Abstract
Domestication is predicted to reduce resistance of agricultural crops against insect herbivores; however, its impact on herbivores with different feeding modes and evolutionary histories needs investigation. To this end, we conducted greenhouse experiments to explore the effects of domestication of blueberries (Vaccinium corymbosum), a crop native to North America, on the performance of two chewing herbivores [the native Sparganothis fruitworm (Sparganothis sulfureana (Clemens)) and non-native gypsy moth (Lymantria dispar L.)], and one piercing-sucking herbivore [the blueberry aphid (Illinoia azaleae (Mason))]. Lymantria dispar performed better (i.e., larvae gained more mass, damaged more leaves, and had greater survival) on cultivated V. corymbosum than on its wild counterpart. In contrast, domestication had no impact on the native S. sulfureana larval mass, consumption, and survivorship. Domestication increased survivorship, but not offspring production, of the aphid I. azaleae. To examine changes in plant chemistry due to domestication, we measured phenolic and nutrient (macro- and micro-elements) content in wild and cultivated V. corymbosum leaves. Although there were no differences in total phenolic content, two compounds were absent, while two were at lower and one at higher concentration in domesticated than in wild plants. Wild V. corymbosum leaves had higher amounts of phosphorus, sulfur, and sodium than cultivated leaves; the opposite was found for aluminum. While our findings provide support for the ‘plant domestication-reduced defense’ hypothesis, the effects of domestication were dependent on feeding modes and adaptations of the herbivores such that the non-native chewing species was more positively affected than the chewing and the piercing-sucking natives.
Similar content being viewed by others
References
AphID (2018) Illinoia azaleae. http://aphid.aphidnet.org/Illinoia_azaleae.php. Accessed 16 Jan 2018
Astello-Garcia MG, Cervantes I, Nair V et al (2015) Chemical composition and phenolic compounds profile of cladodes from Opuntia spp. cultivars with different domestication gradient. J Food Compos Anal 43:119–130
Averill AL, Sylvia MM (1998) Cranberry insects of the northeast. University of Massachusetts Cranberry Experiment Sta, Wareham
Beninger CW, Abou-Zaid MM (1997) Flavonol glycosides from four pine species that inhibit early instar gypsy moth (Lepidoptera: Lymantriidae) development. Biochem Syst Ecol 25:505–512
Benrey B, Denno RF (1997) The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999
Benrey B, Callejas A, Rios L, Oyama K, Denno RF (1998) The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol Control 11:130–140
Bunea A, Rugină DO, Pintea AM, Sconta Z, Bunea CI, Socaciu C (2011) Comparative polyphenolic content and antioxidant activities of some wild and cultivated blueberries from Romania. Not Bot Horti Agrobo 39:70–76
Chacón-Fuentes M, Parra L, Rodriguez-Saona C, Seguel I, Ceballos R, Quiroz A (2015) Domestication in murtilla (Ugni molinae) reduced defensive flavonol levels but increased resistance against a native herbivorous insect. Environ Entomol 44:627–637
Chen YH, Gols R, Benrey B (2015a) Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol 60:35–58
Chen YH, Gols R, Stratton CA, Brevik KA, Benrey B (2015b) Complex tritrophic interactions in response to crop domestication: predictions from the wild. Entomol Exp Appl 157:40–59
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti-herbivore defence. Sci 230:895–899
Coville FV (1937) Improving the wild blueberry. Yearbook of Agriculture, United States United States Government Printing Office, Washington DC, pp 559–574
de Lange ES, Balmer D, Mauch-Mani B, Turlings TCJ (2014) Insect and pathogen attack and resistance in maize and its wild ancestors, the teosintes. New Phytol 204:329–341
Doane CC, McManus ML (1981) The gypsy moth: research toward integrated pest management. U.S.D.A. Forest Service Technical Bulletin 1584, Washington, DC
Eck P, Childers NF (1966) The blueberry industry. In: Eck P, Childers NF (eds) Blueberry culture. Rutgers University Press, New Brunswick, pp 3–13
Evans LT (1993) Crop evolution, adaptation and yield. Cambridge University Press, Cambridge
Gaillard MDP, Glauser G, Robert CAM, Turlings TCJ (2018) Fine-tuning the ‘plant-domestication-reduced defense’ hypothesis: specialist vs generalist herbivores. New Phytol 217:355–366
García-Palacios P, Milla R, Delgado-Baquerizo M et al (2013) Side-effects of plant domestication: ecosystem impacts of changes in litter quality. New Phytol 198:504–513
Gepts P (2010) Crop domestication as a long-term selection experiment. In: Janick J (ed) Plant breeding reviews. John Wiley & Sons Inc., Hoboken, pp 1–44
Giese RL, Schneider ML (1979) Cartographic comparison of Eurasian gypsy moth distribution (Lymantria dispar L.; Lepidoptera: Lymantriidae). Entomol News 90:1–16
Giovanelli G, Buratti S (2009) Comparison of polyphenolic composition and antioxidant activity of wild Italian blueberries and some cultivated varieties. Food Chem 112:903–908
Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J Chem Ecol 34:132–143
Hancock J (2001) Blueberry characteristics range among the varieties. The Fruit Growers News, May Issue, pp 36–37
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Horneck DA, Miller RO (1998) Determination of total nitrogen in plant tissue. In: Kalra YP (ed) Handbook and reference methods for plant analysis. CRC Press, New York, pp 75–83
Huang C-Y, Schulte EE (1985) Digestion of plant tissue for analysis by ICP emission spectroscopy. Commun Soil Sci Plant Anal 16:943–958
Kennedy GG, Barbour JD (1992) Resistance variation in natural and managed systems. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 13–41
Lindroth RL, Weisbrod AV (1991) Genetic variation in response of the gypsy moth to aspen phenolic glycosides. Biochem Syst Ecol 19:97–103
López-Uribe MM, Cane JH, Minckley RL, Danforth BN (2016) Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proc R Soc B 283:20160443. https://doi.org/10.1098/rspb.2016.0443
Macfadyen S, Bohan DA (2010) Crop domestication and the disruption of species interactions. Basic Appl Ecol 11:116–125
Magnoler A (1970) Susceptibility of gypsy moth larvae to Lymantria spp. nuclear-and cytoplasmic-polyhedrosis viruses. Entomophaga 15:407–412
Marucci PE (1953) The Sparganothis fruitworm in New Jersey. Am Cranberry Growers’ Ass Proc 83:6–13
Maxwell FG, Jenninggs PE (1980) Breeding plants resistant to insects. John Wiley & Sons Inc., New York
McCormick J (1998) The vegetation of the New Jersey pine barrens. In: Forman RTT (ed) Pine barrens: ecosystem and landscape. Rutgers University Press, New Brunsiwck, pp 229–243
Mikulic-Petkovsek M, Slatnar A, Stampar F, Veberic R (2012) HPLC-MSn identification and quantification of flavonol glycosides in 28 wild and cultivated berry species. Food Chem 135:2138–2146
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450
Moreira, X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol 35:112–123
Peng S, Cassman KG, Virmani SS, Sheehy J, Khush GS (1999) Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Sci 39:1552–1559
Polashock JJ, Caruso FL, Averill AL, Schilder AC (2017) Compendium of blueberry, cranberry, and lingonberry diseases and pests, 2nd edn. APS Press, St. Paul
Ranger CM, Johnson-Cicalese J, Polavarapu S, Vorsa N (2006) Evaluation of Vaccinium spp. for Illinoia pepperi (Hemiptera: Aphididae) performance and phenolic content. J Econ Entomol 99:1474–1482
Ranger CM, Singh AP, Johnson-Cicalese J, Polavarapu S, Vorsa N (2007) Intraspecific variation in aphid resistance and constitutive phenolics exhibited by the wild blueberry Vaccinium darrowi. J Chem Ecol 33:711–729
Rhoades RD (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DA, Applebaum SW (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 1–55
Rivera M, Rodriguez-Saona CR, Jennings DE, Koppenhoffer AM (2015) Assessing the impact of cultivation and plant domestication of highbush blueberry (Vaccinium corymbosum) on soil properties and associated plant-parasitic nematode communities. Soil Biol Biochem 88:25–28
Rodriguez-Saona C, Vorsa N, Singh AP et al (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J Exp Bot 62:2633–2644
Rosenthal JP, Dirzo R (1997) Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives. Evol Ecol 11:337–355
Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338
Sellappan S, Akoh C, Krewer G (2002) Phenolic compounds and antioxidant capacity of Georgia-grown blueberries and blackberries. J Agric Food Chem 50:2432–2438
Turcotte M, Turley NE, Johnson MTJ (2014) The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events. New Phytol 204:671–681
Wang SY, Chen CT, Wang CY (2009) Composition of phenolic compounds and antioxidant activity in the leaves of blueberry cultivars. Food Chem 112:676–684
Waterhouse AL (2002) Determination of total phenolics. In: Wrolstad RE, Acree TE, Decker EA et al. (eds) Current protocols in food analytical chemistry. Wiley, New York, pp. I1.1.1–I1.1.8
Whitehead SR, Turcotte MM, Poveda K (2016) Domestication impacts on plant-herbivore interactions: a meta-analysis. Phil Trans R Soc 372:1–9
Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233
Acknowledgements
We thank Matthew Strom, Gabrielle Pintauro, Mara Schiffhauer, Andrew Lux, and Sarah Ongaro for their assistance in the laboratory, greenhouse, and field, and the growers who provided field sites for this research. We thank Dr. Elvira de Lange and an anonymous reviewer for helpful editorial comments on an earlier draft. Funds for this study were partially provided by the New Jersey Blueberry/Cranberry Research Council and the hatch project NJ08192 to C.R-S.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Gimme Walter.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hernandez-Cumplido, J., Giusti, M.M., Zhou, Y. et al. Testing the ‘plant domestication-reduced defense’ hypothesis in blueberries: the role of herbivore identity. Arthropod-Plant Interactions 12, 483–493 (2018). https://doi.org/10.1007/s11829-018-9605-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-018-9605-1