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Aquaculture-derived trophic subsidy boosts populations of an ecosystem engineer


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Environmental management of coastal aquaculture is focused on acute impacts of organic and nitrogenous wastes close to farms. However, the energy-rich trophic subsidy that aquaculture provides may create cascades with influences over broader spatial scales. In a fjord region with intensive fish farming, we tested whether an ecosystem engineer, the white urchin Gracilechinus acutus, was more abundant at aquaculture sites than control sites. Further, we tested whether diets influenced by aquaculture waste altered reproductive outputs compared with natural diets. Urchins formed barrens at aquaculture sites where they were 10 times more abundant (38 urchins m⁻²) than at control sites (4 urchins m⁻²). Urchins were on average 15 mm larger at control sites. In the laboratory, urchins fed aquafeed diets had 3 times larger gonad indices than urchins fed a natural diet. However, their reproduction was compromised. Eggs from females fed an aquafeed diet had 13% lower fertilisation success and 30% lower larval survival rates at 10 d compared with females fed a natural diet. A reproductive output model showed that enhanced numbers of 10 d old larvae produced by the dense aquaculture-associated aggregations of G. acutus will supersede any detrimental effects on reproduction, with larval outputs from aquaculture sites being on average 5 times greater than control sites. The results show that aquaculture waste can act as a trophic subsidy in fjord ecosystems, stimulating aggregations of urchins and promoting the formation of urchin barrens. Where finfish aquaculture is concentrated, combined effects on the wider environment may produce ecosystem-level consequences.
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Aquacult Environ Interact
Vol. 10: 279–289, 2018 Published June 26
Trophic subsidies occur via the flow of energy be -
tween ecosystems, as both matter and organisms
(Larsen et al. 2016). Subsidies influence food web and
ecosystem dynamics in recipient environments, with
the quantity and quality of the subsidy exerting a
strong effect on the overall impact (Marcarelli et al.
2011). While trophic subsidies occur naturally, in -
creasingly, anthropogenic subsidies are driving
changes to ecosystems and food webs by altering the
distribution, abundance, growth and reproduction of
consumers in recipient environments (Marczak et al.
2007, Oro et al. 2013). Given over half of the human
population lives within 60 km of the coast (UNEP
2016), it is unsurprising that anthropogenic subsidies
© The authors 2018. Open Access under Creative Commons by
Attribution Licence. Use, distribution and reproduction are un -
restricted. Authors and original publication must be credited.
Publisher: Inter-Research ·
*Corresponding author:
Aquaculture-derived trophic subsidy boosts
populations of an ecosystem engineer
C. A. White1,2, 5,*, R. J. Bannister3, S. A. Dworjanyn4, V. Husa3, P. D. Nichols2,
T. Dempster1
1School of BioSciences, University of Melbourne, Parkville, Victoria 3010, Australia
2Oceans and Atmosphere, Commonwealth Scientific and Industrial Research Organization, Castray Esplanade, Hobart,
Tasmania 7000, Australia
3Institute for Marine Research, PO Box 1870, 5817 Bergen, Norway
4National Marine Science Centre, Southern Cross University, Coffs Harbour, New South Wales 2450, Australia
5Present address: Institute of Marine and Antarctic Studies, University of Tasmania, Nubeena Crescent, Taroona,
Tasmania 7053, Australia
ABSTRACT: Environmental management of coastal aquaculture is focused on acute impacts of
organic and nitrogenous wastes close to farms. However, the energy-rich trophic subsidy that
aquaculture provides may create cascades with influences over broader spatial scales. In a fjord
region with intensive fish farming, we tested whether an ecosystem engineer, the white urchin
Gracilechinus acutus, was more abundant at aquaculture sites than control sites. Further, we
tested whether diets influenced by aquaculture waste altered reproductive outputs compared
with natural diets. Urchins formed barrens at aquaculture sites where they were 10 times more
abundant (38 urchins m−2) than at control sites (4 urchins m−2). Urchins were on average 15 mm
larger at control sites. In the laboratory, urchins fed aquafeed diets had 3 times larger gonad
indices than urchins fed a natural diet. However, their reproduction was compromised. Eggs from
females fed an aquafeed diet had 13% lower fertilisation success and 30% lower larval survival
rates at 10 d compared with females fed a natural diet. A reproductive output model showed that
enhanced numbers of 10 d old larvae produced by the dense aquaculture-associated aggregations
of G. acutus will supersede any detrimental effects on reproduction, with larval outputs from
aquaculture sites being on average 5 times greater than control sites. The results show that aqua-
culture waste can act as a trophic subsidy in fjord ecosystems, stimulating aggregations of urchins
and promoting the formation of urchin barrens. Where finfish aquaculture is concentrated, com-
bined effects on the wider environment may produce ecosystem-level consequences.
KEY WORDS: Aquaculture · Echinus acutus · Gracilechinus acutus · Larval survival · Norway ·
Population density · Reproductive output · Sea urchin · Trophic subsidy · Urchin barren
Aquacult Environ Interact 10: 279–289, 2018
are common in marine systems. Examples include the
bulk input of nitrogenous and organic wastes (Gor-
man et al. 2009), fisheries discards (Oro et al. 2013)
and, increasingly, waste products from finfish and
shellfish aquaculture (Fernandez-Jover et al. 2011a).
Aquaculture of carnivorous fish in coastal waters
releases dissolved nitrogen and organic carbon to re-
ceiving environments, particularly through waste
feed and faecal material (Carroll et al. 2003, Bannister
et al. 2014). Outputs from cage aquaculture can drive
community change in the immediate surrounds of a
farm, in both benthic (Keeley et al. 2012) and pelagic
(Riera et al. 2014) systems, often leading to a prolifer-
ation of opportunistic taxa (Macleod et al. 2004, Kutti
et al. 2007). Less well understood are the impacts
of aquaculture subsidies on a broader scale, where
waste may be delivered in quantities more readily as-
similated by the wider ecosystem, with potential con-
sequences for the marine food web (Bannister et al.
2016, Broch et al. 2017). As aquafeed inputs are high
in lipid, waste from aquaculture is an energy-rich re-
source in the marine environment, with wild fauna
benefiting energetically from consumption (Parrish
2009). Wild marine fauna, including fish (Fernandez-
Jover et al. 2011b) and mobile invertebrates (Olsen
et al. 2012, White et al. 2017) consume aquaculture
waste. Proxy fitness measures, such as somatic and
liver condition indices, are higher in farm-associated
wild fish than wild fish caught distant from farms
(Dempster et al. 2011). However, potential repercus-
sions to the fitness of individuals and dynamics of
populations that receive aquaculture-derived trophic
subsidies remain un explored, as are the mechanisms
through which subsidies could cascade through eco-
systems on a broader scale.
As well as bulk quantity, the quality of a trophic re -
source determines ecosystem-level outcomes (Mar -
carelli et al. 2011). Modern aquaculture feeds have
lipid compositions that are relatively alien in the mar-
ine environment, as they are rich in shorter chain
(C18) polyunsaturated fatty acids (PUFA) derived
from terrestrial vegetable oils and meals, and low in
omega-3 long-chain (C20) PUFA (n-3 LC-PUFA),
produced by marine phytoplankton (Turchini et al.
2009, Nichols et al. 2014). As wild marine fauna typi-
cally have diets high in n-3 LC PUFA (Twining et al.
2016), high consumption of aquaculture waste repre-
sents a substantial quantitative and qualitative bio-
chemical shift in dietary intake. A shift in nutritional
quality of diet, combined with other challenges asso-
ciated with near farm environments, such as heavy
metals, synthetic chemicals and persistent organic
pollutants (Burridge et al. 2010, Samuelsen et al.
2015), may supersede fitness benefits associated with
the bulk organic subsidy. In this manner, aquaculture
outputs could function as an ecological trap, whereby
individuals are attracted to the trophic subsidy, with
detrimental fitness and reproductive consequences
(Robertson & Hutto 2006, Hale & Swearer 2016).
Norway is the largest producer of farmed Atlantic
salmon Salmo salar globally, with an annual produc-
tion exceeding 1.3 million t and 990 licensed farms in
2015 (Directorate of Fisheries 2016). In total, the
industry releases approximately 60 000 t of carbon,
34000 t of nitrogen and 9750 t of phosphorus into
fjord and coastal ecosystems (Ta ranger et al. 2015),
where it is available as a trophic resource for wild
fauna. Farms in Norway attract wild fish with an esti-
mated 12 000 t of wild fish aggregating around farms
on any given day in summer (Dempster et al. 2009).
Benthic productivity can also increase in farm areas,
particularly in deep fjords where productivity is lim-
ited and the addition of organic waste contributes
significantly to food supply (Kutti et al. 2007, Olsen et
al. 2012).
Sea urchins are ecosystem engineers in many
coastal ecosystems, altering habitat structure and
function through grazing, with ramifications for the
entire food web (Graham 2004, Ling 2008). The white
sea urchin Gracilechinus acutus (formerly Echi nus
acutus) is an ecosystem driver in the Norwegian
fjords, largely due to high grazing pressure on kelp
vegetation, with barren formation observed in areas
with dense aggregations (Husa et al. 2014). G. acutus
is omnivorous and consumes mussel spat, epibenthic
invertebrates and detritus, and can capitalise on
aquaculture waste as a trophic resource (White et al.
2017). Whether consuming aquaculture waste im -
proves or reduces fitness of G. acutus is at present
We investigated the effect of aquaculture on popu-
lation densities of wild G. acutus and tested the
physio logical and reproductive consequences of con-
suming an aquaculture-derived trophic subsidy. Pop-
ulation densities and reproductive outputs were then
combined to model the consequences of aquaculture
on populations of G. acutus. Current monitoring re -
gimes and management of aquaculture outputs are
generally focused on acute impacts directly associ-
ated with cage or lease zones. If the outcome of aqua-
culture subsidies is to drive broad-scale population
growth of a species able to act as an ecosystem engi-
neer, energy flow through coastal fjord ecosystems
may be altered, with this work having immediate re -
le vance in assessing ecosystem effects of salmon
White et al.: Aquaculture waste subsidies boost urchin populations
Urchin densities close to and distant from
aquaculture sites
In a region of western Norway with intensive
Atlantic salmon farming (Masfjorden; Fig. S1 in the
Supplement at www. int-res. com/ articles/ suppl/ q010
p279_ supp. pdf), we tested whether abundance and
size of the white urchin Gracilechinus acutus differed
between aquaculture and control sites. In August
2015, we assessed urchin abundance per m2 and col-
lected urchins to compare mean size at 4 salmon farm
sites and control sites 1.5−2.0 km away from the
nearest farm. Counts were done within 6 randomly
placed 1 m2 quadrants along a 50 m transect line at
5−10 m depth. At farm sites this was done in the sub-
tidal zone between shoreline and farm and as close
as possible to an active cage. The first 50 urchins
encountered per site were collected and measured
dorsoventrally at their widest point using callipers.
Effects of aquaculture waste feed in diets
on the reproductive outputs and physiological
responses of urchins
To determine whether the level of waste feed from
aquaculture contained in urchin diets affected spaw -
ning, subsequent development of larvae and their
survival, we fed urchins with manipulated diets and
followed the fate of the larvae. Urchins were col-
lected on SCUBA from Masfjorden, Hordaland, Nor-
way from a depth of 5−15 m in January 2015 with the
collection point >5 km from the nearest active farm.
Sixteen animals were randomly assigned to 1 of 15
aquaria (200 l) and supplied with flow-through sea-
water at ambient temperature and salinity (approxi-
mately 8.9°C and 34.8‰). Each of the aquaria were
given one of 3 diets for a period of 10 wk, with 5 repli-
cate aquaria per diet. Diet 1 contained a current com-
mercial Atlantic salmon Salmo salar feed (farm feed),
Diet 2 was a 1:1 combination of the commercial feed
and natural materials (composite feed) and Diet 3
contained only natural materials (natural feed). ‘Nat-
ural’ was defined as anything urchins were ob served
feeding on in the wild, or found within gut contents,
which were analysed from randomly collected wild
urchins prior to commencing the experiment. This
included macroalgae, including fucoid brown algae
Fucus vesiculosus and sugar kelp Sa charina lattis-
sima (70% w/w), mixed red algae (20% w/w),
encrusting flora and fauna from kelp (including
corallines, epiphytic red algae and bryozoans, 5%
w/w), mussel spat, gastropods and various crus-
taceans (5% w/w), all collected by diver from the
shallow subtidal zone.
Artificial diets for urchins were manufactured fol-
lowing the exact methodology outlined in White et
al. (2017). Samples of all 3 diets were retained and
stored at −80°C for subsequent analysis. Sea urchins
were held for 5 d without food prior to the start of the
feeding trial to standardize hunger. Diets were ana-
lysed for carbon, nitrogen and lipid to establish com-
parative energetics of each diet (Table 1). Animals
were fed once every 3 d during the experiment,
which ensured they were never food limited. All mor-
talities were recorded.
After 10 wk of feeding, urchins were induced to
spawn by injection of 2−3 ml of 1.0 M KCl. Eggs from
gravid females were collected in 500 ml beakers of
filtered seawater. Wild males were collected on the
morning of the spawning event and induced to
spawn, with sperm collected on petri dishes using
dry pipettes. Eggs were subsequently checked for
shape and integrity and sperm for motility. The eggs
of each female were fertilized by the sperm from
multiple (n = 5) males. Five lots of 200 eggs from each
female were placed in 100 ml sterile glass rearing
pots. The volume of sperm required to achieve a
sperm:egg ratio of 1000:1 was determined through
haemocytometer counts. The sperm was briefly acti-
vated in filtered seawater and added to containers
holding the eggs. Rearing containers were left for
10 min for fertilisation to occur, then flushed to re -
move excess sperm. Rearing containers were main-
tained at a temperature of 9.0°C (equivalent natural
fjord temperature) and flushed daily with filtered
Each rearing container was scored for percent fer-
tilisation success (2 h post-fertilisation) and percent
survival to 10 d post-fertilisation by counting the
number of viable eggs and larvae in the rearing con-
Aquafeed Composite Natural
% carbon 48.0 21.8 9.1
% nitrogen 2.7 3.0 0.7
% total lipid 13.3 7.9 0.4
% cholesterol 0.07 0.02 0.009
n-3:n-6 0.96 0.95 1.70
Table 1. Carbon, nitrogen and total lipid values for experi-
mental dietary treatments. n-3:n-6 refers to the ratio of
omega-3 polyunsaturated fatty acids to omega-6 polyunsat-
urated fatty acids within dietary treatments. % cholesterol
is given as the % of total lipid45
Aquacult Environ Interact 10: 279–289, 2018
tainers. Photographs of fertilised eggs and larvae
post-metamorphosis were taken using an Olympus
SZX7 dissecting microscope, Olympus DP26 digital
camera and cellSens Entry v1.7 image capture soft-
ware. Diameters of 30 fertilized eggs were measured
from each rearing container using ImageJ (NIH). The
length and symmetry of 10 d old larvae were recor -
ded using the criteria of Sheppard-Brennand et al.
At the conclusion of the experiment, gonad indices
were obtained for 5 randomly selected urchins from
each tank. Urchins were patted down to remove
excess external water and weighed. Gonads were
removed from the test and weighed. An index meas-
ure was obtained by dividing total weight by the
weight of the gonad. From 3 urchins per tank, 1
gonad was fixed in Bouin’s solution for histological
sectioning. Gonads were washed, dehydrated in
ethanol and soaked in a haemotoxylin, erythrosin
and saffron stain, then embedded in wax and cut into
3 µm sections before being set on slides for examina-
tion. The remaining 4 gonads were freeze dried, with
total lipid, n-3 LC-PUFA and n-6 PUFA content
measured using techniques described in White et al.
Statistical analysis
We tested whether abundance and size of urchins
differed between aquaculture and control locations
using ANOVA with location (‘aquaculture’ or ‘con-
trol’) as a fixed factor. The effects of diet on gonad
index, lipid content and respiration were tested using
ANOVA with diet as a fixed factor. For analysis of lar-
val success parameters (fertilisation success, larval
survival, egg size, larval size and symmetry), a single
mean data point for each female derived from larvae
across all 5 rearing containers was determined. We
used a PERMANOVA (Anderson et al. 2008) to test
the overall effect of diet across the multiple parame-
ters of larval success (using PRIMER v7 and its com-
plementary software package PERMANOVA+ (v7))
Monte Carlo (MC) p-values of 0.05 were used to indi-
cate significant differences between treatments.
SIMPER analysis was subsequently used to assess
the contribution of each parameter to the dissimi -
larity between treatments. Following this, 1-way
ANOVA was used to test whether fertilisation suc-
cess, larval survival, egg size, larval size and symme-
try varied with diet. For larval success parameters,
both 2-way multivariate and univariate analysis was
performed first with tank as a factor nested within
diet. Where the effect of tank was highly non-signifi-
cant (p 0.2), the design was collapsed and effects
examined through 1-way analysis with diet as a fixed
factor (Quinn & Keough 2002). All data were checked
for assumptions of normality and homogeneity ac -
cording to Quinn & Keough (2002), and data were
square root transformed where appropriate. Where
diets differed significantly (p 0.05), Tukey-Kramer
post-hoc tests were conducted to detect differences
among means.
Reproductive output model
We modelled the reproductive outputs of farm-
associated and control urchin populations in Mas-
fjord by using our data on the abundance, size and
larval fitness after exposure to different diet types.
The number of 10 d old urchin larvae (N) produced
by 1 m2of habitat in farm and non-farm conditions
was calculated as:
N= (DU/S) × (E/ FS) × LS(1)
where DUrepresents the density of urchins per m2
observed from field data, Srepresents the male:
female ratio (assumed to be 0.5 for all scenarios) and
Erepresents the number of eggs released by each
female, which is size dependent. We assumed the
number of eggs released by urchins increased with
size and was directly proportional as for other inver-
tebrates (Levitan 1991). Fecundity estimates from the
experiment indicated that a ripe 5 cm female pro-
duced 5 million eggs, which was the value used to
scale size-dependent egg release. FSand LSrepre-
sent the fertilization and larval survival rates ob -
tained through the experiment. Nwas calculated
using experimental values obtained for both aqua-
culture feed and composite diets for the ‘farm’ condi-
tions, while values for the natural diet were used to
calculate Nfor ‘non-farm’ conditions.
Urchin densities close to and distant from
aquaculture sites
Abundance of urchins was 3 to 100 times greater at
aquaculture than control sites (F4, 44 = 31.6, p <
0.0001) (Table S1). All 4 aquaculture sites were char-
acterised by high densities of urchins (29−47 m–2)
and urchin barrens, compared with lower densities
(0.2−13.2 m–2) in control locations where only 1 of 4
White et al.: Aquaculture waste subsidies boost urchin populations
sites could be characterised as an urchin barren
(Fig. 1A). Mean test diameters were consistently
smaller (4−25 mm on average) at aquaculture than
control sites (F3, 390 = 33.2, p < 0.0001; Fig. 1B). There
was also a significant location effect for both abun-
dance (F4,44 = 3.2, p < 0.04) and test diameter (F3, 390 =
71.5, p < 0.0001) of urchins.
Effects of aquaculture waste feed in diets
on the reproductive outputs and physiological
responses of urchins
Mortality of adults throughout the 10 wk exposure
period was uniform across dietary treatments and did
not exceed 4 individuals from any tank. Females were
successfully induced to spawn from each treatment.
Diet altered larval survival and growth para meters
(F2,10 = 4.3, p(MC) = 0.03) (Tables S2S4), with % sur-
vival 10 d post fertilisation, fertilisation success and
echinopluteal length identified by SIMPER as con-
tributing to over 70% of dissimilarity be tween diets.
Fertilisation success, egg diameter and echinopluteal
length all increased linearly from aquafeed to com-
posite to natural dietary treatments, while larval
asymmetry decreased (Fig. 2). Survival of larvae 10 d
post-fertilisation varied with dietary treatment (F2, 10
= 7.0, p = 0.01), with survival of larvae from the natu-
ral treatment over 30% higher than the aquafeed
Fig. 1. Results from the field survey of Gracilechinus acutus
(A) urchin abundance (m–2) and (B) average test size ± SE at
control and farm locations across 4 sites in Masfjord, Norway
Fig. 2. Mean (±SE) effects of dietary treatment on larval success and development of Gracilechinus acutus measured as (A) %
fertilisation success and % survival 10 d post fertilisation, (B) egg diameter (µm), (C) pluteal length, being the average length
of the pluteal arms (µm) and (D) % asymmetry obtained by the difference in length of pluteal arms. Superscript letters in (A)
denote significant treatment effects
Aquacult Environ Interact 10: 279–289, 2018
treatment and 24% higher than the composite treat-
ment (Fig. 2).
Urchins fed aquafeed diets had 1.5 and 4.0 times
larger gonads compared with the composite and
natural diets, respectively (F2,12 = 17, p < 0.0001;
Fig. 3A) (Table S5). When examined on a per unit
mass basis, total lipid content in gonads or eggs did
not differ with diet, with gonads ranging from 11.1 to
13.7 mg g−1 total lipid dry mass and eggs slightly
higher at 13.0−18.1 mg g−1 total lipid dry mass
(Fig. 3B). Likewise, the n-3 LC-PUFA:n-6 PUFA ratio
in gonads (F2,12 = 2.0, p = 0.2) and eggs (F2, 6 = 0.1, p =
0.9) was similar across diets, despite the n-3 LC-
PUFA:n-6 PUFA ratio being approximately double in
natural feed, compared with the aquafeed or com-
posite feeds (Fig. 3C, Table 1). Eggs were more
enriched in n-3 LC-PUFA compared with gonads for
all diets, varying between 1.65 and 1.75, which was
also the n-3 LC-PUFA:n-6 PUFA ratio of natural feed
(Fig. 3C, Table 1). Gonad histology indicated that
membrane-bound vesicles within the nutritive pha -
go cyte were emptier in urchins fed the aquafeed or
composite diet, but filled with varying granular con-
tents in urchins fed natural feed (Fig. 4).
Reproductive output model
Model results indicate that aggregations of adult
urchins at aquaculture sites will lead to a net increase
in the number of 10 d old larvae surviving in the
water column, compared with a natural scenario
(Fig. 5). Larval output from 1 m2of fjord in aqua -
culture locations subject to aquaculture feed or com-
posite diets were on average 5 times greater than
control locations with natural diets, although this var-
ied between locations (Fig. 5). Larval outputs under
the most ecologically relevant composite diet were
21% greater than for the aquaculture feed diet due to
greater survivorship of larvae.
We demonstrated that high densities of sea urchins
aggregate at aquaculture sites, while control sites
had far lower urchin densities. High densities of ur -
chins at aquaculture sites could form through attrac-
tion and aggregation of larval, juvenile or adult
urchins, or via reduced mortality of urchins at aqua-
culture sites compared with controls, or a combina-
tion of these processes. While we could not separate
mechanisms leading to aggregations of urchins,
aquaculture sites create suitable conditions for the
formation and persistence of urchin barrens, with
possible wider consequences for fjord ecosystems.
The occurrence of dense populations of urchins at
aquaculture sites places them directly at the source
of the greatest waste deposition, which they readily
consume (White et al. 2017). The trophic subsidy is
qualitatively different from natural feeds and creates
changes in the reproductive capabilities of urchins
that receive it. When abundance data and reproduc-
tive outputs data are combined, each aquaculture
site can be a population source for urchins, produc-
Fig. 3. Mean (±SE) effects of dietary treatment on Graci -
lechinus acutus lipid content measured as (A) standardized
gonad index, (B) total lipid (mg lipid g−1 dry mass) in gonads
and eggs, and (C) n-3 LC-PUFA:n-6 PUFA in gonads and
eggs. Superscript letters in (A) denote significant treatment
White et al.: Aquaculture waste subsidies boost urchin populations
ing 5 times more competent 10 d old
larvae than control sites in the same
fjord. Overall, consuming an aqua -
culture waste subsidy affects both in -
dividuals and populations of ur chins,
with potential ecological consequen -
Effects on individuals
Gonad indices of Gracilechinus acu -
tus differed corresponding to the pro-
portion of aquafeed in the dietary
treatments. As gonads act as both a re-
productive and an energy storage or-
gan in sea urchins (Marsh & Watts
2001, Walker et al. 2001), it is un -
surprising that increases in dietary
carbohydrate, protein and lipid lead to
larger gonad indices. An energy-rich
subsidy in the wild could have impli-
cations for enhanced survival during
periods of food limitation, with urchins
able to reabsorb energy stores when
required to meet metabolic demands
(Kelly 2000). Given the importance of
maternal lipid reserves in facilitating
larval survival (Byrne et al. 2008, Car-
boni et al. 2012), offspring from the
aquafeed and composite dietary treat-
ments would have been expected to
have higher fertilisation and larval
success rates. Paradoxically, the oppo-
site oc curred, with the proportion of
aquafeed in maternal diet correspon-
ding to smaller eggs and decreased
fertilisation and larval survival at 10 d.
While urchins in the experiment were
never food limited, those fed lower-
energy diets may supply resources to
reproductive development in favour of
somatic growth (Kelly & Cook 2001,
Otero-Villanueva et al. 2004). Given
the lower lipid values of the natural
experimental diet, but similar lipid
concentrations in eggs compared with
other diets, combined with larger egg
size, there is some evidence this oc-
curred in females fed natural diets.
The biochemical composition of diet
may play an important role in the
increased success of larvae produced
Fig. 4. Histological examination of the gonads of Gracilechinus acutus using
haemotoxylin erythrosin saffron stain as (A) male urchins fed the aquafeed
treatment, (B) female urchins fed the aquafeed treatment, (C) male urchins
fed the composite treatment, (D) female urchins fed the composite treatment,
(E) male urchins fed the natural treatment and (F) female urchins fed the
natural treatment. NP: nutritive phagocyte; OO: oocyte; SP: spermatozoa.
Scale bar = 50 µm
Fig. 5. Model output showing the number of Gracilechinus acutus 10 d old
larvae (×106) present in the water column from a 1 m2section of fjord in both
aquaculture and control locations, under aquafeed (light grey), composite
(dark grey) and control (white) dietary conditions
Aquacult Environ Interact 10: 279–289, 2018
by females fed natural diets. Lipid composition of the
aquafeeds used were high in terrestrially derived C18
PUFA and low in marine-derived C20 n-3 LC-PUFA,
which is the current global standard for grow-out
feeds in commercial finfish aquaculture (Turchini et
al. 2009, Nichols et al. 2014). Increased levels of ter -
res trially derivedoil in thediet, particularly in creased
n-6 PUFA, led to decreased sperm viability and fertil-
isation rates of guppies (Rahman et al. 2015) and ur -
chins (White et al. 2016), while high intake of marine-
derived n-3 LC-PUFA promotes growth and develop-
ment of urchin larvae (Carboni et al. 2012). There was
no difference in the n-3 LC-PUFA:n-6 PUFA ratio of
gonads or eggs among dietary treatments; however,
G. acutus can selectively accumulate particular fatty
acids from diet or biosynthesize essential fatty acids
from dietary substrates (White et al. 2017). This con-
siderably alters the fatty acid profile of body tissue
compared with diet and can help overcome limita-
tions in essential fatty acids (White et al. 2017). How-
ever, there is a limit to this capacity, and there are
unknown energetic costs (Laurel et al. 2010).
Performance of larvae may also be influenced by
other feed components. Although not measured in
this study, protein is important for successful larval
development and survival in sea urchins (Marsh &
Watts 2001) and interacts with lipid during uptake
and assimilation (Cook et al. 2007). As eggs pro-
duced by G. acutus females fed natural diet are
larger, yet contain similar concentrations of lipids to
the other diets, they may contain a higher proportion
of another metabolic component important to sur-
vival. In the wild, G. acutus forms dense aggrega-
tions on detrital macroalgae and a preference for
macroalgae is common in omnivorous urchins (e.g.
Echinometra chloroticus, Barker 2001; Psammechi-
nus miliaris, Kelly & Cook 2001). Therefore, specific
compounds that improve larval development may
occur in algal components of the natural diet, en -
hancing its overall nutritional value and therefore
larval success. Alternatively, another component of
the aquaculture feed itself may be detrimental to lar-
val success.
Population-level effects
Regardless of the physiological mechanism, female
G. acutus fed diets containing salmon aquaculture
feed produced larvae with lower survival rates at 10 d
than those fed a natural diet. Given the dense aggre-
gations of G. acutus at farms, by reducing re -
productive outcomes, aquaculture waste may act as
an ecological trap (Robertson & Hutto 2006, Hale &
Swearer 2016). The exact effect on populations will be
a balance between the physiological benefits that the
resource provides to individuals and populations, ver-
sus any detrimental effects on reproductive outputs.
Our reproductive model suggested that the numbers
of sea urchins at aquaculture sites negate any detri-
mental effects that consuming aquaculture feed have
on offspring. Barren areas are common where dense
aggregations of G. acutus are found, with urchins
able to maintain a lower limit of kelp vegetation (Husa
et al. 2014). Urchins were smaller at aquaculture com-
pared with control locations, with reduced body sizes
typical where densities of urchins are high (Levitan
1989, 1991). Subsequently, the energetic benefit of
the resource to the individual may be limited due to
high competition for the trophic subsidy. However,
the overall net effect on the population is positive, as
high population densities in broadcast spawners such
as G. acutus can en sure fertilisation success before
gametes become dilu ted (Quinn et al. 1993, Wahle &
Peckham 1999, Gascoigne et al. 2009). As such, in-
creased population densities of G. acutus around
aquaculture sites will increase larval abundances, de-
spite animals being smaller compared with more iso-
lated animals at control locations (Levitan 1991, Levi-
tan et al. 1992, Lundquist & Botsford 2011). As our
model could not account for this important Allee ef-
fect, relative fertilisation success at aquaculture sites
is likely under estimated.
Given the larval retention time for G. acutus is ap-
proximately 50 d (MacBride 1903, Gage et al. 1986),
larvae from aquaculture-associated aggregations will
disperse widely and settle beyond the aquaculture
zone where they were released. While this could in-
crease the spatial influence that aqua culture has on
urchin populations, it may also dilute its effect. How-
ever, in a typical fjordal circulation pattern, where a
thin low-salinity surface layer flows seaward, and
with a compensatory landward flow beneath this, a
large proportion of larvae are likely to be entrained
within the fjord. This phenomenon occurs for the sea
urchin Evechinus chloroticus in New Zealand fjord
systems (Lamare 1998, Wing et al. 2003), which pro-
duces similarly small, negatively buoyant plank-
totrophic larvae to G. acutus with similar development
times (Lamare 1998, Tyler & Young 1998). If entrain-
ment of larvae occurs in fjord systems with intensive
aquaculture, increases in larval production will be
concentrated, with effects compounded over time.
A more precise estimation of the impact of aqua-
culture on G. acutus populations across larger spatial
scales may be possible with further information on a
White et al.: Aquaculture waste subsidies boost urchin populations
number of key variables, such as the extent of suit-
able settling habitat within the fjord, and the spatial
and temporal persistence of aggregations around
aquaculture sites. The link between pelagic and ben-
thic systems and factors that may influence success-
ful metamorphosis and settling of G. acutus larvae
will also aid better estimates of the overall impact
that an aquaculture subsidy may have on a fjord-
wide scale. Moreover, as our survey depth only
extended to 10 m and G. acutus has a depth range
that potentially reaches 2000 m (Tyler & Young
1998), we were only able to capture a small propor-
tion of the total aggregation in our survey. Whether
the aquaculture subsidy actually acts as attractant,
causing G. acutus to migrate to shallower depths
around farms, requires further investigation.
The reproductive output model predicted an in -
crease in the number of larvae in the water column
each year due to aquaculture. When tracing assimila-
tion of farm waste, White et al. (2017) found urchins
consumed feed up to 350 m from farms. Using this
value as the demarcation between ‘aquaculture af -
fected’ and normal fjord, we can examine broader
effects of urchin aggregations around farms. Given
the total coastline of Masfjorden (70 km), this results
in 6% of coastline within the fjord affected by aqua-
culture. When coupled with outputs from the repro-
ductive model, this equates to an increase of approx-
imately 20% in the amount of urchin larvae in the
fjord system each year. Given that aquaculture com-
menced in the 1970s in Norway (Husa et al. 2014)
and has expanded with time, a long-term interaction
of this nature has broad implications for the creation
of urchin larvae population sources in fjord eco -
systems. Only observational data exist on urchin
populations prior to the commencement of aqua -
culture in the fjords (Jorde & Klavestad 1963), mak-
ing it difficult to fully assess the long-term impact of
aquaculture on urchins. However, the wider ecologi-
cal effects of urchin aggregations, such as barren for-
mation, suggest that enhanced production of urchin
larvae on a fjord-wide scale has the potential to drive
ecosystem-level change.
Sea urchins occur naturally in Norwegian fjords,
and localised barren areas existed due to G. acutus
overgrazing prior to the introduction of large-scale
salmon aquaculture (Jorde & Klavestsd 1963, Husa et
al. 2014). However, our results show that these events
can be promoted by aquaculture subsidies. Aquacul-
ture waste is an energy-rich trophic subsidy and can
stimulate dense aggregations of urchins at farm sites.
Consumption of aquaculture waste alters biochemical
physiology and reduces larval success; however,
modelling indicates that adult density ef fects will su-
persede any detrimental effects on reproduction in
terms of net reproductive output. Like many urchin
species, G. acutus is an ecosystem engineer that can
drive ecosystem-level change via barren formation
through overgrazing on kelp. Risk-based assessment
on appropriate spatial and temporal scales is required
to fully understand the extent of interactions between
aquaculture-derived trophic sub sidies and popula-
tions of urchins in fjord eco systems.
The lack of regional baseline data for benthic com-
munities, on both soft and hard substrate, is not an
uncommon scenario in environments where aquacul-
ture has expanded from small-scale operations to
multi-farm operations with high regional densities.
An understanding of localised impacts may be ade-
quate where aquaculture operations are small. How-
ever, when aquaculture operates at high regional
densities, diffuse effects can become additive and
influence change on a much broader spatial scale,
where unfortunately, baseline data are often lacking.
As aquaculture continues to expand, it is critical to
capture a robust environmental baseline through
which broad-scale changes can be evaluated in the
future. Further exploration of the interaction be -
tween G. acutus and finfish aquaculture is warranted
to fully assess and subsequently mitigate any conse-
quences for broader ecosystem function in the Nor-
wegian fjords.
Acknowledgements. This work was supported by a Univer-
sity of Melbourne Overseas Research Experience Scholar-
ship (ORES) and the Norwegian Research Council (Project
no. 228871). The authors thank S. A. Olsen, K. A. Kvestad, B.
Haugland Taraldset, S. Woodcock, N. Keeley, B. Muir, F.
Oppedal, Ø and Ingrid Uglenes Fiksdal. Strand and T.
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Editorial responsibility: Pablo Sánchez Jerez,
Alicante, Spain
Submitted: December 12, 2017; Accepted: May 2, 2018
Proofs received from author(s): June 12, 2018
... Changes in fish feed composition has increase the content of terrestrial-derived n-6 polyunsaturated fatty acids (n-6 PUFAs) and reduced marine-derived omega-3 long chain PUFAs (n-3 LC-PUFAs; Sprague et al., 2016). n-3 LC-PUFAs are known to be critical to growth and reproduction in marine organisms and the consequences of these changes on consumers of waste feed and faeces such as zooplankton, sea urchins, crabs, lobster and fishes are being investigated (Sardenne et al., 2020;Barrett et al., 2018;White et al., 2018;Woodcock et al., 2018;Fernandez-Jover et al., 2011). For example in a laboratory study, White et al. (2018) reported that sea urchin (Gracilechinus acutus) eggs from females fed a fish feed diet low in n-3 LC-PUFAs had 13% lower fertilisation success and 30% lower larval survival rates at 10 days compared with eggs from females fed a natural diet. ...
... n-3 LC-PUFAs are known to be critical to growth and reproduction in marine organisms and the consequences of these changes on consumers of waste feed and faeces such as zooplankton, sea urchins, crabs, lobster and fishes are being investigated (Sardenne et al., 2020;Barrett et al., 2018;White et al., 2018;Woodcock et al., 2018;Fernandez-Jover et al., 2011). For example in a laboratory study, White et al. (2018) reported that sea urchin (Gracilechinus acutus) eggs from females fed a fish feed diet low in n-3 LC-PUFAs had 13% lower fertilisation success and 30% lower larval survival rates at 10 days compared with eggs from females fed a natural diet. Some researchers have suggested that aquaculture feed could act as a trophic subsidy for wild species but the population-level effects of a shift in fatty acid composition in wild species have yet to be examined (Sardenne et al., 2020;White et al., 2018;Fernandez-Jover et al., 2011). ...
... For example in a laboratory study, White et al. (2018) reported that sea urchin (Gracilechinus acutus) eggs from females fed a fish feed diet low in n-3 LC-PUFAs had 13% lower fertilisation success and 30% lower larval survival rates at 10 days compared with eggs from females fed a natural diet. Some researchers have suggested that aquaculture feed could act as a trophic subsidy for wild species but the population-level effects of a shift in fatty acid composition in wild species have yet to be examined (Sardenne et al., 2020;White et al., 2018;Fernandez-Jover et al., 2011). ...
Globally, lobsters are one of the most economically valuable wild species caught in capture fisheries. Catches are dominated by American lobster (Homarus americanus) landed entirely in Atlantic Canada and northeastern United States. In Atlantic Canada, lobster fishing and marine finfish aquaculture take place in the same coastal waters creating the potential for negative environmental, as well as social, interactions. We review the state of knowledge of environmental interactions between American lobster, their habitat and fishery, and marine finfish aquaculture. We first provide a brief overview of key biological, behavioural, and ecological processes and environmental stressors of American lobster at different life-history stages followed by an overview of the pathways of effects of marine finfish aquaculture on coastal ecosystems in general and on American lobster. Our review found that certain finfish aquaculture-lobster interactions have received considerable study (e.g., chemical use), whereas knowledge of other interactions are either limited (e.g., net pens, waste discharges) or lacking (e.g., disease, noise, lights, and odours). An ecosystem-based approach to aquaculture has been proposed for managing these interactions but implementing this approach has proven to be a challenge in part because of complex multi-sector, multi-stakeholder and multi-agency governance issues. While governance solutions await development, practical measures based on the results of scientific research identified in this review, such as better use of existing oceanographic and bathymetric data, habitat and human impact assessment tools, and toxicity information offer regulators ample information and management tools, at least at the farm- and bay-scale, to avoid negative finfish aquaculture-lobster interactions in Atlantic Canada. Bridging the governance gap will likely require new community-based management models that more effectively identify, generate, and integrate local community and fisher knowledge and concerns.
... Broader ecosystem changes may also occur through trophic shifts or interaction of fish wastes with high-value habitats, or in habitats that are more sensitive to organic waste deposits. 9,13,14 To provide more context to potential environmental risks and broader consequences of farming activities, there is thus a clear need to understand how solid fish farm waste is dispersed and assimilated in any given environment. ...
... where increases in terrestrial fatty acid markers in both field and lab conditions indicated that fish waste was assimilated and incorporated into the gonads and eggs. 27 Subsequent work on the same species demonstrated that a diet with high proportions of terrestrial ingredients resulted in lower fertilisation and larval survival rates compared to individuals feeding on natural diets, 14 and thus a generally lower reproductive output. However, despite lower reproductive outcomes at the individual level, when the reproductive output estimates were combined with higher species abundance estimates from the farming area, the overall reproductive output of the population was higher compared to control areas, where urchins were less abundant. ...
Full-text available
Particulate waste from open-cage fish farms in marine systems can cause organic enrichment of seabed habitats and enter the food web through consumption by wild organisms, with potential for broader ecosystem changes. Effects on biogeochemistry and benthic ecology are reasonably well understood in inshore, sheltered and soft sediment systems. However, food web effects and interactions with epifauna and larger consumers is less well understood, as is the fate of these discharges in more dynamic coastal areas with complex hydrodynamic regimes. Expected expansion of the aquaculture industry globally includes farming new areas that are more environmentally dynamic and biodiverse, with potentially sensitive habitats. Therefore, the aim of this review was to examine how biochemical tools can assist in identifying and managing impacts. Biochemical tools such as bulk stable isotopes and fatty acids can reliably trace the fate of fish waste in the environment and the food web, and have advanced our understanding of waste dispersal, as well as providing greater insights into biological interactions with fish wastes. This includes elucidating trophic subsidies to wild organisms, candidate species for co-culture and waste assimilation mechanisms in native communities. Ultimately, biochemical tools can support improved environmental management, by helping to identify the zone of influence for spatial planning, providing additional ‘forensic’ evidence for farm-related change, and by identifying potential risks to high-value species and habitats. In this way, they can inform targeted research to link fish waste inputs meaningfully to potential ecosystem changes to better understand the consequences to support sustainable industry expansion. © 2023 The Authors. Reviews in Aquaculture published by John Wiley & Sons Australia, Ltd.
... In a laboratory experiment, White et al. (2016) found no differences in lipid profiles in gonads or eggs in the sea urchin Heliocidaris erythrogramma fed a natural (mixed), current feed (n3-n6 ratios currently used by the industry), and future feed diets (very low n3-n6 ratios that could be used if the proportion of terrestrial fatty acids keep increasing in feed used by the industry); current feed did not influence reproductive processes, but future feed had serious consequences on egg diameter, fertilization, and larval development and survival. Finally, in the sea urchin Echinus acutus, a laboratory diet of fish feed increased gonad size, gonad, and egg terrestrial fatty acid content when compared to a natural diet (White et al., 2017b), resulting in reduced egg and larval quality (White et al., 2018). While we observed negative impacts of feeding rock crabs solely with salmonid feed, it is important to remember that the experiment was designed to investigate the 'worst-case scenarios' where individuals are obliged to feed on a single item. ...
... Even if individuals spend significant time under farms and consume predominantly finfish feed, the effects at the individual level will translate into changes at the population level based on the proportion of a population that frequents farms (White et al., 2018). In turn, this value will depend on the overall proportion of the habitat where farms are present and farm attraction. ...
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Shellfish and salmonid aquaculture operations in Eastern Canada attract several mobile epibenthic species as a result of added structural complexity and increased food availability (bivalve fall-off and waste salmonid feed). It is not clear whether the aggregation of predators and scavengers below coastal farms contributes positively or negatively to their population dynamics, due to concerns about the quality of food items found under farms. We conducted an 18-month laboratory study to investigate the effect of diets composed of 1) mixed items, 2) mussels (Mytilus edulis), and 3) salmonid feed on the performance and condition of the rock crab, Cancer irroratus. Diet had no impact on crab survival but several negative consequences were observed in crabs fed the salmonid feed diet when compared to the mixed diet: reduced 1) moulting rates during the second growing season, 2) inter-molt growth, 3) gonad and hepatopancreas indices, 4) hemolymph dissolved compounds, 5) hepatopancreatic glycogen, and 6) shell hardness. Crabs fed the mussel diet had similar performance and condition when compared to the mixed diet. Fatty acid composition of muscle, gonad, and hepatopancreas tissues revealed that a salmonid feed diet decreased n3/n6 ratio when compared to a mixed or a mussel diet; those differences were mostly due to increases in the proportions of terrestrial (18:1n9 and 18:2n6) and decreases in proportions of marine essential (20:5n3 and 22:6n3) fatty acids. Together, these results point to a minimal impact of a mussel-only diet on crabs, whereas the salmonid feed diet resulted in negative impacts on condition. Our experimental results explored the consequences of a ‘worst-case scenario’ in which crabs were forced to feed on a single item for a long period of time; the realized impact in field settings will depend on other factors such as consumption of alternate food items underneath a farm, proportion of time spent in farms, and level of overlap between crab habitat and aquaculture facilities.
... Nevertheless, stable isotopes δ 13 C and δ 15 N values, VOFA proportions (OA, LA, ALA) and the ω6 : ω3 FA ratio provide insight into habitat use and dietary habits of cage-associated fish, but sea cage use of wild fish may vary seasonally(Dempster et al. 2002) and further study on a larger temporal scale is needed.Future research areas should focus on individual biological changes, community changes and patterns of wild fish association with sea cages. Aquafeed-derived energetic subsidies have been linked to increases in condition and growth of laboratory G. morhua(Olsen et al. 2015), as well as improved survival, faster maturation and reproduction in cage-associated fish(Rennie et al. 2019), and altered growth and weight observed in sessile cage-associated organisms(Handå et al. 2012, White et al. 2018. Composition and abundances of surrounding benthic communities are also significantly impacted by sea cage aquaculture(Kalantzi & Karakassis 2006, Terlizzi et al. 2010, Cullain et al. 2018), as well as pelagic communities(Papastamatiou et al. 2010. ...
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Sea cage aquaculture can alter the spatial distribution of wild fish populations; however, little is known about the dietary habits and subsequent effects on wild fish. In this thesis, I used stable isotopes δ 13 C and δ 15 N values and proportions of vegetable oil-based fatty acids (VOFAs) to investigate the dietary habits of wild cage-associated Atlantic cod Gadus morhua and Atlantic redfish Sebastes fasciatus. Furthermore, I compared the length, weight and condition of cage-associated G. morhua ages 2-4 years old to reference sites within the local division and outside divisions removed from aquaculture, and used VOFAs as biomarkers for waste feed consumption to identify any role(s) in explaining differences in length, weight and condition among age classes. Juvenile G. morhua captured around sea cages had depleted δ 13 C and δ 15 N values and elevated proportions of VOFAs consistent with waste feed consumption and sea cage residency, whereas differences in δ 13 C, δ 15 N, and VOFAs in cage-associated adult G. morhua and S. fasciatus were predominately absent. Interestingly, waste feed consumption by age 2 cage-associated G. morhua resulted in lower condition than age 2 G. morhua from the local reference division; however, age 4 cage-associated G. morhua were longer and heavier than the local reference division, despite no evidence to support direct or indirect waste-feed consumption. Overall, the results of this thesis suggest that δ 13 C, δ 15 N and VOFAs are suitable biomarkers for tracing sea cage residency and dietary habits of cage-associated wild fish, but waste feed consumption patterns and subsequent effects on wild fish were paradoxical and dependent on species and life stage.
... The addition of nutrients and heavy metals into coastal systems can impact seaweed directly through uptake but also through the interaction with excess sediment (Strain et al. 2015), decreased light availability (Kavanaugh et al. 2009), and other stressors all of which can indirectly impact seaweed communities and their trophic interactions (White et al. 2018). The response of Tasmanian seaweed communities to excess nutrients is comparable to that described by Pearson and Rosenberg (1978) such that, when systems are enriched, longer-lived and more stable species are progressively replaced with faster growing ephemeral species (Fowles et al. 2018a;Oh et al. 2015;White et al. 2022). ...
Tasmania is an island state in south-eastern Australia that has a long and rich history of seaweed use, research, and development. It is a cool-temperate system with 750 macroalgal species currently described. Tasmanian Aboriginal peoples have lived on this land for at least 40,000 years utilising seaweed as food, shelter, water carriers and medicine, as well as for ceremonial reasons. Modern taxonomic investigations began with French naturalist Jacques-Julien Houtou de La Billardière in 1791, and there are 184 type specimens of seaweeds originating from Tasmania. Ecological and physiological studies of seaweed in Tasmania have focussed on the dominant large brown seaweeds (Laminariales and Fucales) and have contributed significantly to the global understanding of these systems, particularly related to community resilience, seaweed-urchin interactions, their habitat-forming role for other species, responses to global change, and restoration of lost habitat. Ocean warming and changing oceanography have caused a 95% decline in surface canopy cover of Macrocystis pyrifera in eastern Tasmania since the 1950s and led to a focus on restoring these lost forests. Tasmanian seaweed communities have a uniquely high proportion (up to ∼90%) of seaweeds that rely solely on CO 2 for photosynthesis, which has implications for responses to ocean acidification. Tasmania has industries that use brown seaweeds for fucoidan extraction and beach-cast harvest for alginates, fertilisers, and feeds for agriculture. New aquaculture initiatives include integrated multi-trophic aquaculture, offshore kelp mariculture and Asparagopsis cultivation for bioactive products to reduce methane emissions in ruminants, as and the development of unexploited species including Caulerpa spp. for food.
... At 2018 feed prices (~$US 2.20 per kg; Iversen et al., 2020), this represents an economic loss of ~$US 500 million per year. Feed loss also has ecological consequences, including accumulation of waste feed in surrounding benthic ecosystems and changing the natural diets of wild fauna around farms (Kutti et al., 2007;Fernandez-Jover et al., 2011;Dempster et al., 2011;White et al., 2018). Solutions lie in more effective feed control strategies and technologies, which have been poorly explored and underdeveloped by the scientific community. ...
Automation of feeding control for sea-caged Atlantic salmon is important to reduce waste feed. Hydroacoustic appetite-led feeding, or echofeeding, uses echo sound to monitor fish biomass in a defined feeding area. As the fish become satiated and begin to leave the feeding area, the monitored biomass falls, enabling the setting of threshold levels of biomass at depth. Software then decides to continue or stop feeding. Here, we implemented a fully autonomous echofeeding system in 3 sea cages with salmon during summer (900 g, ~14 °C) and winter (5300 g, ~5 °C). To find the best signal of feeding activity, fish biomass was monitored with two echo sounder transducers at different depths and echo beam widths, directed upwards towards the feeding area. Prior to echofeeding, we trained salmon to consume their daily ration in short, intense feeding bouts. The fish adapted to consume their daily food ration in just 1 h and sustained their feeding activity close to the surface under the echofeeding regime. The feeding response was positively correlated with feeding intensity and was strongest at the surface (0–1.5 m), with a narrow echo beam from 8 m depth giving the best proxy of fish appetite. Appetite varied between meals and days, yet echofeeding prevented waste feed while fish maintained strong growth rates. Echofeeding is simple to deploy, as farmed salmon, independent of fish size or season, can adapt to changes in feeding regimes. Both feeding intensity and the biomass threshold for feeding cessation were kept static under echofeeding, which challenge the industry's standard manual feeding control practice where feeding intensity is adjusted by visually assessing appetite within meals. Our results provide novel insight into basic principles of hydroacoustic-based feeding and autonomous feeding control in general and highlight echofeeding as a promising technology.
... One striking example is when excessive inputs of allochthonous carbon from newly inundated riparian areas during high river flows create hypoxic conditions that can cause largescale deaths of fish and other riverine organisms, and thus the loss of the steady state [7,8]. Similarly, the transfer of large amounts of organic matter from agricultural activity into natural ecosystems can fundamentally alter trophic dynamics: trophic cascades can be initiated and rare or uncommon species can become invasive while functionally important common species decline [9]. Such examples demonstrate the sensitivity of ecosystems to variation in the direction, extent and biochemical pathways associated with subsidies [10]. ...
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Migratory animals can act as cross-boundary subsidies sustaining ecosystem functioning, such as diadromous fishes that migrate between fresh water and seawater and carry nutrients and energy across the freshwater-marine ecotone. Frequency and timing of migration are however highly variable within and among populations. We hypothesized that in catadromous fishes (i.e., diadromous fishes that grow in freshwater and spawn in the sea, such as eels), the import of subsidies by migratory juveniles could outweigh the export of subsidies by adults due to skipped spawning migration. We used the diamond mullet Planiliza ordensis, as a model species, and determined life-history traits using a combination of length-to-age data, acoustic telemetry and otolith (fish ear stone) microchemistry. We used a mass balance approach to model individual mass acquisition and allocation, and extended our model to other life-history strategies. Our results showed high intra-population variation of migratory behaviour in P. ordensis, with few individuals migrating every year to spawn. We estimated that an individual P. ordensis acted as a net 42.6g biomass subsidy in fresh water, representing a retention of more than 50% of the juvenile mass at freshwater entry. Our model predicts that skipped spawning is likely to alter the allocation of subsidies in diadromous species, highlighting the important effects of individual variation in migratory behaviour on fluxes of energy and nutrient at ecosystem scales. We encourage future studies to consider how variation in migratory behaviour is likely to affect the direction and magnitude of biomass fluxes across ecotone boundaries.
... Future research areas should focus on individual biological changes, community changes and patterns of wild fish association with sea cages. Aquafeedderived energetic subsidies have been linked to increases in condition and growth of laboratory cod (Olsen et al. 2015) as well as improved survival, faster maturation and reproduction in cage-associated fishes (Rennie et al. 2019), and altered growth and weight observed in sessile cage-associated organisms (Handå et al. 2012, White et al. 2018). Composition and abundances of surrounding benthic communities are also significantly impacted by sea cage aquaculture (Kalantzi & Karakassis 2006, Terlizzi et al. 2010, Cullain et al. 2018) as well as pelagic com-munities (Papastamatiou et al. 2010, Arechavala-López et al. 2013. ...
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Sea cage aquaculture can alter the spatial distribution of wild fish populations, however little is known about the dietary habits of wild fish frequenting sea cages. We used wild juvenile cod (Gadus morhua) reared in the laboratory and fed either an aquafeed pellet or marine-based diet to determine trophic discrimination factors (TDFs) of stable carbon (𝛿13C) and nitrogen (𝛿15N) isotope values in white muscle tissue and baseline liver proportions of vegetable-oil based (VOB) fatty acids. We then used 𝛿13C and 𝛿15N and proportions of VOB fatty acids to investigate the dietary habits of wild cage-associated juvenile and adult Atlantic cod and adult Atlantic redfish (Sebastes fasciatus). Cod and redfish were collected in the immediate area of sea cages and reference areas of no aquaculture production. Juvenile cod captured around sea cages had both elevated 𝛿13C and 𝛿15N values and proportions of VOB fatty acids, and isotopic fractionation comparable to laboratory cod fed an aquafeed diet. However, differences in 𝛿13C and 𝛿15N and proportions of VOB fatty acids between cage-associated and reference site adult cod and redfish were predominately absent. Results suggest that sea cages may provide an energetic subsidy to juvenile cod but perhaps not at the level to sustain adult cod or redfish. Therefore, the lack of differences suggests that both adult groups may be using cage sites opportunistically and only for short duration, as isotopic values and fatty acid proportions were not consistent with waste feed consumption despite individuals being collected in close proximity to sea cages.
... Yet, some species of urchin (e.g. Gracilechinus acutus) can regulate the omega-3: omega-6 ratio in their gonads, despite being fed an aquaculture feed high in terrestrial omega-6 polyunsaturated fatty acids (White et al., 2018). To date, most studies investigating the effect of dietary lipid content in formulated urchin feeds found that lipid source or concentration had little effect in improving urchin gonad size after roe enhancement (Gibbs et al., 2013;Kennedy et al., 2007;Pantazis et al., 2000). ...
Sea urchin gonads (roe) are a prized global sea food commodity, with growing demand driving the need for urchin roe enhancement aquaculture. Effective roe enhancement of urchins using formulated feeds require species‐specific optimization and an understanding of the interactions between key dietary components (e.g. protein, lipid, carbohydrate, energy and/or algal supplements). Here, we tested 18 formulated feeds on the sea urchin Heliocidaris erythrogramma, collected from barrens. The 18 iso‐energetic (~20 MJ/kg) feed combinations contained one of three protein levels (250, 375 or 500 g/kg), three lipid levels (73, 101 or 131 g/kg) combined with a single (45 g/kg Sargassum spp.) or multiple (45 g/kg Sargassum spp., 25 g/kg Solieria robusta, 25 g/kg Ulva lactuca) dried algal supplement. From two consecutive 12‐week enhancement trials, the most optimal feed type contained 375 g/kg protein, 73 g/kg lipid and a 45 g/kg algal supplement (Sargassum spp.) and produced gonad indices of 18.5 ± 0.4% (Trial 1) and 21.7 ± 1.2% (Trial 2). Across feed types, there was no significant difference in the proportion of marketable quality (A and B grade) roe produced (56%–85% Trial 1, 65%–85% Trial 2). We conclude that roe enhancement of H. erythrogramma collected from barrens is highly feasible.
... Large grazing fronts of the sea urchin Echinus esculentus (Linnaeus, 1758) were regularly observed and are known to feed on algae and associated epiphytes (Jorde & Klavestad 1963, Comely & Ansell 1988. Sea urchins can also exploit and assimilate farm waste (White et al. 2017(White et al. , 2018, and may benefit from intensive farming. This is a potential ecological factor that was not within the scope of this study but needs to be further examined. ...
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Large-scale finfish farms are increasingly located in dispersive hard-bottom environments where Laminaria hyperborea forests dominate; however, the interactions between farm effluents and kelp forests are poorly understood. Effects of 2 levels of salmonid fish-farming effluents (high and low) on L. hyperborea epiphytic communities were studied by sampling canopy plants from 12 sites in 2 high-energy dispersive environments. Specifically, we assessed if farm effluents stimulated fast-growing epiphytic algae and faunal species on L. hyperborea stipes—as this can impact the kelp forest community composition—and/or an increased lamina epiphytic growth, which could negatively impact the kelp itself. We found that bryozoan biomass on the stipes was significantly higher at high-effluent farm sites compared to low-effluent farm and reference sites, resulting in a significantly different epiphytic community. Macroalgal biomass also increased with increasing effluent levels, including opportunistic Ectocarpus spp., resulting in a less heterogeneous macroalgae community at high-effluent farm sites. This habitat heterogeneity was further reduced by the high bryozoan biomass at the high-effluent sites. Such changes in the epiphyte community could have implications for the faunal community that relies on the epiphytes for food and refuge. On the kelp lamina, no clear response to farm effluents was found.
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A spatially explicit coupled hydrodynamic-mass transport model system was used to simulate dispersal of particulate organic matter from Atlantic salmon (Salmo salar) farming in central Norway. Model setups of 32 m horizontal resolution were run for periods of up to 650 days for 3 sites of different oceanographic characteristics: one fjord location, one medium-exposed location influenced by fjord water, and one coastal location. Records on feed used for each cage at each location were converted to feces released based on a published mass balance model. The results from the simulations were compared with scores from corresponding mandatory benthic surveys (MOM-B) of the sediment layer beneath the farms. The correspondence between simulated and measured thickness of the sediment layer was good, and improved with the inclusion of resuspension processes. At all sites the distribution of organic matter in the bottom layer was non-homogeneous, with significant temporal variation and transport and settling of matter up to at least 0.5 km away from one of the farms. Our results indicate that the monitoring practice used in Norway until now, with a few sediment grab samples taken mainly within the fish farm, may not adequately determine the areal impacts of all salmon farming operations. The patchy distribution of organic matter and the correspondence between simulation and survey results is attributed to the use of full 3D current fields of a high spatiotemporal resolution and a good model for resuspension processes that some previous model studies have failed to properly account for.
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Ecological traps, which occur when animals mistakenly prefer habitats where their fitness is lower than in other available habitats following rapid environmental change, have important conservation and management implications. Empirical research has focused largely on assessing the behavioural effects of traps, by studying a small number of geographically close habitat patches. Traps, however, have also been defined in terms of their population-level effects (i.e. as preferred habitats of sufficiently low quality to cause population declines), and this is the scale most relevant for management. We systematically review the ecological traps literature to (i) describe the geographical and taxonomic distribution of efforts to study traps, (ii) examine howdifferent traps vary in the strength of their effects on preference and fitness, (iii) evaluate the robustness of methods being used to identify traps, and (iv) determine whether the information required to assess the population-level consequences of traps has been considered. We use our results to discuss key knowledge gaps, propose improved methods to study traps, and highlight fruitful avenues for future research. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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Streams and adjacent terrestrial ecosystems are characterised by permeable boundaries that are crossed by resource subsidies. Although the importance of these subsidies for riverine ecosystems is increasingly recognised, little is known about how they may be influenced by global environmental change. Drawing from available evidence, in this review we propose a conceptual framework to evaluate the effects of global change on the quality and spatio-temporal dynamics of stream-terrestrial subsidies. We illustrate how changes to hydrologic and temperature regimes, atmospheric CO2 concentration, land-use, and the distribution of non-indigenous species can influence subsidy fluxes by affecting the biology and ecology of donor and recipient systems and the physical characteristics of stream-riparian boundaries.
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e supply and demand of omega-3 highly unsaturated fatty acids (ω-3 HUFA) in natural ecosystems may lead to resource limitation in a diverse array of animal taxa. Here, we review why food quality in terms of ω-3 HUFAs is important, particularly for neural tissue, across a diversity of animal taxa ranging from invertebrate zooplankton to vertebrates (including humans). Our review is focused on ω-3 HUFAs rather than other unsaturated fatty acids because these compounds are especially important biochemically, but scarce in nature. We discuss the dichotomy between ω-3 HUFA availability between aquatic primary producers, which are often rich in these compounds, and terrestrial primary producers, which are contain little to none of them. We describe the use of fatty acids as qualitative and quantitative tracers for reconstructing animal diets in natural ecosystems. Next, we discuss both direct and indirect ecological implications of ω-3 HUFA limitation at the individual, population, food web, and ecosystem scales, which include: changes in behavior, species composition, secondary production rates, trophic transfer efficiency and cross-ecosystem subsidies. We finish by highlighting future research priorities including a need for more research on ω-3 HUFAs in terrestrial systems, more research their importance for higher order consumers, and more research on the food web and ecosystem-scale effects of ω-3 HUFA limitation.
Trophic subsidies can drive widespread ecological change, thus knowledge of how keystone species respond to subsidies is important. Aquaculture of large carnivorous fish generates substantial waste as faeces and lost feed, providing a food source to mobile benthic invertebrates. We used a controlled feeding study combined with a field survey to better understand the interaction between salmon aquaculture and the sea urchin, Echinus acutus, a dominant mobile invertebrate in Norwegian fjords. We tested if diets affected urchin fatty acid composition by feeding them one of three diet treatments ("aquafeed", "composite" and "natural") for 10weeks. To test if proximity to fish farms altered E. acutus fatty acid composition, populations were sampled at 10 locations in Hardangerfjord and Masfjord (Western Norway) from directly adjacent and up to 12km from farms. Fatty acids were measured in gonads and eggs in the diet experiment and in gonads and gut contents from wild animals. Urchins directly assimilated aquaculture waste at farm sites, as evidenced by elevated linoleic acid (LA), oleic acid (OA) and ∑LA, OA in their tissues. The diet experiment highlighted the biosynthetic and selective dietary sparing capacity of E. acutus in both gonads and eggs, with evidence for the elongation and desaturation of eicosapentaenoic acid (EPA) and arachidonic acid (ARA) from C18 fatty acid precursors. Elevated biosynthesis of non-methylene interrupted (NMI) fatty acids, in particular 20:3Δ7,11,14 and 20:2 Δ5,11, were also linked to a high C18 fatty acid, low ≥C20 long-chain polyunsaturated fatty acid (LC-PUFA) diet. Fatty acid composition of gonads of wild urchins indicated a highly variable diet. The study indicates that the generalist feeding ecology of E. acutus, coupled with extensive biosynthetic capacity, enables it to exploit aquaculture waste as an energy-rich trophic subsidy.
Aquaculture of higher trophic level species is increasingly dependent on the use of terrestrial oil products. The input of terrestrially derived n-6 polyunsaturated fatty acids (PUFA) into marine environments has subsequently increased, with unknown consequences for recipient species. We exposed a sea urchin, Heliocidaris erythrogramma to three experimental diets for 78 days: a high n-3 PUFA marine imitation treatment, a high n-6 PUFA “future aquafeed” treatment and an intermediate “current aquafeed” treatment. Female urchins fed the high n-6 PUFA diet produced larvae with lower survival rates than all other treatments. Males fed the high n-6 PUFA diet produced no viable sperm. Fatty acid composition in reproductive material revealed comprehensive biosynthetic and dietary sparing capabilities in H. erythrogramma. Despite this, the ratio of n-6 PUFA to n-3 PUFA in reproductive tissue increased significantly with diet. We suggest alterations to this ratio is the likely mechanism of negative impact on larval development.
As a part of a general survey of the natural history of the Hardangerfjord, in the county of Hordaland, Norway, a study of the benthonic algal vegetation was made; this was carried out mainly in summer. The area includes the outer coastal area, the outer fjord area (archipelago) and the fjord proper, where glacier-fed rivers discharge very turbid water during summer floods. The algal vegetation changes in composition from the outer to the inner reaches of the area, the “fjord effect” consisting mainly in an impoverishment of the littoral as well as the sublittoral flora. On entering the fjord proper, the lower limit of the vegetation rises from about 30 m to 10–15 m. This level was recorded throughout the fjord, even in the fjord branches where turbidity is very high in summer. The environmental factors which appear to be mainly responsible for the gradual reduction in the number of species are salinity range and water movement (turbulence, exposure). The latter is also suggested as responsible for the change in depth limit on entering the fjord proper. The fjord effect upon the algal vegetation seems to be far more pronounced in the Hardangerfjord than in other Norwegian fjords investigated, apparently as a result of its topography. Detailed records of distribution are given for all species together with charts of distribution for selected species.
Human activities are the main current driver of global change. From hunter-gatherers through to Neolithic soci-eties–and particularly in contemporary industrialised countries–humans have (voluntarily or involuntarily) provided other animals with food, often with a high spatio-temporal predictability. Nowadays, as much as 30–40% of all food produced in Earth is wasted. We argue here that predictable anthropogenic food subsidies (PAFS) provided historically by humans to animals has shaped many communities and ecosystems as we see them nowadays. PAFS improve individual fitness triggering population increases of opportunistic species, which may affect communities, food webs and ecosystems by altering processes such as competition, predator–prey interactions and nutrient transfer between biotopes and ecosystems. We also show that PAFS decrease temporal population variability, increase resilience of opportunistic species and reduce community diversity. Recent environmental policies, such as the regulation of dumps or the ban of fishing discards, constitute natural experiments that should improve our understanding of the role of food supply in a range of ecological and evolutionary processes at the ecosystem level. Comparison of subsidised and non-subsidised ecosystems can help predict changes in diversity and the related ecosystem services that have suffered the impact of other global change agents.
Off-shore fish cages are new artificial habitats that can affect pelagic fish assemblages and constitute an important food source for wild fish assemblages. This aggregation has noticeable ecological consequences in cage areas in impoverished ecosystems such as those in the Canary archipelago (NE Atlantic Ocean). However, this new habitat could be dominated by a single species, reducing its positive ecological effects. Wild fish assemblages associated with an off-shore fish lease on the northeastern coast of Tenerife (Canary Islands) were sampled for six years. Fish assemblage structure beneath fish cages and at controls (>500 m from cages) differed significantly between locations, with 13 times greater abundance at cage locations. These differences were mainly explained by the dominance of bogue (Boops boops) around fish cages. This trend was consistent in the long-term throughout the study period (2004-2009), affecting local fisheries. The presence of fish cages significantly altered wild fish assemblages in the study area, enhancing mainly biomass and abundance of one species, bogue, and causing shifts in species composition.