Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-29T12:50:49.674Z Has data issue: false hasContentIssue false

The dietary arachidonic acid improved growth and immunity of honey bee (Apis mellifera ligustica)

Published online by Cambridge University Press:  08 October 2021

Jing Yu
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Weixing Zhang
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Xuepeng Chi
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Wenfeng Chen
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Zhenfang Li
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Ying Wang*
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Zhenguo Liu
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Hongfang Wang*
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
Baohua Xu*
Affiliation:
College of Animal Science and Technology, Shandong Agricultural University, Tai'an, China
*
Author for correspondence: Baohua Xu, Email: bhxu@sdau.edu.cn; Hongfang Wang, Email: Wanghongfang22@163.com
Author for correspondence: Baohua Xu, Email: bhxu@sdau.edu.cn; Hongfang Wang, Email: Wanghongfang22@163.com
Author for correspondence: Baohua Xu, Email: bhxu@sdau.edu.cn; Hongfang Wang, Email: Wanghongfang22@163.com

Abstract

Honeybees cannot synthesize arachidonic acid (ARA) themselves, only obtain it from food. Most pollen is deficient or contains a small amount of ARA. The necessity of supplementary ARA in bees’ diet has not been studied. The objective of this study was to investigate the effects of dietary ARA levels on the growth and immunity of Apis mellifera ligustica. A total of 25 honeybee colonies were randomly assigned to five dietary groups which were fed basic diets supplemented with 0, 2, 4, 6, and 8% of ARA. The diet with 4% ARA improved the body weight of newly emerged worker bees compared with the control group. Supplement of ARA in honeybee diets changed the fatty acid composition of honeybee body. SFA and MUFA contents of bees’ body declined, and PUFA content rised in the ARA group. Compared with the control group, the supplement of ARA in honeybee diets increased the contents of ARA, C22:6n-3 (DHA) and C18:3n-6 in bees’ body significantly, but decreased the contents of C16:1 and C18:3n-3. The diet supplied with 4% ARA reduced the mortality rate of honeybee infected with Escherichia coli. The activity of immune enzymes (phenoloxidase, antitrypsin, and lysozyme) and the mRNA expression levels of immune genes (defensin-2, toll, myd88, and dorsal) were improved by ARA diets to varying degrees depending on the ARA levels, especially 4% ARA. These results suggested that dietary ARA could improve the growth, survival, and immune functions of honeybees. Supplement of ARA in bees’ diet would be valuable for the fitness of honeybees.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguilar, V, Racotta, IS, Goytortúa, E, Wille, M, Sorgeloos, P, Civera, R and Palacios, E (2012) The influence of dietary arachidonic acid on the immune response and performance of Pacific whiteleg shrimp, Litopenaeus vannamei, at high stocking density. Aquaculture Nutrition 18, 258271.CrossRefGoogle Scholar
Anholt, VRD (2004) Arachidonic acid reduces the stress response of gilthead seabream Sparus L. Journal of Experimental Biology 207(19), 34193430.CrossRefGoogle ScholarPubMed
Arien, Y, Dag, A, Zarchin, S, Masci, T and Shafir, S (2015) Omega-3 deficiency impairs honey bee learning. Proceedings of the National Academy of Sciences of the USA 112, 1576115766.CrossRefGoogle ScholarPubMed
Atalah, E, Hernández-Cruz, CM and Benítez-Santana, T (2011) Importance of the relative levels of dietary arachidonic acid and eicosapentaenoic acid for culture performance of gilthead sea bream (Sparus aurata) larvae. Aquaculture Research 42, 12791288.CrossRefGoogle Scholar
Avadhanula, V, Weasner, BP, Hardy, GG, Kumar, JP and Hardy, RW (2009) A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathogens 5, e1000582.CrossRefGoogle ScholarPubMed
Bedick, JC, Tunaz, H, Nor Aliza, AR, Putnam, S, Ellis, MD and Stanley, DW (2001) Eicosanoids act in nodulation reactions to bacterial infections in newly emerged adult honey bees, Apis mellifera, but not in older foragers. Comparative Biochemistry & Physiology Toxicology & Pharmacology CBP 130, 107117.CrossRefGoogle ScholarPubMed
Bell, JG and Sargent, JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218, 491499.CrossRefGoogle Scholar
Bessonart, M, Izquierdo, MS, Salhi, M, Hernández-Cruz, CM, González, MM and Fernández-Palacios, H (1999) Effect of dietary arachidonic acid levels on growth and survival of gilthead sea bream (Sparus aurata l.) larvae. Aquaculture 179, 265275.CrossRefGoogle Scholar
Block, RC, Harris, WS and Pottala, JV (2008) Clinical investigation: determinants of blood cell omega-3 fatty acid content. Open Biomarkers Journal 1, 16.CrossRefGoogle ScholarPubMed
Brodschneider, R and Crailsheim, K (2010) Nutrition and health in honey bees. Apidologie 41, 278294.CrossRefGoogle Scholar
Brutscher, LM, Daughenbaugh, KF and Flenniken, ML (2015) Antiviral defense mechanisms in honey bees. Current Opinion in Insect Science 10, 7182.CrossRefGoogle ScholarPubMed
Calder, PC (2003) Polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38, 343352.CrossRefGoogle ScholarPubMed
Costa, A, Jan, E, Sarnow, P and Schneider, D (2009) The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 4, e7436.CrossRefGoogle ScholarPubMed
Delaporte, M, Soudant, P, Moal, J, Giudicelli, E, Lambert, C and Séguineau, C (2006) Impact of 20:4n-6 supplementation on the fatty acid composition and hemocyte parameters of the pacific oyster Crassostrea gigas. Lipids 41, 567576.CrossRefGoogle ScholarPubMed
Ding, Z, Zhou, J, Kong, Y, Zhang, Y and Ye, J (2017) Dietary arachidonic acid promotes growth, improves immunity, and regulates the expression of immune-related signaling molecules in macrobrachium nipponense (de haan). Aquaculture 484, 112119.CrossRefGoogle Scholar
Fain, JN, Leffler, CW and Bahouth, SW (2000) Eicosanoids as endogenous regulators of leptin release and lipolysis by mouse adipose tissue in primary culture. Journal of Lipid Research 41, 16891694.CrossRefGoogle ScholarPubMed
Fountoulaki, E, Alexis, MN, Nengas, I and Venou, B (2003) Effects of dietary arachidonic acid (20:4n-6), on growth, body composition, and tissue fatty acid profile of gilthead bream fingerlings (Sparus aurata l.). Aquaculture 225, 309323.CrossRefGoogle Scholar
Gabler, NK, Spencer, JD, Webel, DM and Spurlock, ME (2008) n-3 PUFA attenuate lipopolysaccharide-induced down-regulation of toll-like receptor 4 expression in porcine adipose tissue but does not alter the expression of other immune modulators. The Journal of Nutritional Biochemistry 19, 815.CrossRefGoogle Scholar
Heike, G, Klara, A, Tautz, Jürgen, Hildburg, B and Muriel, M (2013) Antibacterial immune competence of honey bees (Apis mellifera) is adapted to different life stages and environmental risks. PLoS ONE 8, e66415.Google Scholar
Hendrickx, F (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. Journal of Applied Ecology 44, 340351.CrossRefGoogle Scholar
Hulbert, AJ and Abbott, SK (2012) Nutritional ecology of essential fatty acids: an evolutionary perspective. Australian Journal of Zoology 59, 369.CrossRefGoogle Scholar
Hurtado, MA, Reza, M, Ibarra, AM, Wille, M, Sorgeloos, P, Soudant, P and Palacios, E (2009) Arachidonic acid (20:4n-6) effect on reproduction, immunology, and prostaglandin E2 levels in Crassostrea corteziensis (Hertlein, 1951). Aquaculture 294, 300305.CrossRefGoogle Scholar
Jacobi, SK, Moeser, AJ, Corl, BA, Harrell, RJ and Bilksager, AT (2012) Dietary long-chain PUFA enhances acute repair of ischemia-injured intestine of suckling pigs. Journal of Nutrition 142, 12661271.CrossRefGoogle ScholarPubMed
James, MJ, Gibson, RA and Cleland, LG (2000) Dietary polyunsaturated fatty acids and inflammatory mediator production. The American Journal of Clinical Nutrition 71, 343S348S.CrossRefGoogle ScholarPubMed
Jeffries, KA, Dempsey, DR, Behari, AL, Anderson, RL and Merkler, DJ (2014) Drosophila melanogaster as a model system to study long-chain fatty acid amide metabolism. FEBS Letters 588, 15961602.CrossRefGoogle ScholarPubMed
Jin, M, Lu, Y, Yuan, Y, Li, Y, Qiu, H, Sun, P, Ma, HN, Ding, LY and Zhou, QC (2017) Regulation of growth, antioxidant capacity, fatty acid profiles, hematological characteristics and expression of lipid related genes by different dietary n-3 highly unsaturated fatty acids in juvenile lack sea bream (Acanthopagrus schlegelii). Aquaculture 471, 5565.CrossRefGoogle Scholar
Kalev, H, Dag, A and Shafir, S (2002) Feeding pollen supplements to honey bee colonies during pollination of sweet pepper in enclosures. American Bee Journal 142, 675679.Google Scholar
Kan, H, Kim, CH, Kwon, HM, Park, JW, Roh, KB and Lee, H (2008) Molecular control of phenoloxidase-induced melanin synthesis in an insect. Journal of Biological Chemistry 283, 2531625323.CrossRefGoogle Scholar
Khozin, GI, Cohen, Z, Pimenta, LM, Nechev, J and Zilberg, D (2006) Feeding with arachidonic acid-rich triacylglycerols from the microalga Parietochloris incisa improved recovery of guppies from infection with Tetrahymena sp. Aquaculture 255, 142150.CrossRefGoogle Scholar
Koven, W, Barr, Y, Lutzky, S, Ben-Atia, I, Weiss, R and Harel, M (2001) The effect of dietary arachidonic acid (20:4n-6) on growth, survival and resistance to handling stress in gilthead sea bream (Sparus aurata) larvae. Aquaculture 193, 107122.CrossRefGoogle Scholar
Kremen, C, Williams, NM and Thorp, RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences 99, 1681216816.CrossRefGoogle ScholarPubMed
Kumar, S, Christophides, GK, Cantera, R, Charles, B, Han, YS and Meister, S (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proceedings of the National Academy of Sciences 100, 1413914144.CrossRefGoogle ScholarPubMed
Lamiable, O and Imler, JL (2014) Induced antiviral innate immunity in Drosophila. Current Opinion in Microbiology 20, 6268.CrossRefGoogle ScholarPubMed
Lemaitre, B and Hoffmann, J (2007) The host defense of Drosophila melanogaster. Annual Review of Immunology 25, 697743.CrossRefGoogle ScholarPubMed
Li, M, Chen, LQ, Qin, JG, Yu, N, Chen, YL, Ding, ZL and Li, EC (2015) Growth, immune response and resistance to Aeromonas hydrophila of darkbarbel catfish Pelteobagrus vachelli fed diets with different linolenic acids, vitamins C and E levels. Aquaculture Research 22, 667674.Google Scholar
Luo, Z, Li, X, Bai, H and Gong, S (2008) Effects of dietary fatty acid composition on muscle composition and hepatic fatty acid profile in juvenile Synechogobius hasta. Journal of Applied Ichthyology 24, 116119.CrossRefGoogle Scholar
Luo, Z, Tan, XY, Li, X-D and Yin, GJ (2012) Effect of dietary arachidonic acid levels on growth performance, hepatic fatty acid profile, intermediary metabolism and antioxidant responses for juvenile Synechogobius hasta. Aquaculture Nutrition 18, 340348.CrossRefGoogle Scholar
Ma, LT, Wang, Y, Hang, XB, Wang, HF, Yang, WR and Xu, BH (2015) Nutritional effect of alpha-linolenic acid on honey bee colony development (Apis mellifera L.). Journal of Apicultural Science 59, 6372.CrossRefGoogle Scholar
Manning, R (2001) Fatty acids in pollen: a review of their importance for honey bees. Bee World 82, 6075.CrossRefGoogle Scholar
Naug, D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation 142, 23692372.CrossRefGoogle Scholar
Norambuena, F, Morais, S, Estévez, A, Bell, JG, Tocher, DR, Navarro, JC, Cerdà, J and Duncan, N (2013) Dietary modulation of arachidonic acid metabolism in Senegalese sole (Solea senegalensis) broodstock reared in captivity. Aquaculture 372, 8088.CrossRefGoogle Scholar
Nugent, C, Prins, JB, Whitehead, JP, Wentworth, JM, Chatterjee, VK and O'Rahilly, S (2001) Arachidonic acid stimulates glucose uptake in 3t3-l1 adipocytes by increasing glut1 and glut4 levels at the plasma membrane evidence for involvement of lipoxygenase metabolites and peroxisome proliferator-activated receptor γ. Journal of Biological Chemistry 276, 91499157.CrossRefGoogle ScholarPubMed
Piomelli, D (1993) Arachidonic acid in cell signaling. Current Opinion in Cell Biology 5, 274280.CrossRefGoogle ScholarPubMed
Pozzi, A and Zent, R (2009) Regulation of endothelial cell functions by basement membrane- and arachidonic acid-derived products. Wiley Interdisciplinary Reviews Systems Biology & Medicine 1, 254272.CrossRefGoogle ScholarPubMed
Randolt, K, Gimple, O, Geissend-Rfer, J, Reinders, J, Prusko, C and Mueller, MJ (2008) Immune-related proteins induced in the hemolymph after aseptic and septic injury differ in honey bee worker larvae and adults. Archives of Insect Biochemistry and Physiology 69, 155167.CrossRefGoogle ScholarPubMed
Rezek, TC, Watanabe, WO, Harel, M and Seaton, PJ (2010) Effects of dietary docosahexaenoic acid (22:6n-3) and arachidonic acid (20:4n-6) on the growth, survival, stress resistance and fatty acid composition in black sea bass Centropristis striata (Linnaeus 1758) larvae. Aquaculture Research 41, 13021314.CrossRefGoogle Scholar
Schmidt, LS, Schmidt, JO, Rao, H, Wang, W and Xu, L (1995) Feeding preference and survival of young worker honey-bees (Hymenoptera, Apidae) fed rape, sesame, and sunflower pollen. Journal of Economic Entomology 88, 15911595.CrossRefGoogle Scholar
Shahkar, E, Yun, H, Lee, S, Kim, DJ, Kim, SK, Lee, BI and Bai, SC (2016) Evaluation of the optimum dietary arachidonic acid level and its essentiality based on growth and non-specific immune responses in Japanese eel, Anguilla japonica. Aquaculture 452, 209216.CrossRefGoogle Scholar
Sharma, P, Kumar, V, Sinha, AK, Ranjan, J, Kithsiri, HMP and Venkateshwarlu, G (2010) Comparative fatty acid profiles of wild and farmed tropical freshwater fish rohu (Labeo rohita). Fish Physiology & Biochemistry 36, 411417.CrossRefGoogle Scholar
Shen, LR, Lai, CQ, Feng, X, Parnell, LD, Wan, JB, Wang, JD, Li, D, Ordovas, JM and Kang, JX (2010) Drosophila lacks c20 and c22 PUFAs. The Journal of Lipid Research 51, 29852992.CrossRefGoogle ScholarPubMed
Stanley-Samuelson, DW and Pedibhotla, VK (1996) What can we learn from prostaglandins and related eicosanoids in insects. Insect Biochemistry and Molecular Biology 26, 223234.CrossRefGoogle ScholarPubMed
Stanley, D (2011) Eicosanoids: progress towards manipulating insect immunity. Journal of Applied Entomology 135, 534545.CrossRefGoogle Scholar
Stoate, C, Boatman, ND, Borralho, RJ, Carvalho, CR, Snoo, GRD and Eden, P (2001) Ecological impacts of arable intensification in Europe. Journal of Environmental Management 63, 337365.CrossRefGoogle ScholarPubMed
Tallima, H and Ridi, RE (2018) Arachidonic acid: physiological roles and potential health benefits – a review. Journal of Advanced Research 11, 3341.CrossRefGoogle ScholarPubMed
Tian, J, Ji, H, Oku, H and Zhou, J (2014) Effects of dietary arachidonic acid (ARA) on lipid metabolism and health status of juvenile grass carp, Ctenopharyngodon idellus. Aquaculture 430, 5765.CrossRefGoogle Scholar
Vanbergen, AJ (2013) Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology & the Environment 11, 251259.CrossRefGoogle Scholar
Villalta, M, Estévez, A and Bransden, MP (2005) Arachidonic acid enriched live prey induces albinism in Senegal sole (Solea senegalensis) larvae. Aquaculture 245, 193209.CrossRefGoogle Scholar
Wang, SM, Chen, SL and Cui, YB (1993) On the procedures of chloroform-methanol extraction for the determination of lipid content of fish samples. Acta Hydrobiologica Sinica 17, 193196.Google Scholar
Wang, Y, Ma, L, Zhang, W, Cui, X, Wang, H and Xu, B (2016) Comparison of the nutrient composition of royal jelly and worker jelly of honey bees (Apis mellifera). Apidologie 47, 4856.CrossRefGoogle Scholar
Willey, S, Bengtson, DA and Harel, M (2003) Arachidonic acid requirements in larval summer flounder, Paralichthys dentatus. Aquaculture International 11, 131149.CrossRefGoogle Scholar
Wu, FC and Chen, HY (2012) Effects of dietary linolenic acid to linoleic acid ratio on growth, tissue fatty acid profile and immune response of the juvenile grouper Epinephelus malabaricus. Aquaculture 324, 324325.Google Scholar
Xu, H, Ai, Q, Mai, K, Xu, W, Wang, J, Ma, H, Zhang, WB, Wang, XJ and Liufu, ZG (2010) Effects of dietary arachidonic acid on growth performance, survival, immune response and tissue fatty acid composition of juvenile Japanese sea bass, Lateolabrax japonicus. Aquaculture 307, 7582.CrossRefGoogle Scholar
Yang, YT (2014) Fatty Acid Profiles in 20 Different Species of Bee Pollens (Dissertation). Chinese Academy of Agricultural Sciences, Beijing, China.Google Scholar
Yuan, YH, Li, SL, Mai, KS, Xu, W, Zhang, YJ and Ai, QH (2015) The effect of dietary arachidonic acid (ARA) on growth performance, fatty acid composition and expression of ARA metabolism-related genes in larval half-smooth tongue sole (Cynoglossus semilaevis). The British Journal of Nutrition 113, 15181530.CrossRefGoogle Scholar
Zaytoon, AA, Matsuka, M and Sasaki, M (1988) Feeding efficiency of pollen substitutes in a honeybee colony: effect of feeding site on royal jelly and queen production. Applied Entomology & Zoology 23, 481487.CrossRefGoogle Scholar
Zhang, WX, Chen, WF, Li, ZF, Ma, LT, Yu, J, Wang, HF, Liu, ZG and Xu, BH (2018) Identification and characterization of three new cytochrome p450 genes and the use of RNA interference to evaluate their roles in antioxidant defense in Apis cerana cerana fabricius. Frontiers in Physiology 15, 9.Google Scholar
Zuo, R, Ai, Q, Mai, K, Xu, W, Wang, J, Xu, H, Liufu, Z and Zhang, Y (2012) Effects of dietary n-3 highly unsaturated fatty acids on growth, nonspecific immunity, expression of some immune related genes and disease resistance of large yellow croaker (Larmichthys crocea) following natural infestation of parasites (Cryptocaryon irritans). Fish & Shellfish Immunology 32, 249258.CrossRefGoogle Scholar