. & Koch, G.G. (1977). The measurement of observer agreement for categorical data. Biometrics, 36, 207–216. PubMed
Leck, M.A. , Parker, V.T. & Simpson, R.L. (2008). Seedling Ecology and Evolution. Cambridge University Press, Cambridge, UK.
Leigh, E.G.J. (1999). Tropical Forest Ecology. A View from Barro Colorado Island. Oxford University Press Inc., New York.
Lewis, O.T. & Gripenberg, S. (2008). Insect seed predators and environmental change. J. Appl. Ecol., 45, 1593–1599.
Lewis, O.T. , Memmott, J. , Lasalle, J. , Lyal, C.H.C. , Whitefoord, C. & Godfray, H.C.J. (2002). Structure of a diverse tropical forest insect‐parasitoid community. J. Anim. Ecol., 71, 855–873.
Lill, J.T. , Marquis, R.J. & Ricklefs, R.E. (2002). Host plants influence parasitism of forest caterpillars. Nature, 417, 170–173. PubMed
Loranger, J. , Meyer, S.T. , Shipley, B. , Kattge, J. , Loranger, H. , Roscher, C. et al (2012). Predicting invertebrate herbivory from plant traits: evidence from 51 grassland species in experimental monocultures. Ecology, 93, 2674–2682. PubMed
Marquis, R.J. , Diniz, I.R. & Morais, H.C. (2001). Patterns and correlates of interspecific variation in foliar insect herbivory and pathogen attack in Brazilian cerrado. J. Trop. Ecol., 17, 127–148.
McArt, S.H. , Halitschke, R. , Salminen, J.‐P. & Thaler, J.S. (2013). Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology, 94, 966–975.
Müller, C.B. , Adriaanse, I.C.T. , Belshaw, R. & Godfray, H.C.J. (1999). The structure of an aphid‐parasitoid community. J. Anim. Ecol., 68, 346–370.
Novotny, V. , Basset, Y. , Miller, S.E. , Weiblen, G.D. , Bremer, B. , Cizek, L. et al (2002). Low host specificity of herbivorous insects in a tropical forest. Nature, 416, 841–844. PubMed
Novotny, V. , Miller, S.E. , Baje, L. , Balagawi, S. , Basset, Y. , Cizek, L. et al (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. PubMed
Orme, D. , Freckleton, R. , Thomas, G. , Petzoldt, T. , Fritz, S. , Isaac, N. et al (2018). caper: comparative analyses of phylogenetics and evolution in R. R package version 1.0.1. https://CRAN.R-project.org/package=caper.
Pacala, S.W. & Crawley, M.J. (1992). Herbivores and plant diversity. Am. Nat., 140, 243–260. PubMed
Pinzón‐Navarro, S. , Barrios, H. , Múrria, C. , Lyal, C.H.C. & Vogler, A.P. (2010). DNA‐based taxonomy of larval stages reveals huge unknown species diversity in neotropical seed weevils (genus Conotrachelus): relevance to evolutionary ecology. Mol. Phyl. Evol., 56, 281–293. PubMed
Ratnasingham, S. & Hebert, P.D.N. (2013). A DNA‐based registry for all animal species: The Barcode Index Number (BIN) system. PLoS ONE, 8, e66213. PubMed PMC
Revell, L.J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol., 3, 217–223.
Sam, K. , Ctvrtecka, R. , Miller, S.E. , Rosati, M.E. , Molem, K. , Damas, K. et al (2017). Low host specificity and abundance of frugivorous lepidoptera in the lowland rain forests of Papua New Guinea. PLoS ONE, 12, e0171843. PubMed PMC
Sang, J.P. , Minchinton, I.R. , Johnstone, P.K. & Truscott, R.J.W. (1984). Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Canad. J. Plant Sci., 64, 77–93.
Schemske, D.W. , Mittelbach, G.G. , Cornell, H.V. , Sobel, J.M. & Roy, K. (2009). Is there a latitudinal gradient in the importance of biotic interactions? Annu. Rev. Ecol. Evol. Syst., 40, 245–269.
Schuldt, A. , Bruelheide, H. , Durka, W. , Eichenberg, D. , Fischer, M. , Kröber, W. et al (2012). Plant traits affecting herbivory on tree recruits in highly diverse subtropical forests. Ecol. Lett., 15, 732–739. PubMed
Sedio, B.E. & Ostling, A.M. (2013). How specialised must natural enemies be to facilitate coexistence among plants? Ecol. Lett., 16, 995–1003. PubMed
Strobl, C. , Boulesteix, A.‐L. , Zeileis, A. & Hothorn, T. (2007). Bias in random forest variable importance measures: Illustrations, sources and a solution. BMC Bioinformatics, 8, 25. PubMed PMC
Turcotte, M.M. , Davies, T.J. , Thomsen, C.J.M. & Johnson, M.T.J. (2014). Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proc. R. Soc. Lond. B: Biol. Sci., 281, 20140555. PubMed PMC
Visser, M.D. , Muller‐Landau, H.C. , Wright, S.J. , Rutten, G. & Jansen, P.A. (2011). Tri‐trophic interactions affect density dependence of seed fate in a tropical forest palm. Ecol. Lett., 14, 1093–1100. PubMed
Walters, D.R. (2011). Plant Defense: Warding off Attack by Pathogens, Herbivores, and Parasitic Plants. Wiley‐Blackwell, Chichester, UK.
Willig, M.R. , Kaufman, D.M. & Stevens, R.D. (2003). Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis. Annu. Rev. Ecol. Evol. Syst., 34, 273–309.
Wolda, H. (1988). Insect seasonality: why? Ann. Rev. Ecol. Syst., 19, 1–18.
Wright, S.J. (1983). The dispersion of eggs by a bruchid beetle among Scheelea palm seeds and the effect of distance to the parent palm. Ecology, 64, 1016–1021.
Wright, S.J. & Calderón, O. (2006). Seasonal, El Niño and longer term changes in flower and seed production in a moist tropical forest. Ecol. Lett., 9, 35–44. PubMed
Wright, S.J. , Muller‐Landau, H.C. , Calderón, O. & Hernandéz, A. (2005). Annual and spatial variation in seedfall and seedling recruitment in a neotropical forest. Ecology, 86, 848–860.
Yu, G. , Smith, D.K. , Zhu, H. , Guan, Y. & Tsan-Yuk Lam, T. (2017). GGTREE: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol., 8, 28–36.
Zalamea, P.‐C. , Dalling, J.W. , Sarmiento, C. , Arnold, A.E. , Delevich, C. , Berhow, M.A. et al (2018). Dormancy‐defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species. Ecology, 99, 1988–1998. PubMed
Zimmerman, J.K. , Wright, S.J. , Calderón, O. , Pagan, M.A. & Paton, S. (2007). Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: the role of annual changes in irradiance. J. Trop. Ecol., 23, 231–251.