Advertisement

Tropical Ecology

, Volume 60, Issue 2, pp 238–251 | Cite as

Functional attributes of two Croton species in different successional stages of tropical dry forest: effects on herbivory and fluctuating asymmetry patterns

  • José Gerardo González-Esquivel
  • Pablo Cuevas-Reyes
  • Antonio González-Rodríguez
  • Luis Daniel Ávila-Cabadilla
  • Mariana Yolotl Álvarez-Añorve
  • Marcilio Fagundes
  • Yurixhi Maldonado-LópezEmail author
Research Article
  • 2 Downloads

Abstract

Tropical dry forests are among the most threatened ecosystems in the world. After habitat perturbation occurs, the habitat recovers naturally through ecological succession. This succession can modify functional attributes of plants, which in turn, can affect herbivorous insects’ performance. We analyzed morphological, functional, and chemical traits associated with herbivory patterns in Croton roxanae and C. suberosus, that occur in mature and secondary forests in the tropical dry forest of Chamela, Jalisco. Leaf area and leaf thickness were higher in secondary forest, while leaf density and fresh leaf mass were higher in mature forest. Dry leaf mass, specific leaf area, chlorophyll content, and water content showed variation between species in both forest conditions. The concentration of secondary metabolites showed variation between species and forest conditions. Croton roxanae showed higher herbivory in mature forest, and C. suberosus did not show differences between the two conditions. Leaves in secondary forest were slightly longer and broader than leaves in mature forest. Croton species showed higher fluctuating asymmetry in secondary forest. Herbivory was not associated with levels of fluctuating asymmetry levels in both Croton species. Our results suggest that plant attributes are influenced by forest condition, which in turn, indirectly affect the attack of herbivores.

Keywords

Alkaloids Chemical defense Herbivores Land use change Morphological variation Phenols Succession 

Notes

Acknowledgements

González-Esquivel thanks CONACyT for the scholarship awarded. Pablo Cuevas-Reyes thanks Coordinación de la Investigación Científica, UMSNH for their generous support. We also thank Fidel Anguiano for editing figures. This project was supported by CONACYT Project no. CB222202.

References

  1. Aboshi T, Ishiguri S, Shiono Y, Murayama T (2018) Flavonoid glycosides in Malabar spinach Basella alba inhibit the growth of Spodoptera litura larvae. Biosci Biotechnol Biochem 82:9–14CrossRefGoogle Scholar
  2. Abramoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42Google Scholar
  3. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149CrossRefGoogle Scholar
  4. Albarrán-Lara AL, Mendoza-Cuenca L, Valencia-Avalos S, González-Rodríguez A, Oyama K (2010) Leaf fluctuating asymmetry increases with hybridization and introgression between Quercus magnolifolia and Quercus resinosa (Fagaceae) through an altitudinal gradient in Mexico. Int J Plant Sci 171:310–322CrossRefGoogle Scholar
  5. Ali MB, Singh N, Shohael AM, Hahn EJ, Paek KY (2006) Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress. Plant Sci 171:147–154CrossRefGoogle Scholar
  6. Alvarez-Añorve MY, Quesada M, Sánchez-Azofeifa GA, Ávila-Cabadilla LD, Gamon JA (2012) Functional regeneration and spectral reflectance of trees during succession in a highly diverse tropical dry forest ecosystem. Am J Bot 99:816–826CrossRefGoogle Scholar
  7. Alves-Silva E, Del-Claro K (2016) Herbivory-induced stress: leaf developmental instability is caused by herbivore damage in early stages of leaf development. Ecol Ind 61:359–365CrossRefGoogle Scholar
  8. Arroyo-Rodríguez V, Melo FP, Martínez-Ramos M, Bongers F, Chazdon RL, Meave JA, Tabarelli M (2017) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev 92:326–340CrossRefGoogle Scholar
  9. Balvanera P, Quijas S, Pérez-Jiménez A (2011) Distribution patterns of tropical dry forest trees along a mesoscale water availability gradient. Biotropica 43:414–422CrossRefGoogle Scholar
  10. Beltrán-Rodríguez LA, Valdez-Hernández JI, Luna-Cavazos M, Romero-Manzanares A, Pineda-Herrera E, Maldonado-Almanza B, Blancas-Vázquez J (2018) Estructura y diversidad arbórea de bosques tropicales caducifolios secundarios en la Reserva de la Biosfera Sierra de Huautla, Morelos. Rev Mex Biodivers 89:108–122Google Scholar
  11. Bielinis E, Jozwiak W, Robakowski P (2015) Modelling of the relationship between the SPAD values and photosynthetic pigments content in Quercus petraea and Prunus serotina leaves. Dendrobiology 2015:73Google Scholar
  12. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New YorkGoogle Scholar
  13. Carneiro-Torres DS, Cordeiro I, Giulietti AM, Berry PE, Riina R (2011) Three new species of Croton (Euphorbiaceae ss) from the Brazilian Caatinga. Brittonia 63:122–132CrossRefGoogle Scholar
  14. Chazdon RL, Guariguata MR (2016) Natural regeneration as a tool for large-scale forest restoration in the tropics: prospects and challenges. Biotropica 48:716–730CrossRefGoogle Scholar
  15. Chazdon R, Letcher S, Van Breugel M, Martinez-Ramos M, Bongers F, Finegan B (2007) Rates of change in tree communities of secondary neotropical forests following major disturbances. Philos Trans R Soc B Biol Sci 362:273–289CrossRefGoogle Scholar
  16. Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233CrossRefGoogle Scholar
  17. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  18. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivory defense. Science 230:895–899CrossRefGoogle Scholar
  19. Cornelissen T, Stiling P (2005) Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia 142:46–56CrossRefGoogle Scholar
  20. Cornelissen T, Stiling P (2011) Similar responses of insect herbivores to leaf fluctuating asymmetry. Arthropod Plant Interact 5:59–69CrossRefGoogle Scholar
  21. Costa FV, Pinheiro IF, Braga LL, Perillo L, Neves FS, Leite LO, Silva BL, Ribeiro LC, Fernandes GW, Cuevas-Reyes P (2012) Fluctuating asymmetry and herbivory in two ontogenetical stages of Chamaecrista semaphora in restored and natural environments. J Plant Interact 8:179–186CrossRefGoogle Scholar
  22. Creighton JC (2005) Population density, body size, and phenotypic plasticity of brood size in a burying beetle. Behav Ecol 16:1031–1036CrossRefGoogle Scholar
  23. Cuevas-Reyes P, Quesada M, Oyama K (2006) Abundance and leaf damage caused by gall-inducing insects in a Mexican Tropical Dry Forest. Biotropica 38:107–115Google Scholar
  24. Cuevas-Reyes P, Oyama K, González-Rodríguez A, Fernandes GW, Mendoza-Cuenca L (2011) Contrasting herbivory patterns and leaf fluctuating asymmetry in Heliocarpus pallidus between different habitat types within a Mexican tropical dry forest. J Trop Ecol 27:383–391CrossRefGoogle Scholar
  25. Cuevas-Reyes P, Canché-Delgado A, Maldonado-López Y, Fernandes GW, Oyama K, Gonzalez-Rodríguez A (2018a) Patterns of herbivory and leaf morphology in two Mexican hybrid oak complexes: importance of fluctuating asymmetry as indicator of environmental stress in hybrid plants. Ecol Ind 90:164–170CrossRefGoogle Scholar
  26. Cuevas-Reyes P, Pereira GCN, Gélvez-Zuñiga I, Fernandes GW, Venancio H, Santos JC, Maldonado-López Y (2018b) Effects of ferric soils on arthropod abundance and herbivory on Tibouchina heteromalia (Melastomataceae): is fluctuating asymmetry a good indicator of environmental stress? Plant Ecol 219:69–78CrossRefGoogle Scholar
  27. Derroire G, Balvanera P, Castellanos-Castro C, Decocq G, Kennard DK, Lebrija-Trejos E, Tigabu M (2016) Resilience of tropical dry forests—a meta-analysis of changes in species diversity and composition during secondary succession. Oikos 125:1386–1397CrossRefGoogle Scholar
  28. Derroire G, Powers JS, Hulshof CM, Varela LEC, Healey JR (2018) Contrasting patterns of leaf trait variation among and within species during tropical dry forest succession in Costa Rica. Sci Rep 8:285CrossRefGoogle Scholar
  29. Domínguez CA, Dirzo R, Bullock SH (1989) On the function of floral nectar in Croton suberosus (Euphorbiaceae). Oikos 1989:109–114CrossRefGoogle Scholar
  30. Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE, Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursarand TA, Coley PD (2007) Host specificity of Lepidoptera in tropical and temperature forests. Nature 448:696–700CrossRefGoogle Scholar
  31. Fonseca MB, Silva JO, Falcão LA, Dupin MG, Melo GA, Espírito-Santo MM (2018) Leaf damage and functional traits along a successional gradient in Brazilian tropical dry forests. Plant Ecol 219:403–415CrossRefGoogle Scholar
  32. García-Oliva F, Camou A, Maass JM (2002) El clima de la región central de la costa del Pacífico mexicano. Hist Nat Cham 2002:3–10Google Scholar
  33. Gentry AH (1995) Diversity and floristics composition of Neotropical dry forests. In: Bullock SH, Mooney HA, Medina E (eds) Seasonally dry tropical forests. Cambridge University PressGoogle Scholar
  34. Jimenez-Rodríguez DL, Alvarez-Añorve MY, Pineda-Cortes M, Flores-Puerto JI, Benítez-Malvido J, Oyama K, Avila-Cabadilla LD (2018) Structural and functional traits predict short term response of tropical dry forests to a high intensity hurricane. For Ecol Manag 426:101–114CrossRefGoogle Scholar
  35. Kortbeek RW, van der Gragt M, Bleeker PM (2018) Endogenous plant metabolites against insects. Eur J Plant Pathol 2018:1–24Google Scholar
  36. Larcher W (1995) Photosynthesis as a tool for indicating temperature stress events. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis, vol 100. Springer, BerlinGoogle Scholar
  37. Lebrija-Trejos E, Bongers F, Pérez-García A, Meave J (2008) Successional change and resilience of a very dry tropical deciduous forest following shifting agriculture. Biotropica 40:422–431CrossRefGoogle Scholar
  38. Lebrija-Trejos E, Meave JA, Poorter L, Pérez-García EA, Bongers F (2010) Pathways, mechanisms and variability of tropical dry forest succession. Perspect Plant Ecol Evolut Syst 12:267–275CrossRefGoogle Scholar
  39. Lebrija-Trejos E, Pérez-García EA, Meave JA, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–489CrossRefGoogle Scholar
  40. Li C, Zhang X, Liu X, Luukkanen O, Berninger F (2006) Leaf morphological and physiological responses of Quercus aquifolioides along an altitudinal gradient. Silva Fennica 40:5–13CrossRefGoogle Scholar
  41. Lohbeck M, Poorter L, Lebrija-Trejos E, Martínez-Ramos M, Meave JA, Paz H, Pérez-García EA, Romero-Pérez EI, Tauro A, Bongers F (2013) Successional changes in functional composition contrast for dry and wet tropical forest. Ecology 94:1211–1216CrossRefGoogle Scholar
  42. Madeira BG, Espírito-Santo MM, Neto SDA, Nunes YR, Azofeifa GAS, Fernandes GW, Quesada M (2009) Changes in tree and liana communities along a successional gradient in a tropical dry forest in south-eastern Brazil. Forest ecology. Springer, Dordrecht, pp 291–304CrossRefGoogle Scholar
  43. Maldonado-López Y, Cuevas Reyes P, Sánchez Montoya G, Oyama K, Quesada M (2014) Growth, plant quality and leaf damage patterns in a dioecious tree species: is gender important? Arthropod Plant Interact 8:241–251Google Scholar
  44. Maldonado-López Y, Cuevas-Reyes P, Stone GN, Nieves-Aldrey JL, Oyama K (2015) Gall wasp community response to fragmentation of oak tree species: importance of fragment size and isolated trees. Ecosphere 6:1–15CrossRefGoogle Scholar
  45. Martínez-Gordillo M, Jiménez Ramírez J, Cruz Durán R, Juárez Arriaga E, García R, Cervantes A, Mejía-Hernández R (2002) Los géneros de la familia Euphorbiaceae en México (parte D). Anal Inst Biol Ser Bot 73:2Google Scholar
  46. Mayori A (2017) Ethnomedicinal uses and pharmacological activities of r Mull Arg: a systematic review. Trop J Pharm Res 16:2535–2543Google Scholar
  47. Miles L, Newton AC, De Fries RS, Ravilious C, May I, Blyth S, Kapos K, Gordon JE (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491–505CrossRefGoogle Scholar
  48. Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, UKGoogle Scholar
  49. Narbona E, Dirzo R (2010) A reassessment of the function of floral nectar in Croton suberosus (Euphorbiaceae): a reward for plant defenders and pollinators. Am J Bot 97:672–679CrossRefGoogle Scholar
  50. Neves FS, Silva JO, Espírito-Santo MM, Fernandes GW (2014) Insect herbivores and leaf damage along successional and vertical gradients in a tropical dry forest. Biotropica 46:14–24CrossRefGoogle Scholar
  51. Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  52. Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421CrossRefGoogle Scholar
  53. 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 24:329–336CrossRefGoogle Scholar
  54. Poorter L (2009) Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytol 181:890–900CrossRefGoogle Scholar
  55. Poorter L, Bongers F (2016) Biomass resilience of Neotropical secondary forests. Nature 530:211CrossRefGoogle Scholar
  56. Poorter L, van de Plassche M, Willems S, Boot RGA (2004) Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biol 6:746–754CrossRefGoogle Scholar
  57. Portillo-Quintero CA, Sánchez-Azofeifa GA (2010) Extent and conservation of tropical dry forests in the Americas. Biol Cons 143:144–155CrossRefGoogle Scholar
  58. Reich PB (2014) The world-wide ‘fast–slow’plant economics spectrum: a traits manifesto. J Ecol 102:275–301CrossRefGoogle Scholar
  59. Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleskyn J, Westoby M, Walters M (2003) The evolution of plant functional variations: traits, spectra and strategies. Int J Plant Sci 164:S143–S164CrossRefGoogle Scholar
  60. Rohlf FJ (1990) TpsDIG thin plate spline digitized landmark. Department of Ecology and Evolution, States University of New York, New YorkGoogle Scholar
  61. Royer DL, Wilf P, Janesko DA, Kowalski EA, Dilcher DL (2005) Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. Am J Bot 92:1141–1151CrossRefGoogle Scholar
  62. Royer DL, Meyerson LA, Robertson KM, Adams JM (2009) Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLoS One 4:e7653CrossRefGoogle Scholar
  63. Salatino A, Faria-Salatino ML, Negri G (2007) Traditional uses, chemistry and pharmacology of Croton species (Euphorbiaceae). J Braz Chem Soc 18:11–33CrossRefGoogle Scholar
  64. Sánchez-Azofeifa AG, Quesada M, Rodriguez JP, Nassar JM, Stoner KE, Castillo-Garvin AT, Zent EL, Calvo J, Kalacska M, Fajardo L, Gamon J, Cuevas-Reyes P (2005) Research priorities for neotropical dry forests. Biotropica 37:477–485Google Scholar
  65. Sánchez-Azofeifa GA, Quesada M, Cuevas-Reyes P, Castillo A, Sánchez-Montoya G (2009) Land cover and conservation in the area of influence of the Chamela-Cuixmala Biosphere Reserve, Mexico. For Ecol Manag 258:907–912CrossRefGoogle Scholar
  66. Sánchez-Azofeifa A, Powers JS, Fernandes GW, Quesada M (eds) (2013) Tropical dry forests in the americas: ecology, conservation, and management. CRC Press, Boca RatonGoogle Scholar
  67. Santos JC, Alves-Silva E, Cornelissen T, Fernandes GW (2013) The effect of fluctuating asymmetry and leaf nutrients on gall abundance and survivorship. Basic Appl Ecol 14:489–495CrossRefGoogle Scholar
  68. SAS (2000) Categorical data analysis using the SAS system. SAS Institute, Cary, pp 34–35Google Scholar
  69. Schöb C, Armas C, Guler M, Prieto I, Pugnaire FI (2013) Variability in functional traits mediates plant interactions along stress gradients. J Ecol 101:753–762CrossRefGoogle Scholar
  70. Silva JO, Espírito-Santo MM, Morais HC (2015) Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest. Basic Appl Ecol 16:210–219CrossRefGoogle Scholar
  71. Sokal RR, Crovello TJ, Unnasch RS (1986) Geographic variation of vegetative characters of Populus deltoides. Syst Bot 11:141–155CrossRefGoogle Scholar
  72. Somit D, Priyankar D, Kumar CT (2013) Quantification and correlation of the bioactive phytochemicals of Croton bonplandianum leaves of Sub-Himalayan region of West Bengal. Asian J Pharm Clin Res 6:142–147Google Scholar
  73. Souza GM, Ribeiro RV, Santos MG, Ribeiro HL, Oliveira RF (2004) Functional groups of forest succession as dissipative structures: an applied study. Br J Biol 64:707–718CrossRefGoogle Scholar
  74. Steinmann VW (2014) Croton lindquistii (Euphorbiaceae): a new arborescent species from western Mexico. Phytotaxa 166:235–240CrossRefGoogle Scholar
  75. Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 2nd edn. SAS, CaryGoogle Scholar
  76. Telhado C, Esteves D, Cornelissen T, Fernandes GW, Carneiro MAA (2010) Insect herbivores of Coccoloba cereifera do not select asymmetric plants. Environ Entomol 39:849–855CrossRefGoogle Scholar
  77. Telhado C, Silveira FA, Fernandes GW, Cornelissen T (2017) Fluctuating asymmetry in leaves and flowers of sympatric species in a tropical montane environment. Plant Species Biol 32:3–12CrossRefGoogle Scholar
  78. Uribe-Salas D, Saenz-Romero C, González-Rodríguez A, Tellez-Valdez O, Oyama K (2008) Foliar morphological variation in the white oak Quercus rugosa Née (Fagaceae) along a latitudinal gradient in Mexico: potential implications for management and conservation. For Ecol Manag 256:2121–2126CrossRefGoogle Scholar
  79. Vieira de Souza AV, de Britto D, dos Santos US, Bispo LD, Turatti ICC, Lopes NP, de Oliveira AP, Almeida JRGD (2017) Influence of season, drying temperature and extraction time on the yield and chemical composition of “marmeleiro” (Croton sonderianus) essential oil. J Essent Oil Res 29:76–84CrossRefGoogle Scholar
  80. Webster G, Del Arco-Aguilar D, Smith S (1996) Systematic distribution of foliar trichome types in Croton (Euphorbiaceae). Bot J Linn Soc 121:41–57Google Scholar
  81. Wen-Hui X, Wei-Y L, Qian L (2018) Chemical constituents from Croton species and their biological activities. Molecules 23:2333CrossRefGoogle Scholar
  82. Xu F, Guo W, Xu W, Wei Y, Wang R (2009) Leaf morphology correlates with water and light availability: ¿What consequences for simple and compound leaves? Prog Nat Sci 19:1789–1798Google Scholar
  83. Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27CrossRefGoogle Scholar

Copyright information

© International Society for Tropical Ecology 2019

Authors and Affiliations

  • José Gerardo González-Esquivel
    • 1
  • Pablo Cuevas-Reyes
    • 2
  • Antonio González-Rodríguez
    • 3
  • Luis Daniel Ávila-Cabadilla
    • 4
  • Mariana Yolotl Álvarez-Añorve
    • 4
  • Marcilio Fagundes
    • 5
  • Yurixhi Maldonado-López
    • 6
    Email author
  1. 1.Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Laboratorio de Ecología de InteraccionesUniversidad Michoacana de San Nicolás de Hidalgo, Ciudad UniversitariaMoreliaMexico
  3. 3.Laboratorio de Genética de la ConservaciónInstituto de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de MéxicoMoreliaMexico
  4. 4.Escuela Nacional de Estudios Superiores, Unidad Mérida, Universidad Nacional Autónoma de MéxicoMéridaMexico
  5. 5.Laboratório de Biologia da ConservaçãoDBG/CCBS, Universidade Estadual de Montes ClarosMontes ClarosBrazil
  6. 6.Cátedras CONACYT-Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de HidalgoMoreliaMexico

Personalised recommendations