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The rapid growth of aquaculture raises questions about the welfare status of mass-produced species. Sagittal otoliths are primary hearing structures in the inner ear of all teleost (bony) fishes and are normally composed of aragonite, though abnormal vaterite replacement is sometimes seen in the wild. We provide the first widespread evaluation of the prevalence of vaterite in otoliths, showing that farmed fish have levels of vaterite replacement over 10 times higher than wild fish, regardless of species. We confirm this observation with extensive sampling of wild and farmed Atlantic salmon in Norway, the world's largest producer, and verify that vateritic otoliths are common in farmed salmon worldwide. Using a mechanistic model of otolith oscillation in response to sound, we demonstrate that average levels of vaterite replacement result in a 28-50% loss of otolith functionality across most of a salmonid's known hearing range and throughout its life cycle. The underlying cause(s) of vaterite formation remain unknown, but the prevalence of hearing impairment in farmed fish has important implications for animal welfare, the survival of escapees and their effects on wild populations, and the efficacy of restocking programs based on captive-bred fish.
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Scientific RepoRts | 6:25249 | DOI: 10.1038/srep25249
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High prevalence of vaterite in
sagittal otoliths causes hearing
impairment in farmed sh
T. Reimer1,2, T. Dempster1, F. Warren-Myers1,2, A. J. Jensen3 & S. E. Swearer2
The rapid growth of aquaculture raises questions about the welfare status of mass-produced species.
Sagittal otoliths are primary hearing structures in the inner ear of all teleost (bony) shes and are
normally composed of aragonite, though abnormal vaterite replacement is sometimes seen in the
wild. We provide the rst widespread evaluation of the prevalence of vaterite in otoliths, showing
that farmed sh have levels of vaterite replacement over 10 times higher than wild sh, regardless of
species. We conrm this observation with extensive sampling of wild and farmed Atlantic salmon in
Norway, the world’s largest producer, and verify that vateritic otoliths are common in farmed salmon
worldwide. Using a mechanistic model of otolith oscillation in response to sound, we demonstrate
that average levels of vaterite replacement result in a 28–50% loss of otolith functionality across most
of a salmonid’s known hearing range and throughout its life cycle. The underlying cause(s) of vaterite
formation remain unknown, but the prevalence of hearing impairment in farmed sh has important
implications for animal welfare, the survival of escapees and their eects on wild populations, and the
ecacy of restocking programs based on captive-bred sh.
Aquaculture is the world’s fastest-growing food production industry, producing over 66 million tonnes of sea-
food per year1. Growth in production has been driven by increased use of intensive farming systems, creating
health and welfare challenges, such as increased incidence of deformities, diseases and parasites. As such, welfare
outcomes for farmed sh in aquaculture systems have received heightened attention. Guidelines in many juris-
dictions are based on the ‘Five Freedoms’2, which specify freedom from discomfort, pain, injury, disease, fear and
distress, and stipulate freedom to exhibit normal behaviours. Intensive culture systems are also widely used for
re-stocking and conservation purposes3; if the performance of reared sh is compromised, the ecacy of such
programs is likely diminished.
One approach for detecting potential welfare eects of animal culture systems is to document dierences
between wild and farmed populations. Recently, dierences have been observed between the otoliths of farmed
and wild sh4. Otoliths are calcium carbonate structures in the inner ear labyrinths of vertebrates. ey are primi-
tive and conserved sensory organs which contribute to hearing, balance, gravity sensation and linear acceleration,
and are thus crucial for survival5. Otoliths are well studied in many wild sh species, as sagittal otoliths in par-
ticular provide an accurate record of age and growth. However, as the age and growth of farmed shes is usually
known, their otoliths are rarely studied. Sagittal otoliths are normally composed of aragonite, a polymorph of
calcium carbonate, but otoliths with inclusions of vaterite, an alternate polymorph, also occur6. ese ‘vaterite
otoliths’ are transparent and larger than their aragonite counterparts (Fig.1). Vaterite otoliths typically occur in
fewer than 10% of wild sh, although there are exceptions7. Prevalence of vateritic otoliths in farmed sh may
dier markedly from wild populations; several studies report vaterite in 50–60% of otoliths from hatchery-reared
sh8–13. However, comparisons between the prevalence of vaterite otoliths in farmed and wild populations are few.
No large-scale sampling has yet determined if vaterite is consistently more common in farmed populations, nor
if the phenomenon is localised or widespread.
e causes of vaterite replacement in sagittal otoliths are unknown, but the consequences have been partially
investigated. Oxman et al.14 used the auditory brainstem response (ABR) technique to test the hearing of Chinook
1Sustainable Aquaculture Laboratory – Temperate and Tropical (SALTT), School of BioSciences, University of
Melbourne, Victoria 3010, Australia. 2Research on the Ecology and Evolution of Fishes (REEF) laboratory, School of
BioSciences, University of Melbourne, Victoria 3010, Australia. 3Norwegian Institute for Nature Research (NINA), PO
Box 5685 Sluppen, 7485 Trondheim, Norway. Correspondence and requests for materials should be addressed to T.R.
(email: treimer@student.unimelb.edu.au)
Received: 13 November 2015
Accepted: 13 April 2016
Published: 28 April 2016
OPEN
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salmon with vaterite otoliths against those with normal otoliths. Salmon with at least one vateritic otolith (having
> 33% of otolith planar area replaced by vaterite) experienced a loss in otolith functionality, especially at fre-
quencies between 100–200 Hz. ese results show important dierences, but the authors used a coarse method
of vaterite classication and measured hearing loss only in relation to sound pressure level despite evidence that
salmonids rely on particle motion for sound detection15,16. It is therefore dicult to fully assess the eect of
vaterite on otolith functionality despite their ndings showing that no other part of the inner ear was aected by
the presence of vaterite14. Consequently, the authors’ conclusions that having one or two vaterite otoliths impairs
hearing to the same degree may be premature.
Modelling the hearing of sh may circumvent some limitations of experimental studies and provide a mech-
anistic understanding of how vaterite aects hearing. Lychakov and Rebane17 developed a model for predicting
the eect of otolith mass-asymmetry on sh hearing. Based on the physics of otolith movement, it can be eas-
ily adapted to model sensitivity dierences between vateritic and aragonitic otoliths. Models can also predict
responses outside the frequency ranges of conventional hearing tests; for salmon, which can hear sounds as low
as 0.1 Hz18, the eect of vaterite in the infrasound range is worth investigating. e model is based on parti-
cle motion rather than sound pressure, making it more suitable for assessing the eects of vaterite otoliths on
salmonids19.
Here, we synthesise previous knowledge on vaterite otoliths, and provide a detailed and mechanistic under-
standing of their consequences. We analysed all known published comparisons of vaterite otoliths in wild and
farmed populations to test if they are more prevalent in farmed sh. We conducted broad-scale sampling of
farmed and wild Atlantic salmon throughout Norway, the world’s largest farmed salmon producer and a country
with extensive wild populations, to eliminate confounding variables related to species, age and method of vaterite
classication. To test if patterns were globally generalizable, we also sampled harvest-size farmed Atlantic salmon
from Australia, Scotland, Canada and Chile. Finally, using a mechanistic model and data from Atlantic salmon
of three dierent sizes, we examined how the extent of vaterite replacement aects hearing, including into the
infrasound range, at dierent stages of the life history.
Materials and Methods
Analysis of existing literature for vaterite prevalence. We compiled previously published experi-
mental data to assess whether farmed sh consistently have a higher prevalence of vaterite otoliths. Studies were
found by searching for the keywords “vaterite, “aberrant”, “abnormal” or “crystalline” in relation to the sagittal
otoliths of any species using Web of Science and Google Scholar. To be included, papers must have (a) mentioned
vaterite specically or provided a suciently detailed description to allow its identication, and (b) provided data
on vaterite otoliths from both farmed and wild populations of the same species in a similar area. In total, seven
studies met the selection criteria. Where multiple age classes were available, only data from similar-aged sh was
used. To control for dierent scoring methods, prevalence of vaterite otoliths was measured as the proportion of
otolith samples containing any visible vaterite.
Vateritic otoliths in farmed and wild Atlantic salmon. Wild Norwegian Atlantic salmon were col-
lected from 21 rivers across Norway between 1986 and 2010 (Fig.2a). Otoliths from ten Atlantic salmon per
river were removed, cleaned of adhering tissue with ethanol and dried. Fiy individuals from ve populations of
farmed Atlantic salmon were sourced from four Norwegian hatcheries in 2014. e salmon were frozen whole
and sent to the Institute of Marine Research (IMR) in Matredal, Norway, where their otoliths were extracted,
cleaned of adhering tissue and dried. Otoliths were photographed under a dissecting microscope at 10–30×
magnication (depending on otolith size) and scored as ‘vaterite’ if any vaterite crystals were clearly identiable
Figure 1. Sagittal otoliths from a farmed Atlantic salmon juvenile. e le otolith (a) is entirely aragonite.
e right otolith (b) is approximately 90% vaterite by planar area, and the red line marks the border between the
aragonite core (dashed) and the surrounding vaterite (solid).
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or ‘aragonite’ if vaterite crystals were unclear or not present. Prevalence of vaterite was dened as the proportion
of vaterite otoliths in the sample. Otoliths were measured for total area and vaterite area using ImageJ.
To measure the changes in vaterite prevalence and extent over time, we used otoliths from three cohorts of
dierent sized sh: small (mean 33 g, range 17–53 g), medium (mean 334 g, range 108–582 g) and large (mean
4658 g, range 2775–6360 g), which correspond to approximate ages of 7, 12 and 18 months post-hatching, respec-
tively. ese salmon were reared at the Institute of Marine Research hatchery in Matre, Norway20–22. We also
collected 10–60 harvest-sized sh (4–6 kg) from Australia, Scotland, Canada and Chile. Where possible, sh were
purchased from multiple sources in each country to ensure samples came from several farms.
Otolith oscillation and mass-asymmetry model. We used a model that was developed by Lychakov
and Rebane17 to describe the dierential oscillation of mass-asymmetrical otolith pairs in response to acoustic
stimulation (1). is model was chosen for its explicit inclusion of otolith density, mass, planar area and volume,
as these factors are changed by vaterite replacement.
ωρ
γ
ρ
γ
∆=
+
+
αβ
αεα
α
βεβ
β
Aa
mV
A
mV
B() ()
(1)
xx
xx
2
2222
where Ax is oscillation amplitude, α and β are aragonite and vaterite otoliths respectively (replacing the original
R and L notation), ax is the oscillation of water and the sh’s body, ω is the wavelength of sound, m is mass in mg,
ρ=
ε1
g/cm3 is endolymph density, V is otolith volume,
γ=. ×
s13510
x
4
is a friction coecient,
s
is otolith area
in mm2, and
ωρδ=− +−+
αα
ε
αα
Ak mV
() (2)
xx
2
Figure 2. (a) Map of Norway showing sampling locations of farmed (green circle) and wild (red diamond)
populations. (b) Prevalence of vaterite sagittal otoliths in farmed (n = 5) and wild (n = 23) Atlantic salmon
populations. Map modied from https://pixabay.com/en/norway-map-country-europe-23574/.
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ωρδ=− +−+
ββ
ε
ββ
Bk mV
() (3)
xx
2
where =. ×
k s10810
x
7
is the stiness coecient for a saccular otolith and
δ=. m00241
x
is the additional mass of
an ellipsoid otolith. Otolith volumes were calculated by:
σρ σρ
=+−
V
m
(1 )
(4)
va
where
σ
is the proportion of planar area replaced with vaterite (expressed as a decimal), ρ
a = 2.95 g/cm3 is the
density of bioaragonite and ρ
v = 2.54 g/cm3 is the density of biovaterite23.
To realistically model otolith oscillation for farmed sh, model parameters were estimated using the oto-
liths of three dierent sizes of sh (Table1). Samples were weighed (± 0.05 mg for medium and large otoliths,
± 0.0005 mg for small otoliths) and mα was determined experimentally as the average mass of all aragonite oto-
liths for a given sh weight. mβ was determined by:
σ=. ′−.+.
βα
mm0951 0569 0237 (5)
where mα is the mass of the corresponding aragonite otolith. Similarly, aragonite planar area was determined as
the average area of aragonite otoliths for each size of sh. e planar area of vaterite otoliths was determined by:
σ=. +. +.
ββ
sm1113 1223 05089 (6)
Only one fully aragonite otolith was found among the large sh, so Eqs 5 and 6 were used to estimate the cor-
responding aragonite otolith parameters from vaterite samples.
is work was conducted in accordance with the laws and regulations of the Norwegian Regulation on Animal
Experimentation 1996. Experimental protocols were approved by the Norwegian Animal Research Authority.
Data analysis. Analysis of previous literature for vaterite prevalence. We calculated eect size by dividing
the proportion of otolith samples aected by vaterite in populations of farmed sh by those of wild sh. Statistical
signicance was tested using a paired t-test with studies as replicates.
Vateritic otoliths in farmed and wild Atlantic salmon. Prevalence of vaterite was analysed with an unpaired t-test
with the proportion of otoliths aected by vaterite in each area as replicates.
e proportion of vateritic otoliths in a sample was used to represent the probability of the onset of vaterite
formation. is probability was assumed to be independent between le and right labyrinths. To determine if
vaterite formation is biased towards one side, proportions of vateritic le and right otoliths were analysed with a
paired t-test across all sample sets. e expected number of sh with two vateritic otoliths was determined using
the product of the proportions of vateritic le and right otoliths, and was analysed against observed numbers with
a Chi-square test.
Results
Analysis of previous literature for vaterite prevalence. Existing studies indicated that farmed popu-
lations had 10.4 times higher incidence of vaterite sagittal otoliths (Table2, p < 0.001). Levels of vaterite did not
vary consistently with year of study or species. Overall, 8.6% of wild otoliths and 48.7% of farmed otoliths had
some level of vaterite replacement.
Vateritic otoliths in farmed and wild salmon. Norwegian Atlantic salmon yearlings raised in hatcheries
had 3.7 times higher incidence of vateritic otoliths than wild populations (Fig.2b, p < 0.0001). e percentage of
Norwegian sh aected increased with sh size, with 66% of small sh, 75% of medium sh and 100% of large sh
having at least one vateritic otolith. Average level of vaterite replacement also increased with sh size, from 47% in
small sh to 56% in medium sh and 88% in large sh, so that large sh had 1.9 times the vaterite replacement of
small sh (Table1). Le otoliths were more likely to be vateritic than right otoliths, with 58% and 52% of otoliths
showing vaterite formation, respectively (df = 64, p = 0.005). Of all sh sampled, 42% had two vateritic otoliths,
which was higher than the expected proportion of 39% (df = 1, p = 0.004). Incidence of vateritic otoliths was
similarly high in populations of harvest-size farmed Atlantic salmon from Australia (57% of otoliths vateritic,
Parameter
Fish size
Small Medium Large
Aragonite otolith mass (mα, mg) 0.83 3.2 9.2
Vaterite otolith mass (mβ, mg) 0.76 3.0 8.4
Aragonite otolith planar area (sα, mm2) 1.7 4.1 8.4
Vaterite otolith planar area (sβ, mm2) 1.9 4.5 11
Mean vaterite replacement (σ , %) 47 56 88
Table 1. Summary of model parameters calculated for aragonite and vaterite otoliths using three dierent
sizes of sh.
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n = 102), Scotland (58%, n = 38), Canada (30%, n = 64) and Chile (64%, n = 28), as well as rainbow trout from
Chile (48%, n = 17).
Otolith oscillation and mass-asymmetry model. Vaterite otoliths were on average 17% larger and 8%
lighter than their aragonite counterparts (Table1). All otoliths with vaterite replacement lost oscillation amplitude
compared to their aragonite counterparts, and increasing severity of vaterite replacement consistently resulted in
a larger loss of amplitude (Fig.3). When the level of vaterite replacement was the same across otolith sizes, small
otoliths lost the most oscillation amplitude, with a maximum of 46% lost at mean replacement (Fig.3, black lines).
Small otoliths were also greatly inuenced by changes in vaterite replacement, such that their maximum level of
oscillation loss varied by 39% within one standard deviation from the mean. Large otoliths were least aected by
changes in vaterite replacement, with oscillation loss varying by only 7.5% within the same interval. As observed
levels of vaterite replacement increased with otolith size (Table1), maximum average oscillation loss was 51% at
522 Hz for large sh, 29% at 583 Hz for medium sh, and 29% at 708 Hz for small sh (Fig.3, red lines). In the
infrasound range (1–20 Hz) small, medium and large otoliths with overall mean vaterite replacement lost 22%,
19% and 35% of oscillation amplitude, respectively.
Discussion
Fish raised in hatcheries are up to 10 times more likely to have vateritic sagittal otoliths than their wild counter-
parts, and may experience hearing loss as a result. Previous research has found dierences in the prevalence of
vaterite otoliths of 8.4–55% between wild and farmed sh (Table2). Our results show a dierence of 33%; farmed
Norwegian Atlantic salmon have levels of vaterite 3.7 times higher than their wild equivalents. is result is not
limited to Norway, as farmed Atlantic salmon from Australia, Scotland, Canada and Chile also have high levels of
vaterite replacement. Vaterite otoliths have decreased oscillation amplitude in response to sound, which impairs
functionality relative to aragonite otoliths. When vaterite replacement is consistent across all sizes, the eect is
more pronounced in smaller otoliths. However, larger otoliths have higher average vaterite coverage, so large sh
would suer the most impairment. is loss of oscillation amplitude due to vaterite occurs across the majority of
the salmon hearing range, including the infrasound.
Cultured sh worldwide may lose hearing sensitivity due to the farming process. e primary hearing range
of salmon is between 100 and 300 Hz, with a maximum tested frequency of 1000 Hz and a minimum of 0.1 Hz14,18.
Our results show that the more extensive an otolith’s vaterite coverage, the more its function is likely to be
impaired. is implies that sh with two vaterite otoliths will be more aected than those with only one, but this
is not supported by experimental evidence14. is dierence may be due to technical limitations inherent in the
non-invasive ABR technique and the coarse method of vaterite classication used by Oxman et al.14. Testing the
sensitivity of individual ears using our more precise measurement of vaterite coverage may discover the cause
of the discrepancy. Diculties could also stem from the measurement of sound pressure rather than particle
motion, which is the more relevant variable and can produce vastly dierent results24. Finally, the dierence in
results could be indicative of a compensatory mechanism in salmon aected by vaterite. However, this mecha-
nism evidently fails to fully compensate for hearing loss due to vaterite replacement and may only be present in
extreme cases. Further study of a compensatory mechanism would supplement our limited understanding of
salmonid hearing and how it is aected by culture systems.
Species with large otoliths are likely to be more severely aected by changes to the size, shape and density
of their otoliths due to vaterite replacement (Fig.3C). Some species also have an “indirect” pathway for sound
detection, where acoustic pressure is detected by the swim bladder, but this signal is still mediated by the oto-
liths16,25. erefore, even species with secondary hearing mechanisms may be susceptible to hearing impairment
from vaterite replacement. Hearing loss may be especially relevant in the infrasound range, as many underwater
mechanical sounds (such as those produced by swimming predators or struggling prey) are below 20 Hz15. e
results from our model show that vaterite may impair sensitivity in the infrasound as much as in the rest of
the salmonid hearing range, but hearing impairment has never been tested below 100 Hz. With further testing,
vaterite replacement could explain why hatchery salmon demonstrate decreased predator evasion and increased
mortality compared to wild shes3,26.
Study (data set) Species
Vaterite Prevalence (%)
Wild Farmed Dierence Eect size
Wat s o n 8Clupea harengus 6.1 60 53.9 9.8
Peck9O ncorhynchus kisutch 1.4 55.9 54.5 39.9
Bowen II et al.10 (5–12 yr) Salvelinus namaycush 24 48 24 2
Sweeting et al.11 (1997) Oncorhynchus kisutch 7 52 45 7.4
Sweeting et al.11 (1998) Oncorhynchus kisutch 8.4 56.6 48.2 6.7
Tomás & Geen23 Clupea harengus 5.5 13.9 8.4 2.5
Sweeting et al.12 Oncorhynchus kisutch 11.8 52.9 41.1 4.5
Brown et al.13 Oncorhynchus mykiss 5 50 45 10
Table 2. Analysis of previous literature comparing vaterite prevalence in sagittal otoliths of farmed and
wild populations. Sources8–13,23.
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Vaterite formation may also impair hearing directionality by creating mass asymmetry or, if only one otolith
is required for directional hearing, changing the way the otolith moves in relation to its associated hair cells27–29.
Our results show that vaterite formation results in a larger, lighter otolith and may be slightly biased towards the
le ear, but also suggest that once one otolith has begun vaterite formation, the other otolith is more likely to as
well. is implies that a large mass asymmetry is rare even in sh with vateritic otoliths. Lychakov and Rebane17
estimate that serious problems in directionality may only occur where mass asymmetry between otoliths is > 0.2,
and only one individual (< 0.1%) in this study achieved this. Vaterite replacement also changes the density, brit-
tleness, size, and shape of the otolith; density in particular may have a strong eect on directionality30. However,
the lagena and utricle also contribute to sound localisation, and aected sh may be able to develop compensatory
mechanisms. Further study is required to determine the individual and synergistic eects of vaterite’s properties
on the full range of otolith functions.
e high incidence of vaterite otoliths and their eect on hearing contravenes two of the ‘Five Freedoms,
thereby lowering the welfare of farmed shes2,31. Although our results cannot directly quantify the nature or
extent of hearing loss, we provide a mechanistic understanding and basis from which to study its potential behav-
ioural impacts. Impairment of a sh’s hearing due to vaterite replacement may prevent the expression of normal
behaviour, which is especially relevant in farmed species that communicate using sound (e.g. Yellow and Japanese
croaker32; Nile tilapia33). As deformity is a consequence of disease, the formation of vateritic sagittal otoliths
infringes on the freedom from pain, injury or disease. Other physical deformities are common in farmed salmon,
particularly in the jaw and spine34, and research into methods of prevention and treatment is ongoing35. As vater-
ite appears to be permanent once formation has begun, future control eorts should focus on prevention. Further
research is needed to investigate the cause(s) of vaterite formation in the otoliths of farmed sh.
Loss of hearing in captive-bred shes could have negative ecological impacts worldwide. Many wild rivers
are deliberately stocked with hatchery-reared salmon: in 2013, 5 × 109 juveniles were released into the Northern
Pacic Ocean alone36, and in some areas reared juveniles comprise over 70% of returning salmon11. However,
ocean survival rate of reared salmon is low, varying between 1% and 15%37,38. Vaterite replacement may contribute
Figure 3. Loss of otolith oscillation amplitude due to vaterite replacement at varying sound frequencies for (a)
small, (b) medium and (c) large salmon. Black lines represent average levels of vaterite replacement across all
sh at 64 ± 22% planar area [Mean ± SD]. Red lines represent the eect of mean levels of vaterite replacement
for small (47%), medium (56%), and large sh (88%).
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to this low return rate by impairing navigation and habitat selection important for survival27. Lack of hearing sen-
sitivity in the infrasound range may also reduce the eectiveness of acoustic dams, which rely on salmon showing
a strong aversion to infrasound15. Vaterite has never been investigated in salmon returning from the ocean, or
with respect to predator aversion and mortality. Future research into these areas could shed light on whether
hearing impairment is one of the underlying causes of dierential survival and reproductive success between
hatchery-produced and wild sh.
Data accessibility. e dataset supporting this article have been uploaded as part of the supplementary
material.
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www.nature.com/scientificreports/
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Scientific RepoRts | 6:25249 | DOI: 10.1038/srep25249
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Acknowledgements
e authors would like to acknowledge Dion Oxman and Allison Con for providing access to unpublished data
and Per-Gunnar Fjelldal and Tom Hansen for valuable discussions and support. is work was funded by the
University of Melbourne, Victoria, Australia.
Author Contributions
T.R. participated in study conception and design, collected data, conducted data analysis, interpreted results and
draed the manuscript; T.D. and S.S. participated in study conception and design, helped interpret results and
critically revised the manuscript; F.W.-M. participated in study conception and helped with data collection and
interpretation of results; A.J. collected wild Norwegian samples and critically revised the manuscript. All authors
gave nal approval for publication.
Additional Information
Supplementary information accompanies this paper at http://www.nature.com/srep
Competing nancial interests: e authors declare no competing nancial interests.
How to cite this article: Reimer, T. et al. High prevalence of vaterite in sagittal otoliths causes hearing
impairment in farmed sh. Sci. Rep. 6, 25249; doi: 10.1038/srep25249 (2016).
is work is licensed under a Creative Commons Attribution 4.0 International License. e images
or other third party material in this article are included in the article’s Creative Commons license,
unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license,
users will need to obtain permission from the license holder to reproduce the material. To view a copy of this
license, visit http://creativecommons.org/licenses/by/4.0/
... In teleost fishes, the largest pair of otoliths (the sagittae) are usually composed of a polymorph of calcium carbonate called aragonite. However, substitution of aragonite by vaterite, an alternative polymorph, has been documented in several species (1)(2)(3)(4)(5)(6)(7). Vaterite otoliths are larger, are deformed and have a lower density than aragonite otoliths (3,6,8). ...
... However, substitution of aragonite by vaterite, an alternative polymorph, has been documented in several species (1)(2)(3)(4)(5)(6)(7). Vaterite otoliths are larger, are deformed and have a lower density than aragonite otoliths (3,6,8). While relatively rare in wild fish, vaterite deposition is very common in hatchery fish and in aquaculture (2,4,6). ...
... Vaterite otoliths are larger, are deformed and have a lower density than aragonite otoliths (3,6,8). While relatively rare in wild fish, vaterite deposition is very common in hatchery fish and in aquaculture (2,4,6). Previous studies suggest that the presence of vaterite may impair hearing in salmonids (6,8) and alter the escape kinematics (9) in salmonids as young as 6 months old. ...
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... aragonite, Baltic herring, mineral composition, otoliths, vaterite, XRD The calcium carbonate (CaCO 3 ) matrix of sagittal otoliths is, in most cases, composed of aragonite, whereas the two other polymorphs, calcite and vaterite, are used relatively infrequently (Carlström, 1963;Gauldie, 1986;Reimer et al., 2016;Strong et al., 1986). Each of these polymorphs have their characteristic crystal structure, and a 'switch' from aragonite to either calcite or vaterite results in the formation or coprecipitation of a translucent or 'glass-like' crystalline matrix, which often also causes considerable distortion to the shape, density, brittleness, and ...
... size of the otolith (e.g., Gauldie, 1986;Tomás & Geffen, 2003). This nonaragonite crystallization, also referred to in the literature as 'aberrant' crystallization, has been documented in the otoliths of several fish species in various environments (e.g., Budnik et al., 2020;Loeppky et al., 2021;Melancon et al., 2005;Reimer et al., 2016;Tzeng et al., 2007), including juvenile Atlantic herring Clupea harengus L. in the Celtic and Clyde Seas (T omas and Geffen, 2003;T omas et al., 2004). Yet, the ultimate factors determining which CaCO 3 polyform is produced are still not completely understood (Thomas & Swearer, 2019). ...
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We report observations of vateritic crystallization in the sagittal otoliths of the Baltic herring Clupea harengus membras in the northern Baltic Sea. While the existence of vaterite in the calcium carbonate matrix of sagittal otoliths has been observed in various species globally, reports from the brackish Baltic Sea are few in number. Large variation in the frequency of vaterite in 1984, 1988, 1997, 2010 and 2017 was observed, suggesting that the phenomenon is not static and more long-term studies should be conducted in search of the ultimate causing factors. This article is protected by copyright. All rights reserved.
... Aragonite and vaterite otoliths differ in their densities and lattice structure; vaterite is less dense than aragonite (Tomas and Geffen 2003;Chakoumakos et al. 2016;Neves et al. 2017), resulting in otolith mass asymmetry (Vignon and Aymes 2020). The vaterite precipitation has a negative impact on auditory sensitivity in fishes (Reimer et al. 2016). Moreover, the functional, behavioural, and ecological implications of vaterite deposition at the organismal level are usually untested experimentally (Vignon and Aymes 2020). ...
... Several studies have reported abnormal otoliths which have different size, shape, and density as compared to normal otoliths in a number of freshwater and marine fishes (Sweeting et al. 2004;Oxman et al. 2007;Ma et al. 2008;Reimer et al. 2016). In the case of abnormal otoliths, the aragonite is replaced by vaterite but in some species, calcite may replace aragonite (Gauldie 1993;Campana 1999;Ma et al. 2008;Reimer et al. 2017). ...
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Otoliths are calcified structures and the information contained within their chemistry or shape can be used to infer life history events, migration patterns, and stock structure of a fish population. Understanding how otolith chemistry is affected by temperature, salinity, interactive effects of abiotic factors, ontogeny, physiology, etc. is essential for the reconstruction of the environment that affected the fish. Otolith shape is also affected by environmental conditions in addition to the genotype. The applications of otolith chemistry and shape for stock discrimination have increased in recent years because of the advancements in analytical methods and the related software. The stock identification methods sometimes provide variable results but if we use complementary approach the information generated could be more reliable which can be used to prepare effective management and conservation strategies. It appears warranted to generate more information on the factors influencing otolith chemistry and shape especially when two or more factors exert synergetic influence. Therefore, the objectives of this review paper were to provide comprehensive information on various factors influencing the otolith chemistry and shape, and the utility of otolith chemistry and shape for fish stock discrimination with an emphasis towards the research areas needing additional studies.
... Sagitta otoliths are normally composed of CaCO3 crystals arranged as aragonite. However, in aberrant sagitta, vaterite and calcite forms can be found in some species like salmon (Reimer et al., 2016;Austad et al., 2021), trout (Vignon & Aymes, 2020) and herring (Long et al., 2021) among others. Atlantic bluefin tuna (ABFT, Thunnus thynnus) is an oceanic marine species with an expansion in aquaculture. ...
... Vaterite deposition is commonly found in a range of fishes reared under aquaculture conditions, up to 3.7 times more frequent compared to wild populations (David et al., 1994;Tomas and Geffen, 2003). However, this proportion is much higher in the case of salmonids, with some studies reporting up to 80-100% of the individuals showing some degree of vaterite deposition (Gauldie, 1986;Reimer et al., 2016a;Sweeting et al., 2004). Vaterite otoliths are larger, more translucent, more fragile, and irregular than those formed by aragonite. ...
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In fish otoliths, CaCO3 normally precipitates as aragonite, and more rarely as vaterite or calcite. A higher incidence of vaterite deposition in otoliths from aquaculture-reared fish has been reported and it is thought that high growth rates under farming conditions might promote its deposition. To test this hypothesis, otoliths from growth hormone (GH) transgenic coho salmon (TF) and non-transgenic (NT) fish of matching size were compared. Once morphometric parameters were normalized by animal length, we found that TF fish otoliths were smaller (-24%, -19%, -20% and -30%; P<0.001 for length, width, perimeter and area, respectively) and rounder (-12%, +13.5%, +15% and -15.5% in circularity, form factor, roundness and ellipticity; P<0.001) than otoliths from non-transgenic fish of matching size. Interestingly, transgenic fish had smaller eyes (-30% eye diameter) and showed a strong correlation between eye and otolith size. We also found that the percentage of otoliths showing vaterite deposition was significantly smaller in transgenic fish (21-28%) compared to non-transgenic (69%; P<0.001). Likewise, the area affected with vaterite deposition within individual otoliths was reduced in transgenic fish (21-26%) compared to non-transgenic (42.5%; P<0.001). Our results suggest that high growth rates per se are not sufficient to cause vaterite deposition in all cases, and that GH overexpression might have a protective role against vaterite deposition, an hypothesis that needs further investigation.
... Sagitta otoliths are normally composed of CaCO3 crystals arranged as aragonite. However, in aberrant sagitta, vaterite and calcite forms can be found in some species like salmon (Reimer et al., 2016;Austad et al., 2021), trout (Vignon & Aymes, 2020) and herring (Long et al., 2021) among others. Atlantic bluefin tuna (ABFT, Thunnus thynnus) is an oceanic marine species with an expansion in aquaculture. ...
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... Vaterite, but not calcite, otoliths are commonly found in many aquaculture-reared fish species (Gauldie et al. 1997;Whitley et al. 1999), and some authors have suggested that vaterite deposition is the result of abnormally high growth rates (Reimer et al. 2017) or high animal density in the farms (Austad et al. 2021). Functionally, transmission of sound waves through otoliths is significantly influenced by the size of the otolith and the presence of non-aragonite CaCO 3 polymorphs, indicating that ocean acidification might have a negative impact on fish hearing and navigation if size and/or CaCO 3 composition are affected (Bignami et al. 2013;Radford et al. 2021;Reimer et al. 2016). Despite advances in understanding the effects of ocean acidification on otolith formation, the vast majority of studies have been focusing on larval and juvenile stages. ...
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The percentage of hatchery-reared coho salmon Oncorhynchus kisutch in the Strait of Georgia, British Columbia, increased from nearly 0% in the early 1970s to more than 70% by 2001. These estimates were derived from fin clip and coded wire tag data collected from commercial and sport fisheries, research surveys conducted in the summer and fall of 1997 to 2000, and examination of the microstructure of otoliths extracted from juvenile coho salmon collected during our marine surveys. The increasing trend may be related to the proportions of hatchery and wild smolts entering saltwater, fishing rates, and changes in the ecological processes regulating coho salmon production in the ocean. The consequence for management is that the abundance of wild spawning salmon (escapement) depends on hatchery as well as wild production. The consequence for policy makers is that future enhancement activities need to have clear policies for assessing the effects of hatchery fish on the population dynamics of wild fish as well as for producing hatchery fish.
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Aragonite is the normal form of calcium carbonate found in teleost otoliths, but it is sometimes replaced by vaterite, an alternate crystalline structure. We investigated the assumption that sagittal otoliths with vaterite replacement were unique to stocked lake trout Salvelinus namaycush in the Laurentian Great Lakes. Earlier studies had attributed these abnormalities to stocking stress, and proposed that the presence of vaterite could separate individual unmarked stocked lake trout from their wild counterparts. We examined and described the frequency of vateritic sagittae in two wild and three stocked populations of lake trout from the Great Lakes and a wild population from a remote inland lake in northern Canada. Among lake trout caught 2–12 years after being stocked, prevalence of vateritic sagittae was 66% for Lake Superior fish, 75% for Lake Huron fish, and 86% for Lake Ontario fish. Among wild fish caught, vateritic sagittae were present in 37% of Lake Superior fish, 22% of Lake Huron fish, and 49% of northern Canada fish. We also compared year-to-year differences in prevalence in four year-classes of fingerling lake trout reared in two U.S. national lake trout hatcheries. Prior to release, between 53 and 84% of the hatchery fish had at least one vateritic sagitta, and prevalence increased with handling associated with hatchery practices. Vateritic sagittae in wild fish might also indicate stress in nature. The presence of vateritic sagittae in both wild and stocked fish compromises the use of this characteristic as an unequivocal indicator of a particular fish's origin. Among-population differences in both the prevalence and the extent of vaterite replacement, however, may provide a means of differentiating between stocks of sympatric unmarked wild and stocked lake trout.
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The study of how fish make and respond to sound has important implications for communication, physiology, behavior, and commercial techniques. Fish Bioacoustics, a new definitive volume on fish auditory systems, will interest investigators in both basic research of fish bioacoustics as well as investigators in applied aspects of fisheries and resource management. Topics cover structure, physiology, localization, and acoustic behavior as well as more applied topics such as using sound to detect and locate fish. Contents: • Introduction to Fish Bioacoustics Richard R. Fay, Arthur N. Popper, and Jacqueline F. Webb • Hearing and Acoustic Behavior (Basic and Applied) Arthur N. Popper and Carl R. Schilt • Structures and Functions of the Auditory Nervous System of Fishes Richard R. Fay and Peggy L. Edds-Walton • Evolution of Peripheral Mechanisms for the Enhancement of Sound Reception Christopher B. Braun and Terry Grande • Bioacoustics and the Lateral Line of Fishes Jacqueline F. Webb, John Montgomery, and Joachim Mogdans • Orientation to Auditory and Lateral Line Stimuli Olav Sand and Horst Bleckmann • Multipole Mechanisms for Directional Hearing in Fish Peter H. Rogers and David G. Zeddies • Vocal-Acoustic Communication: From Neurons to Behavior Andrew H. Bass and Friedrich Ladich • Active and Passive Acoustics to Locate and Study Fish David A. Mann, Anthony D. Hawkins, and J. Mike Jech About the editors: Jacqueline F. Webb is Professor of Biological Sciences, and Coordinator of the Marine Biology Program, at the University of Rhode Island, Kingston. Richard R. Fay is Director of the Parmly Hearing Institute and Professor of Psychology at Loyola University of Chicago. Arthur N. Popper is Professor in the Department of Biology and Co-Director of the Center for Comparative and Evolutionary Biology of Hearing at the University of Maryland, College Park. About the series: The Springer Handbook of Auditory Research presents a series of synthetic reviews of fundamental topics dealing with auditory systems. Each volume is independent and authoritative; taken as a set, this series is the definitive resource in the field.
Article
Host-parasite interactions are moderated by the environmental conditions of the interaction medium (e.g. air or water). Encounter rate and the time available for a parasite to make physical contact with a host are both influenced by fluid dynamics, yet how they interact is poorly known. Here, we tested whether current velocities altered the initial attachment and post-settlement survival of an ecto-parasitic copepod (Lepeophtheirus salmonis) on Atlantic salmon. Current velocities strongly influenced attachment; infestation levels were 2.5 and 1.3 times higher in moderate than high and low velocity currents, respectively, while current velocities did not affect post-settlement survival. An interplay between a reduced host-parasite encounter rate in a low velocity current and reduced contact time in a high velocity current likely explains this result. Initial parasite attachment position was influenced by an interaction between current velocity and swimming behaviour, likely due to different fin positioning by fish in flows of different velocities. Our results imply that rapid swimming by salmon migrating out of coastal waters, usually described as adaptive against predation, could also be adaptive against parasitism. Infestation rates were also highest at the typical swimming speed of farmed salmon in coastal fish farms, which may be a hitherto unrecognised factor contributing to L. salmonis epidemics. Copyright © 2015. Published by Elsevier Ltd.
Article
Determining the value of restocking wild fisheries with hatchery-reared fish requires the ability to identify and quantify the survival of hatchery fish after release. However, to obtain accurate estimates of survival rates, multiple fish identification techniques are often used, making the monitoring of restocking inefficient and costly. Here we test a new immersion marking method to determine its efficiency and cost effectiveness for marking millions of hatchery-reared Atlantic salmon (Salmo salar). Salmon eggs were marked during the egg swelling stage by immersing eggs in a solution containing seven enriched stable isotopes (134Ba, 135Ba, 136Ba, 137Ba, 86Sr, 87Sr, and 26Mg) for 2 h immediately after fertilisation. One hundred percent successful marks were detected in the otoliths of resulting larvae at a concentration of 1000 μg·L-1 for 136Ba and 100 μg·L-1 for 135Ba and 137Ba, with no detrimental effects on survival or health of egg and yolk sac larvae. We estimate that seven unique mark combinations can be made at a cost of $0.0001 to $0.0017 (US) per egg and conclude that marking via egg immersion is suitable for low cost, accurate marking of hatchery-reared salmonids destined for restocking purposes. © 2015, National Research Council of Canada. All Rights Reserved.
Article
The otoliths of wild common sole, Solea solea, and Senegal sole, Solea senegalensis, from the Tagus and the Douro estuaries, and captive S. senegalensis were examined for the detection of anomalies. The anomalies detected were granules of crystals, a dark coloration over the entire otolith, a dark mark concentric to the nucleus and multiple nuclei. A higher proportion of anomalies was found in wild individuals of these species (16–63%) than is usually reported for other species. Captive S. senegalensis exhibited an incidence of anomalies within the range previously reported for other species also reared in captivity. The oceanographic–climatic conditions of the Portuguese coast, which cause strong and abrupt changes in water temperature, salinity and mineral composition, may be an important factor contributing to or causing otolith anomalies. Heatwaves, intense solar radiation and anthropogenic pollution affecting the estuarine nursery grounds may also play an important role. However, more experimental studies are needed to elucidate what causes otolith anomalies.
Article
In order to study the short-term effects of dietary P levels during juvenile rearing on mineral status (bone ash content), and its long-term effects on the development of vertebral deformities (radiography and external examination), triplicate groups of Atlantic salmon juveniles (1.3 g) were fed blue whiting meal (67%) based diets added 0 (0P), 3 (3P) and 6 (6P) g inorganic P kg− 1 (15, 18 or 21 g kg− 1 total P) for 77 days (18.3 g), and then followed up on a common commercial diet for 432 days (1927 g). At the termination of the period on the experimental feeds the vertebrae of the fish fed the 0P diet had a significantly lower ash weight than those fed the 3P and 6P diets, while there was no difference in the occurrence of radiological deformed fish. 252 days later, the 0P (31.7 ± 5.5%) dietary group had a significant higher occurrence of radiological deformed fish than the 6P dietary group (9.4 ± 5.6%), while the 3P dietary group displayed an intermediate level (19.7 ± 2.8%). At termination, 432 days after the termination of the experimental feeds, the 0P dietary group (5.9 ± 0.7%) had a significantly higher prevalence of externally deformed fish compared to the 3P (3.5 ± 0.9%) and 6P (2.0 ± 0.4%) dietary groups. This was mainly caused by a higher level of deformities in the caudal region (V31–58) of the vertebral column in the 0P group. There were no effects on mortality or growth of the present diets.The results show that inadequate P nutrition in a short period during the juvenile stage can predispose Atlantic salmon to develop vertebral deformities following seawater transfer.
Article
Although the physiological significance of the static organ is rather well established, little attention has been paid to the structure and composition of the dense bodies in the labyrinth of vertebrates. One exception is the work done on the well-known "ear-stones" of bony fishes. Ever since 1899, when Reibisch demonstrated that fish otoliths could be used for accurate age determinations, these bodies have been subjected to extensive studies. But on the whole, the information available regarding the nature of the calcareous deposits in the labyrinth of vertebrates other than teleosts is very meager. It has long been known that the dense bodies in the inner ear occur either as solitary large "ear-stones" or as masses of minute particles, "ear-dust." In what follows, the former will be referred to as "statoliths," and the latter as "statoconia." As is customary, the term "otolith" is used in a broader sense to mean any type of a dense body in the labyrinth. It is true that the function of statoliths and statoconia is not exclusively a static one (Lowenstein, 1950), but we prefer the use of these well-known terms to the introduction of entirely new ones. In the labyrinth of teleosts there are generally three large statoliths, each having an irregular unsymmetrical shape which is characteristic of the species. These bodies derive their names from their shape in carps: sagitta (arrow), lapillus (small stone), and asteriscus (star). They are located in sacculus, utriculus and lagena, respectively. Most other vertebrates, however, have otolith masses consisting of a very great number of small statoconia held more or less firmly together by an organic gel. The statoconia have microscopic dimensions, usually between 1 and 50 microns, are symmetrically shaped and are not characteristic for the species. Recently, otoliths having a size somewhere between statoliths and statoconia have been described by Frizzell and Exline (1958), who suggested the name "ossiculiths" (ossiculum bonelet + lithos stone) for such bodies. This term is rather unfortunate, not only because of the mixture of Latin and Greek, but especially because these bodies have nothing at all to do with bone. According to these authors, "ossiculiths" should be small (50-500 tL) plano-convex or irregularly shaped particles which are found occasionally with the ordinary statoliths of teleosts. However, in a high percentage of the individuals they occur in one of the labyrinths only, and are then often associated with malformed or abnormal statoliths (Weiler, 1959). "Ossiculiths" can thus hardly be regarded as normal formations in the teleost labyrinth. Irregularly shaped small bodies may, on the other hand, be found regularly together with statoconia, as in the labyrinth of the lamprey, Lamnpetra (Studnicka, 1912). In the labyrinth of sturgeons, Acipenser, all stages in shape and structure between statoconia and statoliths are found. Some of these intermediate-sized bodies have evidently
Article
The validity of the otolith technique for aging young Atlantic herring (Clupea harengus harengus) of the Maine commercial fishery was established by the Petersen and known-age methods. Tests of interpretation among different observers demonstrated a reproducibility of better than 90 percent.The study is based upon a collection of approximately 20,000 length measurements and 7,500 otoliths assembled from the catches between 1960 and 1962, and shows that the fishery is essentially a one-year-class fishery for 2-year-old herring.