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Ants visiting extrafloral nectaries and pyrrolizidine alkaloids may shape how a specialist herbivore feeds on its host plants

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Abstract

The presence of extrafloral nectaries (EFNs) attracts predators and parasitoids, and protects the plant against herbivorous insects. By improving plant defences, EFNs reduce the fitness of herbivores. The use of similar host plants with no EFNs or adaptations in response to predators and parasitoids may enhance herbivore fitness. In this context, we studied the feeding habit (on leaves or on unripe seeds inside the pods) of larvae of the specialist moth Utetheisa ornatrix in two Crotalaria host plant species in which EFNs are present (C. micans) or absent (C. paulina). We hypothesized that the moths’ feeding habit was influenced by its natural enemies via their presence on EFNs. In C. micans, we found more larvae feeding inside the pods rather than on the leaves, while in C. paulina, larvae were found in both parts of the plant. There was greater activity of natural enemies in C. micans than in C. paulina. The moth sequesters enough pyrrolizidine alkaloid (PAs) to defend against predators in the leaves and seeds of C. paulina, but only in seeds of C. micans. Therefore, a change in the feeding habit in U. ornatrix larvae is a plastic response that depends on whether EFNs are present or not, or whether PA concentrations are low or high. This change does not affect overall moth performance. However, other factors, such as pod hardness, predation by organisms other than those visiting EFNs or even parasitoids cannot be ruled out as being responsible for the change in feeding habit. To date, both the EFNs and PAs in Crotalaria species are a parsimonious explanation of how larvae of U. ornatrix use different species of Crotalaria for feeding.

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References

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Clancy KM, Price PW (1987) Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68:736–738

    Article  Google Scholar 

  • Cogni R, Trigo JR, Futuyma D (2012) A free lunch? No cost for acquiring defensive plant pyrrolizidine alkaloids in a specialist arctiid moth (Utetheisa ornatrix). Mol Ecol 21:6152–6162

    Article  CAS  PubMed  Google Scholar 

  • Conner WE, Jordan AT (2009) From armaments to ornaments: the relationship between chemical defense and sex in tiger moths. In: Conner WE (ed) Tiger moths and woolly bears. Behavior, ecology, and evolution of the Arctiidae. Oxford University Press, New York, pp 152–155

    Google Scholar 

  • Cuautle M, Rico-Gray V (2003) The effect of wasps and ants on the reproductive success of the extrafloral nectaried plant Turnera ulmifolia (Turneraceae). Func Ecol 17:417–423

    Article  Google Scholar 

  • Da Costa MA (2010) Phylogeny of Utetheisa s. str. (Lepidoptera: Noctuidae: Arctinae) with comments on the evolution of colour, hind wing scales and origin of new world species. Invert Syst 24:113–130

    Article  Google Scholar 

  • Díaz-Castelazo C, Rico-Gray V, Ortega F, Ángeles G (2005) Morphological and secretory characterization of extrafloral nectaries in plants of coastal Veracruz, Mexico. Ann Bot 96:1175–1189

    Article  PubMed  PubMed Central  Google Scholar 

  • Eisner T, Meinwald J (1995) The chemistry of sexual selection. Proc Natl Acad Sci USA 92:50–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferro VG, Guimarães PR, Trigo JR (2006) Why do larvae of Utetheisa ornatrix penetrate and feed in pods of Crotalaria species? Larval performance vs. chemical and physical constraints. Entomol Exp Appl 121:23–29

    Article  Google Scholar 

  • Flores AS (2004) Taxonomia, números cromossômicos e química de espécies de Crotalaria L. (Leguminosae-Papilionoideae) no Brasil. Dr. Sc. Thesis, Universidade Estadual de Campinas, Campinas, São Paulo, Brasil

  • Flores AS, Tozzi AMGA, Trigo JR (2009) Pyrrolizidine alkaloid profiles in Crotalaria species from Brazil: chemotaxonomic significance. Biochem Syst Ecol 37:459–469

    Article  CAS  Google Scholar 

  • Freitas AVL, Oliveira PS (1996) Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. J Anim Ecol 65:205–210

    Article  Google Scholar 

  • Guimarães PR, Raimundo LG, Bottcher C, Silva RR, Trigo JR (2006) Extrafloral nectaries as a deterrent mechanism against seed predators in the chemically protected weed Crotalaria pallida (Leguminosae). Austral Ecol 31:776–782

    Article  Google Scholar 

  • Heidel-Fischer HM, Vogel H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci 8:8–14

    Article  Google Scholar 

  • Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2015) Extrafloral nectar at the plant-insect interface: A spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu Rev Entomol 60:213–232

    Article  CAS  PubMed  Google Scholar 

  • Iyengar VK, Rossini C, Hoebeke ER, Conner WE, Eisner T (1999) First record of the parasitoid Archytasa terrimus (Diptera: Tachinidae) from Utetheisa ornatrix (Lepidoptera: Arctiidae). Entomol News 110:144–146

    Google Scholar 

  • Jung S, Rickerta DA, Deaka NA, Aldina ED, Recknorc J, Johnson LA, Murphy PA (2003) Comparison of Kjeldahl and Dumas methods for determining protein contents of soybean products. J Am Oil Chem Soc 80:1169–1173

    Article  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced response to herbivory. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Boulder

    Google Scholar 

  • le Roux MM, Boatwright JS, van Wyk B-E (2013) A global infrageneric classification system for the genus Crotalaria (Leguminosae) based on molecular and morphological evidence. Taxon 62:957–971

    Article  Google Scholar 

  • Marquis RJ (1992) Selective impact of herbivores. In: Fritz RS, Simms EW (eds) Ecology and plant resistance to herbivores and pathogens. University of Chicago Press, Chicago, pp 301–325

  • Martins CHZ, Cunha BP, Solferini VN, Trigo JR (2015) Feeding on host plants with different concentrations and structures of pyrrolizidine alkaloids impacts the chemical-defense effectiveness of a specialist herbivore. PLoS One 10:e0141480

    Article  PubMed  PubMed Central  Google Scholar 

  • Massuda KF, Trigo JR (2014) Hiding in plain sight: Cuticular compound profile matching conceals a larval tortoise beetle in its host chemical cloud. J Chem Ecol 40:341–354

    Article  CAS  PubMed  Google Scholar 

  • Mathews CR, Bottrell DG, Brown MW (2011) Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on peach (Rosales: Rosaceae). Environ Entomol 40:42–51

    Article  PubMed  Google Scholar 

  • Mccullagh P, Nelder JA (1989) Generalized linear models. 2nd edn. Chapman and Hall, London

    Book  Google Scholar 

  • Melo Y, Machado SR, Alves M (2010) Anatomy of extrafloral nectaries in Fabaceae from dry-seasonal forest in Brazil. Bot J Linn Soc 163:87–98

    Article  Google Scholar 

  • Miller JS, Feeny P (1983) Effects of benzylisoquinoline alkaloids on the larvae of polyphagous Lepidoptera. Oecologia 58:332–339

    Article  PubMed  Google Scholar 

  • Mithöfer A, Boland W (2012) Plant defense against herbivores: Chemical aspects. Annu Rev Plant Biol 63:431–450

    Article  PubMed  Google Scholar 

  • 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 97:672–679

    Article  PubMed  Google Scholar 

  • Pemberton RW (1993) Observations of extrafloral nectar feeding by predaceous and fungivorous mites. Proc Entomol Soc Wash 95:642–643

    Google Scholar 

  • Pemberton RW, Lee JH (1996) The influence of extrafloral nectaries on parasitism of an insect herbivore. Am J Bot 83:1187–1194

    Article  Google Scholar 

  • Pereira MF, Trigo JR (2013) Ants have a negative rather than a positive effect on extrafloral nectaried Crotalaria pallida performance. Acta Oecol 51:49–53

    Article  Google Scholar 

  • Polhill RM (1982) Crotalaria in Africa and Madagascar. AA Balkema, Rotterdam

    Google Scholar 

  • Rehr SS, Feeny PP, Janzen DH (1973) Chemical defence in Central American non-ant-acacias. J Anim Ecol 42:405–416

    Article  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Romero GQ, Koricheva J (2011) Contrasting cascade effects of carnivores on plant fitness: a meta-analysis. J Anim Ecol 80:696–704

    Article  PubMed  Google Scholar 

  • Rossini C, Hoebeke ER, Iyengar VK, Conner WE, Eisner M, Eisner T (2000) Alkaloid content of parasitoids reared from pupae of an alkaloid-sequestering arctiid moth (Utetheisa ornatrix). Entomol News 111:287–290

    Google Scholar 

  • Sendoya SF, Freitas AVL, Oliveira PS (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am Nat 174:134–140

    Article  PubMed  Google Scholar 

  • Singer MS (2008) Evolutionary ecology of polyphagy. In: Tilmon K (ed) Specialization, speciation, and radiation-evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp. 29–42

    Google Scholar 

  • Singer MS, Carriere Y, Theuring C, Hartmann T (2004a) Disentangling food quality from resistance against parasitoids: diet choice by a generalist caterpillar. Am Nat 164:423–429

    Article  PubMed  Google Scholar 

  • Singer MS, Rodrigues D, Stireman JO III, Carrriere Y (2004b) Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology 85:2727–2753

    Article  Google Scholar 

  • Slansky F (1993) Nutritional ecology: the fundamental quest for nutrients. In: Stamp NE, Casey TM (eds) Caterpillars. Ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 29–91

    Google Scholar 

  • Sourakov A (2015) You are what you eat: native versus exotic Crotalaria species (Fabaceae) as host plants of the Ornate Bella Moth, Utetheisa ornatrix (Lepidoptera: Erebidae: Arctiinae). J Nat Hist 49:2397–2415

    Article  Google Scholar 

  • Sourakov A, Locascio LM (2013) Exotic Crotalaria species (Fabales: Fabaceae) as host plants of the Ornate Bella Moth, Utetheisa ornatrix (Lepidoptera: Erebidae), in Florida: laboratory biology. Fla Entomol 96:344–350

    Article  Google Scholar 

  • Statsoft, inc. (2004) Statistica (data analysis software system), version 7. http://www.statsoft.com

  • Thompson JN (1994) The coevolutionary process. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98

    Article  CAS  Google Scholar 

  • Whitehead SR, Reid E, Sapp J, Poveda K, Royer AM, Posto AL, Kessler A (2014) A specialist herbivore uses chemical camouflage to overcome the defenses of an ant plant mutualism. PLoS One 9:e102604

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams IS (1999) Slow growth, high mortality. A general hypothesis, or is it? Ecol Entomol 24:490–495

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgements

We acknowledge Andréia Silva Flores for identifying the Crotalaria species, and José Carlos da Silva and Daniela Rodrigues for helping with the plant and moth rearing. Lucas Kaminski and two anonymous reviewers made valuable comments in an early draft of the manuscript. We thank Espaço da Escrita—Coordenadoria Geral da Universidade—UNICAMP—for the language services provided. Financial support was provided by FAPESP (2011/17708-0) and CNPq (306103/2013-3) to JRT, and by FAPESP (2013/15612-1) to CHZM.

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  1. Laboratório de Ecologia Química, Departamento de Biologia Animal, Instituto de Biologia, Unicamp, Caixa Postal 6109, Campinas, São Paulo, 13083-970, Brazil

    Alexandre Eduardo Magalhães, Carlos Henrique Zanini Martins, Diomar Verçosa, Kamila Ferreira Massuda & José Roberto Trigo

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  1. Alexandre Eduardo Magalhães
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  2. Carlos Henrique Zanini Martins
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  3. Diomar Verçosa
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  4. Kamila Ferreira Massuda
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  5. José Roberto Trigo
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Correspondence to José Roberto Trigo.

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Magalhães, A.E., Martins, C.H.Z., Verçosa, D. et al. Ants visiting extrafloral nectaries and pyrrolizidine alkaloids may shape how a specialist herbivore feeds on its host plants. Arthropod-Plant Interactions 11, 629–639 (2017). https://doi.org/10.1007/s11829-017-9510-z

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