Zebrafish is a well-established model organism in hearing research. Although the acoustic environment is known to shape the structure and sensitivity of auditory systems, there is no information on the natural soundscape of this species. Moreover, zebrafish are typically reared in large-scale housing systems (HS), although their acoustic properties and potential effects on hearing remain unknown. We characterized the soundscape of both zebrafish natural habitats and laboratory captive conditions, and discussed possible impact on auditory sensitivity. Sound recordings were conducted in five distinct zebrafish habitats (Southwest India), from quieter stagnant environments with diverse biological/abiotic sounds to louder watercourses characterized by current and moving substrate sounds. Sound pressure level (SPL) varied between 98 and 126 dB re 1 μPa. Sound spectra presented most energy below 3000 Hz and quieter noise windows were found in the noisiest habitats matching the species best hearing range. Contrastingly, recordings from three zebrafish HS revealed higher SPL (122–143 dB) and most energy below 1000 Hz with more spectral peaks, which might cause significant auditory masking. This study establishes an important ground for future research on the adaptation of zebrafish auditory system to the natural soundscapes, and highlights the importance of controlling noise conditions in captivity.
Get full access to this article
View all access options for this article.
References
1.
LadichF, Schulz-MirbachT. Diversity in fish auditory systems: one of the riddles of sensory biology. Front Ecol Evol, 2016; 4:2–26.
2.
PopperAN, FayRR. Sound detection and processing by fish critical review and major research questions. Brain Behav Evol, 1993; 41:14–38.
3.
LadichF. Diversity in hearing in fishes: ecoacoustical, communicative, and developmental constraints. In: Insights from Comparative Hearing Research. KöpplC, ManleyGA, PopperAN, and FayRR(eds), pp. 217–236, Springer-Verlag New York, New York, 2013.
4.
LagardereJP, BegoutML, LafayeJY, VillotteJP. Influence of wind-produced noise on orientation in the Sole (Solea-Solea). Can J Fish Aquat Sci, 1994; 51:1258–1264.
5.
FayR. Soundscapes and the sense of hearing of fishes. Integr Zool, 2009; 4:26–32.
6.
BretschneiderF, van VeenH, TeunisPFM, PetersRC, van den Berg AV. Zebrafish can hear sound pressure and particle motion in a synthesized sound field. Anim Biol, 2013; 63:199–215.
7.
AmoserS, LadichF. Are hearing sensitivities of freshwater fish adapted to the ambient noise in their habitats?. J Exp Biol, 2005; 208:3533–3542.
8.
LugliM, YanHY, FineML. Acoustic communication in two freshwater gobies: the relationship between ambient noise, hearing thresholds and sound spectrum. J Comp Physiol A, 2003; 189:309–320.
9.
SoaresD, NiemillerML. Sensory adaptations of fishes to subterranean environments. Bioscience, 2013; 63:274–283.
10.
PopperAN, FewtrellJ, SmithME, McCauleyRD. Anthropogenic sound: effects on the behavior and physiology of fishes. Mar Technol Soc J, 2003; 37:35–40.
11.
SmithME, KaneAS, PopperAN. Noise-induced stress response and hearing loss in goldfish (Carassius auratus). J Exp Biol, 2004; 207:427–435.
12.
SlabbekoornH, BoutonN, van OpzeelandI, CoersA, ten CateC, PopperAN. A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol Evol, 2010; 25:419–427.
13.
LagardereJP. Effects of noise on growth and reproduction of Crangon crangon in rearing tanks. Mar Biol, 1982; 71:177–185.
14.
BartAN, ClarkJ, YoungJ, ZoharY. Underwater ambient noise measurements in aquaculture systems: a survey. Aquac Eng, 2001; 25:99–110.
15.
WysockiLE, DavidsonJW, SmithME, FrankelAS, EllisonWT, MazikPM, et al.Effects of aquaculture production noise on hearing, growth, and disease resistance of rainbow trout Oncorhynchus mykiss. Aquaculture, 2007; 272:687–697.
16.
BannerA, HyattM. Effects of noise on eggs and larvae of two estuarine fishes. Trans Am Fish Soc, 1973; 102:142–144.
17.
TerhuneJM, FriarsGW, BaileyJK, O'FlynnFM. Noise levels may influence Atlantic salmon smolting rates in tanks. J Fish Biol, 1990; 37:185–187.
18.
DavidsonJ, BebakJ, MazikP. The effects of aquaculture production noise on the growth, condition factor, feed conversion, and survival of rainbow trout, Oncorhynchus mykiss. Aquaculture, 2009; 288:337–343.
19.
GutscherM, WysockiLEVA, LadichF. Aquarium and pond noise on hearing sensitivity in an otophysine fish. Int J Anim Sound its Rec, 2011; 20:117–136.
20.
WhitfieldTT. Zebrafish as a model for hearing and deafness. J Neurobiol, 2002; 53:157–171.
21.
BeverMM, FeketeDM. Atlas of the developing inner ear in zebrafish. Dev Dyn, 2002; 223:536–543.
22.
WangJ, SongQ, YuD, YangG, XiaL, SuK, et al.Ontogenetic development of the auditory sensory organ in zebrafish (Danio rerio): changes in hearing sensitivity and related morphology. Sci Rep, 2015; 5:15943.
23.
WhitfieldTT, RileyBB, ChiangM-Y, PhillipsB. Development of the zebrafish inner ear. Dev Dyn, 2002; 223:427–458.
24.
BangPI, SewellWF, MalickiJJ. Morphology and cell type heterogeneities of the inner ear epithelia in adult and juvenile zebrafish (Danio rerio). J Comp Neurol, 2001; 438:173–190.
25.
MonroeJD, ManningDP, UribePM, BhandiwadA, SisnerosJA, SmithME, et al.Hearing sensitivity differs between zebrafish lines used in auditory research. Hear Res, 2016; 341:220–231.
26.
SpenceR, GerlachG, LawrenceC, SmithC. The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev, 2008; 83:13–34.
27.
AvdeshA, ChenM, Martin-IversonMT, MondalA, OngD, Rainey-SmithS, et al.Regular care and maintenance of a zebrafish (Danio rerio) laboratory: an introduction. J Vis Exp, 2012:e4196.
28.
LawrenceC, BestJ, JamesA, MaloneyK. The effects of feeding frequency on growth and reproduction in zebrafish (Danio rerio). Aquaculture, 2012; 368–369:103–108.
29.
ArunachalamM, RajaM, VijayakumarC, MalaiammalP, MaydenRL. Natural history of zebrafish (Danio rerio) in India. Zebrafish. 2013; 10:1–14.
30.
WysockiLE, AmoserS, LadichF. Diversity in ambient noise in European freshwater habitats: noise levels, spectral profiles, and impact on fishes. J Acoust Soc Am, 2007; 121:2559–2566.
31.
AmoserS, LadichF. Year-round variability of ambient noise in temperate freshwater habitats and its implications for fishes. Aquat Sci, 2010; 72:371–378.
32.
WysockiLE, LadichF. Hearing in fishes under noise conditions. J Assoc Res Otolaryngol, 2005; 6:28–36.
33.
HiggsDM, SouzaMJ, WilkinsHR, PressonJC, PopperAN. Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J Assoc Res Otolaryngol, 2001; 3:174–184.
34.
SamuelY, MorrealeSJ, ClarkCW, GreeneCH, RichmondME. Underwater, low-frequency noise in a coastal sea turtle habitat. J Acoust Soc Am, 2005; 117:1465–1472.
35.
McDonaldMA, HildebrandJA, WigginsSM. Increases in deep ocean ambient noise in the Northeast Pacific west of San Nicolas Island, California. J Acoust Soc Am, 2006; 120:711–718.
36.
CodarinA, WysockiLE, LadichF, PicciulinM. Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy). Mar Pollut Bull, 2009; 58:1880–1887.
37.
BertucciF, ParmentierE, LecellierG, HawkinsAD, LecchiniD. Acoustic indices provide information on the status of coral reefs: an example from Moorea Island in the South Pacific. Sci Rep, 2016; 6:1–9.
38.
BuscainoG, CerauloM, PierettiN, CorriasV, FarinaA, FiliciottoF, et al.Temporal patterns in the soundscape of the shallow waters of a Mediterranean marine protected area. Sci Rep, 2016; 6:1–13.
39.
PutlandRL, ConstantineR, RadfordCA. Exploring spatial and temporal trends in the soundscape of an ecologically significant embayment. Sci Rep, 2017; 7:1–12.
40.
CrawfordJD, JacobP, BénechV. Sound Production and reproductive ecology of strongly acoustic fish in Africa: Pollimyrus isidori, Mormyridae. Behaviour, 1997; 134:677–725.
41.
LugliM. Sounds of shallow water fishes pitch within the quiet window of the habitat ambient noise. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 2010; 196:439–451.
42.
AmoserS, WysockiLE, LadichF. Noise emission during the first powerboat race in an Alpine lake and potential impact on fish communities. J Acoust Soc Am, 2004; 116:3789–3797.
43.
NeoYY, HubertJ, BolleL, WinterHV, Ten CateC, SlabbekoornH. Sound exposure changes European seabass behaviour in a large outdoor floating pen: effects of temporal structure and a ramp-up procedure. Environ Pollut, 2016; 214:26–34.
44.
NedelecSL, SimpsonSD, MorleyEL, NedelecB, RadfordAN. Impacts of regular and random noise on the behaviour, growth and development of larval Atlantic cod (Gadus morhua). Proc R Soc B, 2015; 282:20151943.
45.
National Research Council. Guide for the Care and Use of Laboratory Animals: Eighth Edition. Washington, DC: The National Academies Press, 2011.
46.
AndersonPA. Acoustic characterization of seahorse tank environments in public aquaria: a citizen science project. Aquac Eng, 2013; 54:72–77.
47.
LawrenceC, MasonT. Zebrafish housing systems: a review of basic operating principles and considerations for design and functionality. ILAR J, 2015; 53:179–191.
48.
HiggsDM, RolloAK, SouzaMJ, PopperAN. Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J Acoust Soc Am, 2003; 113:1145–1154.
49.
ScholzK, LadichF. Sound production, hearing and possible interception under ambient noise conditions in the topmouth minnow Pseudorasbora parva. J Fish Biol, 2006; 69:892–906.
50.
AmoserS, LadichF. Diversity in noise-induced temporary hearing loss in otophysine fishes. J Acoust Soc Am, 2003; 113:2170–2179.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
