收稿日期: 2020-07-27
录用日期: 2020-11-05
网络出版日期: 2020-11-11
基金资助
国家自然科学基金(31970410);国家自然科学基金(31672315);辽宁省重点研发计划(2018103004);辽宁省自然科学基金(20170540816);辽宁省教育厅青年项目(LQN201701);沈阳师范大学重大孵化项目(ZD201521)
Advances in spider ballooning research
Received date: 2020-07-27
Accepted date: 2020-11-05
Online published: 2020-11-11
种群扩散能够避免生物类群在同一栖息地中的资源竞争和同类相残, 促进基因流动, 具有重要的进化和生态意义。相比于昆虫的迁飞行为, 某些不具翅的节肢动物也能够借助细丝的作用而实现远距离扩散, 即飞航。蜘蛛为肉食性动物, 是陆地生态系统的重要组成部分, 在生态系统中防控害虫方面作用显著。飞航是蜘蛛的一种重要扩散方式, 在其物种形成、生态位分化及害虫防控等方面具有重要意义, 但有关其飞航扩散的报道较少。本文回顾了蜘蛛飞航的研究历程, 大致可分为三个阶段; 总结了其研究现状, 包括飞航蜘蛛的优势类群及特征、飞航过程中的三个环节(即起飞、空中航行和降落)及影响因子、两种飞航机制及四种相关模型、飞航蜘蛛采集和研究方法。同时基于过往研究, 指出了未来蜘蛛飞航研究的重点领域: 加强飞航蜘蛛类群鉴定工作, 继续深度挖掘飞航数据与环境因子间的关系, 探索蜘蛛飞航的全过程(包括起飞、空中航行和降落), 更加明确蜘蛛飞航作为一种扩散方式的意义。本综述将为蜘蛛飞航的知识普及、资源保护和利用等方面提供重要参考。
武鹏峰, 崔淑艳, Abid Ali, 郑国 . 蜘蛛飞航研究进展[J]. 生物多样性, 2021 , 29(4) : 517 -530 . DOI: 10.17520/biods.2020301
Backgrounds: Population dispersal is important for avoiding resource competition and cannibalism in the same habitat, and for ensuring gene flow which has an evolutionary and ecological importance. Some wingless arthropods can achieve long-distance dispersal using their filaments (which is called ballooning). Spiders are important for terrestrial ecosystems and can play a significant role in pest control due to being carnivores. Ballooning is one of the most important dispersal modes for spiders and is believed to be important for speciation, niche differentiation and pest control. Yet, focus on the role ballooning plays for dispersal has been given less attention.
Progresses: In this study, we review the research history of spider ballooning (which can be categorized into three periods) and summarize the progress that had been made which includes: the dominant groups and characteristics of ballooning spiders, understanding the three stages of ballooning (take-off, flight, and setting) and influencing factors, two prevalent theories explaining the mechanism of ballooning with four related models, and information on the collection of spiders as well as other research methods.
Prospects: In order to exclusively understand the significance of ballooning for population dispersal, research emphases are being put forward to strengthen the identification of ballooning spiders, better understanding the relationship between ballooning data with environmental factors, and to explore the whole process of spider ballooning (e.g., take-off, flight, and setting). We hope this study will serve as an important reference for knowledge popularization, resource protection and utilization of ballooning.
| [1] | Barth FG ( 1985) Slit sensilla and the measurement of cuticular strains. In: Neurobiology of Arachnids (ed. Barth FG), pp. 162-188. Springer, Berlin. |
| [2] | Barth FG (2000) How to catch the wind: Spider hairs specialized for sensing the movement of air. Naturwissenschaften, 87,51-58. |
| [3] | Bell JR, Bohan DA, Shaw EM, Weyman GS (2005) Ballooning dispersal using silk: World fauna, phylogenies, genetics and models. Bulletin of Entomological Research, 95,69-114. |
| [4] | Bishop L (1990) Meteorological aspects of spider ballooning. Environmental Entomology, 19,1381-1387. |
| [5] | Bishop L, Riechert SE (1990) Spider colonization of agroecosystems: Mode and source. Environmental Entomology, 19,1738-1745. |
| [6] | Blackwall J (1827) Observations and experiments, made with a view to ascertain the means by which the spiders that produce gossamer effect their aerial excursions. Transactions of the Linnean Society of London, 15,449-459. |
| [7] | Blandenier G, Fürst PA (1998) Ballooning spiders caught by a suction trap in an agricultural landscape in Switzerland. Proceedings of the 17th European Colloquium of Arachnology, Edinburgh. |
| [8] | Blandenier G (2009) Ballooning of spiders (Araneae) in Switzerland, general results from an eleven-year survey. Arachnology, 14,308-316. |
| [9] | Blandenier G, Bruggisser OT, Rohr RP, Bersier LF (2013) Are phenological patterns of ballooning spiders linked to habitat characteristics? Journal of Arachnology, 41,126-132. |
| [10] | Blandenier G, Bruggisser OT, Bersier LF (2014) Do spiders respond to global change? A study on the phenology of ballooning spiders in Switzerland. Ecoscience, 21,79-95. |
| [11] | Bonte D, Vandenbroecke N, Lens L, Maelfait JP (2003a) Low propensity for aerial dispersal in specialist spiders from fragmented landscapes. Proceedings of the Royal Society of London B, 270,1601-1607. |
| [12] | Bonte D, Deblauwe I, Maelfait JP (2003b) Environmental and genetic background of tiptoe-initiating behaviour in the dwarfspider Erigone atra. Animal Behaviour, 66,169-174. |
| [13] | Bonte D, Travis JMJ, De Clercq N, Zwertvaegher I, Lens L (2008) Thermal conditions during juvenile development affect adult dispersal in a spider. Proceedings of the National Academy of Sciences, USA, 105,17000-17005. |
| [14] | Bonte D (2013) Cost-benefit balance of dispersal and the evolution of conditional dispersal strategies in spiders. In: Spider Ecophysiology ( ed ed. Nentwig W), pp.67-78. Springer, London. |
| [15] | Bristowe WS (1939) The Comity of Spiders. Quarith Ltd, London. |
| [16] | Chen YX (1986) Observation of habits of ballooning spiders. Chinese Journal of Zoology, 21(3),37-39. (in Chinese) |
| [16] | [ 陈毓祥 (1986) 蜘蛛飞航习性观察. 动物学杂志, 21(3),37-39. ] |
| [17] | Cho M, Neubauer P, Fahrenson C, Rechenberg I (2018) An observational study of ballooning in large spiders, Nanoscale multifibers enable large spiders’ soaring flight. PLoS Biology, 16,e2004405. |
| [18] | Clarke D, Whitney H, Sutton G, Robert D (2013) Detection and learning of floral electric fields by bumblebees. Science, 340,66-69. |
| [19] | Coyle FA (1983) Aerial dispersal by mygalomorph spiderlings (Araneae, Mygalomorphae). Journal of Arachnology, 11,283-286. |
| [20] | Coyle FA (1985) Ballooning behaviour of Ummidia spiderlings (Araneae, Ctenizidae). Journal of Arachnology, 13,137-138. |
| [21] | Coyle FA, Greenstone MH, Hultsch AL, Morgan CE (1985) Ballooning mygalomorphs: Estimates of the masses of Sphodros and Ummidia ballooners (Araneae: Atypidae, Ctenizidae). Journal of Arachnology, 13,291-296. |
| [22] | Darwin CR (1845) Journal of Researches into the Natural History and Geology of the Countries Visited during the Voyage of H. M. S. Beagle Round the World, under the Command of Capt. Fitz Roy, R. N., 2nd edn. John Murray, London. |
| [23] | Dean DA, Sterling WL (1985) Size and phenology of ballooning spiders at two locations in Eastern Texas. Journal of Arachnology, 13,111-120. |
| [24] | Duffey E (1956) Aerial dispersal in a known spider population. Journal of Animal Ecology, 25,85-111. |
| [25] | Duffey E (1997) Spider adaptation to artificial biotopes: The fauna of percolating filter beds in a sewage treatment works. Journal of Applied Ecology, 34,1190-1202. |
| [26] | Felt EP (1928) Dispersal of insects by air currents. New York State Museum Bulletin, 274,59-129. |
| [27] | Foelix RF ( In: In: Neurobiology of Arachnids ( ed ed. Barth FG), 1985) Mechano- and chemoreceptive sensilla. In: Neurobiology of Arachnids (ed. Barth FG), pp. 118-137 . Springer, Berlin. |
| [28] | Foelix RF (2011) Biology of Spiders, 3rd edn. Oxford University Press, Oxford. |
| [29] | Follner K, Klarenberg AJ (1995) Aeronautic behaviour in the wasp-like spider, Argiope bruennichi (Scopoli) (Araneae, Argiopidae). Proceedings of the 15th European Colloquium of Arachnology, Ceske Budejovice. |
| [30] | Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK (2012) Long-distance dispersal: A framework for hypothesis testing. Trends in Ecology and Evolution, 27,47-56. |
| [31] | Glick PA (1939) The distribution of insects, spiders, and mites in the air. United States Department of Agriculture, Technical Bulletin, 673,1-150. |
| [32] | Gorham PW (2013) Ballooning spiders, the case for electrostatic flight. https://arxiv.org/pdf/1309.4731v1.pdf. (accessed on 2020-07-10) |
| [33] | Greenstone MH (1982) Ballooning frequency and habitat predictability in two wolf spider species (Lycosidae, Pardosa). The Florida Entomologist, 65,83-89. |
| [34] | Greenstone MH, Morgan CE, Hultsch AL (1985) Spider ballooning: Development and evaluation of filed trapping methods (Araneae). Journal of Arachnology, 13,337-345. |
| [35] | Greenstone MH, Morgan CE, Hultsch AL (1987) Ballooning spiders in Missouri, USA, and New South Wales, Australia, family and mass distributions. Journal of Arachnology, 15,163-170. |
| [36] | Greenstone MH (1990) Meteorological determinants of spider ballooning: The roles of thermals vs. the vertical windspeed gradient in becoming airborne. Oecologia, 84,164-168. |
| [37] | Gressitt JL (1965) Biogeography and ecology of land arthropods of Antarctica. In: Biogeography and Ecology in Antarctica (eds van Miegham J, van Oye P), pp.431-490. Springer, Dordrecht. |
| [38] | Henschel JR, Schneider J, Lubin YD (1995) Dispersal mechanisms of Stegodyphus (Eresida): Do they balloon? Journal of Arachnology, 23,202-204. |
| [39] | Hogg B, Daane K (2018) Aerial dispersal ability does not drive spider success in a crop landscape. Ecological Entomology, 43,683-694. |
| [40] | Horner NV (1975) Annual aerial dispersal of jumping spiders in Oklahoma (Araneae, Salticidae). Journal of Arachnology, 2,101-105. |
| [41] | Humphrey JAC (1987) Fluid mechanic constraints on spider ballooning. Oecologia, 73,469-477. |
| [42] | Jiang XF, Zhang L, Cheng YX, Luo LZ (2016) Research advances and perspectives on migration-induced mechanisms promoting outbreaks of major Lepidopteran insect pests in China. Scientia Sinica Vitae, 46,565-572. (in Chinese with English abstract) |
| [42] | [ 江幸福, 张蕾, 程云霞, 罗礼智 (2016) 中国主要鳞翅目农业害虫迁飞致灾机制研究与展望. 中国科学: 生命科学, 46,565-572. ] |
| [43] | Johnson C (1960) A basis for a general system of insect migration and dispersal by flight. Nature, 186,348-350. |
| [44] | Kokko H, López-Sepulcre A (2006) From individual dispersal to species ranges: Perspectives for a changing world. Science, 313,789-791. |
| [45] | Larrivée M, Buddle CM (2011) Ballooning propensity of canopy and understorey spiders in a mature temperate hardwood forest. Ecological Entomology, 36,144-151. |
| [46] | Lee VMJ, Kuntner M, Li DQ (2015) Ballooning behavior in the golden orbweb spider Nephila pilipes (Araneae: Nephilidae). Frontiers in Ecology and Evolution, 3,1-5. |
| [47] | Marc PA, Canard A, Ysnel F (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agriculture, Ecosystems & Environment, 74,229-273. |
| [48] | Meijer J (1977) The immigration of spiders (Araneida) into a new polder. Ecological Entomology, 2,81-90. |
| [49] | Morley EL, Robert D (2018) Electric fields elicit ballooning in spiders. Current Biology, 28,2324-2330. |
| [50] | Murray J (1830) Researches in Natural History, 2nd edn. John Murray, London. |
| [51] | Nielsen E (1932) The Biology of Spiders. Levin & Munksgaard, Copenhagen. |
| [52] | Nyffeler M, Birkhofer K (2017) An estimated 400-800 million tons of prey are annually killed by the global spider community. The Science of Nature, 104,30. |
| [53] | Pearce S, Zalucki MP, Hassan E (2005) Spider ballooning in soybean and non-crop areas of southeast Queensland. Agriculture, Ecosystems & Environment, 105,273-281. |
| [54] | Postiglioni R, Aisenberg A, Carlozzi A, Bidegaray-Batista L (2017) The dark side of ballooning: Nocturnal aerial dispersal in wolf spiders from the South American coastline. Arachnology, 17,312-316. |
| [55] | Qiao GX, Qin QL, Liang HB, Cao YZ, Xu GQ, Gao ZL, Xu WJ, Wu YQ, Li XJ, Zhao ZW, Cheng XY (2011) A new aphid-monitoring network system based on suction trapping and development of “green techniques” for aphid management. Chinese Journal of Applied Entomology, 48,1596-1601. (in Chinese with English abstract) |
| [55] | [ 乔格侠, 秦启联, 梁红斌, 曹雅忠, 许国庆, 高占林, 徐伟钧, 武予清, 李学军, 赵章武, 成新跃 (2011) 蚜虫新型预警网络的构建及其绿色防控技术研究. 应用昆虫学报, 48,1596-1601. ] |
| [56] | Reling D, Taylor RAJ (1984) A collapsible tow net used for sampling arthropods by airplane. Journal of Economic Entomology, 77,1615-1617. |
| [57] | Reynolds AM, Bohan DA, Bell JR (2006) Ballooning dispersal in arthropod taxa with convergent behaviours: Dynamic properties of ballooning silk in turbulent flows. Biology Letters, 2,371-373. |
| [58] | Reynolds AM, Bohan DA, Bell JR (2007) Ballooning dispersal in arthropod taxa: Conditions at take-off. Biology Letters, 3,237-240. |
| [59] | Richter CJ (1970) Aerial dispersal in relation to habitat in eight wolf spider species (Pardosa, Araneae, Lycosidae). Oecologia, 5,200-214. |
| [60] | Salmon JT, Horner NV (1977) Aerial dispersion of spiders in North Central Texas. Journal of Arachnology, 5,153-157. |
| [61] | Schneider JM, Roos J, Lubin Y, Henschel JR (2001) Dispersal of Stegodyphus dumicola (Araneae, Eresidae): They do balloon after all! Journal of Arachnology, 29,114-116. |
| [62] | Sheldon KS, Zhao LH, Chuang A, Panayotova IN, Miller LA, Bourouiba L (2017) Revisiting the Physics of Spider Ballooning. Women in Mathematical Biology, 8,163-178. |
| [63] | Simonneau M, Courtial C, Pétillon J (2016) Phenological and meteorological determinants of spider ballooning in an agricultural landscape. Comptes Rendus Biologies, 339,408-416. |
| [64] | Song DX (1983) Ballooning spiders over the East China Sea. Chinese Journal of Zoology, 18(3),50. (in Chinese) |
| [64] | [ 宋大祥 (1983) 东海上空的飞航蜘蛛. 动物学杂志, 18(3),50. ] |
| [65] | Stevens T, Zhao LH, Courtney R, Zhang W, Miller L (2019) Flying spiders: Effects of the dragline length and the spider mass in free-fall. Proceedings of ASME-JSME-KSME 2019 8th Joint Fluids Engineering Conference, July 28-August 1, 2019, San Francisco. |
| [66] | Sunderland KD, Fraser AM, Dixon AFG (1986) Distribution of linyphiid spiders in relation to capture of prey in cereal fields. Pedobiologia, 29,367-375. |
| [67] | Suter RB (1991) Ballooning in spiders: Results of wind tunnel experiments. Ethology Ecology & Evolution, 3,13-25. |
| [68] | Suter RB (1999) An aerial lottery, the physics of ballooning in a chaotic atmosphere. Journal of Arachnology, 27,281-293. |
| [69] | Szymkowiak P, Górski G, Bajerlein D (2007) Passive dispersal in arachnids. Biological Letters, 44,75-101. |
| [70] | Thomas CFG (1996) Modeling aerial dispersal of linyphiid spiders. Aspects of Applied Biology, 46,217-222. |
| [71] | Thomas CFG, Jepson PC (1999) Differential aerial dispersal of linyphiid spiders from a grass and a cereal field. Journal of Arachnology, 27,294-300. |
| [72] | Thomas CFG, Brain P, Jepson PC (2003) Aerial activity of linyphiid spiders: Modelling dispersal distances from meteorology and behaviour. Journal of Applied Ecology, 40,912-927. |
| [73] | Thorbek P, Topping CJ, Sunderland KD (2002) Validation of a simple method for monitoring aerial activity of spiders. Journal of Arachnology, 30,57-64. |
| [74] | Toft S (1995) Two functions of gossamer dispersal in spiders? In: Arthropod Natural Enemies in Arable Land I: Density, Spatial Heterogeneity and Dispersal (eds Toft S, Riedel W), pp.257-268. Aarhus University Press, ?rhus, Denmark. |
| [75] | Tolbert WW (1977) Aerial dispersal behavior of two orb weaving spiders. Psyche, 84,13-27. |
| [76] | Topping CJ, Sunderland KD, Bewsey J (1992) A large improved rotary trap for sampling aerial invertebrates. Annals of Applied Biology, 121,707-714. |
| [77] | Topping CJ, Sunderland KD (1995) Methods for monitoring aerial dispersal by spiders. In: Arthropod Natural Enemies in Arable Land I: Density, Spatial Heterogeneity and Dispersal (eds Toft S, Riedel W), pp.245-256. Aarhus University Press, ?rhus, Denmark. |
| [78] | van Wingerden WKRE, Vugts HF (1974) Factors influencing aeronautic behaviour of spiders. Bulletin of the British Arachnology Society, 3,6-10. |
| [79] | Vugts HF, van Wingerden WKRE (1976) Meteorological aspects of aeronautic behavior of spiders. Oikos, 27,433-444. |
| [80] | Walter A, Bliss P, Moritz RFA (2005) The wasp spider Argiope bruennichi (Arachnida, Araneidae): Ballooning is not an obligate life history phase. Journal of Arachnology, 33,516-522. |
| [81] | Wang YN, Sun J, Yang WM (2020) A review on dispersal behavior of small mammals. Journal of Zhejiang Normal University (Natural Sciences), 43,66-71. (in Chinese with English abstract) |
| [81] | [ 王艳妮, 孙佼, 杨文敏 (2020) 小型哺乳动物的扩散行为研究进展. 浙江师范大学学报(自然科学版), 43,66-71. ] |
| [82] | Weyman GS (1993) A review of the possible causative factors and significance of ballooning in spiders. Ethology Ecology & Evolution, 5,279-291. |
| [83] | Weyman GS, Sunderland KD, Fenlon JS (1994) The effect of food deprivation on aeronautic dispersal behaviour (ballooning) in Erigone spp. spiders. Entomologia Experimentalis et Applicata, 73,121-126. |
| [84] | Weyman GS, Jepson PC, Sunderland KD (1995) Do seasonal changes in numbers of aerially dispersing spiders reflect population density on the ground or variation in ballooning motivation? Oecologia, 101,487-493. |
| [85] | Weyman GS, Sunderland KD, Jepson PC (2002) A review of the evolution and mechanisms of ballooning by spiders inhabiting arable farmland. Ethology Ecology & Evolution, 14,307-326. |
| [86] | Wickler W, Seibt U (1986) Aerial dispersal by ballooning in adult Stegodyphus mimosarum. Naturwissenschaften, 73,628-629. |
| [87] | Wilson CTR (1903) Atmospheric electricity. Nature, 68,102-104. |
| [88] | Woolley C, Thomas C, Hutchings L, Goodacre S, Hewitt G, Brooks S (2007) A novel trap to capture ballooning spiders. Journal of Arachnology, 35,307-312. |
| [89] | Woolley C, Thomas CFG, Blackshaw RP, Goodacre SL (2016) Aerial dispersal activity of spiders sampled from farmland in southern England. Journal of Arachnology, 44,347-358. |
| [90] | Yeargen KV (1975) Factors influencing the aerial dispersal of spiders (Arachnida: Araneida). Journal of the Kansas Entomological Society, 48,403-408. |
| [91] | Zhang SH ( Electricity and Magnetism, 2009) College Physics: Mechanics, 3rd edn. Tsinghua University Press, Beijing. (in Chinese) |
| [91] | [ 张三慧 (2009) 大学物理学: 力学、电磁学( 第3版). 清华大学出版社, 北京. ] |
| [92] | Zhao L, Panayotova IN, Chuang A, Sheldon KS, Bourouiba L, Miller LA (2017) Flying spiders: Simulating and modeling the dynamics of ballooning. Women in Mathematical Biology, 8,179-210. |
| [93] | Zheng G, Li XJ, Wang SX, Chen Q, Xu B, Xing X (2011) Community composition and its characteristics of ballooning spiders in east Liaoning Province of Northeast China. Chinese Journal of Ecology, 30,40-44. (in Chinese with English abstract) |
| [93] | [ 郑国, 李学军, 王淑贤, 陈强, 许彪, 邢星 (2011) 辽宁东部地区飞航蜘蛛的群落组成及特征. 生态学杂志, 30,40-44. ] |
| [94] | Zhou Y, Zhang HW, Wu KM (2020) Frequency of migration of agricultural pests across the Bohai Sea in northern China and a control strategy for these species. Chinese Journal of Applied Entomology, 57,233-243. (in Chinese with English abstract) |
| [94] | [ 周燕, 张浩文, 吴孔明 (2020) 农业害虫跨越渤海的迁飞规律与控制策略. 应用昆虫学报, 57,233-243. ] |
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