Advertisement

Parasitology Research

, Volume 113, Issue 9, pp 3121–3141 | Cite as

The major bioactive components of seaweeds and their mosquitocidal potential

  • Ke-Xin Yu
  • Ibrahim Jantan
  • Rohani Ahmad
  • Ching-Lee Wong
Review

Abstract

Seaweeds are one of the most widely studied natural resources for their biological activities. Novel seaweed compounds with unique chemical structures have been reported for their pharmacological properties. The urge to search for novel insecticidal compound with a new mode of action for development of botanical insecticides supports the relevant scientific research on discovering the bioactive compounds in seaweeds. The mosquitocidal potential of seaweed extracts and their isolated compounds are documented in this review paper, along with the discussion on bioactivities of the major components of seaweeds such as polysaccharides, phenolics, proteins, terpenes, lipids, and halogenated compounds. The effects of seaweed extracts and compounds toward different life stages of mosquito (egg, larva, pupa, and adult), its growth, development, and reproduction are elaborated. The structure-activity relationships of mosquitocidal compounds are discussed to extrapolate the possible chemical characteristics of seaweed compounds responsible for insecticidal properties. Furthermore, the possible target sites and mode of actions of the mosquitocidal seaweed compounds are included in this paper. The potential synergistic effects between seaweeds and commercial insecticides as well as the toxic effects of seaweed extracts and compounds toward other insects and non-target organisms in the same habitat are also described. On top of that, various factors that influence the mosquitocidal potential of seaweeds, such as abiotic and biotic variables, sample preparation, test procedures, and considerations for a precise experimental design are discussed. The potential of active seaweed extracts and compounds in the development of effective bioinsecticide are also discussed.

Keywords

Mosquito Larvicidal activity Toxic effects Insecticide 

Notes

Acknowledgments

Financial assistance from Universiti Kebangsaan Malaysia postgraduate fund is gratefully acknowledged. The authors thank Prof. Simon Gibbons from University College London for his input to the manuscript and Miss Chiong Kai Shing from Universiti Malaya for proofreading the manuscript.

References

  1. Abou-Elnaga ZS, Alarif WM, Al-lihaibi SS (2011) New larvicidal acetogenin from the red alga Laurencia papillosa. CLEAN-Soil Air Water 39(8):787–794. doi: 10.1002/clen.201000597 CrossRefGoogle Scholar
  2. Afolayan AF, Bolton JJ, Lategan CA, Smith PJ, Beukes DR (2008) Fucoxanthin, tetraprenylated toluquinone and toluhydroquinone metabolites from Sargassum heterophyllum inhibit the in vitro growth of the malaria parasite Plasmodium falciparum. Z Naturforsch C 63:848–852PubMedGoogle Scholar
  3. Ahmad R, Chu WL, Ismail Z, Lee HL, Phang SM (2004) Effect of ten chlorophytes on larval survival, development and adult body size of the mosquito Aedes aegypti. Southeast Asian J Trop Med Public Health 35(1):79–87Google Scholar
  4. Ahn GN, Kim KN, Cha SH, Song CB, Lee J, Heo MS, Yeo IK, Lee NH, Jee YH, Kim JS, Heu MS, Jeon YJ (2007) Antioxidant activities of phlorotannins purified from Ecklonia cava on free radical scavenging using ESR and H2O2-mediated DNA damage. Eur Food Res Technol 226:71–79CrossRefGoogle Scholar
  5. Alarif WM, Abou-Elnaga ZS, Ayyad SE, Al-lihaibi SS (2010) Insecticidal metabolites from the green alga Caulerpa racemosa. CLEAN-Soil Air Water 38(5–6):548–557. doi: 10.1002/clen.201000033 CrossRefGoogle Scholar
  6. Ali MS, Ravikumar S, Beula JM (2013) Mosquito larvicidal activity of seaweeds extracts against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Asian Pac J Trop Dis 3(3):196–201. doi: 10.1016/S2222-1808(13)60040-7 PubMedCentralCrossRefGoogle Scholar
  7. Al-Mehmadi RM, Al-Khalaf AA (2010) Larvicidal and histological effects of Melia azedarach extract on Culex quinquefasciatus Say larvae (Diptera: Culicidae). J King Saud Univ (Science) 22:77–85CrossRefGoogle Scholar
  8. Amer A, Mehlhorn H (2006a) Repellency effect of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes. Parasitol Res 99(4):478–490. doi: 10.1007/s00436-006-0184-1 PubMedCrossRefGoogle Scholar
  9. Amer A, Mehlhorn H (2006b) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99(4):466–472. doi: 10.1007/s00436-006-0182-3 PubMedCrossRefGoogle Scholar
  10. Andrianasolo EH, France D, Cornell-Kennon S, Gerwick WH (2006) DNA methyl transferase inhibiting halogenated monoterpenes from the Madagascar red marine alga Portieria hornemannii. J Nat Prod 69:576–579PubMedCrossRefGoogle Scholar
  11. Argandoña V, Pozo Del T, San-Martín A, Rovirosa J (2000) Insecticidal activity of Plocamium cartilagineum monoterpenes. Bol Soc Chil Quím. doi: 10.4067/S0366-16442000000300006
  12. Arias JR, Mulla MS (1975) Morphogenetic aberrations induced by a juvenile hormone analogue in the mosquito Culex tarsalis (Diptera: Culicidae). J Med Entomol 12(3):309–318PubMedGoogle Scholar
  13. Asha A, Martin Rathi J, Patric Raja D, Sahayaraj K (2012) Biocidal activity of two marine green algal extracts against third instar nymph of Dysdercus cingulatus (Fab.) (Hemiptera: Pyrrhocoridae). J Biopest 5(Supplementary):129–134Google Scholar
  14. Awad NE (2004) Bioactive brominated diterpenes from the marine red alga Jania rubens (L.) Lamx. Phytother Res 18:275–279PubMedCrossRefGoogle Scholar
  15. Ayesha H, Sultana V, Ara J, Ehteshamul-Haque S (2010) In vitro cytotoxicity of seaweeds from Karachi Coast on brine shrimp. Pak J Bot 42(5):3555–3560, http://www.pakbsorg/pjbot/tcontents/tcontent42(5)61–70.html. Accessed 15 June 2014Google Scholar
  16. Ayyad SEN, Ezmirly ST, Basaif SA, Alarif WM, Badria AF, Badria FA (2011) Antioxidant, cytotoxic, antitumor, and protective DNA damage metabolites from the red sea brown alga Sargassum sp. Pharmacognosy Res 3:160–165. doi: 10.4103/0974-8490.85000 PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bantoto V, Dy D (2013) The larvicidal activity of brown algae Padina minor (Yamada 1925) and Dictyota linearis (Greville 1830) against the dengue vector, Aedes aegypti (Linn 1762) (Diptera: Culicidae). J Vect Borne Dis 50:68–70Google Scholar
  18. Barbosa JDF, Silva VB, Alves PB, Gumina G, Santos RLC, Sousa DP, Cavalcanti SCH (2012) Structure–activity relationships of eugenol derivatives against Aedes aegypti (Diptera: Culicidae) larvae. Pest Manag Sci 68:1478–1483. doi: 10.1002/ps.3331 PubMedCrossRefGoogle Scholar
  19. Bianco EM, Pires L, Santos GKN, Dutra KA, Reis TNV, Vasconcelos ERTPP, Cocentino ALM, Navarro DMAF (2013) Larvicidal activity of seaweeds from northeastern Brazil and of a halogenated sesquiterpene against the dengue mosquito (Aedes aegypti). Ind Crop Prod 43:270–275. doi: 10.1016/j.indcrop.2012.07.032 CrossRefGoogle Scholar
  20. Black WAP (1954) Concentration gradients and their significance in Laminaria saccharina (L.) Lamour. J Mar Biol Assoc UK 33(1):49–60CrossRefGoogle Scholar
  21. Bloomquist JR (1993) Toxicology, mode of action and target site-mediated resistance to insecticides acting on chloride channels. Comp Biochem Physiol C 106(2):301–314PubMedGoogle Scholar
  22. Bloomquist JR (1996) Ion channels as targets for insecticides. Ann Rev Entomol 41:163–190CrossRefGoogle Scholar
  23. Bonnard I, Manzanares I, Rinehart KL (2003) Stereochemistry of Kahalalide F. J Nat Prod 66(11):1466–1470PubMedCrossRefGoogle Scholar
  24. Born FS, Bianco ÉM, Da Camara CAG (2012) Acaricidal and repellent activity of terpenoids from seaweeds collected in Pernambuco, Brazil. Nat Prod Commun 7:463–466PubMedGoogle Scholar
  25. Bourel-Bonnet L, Rao KV, Hamann MT, Ganesan A (2005) Solid-phase total synthesis of Kahalalide A and related analogues. J Med Chem 48(5):1330–1335PubMedCrossRefGoogle Scholar
  26. Campos A, Souza CB, Lhullier C, Falkenberg M, Schenkel EP, Ribeiro-do-Valle RM, Siqueira JM (2012) Anti-tumour effects of elatol, a marine derivative compound obtained from red algae Laurencia microcladia. J Pharm Pharmacol 64(8):1146–1154. doi: 10.1111/j.2042-7158.2012.01493 PubMedCrossRefGoogle Scholar
  27. Cardozo KH, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C Toxicol Pharmacol 146(1–2):60–78. doi: 10.1016/j.cbpc.2006.05.007 PubMedCrossRefGoogle Scholar
  28. Casida JE (1980) Pyrethrum flowers and pyrethroid insecticides. Environ Health Perspect 34:189–202PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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 Contr 31(1):138–144CrossRefGoogle Scholar
  30. Chan JCC, Cheung PCK, Ang PO (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag. J Agric Food Chem 45(8):3056–3059. doi: 10.1021/jf9701749 CrossRefGoogle Scholar
  31. Chandini S, Kumar GP, Suresh PV, Bhaskar N (2008) Seaweeds as source of nutritionally beneficial compounds—a review. J Food Sci Technol 45(1):1–13, http://irc.ftri.com/1608/. Accessed 11 May 2014Google Scholar
  32. Chattopadhyay N, Ghosh T, Sinha S, Chattopadhyay K, Karmakar P, Ray B (2010) Polysaccharides from Turbinaria conoides: structural features and antioxidant capacity. Food Chem 118:823–829. doi: 10.1016/j.foodchem.2009.05.069 CrossRefGoogle Scholar
  33. Christophers SR (1960) Aëdes aegypti (L.) the yellow fever mosquito: Its life history, bionomics, and strucure. Cambridge University Press, New YorkGoogle Scholar
  34. Connan S, Stengel DB (2011) Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquat Toxicol 104(1–2):1–13PubMedGoogle Scholar
  35. Coppejans E, Leliaert F, Dargent O, Gunasekara R, De Clerck O (2009) Sri Lankan seaweeds—methodologies and field guide to the dominant species. Abc Taxa 6(i-viii):265Google Scholar
  36. Copping LG, Menn JJ (2000) Biopesticides: a review of their action, applications and efficacy. Pest Manag Sci 56:651–676CrossRefGoogle Scholar
  37. Crews P, Mayers BL, Naylor S, Clason EL, Jacobs RS, Staal GB (1984) Bio-active monoterpenes from red seaweeds. Phytochemistry 23(7):1449–1451CrossRefGoogle Scholar
  38. Cronin G, Hay ME (1996) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77(8):2287–2301CrossRefGoogle Scholar
  39. David J, Rey D, Pautou M, Meyran J (2000) Differential toxicity of leaf litter to dipteran larvae of mosquito developmental sites. J Invertebr Pathol 75:9–18PubMedCrossRefGoogle Scholar
  40. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899. doi: 10.1016/j.foodchem.2006.09.041 CrossRefGoogle Scholar
  41. de Lima GP, de Souza TM, de Paula FG, Farias DF, Cunha AP, Ricardo NM, de Morais SM, Carvalho AF (2013) Further insecticidal activities of essential oils from Lippia sidoides and Croton species against Aedes aegypti L. Parasitol Res 112(5):1953–1958. doi: 10.1007/s00436-013-3351-1 PubMedCrossRefGoogle Scholar
  42. Devi P, Solimabi W, D’Souza L, Kamat SY (1997) Toxic effects of coastal and marine plant extracts on mosquito larvae. Bot Mar 40:533–535CrossRefGoogle Scholar
  43. Devi P, Solimabi W, D’Souza L, Kamat SY (1998) Larvicidal activity of some marine macrophytes against Artemia salina. Ad Bios 17(11):75–84, http://drs.nio.org/drs/handle/2264/1922. Accessed 11 May 2014Google Scholar
  44. Dias CN, Moreas DFC (2014) Essential oils and their compounds as Aedes aegypti L. (Diptera: Culicidae) larvicides: review. Parasitol Res 113(2):565–592. doi: 10.1007/s00436-013-3687-6
  45. Dos Santos AO, Veiga-Santos P, Ueda-Nakamura T, Dias-Filho BP, Sudatti DB, Bianco EM, Pereira RC, Nakamura CV (2010) Effect of elatol, isolated from red seaweed Laurencia dendroidea, on Leishmania amazonensis. Mar Drugs 8:2733–2743. doi: 10.3390/md8112733 PubMedCentralPubMedCrossRefGoogle Scholar
  46. El Sayed K, Bartyzel P, Shen X, Perry TL, Zjawiony JK, Hamann MT (2000) Marine natural products as antituberculosis agents. Tetrahedron 56:949–953CrossRefGoogle Scholar
  47. Elbanna SM, Hegazi MM (2011) Screening of some seaweeds species from South Sinai. Red Sea as potential bioinsecticides against mosquito larvae; Culex pipiens. Egypt Acad J Biol Sci 4(2):21–30, http://entomology.eajbs.eg.net/vol4-no2.html. Accessed 15 June 2014Google Scholar
  48. Enan EE (2005) Molecular and pharmacological analysis of an octopamine receptor from American cockroach and fruit fly in response to plant essential oils. Arch Insect Biochem 59(3):161–171CrossRefGoogle Scholar
  49. FAO (Food and Agriculture Organization of the United Nations) (2004) The state of world fisheries and aquaculture. Part 3. Highlights of special FAO studies. http://www.fao.org/docrep/007/y5600e/y5600e00.htm. Accessed 24 Jan 2014
  50. Ferkany JW, Coyle JT (1983) Kainic acid selectively stimulates the release of endogenous excitatory acidic amino acids. J Pharmacol Exp Therapeut 225:399–406Google Scholar
  51. Ferriera LG, Noseda MN, Gonҫalves AG, Ducatti DRB, Fujii MT, Duarte MER (2012) Chemical strucute of the complex pyruvylated and sulfated agaran from the red seaweed Palisada flagellifera (Cermiales, Rhodophyta). Carbohydr Res 347:83–94. doi: 10.1016/j.carres.2011.10.007 CrossRefGoogle Scholar
  52. Fisch K, Böhm V, Wright AD, König GM (2003) Antioxidative meroterpenoids from the brown alga Cystoseira crinita. J Nat Prod 66(7):968–975PubMedCrossRefGoogle Scholar
  53. Fukuzawa A, Masamune T (1981) Laurepinnacin and isolaurepinnacin, new acetylenic cyclic ethers from the marine red alga Laurencia pinnata Yamada. Tetrahedron Lett 22(41):4081–4084CrossRefGoogle Scholar
  54. Fuller RW, Cardellina JH, Kato Y, Brinen LS, Clardy J, Sander KM, Boyad MR (1992) A pentahalogenated monoterepene from the red alga Portieria hornemannii produced a novel cytotoxicity profile against a diverse panel of human tumor cell lines. J Med Chem 35:3007–3011PubMedCrossRefGoogle Scholar
  55. Fuller RW, Cardellina JH, Jurek J, Scheuer PJ, Alvarado-Linder B, McGuier M, Gray GN, Steiner IR, Clardy I, Menez E, Shoemaker RH, Newman DI, Sander KM, Boyad MR (1994) Isolation and structure/activity features of halomon-related antitumor monoterpenes from the red alga Portieria hornemannii. J Med Chem 37:4407–4411PubMedCrossRefGoogle Scholar
  56. Gerwick W, Fenical W (1981) Ichthytoxic and cytotoxic metabolite of the tropical brown alga Stypopodium zonale (Lamouroux) Papenfuss. J Org Chem 46:22–27Google Scholar
  57. Ghosh A, Chowdhury N, Chandra G (2012) Plant extracts as potential mosquito larvicides. Indian J Med Res 135:581–598PubMedCentralPubMedGoogle Scholar
  58. Gkinis G, Michaelakis A, Koliopoulos G, Ioannou E, Tzakou O, Roussis V (2014) Evaluation of the repellent effects of Nepeta parnassica extract, essential oil, and its major nepetalactone metabolite against mosquitoes. Parasitol Res 113(3):1127–1134. doi: 10.1007/s00436-013-3750-3 PubMedCrossRefGoogle Scholar
  59. Glyantsev S, Annaev A, Savvina TV (1993) Morphological basis for selecting composition and structure of biologically active compounds based on sodium alginate for wound treatment. Byull Eksp Biol Med 115:65–67CrossRefGoogle Scholar
  60. Govindarajan M, Mathivanan T, Elumalai K, Krishnappa K, Anandan A (2011) Mosquito larvicidal, ovicidal, and repellent properties of botanical extracts against Anopheles stephensi, Aedes aegypti, and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 109(2):353–367. doi: 10.1007/s00436-011-2263-1
  61. Hamann MT, Otto CS, Scheuer PJ, Dunbar DC (1996) Kahalides: bioactive peptides from a marine mollusk Elysia rufescens and its algal diet Bryopsis sp. J Org Chem 61:6594–6600PubMedCrossRefGoogle Scholar
  62. Hayashi K, Nakano T, Hashimoto M, Kanekiyo K, Hayashi T (2008) Defensive effects of a fucoidan from brown alga Undaria pinnatifida against Herpes simplex virus infection. Int Immunopharmacol 8:109–116PubMedCrossRefGoogle Scholar
  63. Hemmingson JA, Falshaw R, Furneaux RH, Thompson K (2006) Structure and antiviral activity of the galactofucan sulfates extracted from Undaria pinnatifida (Phaeophyta). J Appl Phycol 18:185–193. doi: 10.1007/s10811-006-9096-9 CrossRefGoogle Scholar
  64. Holdt SL, Kraan S (2011) Bioactive compounds in seaweeds: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  65. Insun D, Choochote W, Jitpakdi A, Chaithong U, Tippawangkosol P, Pitasawat B (1999) Possible site of action of Kaempferia galanga in killing Culex quinquefasciatus larvae. Southeast Asian J Trop Med Public Health 30(1):195–199PubMedGoogle Scholar
  66. Iverson F, Truelove J, Nera E, Tryphonas L, Campbell J, Lok J (1989) Domoic acid poisoning and mussel-associated intoxication: Preliminary investigations into the response of mice and rats to toxic mussel extract. Food Chem Toxicol 27(6):377–384PubMedCrossRefGoogle Scholar
  67. Jantan I, Ping WO, Visuvalingam SD, Ahmad NW (2003) Larvicidal activity of essential oils and methanol extracts of Malaysian plants on Aedes aegypti. Pharm Biol 41:234–236CrossRefGoogle Scholar
  68. Jantan I, Yalvema MF, Ahmad NW, Jamal JA (2005) Insecticidal activities of the leaf oils of eight Cinnamomum species against Aedes aegypti and Aedes albopictus. Pharm Biol. doi: 10.1080/13880200500220771 Google Scholar
  69. Jung HA, Hyun SK, Kim HR, Choi JS (2006) Angiotensin-converting enzyme I inhibitory activity of phlorotannins from Ecklonia stolonifera. Fish Sci 72:1292–1299CrossRefGoogle Scholar
  70. Kalyanasundaram M, Babu CJ (1982) Biological active plant extracts as mosquito larvicides. Indian J Med Res 76:102–106PubMedGoogle Scholar
  71. Kalyanasundaram M, Das PK (1985) Larvicidal and synergistic activity of plant extracts for mosquito control. Indian J Med Res 82:19–23Google Scholar
  72. Kapetanovic R, Sladic D, Popov S, Zlatovic M, Kljajic Z, Gasic MJ (2005) Sterol composition of the Adriatic sea algae Ulva lactuca, Codium dichotomum, Cystoseira adriatica and Fucus virsoides. J Serb Chem Soc 70:1395–1400CrossRefGoogle Scholar
  73. Karmegam N, Sakthivadivel M, Anuradha V, Daniel T (1997) Indigenous plant extracts as larvicidal agents against Culex quinquefasciatus Say. Bioresour Technol 59:137–140CrossRefGoogle Scholar
  74. Khanavi M, Toulabi PB, Abai MR, Sadati N, Hadjiakhoondi F, Hadjiakhoondi A, Vatandoost H (2011) Larvicidal activity of marine algae, Sargassum swartzii and Chondria dasyphylla, against malaria vector Anopheles stephensi. J Vector Borne Dis 48(4):241–244PubMedGoogle Scholar
  75. Khandagle AJ, Tare VS, Raut KD, Morey RA (2011) Bioactivity of essential oils of Zingiber officinalis and Achyranthes aspera against mosquitoes. Parasitol Res 109(2):339–343. doi: 10.1007/s00436-011-2261-3
  76. Khotimchenko YS, Kovalev VV, Savchenko OV, Ziganshina OA (2001) Physical–chemical properties, physiological activity, and usage of alginates, the polysaccharides of brown algae. Russ J Mar Biol 27:53–64CrossRefGoogle Scholar
  77. Kitamura K, Matsuo M, Yasui T (1991) Fucoidan from brown seaweed Laminaria angustata var. longissima. Agric Biol Chem 55(2):615–616CrossRefGoogle Scholar
  78. Kostetsky EY, Goncharova SN, Sanina NM, Shnyrov VL (2004) Season influence on lipid composition of marine macrophytes. Bot Mar 47:134–139CrossRefGoogle Scholar
  79. Kovendan K, Murugan K, Kumar PM, Thiyagarajan P, William SJ (2013) Ovicidal, repellent, adulticidal and field evaluations of plant extract against dengue, malaria and filarial vectors. Parasitol Res 112(3):1205–1219. doi: 10.1007/s00436-012-3252-8
  80. Kubanek I, Prusak AC, Snell TW, Giese RA, Hardcastle KI, Fairchild CR, Aalbersberg W, Raventos-Suarez C, Hay ME (2005) Antineoplastic diterpene-benzoate macrolides from the Fijian red alga Callophycus serratus. Org Lett 7:261–264Google Scholar
  81. Kukel CF, Jennings KR (1994) Delphinium alkaloids as inhibitors of alpha-bungarotoxin binding to rat and insect neural membranes. Can J Physiol Pharmacol 72:104–107PubMedCrossRefGoogle Scholar
  82. Kumar S, Singh AP, Nair G, Batra S, Seth A, Wahab N, Warikoo R (2011) Impact of Parthenium hysterophorus leaf extracts on the fecundity, fertility and behavioural response of Aedes aegypti L. Parasitol Res 108(4):853–859. doi: 10.1007/s00436-010-2126-1
  83. Kumar KP, Murugan K, Kovendan K, Kumar AN, Hwang JS, Barnard DR (2012) Combined effect of seaweed (Sargassum wightii) and Bacillus thuringiensis var. israelensis on the coastal mosquito, Anopheles sundaicus, in Tamil Nadu, India. ScienceAsia 38:141–146CrossRefGoogle Scholar
  84. Kumari P, Kumar M, Gupta V, Reddy CRK, Jha B (2009) Tropical marine macroalgae as potential sources of nutritionally important PUFAs. Food Chem 120:749–757. doi: 10.1016/j.foodchem.2009.11.006 CrossRefGoogle Scholar
  85. LaLonde RT, Morris CD, Wong CF, Gardener LC, Eckert DJ, King DR, Zimmerman RH (1979) Response of Aedes triseriatus larvae to fatty acids of Cladophora. J Chem Ecol 5(3):371–381CrossRefGoogle Scholar
  86. Laurens A, Fourneau C, Hocquemiller R, Cave A, Bories C, Loiseau PM (1997) Antivectorial activities of cashew nut shell extracts from Anacardium occidentale L. Phytother Res 11:145–146CrossRefGoogle Scholar
  87. Lee YS, Shin KH, Kim BK, Lee S (2004) Anti-diabetic activities of fucosterol from Pelvetia siliquosa. Arch Pharmacol Res 27(11):1120–1122CrossRefGoogle Scholar
  88. Li B, Lu F, Wei X, Zhao Z (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695PubMedCrossRefGoogle Scholar
  89. Ma M, Zhao J, Wang S, Li S, Yang Y, Shi J, Fan X, He L (2006) Bromophenols coupled with methyl gamma-ureidobutyrate, bromophenol sulfates from the red alga Rhodomela confervoides. J Nat Prod 69:206–210PubMedCrossRefGoogle Scholar
  90. Maeda M, Kodama T, Tanaka T, Ohfune Y, Nomoto K, Nishimura K, Fujita T (1984) Insecticidal and neuromuscular activities of domoic acid and its related compounds. J Pestic Sci 9(1):27–32CrossRefGoogle Scholar
  91. Maeda M, Kodama T, Tanaka T, Yoshizumi H, Takemoto T, Nomoto K, Fujita T (1986) Structures of isodomoic acids A, B and C, novel insecticidal amino acids from the red alga Chondria armata. Chem Pharm Bull 34:4892–4895CrossRefGoogle Scholar
  92. Maeda H, Hosokawa M, Sashima T, Murakami-Funayama K, Miyashita K (2009) Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol Med Rep 2:897–902PubMedGoogle Scholar
  93. Manilal A, Sujith S, Kiran GS, Selvin J, Shakir C, Gandhimathi R, Panikkar MVN (2009) Biopotentials of seaweeds collected from southwest coast of India. J Mar Sci Technol 17(1):67–73, http://jmst.ntou.edu.tw/marine/search2.php?keyin=17(1). Accessed 15 June 2014Google Scholar
  94. Manilal A, Thajuddin N, Selvin J, Idhayadhulla A, Kumar RS, Sujith S (2011) In vitro mosquito larvicidal activity of marine algae against the human vectors, Culex quinquefasciatus (Say) and Aedes aegypti (Linnaeus) (Diptera: Culicidae). Int J of Zool Res 7(3):272–278CrossRefGoogle Scholar
  95. Margaret Beula J, Ravikumar S, Syed Ali M (2011) Mosquito larvicidal efficacy of seaweed extracts against dengue vector of Aedes aegypti. Asian Pac J Trop Biomed. 1(2)Supplement:S143–S146. doi: 10.1016/S2221-1691(11)60143-3
  96. Matasyoh JC, Dittrich B, Schueffler A, Laatsch H (2011) Larvicidal activity of metabolites from the endophytic Podospora sp. against the malaria vector Anopheles gambiae. Parasitol Res 108(3):561–566. doi: 10.1007/s00436-010-2098-1
  97. McLaughlin JL, Rogers LL, Anderson JE (1998) The use of biological assays to evaluate botanicals. Drug Inf J 32:513–524. doi: 10.1177/009286159803200223. http://dij.sagepub.com/content/32/2.toc. Acessed 18 July 2014Google Scholar
  98. Meyer BN, Ferrigni NR, Putnam JE, Jacobsen LB, Nichols DE, McLaughlin JL (1982) Brine shrimp: a convenient general bioassay for active plant constituents. Planta Med 45:31–34CrossRefGoogle Scholar
  99. Mnyone LL, Kirby MJ, Mpingwa MW, Lwetoijera DW, Knols BGJ, Takken W, Koenraadt CJM, Russell TL (2011) Infection of Anopheles gambiae mosquitoes with entomopathogenic fungi: effect of host age and blood-feeding status. Parasitol Res 108(2):317–322. doi: 10.1007/s00436-010-2064-y
  100. Nagayama K, Iwamura Y, Shibata T, Hirayama I, Nakamura T (2002) Bacterial activity of phlorotannins from the brown alga Ecklonia kurome. J Antimicrob Chemoth 50:889–893CrossRefGoogle Scholar
  101. Natarajan S, Pandian K, Pandima S, Kasi D (2009) Cholinesterase inhibitors from Sargassum and Gracilaria gracillis: seaweeds inhabiting south Indian coastal areas (Hare Island, Gulf of Mannar). J Nat Prod Res 23(4):355–369CrossRefGoogle Scholar
  102. Nishino T, Nagumo T (1987) Sugar constituents and blood-anticoagulant activities of fucose-containing sulfated polysaccharides in nine brown seaweed species. Nippon Nogeikagaku Kaishi 61:361–363CrossRefGoogle Scholar
  103. Oliveira PV, Ferreira JC Jr, Moura FS, Lima GS, de Oliveira FM, Oliveira PE, Conserva LM, Giulietti AM, Lemos RP (2010) Larvicidal activity of 94 extracts from ten plant species of northeastern of Brazil against Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 107:403-407. doi: 10.1007/s00436-010-1880-4
  104. Paeporn P, Komalamisra N, Deesin V, Rongsriyam Y, Eshita Y, Thongrungkiat S (2003) Temephos resistance in two forms of Aedes aegypti and its significance for the resistance mechanism. Southeast Asian J Trop Med Public Health 34(4):786–792PubMedGoogle Scholar
  105. Patil CD, Patil SV, Salunke BK, Salunkhe RB (2011) Bioefficacy of Plumbago zeylanica (Plumbaginaceae) and Cestrum nocturnum (Solanaceae) plant extracts against Aedes aegypti (Diptera: Culicide) and nontarget fish Poecilia reticulata. Parasitol Res 108(5):1253–1263. doi: 10.1007/s00436-010-2174-6
  106. Pitasawat B, Champakaew D, Choochote W, Jitpakdi A, Chaithong U (2007) Aromatic plant-derived essential oil: An alternative larvicide for mosquito control. Fitoterapia 78:205–210PubMedCrossRefGoogle Scholar
  107. Priestley CM, Williamson EM, Wafford KA, Sattelle DB (2003) Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABA(A) receptors and a homo-oligomeric GABA receptor from Drosophila melanogaster. Br J Pharmacol 140(8):1363–1372PubMedCentralPubMedCrossRefGoogle Scholar
  108. Rademaker-Lakhai JM, Horenblas S, Meinhardt W, Stokvis E, Reijke TM, Jimeno JM, Lopez-Lazaro L, Lopez Martin JA, Beijnen JH, Schellens JHM (2005) Phase I clinical and pharmacokinetic study of Kahalalide F in patients with advanced androgen refractory prostate. Cancer Clin Cancer Res 11:1854–1862CrossRefGoogle Scholar
  109. Rao AV, Rao JG (2007) Carotenoids and human health. Pharmacol Res 55(3):207–216. doi: 10.1016/j.phrs.2007.01.012 PubMedCrossRefGoogle Scholar
  110. Rasmussen RS, Morrissey MT (2007) Marine biotechnology for production of food ingredients. Adv Food Nutr Res 52:237–292PubMedCrossRefGoogle Scholar
  111. Ratanatham S, Rojanasunan W, Upatham ES (1994) Morphological aberrations induced by methoprene, a juvenile hormone analogue, in Anopheles dirus s.s. and An. Sawadwongporni (Diptera: Culicidae). J Sci Soc Thailand 20:171–182CrossRefGoogle Scholar
  112. Ratanatham S, Dinh PX, Upatham ES, Sukhapanth N, Chitramvong Y (1996) Effects of diflubenzuron against the larval stages of Anopheles (cellia) dirus and Anopheles (cellia) maculatus (Diptera: Anophelinae). J Sci Soc Thailand 22:189–200CrossRefGoogle Scholar
  113. Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920. doi: 10.1016/j.cropro.2010.05.008 CrossRefGoogle Scholar
  114. Rim HJ, Ha JH, Lee JS, Hyun I, Uh KB (1974) Pyrantel embonate in mass treatment of ascariasis and comparison with piperazine adipate and santonin-kainic acid complex. Korean J Parasitol 12(2):141–146CrossRefGoogle Scholar
  115. Roark RC (1947) Some promising insecticidal plants. Econ Bot 1:437–445CrossRefGoogle Scholar
  116. Ryu G, Hee S, Sook E, Wook B, Ryu S, Ho B (2003) Cholinesterase inhibitory activity of two farnesylacetone derivatives from the brown alga Sargassum sagamianum. J Arch Pharm Res 26(10):796–799CrossRefGoogle Scholar
  117. Sahayaraj K, Kalidas S (2011) Evaluation of nymphicidal and ovicidal effect of a seaweed, Padina pavonica (Linn.) (Phaeophyceae) on cotton pest, Dysdercus cingulatus (Fab.). Indian J Mar Sci 40(1):125–129, http://www.niscair.res.in/sciencecommunication/researchjournals/rejour/ijms/ijms2k11/ijms_feb11.asp. Accessed 15 June 2014Google Scholar
  118. Samidurai K, Saravanakumar A (2011) Mosquitocidal properties of nereistoxin against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitol Res 109(4):1107–1112Google Scholar
  119. San-Martin A, Negrete R, Rovirosa J (1991) Insecticide and acaricide activities of polyhalogenated monoterpenes from Chilean Plocamium cartilagineum. Phytochemistry 30(7):2165–2169CrossRefGoogle Scholar
  120. Schaeffer DJ, Krylov VS (2000) Anti-HIV activity of extracts and compounds from algae and cyano bacteria. Ecotoxicol Environ Saf 45:208–227PubMedCrossRefGoogle Scholar
  121. Schmutterer H (1990) Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annu Rev Entomol 35:197–271Google Scholar
  122. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62(3):775–806PubMedCentralPubMedGoogle Scholar
  123. Selvin J, Lipton AP (2004) Biopotentials of Ulva fasciata and Hypnea musciformis collected from the peninsular coast of India. J Mar Sci Technol 12(1):1–6, http://jmst.ntou.edu.tw/marine/search2.php?keyin=12(1). Accessed 15 June 2014Google Scholar
  124. Sen AK, Das AK, Banerji N, Siddhanta AK, Mody KH, Ramavat BK, Chauhan VD, Vedasiromoni JR, Ganguly DK (1994) A new sulfated polysaccharides with potent blood anti-coagulant activity from the new seaweed Grateloupia indica. Int J Biol Macromol 16:279–280PubMedCrossRefGoogle Scholar
  125. Senthil-Nathan S, Choi MY, Paik CH, Seo HY, Kalaivani K, Kim JD (2008) Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown planthopper Nilaparvata lugens (Stål). Ecotoxicol Environ Saf 70:244–250PubMedCrossRefGoogle Scholar
  126. Service MW (1980) A guide to medical entomology Macmillan tropical and sub-tropical medical texts. Macmillan, LondonGoogle Scholar
  127. Shaalan EAS, Canyon D, Younes MWF, Abdel-Wahab H, Mansour AH (2005) A review of botanical phytochemicals with mosquitocidal potential. Environ Int 31:1149–1166PubMedCrossRefGoogle Scholar
  128. Sharma OP (2011) Series on diversity of microbes and cryptogams Algae. McGraw Hill, New DelhiGoogle Scholar
  129. Sharma P, Mohan L, Srivastava CN (2006) Impact analysis of neem kernel extracts on the development profile of Anopheles stephensi. J Asia-Pac Entomol 9(1):11–17. doi: 10.1016/S1226-8615(08)60270-8 CrossRefGoogle Scholar
  130. Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16(4):245–262. doi: 10.1023/B:JAPH.0000047783.36600.ef CrossRefGoogle Scholar
  131. Sperk G, Lassmann H, Baran H, Kish SJ, Seitelberger F, Hornykiewicz O (1983) Kainic acid induced seizures: neurochemical and histopathological changes. Neurosci 10(4):1301–1315CrossRefGoogle Scholar
  132. Spieler R (2002) Seaweed compound’s anti-HIV efficacy will be tested in southern Africa. Lancet 359(9318):1675. doi: 10.1016/S0140-6736(02)08605-1 PubMedCrossRefGoogle Scholar
  133. Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29(5):483–501. doi: 10.1016/j.biotechadv.2011.05.016 PubMedCrossRefGoogle Scholar
  134. Subramonia Thangam T, Kathiresan K (1996) Marine plants for mosquito control. In: Wildey KB (ed) Proceedings of the second international conference on urban pests. Edinburgh, ScotlandGoogle Scholar
  135. Sukumar K, Perich MJ, Boobar LR (1991) Botanical derivatives in mosquito control: a review. J Am Mosq Control Assoc 7(2):210–217PubMedGoogle Scholar
  136. Takahashi Y, Daitoh M, Suzuki M, Abe T, Masuda M (2002) Halogenated metabolites from the new Okinawan red alga Laurencia yonaguniensis. J Nat Prod 65:395–398PubMedCrossRefGoogle Scholar
  137. Terasaki M, Hirose A, Narayan B, Baba B, Kawagoe B, Yasui H, Saga H, Hosokawa M, Miyashita K (2009) Evaluation of recoverable functional lipid components of several brown seaweeds (Phaeophyta) from Japan with special reference to fucoxanthin and fucosterol contents. J Phycol 45(4):974–980. doi: 10.1111/j.1529-8817.2009.00706 CrossRefGoogle Scholar
  138. Thangam TS, Kathiresan K (1991a) Mosquito larvicidal activity of marine plant extracts with synthetic insecticides. Bot Mar 34:537–539Google Scholar
  139. Thangam TS, Kathiresan K (1991b) Mosquito larvicidal effect of seaweed extracts. Bot Mar 34:433–435Google Scholar
  140. Warikoo R, Kumar S (2013) Impact of Argemone mexicana extracts on the cidal, morphological, and behavioral response of dengue vector, Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 112(10):3477–3484. doi: 10.1007/s00436-013-3528-7
  141. Watanabe K, Miyakado M, Ohno N, Okada A, Yanagi K, Moriguchi K (1989a) A polyhalogenated insecticidal monoterpene from the red alga, Plocamium telfairiae. Phytochemistry 28(1):77–78CrossRefGoogle Scholar
  142. Watanabe K, Umeda K, Miyakado M (1989b) Isolation and identification of three insecticidal principles from the red alga, Laurencia nipponica. Agric Biol Chem 53:2513–2515CrossRefGoogle Scholar
  143. Watanabe K, Umeda K, Kurita Y, Takayama C, Miyakado M (1990) Two insecticidal monoterpenes, telfairine and aplysiaterpenoid A, from the red alga Plocamium telfairiae: Structure elucidation, biological activity, and molecular topographical consideration by a semiempirical molecular orbital study. Pestic Biochem Physiol 37(3):275–286CrossRefGoogle Scholar
  144. Wong K, Cheung PC (2001) Influence of drying treatment on three Sargassum species. J Appli Phyco 13(1):43–50CrossRefGoogle Scholar
  145. Wong CL, Phang SM (2004) Biomass production of two Sargassum species at Cape Rachado. Hydrobiologia 512:79–88CrossRefGoogle Scholar
  146. World Health Organization (1996) Evaluation on the testing of insecticides—report of the WHO informal consultation, 7–11 October 1996, Geneva. Ref: CTD/WHOPES/IC/96.1. http://www.who.int/whopes/resources/resources_1996/en/. Accessed 11 May 2014
  147. World Health Organization (1998) Test procedures for insecticide resistance monitoring in malaria vectors, bioefficacy and persistence of insecticides on treated surfaces. Ref: WHO/CDS/CPC/MAL/98.12. http://www.who.int/whopes/resistance/en/. Accessed 18 July 2014
  148. World Health Organization (2005) Guidelines for laboratory and field testing of mosquito larvicides. Ref: WHO/CDS/WHOPES/GCDPP/2005.13. http://www.who.int/whopes/guidelines/en/. Accessed 14 Jun 2014
  149. World Health Organization (2011a) Generic risk assessment model for insecticides used for larviciding. Ref: WHO/HTM/NTD/WHOPES/2010.4.Rev1. http://www.who.int/whopes/guidelines/en/. Accessed 14 Jun 2014
  150. World Health Organization (2011b) Generic risk assessment model for indoor residual spraying of insecticides. Ref: WHO/HTM/NTD/WHOPES/2010.5.Rev1. http://www.who.int/whopes/guidelines/en/. Accessed 14 Jun 2014
  151. World Health Organization (2013) Dengue and severe dengue. http://www.who.int/mediacentre/factsheets/fs117/en/. Accessed 2 February 2014
  152. Xu N, Fan X, Yan X, Li X, Niu R, Tseng CK (2003) Antibacterial bromophenols from the marine red alga Rhodomela confervoides. Phytochemistry 62(8):1221–1224PubMedCrossRefGoogle Scholar
  153. Zhou GF, Sun Y, Xin H, Zhang Y, Li Z, Xu Z (2005) In vivo antitumor and immunomodulation activities of different molecular weight lambda-carrageenans from Chondrus ocellatus. Pharmacol Res 50:47–53CrossRefGoogle Scholar
  154. Zoubiri S, Baaliouamer A (2011) Potentiality of plants as source of insecticide principles. J Saudi Chem Soc. doi: 10.1016/j.jscs.2011.11.015 Google Scholar
  155. Zubia M, Payri C, Deslandes E (2008) Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J Appl Phycol 20(6):1033–1043CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ke-Xin Yu
    • 1
  • Ibrahim Jantan
    • 1
  • Rohani Ahmad
    • 2
  • Ching-Lee Wong
    • 3
  1. 1.Drug and Herbal Research Centre, Faculty of PharmacyUniversiti Kebangsaan MalaysiaKuala LumpurMalaysia
  2. 2.Medical Entomology Unit, Infectious Disease Research CentreInstitute for Medical ResearchKuala LumpurMalaysia
  3. 3.School of BiosciencesTaylor’s UniversitySubang JayaMalaysia

Personalised recommendations