Abstract
Visual prey luring in animals is typically achieved by brightly colored body parts or excretions of the signal sender, and using signals from other organisms is rarely reported. However, certain species of kleptoparasitic Argyrodes spiders usually reside in the webs of Cyrtophora spiders, and their brightly colored bodies have been demonstrated to serve as a visual lure that attracts prey to host webs. The golden orb-web spider Nephila pilipes spins giant orb webs and also attracts web coinhabitants such as mate-seeking males and kleptoparasitic spider Argyrodes miniaceus. These two types of spiders have similar orange-red body coloration, leading us to investigate the function of this shared trait by manipulating their body color and recording the response of prey insects in the field using video cameras. Our results showed that, in both diurnal and nocturnal conditions, female N. pilipes webs with naturally colored male N. pilipes and A. miniaceus had a significantly higher prey attraction rate than those with body color altered coinhabitants. Specifically, A. miniaceus lure more prey at nighttime. These results indicate that the conspicuously colored web coinhabitants may potentially bring foraging benefits to the hosts through prey luring and provide new perspectives on the ecology and evolution of symbiotic relationships between animals.
Significance statement
It has been known that the body coloration of some spiders can lure prey to their webs, and even some kleptoparasitic Argyrodes spiders can lure prey to their hosts’ webs. However, whether the conspicuous body coloration of mate-seeking males plays any role remains untested. We showed for the first time that the orange-red body coloration shared by male Nephila pilipes and kleptoparasitic Argyrodes miniaceus spiders inhabiting webs of female N. pilipes can visually lure prey. Findings of this study can potentially strengthen our current understanding of the function of body coloration of spiders, shed light on evolution of spider body coloration, and provide new perspectives on symbiotic relationships between animals.
Similar content being viewed by others
Data availability
Raw data are available from the Dryad Digital Repository https://doi.org/10.5281/zenodo.6820697.
References
Blamires SJ, Lai CH, Cheng RC, Liao CP, Shen PS, Tso IM (2012) Body spot coloration of a nocturnal sit-and-wait predator visually lures prey. Behav Ecol 23:69–74. https://doi.org/10.1093/beheco/arr152
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510. https://doi.org/10.1146/annurev.ento.46.1.471
Bush AA, Yu DW, Herberstein ME (2008) Function of bright coloration in the wasp spider Argiope bruennichi (Araneae: Araneidae). Proc Roy Soc B 275:1337–1342. https://doi.org/10.1098/rspb.2008.0062
Caves EM, Brandley NC, Johnsen S (2018) Visual acuity and the evolution of signals. Trends Ecol Evol 33:358–372. https://doi.org/10.1016/j.tree.2018.03.001
Cheng RC, Tso IM (2007) Signaling by decorating webs: luring prey or deterring predators? Behav Ecol 18:1085–1091. https://doi.org/10.1093/beheco/arm081
Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–543. https://doi.org/10.1007/BF00199331
Chuang CY, Yang EC, Tso IM (2007) Diurnal and nocturnal prey luring of a colorful predator. J Exp Biol 210:3830–3837. https://doi.org/10.1242/jeb.007328
Craig CL (1986) Orb-web visibility: the influence of insect flight behaviour and visual physiology on the evolution of web designs within the Araneoidea. Anim Behav 34:54–68. https://doi.org/10.1016/0003-3472(86)90006-0
Dyer AG, Chittka L (2004) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227. https://doi.org/10.1007/s00114-004-0508-x
Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MGP, Simonov V, Wong BBM (2012) Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc R Soc B 279:3606–3615. https://doi.org/10.1098/rspb.2012.0827
Fan CM, Yang EC, Tso IM (2009) Hunting efficiency and predation risk shapes the color-associated foraging traits of a predator. Behav Ecol 20:808–816. https://doi.org/10.1093/beheco/arp064
Foelix R (2011) Biology of spiders. Oxford University Press, New York
Goyret J, Kelber A (2012) Chromatic signals control probiscus movements during hovering in the hummingbird hawkmoth Macroglossus stellatarum. PLoS ONE 7:e34629. https://doi.org/10.1371/journal.pone.0034629
Graf B, Nentwig W (2001) Ontogenetic change in coloration and web-building behavior in the tropical spider Eriophora fuliginea (Araneae, Araneidae). J Arachnol 29:104–110. https://doi.org/10.1636/0161-8202(2001)029%5B0104:OCICAW%5D2.0.CO;2
Herberstein ME, Tso IM (2000) Evaluation of formulae to estimate the capture area and mesh height of orb webs (Araneoidea, Araneae). J Arachnol 28:180–184. https://doi.org/10.1636/0161-8202(2000)028[0180:eoftet]2.0.co;2
Hill EM, Christenson T (1988) Male residency on juvenile female Nephila clavipes (Araneae, Araneidae) webs. J Arachnol 16:257–259
Johnsen S, Kelber A, Warrant E, Sweeney AM, Widder EA, Lee RL, Hernández-Andrés J (2006) Crepuscular and nocturnal illumination and its effects on color perception by the nocturnal hawkmoth Deilephila elpenor. J Exp Biol 209:789–800. https://doi.org/10.1242/jeb.02053
Kelber A, Balkenius A, Warrant EJ (2003) Colour vision in diurnal and nocturnal hawkmoths. Integr Comp Biol 43:571–579. https://doi.org/10.1093/icb/43.4.571
Koh TH, Li DQ (2002) Population characteristics of a kleptoparasitic spider Argyrodes flavescens (Araenae : Theridiidae) and its impact on a host spider Nephila pilipes (Araneae : Tetragnathidae) from Singapore. Raffles Bull Zool 50:153–160
Lai CW, Zhang S, Piorkowski D, Liao CP, Tso IM (2017) A trap and a lure: dual function of a nocturnal animal construction. Anim Behav 130:159–164. https://doi.org/10.1016/j.anbehav.2017.06.016
Oxford GS, Gillespie RG (1998) Evolution and ecology of spider coloration. Ann Rev Entomol 43:619–643. https://doi.org/10.1146/annurev.ento.43.1.619
Peng P, Blamires Sean J, Agnarsson I, Lin HC, Tso IM (2013) A color-mediated mutualism between two arthropod predators. Curr Biol 23:172–176. https://doi.org/10.1016/j.cub.2012.11.057
Peng P, Stuart-Fox D, Chen SW, Tan EJ, Kuo GL, Blamires SJ, Tso IM, Elgar MA (2020) High contrast yellow mosaic patterns are prey attractants for orb-weaving spiders. Funct Ecol 34:853–864. https://doi.org/10.1111/1365-2435.13532
R Core Team (2022) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org
Rigosi E, Wiederman SD, O’Carroll DC (2017) Visual acuity of the honey bee retina and the limits for feature detection. Sci Rep 7:1–7. https://doi.org/10.1038/srep45972
Robinson MH, Robinson B (1973) Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithson Contr Zool 149:1–76. https://doi.org/10.5479/si.00810282.149
Schneider J, Andrade M (2011) Mating behaviour and sexual selection. In: Herberstein ME, editor. Spider behaviour: flexibility and versatility Cambridge: Cambridge University Press. p. 215–274
Somanathan H, Borges RM, Warrant EJ, Kelber A (2008) Nocturnal bees learn landmark colours in starlight. Curr Biol 18:R996–R997. https://doi.org/10.1016/j.cub.2008.08.023
Stöckl AL, O’Carroll DC, Warrant EJ (2020) Hawkmoth lamina monopolar cells act as dynamic spatial filters to optimize vision at different light levels. Sci Adv 6:eaaz8645. https://doi.org/10.1126/sciadv.aaz8645
Su YC, Smith D (2014) Evolution of host use, group-living and foraging behaviours in kleptoparasitic spiders: molecular phylogeny of the Argyrodinae (Araneae : Theridiidae). Invertebr Syst 28:415–431. https://doi.org/10.1071/IS14010
Théry M, Casas J (2009) The multiple disguises of spiders: web colour and decorations, body colour and movement. Philos Trans Roy Soc B 361:471–480. https://doi.org/10.1098/rstb.2008.0212
Tso IM (1996) Stabilimentum of the garden spider Argiope trifasciata: a possible prey attractant. Anim Behav 52:183–191. https://doi.org/10.1006/anbe.1996.0163
Tso IM, Lin CW, Yang EC (2004) Colourful orb-weaving spiders, Nephila pilipes, through a bee’s eyes. J Exp Biol 207:2631–2637. https://doi.org/10.1242/jeb.01068
Tso IM, Huang JP, Liao CP (2007) Nocturnal hunting of a brightly coloured sit-and-wait predator. Anim Behav 74:787–793. https://doi.org/10.1016/j.anbehav.2006.09.023
Tso IM, Zhang S, Tan WL, Peng P, Blamires SJ (2016) Prey luring coloration of a nocturnal semi-aquatic predator. Ethology 122:671–681. https://doi.org/10.1111/eth.12512
Vollrath F (1979) Vibrations: their signal function for a spider kleptoparasite. Science 205:1149–1151. https://doi.org/10.1126/science.205.4411.1149
Vollrath F (1985) Web spider’s dilemma: a risky move or site dependent growth. Oecologia 68:69–72. https://doi.org/10.1007/BF00379476
Wang B, Yu L, Ma N, Zhang Z, Gong D, Liu R, Li D, Zhang S (2022) Conspicuous cruciform silk decorations deflect avian predator attacks. Integr Zool 17:1–15. https://doi.org/10.1111/1749-4877.12621
Warrant E (2004) Vision in the dimmest habitats on earth. J Comp Physiol A 190:765–789. https://doi.org/10.1007/s00359-004-0546-z
Warrant EJ, Locket NA (2004) Vision in the deep sea. Biol Rev 79:671–712. https://doi.org/10.1017/S1464793103006420
Warrant EJ, Nilsson DE (1998) Absorption of white light in photoreceptors. Vision Res 38:195–207. https://doi.org/10.1016/S0042-6989(97)00151-X
Whitehouse M (2011) Kleptoparasitic spiders of the subfamily Argyrodinae: a special case of behavioural plasticity. In: Herberstein M (ed) Spider Behaviour: Flexibility and Versatility. Cambridge University Press, Cambridge, pp 348–386
Ximenes NG, Moraes VDS, Ortega JC, Gawryszewski FM (2020) Color lures in orb-weaving spiders: a meta-analysis. Behav Ecol 31:568–576. https://doi.org/10.1093/beheco/arz210
Yeh CW, Blamires S, Liao CP, Tso IM (2015) Top down and bottom up selection drives variations in frequency and form of a visual signal. Sci Rep 5:9543. https://doi.org/10.1038/srep09543
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25. https://doi.org/10.18637/jss.v027.i08
Zhang S, Chen HL, Chen KY, Huang JJ, Chang CC, Piorkowski D, Liao CP, Tso IM (2015) A nocturnal cursorial predator attracts flying prey with a visual lure. Anim Behav 102:119–125. https://doi.org/10.1016/j.anbehav.2014.12.028
Zhang S, Yip HY, Lee MY, Liu L, Piorkowski D, Liao CP, Tso IM (2018) Vision-mediated courtship in a nocturnal arthropod. Anim Behav 142:185–190. https://doi.org/10.1016/j.anbehav.2018.06.016
Funding
The study was funded by a Ministry of Science and Technology (MOST, Taiwan) grant (MOST-102–2311-B-029–001-MY3) to I.M.T and two MOST postdoctoral grants (MOST 103–2811-B-029–001, 103–2811-B-029–003) to S. Z.
Author information
Authors and Affiliations
Contributions
SZ and IMT designed research; SZ, YCL, and HHC performed research; SZ and CPL analyzed data; SZ, DP, and IMT wrote the paper.
Corresponding author
Ethics declarations
Ethics approval
All spiders were treated in accordance with the “research ethics and animal treatment” legal requirements of Tunghai University, where the study was carried out.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated By E. M. Jakob
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, S., Leu, YC., Chou, HH. et al. Two coinhabitants visually lure prey to host territory through a shared conspicuous trait. Behav Ecol Sociobiol 76, 145 (2022). https://doi.org/10.1007/s00265-022-03249-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-022-03249-8