Vibratory noise in anthropogenic habitats and its effect on prey detection in a web-building spider

In nature, animals must contend with the presence of noise, which may limit their ability to detect prey, attract mates and escape predators. Sources of noise vary and may originate from natural (e.g. animal sounds, water) or anthropogenic (e.g. traffic, construction) sources. The vibratory sensory modality has long been overlooked in the study of anthropogenic effects on wildlife. Human-induced environmental changes may introduce noise sources as well as artificial substrates that alter vibratory noise profiles, leading to maladaptive behavioural responses. We conducted field measurements of vibratory noise on various substrate types (natural and artificial) used by animals in human-developed habitats. Next, we conducted laboratory experiments on how vibratory noise affects the prey detection ability of the European garden spider, Araneus diadematus. We tested whether changes in vibratory noise profiles consistent with anthropogenic alterations of vibratory habitats are sufficient to alter the spider's sensitivity to prey cues. We found that overall noise amplitude on artificial substrates was lower and less variable across contexts compared with natural substrates. In experiments with different noise levels, we observed that garden spiders showed noise-dependent changes in sensitivity to prey-mimicking cues, with response thresholds lowest at intermediate noise levels. Experimental levels of intermediate noise consistent with field measurements on natural substrates suggest that spiders' predatory performance is higher when webs are constructed on natural substrates. This suggests that human-introduced substrates may interfere with spiders' predatory performance. As human activities and habitat alteration are widespread, our findings highlight the need to consider the vibratory sensory channel in assessing anthropogenic impacts on wildlife.

[1]  Daniel T. Blumstein,et al.  Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis , 2010, Biology Letters.

[2]  J. McDaniel,et al.  Frequency information in the vibration-cued escape hatching of red-eyed treefrogs , 2009, Journal of Experimental Biology.

[3]  E. F. Edwards,et al.  Anthropogenic Noise as a Stressor in Animals: A Multidisciplinary Perspective , 2007 .

[4]  Peter M. Narins,et al.  Effects of masking noise on evoked calling in the Puerto Rican coqui (Anura: Leptodactylidae) , 1982, Journal of comparative physiology.

[5]  F. G. Barth,et al.  Vibrations in the orb web of the spider Nephila clavipes: cues for discrimination and orientation , 1996, Journal of Comparative Physiology A.

[6]  R. Hoy,et al.  The effect of substrate on the efficacy of seismic courtship signal transmission in the jumping spider Habronattus dossenus (Araneae: Salticidae) , 2004, Journal of Experimental Biology.

[7]  J. Maes,et al.  Effects of noise on the performance of rats in an operant discrimination task , 2003, Behavioural Processes.

[8]  David N. Reznick,et al.  Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments , 2007 .

[9]  M. Herberstein,et al.  Spider Behaviour: Flexibility And Versatility , 2011 .

[10]  A. Popper,et al.  A noisy spring: the impact of globally rising underwater sound levels on fish. , 2010, Trends in ecology & evolution.

[11]  H. Slabbekoorn,et al.  Fluid dynamics: Vortex rings in a constant electric field , 2003, Nature.

[12]  E. E. Ungar,et al.  Structure-borne sound , 1974 .

[13]  Caitlin R. Kight,et al.  How and why environmental noise impacts animals: an integrative, mechanistic review. , 2011, Ecology letters.

[14]  F. Lang Noise filtering in the auditory system of Locusta migratoria L , 1996, Journal of Comparative Physiology.

[15]  J. McDaniel,et al.  Is it safe? Red-eyed treefrog embryos assessing predation risk use two features of rain vibrations to avoid false alarms , 2010, Animal Behaviour.

[16]  H. Markl,et al.  Transmission of vibration in a spider's web , 1986 .

[17]  P. Warren,et al.  Urban bioacoustics: it's not just noise , 2006, Animal Behaviour.

[18]  Joachim Ostwald,et al.  Foraging bats avoid noise , 2008, Journal of Experimental Biology.

[19]  K. Reinhold,et al.  How grasshoppers respond to road noise: developmental plasticity and population differentiation in acoustic signalling , 2014 .

[20]  A. Horn,et al.  Ambient noise increases missed detections in nestling birds , 2012, Biology Letters.

[21]  H. Slabbekoorn,et al.  Birdsong and anthropogenic noise: implications and applications for conservation , 2008, Molecular ecology.

[22]  A. Mason,et al.  Substrate-dependent signalling success in the wolf spider, Schizocosa retrorsa , 2008, Animal Behaviour.

[23]  Mark A. Bee,et al.  Auditory masking of anuran advertisement calls by road traffic noise , 2007, Animal Behaviour.

[24]  P. Narins Vibration Communication in Vertebrates , 2001 .

[25]  A. Zuur,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[26]  Michael F. Benard Predator-induced phenotypic plasticity in organisms with complex life histories , 2004 .

[27]  Reginald B. Cocroft,et al.  Wind-induced noise alters signaler and receiver behavior in vibrational communication , 2010, Behavioral Ecology and Sociobiology.

[28]  C. Henry Vibrational Communication in Animals , 2009 .

[29]  Kai-Jung Chi,et al.  The effects of wind on trap structural and material properties of a sit-and-wait predator , 2009 .

[30]  C. F. Ng,et al.  STRUCTURE-BORNE NOISE AND VIBRATION OF CONCRETE BOX STRUCTURE AND RAIL VIADUCT , 2002 .

[31]  Jernej Polajnar,et al.  The effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae) , 2008, Central European Journal of Biology.

[32]  C. Hieber Orb‐web Orientation and Modification by the Spiders Araneus diadematus and Araneus gemmoides (Araneae: Araneidae) in Response to Wind and Light , 2010 .

[33]  C Walcott A spider's vibration receptor: its anatomy and physiology. , 1969, American zoologist.

[34]  M. Virant-Doberlet,et al.  Effects of heterospecific and conspecific vibrational signal overlap and signal-to-noise ratio on male responsiveness in Nezara viridula (L.) , 2010, Journal of Experimental Biology.

[35]  C. Frohlich,et al.  Transmission and attenuation of vibration in orb spider webs , 1982 .

[36]  K. Warkentin How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs , 2005, Animal Behaviour.

[37]  Linda S. Weilgart The impacts of anthropogenic ocean noise on cetaceans and implications for management , 2007 .

[38]  Damian O. Elias,et al.  Dynamic Population Structure and the Evolution of Spider Mating Systems , 2011 .

[39]  Christopher W Clark,et al.  Exposure to seismic survey alters blue whale acoustic communication , 2009, Biology Letters.

[40]  T. U. Grafe,et al.  The function of call alternation in the African reed frog (Hyperolius marmoratus): precise call timing prevents auditory masking , 1996, Behavioral Ecology and Sociobiology.

[41]  R. Fay,et al.  Comparative Hearing: Birds and Reptiles , 2000, Springer Handbook of Auditory Research.

[42]  P. Tyack,et al.  Responses of cetaceans to anthropogenic noise , 2007 .

[43]  Gail L. Patricelli,et al.  Impacts of Anthropogenic Noise on Wildlife: Research Priorities for the Development of Standards and Mitigation , 2010 .

[44]  R. Cocroft,et al.  The Behavioral Ecology of Insect Vibrational Communication , 2005 .

[45]  P. Fialaa,et al.  Numerical modelling of ground-borne noise and vibration in buildings due to surface rail traffic , 2007 .

[46]  Friedrich G. Barth,et al.  Spiders of the genus Cupiennius Simon 1891 (Araneae, Ctenidae) , 1988, Oecologia.

[47]  W. M. Masters,et al.  Vibrations in the orbwebs of Nuctenea sclopetaria (Araneidae) , 1984, Behavioral Ecology and Sociobiology.

[48]  H. Brumm,et al.  Acoustic Communication in Noise , 2005 .

[49]  Klaus Reinhold,et al.  Staying tuned: grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components , 2012 .

[50]  Friedrich G. Barth,et al.  Vibratory signals and prey capture in orb-weaving spiders (Zygiella x-notata, Nephila clavipes; Araneidae) , 1982, Journal of comparative physiology.

[51]  J. Hildebrand Anthropogenic and natural sources of ambient noise in the ocean , 2009 .

[52]  Donald H. Owings,et al.  The effects of wind turbines on antipredator behavior in California ground squirrels (Spermophilus beecheyi) , 2006 .

[53]  P. Gowaty Developmental Plasticity and Evolution Mary Jane West-Eberhard , 2005, Animal Behaviour.

[54]  W. Nentwig Prey analysis of four species of tropical orb-weaving spiders (Araneae: Araneidae) and a comparison with araneids of the temperate zone , 1985, Oecologia.

[55]  H. Markl,et al.  Vibration signal transmission in spider orb webs. , 1981, Science.

[56]  B. Young,et al.  The use of ground-borne vibrations for prey localization in the Saharan sand vipers (Cerastes). , 2002, The Journal of experimental biology.

[57]  Wouter Halfwerk,et al.  Negative impact of traffic noise on avian reproductive success , 2011 .

[58]  A. Mason,et al.  A signal-substrate match in the substrate-borne component of a multimodal courtship display , 2010 .

[59]  Nicolas Pinet,et al.  Exposure to seismic survey alters blue whale acoustic communication , 2010 .

[60]  F. Barth,et al.  Spider vibration receptors: Threshold curves of individual slits in the metatarsal lyriform organ , 1982, Journal of comparative physiology.

[61]  Jörn Christoffer Groos,et al.  Time domain classification and quantification of seismic noise in an urban environment , 2009 .

[62]  R. Brooks,et al.  It's All Who You Know: The Evolution Of Socially Cued Anticipatory Plasticity As A Mating Strategy , 2011, The Quarterly Review of Biology.

[63]  Daniel T. Blumstein,et al.  Increased amplitude and duration of acoustic stimuli enhance distraction , 2010, Animal Behaviour.

[64]  David Blair,et al.  Vehicle-induced seismic effects at a gravitational wave observatory , 2003 .

[65]  D. Parrinello,et al.  Physiological and agonistic behavioural response of Procambarus clarkii to an acoustic stimulus , 2013, Journal of Experimental Biology.

[66]  John L. Quinn,et al.  Noise, predation risk compensation and vigilance in the chaffinch Fringilla coelebs , 2006 .

[67]  L. G. Kurzweil,et al.  GROUND-BORNE NOISE AND VIBRATION FROM UNDERGROUND RAIL SYSTEMS , 1979 .

[68]  F. Schilcher The function of pulse song and sine song in the courtship of Drosophila melanogaster , 1976, Animal Behaviour.

[69]  Clinton D. Francis,et al.  Noise Pollution Changes Avian Communities and Species Interactions , 2009, Current Biology.

[70]  J. Yack,et al.  Vibration detection and discrimination in the masked birch caterpillar (Drepana arcuata) , 2012, Journal of Comparative Physiology A.

[71]  R. Jackson,et al.  Exploitation of environmental noise by an araneophagic assassin bug , 2011, Animal Behaviour.

[72]  Peter M. Narins,et al.  Seismic Communication in Anuran AmphibiansWhite-lipped frogs thump the ground as they chirp , 1990 .

[73]  Micheal L. Dent,et al.  Hearing in Birds and Reptiles , 2000 .

[74]  Peggy S. M. Hill,et al.  How do animals use substrate-borne vibrations as an information source? , 2009, Naturwissenschaften.

[75]  M. Virant-Doberlet,et al.  Vibrational communication in insects , 2004 .

[76]  Jochen Speck,et al.  Vibration sensitivity of pretarsal slit sensilla in the spider leg , 1982, Journal of comparative physiology.

[77]  J. Hailman,et al.  Temporal Pattern Shifts to Avoid Acoustic Interference in Singing Birds , 1974, Science.

[78]  M. Virant-Doberlet,et al.  Disruption of the reproductive behaviour of Scaphoideus titanus by playback of vibrational signals , 2009 .

[79]  R. Bishop,et al.  The Mechanics of Vibration , 2011 .

[80]  R. Cocroft,et al.  Host shifts favor vibrational signal divergence in Enchenopa binotata treehoppers , 2008 .

[81]  Kevin R Crooks,et al.  The costs of chronic noise exposure for terrestrial organisms. , 2010, Trends in ecology & evolution.

[82]  A. Foote,et al.  Environment: Whale-call response to masking boat noise , 2004, Nature.

[83]  W. Mitch Masters,et al.  Vibrations in the orbwebs of Nuctenea sclopetaria (Araneidae) , 1984, Behavioral Ecology and Sociobiology.

[84]  Christopher W. Clark,et al.  Effect of anthropogenic low‐frequency noise on the foraging ecology of Balaenoptera whales , 2001 .

[85]  Friedrich G. Barth,et al.  Spiders of the genus Cupiennius Simon 1891 (Araneae, Ctenidae) , 1988, Oecologia.