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Insights into the Interaction between the Monophagous Tephritid Fly Anastrepha acris and its Highly Toxic Host Hippomane mancinella (Euphorbiaceae)

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Abstract

Despite their enormous economic importance and the fact that there are almost 5000 tephritid (Diptera) species, fruit fly – host plant interactions are poorly understood from a chemical perspective. We analyzed the interactions among Anastrepha acris (a little studied monophagous tephritid) and its highly toxic host plant Hippomane mancinella from chemical, ecological and experimental perspectives, and also searched for toxicants from H. mancinella in the larval-pupal endoparasitoid Doryctobracon areolatus. We identified 18 phenolic compounds from H. mancinella pulp belonging to different chemical groups including phenylpropanoids, flavonoids, chalcones and coumarins. No traces of Hippomanin A were detected in larvae, pupae or A. acris adults, or in D. areolatus adults, implying that A. acris larvae can metabolize this toxicant, that as a result does not reach the third trophic level. We tested the “behavioral preference – lack of larval specialization-hypothesis” via feeding experiments with a larval rearing medium containing H. mancinella fruit (skin + pulp or pulp alone). The high toxicity of H. mancinella was confirmed as only two (out of 2520 in three experiments) A. ludens larvae (a polyphagous pest species that preferentially feeds on plants within the Rutaceae) survived without reaching the adult stage when fed on media containing H. mancinella, whereas A. acris larvae developed well and produced healthy adults. Together, these findings open a window of opportunity to study the detoxification mechanisms used by tephritid fruit flies.

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References

  • Adolf W, Hecker E (1975) On the irritant and co-carcinogenic principles of Hippomane mancinella. Tetrahedron Lett 16:1587–1590

    Google Scholar 

  • Adolf W, Hecker E (1984) On the active principles of the spurge family, X. skin irritants, cocarcinogens, and cryptic cocarcinogens from the latex of the manchineel tree. J Nat Prod 47:482–496

    PubMed  CAS  Google Scholar 

  • Aguilera-Carbo A, Augur C, Prado-Barragan LA, Favela-Torres E, Aguilar CN (2008) Microbial production of ellagic acid and biodegradation of ellagitannins. Appl Microbiol Biotechnol 78:189–199

    PubMed  CAS  Google Scholar 

  • Aluja M (1994) Bionomics and management of Anastrepha. Annu Rev Entomol 39:155–178

    Google Scholar 

  • Aluja M, Norrbom AL (1999) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, FL

    Google Scholar 

  • Aluja M, Mangan RL (2008) Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annu Rev Entomol 53:473–502

    PubMed  CAS  Google Scholar 

  • Aluja M, Arredondo J, Díaz-Fleischer F, Birke A, Rull J, Niogret J, Epsky N (2014) Susceptibility of 15 mango (Sapindales: Anacardiaceae) cultivars to the attack by Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae) and the role of underdeveloped fruit as pest reservoirs: management implications. J Econ Entomol 107:375–388

    PubMed  CAS  Google Scholar 

  • Anderson MJ, Whitcomb PJ (2005) RSM simplified-optimizing processes using response surface methods for Design of Experiments. Productivity Inc., New York

    Google Scholar 

  • Astello-García MG, Cervantes I, Nair V, del Socorro S-DM, Reyes-Agüero A, Guéraud F, Negre-Salvayre A, Rossignol M, Cisneros-Zevallos L, Barba de la Rosa APB (2015) Chemical composition and phenolic compounds profile of cladodes from Opuntia spp. cultivars with different domestication gradient. J Food Compos Anal 43:119–130

    Google Scholar 

  • Becerra JX (2003) Synchronous coadaptation in an ancient case of herbivory. Proc Natl Acad Sci 100:12804–12807

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ben-Yosef M, Pasternak Z, Jurkevitch E, Yuval B (2015) Symbiotic bacteria enable olive fly larvae to overcome host defenses. R Soc Open Sci 2:150170

    PubMed  PubMed Central  Google Scholar 

  • Benelli G (2014) Aggressive behavior and territoriality in the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae): role of residence and time of day. J Insect Behav 27:145–161

    Google Scholar 

  • Bernays EA, Chamberlain DJ, Woodhead S (1983) Phenols as nutrients for a phytophagous insects Anacridium melanorhodon. J Insect Physiol 29:535–539

    CAS  Google Scholar 

  • Birke A, Aluja M, Greany P, Bigurra E, Pérez-Staples D, McDonald R (2006) Long aculeus and behavior of Anastrepha ludens render gibberellic acid ineffective as an agent to reduce ‘ruby red’ grapefruit susceptibility to the attack of this pestiferous fruit fly in commercial groves. J Econ Entomol 99:1184–1193

    PubMed  Google Scholar 

  • Birke A, Acosta E, Aluja M (2015) Limits to the host range of the highly polyphagous tephritid fruit fly Anastrepha ludens in its natural habitat. Bull Entomol Res 105:743–753

    PubMed  CAS  Google Scholar 

  • Birke A, Aluja M (2018) Do mothers really know best? Complexities in testing the preference-performance hypothesis in polyphagous frugivorous fruit flies. Bull Entomol Res 108:674–684

    PubMed  CAS  Google Scholar 

  • Blue LM, Sailing C, DeNapoles C, Fondots J, Johnson ES (2011) Manchineel dermatitis in north American students in the Caribbean. J Travel Med 18:422–424

    PubMed  Google Scholar 

  • Bower CR (1977) Inhibition of larval growth of the Queensland fruit fly, Dacus tryoni (Diptera: Tephritidae) in apples. Ann Entomol Soc Am 70:97–100

    Google Scholar 

  • Cherif M, Arfaoui A, Rhaiem A (2007) Phenolic compounds and their role in bio-control and resistance of chickpea to fungal pathogenic attacks. Tunis J Plant Prot 2:7–21

    Google Scholar 

  • Chown SL, Nicolson S (2004) Insect physiological ecology: mechanisms and patterns. Oxford University Press, New York

    Google Scholar 

  • Duffey SS, Stout MJ (1996) Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem 32:3–37

    CAS  Google Scholar 

  • Erbout N, De Meyer M, Vangestel C, Lens L (2009) Host plant toxicity affects developmental rates in a polyphagous fruit fly: experimental evidence. Biol J Linnean Soc 97:728–737

    Google Scholar 

  • Fernández-Yépez F (1953) Contribución al estudio de las moscas de las frutas del género Anastrepha Schiner (Diptera: Trypetidae) de Venezuela. En: II Congreso de Ciencias Naturales y Afines. Caracas, Venezuela 7:5–41

    Google Scholar 

  • Fitt GP (1984) Oviposition behaviour of two tephritid fruit flies, Dacus tryoni and Dacus jarvisi, as influenced by the presence of larvae in the host fruit. Oecologia 62:37–46

    PubMed  Google Scholar 

  • Fitt GP, O'Brien RW (1985) Bacteria associated with four species of Dacus (Diptera: Tephritidae) and their role in the nutrition of the larvae. Oecologia 67:447–454

    PubMed  Google Scholar 

  • Fitt GP (1986a) The influence of a shortage of hosts on the specificity of oviposition behaviour in species of Dacus (Diptera: Tephritidae). Physiol Entomol 11:133–143

    Google Scholar 

  • Fitt GP (1986b) The roles of adult and larval specializations in limiting the occurrence of five species of Dacus (Diptera: Tephritidae) in cultivated fruits. Oecologia 69:101–109

    PubMed  Google Scholar 

  • Fitt GP (1990) Comparative fecundity, clutch size, ovariole number and egg size of Dacus tryoni and D. jarvisi, and their relationship to body size. Entomol Exp Appl 55:11–21

    Google Scholar 

  • Guillén L, Aluja M, Rull J, Höhn H, Schwizer T, Samietz J (2011) Influence of walnut cultivar on infestation by Rhagoletis completa: behavioural and management implications. Entomol Exp Appl 140:207–217

    Google Scholar 

  • Guillén L, Adaime R, Birke A, Velázquez O, Angeles G, Ortega F, Ruiz E, Aluja M (2017) Effect of resin ducts and sap content on infestation and development of immature stages of Anastrepha obliqua and Anastrepha ludens (Diptera: Tephritidae) in four mango (Sapindales: Anacardiaceae) cultivars. J Econ Entomol 110:719–730

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Isman M (2002) Insect antifeedants. Pestic outlook 13:152–157

    CAS  Google Scholar 

  • Jácome I, Aluja M, Liedo P (1999) Impact of adult diet on demographic and population parameters of the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). Bull Entomol Res 89:165–175

    Google Scholar 

  • Joel DM (1978) The secretory ducts of mango fruits: a defense system effective against the Mediterranean fruit fly. Isr J Bot 27:44–45

    Google Scholar 

  • Juárez-Trujillo N, Monribot-Villanueva JL, Jiménez-Fernández V, Suárez-Montaño R, Aguilar-Colorado AS, Guerrero-Analco JA, Jiménez M (2018) Phytochemical characterization of Izote (Yucca elephantipes) flowers. J App Bot Food Qual 91:202–210

    Google Scholar 

  • Knaggs AR (2000) The biosynthesis of shikimate metabolites. Nat Prod Rep 17:269–292

    PubMed  CAS  Google Scholar 

  • Knaggs AR (2003) The biosynthesis of shikimate metabolites. Nat Prod Rep 20:119–136

    PubMed  CAS  Google Scholar 

  • Landolt PJ (1999) Behavior of flies in the genus Toxotrypana (Trypetinae: Toxotrypanini). In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, FL, pp 363–372

    Google Scholar 

  • Leow SS, Luu A, Shrestha S, Hayes KC, Sambanthamurthi R (2018) Drosophila larvae fed palm fruit juice (PFJ) delay pupation via expression regulation of hormetic stress response genes linked to ageing and longevity. Exp Gerontol 106:198–221

    PubMed  CAS  Google Scholar 

  • Liquido NJ, McQuate GT, Suiter KA, Norrbom AL, Yee WL, Chang CL (2019) Compendium of fruit fly host plant information. The USDA primary reference in establishing fruit fly regulated host plants. In: Pérez-Staples D, Díaz-Fleischer F, Montoya P, Vera MT (eds) Area-wide management of fruit fly pests. CRC Press, Boca Raton, pp 363–368

    Google Scholar 

  • López-Ortega M, Pérez-Rodríguez P, Rojas JC, Hernández RMS, López-Mata L, Rico-Gray V (2013) Host use and resource sharing by fruit/seed-infesting insects on Schoepfia schreberi (Olacaceae). Environ Entomol 42:231–239

    PubMed  Google Scholar 

  • López-Palacios C, Reyes-Agüero JA, Peña-Valdivia CB, Aguirre-Rivera JR (2019) Physical characteristics of fruits and seeds of Opuntia sp. as evidence of changes through domestication in the southern Mexican plateau. Genet Resour Crop Evol 66:349–362

    Google Scholar 

  • Luna-Ruiz JDJ, Nabhan GP, Aguilar-Melendez A (2018) Shifts in plant chemical defenses of Chile pepper (Capsicum annuum L.) due to domestication in Mesoamerica. Front Ecol Evol. https://doi.org/10.3389/fevo.2018.00048

  • Manuja R, Sachdeva S, Jain A, Chaudhary J (2013) A comprehensive review on biological activities of p-hydroxy benzoic acid and its derivatives. Int J Pharm Sci Rev Res 22:109–115

    Google Scholar 

  • Massei G, Hartley SE (2000) Disarmed by domestication? Induced responses to browsing in wild and cultivated olive. Oecologia 122:225–231

    PubMed  CAS  Google Scholar 

  • Merkl R, Hradkova I, Filip V, Smidrkal J (2010) Antimicrobial and antioxidant properties of phenolic acids alkyl esters. Czech J Food Sci 28:275–279

    CAS  Google Scholar 

  • Meyer RS, Whitaker BD, Little DP, Wu SB, Kennelly EJ, Long CL, Litt A (2015) Parallel reductions in phenolic constituents resulting from the domestication of eggplant. Phytochemistry 115:194–206

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Neuenschwander P (1982) Beneficial insects caught by yellow traps used in mass-trapping of the olive fly, Dacus oleae. Entomol Exp Appl 32:286–296

    Google Scholar 

  • Neuenschwander P, Michelakis S (1978) The infestation of Dacus oleae (Gmel.) (Diptera, Tephritidae) at harvest time and its influence on yield and quality of olive oil in Crete. J Appl Entomol 86:420–433

    Google Scholar 

  • Neuenschwander P, Michelakis S, Holloway P, Berchtol W (1985) Factors affecting the susceptibility of fruits of different olive varieties to attack by Dacus oleae (Gmel.) (Dipt., Tephritidae). J Appl Entomol 100:174–188

    CAS  Google Scholar 

  • Norrbom AL (2010) Tephritidae (Fruit flies, Moscas de las Frutas). In: Brown BV, Borkent A, Cumming JM, Wood DM, Woodley NE, Zumbado MA (eds) Manual of central American Diptera. NRC Research Press, Ottawa, pp 909–954

    Google Scholar 

  • Norrbom AL, Castillo-Meza AL, García-Chávez JH, Aluja M, Rull J (2014) A new species of Anastrepha (Diptera: Tephritidae) from Euphorbia tehuacana (Euphorbiaceae) in Mexico. Zootaxa 3780:567–576

    PubMed  Google Scholar 

  • Nunes BS, Carvalho FD, Guilhermino LM, Van Stappen G (2006) Use of the genus Artemia in ecotoxicity testing. Environ Pollut 144:453–462

    PubMed  CAS  Google Scholar 

  • Olivero-Verbel J, Güette-Fernandez J, Stashenko E (2009) Acute toxicity against Artemia franciscana of essential oils isolated from plants of the genus Lippia and Piper collected in Colombia. Bol Latinoam Caribe Pl Med Aromat 8:419–427

    CAS  Google Scholar 

  • Oroño L, Aluja M, Ovruski S, Rull J, Interdonato R, Prado FE, Hilal M (2019) Dynamics of soluble sugars and secondary metabolites in fruit of Juglans australis attacked by Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Arthropod-Plant Interact 13:411–421

    Google Scholar 

  • Papanastasiou SA, Bali EMD, Ioannou CS, Papachristos DP, Zarpas KD, Papadopoulos NT (2017) Toxic and hormetic-like effects of three components of citrus essential oils on adult Mediterranean fruit flies (Ceratitis capitata). PLoS One 12:e0177837

    PubMed  PubMed Central  Google Scholar 

  • Pascacio-Villafán C, Williams T, Sivinski J, Birke A, Aluja M (2015) Costly nutritious diets do not necessarily translate into better performance of artificially reared fruit flies (Diptera: Tephritidae). J Econ Entomol 108:53–59

    PubMed  PubMed Central  Google Scholar 

  • Pitts JF, Barker NH, Gibbons DC, Jay J (1993) Manchineel keratoconjunctivitis. Br J Ophthalmol 77:284–288

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pree DJ (1977) Resistance to development of larvae of the apple maggot in crab apples. J Econ Entomol 70:611–614

    CAS  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna

    Google Scholar 

  • Rao KV (1974) Toxic principles of Hippomane mancinella I. Planta Med 25:166–171

    PubMed  CAS  Google Scholar 

  • Rao KV (1977) Toxic principles of Hippomane mancinella. II Structure of Hippomanin A Lloydia 40:169–172

    PubMed  CAS  Google Scholar 

  • Rashmi MA, Verghese A, Shivashankar S, Chakravarthy AK, Sumathi M, Kandakoor S (2017) Does change in tannin content in mango (Mangifera indica) fruits influence the extent of fruit fly (Bactrocera dorsalis Hendel) herbivory? J Entomol Zool Stud 5:381–385

    Google Scholar 

  • Reissig WH, Brown SK, Lamb RC, Cummins JN (1990) Laboratory and field studies of resistance of crab apple clones to Rhagoletis pomonella (Diptera: Tephritidae). Environ Entomol 19:565–572

    Google Scholar 

  • Saha T, Nithya C (2016) Encyclopaedia of fruit flies. Write & Print Publications, New Delhi

    Google Scholar 

  • Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis-modulation by salt stress in rice seedlings. Plant Sci 171:263–270

    CAS  Google Scholar 

  • Schaeffer HJ, Lauter WM, Foote PA (1954) A preliminary phytochemical study of Hippomane mancinella. J Am Pharm Assoc 43:43–45

    CAS  Google Scholar 

  • Simmonds MS (2001) Importance of flavonoids in insect–plant interactions: feeding and oviposition. Phytochem 56:245–252

    CAS  Google Scholar 

  • Solinas M, Rebora M, De Cristofaro A (2016) Functional morphology of Bactrocera oleae Gmel. (Diptera: Tephritidae) tarsal chemosensilla involved in interactions with the host-plant. Entomologica 35:103–123

    Google Scholar 

  • Styer SC, Greany PD (1983) Increased susceptibility of laboratory-reared vs. wild Caribbean fruit fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae), larvae to toxic citrus allelochemics. Environ Entomol 12:1606–1608

    Google Scholar 

  • Vattem DA, Shetty K (2005) Biological functionality of ellagic acid: a review. J Food Biochem 29:234–266

    CAS  Google Scholar 

  • Veberic R, Jurhar J, Mikulic-Petkovsek M, Stampar F, Schmitzer V (2010) Comparative study of primary and secondary metabolites in 11 cultivars of persimmon fruit (Diospyros kaki L.). Food Chem 119:477–483

    CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    PubMed  PubMed Central  Google Scholar 

  • Widhalm JR, Dudareva N (2015) A familiar ring to it: biosynthesis of plant benzoic acids. Mol Plant 8:83–97

    PubMed  CAS  Google Scholar 

  • White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. CAB International, Wallingford

    Google Scholar 

  • Wolfe K, Xianzhong W, Rui Hai L (2003) Antioxidant activity of apple peels. J Agric Food Chem 51:609–614

    PubMed  CAS  Google Scholar 

  • Wu K, Zhang J, Zhang Q, Zhu S, Shao Q, Clark KD, Liu Y, Ling E (2015) Plant phenolics are detoxified by prophenoloxidase in the insect gut. Sci Rep 5:16823. https://doi.org/10.1038/srep16823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zunjarrao SS, Tellis MB, Joshi SN, Joshi RS (2019) Plant-insect interaction: the saga of molecular coevolution. In: Merillon JM, Ramawat KG (eds) Co-evolution of secondary metabolites, Springer, Switzerland, pp 1–27

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Acknowledgements

We are grateful to Nicole M. van Dam, Associate Editor of the Journal of Chemical Ecology who handled the initial part of the refereeing process of this manuscript providing many important suggestions for improvement and also shared links containing practical advice on scientific manuscript writing. The final part of the refereeing process was handled by Editor-in-Chief, Gary W. Felton, and we also thank him for many valuable suggestions for improvement and for seeking the opinion of two additional referees. We gratefully acknowledge the important contributions of six anonymous referees, who provided many specific suggestions for improvement and the meticulous revision by the native English speaker Dr. Trevor Williams, who significantly improved the usage of the foreign language. We thank Gabriel A. Hernández-Velázquez, Adriana Santos-Ramiro and Uriel Gallardo Valencia (INECOL) for technical assistance. This work was partially financially by the Asociación de Productores y Empacadores Exportadores de Aguacate de México (Project APEAM-INECOL 41010 to M.A.). Additional funding was provided by the Mexican Campaña Nacional contra Moscas de la Fruta (DGSV-SENASICA-SAGARPA) through the Consejo Nacional Consultivo Fitosanitario (CONACOFI), the MIT-Veracruz Fund, (both to M.A), and the Instituto de Ecología, A.C. (INECOL).

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  1. Instituto de Ecología, A.C. - INECOL, Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic®, Carretera antigua a Coatepec 351, 91073, Xalapa, Veracruz, Mexico

    Martín Aluja, Carlos Pascacio-Villafán, Alma Altúzar-Molina, Erick Enciso, Rafael Ortega, Emilio Acosta & Larissa Guillén

  2. Instituto de Ecología, A.C. – INECOL, Red de Estudios Moleculares Avanzados, Clúster Científico y Tecnológico BioMimic®, Carretera antigua a Coatepec 351, 91073, Xalapa, Veracruz, Mexico

    Juan Monribot-Villanueva & José A. Guerrero-Analco

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  1. Martín Aluja
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Aluja, M., Pascacio-Villafán, C., Altúzar-Molina, A. et al. Insights into the Interaction between the Monophagous Tephritid Fly Anastrepha acris and its Highly Toxic Host Hippomane mancinella (Euphorbiaceae). J Chem Ecol 46, 430–441 (2020). https://doi.org/10.1007/s10886-020-01164-8

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