**Author details**

Subhankar Gurung and Arun Chettri\* Taxonomy and Biodiversity Lab, Department of Botany, Sikkim University, Gangtok, Sikkim, India

\*Address all correspondence to: achettri01@cus.ac.in

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Threat to* Citrus *in a Global Pollinator Decline Scenario: Current Understanding of Its… DOI: http://dx.doi.org/10.5772/intechopen.101159*

### **References**

[1] Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, et al. Safeguarding pollinators and their values to human well-being. Nature. 2016;**540**:220-229. DOI: 10.1038/nature20588

[2] Das A, Sau S, Pandit MK, Saha K. A review on: Importance of pollinators in fruit and vegetable production and their collateral jeopardy from agro-chemicals. Journal of Entomology and Zoology Studies. 2018;**6**(4):1586-1591

[3] Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B: Biological Sciences. 2007;**274**:303-313

[4] Sundriyal M, Sundriyal RC. Wild edible plants of the Sikkim Himalaya: Nutritive values of selected species. Economic Botany. 2004;**58**:286-299. DOI: 10.1663/0013-0001(2004) 058[0286,WEPOTS]2.0.CO;2

[5] IPBES. The Assessment Report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on Pollinators, Pollination and Food Production. Bonn, Germany: Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services; 2016

[6] Greenleaf SS, Kremen C. Wild bees enhance honey bees' pollination of hybrid sunflower. Proceedings of the National Academy of Sciences of the United States of America. 2006; **103**:13890-13895. DOI: 10.1073/pnas. 0600929103

[7] Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM. The second silent spring? Nature. 1999;**400**:611-612

[8] Tscharntke T, Kelin AM, Kruess A, Steffan-Dewenter I, Thies C. Landscape perspective on agricultural intensification and biodiversityecosystem service management. Ecology Letters. 2005;**8**:857-874

[9] Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller Edwards M, Peeters T, Schaffers AP, et al. Parallel declines in pollinators and insectpollinated plans in Britain and the Netherlands. Science. 2006;**313**:351-354

[10] Rathcke B. Competition and facilitation among plants for pollination. In: Real L, editor. Pollination Biology. London, UK: Academic Press; 1983. pp. 305-329

[11] Rodrigo J, Herrero M. Evaluation of pollination as the cause of erratic fruit set in apricot 'Moniqui'. Journal of Horticultural Science. 1996;**71**:801-805

[12] Partap UMA, Partap TEJ, Yonghua, HE. Pollination failure in apple crop and farmers' management strategies in Hengduan Mountains. China: Acta Horticulturae. 2000;**561**:225-230

[13] Corbet SA. Which bees do plants need? In: Matheson A, Buchmann SL, O'Toole C, Westrich P, Williams JH, editors. The Conservation of Bees. London, UK: Academic Press; 1991. pp. 105-114

[14] Williams IH. The dependence of crop production within the European Union on pollination by honeybees. Agricultural Zoological Review. 1994;**6**:229-257

[15] Kevan PG, Philips T. The economics of pollinator declines: Assessing the consequences. Conservation Ecology. 2001;**5**:8

[16] Ghazoul J. Buzziness as usual? Questioning the global pollination crisis. Trends in Ecology and Evolution. 2005; **20**:367-373

[17] van der JP S, Vaage NS. Pollinators and global food security: The need for holistic global stewardship. Food Ethics. 2016;**1**:75-91

[18] Steffan-Dewenter I, Potts SG, Packer L. Pollinator diversity and crop pollination services are at risk. Trends in Ecology and Evolution. 2005;**20**:651-652

[19] Klein AM, Vaissiere BE, Cane J, Steffan-Dewenter I, Cunningham S, Kremen C, et al. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B: Biological Sciences. 2006;**274**(1608):303-313. DOI: 10.1098/rspb.2006.3721

[20] Casas A, Valiente-Banuet A, Rojas-Martinez A, Dávila P. Reproductive biology and the process of domestication of the columnar cactus *Stenocereus stellatus* in central Mexico. American Journal of Botany. 1999; **86**:534-542

[21] Casas A, Otero-Arnaiz A, Perez-Negron E, Valiente-Banuet A. In situ management and domestication of plants in Mesoamerica. Annals of Botany. 2007;**100**:1101-1115

[22] McGregor SE. Insect pollination of cultivated crop plants. In: Agriculture Handbook 496. USA: USDA-ARS; 1976. p. 395

[23] Webber J, Batchelor LD. The Citrus Industry. 2nd ed. Berkeley and Los Angeles: University of California Press; 1943

[24] Halder S, Ghosh S, Khan R, Khan AA, Perween T, Hasan MA. Role of pollination in fruit crops: A Review. The Pharma Innovation Journal. 2019;**8**(5):695-702

[25] Roubik DW. Pollination of Cultivated Plants in the Tropics. Rome: FAO Agricultural Service Bulletin; 1995 [26] Futch SH, Jackson LK. Pollination of Citrus Hybrids. Florida Cooperative Extension Service IFAS. USA: University of Florida; Fact Sheet No. HS-102. 2003. p. 2

[27] Iwamasa M, Oba Y. Seedlessness due to self-incompatibility in Egami-Buntan, a Japanese pummel cultivar. Agricultural Bulletin of Saga University. 1980;**49**:39-45

[28] Li SJ. Self-incompatibility in 'Matou' wentan (*Citrus grandis* (L.) Osb.). HortScience. 1980;**15**:298-300

[29] Sanford RL, Paaby P, Luvall JC, Phillips E. Climate, geomorphology and aquatic ecosystems. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS, editors. La Selva: Ecology and Natural History of a Neotropical Rain Forest. University of Chicago Press, Chicago, Illinois: USA; 2003. pp. 161-182

[30] Krezdorn AH. Citrus Flowering, Fruit Set and Development. Lake Alfred, FL: Citrus Research and Education Center; 1986

[31] Burger DW. Pollination effects on fruit production of 'Star Ruby' grapefruit (*Citrus paradisi* Macf.). Scientia Horticulturae. 1985;**25**:71-76

[32] Rahman A. Apiculture. In: Kumar AT, Pradhan S, editors. Handbook of Agriculture. Indian Council of Agricultural Research: New Delhi; 2006. pp. 509-529

[33] van Engelsdorp D, Hayes J Jr, Underwood RM, Pettis J. A survey of honeybee colony losses in the U.S., Fall 2007 to Spring 2008. PLos One. 2008;**3**:e4071. DOI: 10.1371/journal. pone.0004071

[34] Potts SG, Roberts SPM, Dean R, Marris G, ABrown M, Jones R, et al. Declines of managed honeybees and beekeepers in Europe? Journal of Apicultural Research. 2010;**49**:15-22

*Threat to* Citrus *in a Global Pollinator Decline Scenario: Current Understanding of Its… DOI: http://dx.doi.org/10.5772/intechopen.101159*

[35] Garibaldi LA et al. Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science. 2013;**339**:1608-1611

[36] Thompson CE, Biesmeijer JC, Allnutt TR, Pietravalle S, Budge GE. Parasite pressures on feral honeybees (*Apis mellifera* sp.). PLoS One. 2014;**9**:e105164. DOI: 10.1371/journal. pone.0105164

[37] Kraus B, Page REJ. Effect of *Varroa jacobsoni* (Mesostigmata: Varroidae) on feral *Apis mellifera* (Hymenoptera: Apidae) in California. Environment Entomology. 1995;**24**:1473-1480

[38] Hung JKL, Kingston JM, Albrecht M, Holway DA, Kon JR. The worldwide importance of honeybees as pollinators in natural habitats. Proceedings of Royal Society B. 2017;**285**:20172140. DOI: 10.1098/ rspb.2017.2140

[39] Thomson D. Competitive interactions between the invasive European honeybee and native bumblebees. Ecology. 2004;**85**:458-470. DOI: 10.1890/02-0626

[40] Thomson DM. Local bumblebee decline linked to recovery of honeybees, drought effects on floral resources. Ecology Letters. 2016;**19**:1247-1255. DOI: 10.1111/ele.12659

[41] Gross CL, Mackay D. Honeybees reduce fitness in the pioneer shrub *Melastoma affine* (Melastomaceae). Biological Conservation. 1998;**86**:169- 178. DOI: 10.1016/SOOO6-3207(98) 00010-X

[42] Cholis MN, Atmowidi TA, Kahono S. The diversity and abundance of visitor insects on pummel (*Citrus maxima* (burm) Merr) cv. Nambangan. Journal of Entomology and Zoology Studies. 2020;**8**(4):344-351

[43] Free JB. Insect Pollination of Crops. New York: Academic Press; 1970

[44] Zhang S, Liang M, Wang N, Xu Q, Xiuxin D, Chai L. Reproduction in woody perennial Citrus: An update on nucellar embryony and selfincompatibility. Plant Reproduction. 2018;**31**:43-57

[45] Hearn GH, Watkins WG, Bishop RK. Orange nectar and pollen in relation to bee activity. Journal of Economic Entomology. 1942;**35**:321-323

[46] Reece PC, Hearn CJ, Gardner FE. Nova tangelo—an early maturing tangerine hybrid. Proceedings of the Florida State Horticultural Society. 1964;**77**:109

[47] Cameron JW, Frost HB. Genetics, breeding and nucellar embryony. In: Reuther W, Webber HJ, Batchelor LD, editors. The Citrus Industry. Revised ed. Vol. II. Berkely: Div. Agric. Sci., University of California; 1968, Chapter 5

[48] Atawia AR, Abd EL-Latif FM, EL-Badawy HE, Abo-Aziz AB, Abou Rayya MSM, Baiea MHM, et al. Effect of various pollination treatments on yield characteristics and fruit quality of shaddock fruits. International Journal of Scientific & Engineering Research. 2016;**7**(5):1-9

[49] Lacarelle A, Miedzyrzecki C. New contributions on the study of clementines, Morocco. In: Experimentation Fruitiere et Maraichere, Rabat, Morocco. Edition Terre Marocaine ed. France; 1937. p. 22

[50] Mesejo C, Martinez-Fuentes A, Reig C, Agusti M. The effective pollination period in 'Clemenules' mandarin, 'Owari' *Satsuma mandarin* and 'Valenia' sweet orange. Plant Science. 2007;**173**(2):223-230

[51] Hearn CJ, Reece PC. Pollination needs of Page, Lee, Nova and Robinson Citrus hybrids. Citrus Indus. 1967; **48**(4):19-23

[52] Gambetta G, Gravina A, Fasiolo C, Fornero C, Galiger S, Inzaurralde C, et al. Self-incompatibility, parthenocarpy and reduction of seed presence in 'Afourer' mandarin. Scientia Horticulturae. 2013;**164**:183-188

[53] Reece PC, Register PD. Influence of pollinators on fruit set of Robinson and Osceola tangerine hybrids. Florida State Horticultural Society Proceedings. 1961;**74**:64-106

[54] Miwa T. On pollination, fertilization phenomena and problems connected with fruit drop in the hyuganatsu mandarin. Bulletin of the Miyazaki University. Natural Science. 1951;**2**:2-67

[55] Zhgenti SK. Pollination of the Japanese persimmon and mandarin orange. In: Krischunas IV, Gubin AF, editors. Pollination of Agricultural Plants. Russia: Moskva, Gos. Izd-vo SelKhoz Lit-ry; 1956. pp. 193-199

[56] Zavrashvili RM. Importance of nectar in flowers of mandarin orange Unshiu. Soobscenija Akademii Nauk Gruzinskoj. 1967;**45**:1, 205-212

[57] Zavrashvili RM. Influence of bees on the yield of citrus trees on the commercial plantations of Georgia. In: 21st International Apiculture Congress Proceedings College Park, Md. USA. 1967. pp. 450-451

[58] Vardi A, Levin I, Carmin N. Induction of seedlessness in citrus: From classical techniques to emerging biotechnological approaches. Journal of the American Society for Horticultural Sciences. 2008;**133**:117-126

[59] Hearn CJ, Reece PC, Fenton R. Self-incompatibility and the effects of different pollen sources upon fruit characteristics of four citrus hybrids. In: 1st International Symposium Citrus Symposium Proceedings. USA: University of California; Vol. 1. 1969. pp. 183-187

[60] Mustard MJ. Progress Report on the Unfruitfulness of the Minneola Tangelo; Ceiba. 1961;**9**(1):45-48

[61] Ngo BX, Wakana A, Park SM, Nada Y, Fukudome I. Pollen tube behaviours in self-incompatible and self-compatible *Citrus* cultivars. Journal of the Faculty of Agriculture, Kyushu University. 2001;**45**:443-457

[62] Yamamoto M, Kubo T, Tominaga S. Self- and cross-incompatibility of various *Citrus* accessions. Journal of the Japanese Society for Horticultural Science. 2006;**75**(5):372-378

[63] Malerbo-Souza DT, Nogueira-Couto RH, Couto LA. Pollination in orange sweet crop (*Citrus sinensis* L. Osbeck, var. Pera-Rio). Brazilian Journal of Veterinary Research and Animal Science. 2003;**40**(4):237- 242. DOI: 10.1590/S1413-95962003 00040001

[64] Malerbo-Souza DT, Nogueira-Couto RH, Couto LA. Honeybee attractants and pollination in sweet orange, *Citrus sinensis* (L.) Osbeck, var. Pera-Rio. Journal of Venomous Animals and Toxins including Tropical Diseases. 2004;**10**(2):144-153

[65] Francke R, Jorge A, Mathieu JM. Effects of insect pollinators on the production of valencia oranges: The honey bee and its effects on citrus production. Agronomia (Monterrey). 1969;**122**:7

[66] Sanford MT. RF-AA092. Pollination of Citrus by Honeybees. Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences. USA: University of Florida; 1992

[67] Koltunow AM, Soltys K, Nito N, McClure S. Anther, ovule, seed and nucellar embryo development of *Citrus sinensis* cv. Valencia. Canadian Journal of Botany. 1995;**73**:1567-1582

*Threat to* Citrus *in a Global Pollinator Decline Scenario: Current Understanding of Its… DOI: http://dx.doi.org/10.5772/intechopen.101159*

[68] Krezdorn AH. Fruit setting problems in Citrus. American Journal of Horticultural Science Carribean Region Proceedings. 1965;**9**(13):85-92

[69] Krezdorn AH. Pollination requirements of Citrus. In: The Indispensable Pollinators. Vol. 127. USA: Arkansas Agriculture Extension Service Misc. Pub.; 1970. pp. 211-218

[70] Atkins EL. Honeybees and agriculture. California Citrograph. 1963;**49**(2):81-82

[71] Wafa AK, Ibrahim SH. Effect of the honeybee as a pollinating agent on the yield of orange. Elfelaha. Egypt: Cairo University; 1960:AA-448/63

[72] Davenport TL. Citrus flowering. Horticultural Reviews. 1986;**12**:349-408

[73] Busch JW, Schoen DJ. The evolution of self-incompatibility when mates are limiting. Trend in Plant Science. 2008;**13**(3):128-136

[74] Aala FT. Effects of Hand pollination on the production of Siamese pummel. Phillipines Journal of Agriculture. 1953;**18**(1-4):101-113

[75] Hoang TT, Nguyen TH, Le HT, Ngo BX, Wakana A. Self-incompatibility in pummel [*Citrus grandis* (L.) Osbeeck] with focus on Vietnamese cultivars with or without parthenocarpy. Journal of the Faculty of Agriculture, Kyushu University. 2014;**59**:65-70

[76] Chacoff NP, Aizen MA. Pollination requirements of pigmented grapefruit (*Citrus paradisi* Macf.) from Northwestern Argentina. Crop Science. 2007;**47**:1-9

[77] Krezdorn AH. Pollination requirements of Citrus. Citrus Indus. 1972;**53**:5-7, 28

[78] Wright N. Pollination and the seediness of marsh grapefruit.

Proceedings of the Agricultural Society of Trinidad and Tobago. 1937;**37**:51-60

[79] Crane E, Walker P. Pollination Directory for World Crops. Bucks, UK: International Bee Research Association; 1984

[80] Karmakar P. Pollination biology of *Citrus aurantiifolia* (Christm.) Swingle: A medicinally important fruit plant. International Journal of Innovative Research and Development. 2013; **2**(7):138-142

[81] Soost RK, Cameron JW. 'Oroblanco' a tripliod pummel-grapefruit hybrid. HortScience. 1980;**15**:667-669

[82] Abrahimy Y, Haji VS. Comparison of Minab Lime, Rodan Lime and Persian Lime Cultivars on Different Citrus Rootsocks in Minab, Hormozgan, Iran. Bandar Abas (Iran): Iran Citrus Research Institute—ICRI; 2004. Available from: http://www.agrisis.org

[83] Motial VS. Fruit-set studies in sweet lime. Indian Academy of Science Proceedings Section B. 1964; **60**(6):371-379

[84] Haldhar SM, Kumar R, Samadia DK, Singh B, Singh H. Role of insect pollinators and pollinizers in arid and semi-arid horticultural crops. Journal of Agriculture and Ecology. 2018;**5**:1-25

[85] Hossain MI, Rabbani MG. Study on the cross compatibility of some lemon genotypes (*Citrus limon* L.). Bangladesh Journal of Agriculture Research. 2011;**36**(2):241-246

[86] Webber HJ. Influence of pollination on set of fruit in citrus. California Citrog. 1930;**15**(7):304:322-323

[87] Zhang SW, Huang GX, Ding F, He XH, Pan JC. Mechanism of seedlessness in a new lemon cultivar 'Xiangshui' [*Citrus limon* (L.) Burm, F.]. Sex Plant Reproduction. 2012; **25**:337-345

[88] Zavrashvili RM. Bees and the citrus crop. Pchelovodstvo. 1964;**84**(8):19

[89] Moore GA. Oranges and lemons: Clues to the taxonomy of *Citrus* from molecular markers. Trends in Genetics. 2001;**50**:670-672

[90] Scora RW. On the history an origin of *Citrus*. Bulletin of the Torey Botanical Club. 1975;**102**:369-375

[91] Barkley NA, Roose ML, Krueger RR, Federici CT. Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theoretical and Applied Genetics. 2006;**112**:1519-1531

[92] Luro FN, Venturini G, Costantino J, Paolini J, Ollitrault P, Costa J. Genetic and chemical diversity of citron (*Citrus medica* L.) based on nuclear and cytoplasmic markers and leaf essential oil composition. Phytochemistry. 2012;**77**:186-196

[93] Goldschmidt EE. Citron propagation: Seeds or cuttings? Alon Hanoeta. 2009;**63**:44-46. (Hebrew)

## **Chapter 5**
