Abstract
Rapidly changing environments impose novel selection pressures on organisms, and sometimes adaptive phenotypic plasticity allows organisms to survive and reproduce in the face of environmental change. However, plastic responses can also be maladaptive. In this study, we investigate whether male reproductive investment responds plastically to varied experience with traffic noise. We exposed male crickets chronically to one of three noise treatments from the 2nd-3rd instar until their natural death: masking traffic noise (including noise that overlaps in frequency with the male crickets’ mating calls), non-masking traffic noise (an identical traffic noise track from which we digitally removed the frequencies that mask the crickets’ mating call), and silence. We dissected and weighed their testes and spermatophore molds. Controlling for body mass, we found that the spermatophore molds of crickets reared in masking and non-masking noise were 29% and 24% lighter, respectively, than those of crickets reared in silence. There were no differences in body mass-adjusted testes mass among treatments. If spermatophore mold mass is positively associated with male reproductive output, this reduction in size could have negative fitness consequences for animals exposed to traffic noise. We encourage future work to investigate impacts of noise on reproductive investment in other study systems that are likely sensitive to anthropogenic noise (e.g., birds, frogs, singing insects).
Significance statement
Anthropogenic noise is a pervasive pollutant and chronic noise can negatively affect fitness. How does anthropogenic noise influence reproductive investment? Phenotypically plastic responses to noise may increase survival and reproduction in noisy environments. Traffic noise masks the sounds crickets make, potentially changing conspecifics’ perception of population density, mate availability, and the risk of sperm competition. We found that male crickets reared in silence developed significantly larger spermatophore molds (a reproductive structure that delivers the sperm containing packet to the female) than those reared in traffic noise. If the spermatophore mold influences male reproductive output, this reduction in size may have negative impacts on reproductive success of animals exposed to masking traffic noise.
Similar content being viewed by others
Data availability
The datasets generated and analyzed in this study are available in the Dryad repository (https://doi.org/10.5061/dryad.zcrjdfn8d).
Change history
27 April 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00265-022-03169-7
References
Bailey NW, Zuk M (2008) Acoustic experience shapes female mate choice in field crickets. Proc R Soc B 275:2645–2650
Bailey NW, Gray B, Zuk M (2010) Acoustic experience shapes alternative mating tactics and reproductive investment in male field crickets. Curr Biol 20:845–849
Barber JR, Crooks KR, Fristrup KM (2010) The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol 25:180–189
Bent AM, Ings TC, Mowles SL (2018) Anthropogenic noise disrupts mate searching in Gryllus bimaculatus. Behav Ecol 29:1271–1277
Bermúdez-Cuamatzin E, Ríos-Chelén AA, Gil D, Garcia CM (2011) Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett 7:36–38
Buxton RT, McKenna MF, Mennitt D, Fristrup K, Crooks K, Angeloni L, Wittemyer G (2017) Noise pollution is pervasive in US protected areas. Science 356:531–533
Castellano S, Cucco M, Giacoma C (2004) Reproductive investment of female green toads (Bufo viridis). Copeia 2004:659–664
Costello RA, Symes LB (2014) Effects of anthropogenic noise on male signalling behaviour and female phonotaxis in Oecanthus tree crickets. Anim Behav 95:15–22
Cunnington GM, Fahrig L (2013) Mate attraction by male anurans in the presence of traffic noise. Anim Conserv 16:275–285
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Gallego-Abenza M, Mathevon N, Wheatcroft D (2020) Experience modulates an insect’s response to anthropogenic noise. Behav Ecol 31:90–96
Gage MJ (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc R Soc B 261:25–30
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407
Godin JG (1995) Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia 103:224–229
Groot AT, Claβen A, Staudacher H, Schal C, Heckel DG (2010) Phenotypic plasticity in sexual communication signal of a noctuid moth. J Evol Biol 23:2731–2738
Gross K, Pasinelli G, Kunc HP (2010) Behavioral plasticity allows short-term adjustment to a novel environment. Am Nat 176:456–464
Gurule-Small GA, Tinghitella RM (2018) Developmental experience with anthropogenic noise hinders adult mate location in an acoustically signaling invertebrate. Biol Lett 14:20170714
Gurule-Small GA, Tinghitella RM (2019) Life-history consequences of developing in anthropogenic noise. Glob Chang Biol 25:1957–1966
Halfwerk W, Holleman LJ, Slabbekoorn H (2010) Negative impact of traffic noise on avian reproductive success. J Appl Ecol 48:210–219
Hanna D, Blouin-Demers G, Wilson DR, Mennill DJ (2011) Anthropogenic noise affects song structure in red-winged blackbirds (Agelaius phoeniceus). J Exp Biol 214:3549–3556
Imaizumi K, Pollack GS (1999) Neural coding of sound frequency by cricket auditory receptors. J Neurosci 19:1508–1516
Injaian AS, Poon LY, Patricelli GL (2018) Effects of experimental anthropogenic noise on avian settlement patterns and reproductive success. Behav Ecol 29:1181–1189
Khalifa A (1949) The mechanism of insemination and the mode of action of the spermatophore in Gryllus pennsylvanicus. Q J Microsc Sci 90:281–292
Kight CR, Swaddle JP (2011) How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol Lett 14:1052–1061
Kight CR, Saha MS, Swaddle JP (2012) Anthropogenic noise is associated with reductions in the productivity of breeding Eastern Bluebirds (Sialia sialis). Ecol Appl 22:1989–1996
Kleist NJ, Guralnick RP, Cruz A, Lowry CA, Francis CD (2018) Chronic anthropogenic noise disrupts glucocorticoid signaling and has multiple effects on fitness in an avian community. Proc Natl Acad Sci 115:E648–E657
Klemme I, Soulsbury CD, Henttonen H (2014) Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species. Proc R Soc B 281:20141291
Lampe U, Schmoll T, Franzke A, Reinhold K (2012) Staying tuned: grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components. Funct Ecol 26:1348–1354
LaZerte SE, Otter KA, Slabbekoorn H (2015) Relative effects of ambient noise and habitat openness on signal transfer for chickadee vocalizations in rural and urban green-spaces. Bioacoustics 24:233–252
Mappes J, Mappes T, Lappalainen T (1997) Unequal maternal investment in offspring quality in relation to predation risk. Evol Ecol 11:237–243
Mason JT, McClure CJ, Barber JR (2016) Anthropogenic noise impairs owl hunting behavior. Biol Conserv 199:29–32
McCullough EL, Buzatto BA, Simmons LW (2018) Population density mediates the interaction between pre- and post-mating sexual selection. Evolution 72:893–905
Mennitt D, Fristrup K, Sherrill K, Nelson L (2013) Mapping sound pressure levels on continental scales using a geospatial sound model. Proc Inter-Noise:1–11 Innsbruck, Austria
Morley EL, Jones G, Radford AN (2014) The importance of invertebrates when considering the impacts of anthropogenic noise. Proc R Soc B 281(1776):20132683
Orci KM, Petróczki K, Barta Z (2016) Instantaneous song modification in response to fluctuating traffic noise in the tree cricket Oecanthus pellucens. Anim Behav 112:187–194
Parker GA, Ball MA, Stockley P, Gage MJ (1997) Sperm competition games: a prospective analysis of risk assessment. Biol Sci 264:1793–1802
Radford AN, Kerridge E, Simpson SD (2014) Acoustic communication in a noisy world: can fish compete with anthropogenic noise? Behav Ecol 25:1022–1030
Reznick D, Yang AP (1993) The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies. Ecology 74:2011–2019
Rising JD (1996) Relationship between testis size and mating systems in American Sparrows. Auk 113:224–228
Robinson MR, Beckerman AP (2013) Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history. Ecol Lett 16:281–290
Rowell GA, Cade WH (1993) Simulation of alternative male reproductive behavior: calling and satellite behavior in field crickets. Ecol Model 65:265–280
Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17: 474-480
Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85:1077–1088
Slabbekoorn H, Peet M (2003) Ecology: birds sing at a higher pitch in urban noise. Nature 424:267
Stockley P, Purvis A (1993) Sperm competition in mammals: a comparative study of male roles and relative investment in sperm production. Funct Ecol 7:560–570
Thünken T, Meuthen D, Bakker TC, Kullmann H (2010) Parental investment in relation to offspring quality in the biparental cichlid fish Pelvicachromis taeniatus. Anim Behav 80:69–74
Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev 86:640–657
Van Buskirk J (2012) Changes in the annual cycle of North American raptors associated with recent shifts in migration timing. Auk 129:691–698
Van Baaren J, Candolin U (2018) Plasticity in a changing world: behavioural responses to human perturbations. Curr Opin Insect Sci 27:21–25
Verzijden MN, Ripmeester EAP, Ohms VR, Snelderwaard P, Slabbekoorn H (2010) Immediate spectral flexibility in singing chiffchaffs during experimental exposure to highway noise. J Exp Biol 213:2575–2581
Acknowledgments
E. Larson, S. Nichols, and two anonymous reviewers provided helpful comments on earlier versions of the manuscript.
Funding
Funding was provided by a University of Denver Summer Research Grant to AB, Sigma Xi and Orthopterists’ Society grants to GGS, and funding from the University of Denver to RMT.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by K. Shaw
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original version of this article was revised: In the original version of this article the order of treatments is incorrect along the x-axis of Figure 2 and should read (from left to right): masking, non-masking, silent.
Rights and permissions
About this article
Cite this article
Bowen, A.E., Gurule-Small, G.A. & Tinghitella, R.M. Anthropogenic noise reduces male reproductive investment in an acoustically signaling insect. Behav Ecol Sociobiol 74, 103 (2020). https://doi.org/10.1007/s00265-020-02868-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-020-02868-3