Abstract
The leaves of Piper nigrum L. (Piperaceae) were evaluated for chemical constituents and mosquito larvicidal activity against the larvae of Aedes aegypti. GC and GC–MS analyses revealed that the crude extracts contain 16 compounds. Thymol (20.77 %) and ç-elemene (10.42 %) were identified as the major constituents followed by cyclohexene, 4-ethenyl-4-methyl-3-(1-methylethenyl)-1-(1 methylethyl)-, (3R-trans) (7.58 %), 4,6-octadienoic acid, 2-acetyl-2-methyl-, ethyl ester (6.98), 2(3H)-furanone, 3,4-bis(1,3-benzodioxol-5-ylmethyl) dihydro-, (3R-trans) (6.95 %), 1-naphthalenol, 1,2,3,4,4a,7,8,8a-octahydro-1,6-dimethyl-4-(1-methylethyl)-, [1R-(1à,4á,4aá,8aá)]-(Cedreanol) (5.30 %), trans-2-undecen-1-ol (4.48 %), phytol (4.22 %), 1,6-cyclodecadiene, 1-methyl-5-methylene-8-(1-methylethyl)-,[s-(E,E)] (3.78 %) and 2,6-dimethyl-3,5,7-octatriene-2-ol, Z,Z (2.39 %). Larval mortality was observed after 3 h of exposure period. The crude extract showed remarkable larvicidal activity against Ae. aegypti (LC50 = 34.97). The larvae of Ae. aegypti exposed to the P. nigrum, significantly reduced the activities of α- and β-carboxylesterases and superdioxide. Further, P. nigrum extract was severely affecting the mosquito gut cellular organelles. Based on the results, the chemical constituents of crude extracts of P. nigrum can be considered as a new source of larvicide for the control of Ae. aegypti.
Similar content being viewed by others
References
Abbotts WS (1925) A method for computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Agra-Neto AC, Napoleão TH, Pontual EV, Santos NDL, Luz LA, Oliveira CMF, Melo-Santos MAV, Coelho LCBB, Navarro DMAF, Paiva PMG (2015) Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res 113:175–184
Ahmad S (1976) Larval and adult housefly carboxylesterase: isozymic composition and tissue pattern. Insect Biochem 6:541–547
Ahmad S, Forgash AJ (1976) Nonoxidative enzymes in the metabolism of insecticides. Drug Metab Rev 5:141–164
Amer A, Mehlhorn H (2006a) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Amer A, Mehlhorn H (2006b) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490
Amer A, Mehlhorn H (2006c) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477
Bagheri H, Manap MYBA, Solati Z (2014) Antioxidant activity of Piper nigrum L. essential oil extracted by supercritical CO2 extraction and hydro-distillation. Talanta 121:220–228
Benelli G (2015) Research in mosquito control: current challenges for a brighter future. Parasitol Res. doi:10.1007/s00436-015-4586-9
Boll PM, Parmar VS, Tyagi OD, Prasad A, Wengel J, Olseng CE (1994) Some recent isolation studies from potential insecticidal Piper species. Pure Appl Chem 66:2339–2342
Carvalho AFU, Melo VMM, Craveiro AA, Machado MIL, Bantim MB, Rabelo EF (2003) Larvicidal activity of the essential oil from Lippia sidoides Cham. against Aedes aegypti Linn. Mem Inst Oswaldo Cruz, Rio de Janeiro 98:569–571
Chaithong U, Choochote W, Kamsuk K, Jitpakdi A, Tippawangkosol P, Chaiyasit D, Champakaew D, Tuetun B, Pitasawat B (2006) Larvicidal effect of pepper plants on Aedes aegypti (L.) (Diptera: Culicidae). J Vector Ecol 31:138–144
Chansang U, Zahiri NS, Bansiddhi J, Boonruad T, Thongsrirak P, Mingmuang J, Benjapong N, Mulla MS (2005) Mosquito larvicidal activity of aqueous extracts of long pepper (Piper retrofractum Vahl) from Thailand. J Vector Ecol 30:195–200
Cheng S, Liu J, Tsai K, Chen W, Chang S (2004) Chemical composition and mosquito larvicidal activity of essential oils from leaves of different Cinnamomum osmophloeum provenances. J Agric Food Chem 52:4395–4400
Choochote W, Chaithong U, Kamsuk K, Rattanachanpichai E, Jitpakdi A, Tippawangkosol P, Chaiyasit D, Champakaew D, Tuetun B, Pitasawat B (2006) Adulticidal activity against Aedes (Stegomyia aegypti) (Diptera: Culicidae) of three Piper spp. Rev Inst Med Trop Sao Paulo 48(1):33–37
de Morais SM, Facundo VA, Bertini LM, Cavalcanti ESB, Anjos Júnior JF, Ferreira SA, Brito ES, Souza Neto MA (2007) Chemical composition and larvicidal activity of essential oils from Piper species. Biochem Syst Ecol 35:670–675
Devine GJ, Furlong MJ (2007) Insecticide use: contexts and ecological consequences. Agri Human Values 24(3):281–306
Facundo VA, Silveira ASP, Morais SM (2005) Constituents of Piper alatabacum Trel and Yuncker (Piperaceae). Biochem Syst Ecol 33:753–756
Fazal NAH, Abbasi BH, Farooq S, Ali M, Khan MA (2012) Biological role of Piper nigrum L. (Black pepper): a review. Asian Pac J Trop Biomed 1945–1953
He W, Huang B (2011) A review of chemistry and bioactivities of a medicinal spice: Foeniculum vulgare. J Med Plants Res 5:3595–3600
Hemingway J, Karunaratne SH (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol 12(1):1–12
Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391
Jagadeshwaran U, Vijayan VA (2009) Biochemical characterization of deltamethrin resistance in a laboratory-selected strain of Aedes aegypti. Parasitol Res 104:1431–1438
Kalaivani K, Senthil-Nathan S, Murugesan AG (2012) Biological activity of selected Lamiaceae and Zingiberaceae plant essential oils against the dengue vector Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 110:1261–1268
Kapin MA, Ahmad S (1980) Esterases in larval tissues of gypsy moth, Lymantria dispar (L.): optimum assay conditions, quantification and characterization. Insect Biochem 10(3):331–337
Koodalingam A, Mullainadhan P, Arumugam M (2011) Effects of extract of soapnut Sapindus emarginatus on esterases and phosphatases of the vector mosquito, Aedes aegypti (Diptera: Culicidae). Acta Trop 118(1):27–36
Laranja AT, Manzatto AJ, Campos-Bicudo HEM (2003) Effects of caffeine and used coffee grounds on biological features of Aedes aegypti (Diptera, Culicidae) and their possible use in alternative control. Genet Mole Biol 26(4):419–429
Lassiter MT, Apperson CS, Roe RM (1996) Juvenile hormone metabolism in the ovary, gut, head and carcass after blood feeding in the southern house mosquito, Culex quinquefasciatus. Comp Biochem Physiol B Biochem Mol Biol 113:229–237
Lee SE (2000) Mosquito larvicidal activity of pipernonaline a piperidine alkaloid derived from long pepper Piper longum. J Am Mosq Contr Assoc 16:245–247
Lee HS (2005) Pesticidal constituents derived from Piperaceae fruits. Agric Chem Biotechnol 48(2):65–74
Lee CH, Sung BK, Lee HS (2006) Acaricidal activity of fennel seed oils and their main components against Tyrophagus putrescentiae, a stored-food mite. J Stored Prod Res 42:8–14
Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara L, Somboon P, Lycett G, Ranson H (2011) The role of the Aedes aegypti Epsilon glutathione transferases in conferring. Insect Biochem Mol Biol 41:203–209
Macedo MLR, Freire MGM, Silva MBR, Coelho LCBB (2007) Insecticidal action of Bauhinia monandra leaf lectin (BmoLL) against Anagasta kuehniella (Lepidoptera: Pyralidae), Zabrotes subfasciatus, and Callosobruchus maculatus (Coleoptera: Bruchidae). Comp Biochem Physiol A 146:486–498
Madhu SK, Vijayan VA, Shaukath AK (2011) Bioactivity guided isolation of mosquito larvicide from Piper longum. Asian Pacific J Trop Med 4(2):112–116
Mann RS, Kaufman PE (2012) Natural product pesticides: their development, delivery vectors. Mini Rev Org Chem 9:185–202
Marcombe S, Poupardin R, Darriet F, Reynaud S, Bonnet J, Strode C, Brengues C, Yebakima A, Ranson H, Corbel V, David JP (2009) Exploring the molecular basis of insecticide resistance in the dengue vector Aedes aegypti: a case study in Martinique Island (French West Indies). BMC Genomics 10(494):1–14
Menon AN (2000) Insecticidal unsaturated isobutylamides from natural plant products to agrochemical leads. In: Arnason, J.T., Philogene, B.J.R., Morand, P. (Ed.). ACS Symposium Series Washington, D.C. J Med Aromat Plant Sci 185–190
Milam CD, Farris JL, Wilhide JD (2000) Evaluating mosquito control pesticides for effect on target and non-target organisms. Arch Environ Contam Toxicol 39:324–328
Miyakado M, Nakayama I, Ohno N (1989) International unsaturated isobutylamides. From natural products to agrochemical leads. In insecticides of plant origin. ACS symposium series 387. American Chemical Society, Washington, DC, pp 173–187
Napoleão TH, Pontual EV, Lima TA, Santos NDL, Sá RA, Coelho LCBB, Navarro DMAF, Paiva PMG (2012) Effect of Myracrodruon urundeuva leaf lectin on survival and digestive enzymes of Aedes aegypti larvae. Parasitol Res 110:609–616
Narayana DBA, Brindavanam NB, Dobriyal RM, Katiyar KC (2000) Indian spices: an overview with special reference to nutraceuticals. J Med Arom Plant Sci 22:236–246
Navickiene HMD, Ale’ cio AC, Kato MJ, Bolzani VS, Young MCM, Cavalheiro AJ, Furlan M (2000) Antifungal amides from Piper hispidum and Piper tuberculatum. Phytochemistry 55:621–626
Nawaz R, Rathor RH, Bilal H, Hassan SA, Khan AI (2011) Adulticidal activity of Olea vera, Linum usitatissimum and Piper nigera against Anopheles stephensi and Aedes aegypti under laboratory conditions. Iran J Arth Dis 5:2–9
Nivsarkar M, Kumar GP, Laloraya M, Laloraya MM (1991) Superoxide dismutase in the anal gills of the mosquito larvae of Aedes aegypti : its inhibition by alpha-terthienyl. Arch Insect Biochem Physiol 16:249–255
Park IK, Lee SG, Shin SC, Park JD, Ahn YJ (2002a) Larvicidal activity of isobutylamides identified in Piper nigrum fruits against three mosquito species. J Agric Food Chem 50:1866–1870
Park IK, Lee SG, Shin SC, Park JD, Ahn YJ (2002b) Larvicidal activity of isobutylamides identified in Piper nigrum fruits against three mosquito species. J Agri Food Chem 50(7):1866–1870
Parmar VS, Jain SC, Bisht KS, Jain R, Taneja P, Jhe A, Tyagi OD, Prasad AK, Wengel J, Olsen CE, Boll PM (1997) Phytochemistry of the genus piper. Phytochemistry 46:567–673
Parmar VS, Jain SC, Gupta S, Talwar S, Rajwanshi VK, Kumar R, Azim A, Malhotra S, Kumar N, Jain R, Sharama NK, Tyagi OW, Lawrie SJ, Errington W, Howarth OW, Olsen CE, Singh SK, Wengel J (1998) Polyphenols and alkaloids from Piper species. Phytochemistry 49:1069–1078
Parthasarathy U, Asish GR, Zacharia TJ, Saji KV, Johson KG, Jayarajan K, Mathew PA, Parthasarathy VA (2008) Spatial influence on the important volite oils of Piper nigrum leaves. Cur Sci 94:1632–1635
Pradeepa V, Sathish-Narayanan S, Kirubakaran SA, Senthil-Nathan S (2014) Antimalarial efficacy of dynamic compound of plumbagin chemical constituent from Plumbago zeylanica Lin (Plumbaginaceae) against the malarial vector Anopheles stephensi Liston (Diptera: Culicidae). Parasitol Res 113(8):3105–3109
Pradeepa V, Sathish-Narayanan S, Kirubakaran SA, Thanigaivel A, Senthil-Nathan S (2015) Toxicity of aristolochic acids isolated from Aristolochia indica Linn (Aristolochiaceae) against the malarial vector Anopheles stephensi Liston (Diptera: Culicidae). Exp Parasitol 153:8–16
Rana IS, Rana AS (2012) Efficacy of essential oils of aromatic plants as larvicide for the management of filarial vector Culex quinquefasciatus Say (Diptera:Culicidae) with special reference to Foeniculum vulgare. Asian Pac J Trop Dis 184–189
Revathi K, Chandrasekaran R, Thanigaivel A, Kirubakaran SA, Senthil-Nathan S (2013) Effects of Bacillus subtilis metabolites on larval Aedes aegypti L. Pest Biochem Physiol 107(2):250–257
Rodriguez MM, Bisset J, De Fernandez DM, Lauzan L, Soca A (2001) Detection of insecticide resistance in Aedes aegypti (Diptera: Culicidae) from Cuba and Venezuela. J Med Entomol 38(5):623–628
Scott I, Jensen H, Philog’ene B, Arnason J (2008) A review of Piper spp. (Piperaceae) phytochemistry, insecticidal activity and mode of action. Phytochem Rev 7:65–75
Senthilkumar A, Jayaraman M, Venkatesalu V (2013) Chemical constituents and larvicidal potential of Feronia limonia leaf essential oil against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Parasitol Res 112:1337–1342
Senthil-Nathan S (2007) The use of eucalyptus leaf extract as a natural larvicidal agent against malarial vector Anopheles stephensi Liston (Diptera: Culicidae). Biores Technol 98(9):1856–1860
Senthil-Nathan S (2013) Physiological and biochemical effect of Neem and other Meliaceae plants secondary metabolites against Lepidopteran insects. Front Physiol 4(359):1–17
Senthil-Nathan S (2015) A review of biopesticides and their mode of action against insect pests, In: Environmental Sustainability-Role of green technologies, Springer-Verlag, pp 49–63
Senthil-Nathan S, Kalaivani K (2005) Combined effects of azadirachtin and nucleopolyhedrovirus (SpltNPV) on Spodoptera litura Fabricius (Lepidoptera: Noctuidae) larvae. Biol Control 36(1):94–104
Senthil-Nathan S, Kalaivani K (2006) Efficacy of nucleopolyhedrovirus (NPV) and azadirachtin on Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Biol Control 34(1):93–98
Senthil-Nathan S, Kalaivani K, Murugan K, Chung PG (2005) Effects of neem limonoids on the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Acta Trop 96(1):47–55
Senthil-Nathan S, Kalaivani K, Sehoon K (2006) Effects of Dysoxylum malabaricum Bedd. (Meliaceae) extract on the malarial vector Anopheles stephensi Liston (Diptera: Culicidaae). Biores Technol 97(16):2077–2083
Senthil-Nathan S, Choi MY, Paik CH, Seo HY (2007) Food consumption, utilization, and detoxification enzyme activity of the rice leaffolder larvae after treatment with Dysoxylum triterpenes. Pest Biochem Physiol 88(3):260–267
Senthil-Nathan S, Choi MY, Paik CH, Seo HY, Kalivani K, Kim JD (2008) Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown planthopper Nilaparvata lugens (Stal). Ecotoxicol Environ Saf 70:244–250
Shanmugapriya K (2012) Antioxitent potential of pepper (P. nigrum) leaves and its microbial potential against some pathogenic microbes. Indian J Nat Prod Resour 3:570–577
Siddique BS, Gulzar T, Mahmood A, Begum S, Khan B, Afshan F (2004) New insecticidal amides from petroleum ether extract of dried Piper nigrum L. whole fruits. Chem Pharm Bull 52:1349–1352
Siddique BS, Gulzar T, Mahmood A, Begum S, Khan B, Afshan F (2005) Insecticidal amides from fruits of Piper nigrum Linn. Nat Prod Res 19:143–150
Škrinjarić-Špoljar M, Matthews HB, Engel JL, Casida JE (1971) Response of hepatic microsomal mixed-function oxidases to various types of insecticide chemical synergists administered to mice. Biochem Pharmacol 20(7):1607–1618
Sumathykutty MA, Rao JM, Padmakumari KP, Narayanan CS (1999) Essential oil constituents of some Piper species. Flavour Fragr J 14:279–282
Thanigaivel A, Chandarasekaran R, Revathi K, Nisha S, Kirubakaran SA, Sathish-Narayanan S, Senthil-Nathan S (2012) Larvicidal efficacy of Adhatoda vasica (L.) Nees against the bancroftian filariasis vector Culex quinquefasciatus Say and dengue vector Aedes aegypti L. in vitro condition. Parasitol Res 110:1993–1999
Traboulsi AF, El-Haj S, Tuene M, Taoubi K, Nader NA, Mrad A (2005) Repellency and toxicity of aromatic plant extracts against the mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Manag Sci 61:597–604
Tripathi AKJ, Kumar S (1996) Secondary metabolites and their biological and medicinal activities of Piper species plants. J Med Aromat Plt Sci 18:302–321
Urich K (1994) Comparative animal biochemistry. Springer, Berlin, p 782
van Asperen A (1962) Study of housefly esterases by means of a sensitive colorimetric method. J Insect Physiol 8:401–416
Vasilakis N, Shell EJ, Fokam EB, Mason PW, Hanley KA, Estes DM, Weaver SC (2007) Potential of ancestral sylvatic dengue-2 viruses to re-emerge. Virol J 358:402–412
Vogel A (1978) A text book of quantitative inorganic analysis including instrumental analysis. Longman, London and New York, pp 69–74
Waliwitiya R, Nicholson RA, Kennedy CJ, Lowenberger CA (2012) The synergistic effects of insecticidal essential oils and piperonyl butoxide on biotransformational enzyme activities in Aedes aegypti (Diptera: Culicidae). J Med Entomol 49:14–23
Walter K, Schütt C (1974) Phosphatases. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic, New York, pp 856–870
Wheelock CE, Shan G, Ottea J (2005) Overview of carboxylesterase and their role in the metabolism of insecticides. J Pestic Sci 30:75–83
Wirth MC, Georghiou GP (1999) Selection and characterization of temephos resistance in a population of Aedes aegypti from Tortola. British Virgin Islands. J Am Mosq Control Assoc 15(3):315–320
World Health Organisation (1981) Instruction for determining the susceptibility or resistance of mosquito larvae to insecticides. WHOVBC 81(807):1–6
World Health Organization (1992) Vector resistance to pesticides. Fifteenth report of the WHO expert committee on vector biology and control. WHO technical report, Geneva
World Health Organization (2015) Dengue and severe dengue fact sheet N°117. World malaria report. WHO, National Press Club in Washington, Washington, DC
Yang YC, Lee SG, Lee HK, Kim MK, Lee SH, Lee HS (2002) A piperidine amide extracted from Piper longum L. fruit shows activity against Aedes aegypti mosquito larvae. J Agric Food Chem 50:3765–3767
Zibaee A, Bandani AR (2010) Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauveria bassiana. Bull Entomol Res 100(02):185–196
Acknowledgments
Author Dr.AAM was supported by the Deanship of Scientific Research at King Saud University for providing funding for this work through the research group project No. RGP 010. The authors would thank an anonymous referee for his valuable suggestion and comments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lija-Escaline, J., Senthil-Nathan, S., Thanigaivel, A. et al. Physiological and biochemical effects of botanical extract from Piper nigrum Linn (Piperaceae) against the dengue vector Aedes aegypti Liston (Diptera: Culicidae). Parasitol Res 114, 4239–4249 (2015). https://doi.org/10.1007/s00436-015-4662-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4662-1