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Effects of temperature on macronutrient selection, metabolic and swimming performance of the Indo-Pacific Damselfish (Abudefduf vaigiensis)

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Temperature fluctuations have caused considerable biological and ecological impacts on marine organisms and their communities. For example, increased temperatures in sub-tropical environments have led to the influx of tropical “vagrant” marine species into cooler temperate waters in a phenomenon called ‘tropicalisation’. Here we combine metabolic performance metrics, feeding manipulations and nutritional geometry models to examine the influence of temperature on macronutrient selection (energy amounts of protein, lipid and carbohydrates) in the Indo-Pacific damselfish Abudefduf vaigiensis and explore the role of temperature and macronutrient intake on individual performance (active and routine metabolic rate, and burst swim speed). Indo-pacific damselfish fed non-randomly from presented food blocks, showing selection for their macronutrient intake. In our high-temperature treatment we observed a significant increase in the intake of protein and lipid, but not carbohydrate. The fish in our low-temperature treatment had a significantly higher active metabolic rate and burst swim speed compared to our high-temperature treatment. Our findings provide evidence that the vagrant Indo-Pacific Damselfish in Sydney are able to select specific macronutrients in their diets ameliorating the effects on performance when thermally stressed. This work also suggests some underlying level of acclimation to or selection for colder water temperatures in these relatively recently recruited fish. Further studies should benefit from the approach proposed here, to better understand the ecological and evolutionary drivers that influence the survival of tropical species in marginal thermal habitats.
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Marine Biology (2018) 165:178
https://doi.org/10.1007/s00227-018-3435-7
ORIGINAL PAPER
Eects oftemperature onmacronutrient selection, metabolic
andswimming performance oftheIndo‑Pacic Damselsh (Abudefduf
vaigiensis)
ClaireE.Rowe1· WillFigueira1· DavidRaubenheimer1,2· SamanthaM.Solon‑Biet1,2·
GabrielE.Machovsky‑Capuska1,2
Received: 30 January 2018 / Accepted: 12 October 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Temperature fluctuations have caused considerable biological and ecological impacts on marine organisms and their commu-
nities. For example, increased temperatures in sub-tropical environments have led tothe influx of tropical “vagrant” marine
species into cooler temperate waters in a phenomenon called ‘tropicalisation. Here we combine metabolic performance
metrics, feeding manipulations and nutritional geometry models to examine the influence of temperature on macronutri-
ent selection (energy amounts of protein, lipid and carbohydrates) in the Indo-Pacific damselfish Abudefduf vaigiensis and
explore the role of temperature and macronutrient intake on individual performance (active and routine metabolic rate, and
burst swim speed). Indo-pacific damselfish fed non-randomly from presented food blocks, showing selection for their macro-
nutrient intake. In our high-temperature treatment we observed a significant increase in the intake of protein and lipid, but
not carbohydrate. The fish in our low-temperature treatment had a significantly higher active metabolic rate and burst swim
speed compared to our high-temperature treatment. Our findings provide evidence that the vagrant Indo-Pacific Damselfish
in Sydney are able to select specific macronutrients in their diets ameliorating the effects on performance when thermally
stressed. This work also suggests some underlying level of acclimation to or selection for colder water temperatures in these
relatively recently recruited fish. Further studies should benefit from the approach proposed here, to better understand the
ecological and evolutionary drivers that influence the survival of tropical species in marginal thermal habitats.
Introduction
Understanding the impacts of climate change is a central
theme in ecology (Walther etal. 2002). In marine systems,
temperature fluctuations have caused considerable biological
and ecological impacts to organisms and their communities
(Hughes etal. 2003; Karl and Trenberth 2003; Poloczanska
etal. 2013). Thermal conditions can strongly influence the
morphology, physiology, distribution, activity patterns and
evolution of some organisms (Huey and Kingslover 1989).
Strong latitudinal shifts have been observed in a wide range
of species in response to increases in sea surface tempera-
ture (Cheung etal. 2012; Bates etal. 2014). Movements
are thought to be linked to organisms searching for suitable
habitats and optimal physiological conditions to survive
(Perry etal. 2005).
Tropical ectotherms have evolved to be ‘thermal special-
ists’ as a result of thermally stable environments (Tewksbury
etal. 2008; Payne and Smith 2017). Within this group, fish
often live close to their upper thermal limits and are likely
Responsible Editor: K. D. Clements.
Reviewed by Undisclosed experts.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0022 7-018-3435-7) contains
supplementary material, which is available to authorized users.
* Claire E. Rowe
crow8775@uni.sydney.edu.au
* Gabriel E. Machovsky-Capuska
g.machovsky@sydney.edu.au
1 School ofLife andEnvironmental Sciences, The University
ofSydney, Sydney, Australia
2 Charles Perkins Centre, The University ofSydney, Sydney,
Australia
Marine Biology (2018) 165:178
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178 Page 2 of 12
to be most vulnerable to global warming (Rummer etal.
2014). Increases in temperature in sub-tropical environments
have led to considerable influx of tropical marine species
into cooler temperate waters in a phenomenon that has been
called ‘tropicalisation’ (Hughes etal. 2003; Cheung etal.
2012; Vergés etal. 2014). Tropical fish that have settled in
temperate regions are likely to reduce their metabolic rate,
possibly increasing their risk of mortality (Clements and
Raubenheimer 2006). Indeed, winter water temperature is
strongly linked to overwinter survival for a number of com-
mon vagrant tropical species on the east coast of Australia
(Figueira and Booth 2010). However, the requirements for
adapting to an altered environment involve a range of linked
phenotypic traits including physiology, nutrition, morphol-
ogy and life history (Raubenheimer etal. 2012a). There-
fore, understanding how fish interact with their habitats and
their thermal ecology is important to predict how they will
respond to environmental changes.
Temperature and food are vital factors that influence the
ability of an organism to reproduce, grow and succeed in a
novel environment (Feary etal. 2014). Although the effects
of temperature and nutrition on metabolism are often con-
sidered separately (Sánchez-Vázquez etal. 1999), tempera-
ture is well known to alter metabolic rates and influence the
amounts and ratios of macronutrients that an animal needs
(Raubenheimer etal. 2012a; Simpson and Raubenheimer
2012; Clissold etal. 2013). Species, and even individuals
within species, have their own specific nutritional require-
ments that differ according to traits such as growth rate,
mass, sex, age, life-history stage, or reproductive status
(Raubenheimer etal. 2009; Simpson and Raubenheimer
2012). Nutritional geometry has streamlined the complexi-
ties of modeling foods in relation to animal’s performance,
providing a new ecological view of nutrition and a powerful
framework to link thermal and nutritional ecology (Rauben-
heimer etal. 2012b; Schmitz etal. 2016).
Indo-Pacific Damselfish (Abudefduf vaigiensis) are gen-
eralist omnivores, with a diet consisting mainly of pelagic
copepods and a small proportion of benthic algae and sessile
invertebrates (Clarke and Bishop 1948; Evjemo etal. 2003;
Frédérich etal. 2009). A. vaigiensis have evolved features
including bristled individual teeth and protusible gill rak-
ers to improve their swimming efficiency and capture of
zooplankton (Narayani etal. 2015; Aguilar-Medrano and
Barber 2016). They successfully live and reproduce within
tropical and sub-tropical regions of Australia including the
Great Barrier Reef (GBR, Figueira etal. 2009; Figueira and
Booth 2010), and they are also under the influence of the
East Australian Current (EAC) that often transports their
pelagic larvae from tropical to temperate waters of Sydney
(Booth etal. 2007). Although other members of this genus
have been shown to have reasonable tolerance to low tem-
peratures (critical limits below 15°C; Eme and Bennett
2008), survivorship, feeding rate, growth and burst swim-
ming ability of A. vaigiensis were found to be reduced at
winter water temperatures within this region (Figueira etal.
2009). However, rising ocean temperatures within the south-
east coast of Australia were linked to higher A. vaigiensis
survival (Figueira and Booth 2010). Therefore, this species
can provide a powerful model system for testing how spe-
cies arriving in novel habitats adjust their nutritional goals
to changes in environmental conditions in order to survive.
Here we combine metabolic performance metrics, feeding
manipulations and nutritional geometry models to investi-
gate the nutritional ecology of the Indo-Pacific damself-
ish. In particular, we addressed three questions to test the
prediction that this species non-randomly selects specific
macronutrients and adjusts its preference in response to tem-
perature: (i) Does temperature influence energy intake by A.
viagiensis? (ii) Does temperature influence the selection of
protein (P), lipid (L) and carbohydrates (C) by A. vaigiensis?
(iii) Does temperature and macronutrient intake influence
metabolic performance (active and routine metabolic rate,
and burst swim speed) in A. vaigiensis?
Methods
Animal collection andhousing
We collected A. vaigiensis in March 2016 from Long Reef (S
334417, E 1511833) and Freshwater Beach (S 334655,
E 1511740) in Sydney, Australia using hand nets and an
anaesthetic (20% clove oil diluted in 90% ethanol). The aver-
age water temperature was 22°C at the time of collection
and the temperature range for the area is 25°C for summer
down to 16°C in winter. A total of 34 fish were collected
with a mean total length of 42.47 ± 4.22mm and an average
wet mass of 1.07 ± 0.37g. Fish were transported to Sydney
Institute of Marine Sciences, Sydney, Australia and were
individually held in insulation wrapped 14 L plastic aquaria
with a 100-um filtered flow through seawater (~ 1 L/h) from
Sydney Harbour at ambient temperature (~ 22°C). Follow-
ing Figueira etal. (2009), fish were fed daily with fish food
(AquaOne tropical fish food flakes) for 3weeks and provided
with a 15-cmsection of PVC tubing (10cm in diameter) for
shelter. The lighting cycle was set to a 13-h dark: 11-h light
representing the duration of night and day time at the time
of collection.
Diet treatments
After 2 weeks of habituation to the captive environment,
fish were offered foods presented in blocks of agar due to its
well-established characteristics as a binding agent, insoluble
nature and minimal nutritional value (Armisen and Galatas
Marine Biology (2018) 165:178
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Page 3 of 12 178
1987). Each food block contained high-protein (HP), high-
lipid (HL) or high-carbohydrates (HC), but all three were
isocaloric (750 Cal/g), thereby enabling the effects of spe-
cific macronutrients to be established independent of energy
density (Table1). Following Sánchez-Vázquez etal. (1998)
and Solon-Biet (2008), the foods were formulated using egg
white protein and casein (protein sources), dextrin (hydro-
lysed starch as a carbohydrate source) and Cod Liver Oil and
Canola oil (lipid sources). Since each of these ingredients
is almost entirely a single macronutrient, we were able to
manipulate the dietary macronutrient ratios by varying the
concentrations of the three in the diets. The cod liver oil has
been found to increase the performance of other omnivore
species such as the gilthead bream (Sparus aurata) over
plant-based lipid sources (Kalogeropoulos etal. 1992). How-
ever, adding canola oil to the food allows the diet to span
animal and plant food sources, as is appropriate for an omni-
vore. Hydrolysed starch in the form of dextrin is widely used
as a carbohydrate source in aquaculture due to its utilization
efficiency (Lee etal. 2003; Enes etal. 2010). This is similar
to casein, which is commonly used as an amino acid source
in aquaculture (Walton and Wilson 1986). Casein is also
used in aquaculture because it is a good pellet binder when
combined with gelatin, improving the water durability of the
pellets. However, if casein is provided to the fish alone, then
it has the potential to reduce feed intake and reduce growth
rates, which is why it should be combined with another pro-
tein source (Hertrampf and Piedad-Pascual 2012). Egg white
powder is often used as an additional protein source in aqua-
culture due to experiments showing that the presence of anti-
phospholipase A2 in the egg whites, increasing fish growth
(Barry and Yang 2008). These ingredients are widely used
in macronutrient studies involving fish (Adron etal. 1973;
Adranda etal. 2000; Vivas etal. 2006). Food blocks were
replaced every 24h during the feeding portion of each trial
(described below) and the total amount of each block eaten
(hereafter referred to as “intake”) was assessed by change
in block weight over the deployment period. We used pilot
experiments to optimize a procedure for stabilizing the pre-
deployment weight of food blocks. In the final procedure,
blocks were notched (to facilitate the absorption of water)
andsoaked in water at the treatment-specific temperature for
24h prior to each experiment.
Experimental procedures
Fish were randomly assigned into two temperature groups
of 17 fish each, one simulating southern GBR temperatures
(24°C) and the other representing Sydney temperatures
(20°C). A. vaigiensis are thoughtto have a minimum critical
thermal temperature of 15°C (Figueira etal. 2009) and ther-
mal optimum of 28°C (Nakano etal. 2004; Johansen and
Jones 2011), placing our temperature treatments in the mid-
dleof their thermal range. Water temperatures were changed
from the base of 22°C to the target temperature at a rate of
0.25°C every 6h. Each individual fish was exposed to a
series of five different diets offered for fivedays, where feed-
ing manipulations methodology was adapted from Sánchez-
Vázquez etal. (1998) and Solon-Biet (2008). Three blocks of
food were always available adlibitum. Each week we altered
the macronutrient combinations (HC, HL and HP) avail-
able to achieve five different dietary treatments (one uncon-
strained and four constrained). During the unconstrained
treatment fish were free to select a diet from protein (P), lipid
(L) and carbohydrates (C) (hereafter treatment PLC), while
the constrain treatments comprised: (i) only protein (P), (ii)
carbohydrates and lipids (CL), (iii) protein and lipid (PL)
and (iv) protein and carbohydrates (PC) diets. To be consist-
ent with the number of blocks provided, a food block con-
taining only water and agar was used as replacement when
a macronutrient (e.g. C and L) was absent from a treatment.
To avoid a potential “order-effect” the sequence of diets was
randomized amongst the fish. Because it was not logistically
possible to implement all permutations of diet sequence, we
created five ‘streams’, each consisting of a unique sequence
of diet presentations. Fish were given each nutritional treat-
ment for fivedays, with blocks replaced each day. On day six
of each cycle, fish were fasted for 24h prior to performance
tests (described below) which took place on the seventh day.
Following testing the fish were given a recovery day where
they were offered fish flake food. At any time, there were 3–4
fish within each combination of temperature and diet stream.
Performance testing
Following Donelson etal. (2012) and Rodgers etal. (2016),
every sevendays we tested the oxygen consumption as a
proxy for metabolic rate (routine and active) and burst swim
performance of each individual fish. Routine metabolic rate
(MO2Routine) measures respiration rates using a single trace
(30–40min in length) taken at a time after introduction
to the measurement chambers that is adequate for rates to
reach a minus following handling. Following Donelson etal.
Table 1 Components of each of the food block types (mass in g)
High protein High carbo-
hydrate
High lipid Blank
Protein 116 14.8 14.8 0
Carbohydrate 12.8 100 12.8 0
Lipid 13.3 13.3 104 0
Vitamin mix 0.4 0.4 0.4 0
Mineral mix 9.8 9.8 9.8 0
Agar 44 44 44 44
Water 817.9 817.9 817.9 817.9
Marine Biology (2018) 165:178
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(2012), fish were fasted for 24h to remove any effects of
digestion on respiration, before being placed in individual
sealed 220mL opaque-walled chambers with no air. The
lids of the chambers contained an inlet tap connected to a
pump, which moved aerated seawater at the experimental
temperature through the chamber, which then left via an
outlet tap. Chambers were held in a water bath that was set
at the experimental temperature being tested. Fish were
allowed to rest in their chambers with no disturbances for
2h, a period of time which has been shown sufficient to
allow metabolic rates to return to normal following handling
for a number of similar damselfish species (Rummer etal.
2014; Rodgers etal. 2016) as well as for this species in pilot
trials. After 2h, the inlet and outlet tap on the chambers
were closed preventing any water from entering or leaving
the resting chambers. The oxygen consumption rate of the
fish was measured by sampling oxygen concentration in
each chamber every 5min for approximately 35min using
a Witrox 1 Fiber optic Oxygen Meter (Loligo systems).
Oxygen concentration in chambers did not fall below 80%
saturation over this period as per recommended best practice
(Clark etal. 2013). Following this monitoring period, the
inlet and outlet taps were re-opened allowing water to flow
back through the chambers, refreshing the oxygen level. This
combination of trial length and chamber size delivered a
consistent drop in oxygen concentration over time in the test
chambers from which mass-specific oxygen consumption
rates for each fish could be calculated. While this approach
to measuring MO2Rest did allow for the rapid assessment
of a large cohort of fish over a short period of time, which
was necessary for the study design, the use of this static set-
up has potential drawbacks (Clark etal. 2013). However,
issues of erroneous values caused by oxygen stratification in
the chamber have been shown to be minimal for spontane-
ously active species such as that used here (Rodgers etal.
2016) which create some mixing just by the beating of their
fins. An additional benefit of the shorter testing period we
have used is that background activity (which was assessed
here with 2–3 blank chambers in each trial), which can have
increased variability in static respirometry thus affecting
final consumption numbers (Rodgers etal. 2016), was very
nearly zero due to the filtered seawater and short duration
of water residence (~ 35 min) in the chamber before being
replaced by new filtered flow-through water.
To measure the active metabolic rate (MO2Active), fish
were placed in a 320-mL circular swim chamber (85mm
diameter, 80mm high) equipped with a small magnetic
stir bar on the bottom that was separated from the fish by
a mesh screen to create a current inside the chamber via a
magnetic stir plate external to the setup. The chamber was
submerged inside a large glass tank filled with water set at
the experiment temperature and sealed. Following Nilsson
etal. (2009), we adjusted the speed of the magnetic stir bar
so that the fish swam close to its aerobic limit (evidence by
intermittent pectoral and caudal fin swimming). The oxygen
level within the swim chamber was measured continuously
for 5min using the same system described above and this
was used to calculate the mass-specific oxygen consumption
rate over this period. The rate was based on the slope of the
best-fit line to the oxygen-time data and the maximum rate
was identified from a 2-min-long rolling window applied to
the entire data set.
Burst swim speed (BSS) was assessed using a Go-Pro
camera to record the startle response of each individual fish.
The camera was mounted with a top-down view of a white
plastic tray (8cm deep, 45cm long, 50cm tall) filled with
seawater at the experimental temperature. The camera was
set to a narrow field of view, 1080 p resolution and 120
frames per second. Fish were left on a tray for 30s to set-
tle before we started filming. A 45 cm long rod was used
to tap the water behind the fish, eliciting a startle response
causing it to burst forward. This was done three times over
about 30s. The path of an individual fish over each burst
was tracked using the free motion tracking software Kinovea
(v 0.8.15). The video was scaled using a known distance
on the base of the tray and the GoPro field of view dis-
tortion was corrected using calibration from AgiSoft Lens
software (0.4.0). The maximum speed achieved for an indi-
vidual trial was extracted from the time-position points in
MS Excel. Analysis of speed (described below) expressed as
both cms−1 and body length/s gave the same result (due to
similar fish sizes) and thus cm s−1 results are presented here.
Statistical analyses
All analyses were performed in statistical programing envi-
ronment R 3.1.2 (R Development Core Team 2014). Data
were initially tested using Levene’s test for homoscedastic-
ity and Shapiro–Wilk’s test for normality. If any of these
assumptions was violated, natural log transformation was
used when needed. Food and nutritional intake were cor-
rected for fish weight.
Question 1: does temperature inuence energy
intake byA. viagiensis?
In order to assess if there was any effect on consumption
of the order in which treatments were applied, we used a
two-way ANOVA (stream and temperature) to compare calo-
rie intake per body mass (hereafter energy intake) of each
macronutrient across the entire experiment. As there was
no effect of stream or any interaction with temperature (see
Results” section), we pooled across streams for all other
analyses.
The effect of temperature on P versus non-P intake was
then evaluated using one-way ANOVAs (temperature) on the
Marine Biology (2018) 165:178
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Page 5 of 12 178
total consumption of P and non-P in each nutritional treat-
ment separately. Note that in the hypothesis test of whether
temperature influenced macronutrient intake, the dietary
treatments provided a means to simulate variation is nutri-
ent availability, rather than being regarded as experimental
factor in own right. Our analysis, therefore, focused on the
effects of temperature on intake, without including dietary
treatment as a factor in the analysis.
Question 2: does temperature inuence
theselection ofP, L andC byA. vaigiensis?
To test for selectivity in diet choice, a Multivariate analysis
of variance (MANOVA) was used to compare the energy
intake of specific macronutrients consumed from each of
the agar blocks offered in free choice (PLC) and restricted
treatments (P, CL, PC and PL) at low and high temperatures
against a null prediction of random feeding as in Wilder
etal. (2016). The predicted total energy consumed under
a random selection model was determined by dividing the
total amount consumed by a fish by the number of blocks
offered in each choice treatment for each temperature.
We used the right-angled mixture triangle (RMT;
Raubenheimer 2011) as a graphical tool to visualize the
proportional intakes of macronutrients for each of the
dietary treatments at each temperature. These models
enable the proportional contributions of three compo-
nents (in this case the macronutrients) that sum to 100%
to be visualized and compared in a simple two-dimen-
sional plot. We also include an estimate of the natural
diet of A. vaigiensis based on detailed estimates of the
mass contribution of individual prey types consumed by
this species from Frédérich etal. (2009) and estimated
proximate composition from Morris and Hopkins (1983)
and Tabarsa etal. (2012).
Question 3: does temperature andmacronutrient
intake inuence metabolic performance (active
androutine metabolic rate, andburst swim speed)
inA. vaigiensis?
To determine the interactive effect of macronutrient intake
on performance metrics, we used repeated measure gen-
eralised additive models (GAMs) with the mgcv package
of R 3.1.2 (R Development Core Team 2014). For all
GAMS, we analysed the main effects of P, L and C intake
(expressed as Kcal of energy) and their interaction, using
temperature (fixed) and diet treatment (fixed repeated
measures, each fish was subjected to each diet) as factors.
As there was no interaction between diet treatment and
temperature for any macronutrient and there was a signifi-
cant main effect of temperature, we used thin-plate spline
procedures in R (Wood 2006) to generate 2D response
surfaces for low and high temperatures separately. In each
surface, red regions indicate the greatest values for a given
response, with these values decreasing as colours change
to blue. Contour lines within each surface are isolines indi-
cating equal values for each trait along that line. Data are
presented as mean ± standard error.
Results
Question 1: does temperature inuence energy
intake byA. viagiensis?
There was no interaction between stream and temperature
on the P, L and C energy intake (P: F4,26 = 0.50, p = 0.73;
L: F4,25 = 0.27, p = 0.89; C: F4,26 = 0.59, p = 0.67). Stream
also did not have a direct impact on macronutrients intake
(P: F4,26 = 1.59, p = 0.22; L: F4,25 = 2.80, p = 0.06; C:
F4,26 = 0.69, p = 0.08).
On average (± SE), at high temperatures, significantly
more P (21.51 ± 1.76g) and non-P (23.25 ± 1.75g) were
consumed than at low temperatures (P: 11.81 ± 0.94g
and non-P: 15.84 ± 1.43g). (P: F1,26 = 20.46, p < 0.01,
non-P: F1,26 = 6.39, p < 0.01). On a metabolizable energy
basis, fish at high temperatures had significantly higher
intakes (45.62 ± 2.78 Cal/g) than their conspecifics at low
temperatures (25.25 ± 2.99 Cal/g, F1,26 = 29.06, p < 0.01)
(Fig.1).
0
10
20
30
40
50
60
Lo
wH
igh
Mean Total Intake (Cal/g)
Temperature
Fig. 1 The mean overall total energy intake (Cal/g) consumed by
damselfish at high (24°C) and low (20°C) temperatures. Error Bars
are ± 2 SE
Marine Biology (2018) 165:178
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178 Page 6 of 12
Question 2: does temperature inuence
theselection ofP, L andC byA. vaigiensis?
The proportional macronutrient intakes by A. vaigiensis in
different diet and temperature treatments are shown in Fig.2,
together with the macronutrient composition of the experi-
mental foods and an estimate of the natural diet. A first point
to note is that the fish fed non-randomly from their food
blocks (MANOVAs: PLC: Wilks’ λ = 0.39, F2,26 = 23.10,
p < 0.001, LC: Wilks’ λ = 0.83, F2,26 = 4.52, p < 0.05, PC:
Wilks’ λ = 0.42, F2,26 = 34.74, p < 0.001, PL: Wilks’ λ = 0.60,
F2,27 = 16.10, p < 0.001). This is evident in Fig.2 as the pro-
portions of macronutrients eaten by fish differed from the
null hypothesis that A. vaigiensis consumed equal propor-
tions of foods.
There was considerable spread in macronutrient intake
as a result of the different nutritional treatments and there
was a strong effect of temperature, but it varied depend-
ing on the treatment (Fig.2). Specifically, we observed
that high temperatures significantly increased the pro-
portional energy intake on the different nutritional treat-
ments: P (P: F1,26 = 7.40, p < 0.05, C: F1,26 = 7.40, p < 0.05,
L: F1,26 = 7.40, p < 0.05), PL (P: F1,26 = 19.79, p < 0.001,
C: F1,26 = 18.61, p < 0.01, L: F1,26 = 4.9, p < 0.05) and
PC (P: F1,26 = 11.73, p < 0.005, C: F1,26 = 2.14, p = 0.16,
L: F1,26 = 9.79, p < 0.05). However, temperature did not
influence energy intake in PLC (P: F1,26 = 3.64, p = 0.07,
C: F1,26 = 2.42, p = 0.13, L: F1,26 = 3.29, p = 0.08) and
CL (P: F1,26 = 3.55, p = 0.72, C: F1,26 = 2.24, p = 0.15, L:
F1,26 = 2.74, p = 0.11).
Question 3: does temperature andmacronutrient
intake inuence metabolic performance (active
androutine metabolic rate, andburst swim speed)
inA. vaigiensis?
When exposed to the low-temperature treatment, fish
showed significantly higher MO2Active (low temperature
Fig. 2 Right-angled mixture triangle showing foraging choices of
damselfish. Each diet represents a proportional mixture of protein (P),
lipid (L) and carbohydrate (C) (by energy). To geometrically define
diets in an RMT, % P is plotted against % L. Considering that the
three macronutrients in the mixture sum to 100%, plotting % P (first
axis) and % L (second axis) will automatically reflect the value of %
C in the third axis (Raubenheimer 2011). Diets are presented as mean
SE) for each free choice (PLC) and restricted treatments (CL, PC
and PL) and compared with a null hypothesis that damselfish con-
sume equal proportions of foods (solid black) at low (hollow black)
and high temperatures (solid grey). We also included in the RMT
the 98% energetic dietary intake (black square with white cross) of
A. vaigiensis in the wild (estimated from Frédérich etal. 2009). The
grey dotted lines given by the slope of the radial that connects the
point to the origin represent the P:L ratios of the highest and lowest
P:L treatments offered
Marine Biology (2018) 165:178
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Page 7 of 12 178
n = 14 = 0.01295 ± 0.002mgO2/g/min and high tem-
perature n = 14: 0.01179 ± 0.0003 mg O2/g/min, GAM,
p < 0.05), and BSS (low: 155.64 ± 3.23cm/s and high:
126.14 ± 2.80 cm/s, GAM, p < 0.001). No signifi-
cant differences between temperature treatments were
observed for MO2Routine (low: 0.0015 ± 0.0001mg O2/g/
min and high: 0.0015 ± 0.0001 mg O2/g/min, GAM,
p = 0.12). There was no significant difference in fish
mass, low-temperature fish mass = 1.09 ± 0.09 g,
high temp = 1.06 ± 0.08 g and overall = 1.08 ± 0.06 g
(F1,26 = 4.24, p = 0.80) at the end of the experiment.
Although MO2Routine showed a general pattern of
decreasing with increasing P or L intake, being highest
at low to moderate levels of C intake at both tempera-
tures (Fig.3), the inverse relationship with intake of P
(p = 0.04) and the interactive effect of L and C at low tem-
peratures were significant (Table2). For MO2Active there
was a significant interactive effect of P and C intake at
low temperatures, whereas no differences were observed
at high temperatures (Table3 and Fig.4). No signifi-
cant interactions between macronutrients and BSS were
observed at either temperature (see Supplementary infor-
mation Fig. S1 and TableS1).
Fig. 3 Response surfaces of low- and high-temperature-treated fish
showing the relationship between macronutrient intakes and routine
metabolic rate (mg O2/g/min). Points on the surface indicate indi-
vidual fish. For all surfaces, red regions indicate highest values and
decrease as the colours shift to blue. Contour lines within each sur-
face are isolines indicating equal values for each trait along that line.
Data is presented as mean ± standard error
Table 2 Coefficients of the generalised additive model testing the
main effects of protein (P), lipids (L) and carbohydrates (C) and their
interactive effects on routine metabolic rate under low and high tem-
peratures
Significant differences (p ≤ 0.05) marked in bold
Routine metabolic rate
edf df F P
Low temperature
P 1.36E+00 8 0.58 0.04
C 8.03E−05 8 0.00 0.94
L 3.44E−05 8 0.00 0.57
P × C 2.28E−06 3 0.00 0.43
P × L 2.04E−05 3 0.00 0.48
L × C 1.15E+00 3 1.20 0.05
P × C × L 6.41E−05 7 0.00 0.85
High temperature
P 4.75E−04 8 0.00 0.33
C 1.29E−04 8 0.00 0.94
L 9.87E−05 8 0.00 0.41
P × C 5.86E−05 3 0.00 0.61
P × L 1.82E+00 3 2.53 0.01
L × C 5.02E−05 3 0.00 0.77
P × C × L 8.30E−05 7 0.00 0.43
Marine Biology (2018) 165:178
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178 Page 8 of 12
Discussion
With global change likely to increase the incidence of tropi-
calisation, it is important to explore how marine organisms,
in particular fish, respond to environmental conditions they
have not encountered previously. Some progress has been
made towards understanding the relationship between tem-
perature and metabolism of ectotherms (Angilletta etal.
2002; Angilletta 2009; Miller etal. 2009), in particular spe-
cifically tropical vagrants (Eme and Bennett 2008; Figueira
etal. 2009; Johansen and Jones 2011; Norin etal. 2016).
However, the nutritional processes that underpin this critical
survival role have received comparatively little attention.
Our study is the first to combine nutritional and thermal
ecology to evaluate mechanisms underlying range expansion
of marine fish.
We observed that vagrant A. vaigiensis decrease their
energy intake by consuming less P and non-P energy in the
low-temperature treatment (Fig.1). This supports studies
that have examined decreases in the feeding rates of A. vai-
giensis with decreases in temperature despite an abundance
of food sources (Eme and Bennett 2008; Figueira etal.
2009). However, A. vaigiensis did feed non-randomly, sug-
gesting active selection of the dietary macronutrient bal-
ance composition. We observed a tendency to adjust the
Table 3 Coefficients of the generalised additive model testing the
main effects of protein (P), lipids (L) and carbohydrates (C) and their
interactive effects on active metabolic rate under low and high tem-
peratures
Significant differences (p ≤ 0.05) marked in bold
Active metabolic rate
edf df F P
Low temperature
P 4.36E−05 8 0.00 0.73
C 2.47E−05 8 0.00 0.49
L 5.18E−01 8 0.13 0.15
P × C 1.46E+00 3 1.60 0.04
P × L 9.31E−05 3 0.00 0.57
L × C 2.62E−05 3 0.00 0.71
P × C × L 2.18E−05 7 0.00 0.97
High temperature
P 7.05E−05 8 0.00 1.00
C 5.47E−01 8 0.11 0.20
L 6.80E−05 8 0.00 0.70
P × C 1.60E−05 3 0.00 0.80
P × L 1.86E−05 3 0.00 0.69
L × C 8.57E−01 3 0.48 0.18
P × C × L 1.36E−05 7 0.00 0.99
Fig. 4 Response surfaces of low- and high-temperature-treated fish
showing the relationship between macronutrient intakes and active
metabolic rate. Points on the surface indicate individual fish. For all
surfaces, red regions indicate highest values and decrease as the col-
ours shift to blue. Contour lines within each surface are isolines indi-
cating equal values for each trait along that line. Data are presented as
mean ± standard error
Marine Biology (2018) 165:178
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Page 9 of 12 178
macronutrient intake closer to their natural diet, especially
by increasing protein consumption in the high-temperature
treatment (Fig.2). Interestingly, the performance of fish
was greater for all metrics in the low-temperature treatment
but did not seem to be strongly influenced by diet composi-
tion. This could be a result of fish using selective feeding to
control their macronutrient intake when offered restricted
dietary treatments of only two foods (e.g. CL), allowing
them to reach their target energy intake and maintaining
their metabolic rate and swimming performance.
Such nutrient-specific diet selection is consistent with the
ecology of marine organisms, which forage in nutritionally
complex and fluctuating marine environments that vary spa-
tially and temporally (Tait etal. 2014; Machovsky-Capuska
etal. 2016a, 2018). Our results are consistent with previ-
ous findings on macronutrient self-selection in fish species
including goldfish (Carassius auratus, Sánchez-Vázquez
etal. 1998), rainbow trout (Oncorhynchus mykiss, Sánchez-
Vázquez etal. 1999), common carp (Cyprinus carpio, Yama-
moto etal. 2001, 2003), sea-bass (Dicentrarchus labrax,
Rubio etal. 2003) and black bream (Girella tricuspidata,
Raubenheimer etal. 2005). Information on self-selected
nutrient intake and the consequences of restricted diets ver-
sus free choice is important for understanding how animals
cope with temporal and spatial variation in food abundance
and nutrient content (Wilder etal. 2016).
In ectotherms, fluctuations in environmental tempera-
tures can influence an organism’s feeding rate and nutri-
tional goals (Sánchez-Vázquez etal. 1998, 1999; Simpson
and Raubenheimer 2001). Environmental stressors, includ-
ing increased temperatures, are likely to lead individuals
to switch their growth strategy to fulfil energy demanding
maintenance functions to survive (Hawlena and Schmitz
2010). At 24°C A. vaigiensis consumed greater amounts
of protein and lipid that play a vital role in essential body
functions and supply their energy requirements (Clements
and Raubenheimer 2006; Raubenheimer etal. 2012a). Fish
are known to adjust differently their macronutrient intake in
response to changing temperatures (Clements and Rauben-
heimer 2006; Schmitz etal. 2016). Similar results were
found in the common carp, which also increased their pro-
tein intake with temperature (Yamamoto etal. 2003).
Organisms can cope with adverse environmental condi-
tions through acclimation that often involves behavioural,
physiological and metabolic adjustments in relation to
changes in their environment (Angilletta etal. 2002; Ang-
illetta 2009). Tropical species often experience relatively
small temperature fluctuations that likely influence their
ability to acclimate in a wide range of temperatures (Donel-
son etal. 2012). The temperature range evaluated here would
be expected to be below the thermal optima for this species,
whose native range would extend, at most, into the warm
sub-tropical environments of northern New South Wales
(30°2S, 153°17E). As such, we expected to see a decrease
in performance metrics at 20°C, but instead we found quite
consistently, across all metrics, the opposite. Due to the fish
in both temperature treatments having a similar growth rate
through the experiment, and fish mass being accounted for
in the oxygen-consumption calculation, this pattern suggests
that this population had a thermal optimum that was less
than our high temperature of 24°C. If so, this value would
be quite low considering previous studies which suggest
optimal rates around 28°C (Nakano etal. 2004; Johansen
and Jones 2011). Two plausible non-exclusive explanations
could play a critical role into the range expansion of the
fish into temperate habitats. First, there may exist geneti-
cally based variation in the thermal optima across the lati-
tudinal range of the species (Huey and Stevenson 1979).
Second, there is the potential for acclimation to the local
temperatures over the period between settlement and cap-
ture (2–3months based on fish size). It is not possible to
explicitly exclude either of these as mechanisms when
explaining the observed pattern of elevated performance in
our low-temperature fish. However, adaptation to the local
environment would require some level of retainment of any
local produced larvae. While reproduction of this species is
known to occur in the Solitary Islands to the north (Figueira
and Booth 2010), it has not been observed amongst the low
number of overwinter survivors within the Sydney region.
Given this, on balance of evidence, it is more likely that
some level of local, plastic acclimation has occurred during
larval transport and/or after settlement for the fish studied
here.
Improving our understanding of how macronutrient
intake influences metabolism may shed light on the perfor-
mance of fish when confronted with environmental fluctua-
tions. Metabolic processes rely upon fish obtaining adequate
supplies of certain essential nutrients that cannot be synthe-
sised de novo and must be present in the diet (Shimeno etal.
1995). Under low temperatures, MO2Routine was influenced
by the restricted diets of protein alone, and the combina-
tion of lipid and carbohydrates, whereas the combination of
protein and carbohydrates influenced MO2Active. Individuals
in the present study were fed adlibitum and could, there-
fore, obtain sufficient energy to maintain their activity lev-
els. In juveniles, as in the present study, protein intake has
been linked to growth and metabolic rates (Cowey 2013).
However, when protein is limited, individuals are likely to
overconsume lipid and carbohydrate, to secure their protein
ingestion levels and maintain bodily functions (Simpson and
Raubenheimer 2012). This would be especially important in
novel ecosystems where the fish would require a balanced
high-protein diet to maintain their metabolic rate and bodily
functions.
The technique used to estimate low activity levels of oxy-
gen consumption is not directly comparable to MO2Resting
Marine Biology (2018) 165:178
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178 Page 10 of 12
as measured with intermittent flow techniques and thus we
have termed it MO2Routine. While there is no indication that
this technique delivers biased results for the type of spon-
taneously active fish used here (Rodgers etal. 2016), it is
possible that samples may have higher variation as they are
based off a single trace rather than the average of many taken
over 24h. We feel it unlikely that any elevated variation is
responsible for the lack of difference in MO2Routine between
temperatures as the means of the two groups are nearly iden-
tical. Rather we would suggest that the effect of temperature
across the range explored here is simply most pronounced
for high-activity performance such as MO2Active and burst
swimming with effects in low oxygen consumption situa-
tions being minimal. If this trend were to continue we might
expect we would also not see differences in true MO2Resting,
though further testing would be required to confirm this.
To better understand the nutritional requirements of spe-
cies and predict their response to environmental changes
(Machovsky-Capuska etal. 2016b, 2018), we combined
nutritional geometry and metabolic performance. Our find-
ings provide evidence that the A. vaigiensis adjust their
energy intake and select specific macronutrients in their
diets thereby reducing the effects of important environmen-
tal conditions such as thermal variation on critical metrics of
performance when stressed. This work could be the stepping
stone to further explore the likelihood of this species’ abil-
ity to acclimate to temperate waters in the very early stages
of establishment. This could have further implications on
understanding the potential range of expansion of species
under similar ecological constraints. Further studies should
benefit from the proposed approach, to better understand
the ecological and evolutionary drivers that influence the
process of tropicalisation.
Compliance with ethical standards
Conflict of interest The authors declare no conflict of interest.
Ethical approval All applicable international, national and/or institu-
tional guidelines for the care and use of animals were followed. All
procedures performed in studies involving animals were in accordance
with the ethical standards of the University of Sydney Animal Ethics
Committee. This study was conducted under the University of Sydney
Animal Ethics Committee. Project number: 2016/961. This is contri-
bution number 234 to the Sydney Institute of Marine Science.SMS-B
is supported by a NHMRC Early Career Fellowship (1110098) and a
University of Sydney SOAR Fellowship.
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... The application of RMTs is shown in a recent example. To understand the nutritional requirements of species and predict their response to environmental changes, Rowe et al. (2018) combined nutritional geometry and metabolic performance. The authors provide evidence that the Indo-Pacific damselfishes (Abudefduf vaigiensis) adjust their energy intake and select specific macronutrients in their diets, thereby reducing the effects of important environmental conditions such as thermal variation on critical metrics of performance when stressed. ...
... Diets are presented as mean (AE SE) for each free choice (PLC) and restricted treatments (CL, PC, and PL) and compared with a null hypothesis that damselfish consume equal proportions of foods (solid black) at low (hollow black) and high temperatures (solid grey). Rowe et al. (2018) also included in the RMT the 98% energetic dietary intake (black square with white cross) of A. vaigiensis in the wild (estimated from Frédérich et al. (2009)). The grey dotted lines given by the slope of the radial that connects the point to the origin represent the P:L ratios of the highest and lowest P:L treatments offered. ...
Chapter
Proteins represent the dominant biomass of aquatic animals; consequently, proteins are significant nutrients and energy sources with digestive efficiencies between 60 and almost 100%. For most aquatic animals, the quantity of prey available is typically the nutritional bottleneck. A deficiency of dietary protein or amino acids has long been known to impair immune function and increase the susceptibility of animals to infectious disease. In addition to function as energy source, free amino acids can act as osmolytes. The average dietary protein requirement of fishes is 42%; that of invertebrates appears to be below this value. Protein requirement depends on environmental factors, such as salinity and temperature, as well as trophic level and content of the other macronutrients. Interactions with other macronutrients, however, are not yet adequately considered. Adverse effects occur in animals fed deficient or excess proteinaceous diets. Biomolecular modes of action of hyperproteic diets are beginning to be understood; impairment of the immune system is central. Finally, this chapter points out gaps of protein nutrition in aquatic animals.
... phosphofructokinase; McDonald et al., 1998) and more highly correlated with sprint speed. Sprint speed has been examined in one other diet×temperature study in fishes, which measured macronutrient selection and temperature effects on damselfish (Rowe et al., 2018). Macronutrient selection did not change with temperature, but sprint speed was highest in the colder temperature treatment (Rowe et al., 2018). ...
... Sprint speed has been examined in one other diet×temperature study in fishes, which measured macronutrient selection and temperature effects on damselfish (Rowe et al., 2018). Macronutrient selection did not change with temperature, but sprint speed was highest in the colder temperature treatment (Rowe et al., 2018). Fish use two different swimming modes: anaerobically powered burst swimming and sustained aerobically powered swimming. ...
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Thermal acclimation is a key process enabling ectotherms to cope with temperature change. To undergo a successful acclimation response, ectotherms require energy and nutritional building blocks obtained from their diet. However, diet is often overlooked as a factor that can alter acclimation responses. Using a temperate omnivorous fish, opaleye (Girella nigricans), as a model system, we tested the hypotheses that 1) diet can impact the magnitude of thermal acclimation responses and 2) traits vary in their sensitivity to both temperature acclimation and diet. We fed opaleye a simple omnivorous diet (ad libitum Artemia sp. and Ulva sp.) or a carnivorous diet (ad libitum Artemia sp.) at two ecologically relevant temperatures (12 and 20°C) and measured a suite of whole animal (growth, sprint speed, metabolism), organ (cardiac thermal tolerance), and cellular-level traits (oxidative stress, glycolytic capacity). When opaleye were offered two diet options compared to one, they had reduced cardiovascular thermal performance and higher standard metabolic rate under conditions representative of the maximal seasonal temperature the population experiences (20°C). Further, sprint speed and absolute aerobic scope were insensitive to diet and temperature, while growth was highly sensitive to temperature but not diet, and standard metabolic rate and maximum heart rate were sensitive to both diet and temperature. Our results reveal that diet influences thermal performance in trait-specific ways, which could create diet trade-offs for generalist ectotherms living in thermally variable environments. Ectotherms that alter their diet may be able to regulate their performance at different environmental temperatures.
... Proportions-based NGF models were developed to overcome the logistical constrains of field-based research, enabling a graphical representation of the relationships among nutrients, prey, meals and diets (Raubenheimer, 2011). Laboratory and field-based studies using NGF in terrestrial (Hewson-Hughes et al., 2013;Erlenbach et al., 2014;Felton et al., 2016;Coogan et al., 2017) and marine systems (Raubenheimer et al., 2005;Ruohonen et al., 2007;Rowe et al., 2018) have since provided consistent evidence that food selection is likely driven by specific mixtures of nutrients, rather than energy per se. ...
... Interestingly, nonetheless, South African pilchard and eastern Australian salmon (important prey of white sharks in each region) had similar proximate compositions, high in lipid and protein. While lipid content is a key determinant of overall prey energy density, which is often the metric by which prey 'quality' is judged (Spitz et al., 2010a,b), many recent studies in a range of organisms (herbivores, omnivores and carnivores) suggest that food preferences are driven by specific macronutrient content and balance, rather than simply overall energy content (Hewson-Hughes et al., 2013;Erlenbach et al., 2014;Felton et al., 2016;Coogan et al., 2017;Rowe et al., 2018). The specific mixture of macronutrients required depends on the physiological, functional and life history attributes of an animal such that optimal foraging may be achieved by regulating multiple nutrients simultaneously, not just maximising net energy gain (Simpson et al., 2004). ...
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Establishing diets and dietary generalism in marine top predators is critical for understanding their ecological roles and responses to environmental fluctuations. Nutrition plays a key mediatory role in species-environment interactions, yet descriptions of marine predators’ diets are usually limited to the combinations of prey species consumed. Here we combined stomach contents analysis (n = 40), literature prey nutritional data and a multidimensional nutritional niche framework to establish the diet and niche breadths of white sharks (Carcharodon carcharias; mean ± SD precaudal length = 187.9 ± 46.4 cm, range = 123.8–369.0 cm) caught incidentally off New South Wales (NSW), Australia. Our nutritional framework also facilitated the incorporation of existing literature diet information for South African white sharks to further evaluate nutritional niches across populations and sizes. Although teleosts including pelagic eastern Australian salmon (Arripis trutta) were the predominant prey for juvenile white sharks in NSW, the diversity of benthic and reef-associated species and batoids suggests regular benthic foraging. Despite a small sample size (n = 18 and 19 males and females, respectively), there was evidence of increased batoid consumption by males relative to females, and a potential size-based increase in shark and mammal prey consumption, corroborating established ontogenetic increases in trophic level documented elsewhere for white sharks. Estimated nutritional intakes and niche breadths did not differ among sexes. Niche breadths were also similar between juvenile white sharks from Australia and South Africa. An increase in nutritional niche breadth with shark size was detected, associated with lipid consumption, which we suggest may relate to shifting nutritional goals linked with expanding migratory ranges.
... Aquatic organisms, particularly ectotherms, function optimally within specific temperature ranges, varying amongst taxa, populations, life stages, and with age (Pörtner and Farrell, 2008;Schulte et al., 2011). Organisms respond to temperature changes by decreasing or increasing their metabolic rate to maintain performance (Schulte, 2015;Rowe et al., 2018), a phenomena which has been recorded in common jellyfish species, such as Aurelia aurita (Linnaeus) (Møller and Riisgård, 2007). However, adjusting metabolic rate is not the only way jellyfish can respond to changes in temperature. ...
Article
Upside-down jellyfish (Cassiopea spp.) are predominantly tropical, but there have been recent reports of medusae in temperate environments. In 2017 they were recorded in temperate Lake Macquarie, Australia, where they have a tendency to disappear from this area through late winter (Austral, August). This raises questions about the role of temperature as a controlling factor of their abundance, and future density increases with warming oceans as a result of climate change. Here we test the degree to which temperature may drive winter die-offs of the medusa stage in temperate environments, and how this may change with altered thermal regimes. We assessed the physiological response of Cassiopea (via measurement of bell pulsation rate, bell diameter, and routine metabolic rate) under a regime mirroring Lake Macquarie's seasonal temperature drop (autumn into winter) compared to three other temperature profiles: 1) seasonal profile with predicted climate change (+ 2 °C), 2) stable temperatures equivalent to the end of autumn (20 °C) and, 3) a profile that mimicked the increasing temperatures from winter into summer (20 °C increasing to 24 °C). Overall, the results indicate that, compared to the ambient state, elevated temperatures can have positive effects on performance of Cassiopea medusae as evidenced by greater bell pulsation rate and bell diameter. The rate of bell diameter decline was lower in all elevated temperature treatments relative to the ambient profile. This highlights the capacity for elevated temperatures in the future to slow the rate of bell degradation, contributing to an increased probability of overwinter survival, thus increasing the size and duration of Cassiopea blooms in temperate waterways such as Lake Macquarie.
... As long as fishes are given the chance to discriminate between different single macronutrients, dietary adjustments can be made on the basis of post-ingestional cues even in the absence of oral stimuli (Raubenheimer et al. (2012) and references therein). Later, this laboratory confirmed an active selection of the dietary macronutrient balance composition in the Indo-Pacific damselfish (Abudefduf vaigiensis) suggesting the generalizability of this property (Rowe et al. 2018). 1 Fig. 3.2 Self-selection of macronutrient diets in fish. The percentage of energy taken in as carbohydrate (carbo), lipid, and protein by Senegalese sole (Solea senegalensis) and goldfish (Carassius auratus) using self-feeders delivering these three macronutrients in pure form. ...
Chapter
This chapter focuses on the utilization of proteinaceous nutrients in various aquatic animals. In invertebrates, carnivores tend to have the highest and herbivores the lowest protease content and activity. In many fishes, the capability of self-selection of the appropriate diet in terms of quality and quantity can be observed. In a brief inventory, it is shown that most fishes match the hypothesis that the ontogeny of the digestive system is a genetically programmed process where digestive enzymes follow a spatiotemporal pattern of gene transcription during larval development. So far, it appears that only in a few species, the digestive enzymes are translationally regulated. During early fish ontogeny, AAs are important fuel molecules, signaling factors, and major substrates for the synthesis of a wide range of bioactive molecules and proteins. Consequently, feeding protocols based on different proteinaceous sources and preparations are increasingly developed for farmed fishes. Dietary protein formulation of microdiets should be adapted to each developmental stage. Dietary protein excess might have adverse effects. Finally, this chapter points out knowledge gaps of protein utilization by aquatic animals.
... Acute oxygen consumption rate (ṀO 2 ) was measured using 24 Neon tetras and 23 Black Neon tetras (e.g., Eme et al., 2009b;Rowe et al., 2018;Rangel and Johnson, 2018;Scheffler et al., 2019). Our protocol was specifically interested in measuring acute oxygen consumption rates; it is important to note that our protocol does not account for handling stress, but that all fish were treated similarly at all measurement temperatures. ...
Article
Temperature is a primary factor affecting species' ability to thrive in a particular ecological niche, but thermal conditions have changed dramatically in recent decades. Fishes shift their thermal tolerance range with a maximum and minimum temperature correlated to their recent thermal acclimation history, and species can show a reduced temperature quotient (Q10) following chronic thermal acclimation. Neon tetra (Paracheirodon innesi) and Black Neon tetra (Hyphessobrycon herbertaxelrodi) are popular hobbyist aquarium fishes, and both species are examples of freshwater teleosts native to South American river systems that are potentially affected by changing thermal conditions. We acclimated these species to three different constant temperatures (26 °C, 29 °C, and 31 °C) for 15.4 ± 2.1 days, then measured acute critical thermal maxima (CTMax) and acute oxygen consumption rate (Ṁo2) at each acclimation temperature. We also estimated chronic lethal thermal maximum (CLT) for both species following a 2-week acclimation to 30.4 °C. Mean CTMax of both species were found to increase with acclimation temperature from 38.5 to 39.6 °C for Neon tetra and from 39.5 to 41.0 °C for Black Neon tetra, gaining 0.24 (Neon tetra) or 0.29 °C (Black Neon tetra) of tolerance per 1 °C of acclimation. However, Black Neon tetra demonstrated consistently higher CTMax (1.0-1.4 °C). CLT was lower for Neon tetra (33.5 °C), compared to Black Neon tetra (35.9 °C). Mean Ṁo2 were statistically similar across acclimation temperatures within species; Q10 between 26-31 °C were 1.92 and 1.22 for Neon and Black Neon tetra, respectively. Neon and Black Neon tetras physiologically acclimated to changing thermal demands, and although they demonstrate robust CTMax responses, CLT responses indicated both species are unable to survive temperatures 4-5 °C above current average natural values. The demonstrated metabolic plasticity and CTMax values provide a moderate cushion for both species to combat changing temperatures due to climate change, but CLT values suggest vulnerability to projected climate trends.
... If, on the contrary, polar cod populations experience high gene flow, combining dietary data with physiological measurements might reveal essential information regarding the importance of seasonal prey selectivity and its impact on polar cod growth and fecundity. Studies have demonstrated that environmental factors can affect metabolic rate, thereby changing a predator's energetic requirements and its feeding strategy(Rowe, Figueira, Raubenheimer, Solon-Biet, & Machovsky-Capuska, 2018).Considering that polar cod population specialization occurs in fall, at a time period when energetic requirements are particularly high(prewinter and prereproduction, Nahrgang et al., 2014), understanding whether polar cod populations should be treated as distinct units or not seems particularly relevant.The Arctic environment is changing rapidly, altering trophic interactions, selection pressures, and community composition(Edwards & Richardson, 2004;Hoegh-Guldberg & Bruno, 2010;Langbehn & Varpe, 2017;Rice, 1995; Varpe, Daase, & Kristiansen, 2013;Zerba & Collins, 1992); and species response to changes induced by climate change will partly depend on their phenotypic plasticity(Munday, Warner, Monro, Pandolfi, & Marshall, 2013;Sih, Ferrari, & Harris, 2011). Studies have previously reported the selective behavior of polar cod on specific prey types ...
Article
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Species with a broad and flexible diet may be at an advantage in a rapidly changing environment such as in today's Arctic ecosystems. Polar cod (Boreogadus saida), an abundant and ecologically important circumpolar Arctic fish, is often described as a zooplankton generalist feeder, which suggests that it may cope successfully with changes in prey composition. This description is justified based on the relatively broad diet of polar cod across sites and seasons. In this case study, we used polar cod dietary data from fall and winter and from two distinct environments, dominated either by Arctic or Atlantic water masses in Svalbard. Our results point to the importance of time and space when drawing conclusions on dietary plasticity and degree of specialization. Polar cod diet differed significantly between fall and the winter and between Arctic and Atlantic domains. Polar cod from Arctic domains displayed a strong realized population specialization on Themisto libellula in fall, and the larger dietary niche width observed in the winter was the product of realized individual specialization, with increased feeding on fish prey. Overall, we did not observe a generalized feeding behavior. If dietary niche width is to inform conservation management, we argue it must be recognized that populations from a single species may adopt seasonally contrasting degrees of dietary specialization and that these populations may differ in their vulnerability to climate‐induced changes in prey community composition. By taking an alternative approach to dietary analysis, this article challenges the commonly held assumption that polar cod is a generalist predator and argues that it can display strong temporal and geographical dietary specialization.
... Recent work in nutritional ecology, including laboratory (Rowe et al. 2018), field (Machovsky-Capuska et al. 2016c, 2018, and theoretical (Kearney et al. 2010;Machovsky-Capuska et al. 2016d, 2019 studies, have demonstrated the potential of moving beyond single currencies such as energy to explicit consideration of nutrient mixtures in order to generate new insights into foraging and its role in structuring populations, communities, and ecosystems , Wilder et al. 2013, Tait et al. 2014). The conceptual and methodological approach around which these studies have been structured, known as the nutritional geometry framework, models nutrition as a multidimensional process . ...
Article
Apex predators play pivotal roles in marine ecosystems, mediated principally through diet and nutrition. Yet, compared with terrestrial animals, the nutritional ecology of marine predators is poorly understood. One reason is that the field has adhered to an approach that evaluates diet principally in terms of energy gain. Studies in terrestrial systems, by contrast, increasingly adopt a multidimensional approach, the nutritional geometry framework, that distinguishes specific nutrients and calories. We provide evidence that a nutritional approach is likewise relevant to marine apex predators, then demonstrate how nutritional geometry can characterize the nutrient and energy content of marine prey. Next, we show how this framework can be used to reconceptualize ecological interactions via the ecological niche concept, and close with a consideration of its application to problems in marine predator research.
Article
Coral reef ecosystems are under increasing anthropogenic pressures making it ever more important to monitor changes in fish communities to implement appropriate management. In contrast to long-term spatial and temporal variation which has been extensively documented, little work has been carried out to identify variability in fish assemblages on short time scales, with few studies testing patterns of fish assemblages between and within days. Here we investigated the diurnal changes in species richness, relative abundance and assemblage composition in a shallow coral reef fish community in Egypt. To do so, a section of coral reef was filmed during the morning (0600 h), midday (1000 and 1400 h) and afternoon (1800 h) over eleven days. Dusk (0600 h) and dawn samples (1800 h) showed higher species richness compared to late morning (1000 h) and mid-day samples (1400 h) and borderline significantly higher numbers of total individuals, likely associated with feeding activity and predator avoidance. Assemblage composition varied across days and time-of-day, showing greater variability during dusk and dawn associated with a transition between day-time and night-time assemblages. Our results have implications for designing coral reef fish surveys, emphasising that short-term changes in fish communities should be considered when designing experiments to monitor fish assemblages over time. Where possible, we suggest increasing replication within sites and time scales or randomising data within a specific time window at all sites, looking to exclude dusk and dawn.
Article
Climate changes due to global warming result in part from the release of gases such as carbon dioxide (CO2) and methane into the atmosphere and results in warming and acidification of water bodies, and changes precipitation and wind patterns, which might in turn affect water currents, turbulence and turbidity. These changes might affect feeding and its endocrine control. Feeding is regulated by central and peripheral hormones that either stimulate (e.g. orexin, ghrelin) or inhibit (e.g. irisin, cocaine and amphetamine regulated transcript - CART, cholecystokinin - CCK and peptide YY -PYY) food intake. In this study we examined the effects of four climate change-related environmental factors (i.e. temperature, pH, turbulence and turbidity) on food intake and the hypothalamic and intestinal expressions of appetite regulators in fish, using goldfish as a model. High temperatures increased food intake and the brain expression of orexin, and decrease brain CART 1 and intestinal CCK, PYY and ghrelin. Low pHs decreased feeding and increased the expressions of CART1 and CART2 in the hypothalamus and CCK and PYY in the intestine. Turbulence (waves) induced an increase in food intake and a decrease in mRNA expression levels of both CART1 and CART2 in the hypothalamus and both CCK and PYY in the intestine. Turbidity (low visibility) did not affect food intake but increased locomotion and the time taken to reach satiation, while increasing brain orexin and intestinal PYY expression levels and lowering CART1 hypothalamic expression. The results of this study suggest that environmental stress affects feeding physiology of goldfish and bring new insights on how fish might respond to climate changes.
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1.Our understanding of the niche concept will remain limited while the quantity and range of different food types eaten remains a dominant proxy for niche breadth, as this does not account for the broad ecological context that governs diet. Linking nutrition, physiology and behaviour are critical to predict the extent to which a species adjusts its nutritional niche breadth at the levels of prey (“prey composition niche”, defined as the range of prey compositions eaten), and diet (“realized nutritional niche” is the range of diets composed through feeding on the prey). 2.Here we studied adult‐chick rearing Australasian gannets (Morus serrator) to propose an integrative approach using sea surface temperature anomalies (SSTa), geographic location and bathymetry over different years, to explore their relationship with the nutritional composition of prey and diets (i.e., prey composition and nutritional niche breadth), habitat use and foraging behavior. 3.We found that gannets feed on prey that varied widely in their nutritional composition (have a broad prey composition niche), and composed diets from these prey that likewise varied in composition (have a broad realized nutritional niche), suggesting generalism at two levels of macronutrient selection. 4.Across seasons, we established “nutritional landscapes” (hereafter nutriscapes), linking the nutritional content of prey (wet mass protein to‐lipid ratio ‐P:L‐) to the most likely geographic area of capture and bathymetry. Nutriscapes varied in their P:L from 6.06 to 15.28, over time, space and bathymetry (0 to 150 m). 5.During warm water events (strong positive SSTa), gannets expanded their foraging habitat, increased their foraging trip duration and consumed prey and diets with low macronutrient content (wet mass proportions of P and L). They were also constrained to the smallest prey composition and realized nutritional niche breadths. 6.Our findings are consistent with previous suggestions that dietary generalism evolves in heterogeneous environments, and provide a framework for understanding the nutritional goals in wild marine predators and how these goals drive ecological interactions and are, in turn, ultimately shaped by environmental fluctuations.
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The foraging challenge for predators is to find and capture food with adequate levels of energy and nutrients. Marine predators require particularly sophisticated foraging strategies that enable them to balance self- and offspring-feeding, and also in many circumstances simultaneously consider the nutritional constraints of their partners. Here we combined the use of dietary analysis, proximate composition and nutritional geometry (right-angled mixture triangle nutritional models) to examine the macronutrient preferences of Australasian gannets (Morus serrator) at Farewell Spit gannetry in New Zealand. Our results showed intra- and inter-specific variation in the protein, lipid and water composition of prey captured by our sample of 111 Australasian gannets. In addition, we observed significant differences in the Australasian gannets’ nutritional niche between seasons. We provide evidence of sex-specific macronutrient foraging strategies in a successful marine predator in the wild. We have shown that in spite of fluctuations in the nutritional composition of foods available to Australasian gannets, males consistently capture prey with higher protein-to-lipid ratios and lower lipid-to-water ratios than females. These results aid to better understand the evolutionary relationship between macronutrient selection and sex-specific traits in wild animals. They also suggest an incentive for these predators to combine individually imbalanced but nutritionally complementary foods to achieve dietary balance, further highlighting the likelihood that prey selection is guided by the balance of macronutrients, rather than energy alone.
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Coral reefs are home to the most diverse fish assemblages on earth. This high diversity has been hypothesized to partially result from fine-scale niche partitioning of resources. Because niche partitioning might be facilitated by phenotypic diversity, analysis of the morphological variation in an evolutionary context can contribute to our understanding of the speciation and diversification of reef fish. Damselfishes (Pomacentridae) are an extremely diverse group of reef fishes, and Abudefduf genus is one of the youngest clades of this family. Abudefduf is basal clade group benthic feeders, feeding on algae, small benthic invertebrates and zooplankton. In contrast, more derived clades feed primarily on zooplankton. In this study, we examine the relation between morphological and ecological variation to determine the main forces driving diversification in Abudefduf. Results support clear ecomorphological segregation among basal and derived clades, indicating evolution from benthic feeders to zooplanktivorous feeders, suggesting that the shift to a new trophic niche was an important event driving diversification in Abudefduf, and also evidenced by the presence of morphological traits that represent specialized adaptations to chase plankton in the water column. Our analysis demonstrates the utility of morphological and ecological studies to understand the diversification process of reef fish.
Article
Ectotherms from higher latitudes can generally perform over broader temperature ranges than tropical ectotherms. This pattern is thought to reflect trends in temperature variability: tropical ectotherms evolve to be ‘thermal specialists’ because their environment is thermally stable. However, the tropics are also hotter, and most physiological rates increase exponentially with temperature. Using a dataset spanning diverse ectotherms, we show that the temperature ranges ectotherms tolerate (the difference between lower and upper critical temperatures, and between optimum and upper critical temperatures) generally represents the same range of equivalent biological rates (e.g. metabolism) for cool and warm adapted species, and regardless of latitude or elevation. This suggests geographical trends in temperature variability may not be the ultimate mechanism underlying latitudinal and elevational trends in thermal tolerance. Rather, we propose that tropical ectotherms can perform over a narrower range of temperatures than species from higher latitudes because the tropics are hotter. http://onlinelibrary.wiley.com/wol1/doi/10.1111/ele.12707/abstract
Article
Many animals consume foods that vary in all 3 macronutrients: carbohydrates, lipid, and protein. Yet most studies of diet regulation only consider pairs of nutrients (protein and carbohydrate or protein and lipid). Diet regulation also extends beyond nutrient and energy intake to include sources of energy expenditure, such as changes in activity level. We used a right-angled mixture triangle design to quantify the 3-dimensional intake target of fat-tailed dunnarts, Sminthopsis crassicaudata, and to test the consequences of free choice for energy intake, weight gain, and activity level relative to a standard maintenance diet. Dunnarts consistently preferred a relatively high-lipid, low-protein, and low-carbohydrate diet in 3 separate feeding experiments. Dunnarts also consumed a higher total energy intake during choice relative to no-choice periods. However, the weight of dunnarts was not consistently higher at the end of choice relative to no-choice periods, which is likely because dunnarts increased their activity level during periods of choice and decreased their activity when on no-choice diets. This shows that increases in the intake of lipid, which is an important component in the diet of dunnarts, does not necessarily lead to increases in weight gain because these animals can adjust energy expenditure to balance their energy budget. These results have important implications for the design of diets for animals in captivity and demonstrate that consideration of both energy intake and expenditure are needed for a more comprehensive and integrative understanding of diet regulation by animals.
Article
Prey at risk of predation may experience stress and respond physiologically by altering their metabolic rates. Theory predicts that such physiological changes should alter prey nutrient demands from N-rich to C-rich macronutrients and shift the balance between maintenance and growth/reproduction. Theory further suggests that for ectotherms, temperature stands to exacerbate this stress. Yet, the interactive effects of predation stress and temperature stress on diet, metabolism, and survival of ectotherms are not well known. This knowledge gap was addressed with a laboratory study in which wild juvenile grasshoppers were collected, assigned to one of three groups, and raised at three different temperatures. All grasshoppers had access to equal quantities of two diets composed of opposite carbohydrate:protein ratios. Half of the individuals in each temperature group were exposed to predation risk cues from spider predators, while the other half were kept in risk free conditions. Grasshoppers consumed more carbohydrates when exposed to predation risk, but consumption favored greater protein intake as temperature increased. Moreover, the difference in carbohydrate intake between risk cue and risk free treatments diminished as temperature increased. Furthermore, variability between individual consumption patterns both within and between treatments decreased markedly as temperature increased, suggesting that higher temperatures promote more consistent individual consumption behaviors. Grasshoppers grew faster and larger as temperature increased, which translated into higher survival rates at higher temperatures. Warmer grasshoppers also did not alter their metabolic rates in response to predation risk cues, in contrast to colder grasshoppers. Digestive efficiency increased with temperature as well, further indicating that lower temperatures were much more stressful than higher temperatures for grasshoppers. The study shows that physiological responses of ectothermic herbivores to predation stress are highly plastic and temperature dependent, with higher temperatures promoting increased protein intake, growth, development, survival, and digestive efficiency relative to colder temperatures. These findings help to reconcile why dietary responses (proportion of protein vs. carbohydrate intake) to predation stress may vary among different prey taxa studied previously. This article is protected by copyright. All rights reserved.
Article
The dietary generalist-specialist distinction plays a pivotal role in theoretical and applied ecology, conservation, invasion biology, and evolution and yet the concept remains poorly characterised. Diets, which are commonly used to define niche breadth, are almost exclusively considered in terms of foods, with little regard for the mixtures of nutrients and other compounds they contain. We use nutritional geometry (NG) to integrate nutrition with food-level approaches to the dietary niche and illustrate the application of our framework in the important context of invasion biology. We use an example that involves a model with four hypothetical nonexclusive scenarios. We additionally show how this approach can provide fresh theoretical insight into the ways nutrition and food choices impact trait evolution and trophic interactions.
Article
In light of an increasing trend in fish biology towards using static respirometry techniques without the inclusion of a mixing mechanism and without accurately accounting for the influence of microbial (background) respiration, this paper quantifies the effect of these approaches on the oxygen consumption rates (ṀO2) measured from juvenile barramundi Lates calcarifer (mean ± s.e. mass = 20·31 ± 0·81 g) and adult spiny chromis damselfish Acanthochromis polyacanthus (22·03 ± 2·53 g). Background respiration changed consistently and in a sigmoidal manner over time in the treatment with a mixing device (inline recirculation pump), whereas attempts to measure background respiration in the non-mixed treatment yielded highly variable estimates of ṀO2 that were probably artefacts due to the lack of water movement over the oxygen sensor during measurement periods. This had clear consequences when accounting for background respiration in the calculations of fish ṀO2. Exclusion of a mixing device caused a significantly lower estimate of ṀO2 in both species and reduced the capacity to detect differences between individuals as well as differences within an individual over time. There was evidence to suggest that the magnitude of these effects was dependent on the spontaneous activity levels of the fish, as the difference between mixed and non-mixed treatments was more pronounced for L. calcarifer (sedentary) than for A. polyacanthus (more spontaneously active). It is clear that respirometry set-ups for sedentary species must contain a mixing device to prevent oxygen stratification inside the respirometer. While more active species may provide a higher level of water mixing during respirometry measurements and theoretically reduce the need for a mixing device, the level of mixing cannot be quantified and may change with diurnal cycles in activity. To ensure consistency across studies without relying on fish activity levels, and to enable accurate assessments of background respiration, it is recommended that all respirometry systems should include an appropriate mixing device.