Advertisement

Leaf herbivory modulates fruit trait correlations within individual plants

  • Mariana Valoy
  • Juan Carlos López-Acosta
  • Silvia Lomáscolo
  • Facundo Bernacki
  • Omar Varela
  • Mariano OrdanoEmail author
Original Paper

Abstract

Plant performance is based on the relationship between resource acquisition and allocation to complete essential functions. Herbivory causes compromises in resource allocation that impact at the plant and within-plant (sub-individual) levels. This impacts fruit display traits which in turn affect reproductive success and seed dispersal. Because leaf damage affects resource allocation, herbivory should modulate the relationship between fruit display traits. We explore the relation between the level of leaf herbivory (mean damage and coefficient of variation) and fruit display traits in Vassobia breviflora (Solanaceae). According to trait function, we explore relationships between reproductive traits (seed number and weight), reward traits (sugar concentration, pulp weight), and relationships between reproductive and reward traits. We found no effect of herbivory on the correlation between reproductive traits, but an effect was found on the correlation between rewards traits. In conclusion, herbivory affects the correlation between fruit traits, and the magnitude and direction of the association between traits vary according to the magnitude and variation of the damage at the within-plant level. In evolutionary terms, our results suggest that within-plant variation in leaf traits would constitute a strategy to resolve allocation conflicts derived from damage and to maintain fruit display characteristics that favor the interaction with seed dispersers.

Keywords

Foliar damage Insect herbivores Plant resources Fruit trait correlations Evolutionary ecology 

Notes

Acknowledgements

The authors would like to thank Martín Portal and Plásticos La Rioja. This study was partially funded by Fundación Miguel Lillo (Ministry of Education) and National Council for Scientific and Technical Research (CONICET) of Argentina (PIP 11420110100395 given to M. Ordano).

Supplementary material

11829_2020_9740_MOESM1_ESM.r (11 kb)
Supplementary file1 (R 11 kb)
11829_2020_9740_MOESM2_ESM.docx (556 kb)
Supplementary file2 (DOCX 556 kb)
11829_2020_9740_MOESM3_ESM.xls (26 kb)
Supplementary file3 (XLS 26 kb)
11829_2020_9740_MOESM4_ESM.xls (480 kb)
Supplementary file4 (XLS 480 kb)
11829_2020_9740_MOESM5_ESM.xls (162 kb)
Supplementary file5 (XLS 161 kb)

References

  1. Agrawal AA, Lau A, Hambäck PA (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Q Rev Biol 81:349–376PubMedCrossRefPubMedCentralGoogle Scholar
  2. Anton AM, Zuloaga FO (2013) Recuperado de. https://www.floraargentina.edu.ar/
  3. Arceo-Gómez G, Vargas CF, Parra-Tabla V (2017) Selection on intra-individual variation in stigma-anther distance in the tropical tree Ipomoea wolcottiana (Convolvulaceae). Plant Biol 19:454–459PubMedCrossRefPubMedCentralGoogle Scholar
  4. Armbruster WS, Schwaegerle KE (1996) Causes of covariation of phenotypic traits among populations. J Evol Biol 9:261–276CrossRefGoogle Scholar
  5. Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145CrossRefGoogle Scholar
  6. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defense. Bioscience 37:58–67CrossRefGoogle Scholar
  7. Bernacki FG (2014) Biología floral y frutal de Vassobia breviflora (Sedtn.) Hunz. (Solanaceae) en el noroeste argentino (Tesis de licenciatura). Universidad Nacional de Tucumán, Argentina.Google Scholar
  8. Bernacki FG, Albornoz P, Valoy M, Ordano M (2015) Anatomía de flor y fruto de Vassobia breviflora (Solanaceae) en el sur de las Yungas Australes (Argentina). Phyton 82:478–487Google Scholar
  9. Bianchi AR, Yáñez CE (1992) Las precipitaciones en el Noroeste Argentino, (segunda edición). INTA, EEA, SaltaGoogle Scholar
  10. Bihmidine S, Hunter CT, Johns CE, Koch KE, Braun DM (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci 4:177PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu Rev Ecol Evol Syst 16:363–392CrossRefGoogle Scholar
  12. Brancalion PHS, Rodrigues RR (2014) Seed size-number trade-off in Euterpe edulis in plant communities of the atlantic forest. Sci Agric 71:226–231CrossRefGoogle Scholar
  13. Brennan EB, Weinbaum SA, Rosenheim JA, Karban R (2001) Heteroblasty in Eucalyptus globulus (Myricales: Myricaceae) affects ovipositonal and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera: Psyllidae). Environ Entomol 30:1144–1149CrossRefGoogle Scholar
  14. Cabrera AL (1979) Solanaceae. In: Burkart A (ed) Flora ilustrada de entre ríos V Buenos Aires (Argentina). Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, pp 346–452Google Scholar
  15. Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytol 197:576–585PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  17. de Santillán AS, de Santamarina EB, Ricci TR, Würschmidt EJ (1967) La región de las sierras del nordeste de la provincia de Tucumán. Universidad Nacional de Tucumán, TucumánGoogle Scholar
  18. de Vries J, Evers JB, Dicke M, Poelman EH (2019) Ecological interactions shape the adaptive value of plant defence: herbivore attack versus competition for light. Funct Ecol 33:129–138PubMedCrossRefPubMedCentralGoogle Scholar
  19. Digilio AP, Legname PR (1966) Los árboles indígenas de la provincia de Tucumán. Opera Lilloana 15:1–107Google Scholar
  20. Erb M (2018) Plant defenses against herbivory: closing the fitness gap. Trends Plant Sci 23:187–194PubMedCrossRefPubMedCentralGoogle Scholar
  21. Eriksson O (1999) Seed size variation and its effects on germination and seedling performance in the clonal herb Convallaria majalis. Acta Oecol 20:61–66CrossRefGoogle Scholar
  22. Esteve-Altava B (2017) In search of morphological modules: a systematic review. Biol Rev 92:1332–1347PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fenner M (1992) Environmental influences on seed size and composition. Hortic Rev 13:183–213Google Scholar
  24. Fornoni J, Núñez-Farfán J, Valverde PL, Rausher MD (2004) Evolution of mixed strategies of plant defense allocation against natural enemies. Evolution 58:1685–1695PubMedCrossRefPubMedCentralGoogle Scholar
  25. Gómez JM (2003) Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. Am Nat 162:242–256PubMedCrossRefPubMedCentralGoogle Scholar
  26. Harper DGC (2006) Maynard Smith: amplifying the reasons for signal reliability. J Theor Biol 239:203–209PubMedCrossRefPubMedCentralGoogle Scholar
  27. Harper JL, Lovell PH, Moore KG (1970) The shapes and sizes of seeds. Annu Rev Ecol Syst 1:327–356CrossRefGoogle Scholar
  28. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  29. Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuate. I. Large-scale changes in the accumulation of growth-and defense-related plant mRNAs. Plant Physiol 125:683–700PubMedPubMedCentralCrossRefGoogle Scholar
  30. Herrera CM (2009) Multiplicity in unity: plant subindividual variation and interaction with animals. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  31. Herrera CM (2017) The ecology of subindividual variability in plants: patterns, processes, and prospects. Web Ecol 17:51–64CrossRefGoogle Scholar
  32. Honêk A, Martinková Z (2002) Factors of between—and within—plant distribution of Metopolophium dirhodum (Homoptera: Aphididae) on small grain cereals. J Appl Entomol 126:378–383CrossRefGoogle Scholar
  33. Horvitz CC, Schemske DW (2002) Effects of plant size, leaf herbivory, local competition and fruit production on survival, growth and future reproduction of a neotropical herb. J Ecol 90:279–290CrossRefGoogle Scholar
  34. Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287PubMedPubMedCentralCrossRefGoogle Scholar
  35. Irwin RE, Adler LS (2006) Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant. Am J Bot 93:64–72CrossRefGoogle Scholar
  36. Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54:687–708CrossRefGoogle Scholar
  37. Jordano P (1995) Frugivore-mediated selection on fruit and seed size: birds and St. Lucie's cherry Prunus mahaleb. Ecology 76:2627–2639CrossRefGoogle Scholar
  38. Junker RR, Kuppler J, Amo L, Blande JD, Borges RM, van Dam NM et al (2017) Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and ecoevolutionary implications. New Phytol.  https://doi.org/10.1111/nph.14505 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  40. Koenig WD, Knops JM, Carmen WJ, Sage RD (2009) No trade-off between seed size and number in the valley oak Quercus lobata. Am Nat 173:682–688PubMedCrossRefPubMedCentralGoogle Scholar
  41. Lázaro A, Larrinaga AR (2018) A multi-level test of the seed number/size trade-off in two Scandinavian communities. PLoS ONE 13:e0201175PubMedPubMedCentralCrossRefGoogle Scholar
  42. Lehtilä K, Strauss SY (1999) Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. Ecology 80:116–124CrossRefGoogle Scholar
  43. Lomáscolo SB, Levey DJ, Kimball RT, Bolker BM, Halborn HT (2010) Dipersers shape fruit diversity in Ficus (Moraceae). PNAS 107:14668–14672PubMedCrossRefPubMedCentralGoogle Scholar
  44. Matilla A, Gallardo M, Puga-Hermida MI (2005) Structural, physiological and molecular aspects of heterogeneity in seeds: a review. Seed Sci Res 15:63–76CrossRefGoogle Scholar
  45. Mauricio R (2000) Natural selection and the joint evolution of tolerance and resistance as plant defenses. Evol Ecol 14:491–507CrossRefGoogle Scholar
  46. Meyer ST, Roces F, Wirth R (2006) Selecting the drought stressed: effects of plant stress on intraspecific and within-plant herbivory patterns of the leafcutting ant Atta colombica. Funct Ecol 20:973–981CrossRefGoogle Scholar
  47. Minetti JL, Poblete GA, Longhi F (2005) Los mesoclimas del Noroeste Argentino. In: Minetti JL (ed) El Clima del Noreste Argentino. Laboratorio Climatológico Sudamericano, Fundación Carl C, Zon Caldenius, pp 217–234Google Scholar
  48. Murray KG (1987) Selection for optimal fruit-crop size in bird-dispersed plants. Am Nat 129:18–31CrossRefGoogle Scholar
  49. Murren CJ (2002) Phenotypic integration in plants. Plant Species Biol 17:89–99CrossRefGoogle Scholar
  50. Murren CJ, Julliard R, Schlichting CD, Clobert J (2001) Dispersal, individual phenotype, and phenotypic plasticity. In: Clobert J, Danchin E, Dhondt AA, Nichols J (eds) Dispersal. Oxford University Press, Oxford, pp 261–272Google Scholar
  51. Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566CrossRefGoogle Scholar
  52. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  53. Ordano M, Blendinger PG, Lomáscolo SB, Chacoff NP, Sánchez MS, Núñez Montellano MG, Jiménez J, Ruggera R, Valoy M (2017) The role of trait combination in the conspicuousness of fruit display among bird dispersed plants. Funct Ecol 31:1718–1727CrossRefGoogle Scholar
  54. Palacio FX, Ordano M (2018) The strength and drivers of bird-mediated selection on fruit crop size: a meta-analysis. Front Ecol Evol.  https://doi.org/10.3389/fevo.2018.00018 CrossRefGoogle Scholar
  55. Palacio FX, Lacoretz M, Ordano M (2014) Bird-mediated selection on fruit display traits in Celtis ehrenbergiana (Cannabaceae). Evol Ecol Res 16:51–62Google Scholar
  56. Palacio FX, Valoy M, Bernacki FG, Sánchez MS, Núñez-Montellano MG, Varela O, Ordano M (2017) Bird fruit consumption results from the interaction between fruit-handling behaviour and fruit crop size. Ethol Ecol Evol 29:24–37CrossRefGoogle Scholar
  57. Pérez Miranda C (2003). Tucumán y los Recursos Naturales. Biodiversidad. Los recursos silvestres, los ambientes naturales y las áreas protegidas. Gobierno de la Provincia de Tucumán, EPDA PROSAP, Programa de Servicios agrícolas provinciales Bifronte SRL. Buenos Aires, pp 408Google Scholar
  58. Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett 6:265–272CrossRefGoogle Scholar
  59. Pigliucci M, Preston K (2004) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, New YorkGoogle Scholar
  60. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2003) Effects of below-and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135:601–605PubMedCrossRefPubMedCentralGoogle Scholar
  61. R Development Core Team (2019) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna. https://www.R-project.org
  62. Rasband W (1997) ImageJ 1.4. NIH, BethesdaGoogle Scholar
  63. Redman AM, Cipollini DF, Schultz JC (2001) Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126:380–385PubMedCrossRefPubMedCentralGoogle Scholar
  64. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New YorkGoogle Scholar
  65. Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665PubMedCrossRefPubMedCentralGoogle Scholar
  67. Saint-Hilaire EG (1818) Philosophie anatomique. JB. Bailliere, ParisGoogle Scholar
  68. Sánchez-Humanes B, Sork VL, Espelta JM (2011) Trade-offs between vegetative growth and acorn production in Quercus lobata during a mast year: the relevance of crop size and hierarchical level within the canopy. Oecologia 166:101–110PubMedCrossRefPubMedCentralGoogle Scholar
  69. Schaefer HM, Schaefer V, Levey DJ (2004) How plant–animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584CrossRefGoogle Scholar
  70. Schlinkert H, Westphal C, Clough Y, Grass I, Helmerichs J, Tscharntke T (2016) Plant size affects mutualistic and antagonistic interactions and reproductive success across 21 Brassicaceae species. Ecosphere 7:e01529CrossRefGoogle Scholar
  71. Schultz JC, Appel HM, Ferrieri A, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4:324PubMedPubMedCentralCrossRefGoogle Scholar
  72. Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851PubMedPubMedCentralCrossRefGoogle Scholar
  73. Shelton AL (2004) Variation in chemical defenses of plants may improve the effectiveness of defense. Evol Ecol Res 6:709–726Google Scholar
  74. Snow DW (1971) Evolutionary aspects of fruit eating by birds. IBIS 113:194–202CrossRefGoogle Scholar
  75. Sobral MA, Larrinaga AR, Guitián J (2010) Do seed-dispersing birds exert selection on optimal plant trait combinations? Correlated phenotypic selection on the fruit and seed size of hawthorn (Crataegus monogyna). Evol Ecol 24:1277–1290CrossRefGoogle Scholar
  76. Sobral M, Guitián J, Guitián P, Larrinaga AR (2013) Selective pressure along a latitudinal gradient affects subindividual variation in plants. PLoS ONE 8:e74356PubMedPubMedCentralCrossRefGoogle Scholar
  77. Sobral M, Guitián J, Guitián P, Violle C, Larrinaga AR (2019) Exploring subindividual variability: role of ontogeny, abiotic environment and seed dispersing birds. Plant Biol 21(4):688–694PubMedCrossRefPubMedCentralGoogle Scholar
  78. Stephens AE, Westoby M (2015) Effects of insect attack to stems on plant survival, growth, reproduction and photosynthesis. Oikos 124:266–273CrossRefGoogle Scholar
  79. Steppuhn A, Baldwin IT (2008) Induced defenses and the cost-benefit paradigm. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Berlin, pp 61–68CrossRefGoogle Scholar
  80. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedCrossRefPubMedCentralGoogle Scholar
  81. Strauss SY, Armbruster WS (1997) Linking herbivory and pollination-new perspectives on plant and animal ecology and evolution. Ecology 78:1617–1618Google Scholar
  82. Taura HM, Laroca S (2004) Biologia da polinização: interações entre as abelhas (Hym., Apoidea) e as flores de Vassobia breviflora (Solanaceae) [Pollination biology: interactions between bees and flowers of Vassobia breviflora (Solanaceae)]. Acta Biol Parana 33:143–162Google Scholar
  83. Torices R, Méndez M (2014) Resource allocation to inflorescence components is highly integrated despite differences between allocation currencies and sites. Int J Plant Sci 175:713–723CrossRefGoogle Scholar
  84. Valido A, Schaefer HM, Jordano P (2011) Colour, design and reward: phenotypic integration of fleshy fruit displays. J Evol Biol 24:751–760PubMedCrossRefPubMedCentralGoogle Scholar
  85. Valoy M, Ordano M, Bernacki F, Palacio FX, López-Acosta JC, Varela O (2018) Patrones de herbivoría en Vassobia breviflora (Solanaceae): variación en el daño foliar y selección natural mediada por herbívoros. Rev Biol Trop 66:1683–1700CrossRefGoogle Scholar
  86. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142CrossRefGoogle Scholar
  87. Vaughton G, Ramsey M (1998) Sources and consequences of seed mass variation in Banksia marginata (Proteaceae). J Ecol 86:563–573CrossRefGoogle Scholar
  88. Vaughton G, Ramsey M (2001) Relationships between seed mass, seed nutrients, and seedling growth in Banksia cunninghamii (Proteaceae). Int J Plant Sci 162:599–606CrossRefGoogle Scholar
  89. Volis S (2016) Seed heteromorphism in Triticum dicoccoides: association between seed positions within a dispersal unit and dormancy. Oecologia 181:401–412PubMedCrossRefGoogle Scholar
  90. Weiner J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Syst 6:207–215CrossRefGoogle Scholar
  91. Wenk EH, Falster DS (2015) Quantifying and understanding reproductive allocation schedules in plants. Ecol Evol 5:5521–5538PubMedPubMedCentralCrossRefGoogle Scholar
  92. Whippo CW, Hangarter RP (2009) The “sensational” power of movement in plants: a Darwinian system for studying the evolution of behavior. Am J Bot 96:2115–2127PubMedCrossRefPubMedCentralGoogle Scholar
  93. Winn AA (1996) The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. J Evol Biol 9:737–752CrossRefGoogle Scholar
  94. Zhou S, Lou YR, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–1498PubMedPubMedCentralGoogle Scholar
  95. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects modelling for nested data. Mixed effects models and extensions in ecology with R. Springer, New York, pp 101–142CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  1. 1.Fundación Miguel LilloSan Miguel de TucumánArgentina
  2. 2.Centro de Investigaciones TropicalesUniversidad Veracruzana XalapaVeracruzMéxico
  3. 3.Instituto de Ecología RegionalUniversidad Nacional de Tucumán, and Consejo Nacional de Investigaciones científicas y Técnicas (CONICET)Yerba BuenaArgentina
  4. 4.Instituto de Ambientes de Montañas y Regiones ÁridasUniversidad Nacional de Chilecito (UNdeC)ChilecitoArgentina
  5. 5.Fundación Miguel Lillo and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)San Miguel de TucumánArgentina

Personalised recommendations