The evolution of novel animal signals: silk decorations as a model system

Contemporary animal signals may derive from an elaboration of existing forms or novel non‐signalling traits. Unravelling the evolution of the latter is challenging because experiments investigating the maintenance of the signal may provide little insight into its early evolution. The web decorations, or stabilimenta of some orb web spiders represent an intriguing model system to investigate novel animal signals. For over 100 years, biologists have struggled to explain why spiders decorate their webs with additional threads of silk, producing a conspicuous signal on a construction whose function is to entangle unsuspecting prey. The numerous explanations for the maintenance of this behaviour starkly contrast with the absence of a plausible explanation for its evolutionary origin. Our review highlights the difficulties in resolving both the evolution and maintenance of animal signalling, and inferring the causative arrow—even from experimental studies. Drawing on recent research that focuses on physiological processes, we provide a model of the evolutionary progression of web‐decorating behaviour.

[1]  C. C. Horton.  A Defensive Function for the Stabilimenta of Two Orb Weaving Spiders (Araneae, Araneidae) , 1980 .

[2]  W. Eberhard.  Araneus expletus (Araneae, Araneidae): another stabilimentum that does not function to attract prey , 2008 .

[3]  H. Wiehle.  Beiträge zur Biologie der Araneen, insbesondere zur Kenntnis des Radnetzbaues , 1928, Zeitschrift für Morphologie und Ökologie der Tiere.

[4]  D. Peakall,et al.  Conservation of web proteins in the spider, Araneus diadematus. , 1971, The Journal of experimental zoology.

[5]  Daiqin Li,et al.  Stabilimenta attract unwelcome predators to orb–webs , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  F. Enders.  Vertical Stratification in Orb‐Web Spiders (Araneidae, Araneae) and a Consideration of Other Methods of Coexistence , 1974 .

[7]  T. Guilford,et al.  Receiver psychology and the evolution of animal signals , 1991, Animal Behaviour.

[8]  Kensuke Nakata.  Spiders Use Airborne Cues to Respond to Flying Insect Predators by Building Orb‐Web with Fewer Silk Thread and Larger Silk Decorations , 2008 .

[9]  Linden E. Higgins,et al.  Variation in foraging investment during the intermolt interval and before egg-laying in the spiderNephila clavipes (Araneae: Araneidae) , 1990, Journal of Insect Behavior.

[10]  R. Lewis,et al.  Molecular and mechanical characterization of aciniform silk: uniformity of iterated sequence modules in a novel member of the spider silk fibroin gene family. , 2004, Molecular biology and evolution.

[11]  M. Andersson.  Female choice selects for extreme tail length in a widowbird , 1982, Nature.

[12]  D. Hochuli,et al.  Why cross the web: decoration spectral properties and prey capture in an orb spider (Argiope keyserlingi) web , 2008 .

[13]  M. Nyffeler,et al.  Feeding ecology of the orb-weaving spiderArgiope aurantia [Araneae: Araneidae] in a cotton agroecosystem , 1987, Entomophaga.

[14]  M. Justice,et al.  WEB ORIENTATION, STABILIMENTUM STRUCTURE AND PREDATORY BEHAVIOR OF ARGIOPE FLORIDA CHAMBERLIN & IVIE 1944 (ARANEAE, ARANEIDAE, ARGIOPINAE) , 2005 .

[15]  W. Nentwig,et al.  Ecological Aspects of Spider Webs , 1987 .

[16]  K. Cheng,et al.  A natural history of web decorations in the St Andrew’s Cross spider (Argiope keyserlingi) , 2007 .

[17]  L. Simmons,et al.  Nuptial Feeding in Insects: Mating Effort versus Paternal Investment , 2010 .

[18]  Daiqin Li,et al.  Stabilimentum variations in Argiope versicolor (Araneae: Araneidae) from Singapore , 2002 .

[19]  R. Hingston.  Protective Devices in Spiders' Snares, with a Description of seven New Species of Orb–Weaving Spiders , 2009 .

[20]  M. Taborsky,et al.  Extended phenotypes as signals , 2009, Biological reviews of the Cambridge Philosophical Society.

[21]  M. Zuk,et al.  Sexual ornaments as animal signals. , 1991, Trends in Ecology & Evolution.

[22]  D. Rao,et al.  The aggregating behaviour of Argiope radon, with special reference to web decorations , 2007, Journal of Ethology.

[23]  D. Fairbairn,et al.  Selection on male size, leg length and condition during mate search in a sexually highly dimorphic orb-weaving spider , 2005, Oecologia.

[24]  John F Anderson.  The size of spider eggs and estimates of their energy content. , 1990 .

[25]  I. Tso.  Stabilimentum of the garden spider Argiope trifasciata : a possible prey attractant , 1996, Animal Behaviour.

[26]  R. Foelix,et al.  The biology of spiders. , 1987 .

[27]  Daiqin Li,et al.  Age-dependent Stabilimentum-Associated Predator Avoidance Behaviours in Orb-Weaving Spiders , 2003 .

[28]  C. Craig,et al.  SIGNAL POLYMORPHISM IN THE WEB-DECORATING SPIDER ARGIOPE ARGENTATA IS CORRELATED WITH REDUCED SURVIVORSHIP AND THE PRESENCE OF STINGLESS BEES, ITS PRIMARY PREY , 2001, Evolution; international journal of organic evolution.

[29]  R. Bradley.  THE INFLUENCE OF PREY AVAILABILITY AND HABITA T ON ACTIVITY PATTERNS AND ABUNDANCE O F ,ARGIOPE KEYSERLINGI (ARANEAE : ARANEIDAE ) , 1993 .

[30]  C. Demayo,et al.  Salient features of the orb-web of the garden spider, Argiope luzona (Walckenaer, 1841) (Araneae: Araneidae) , 2009 .

[31]  M. Herberstein.  Foraging behaviour in orb-web spiders (Araneidae): do web decorations increase prey capture success in Argiope keyserlingi Karsch, 1878? , 2000 .

[32]  M. Elgar,et al.  Foraging strategies and feeding regimes: Web and decoration investment in Argiope keyserlingi Karsch (Araneae: Araneidae) , 2000 .

[33]  C. Olive.  Foraging Specialization in Orb‐Weaving Spiders , 1980 .

[34]  Wayne W. Tolbert.  Predator Avoidance Behavior and Web Defensive Structures in the Orb Weavers, Argiope aurantia and Argiope trifasciata (Araneae, Araneidae) , 1975 .

[35]  Stephen P. Ellner,et al.  Web Relocation and Habitat Selection in Desert Widow Spider , 1993 .

[36]  T. Schoener,et al.  Stabilimenta characteristics of the spider Argiope argentata on small islands: support of the predator-defense hypothesis , 1992, Behavioral Ecology and Sociobiology.

[37]  C. Krebs,et al.  Measuring the ghost of competition: Insights from density-dependent habitat selection on the co-existence and dynamics of lemmings , 2000 .

[38]  M. Elgar,et al.  Signals for damage control: web decorations in Argiope keyserlingi (Araneae: Araneidae) , 2011, Behavioral Ecology and Sociobiology.

[39]  M. Théry,et al.  The multiple disguises of spiders: web colour and decorations, body colour and movement , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  H. W. Levi.  The orb-weaver genera Argiope, Gea, and Neogea from the Western Pacific Region (Araneae: Araneidae, Argiopinae) , 1983 .

[41]  Todd A. Blackledge,et al.  Does the Giant Wood Spider Nephila pilipes Respond to Prey Variation by Altering Web or Silk Properties , 2007 .

[42]  M. Elgar,et al.  Foraging strategies in orb-spinning spiders: Ambient light and silk decorations in Argiope aetherea Walckenaer (Araneae: Araneoidea) , 1996 .

[43]  Physical constraints on group foraging and social evolution : observations on web-spinning spiders , 1991 .

[44]  I. Tso.  Isolated Spider Web Stabillmentum Attracts Insects , 1998 .

[45]  A. Møller,et al.  Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  M. H. Robinson,et al.  Units of behavior and complex sequences in the predatory behavior of Argiope argentata (Fabricius): (Araneae: Araneidae) , 1971 .

[47]  P. Prokop,et al.  Factors affecting the foraging success of the wasp-like spider Argiope bruennichi (Araneae): Role of web design , 2005 .

[48]  H. Wiehle.  Beiträge zur kenntnis des radnetzbaues der epeiriden, tetragnathiden und uloboriden , 1927, Zeitschrift für Morphologie und Ökologie der Tiere.

[49]  M. Herberstein,et al.  Spider signals: are web decorations visible to birds and bees? , 2005, Biology Letters.

[50]  T. Eisner,et al.  Spider Web Protection Through Visual Advertisement: Role of the Stabilimentum , 1983, Science.

[51]  J. Endler.  Signals, Signal Conditions, and the Direction of Evolution , 1992, The American Naturalist.

[52]  Daiqin Li,et al.  Why do orb-weaving spiders (Cyclosa ginnaga) decorate their webs with silk spirals and plant detritus? , 2010, Animal Behaviour.

[53]  M. Andersson.  EVOLUTION OF CONDITION‐DEPENDENT SEX ORNAMENTS AND MATING PREFERENCES: SEXUAL SELECTION BASED ON VIABILITY DIFFERENCES , 1986, Evolution; international journal of organic evolution.

[54]  M. Elgar,et al.  Web-building spiders attract prey by storing decaying matter , 2004, Naturwissenschaften.

[55]  M. Elgar,et al.  Argiope bruennichi shows a drinking-like behaviour in web hub decorations (Araneae, Araneidae) , 2007, Journal of Ethology.

[56]  M. Herberstein,et al.  The influence of predator cues on orb-web spider foraging behaviour , 2006 .

[57]  M. Vorobyev,et al.  A review of the evolution of animal colour vision and visual communication signals , 2008, Vision Research.

[58]  M. Townley,et al.  The independent regulation of protein synthesis in the major ampullate glands of Araneus cavaticus (Keyserling) , 1986 .

[59]  E. Yang,et al.  Insect form vision as one potential shaping force of spider web decoration design , 2010, Journal of Experimental Biology.

[60]  Fritz Vollrath,et al.  Liquid crystalline spinning of spider silk , 2001, Nature.

[61]  I. Tso,et al.  Stabilimentum-Decorated Webs Spun by Cyclosa conica (Araneae, Araneidae) Trapped More Insects than Undecorated Webs , 1998 .

[62]  T. Blackledge.  Stabilimentum variation and foraging success in Argiope aurantia and Argiope trifasciata (Araneae: Araneidae) , 1998 .

[63]  M. Bruce,et al.  Silk decorations: controversy and consensus , 2006 .

[64]  M. H. Robinson,et al.  THE STABILIMENTUM OF THE ORB WEB SPIDER, ARGIOPE ARGENTATA: AN IMPROBABLE DEFENCE AGAINST PREDATORS , 1970, Canadian Entomologist.

[65]  M. Nyffeler,et al.  Die Beutespektren der Netzspinnen Argiope bruennichi (Scop.), Araneus quadratus Cl. Und Agelena labyrinthica (Cl.) in Ödlandwiesen bei Zürich , 1978 .

[66]  T. Blackledge,et al.  SILK MEDIATED DEFENSE BY AN ORB WEB SPIDER AGAINST PREDATORY MUD-DAUBER WASPS , 2001 .

[67]  D. Saravanan,et al.  Spider Silk - Structure, Properties and Spinning , 2006 .

[68]  A. Janetos.  Foraging tactics of two guilds of web-spinning spiders , 1982, Behavioral Ecology and Sociobiology.

[69]  H. W. Levi,et al.  The spider genera Gea and Argiope in America (Araneae: Araneidae) , 1968 .

[70]  M. H. Robinson,et al.  The Predatory Behavior of Some Araneid Spiders and the Origin of Immobilization Wrapping , 1969 .

[71]  R Cornelis,et al.  Function and structural variability of the stabili- menta of Cyclosainsulana(Costa) (Araneae, Araneidae) , 1990 .

[72]  Philip T. Starks,et al.  The adaptive signifi cance of stabilimenta in orb-webs: a hierarchical approach , 2002 .

[73]  H. M. Peters.  Über das Problem der Stabilimente in Spinnennetzen , 1993 .

[74]  D. Rao.  Stingless bee interception is not affected by variations in spider silk decoration , 2010 .

[75]  James H. Brown,et al.  Anisogamy, sexual selection, and the evolution and maintenance of sex , 1987, Evolutionary Ecology.

[76]  T. Blackledge,et al.  Do stabilimenta in orb webs attract prey or defend spiders , 1999 .

[77]  D. Blumstein,et al.  Ecology and signal evolution in lizards , 2002 .

[78]  M. Elgar,et al.  Wrap attack activates web-decorating behavior in Argiope spiders , 2008 .

[79]  I. Tso,et al.  Signaling by decorating webs: luring prey or deterring predators? , 2007 .

[80]  L. Hurst,et al.  Recent advances in understanding of the evolution and maintenance of sex. , 1996, Trends in ecology & evolution.

[81]  Dumas Gálvez.  Web decoration of Micrathena sexpinosa (Araneae: Araneidae): a frame-web-choice experiment with stingless bees , 2011 .

[82]  Takeshi Watanabe.  Prey attraction as a possible function of the silk decoration of the uloborid spider Octonoba sybotides , 1999 .

[83]  T. Blackledge.  Signal conflict in spider webs driven by predators and prey , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[84]  Kensuke Nakata,et al.  To be or not to be conspicuous: the effects of prey availability and predator risk on spider's web decoration building , 2009, Animal Behaviour.

[85]  D. Peakall.  Regulation of protein production in the silk glands of spiders. , 1966, Comparative biochemistry and physiology.

[86]  I. Tso.  THE EFFECT OF FOOD AND SILK RESERVE MANIPULATION ON DECORATION-BUILDING OF ARGIOPE AETHEROIDES , 2004 .

[87]  Daiqin Li,et al.  Ultraviolet cues affect the foraging behaviour of jumping spiders , 2005, Animal Behaviour.

[88]  J. Endler,et al.  ANIMAL VISUAL SYSTEMS AND THE EVOLUTION OF COLOR PATTERNS: SENSORY PROCESSING ILLUMINATES SIGNAL EVOLUTION , 2005, Evolution; international journal of organic evolution.

[89]  American Spiders and their Spinning Work; a Natural History of the Orb-weaving Spiders of the United States, with Special Regard to their Industry and Habits , 1895, Nature.

[90]  Daiqin Li,et al.  Predator-induced plasticity in web-building behaviour , 2004, Animal Behaviour.

[91]  S. Zschokke.  ULTRAVIOLET REFLECTANCE OF SPIDERS ANDTHEIR WEBS , 2002 .

[92]  M. Elgar,et al.  Signalling conflict between prey and predator attraction , 2001 .

[93]  D. Hochuli,et al.  Habitat selection and web plasticity by the orb spider Argiope keyserlingi (Argiopidae): Do they compromise foraging success for predator avoidance? , 2007 .

[94]  M. Elgar,et al.  Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[95]  M. Herberstein,et al.  Web decorations and foraging success in 'Araneus' eburnus (Araneae: Araneidae) , 2004 .

[96]  G. Nelson.  Ontogeny, Phylogeny, Paleontology, and the Biogenetic Law , 1978 .

[97]  D. Hochuli,et al.  Prey protein influences growth and decoration building in the orb web spider Argiope keyserlingi , 2009 .

[98]  Humphries,et al.  Bower‐building: coevolution of display traits in response to the costs of female choice? , 1999 .

[99]  C. Craig.  Predator foraging behavior in response to perception and learning by its prey: interactions between orb-spinning spiders and stingless bees , 1994, Behavioral Ecology and Sociobiology.

[100]  G. D. Bernard,et al.  INSECT ATTRACTION TO ULTRAVIOLET-REFLECTING SPIDER WEBS AND WEB DECORATIONS' , 1990 .

[101]  M. Hauber.  Web decorations and alternative foraging tactics of the spider Argiope appensa , 1998 .

[102]  M. H. Robinson,et al.  The biology of some Argiope species from New Guinea: predatory behaviour and stabilimentum construction (Araneae: Araneidae) , 1974 .

[103]  B. Opell,et al.  Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk , 1998 .

[104]  W. Eberhard,et al.  BEHAVIORAL CHARACTERS FOR THE HIGHER CLASSIFICATION OF ORB‐WEAVING SPIDERS , 1982, Evolution; international journal of organic evolution.

[105]  M. Elgar,et al.  The functional significance of silk decorations of orb‐web spiders: a critical review of the empirical evidence , 2000, Biological reviews of the Cambridge Philosophical Society.

[106]  A. Kerr.  Low Frequency of Stabilimenta in Orb Webs of Argiope appensa (Araneae: Araneidae) from Guam: An Indirect Effect of an Introduced Avian Predator , 1993 .

[107]  Jennifer L. Williams,et al.  Burrow decorations as antipredatory devices , 2006 .

[108]  Prey attraction as a possible function of discoid stabilimenta of juvenile orb-spinning spiders , 2004, Animal Behaviour.

[109]  M. Elgar,et al.  Molting interferes with web decorating behavior in Argiope keyserlingi (Araneae, Araneidae) , 2008 .

[110]  Fritz Vollrath,et al.  Spider silk as archetypal protein elastomer. , 2006, Soft matter.

[111]  S. Harris,et al.  Symposia of the Zoological Society of London , 1993 .

[112]  W. Eberhard.  Substitution of silk stabilimenta for egg sacs by Allocyclosa bifurca (Araneae: Araneidae) suggests that silk stabilimenta function as camouflage devices , 2003 .

[113]  M. Herberstein,et al.  Web decoration polymorphism in Argiope Audouin, 1826 (Araneidae) spiders: ontogenetic and interspecific variation , 2005 .

[114]  Daiqin Li.  Spiders that decorate their webs at higher frequency intercept more prey and grow faster , 2005, Proceedings of the Royal Society B: Biological Sciences.

[115]  R. Johnstone,et al.  Animal signals , 2013, Current Biology.

[116]  J. Blas,et al.  Raptor Nest Decorations Are a Reliable Threat Against Conspecifics , 2011, Science.

[117]  André Walter.  Are web stabilimenta attractive to praying mantids , 2007 .

[118]  Daniel Pauly,et al.  The Cichlid Fishes : Nature ' s Grand Experiment In Evolution , 2001 .

[119]  C. Olive.  Optimal phenology and body-size of Orb-weaving spiders: Foraging constrains , 1981, Oecologia.

[120]  D. Hochuli,et al.  Does decoration building influence antipredator responses in an orb-web spider (Argiope keyserlingi) in its natural habitat? , 2007 .

[121]  T. Blackledge,et al.  The common house spider alters the material and mechanical properties of cobweb silk in response to different prey. , 2008, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[122]  M. Elgar,et al.  Web damage and feeding experience influence web site tenacity in the orb-web spider Argiope keyserlingi Karsch , 2000, Animal Behaviour.

[123]  M. Ryan,et al.  What do animal signals mean? , 2009, Animal Behaviour.