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Nutritional geometry and macronutrient variation in the diets of gannets: the challenges in marine field studies


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Foraging theory proposes that the nutritional driver of food choice and foraging in carnivores is energy gain. In contrast, recent laboratory experiments have shown that several species of carnivore select prey that provides a diet with a specific balance of macronutrients, rather than the highest energy content. It remains, however, to be determined how nutritionally variable the foods of predators in the wild are, and whether they feed selectively from available prey to balance their diet. Here, we used a geometric method named the right-angled mixture triangle (RMT) for examining nutritional variability in the prey and selected diets of a group of wild carnivores and marine top predators, the gannets (Morus spp.). A prey-level diet analysis was performed on Australasian gannets (M. serrator) from two New Zealand locations, and the macronutrient composition of their chosen prey species was measured. We use RMT to extend the comparison in the compositions of foods and diets from Australasian gannets from Australia as well as Northern gannets (M. bassanus) and Cape gannets (M. capensis). We found nutritional variability at multiple scales: intra- and interspecific variability in the pelagic fish and squid prey themselves; and intra- and interspecific variability in the diets consumed by geographically disparate populations of gannets. This nutritional variability potentially presents these predatory seabirds with both opportunity to select an optimal diet, and constraint if prevented from securing an optimal diet.
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Marine Biology
International Journal on Life in Oceans
and Coastal Waters
ISSN 0025-3162
Volume 161
Number 12
Mar Biol (2014) 161:2791-2801
DOI 10.1007/s00227-014-2544-1
Nutritional geometry and macronutrient
variation in the diets of gannets: the
challenges in marine field studies
Alice H.Tait, David Raubenheimer,
Karen A.Stockin, Monika Merriman &
Gabriel E.Machovsky-Capuska
1 23
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1 3
Mar Biol (2014) 161:2791–2801
DOI 10.1007/s00227-014-2544-1
Nutritional geometry and macronutrient variation in the diets
of gannets: the challenges in marine field studies
Alice H. Tait · David Raubenheimer · Karen A. Stockin ·
Monika Merriman · Gabriel E. Machovsky‑Capuska
Received: 26 March 2014 / Accepted: 12 September 2014 / Published online: 1 October 2014
© Springer-Verlag Berlin Heidelberg 2014
(M. capensis). We found nutritional variability at multiple
scales: intra- and interspecific variability in the pelagic fish
and squid prey themselves; and intra- and interspecific vari-
ability in the diets consumed by geographically disparate
populations of gannets. This nutritional variability poten-
tially presents these predatory seabirds with both opportu-
nity to select an optimal diet, and constraint if prevented
from securing an optimal diet.
It has long been known that herbivores and omnivores
feed on diets that are variable in the ratios of macronutri-
ents (Westoby 1974, 1978) and consequently have evolved
mechanisms for balancing their diet through nutrient-spe-
cific foraging (Chambers et al. 1995; Raubenheimer and
Jones 1996; Rothman et al. 2011). In contrast, it is widely
believed that predators feed on foods that are nutritionally
balanced and therefore have no need to select nutritionally
complementary prey to balance their diet (Westoby 1978;
Stephens and Krebs 1986; Galef 1996; Fryxell and Lund-
berg 1997). Recent studies in the laboratory have shown,
however, that predatory invertebrates (spiders, beetles)
and vertebrates (mink, fish) do feed selectively for prey
that contain specific ratios of macronutrients (Mayntz
et al. 2005, 2009; Raubenheimer et al. 2007; Rubio et al.
2008, 2009). Yet, it remains to be determined how variable
macronutrients in foods of predators in the wild are, and
whether they feed selectively from available prey to bal-
ance their diet (Wilder and Eubanks 2010). This knowledge
is fundamental to our understanding of how ecosystems
work, given the key role that predators play in structuring
ecological communities (Polis et al. 1989; Polis and Holt
1992; Raubenheimer et al. 2007).
Abstract Foraging theory proposes that the nutritional
driver of food choice and foraging in carnivores is energy
gain. In contrast, recent laboratory experiments have shown
that several species of carnivore select prey that provides a
diet with a specific balance of macronutrients, rather than
the highest energy content. It remains, however, to be deter-
mined how nutritionally variable the foods of predators in
the wild are, and whether they feed selectively from avail-
able prey to balance their diet. Here, we used a geometric
method named the right-angled mixture triangle (RMT) for
examining nutritional variability in the prey and selected
diets of a group of wild carnivores and marine top preda-
tors, the gannets (Morus spp.). A prey-level diet analysis
was performed on Australasian gannets (M. serrator) from
two New Zealand locations, and the macronutrient com-
position of their chosen prey species was measured. We
use RMT to extend the comparison in the compositions of
foods and diets from Australasian gannets from Australia as
well as Northern gannets (M. bassanus) and Cape gannets
Communicated by Y. Cherel.
Electronic supplementary material The online version of this
article (doi:10.1007/s00227-014-2544-1) contains supplementary
material, which is available to authorized users.
A. H. Tait · K. A. Stockin · M. Merriman ·
G. E. Machovsky-Capuska
Institute of Natural and Mathematical Sciences,
Massey University, North Shore MSC, Private Bag 102 904,
Auckland, New Zealand
D. Raubenheimer · G. E. Machovsky-Capuska (*)
Faculty of Veterinary Science, The Charles Perkins Centre,
School of Biological Sciences, University of Sydney,
Sydney, Australia
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A factor that has limited objective tests of the variability
of prey composition is the common assumption that asso-
ciates prey quality with the levels in foods of one particu-
lar component, usually energy (Stephens and Krebs 1986).
Several studies have estimated energetic dietary demands
for different seabird species using energy values of prey
(Furness 1978; Ellis 1984; Annett and Pierotti 1999; Wan-
less et al. 2005; Grémillet et al. 2008; Votier et al. 2010;
Machovsky-Capuska et al. 2011a). Recent work involv-
ing herbivores, omnivores and carnivores spanning a wide
range of taxa, both in laboratory and field studies, has dem-
onstrated the importance of evaluating food quality in rela-
tion to the ratios of several nutrients, rather than the lev-
els of any one (Simpson and Raubenheimer 2012). Until
recently, however, studies applying this multidimensional
view of nutrition to ecological questions such as variation
in prey quality have been limited by the lack of a frame-
work for characterising food compositions in multiple
dimensions and relating them to pertinent factors such as
predator identity, geographic location and diet composition.
An approach for this, called the right-angled mixture trian-
gle (RMT), was recommended by Raubenheimer (2011)
(Fig. 1a, b).
Our primary aims in this paper were to apply RMT
in an initial examination of the variability across scales
of the macronutrient composition of prey of a group of
marine top predators, gannets (Morus spp.), and introduce
this approach as a framework for addressing such ques-
tions. Seabirds, including gannets, are known to forage
for patchily distributed foods in foraging trips that can
span hundreds of kilometres over several days (Hamer
et al. 2000; Richoux et al. 2010; Machovsky-Capuska
et al. 2013, 2014). Gannets are highly specialised marine
predators that feed mainly on pelagic fish and squid at the
air–water interface (Robertson 1992; Machovsky-Capuska
et al. 2011b; Schuckard et al. 2012). We were interested in
estimating the macronutrient variability among different
individuals of the same prey species, across different prey
species, across the diets (i.e. combined prey selected by
individual gannets) within and between colonies at differ-
ent degrees of geographic separation and between species
of gannets.
Fig. 1 Right-angled mixture triangles provide a means to plot three
components in 2D graphs. In a each point represents a mixture of
protein (P), lipid (L) and carbohydrate (C). By convention the third,
implicit, variable (in this case carbohydrate) is denoted in square
brackets (Raubenheimer 2011). % P and L increase in the normal
way along the Xaxis and Y-axis, respectively, and the P:L balance of
a mixture is given by the slope of the radial that connects the point
to the origin. % C of a point is determined as the difference between
100 % and the value at which a negative through the point intersects
with the two axes. For example, in a point i contains 60 % P, 20 % L
and 20 % C, with a 3:1 P:C ratio. Point ii has the same % C (20 %),
but a lower P:L (1:3) than i, and point iii contains the same P:L ratio
but higher % C (60 %) than ii. b In this case the third, implicit, vari-
able plotted on the I-axis is 100 (% protein + % lipid). This repre-
sents all components of the diet that effectively dilute macronutrient
concentration (here assuming that carbohydrate content is minimal,
as is the case for many predator diets). Since dilution of macronu-
trients is the inverse of energy concentration, this model integrates
lipid, protein, lipid/protein balance and total energy content in the
diets of gannets. The plot illustrates the fact that if an animal mixes
its intake from two foods (e.g. foods iv, v), the composition of the
diet is constrained to lie somewhere on the line that connects the two
foods (e.g. point x lies on dashed line connecting points iv, v). If its
intake is derived from three foods (e.g. vvii), then the resulting diet
composition is constrained to lie within the triangle connecting these
foods (e.g. point y)
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To achieve this range of scales in our comparison,
we have combined our original data with relevant data
extracted from the literature. In so doing, it became appar-
ent that data are often not collected in a way that facilitates
comparative analyses of diet variability across scales. Our
secondary aim is thus to recommend strategies for data col-
lection that will facilitate data pooling for the analysis of
broad-scale ecological questions concerning food quality.
We show that a range of significant questions in nutritional
ecology can be addressed if appropriate relevant data are
collected for a given system.
Materials and methods
The right-angled mixture triangle
Right-angled mixture triangles enable mixtures of three
components to be graphed in a 2D plot (Fig. 1a, b)
(Raubenheimer 2011). Data are prepared for plotting by
summing the percentages of the three components (e.g. the
macronutrients protein, fat and carbohydrate) in the parent
mixture (e.g. the food) and then expressing each compo-
nent as a percentage of the sum of all three. For example,
if protein (P), lipid (L) and carbohydrate (C) were present
in a food at 10, 20 and 30 % by weight, respectively, then
each would be expressed as follows:
To construct an RMT to display this mixture, % P is
plotted against % L. Because the three nutrients in the mix-
ture sum to 100 %, plotting % P on % L will automatically
result in the point positioning to also reflect the value of %
C. Such plots not only provide a visual representation of a
3D mixture, but also enable various parameters of differ-
ent mixtures to be compared and inter-related (Fig. 1a). A
particularly useful feature of RMTs is their use for mod-
elling meta-mixtures (mixtures of mixtures), for example,
the nutritional composition of diets that result from mixing
multiple foods (Fig. 1b).
Source of data
An examination of the macronutrient variability of the
prey of gannets (or any marine predator) at several scales
involves (1) identifying the foods eaten by individual gan-
nets; (2) collecting representative samples of the prey spe-
cies in the diet over the same temporal and spatial scale as
the gannet diet analysis was conducted; (3) measuring the
macronutrient content of the prey samples using proximate
analysis; (4) examining the data using RMTs; and (5) using
appropriate statistics to test hypotheses of interest. In the
10/60 %
16.7 %;
60 =33.3 %;C=30
60 % =50 %
present study, a complete data set was collected and ana-
lysed for Australasian gannets (M. serrator) from two New
Zealand locations—Hauraki Gulf (HG), North Island and
Farewell Spit (FS), South Island. We also combined pre-
viously published partial data sets to enable a comparison
between colonies within and between other gannet species,
i.e. data on the diet (prey species) consumed by Australa-
sian gannets from Australia, as well as Northern gannets
(M. bassanus) and Cape gannets (M. capensis) from differ-
ent locations were combined with other published data on
the proximate composition of the relevant prey species.
Prey composition of diet
The diet of Australasian gannets was measured using gut
contents of carcasses opportunistically collected from the
waters of HG (36°51S, 174°46E) on the East Coast of the
North Island of New Zealand, and regurgitations collected
from individuals from the FS gannetry (40°33S, 173°02E)
on the West Coast of the South Island of New Zealand. In
HG, carcasses were collected between August 2010 and
January 2011. HG is a shallow (60 m maximum depth),
semi-enclosed body of temperate water (Manighetti and
Carter 1999) that exhibits a high diversity of marine fauna,
including four gannet colonies with an estimated popula-
tion of 7,000 breeding pairs (Nelson 2005). The carcasses
were typically stored frozen and later examined post-
mortem following avian necropsy protocols (Work 2000).
Individual prey items were removed from the oral cavity,
oesophagus and stomach. Prey items that were ingested
ante-mortem were individually weighed to 0.1 g, and stom-
ach contents were washed through a 0.25-mm-mesh sieve
to examine for otoliths and cephalopod beaks (Wingham
1985; Duffy and Jackson 1986). Digestion codes were
assigned to retrieved prey items (following Meynier et al.
2008), and prey species were identified to the lowest pos-
sible taxonomic level using published guides (Paulin et al.
1989). In FS, regurgitations were collected following
Wingham (1985) from individuals in January 2011 during
the chick-rearing period. The FS gannetry in Golden Bay
was established in 1983 with c.75 breeding pairs and is one
of four breeding sites in the South Island (Hawkins 1988).
Since then, the population has increased by an average of
11.5 % per annum, to an estimated at 3,900 pairs in 2011
(Schuckard et al. 2012). Prey items from the regurgitations
were processed as described above for HG samples.
Macronutrient composition of prey
Samples of the prey species found in the diets of gannets
from HG and FS were selected from undigested material
collected from the carcasses and regurgitations. In the HG,
samples of all prey species represented in the diet were
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collected including anchovy (Engraulis australis, n = 5),
jack mackerel (Trachurus novaezelandiae, n = 6), kahawai
(Arripis trutta, n = 5), pilchard (Sardinops neopilchardus,
n = 6), yellow-eye mullet (Aldrichetta forsteri, n = 5) and
arrow squid (Nototodarus spp., n = 5). In FS, samples of
prey species comprising 82.6 % of the mass of the diet
were collected including kahawai (n = 4), pilchard (n = 7)
and arrow squid (n = 3). This enabled us to measure the
proximate composition of 20 out of the 24 regurgitations
(the remaining four regurgitations contained prey species
that were not collected for analysis). All prey samples were
frozen within five hours of collection and stored at 20 °C
until proximate composition analysis.
Prior to analysis, each sample was partially thawed and
weighed to 0.1 g, dried overnight in a convection oven at
60 °C and ground in a coffee grinder. Total nitrogen was
measured by Kjeldahl analysis and crude protein estimated
by multiplying N by a factor of 6.25 (AOAC 981.10, AOAC
2005). Total lipid (ether extract) was measured by the
Mojonnier method (AOAC 954.02). Moisture was meas-
ured by drying the sample in a convection oven at 125 °C
(AOAC 950.46) and combining this moisture loss with ini-
tial loss from the overnight dry down. Ash was measured
by ignition in a furnace at 550 °C (AOAC 920.153).
Data analysis
For each bird, the total weight of prey in the anterior gut
or regurgitation was calculated as the sum of the individual
prey items (Duffy and Jackson 1986) and each prey spe-
cies was assigned a mass percentage (M%), calculated as
the percentage of total prey weight that the species contrib-
uted to the overall diet (Duffy and Jackson 1986; Schuck-
ard et al. 2012). For each location, each prey species was
assigned a numerical abundance percentage (N%) calcu-
lated as the percentage of the total number of prey items
contributed by individuals of a particular species, and a
frequency of occurrence percentage (F%) calculated as the
percentage of birds that had a particular species in their
diet. Data on the proximate composition of prey were ana-
lysed using Kruskal–Wallis and Mann–Whitney U tests to
determine whether there were differences between species
within a location or between locations within a species,
respectively, using SPSS (PASW Statistics 19, IBM Corp.,
Somers, NY, USA). RMTs (Raubenheimer 2011) were
used to explore the relationships among the proportional
content of nutrients in the prey and diets. The nutritional
composition of the prey and diets was examined in terms of
protein (X-axis), lipid (Y-axis) and rest, i.e. 100 (% pro-
tein + % lipid) (I-axis) content, each expressed as a per-
centage of wet weight. This model integrates lipid, protein
and the overall content (the concentration of macronutri-
ents, as represented by I-axis) as opposed to the common
approach of expressing prey composition only by their
caloric content (Raubenheimer 2011).
Reanalysis of published data
To place in broader context our original data collected
from Australasian gannets in HG and FS in New Zea-
land, we also reanalysed published data on the diet of
Australasian gannets from Port Phillip Bay (PPB), Victo-
ria, Australia (Bunce 2001), the diet of Northern gannets
from Funk Island (FI), Newfoundland, Canada (49°45N,
53°11W) (Montevecchi et al. 1984; Garthe et al. 2011) and
Bass Rock (BR), southeast Scotland (Wanless et al. 2005;
Hamer et al. 2007), and the diet of Cape gannets from Mal-
gas Island (MI) (33°03S, 17°55E) on the Western Cape
of South Africa and Bird Island (BI) (33°50S, 26°17E),
on the Eastern Cape of South Africa (Adams et al. 1991;
Pichegru et al. 2007). For each species/location, data
on the prey composition of gannets’ diet and data on the
proximate composition of prey species were necessarily
obtained from different publications, as no one publication
contained both data sets (see Supporting Information S1).
An effort was made to obtain prey proximate composition
data from samples collected at similar spatiotemporal prox-
imity to the study. These data enabled us to calculate the
proximate composition of prey species constituting (as a
percentage of mass) 79 % of the diet of Australasian gan-
nets from PPB, 99.6 and 96.7 % of the diet of Northern
gannets from FI and BR, respectively, and 100 and 83 % of
the diet of Cape gannets from MI and BI, respectively. The
data were plotted on RMTs as described previously for the
New Zealand populations (see Supporting Information S1).
Prey composition of diets
Of the 35 carcasses examined from HG, 30 contained iden-
tifiable prey remains in their anterior gut. The median mass
of prey per carcass was 215.6 g (range 176.2–426.0 g). The
251 individual prey items identified from these 30 samples
included five species of fish and one species of squid, where
71 % of carcasses contained two prey species, 23 % con-
tained one prey species and 6 % contained three prey spe-
cies. Pilchard had the highest frequency of occurrence and
the greatest mass percentage, followed by anchovy, though
anchovy had greater numerical abundance than pilchard
(Table 1). Twenty-four regurgitations were collected from
different individuals from the FS gannetry. The median
mass of prey per regurgitation was 190.0 g (range 100.0–
430.0 g), which equated to an average daily food intake of
9.4 % of body weight (Nelson 2005). The 134 individual
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prey items identified from these 24 samples included seven
species of fish and one species of squid, where 75 % of
regurgitations contained one prey species, 21 % contained
two prey species and 4 % contained three prey species. Pil-
chard had the highest frequency of occurrence, the great-
est mass percentage and numerical abundance. Arrow squid
had the second highest frequency of occurrence and the
second greatest mass percentage, while anchovy had the
second greatest numerical abundance (Table 1).
Macronutrient composition of prey and diets
Within location, prey species collected from HG differed
in their proportion of protein (Kruskal–Wallis, H = 27.39,
df = 5, p < 0.001), lipid (Kruskal–Wallis, H = 26.14,
df = 5, p < 0.001) and rest (Kruskal–Wallis, H = 22.91,
df = 5, p < 0.001), and those collected from FS differed in
their proportion of lipid (Kruskal–Wallis, H = 6.54, df = 5,
p < 0.038). Of the three prey species found in the diet of
both the HG and FS gannet populations whose macronutri-
ent composition was measured, two species showed differ-
ences between locations. Compared to collections from FS,
pilchard collected from HG had lower proportions of pro-
tein (Mann–Whitney, U = 0.01, Z = 3.00, p = 0.003) and
lipid (Mann–Whitney, U = 0.01, Z = 3.00, p = 0.003)
and a higher proportion of rest (Mann–Whitney, U = 0.01,
Z = 3.00, p = 0.003) and kahawai collected from HG had
a higher proportion of lipid (Mann–Whitney, U = 0.00,
Z = 2.44, p = 0.014) and a higher proportion of rest
(Mann–Whitney, U = 0.00, Z = 2.44, p = 0.014). There
was no difference between locations in the macronutrient
composition of arrow squid. RMTs depict these differences
within and between prey species with regard to the balance
of protein to lipid and the level to which these energetic
macronutrients are diluted by other dietary constituents
(rest including moisture, inorganic matter etc.) (Fig. 2a).
The macronutrient composition of gannets’ diets differed
between locations, where gannets from HG had a diet that
contained a lower proportion of protein (Mann–Whitney
U = 29.00, Z = 4.65, p < 0.001) and rest (Mann–Whitney
U = 117.00, Z = 2.55, p < 0.05) but did not differ in the
proportion of lipid (Mann–Whitney U = 204.00, Z = 0.48,
p = 0.633) to the diet of gannets from FS. In plotting the
nutrient space accessible to each gannet population, there was
no overlap between the two spaces implying a lack of oppor-
tunity for the two populations to secure the same balance
of nutrients in their diet (Fig. 2b). The nutrient space acces-
sible to the FS gannets is potentially larger than that shown
(17.4 % of the mass of the diet was not analysed for nutrient
content). However, the entire nutrient content of 20 out of the
24 regurgitations was calculated, so the average composition
of all 24 regurgitations from FS gannets is unlikely to be very
different from that of the 20 regurgitations shown here.
Reanalysis of published data
By combining partial data sets from the literature, we were
able to construct RMTs to investigate differences between
populations within a gannet species in the accessible nutri-
ent space and selected diet, as well as to compare diet
between different gannet species.
For Australasian gannets, we compared our data from the
HG and FS populations in New Zealand with data from the
PPB population in Australia (Fig. 3a). While there was no
overlap between the New Zealand populations in nutrient
space, the nutrient space accessible to the PPB population
overlapped with the HG population. Despite this, the diet
consumed by the PPB population fell outside of the nutrient
space of HG population, comprising a greater proportion of
protein (similar to that of the FS population), a much greater
proportion of lipid and a greater proportion of protein and
lipid combined than either of the New Zealand populations.
For Northern gannets, we compared data from popu-
lations from FI, Canada and BR, Scotland (Fig. 3b). The
nutrient space accessible to each of the two populations
shows an area of overlap, and the average diet consumed by
birds of each population both fall within this area of over-
lap and contain a remarkably similar nutrient balance.
Table 1 Composition of the
diet of the Australasian gannet
as reflected by the analysis of
35 carcasses collected from HG
and 24 regurgitations collected
during the chick-rearing period
at FS, New Zealand
Diet is described by percentage
frequency of occurrence (F%),
mass (M%) and numerical
abundance (N%)
Prey species HG FS
Pilchard 37.3 76.7 37.8 62.1 66.7 84.1
Anchovy 28.1 66.7 56.6 0.8 12.5 5.8
Yellow-eye mullet 15.8 16.7 2.0
Kahawai 12.5 13.3 1.6 8.3 8.3 1.4
Jack mackerel 4.8 6.7 1.6 3.6 4.2 0.7
Arrow squid 1.5 3.3 0.4 12.1 16.7 3.6
Yellowtail kingfish 8.7 12.5 2.2
Barracouta – – – 4.2 4.2 0.7
Garfish – – – 0.3 4.2 1.4
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For Cape gannets, we compared data from MI and BI on
the Western and Eastern Cape of South Africa, respectively
(Fig. 3c). We were unable to separate the nutrient spaces
accessible to these two populations, as their diets con-
sisted of similar prey species and the sites were too close
geographically for differences within prey species between
locations to be identified. However, the composition of the
average diet consumed by the two populations was mark-
edly different with the BI population having a greater pro-
portion of both lipid and protein and lipid combined than
the MI population.
In comparing the diet of different gannet species, we
plotted species as a function of population (location)
because there were differences between populations within
a species. The data suggest that Australasian and Cape
gannets consume diets containing a greater proportion of
protein than Northern gannets, while Australasian gannets
from PPB, Northern gannets and Cape gannets from BI
consume diets containing a greater proportion of lipid than
Australasian gannets from New Zealand or Cape gannets
from MI. Australasian gannets from PPB and Cape gannets
from BI consume diets with a greater proportion of protein
and lipid combined than the other gannets (Fig. 4).
Our study reveals variability in the macronutrient compo-
sition of gannets’ prey on multiple scales. First, we found
nutritional variability among the prey themselves, poten-
tially presenting gannets with both opportunity to select an
optimal diet, and constraint if prevented from securing food
combinations that support an optimal diet. Second, nutri-
tional variability was established among the diets of gannets,
both within and between species. While diversity in nutrient
gain for this top marine predator may reflect differences in
the nutrient requirements of seabirds living in different geo-
graphic locations, there is also evidence to suggest that in
some cases seabirds are prevented from securing an optimal
balance of nutrients, resulting in lower fitness and breeding
success (e.g. Pichegru et al. 2007; Grémillet et al. 2008).
Nutritional variability of gannet prey
It has been suggested that marine prey species can vary in
their macronutrient composition (Lenky et al. 2012). We
found significant differences in the proportion of protein,
lipid and rest in the prey of Australasian gannets at three
Fig. 2 Right-angled mixture triangle showing the composition in
terms of protein, lipid and remaining fresh weight of foods and diets
of Australasian gannets from HG (circles) and FS (triangles), New
Zealand. a Variation in composition of prey items within and across
species. Markers represent individual prey samples, with colour
distinguishing species (grey anchovy, green jack mackerel, purple
kahawai, red pilchard, aqua arrow squid, yellow yellow-eye mullet).
b Variation in the composition of the diets of gannets from HG and
FS. Solid black symbols show the average composition of prey spe-
cies in the diet, and the black polygons show the region of nutrient
space that is accessible to gannets at each site given the composition
of prey. Hollow red markers show the recorded diets of individual
gannets, and solid red markers show the average compositions of the
diets for each site. The prey species shown represent 100 and 82.6 %
of the mass of the recorded diets for HG and FS gannets, respectively.
The negative diagonal represents a total macronutrient content of
26 %—i.e. % protein and % lipid of any point on that line would sum
to 26 % (see Raubenheimer 2011 for the derivation)
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different scales (Fig. 2a). First, we observed differences
between species within a similar geographic location that
could be explained by differences in their trophic lev-
els (Simpson and Raubenheimer 2012). Second, kahawai
from HG and pilchard from FS showed variability between
individuals within locations (kahawai: 3.5–6.6 % lipid,
pilchard: 19.8–22.8 % protein). These results are likely
related to differences in body size, sex or reproductive stage
(Lenky et al. 2012). Third, we found significant geographic
variation within species, including the lipid composition of
pilchards (HG 1.2 %, FS 2.5 % and PPB 9.8 %) that could
be linked to differences in the species’ own diet or in the
latter case (PPB) possible effects of the laboratory methods
used between studies.
In addition to geographic effects, seasonal variation
is likely to influence prey macronutrient composition in
response to changes in productivity or as a function of
reproductive effort or migration patterns (Lenky et al. 2012;
Simpson and Raubenheimer 2012). Prey samples for this
study were collected to ensure an accurate representation
of gannets’ nutrient gain at the time the prey composition
of their diet was studied. Overall, these results highlight the
importance to nutritional ecology studies of analysing spa-
tiotemporal fluctuations in an animal’s diet at both the food
and nutrient levels.
Prey and macronutrient composition of diets
Prey composition of gannets’ diets is believe to reflect the
relative abundance of pelagic fish and squid in their forag-
ing grounds (Jarvis 1970; Wingham 1985; Robertson 1992;
Bunce 2001; Schuckard et al. 2012). In terms of mass,
pilchard was the most important prey species in the gan-
nets’ diet from both New Zealand colonies studied as has
been reported in previous studies (Wingham 1985; Schuck-
ard et al. 2012). Despite similarities in the species of prey
observed in the diets of both colonies, we found a signifi-
cant difference in the macronutrient composition of their
diets between sites (Fig. 2b).
Fig. 3 Right-angled mixture triangles comparing the diet composi-
tions (as a % of wet weight) of a Australasian gannets in New Zea-
land (HG and FS, black polygons) and Australia (PPB, grey poly-
gon). b Northern gannets from FI, Canada (green polygon) and BR,
Scotland (blue polygon) and c Cape gannets on MI, Western Cape
of South Africa (star) and BI, Eastern Cape of South Africa (purple
polygon). Solid-coloured symbols show the average composition of
prey species in the diet, and the coloured polygons show the region of
nutrient space that is accessible to gannets at each site given the com-
position of prey. Red solid symbols show the average compositions
of the diets across gannets at each location. In a, proportion of prey
species represented are HG = 100 %, FS = 82.6 % PPB = 79 %; in
b FI = 99.6 % and BR = 96.7 %; in c MI = 100 % and BI = 83 %
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Gannets from HG consumed a lower proportion of
protein and a lower proportion of lipid and protein com-
bined (i.e. a higher proportion of rest) than their conspe-
cifics from FS. While similar lipid intakes were achieved
between colonies, there is no suggestion as to what level
of protein intake is preferred. Since the nutrient space
accessible to gannets from each location did not overlap,
it is possible that one population was constrained from
securing adequate protein intake which could have fitness
consequences. However, this is perhaps unlikely as the
Australasian gannet population in New Zealand has been
considered to be increasing annually by at least 2.3 % since
1947 (Nelson 2005), suggesting that nutrient requirements
are being met for these seabirds.
It has previously been shown that adult chick-rearing
gannets structure their foraging trips to cover their ener-
getic needs first and those of their offspring second (Rop-
ert-Coudert et al. 2004). The energy required by a gannet
parent to meet their own needs and those of their chick is
equivalent to double that found in an average regurgitation
(Wingham 1989), but it is unknown whether the adults’
nutrient requirements are similar to those of their chick.
This could be an important consideration when analysing
gannet diets from carcasses and regurgitations, in terms
of: (1) whether the adults were rearing chicks; (2) the time
of the last feed, considering that digestion of a complete
fish takes between 2 and 6 h (Davies 1956; Machovsky-
Capuska et al. 2011b); and (iii) whether the diets obtained
represent the adult or the chick’s meal (Richoux et al.
2010). This warrants further investigation.
In the field, there are complex sets of interacting varia-
bles that present several logistical challenges for collecting
reliable daily intake data for nutritional studies. However,
an estimate of the proportional composition of the diet can
be obtained using gut contents analysis (Petry et al. 2007;
Machovsky-Capuska et al. 2011b), regurgitations (Duffy
and Jackson 1986; Schuckard et al. 2012) faecal analy-
sis (Duffy and Jackson 1986; Lea et al. 2002), bite rates
analysis (Paddack et al. 2006), video footage (Machovsky-
Capuska et al. 2011a, 2012), stable isotopes (Cherel et al.
2000, 2005) and when possible a combination of these
techniques. Furthermore, there are other aspects relevant to
the accuracy of the methods use for estimating diet compo-
sition (Duffy and Jackson 1986; Votier et al. 2003). We rec-
ommend combining RMTs’ with pre-existing techniques
to enhance our accurate estimation of dietary intakes in
marine predators.
Interspecific nutritional variability
Do gannets have similar nutrient gains across environ-
ments? We have used published data on the three gannet
species from different populations to illustrate how RMTs
can be used to show how dietary nutrient balance can vary
between populations and that patterns for achieving the
observed nutrient gains differed between populations and
species (Figs. 3a–c, 4).
The diet of the PPB population was higher in lipid and
intermediate in protein compared to the New Zealand pop-
ulations. Although the nutrient space accessible to PPB
overlapped with that of HG, the average diet of PPB did
not fall within this area of overlap. It is possible that PPB
gannets have different nutrient requirements and/or experi-
ence greater fluctuations in prey availability leading them
to select more lipid-rich prey than their conspecifics in
New Zealand (Bunce 2001), though differences in labora-
tory methods for lipid measurement may also have con-
tributed to this finding. Northern gannets from FI and BR
showed a remarkably similar balance of nutrients in their
average diets, which both fell within the area of overlap
in their nutrient spaces. Cape gannets from MI and BI had
the same prey species in their diets thus sharing a region
in nutrient space. However, the diets of BI population were
higher in lipid and protein than their conspecifics from MI.
While gannets from BI consumed high-quality pelagic fish
(mainly sardine, Sardinops sagax and anchovy, Engraulis
encrasicolus), the MI population relied on discarded fish-
eries waste (hake, Merluccius paradoxus) (Pichegru et al.
Fig. 4 Right-angled mixture triangle showing (as a % of wet weight)
the average macronutrient composition of the diet consumed by dif-
ferent populations of Australasian, Northern and Cape gannets.
Marker colour represents gannet species (red Australasian, yellow
Northern, aqua Cape), and marker shape represents population loca-
tion (circle HG, triangle FS, diamond PPB, upside-down triangle FI,
square BR, bowtie MI, oval BI)
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2007). This difference in the macronutrient composition
of the diets related to prey availability and was suggested
to contribute to the decline of the MI population (Pichegru
et al. 2007). An overall comparison of the composition of
diets from the three gannet species showed interspecific
nutritional variability as a function of geographic location.
The lipid intakes of the MI colony and the New Zealand
colonies analysed were relatively similar, despite their
opposite population trends. Life-history responses to nutri-
tional state are likely to play an important role in nutritional
regulation in both species and require further examination.
These results are, however, subject to the caveat that we
were unable to obtain proximate composition values from
the literature that were contemporary and geographically
similar to the dietary studies available for the species stud-
ied. This is likely to influence the shapes of the nutritional
niche landscapes as well as the macronutrient compositions
of the estimated diets.
Macronutrients are, however, clearly not the only func-
tionally important nutritional components of foods: the
constituent molecules in macronutrients (amino acids
and fatty acids, for example) and micronutrients such as
vitamins and minerals also play a critical role in an ani-
mal’s nutritional strategies and physiology (Simpson and
Raubenheimer 2012). Micronutrients, such as essential
minerals, vitamin E and carotenoids, must be obtained
through the diet (Evans and Halliwell 2001). Deficiencies
in dietary micronutrients have been linked to an increased
risk of many diseases (Hegseth et al. 2011; Lucas et al.
Herbivores and omnivores, including species of insects,
birds and mammals, have been shown using geometrical
analysis to regulate their intake of macronutrients and some
micronutrients and to make post-ingestive adjustments to
help attain the optimal balance of nutrients to meet their vari-
ous requirements (Raubenheimer and Jones 1996; Rauben-
heimer et al. 2007; Simpson and Raubenheimer 2012).
Nutritional geometry has been used to model the interactive
effects that nutrients have on different animals and humans
(Raubenheimer et al. 2014), dietary problems in the critically
endangered herbivorous parrot, the kakapo (Strigops habrop-
tila, Raubenheimer and Simpson 2006), and to explain the
patterns of annual migration in giant pandas (Ailuropoda
melanoleuca, Nie et al. 2014). We view similar studies in
seabirds and other marine predators as a priority.
Confirmation of significant nutritional variability at dif-
ferent scales in the diets of these marine predators high-
lights the important question for future field-based stud-
ies as to what extent it provides nutritional opportunity
vs. constraint. A comparison of methods used for macronu-
trient analysis is a priority in order to validate the large dif-
ferences in diet observed between species and studies. The
challenge ahead is to integrate this nutritional modelling
framework for dietary assessments with long-term sys-
tematic collection of samples for proximate analysis. Our
approach allows us to continue to gain a better understand-
ing of the mechanisms governing dietary choices in wild
carnivores, which is of central importance to understand-
ing the evolution and adaptations of predators and their
influence on their food webs (Simpson and Raubenheimer
Acknowledgments We thank Sarah Dwyer, Rob Schuckard, Willie
Cook, David Melville, Danny Boulton, Karen and Sabrina Macho-
vsky and Sonja Clements for their assistance with sample collection.
We also thank the anonymous reviewers for helpful comments on
early versions of the manuscript. Aspects of this work were funded
by Massey University Research Fund (MURF) and Faculty of Vet-
erinary Science (The University of Sydney). Samples were collected
under Department of Conservation permits NM-32772-FAU and
Adams N, Abrams R, Siegrfried W, Nagy K, Kaplan I (1991) Energy
expenditure and food consumption by breeding Cape gannets
Morus capensis. Mar Ecol Prog Ser 70:1–9
Annett CA, Pierotti R (1999) Long-term reproductive output in west-
ern gulls: consequences of alternate tactics in diet choice. Ecol-
ogy 80:288–297
AOAC (2005) Official methods of analysis of AOAC International,
18th edn. AOAC International, Arlington
Bunce A (2001) Prey consumption of Australasian gannets (Morus
serrator) breeding in Port Phillip Bay, southeast Australia, and
potential overlap with commercial fisheries. ICES J Mar Sci
Chambers PG, Simpson SJ, Raubenheimer D (1995) Behavioural
mechanisms of nutrient balancing in Locusta migratoria nymphs.
Anim Behav 50:1513–1523
Cherel Y, Hobson KA, Weimerskirch H (2000) Using stable-isotope
analysis of feathers to distinguish moulting and breeding origins
of seabirds. Oecologia 122:155–162
Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005) Nutrition, phys-
iology, and stable isotopes: new information from fasting and
molting penguins. Ecology 86:2881–2888
Davies DH (1956) The South African pilchard (Sardinops ocellata)
and maasbanker (Trachurus trachurus) bird predators, 1954–
1955. South African Department of Commerce and Industry,
Division of Fisheries Investigational Report 23
Duffy DC, Jackson S (1986) Diet studies of seabirds: a review of
methods. Colon Waterbird 9:1–17
Ellis HI (1984) Energetics of free-ranging seabirds. In: Whittow
GC, Rahn H (eds) Seabird energetics. Springer, New York, pp
Evans P, Halliwell B (2001) Micronutrients: oxidant/antioxidant sta-
tus. Br J Nutr 85:S67–S74
Fryxell JM, Lundberg P (1997) Individual behavior and community
dynamics. Chapman and Hall, New York
Furness RW (1978) Energy requirements of seabird communities: a
bioenergetics model. J Anim Ecol 47:39–53
Galef BG (1996) Food selection: problems in understanding how we
choose foods to eat. Neurosci Biobehav Rev 20:67–73
Garthe S, Montevecchi WA, Davoren GK (2011) Inter-annual changes
in prey fields trigger different foraging tactics in a large marine
predator. Limnol Oceanogr 56:802–812
Author's personal copy
2800 Mar Biol (2014) 161:2791–2801
1 3
Grémillet D, Pichegru L, Kuntz G, Woakes AG, Wilkinson S, Craw-
ford RJM, Ryan PG (2008) A junk-food hypothesis for gannets
feeding on fishery waste. Proc R Soc Lond Biol 275:1149–1156
Hamer KC, Phillips RA, Wanless S, Harris MP, Wood AG (2000)
Foraging ranges, diets and feeding locations of gannets (Morus
bassanus) in the North Sea: evidence from satellite telemetry.
Mar Ecol Prog Ser 200:257–264
Hamer KC, Humphreys EM, Wanless S, Garthe S, Hennicke J, Peters
G, Phillips RA, Harris MP (2007) Annual variation in diets, feeding
locations and foraging behaviour of gannets in the North Sea: flex-
ibility, consistency and constraint. Mar Ecol Prog Ser 338:295–305
Hawkins JM (1988) The Farewell Spit gannetry—a new sea level col-
ony. Notornis 35:249–260
Hegseth MN, Camus L, Helgason LB, Bocchetti R, Gabrielsen GW,
Regoli F (2011) Hepatic antioxidant responses related to levels of
PCBs and metals in chicks of three Arctic seabird species. Comp
Biochem Physiol C Toxicol Pharmacol 154:28–35
Jarvis MJF (1970) Interactions between man and the South African
Gannet Sula capensis. Ostrich 40(Suppl. 8):497–513
Lea MA, Cherel Y, Guinet C, Nichols PD (2002) Antarctic fur seals
foraging in the polar frontal zone: inter-annual shifts in diet as
shown from fecal and fatty acid analyses. Mar Ecol Prog Ser
Lenky C, Eisert R, Oftedal OT, Metcalf V (2012) Proximate com-
position and energy density of nototheniid and myctophid fish
in McMurdo Sound and the Ross Sea, Antarctica. Polar Biol
Lucas A, Morales J, Velando A (2014) Differential effects of specific
carotenoids on oxidative damage and immune response of gull
chicks. J Exp Biol 217:1253–1262
Machovsky-Capuska GE, Vaughn RL, Würsig B, Katzir G, Rauben-
heimer D (2011a) Dive strategies and foraging effort in the Aus-
tralasian gannet Morus serrator revealed by underwater videog-
raphy. Mar Ecol Prog Ser 442:255–261
Machovsky-Capuska GE, Dwyer SL, Alley MR, Stockin KA,
Raubenheimer D (2011b) Evidence for fatal collisions and klep-
toparasitism while plunge diving in gannets. Ibis 153:631–635
Machovsky-Capuska GE, Howland HC, Vaughn RL, Würsig B,
Raubenheimer D, Hauber ME, Katzir G (2012) Visual accommo-
dation and active pursuit of prey underwater in a plunge diving
bird: the Australasian gannet. Proc R Soc B 279:4118–4125
Machovsky-Capuska GE, Hauber ME, Libby E, Amiot C, Raubenhe-
imer D (2013) The contribution of private and public information
in foraging by Australasian gannets. Anim Cogn 17:849–858
Machovsky-Capuska GE, Hauber ME, Dassis M, Libby E, Wikel-
ski MC, Schuckard R, Melville D, Cook W, Houston M,
Raubenheimer D (2014) Foraging behaviour and habitat use of
chick-rearing Australasian Gannets in New Zealand. J Ornithol
Manighetti B, Carter L (1999) Across-shelf sediment dispersal, Hau-
raki Gulf, New Zealand. Mar Geol 160:271–300
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005)
Nutrient-specific foraging in invertebrate predators. Science
Mayntz D, Nielsen VH, Sørensen A, Toft S, Raubenheimer D,
Hejlesen C, Simpson SJ (2009) Balancing of protein and lipid
intake by a mammalian carnivore, the mink Mustela vison. Anim
Behav 77:349–355
Meynier L, Stockin KA, Bando MKH, Duignan PJ (2008) Stomach
contents of common dolphin (Delphinus sp.) from New Zealand
waters. NZ J Mar Freshw 42:257–268
Montevecchi WA, Ricklefs RE, Kirkham IR, Gabaldon D (1984)
Growth energetics of nestling northern gannets (Sula bassanus).
Auk 101:334–341
Nelson JB (2005) Pelicans, cormorants and their relatives. Oxford
University Press, Oxford
Nie Y, Zhang Z, Raubenheimer D, Elser JJ, Wei W, Wei F (2014)
Obligate herbivory in an ancestrally carnivorous lineage: the
giant panda and bamboo from the perspective of nutritional
geometry. Funct Ecol. doi:10.1111/1365-2435.12302
Paddack MJ, Cowen RK, Sponaugle S (2006) Grazing pressure of
herbivorous coral reef fishes on low coral-cover reefs. Coral
Reefs 25:461–472
Paulin C, Stewart A, Roberts C, McMillan P (1989) New Zealand
Fish: a complete guide. In: National museum of New Zealand
miscellaneous series no. 19
Petry MV, Fonseca VSD, Scherer AL (2007) Analysis of stomach
contents from the black-browed albatross, Thalassarche melano-
phris, on the coast of Rio grande do sul, southern Brazil. Polar
Biol 30:321–325
Pichegru L, Ryan P, van der Lingen C, Coetzee J, Ropert-Coudert
Y, Grémillet D (2007) Foraging behaviour and energetics of
Cape gannets Morus capensis feeding on live prey and fishery
discards in the Benguela upwelling system. Mar Ecol Prog Ser
Polis GA, Holt RD (1992) Intraguild predation—the dynamics of
complex trophic interactions. Trends Ecol Evol 7:151–154
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of
intraguild predation: potential competitors that eat each other.
Annu Rev Ecol Syst 20:297–330
Raubenheimer D (2011) Toward a quantitative nutritional ecology:
the right-angled mixture triangle. Ecol Monogr 81:407–427
Raubenheimer D, Jones SA (1996) Nutritional imbalance in an
extreme generalist omnivore: tolerance and recovery through
complementary food selection. Anim Behav 71:1253–1262
Raubenheimer D, Simpson SJ (2006) The challenge of supplementary
feeding: can geometric analysis help save the kakapo? Notornis
Raubenheimer D, Mayntz D, Simpson SJ, Toft S (2007) Nutrient-spe-
cific compensation following diapause in a predator: implications
for intraguild predation. Ecology 88:2598–2608
Raubenheimer D, Machovsky-Capuska GE, Gosby AK, Simpson S
(2014) The nutritional ecology of obesity: from humans to com-
panion animals. Br J Nutr. doi:10.1017/S0007114514002323
Richoux NB, Jaquemet S, Bonnevie BT, Cherel Y, McQuaid CD
(2010) Trophic ecology of grey-headed albatrosses from Marion
Island, Southern Ocean: insights from stomach contents and diet
tracers. Mar Biol 157:1755–1766
Robertson D (1992) Diet of the Australasian gannet Morus serrator
(G.R. Gray) around New Zealand. N Z J Ecol 16:77–81
Ropert-Coudert Y, Grémillet D, Kato A, Ryan P, Naito Y, Le Maho
Y (2004) A fine-scale time budget of Cape gannets provides
insights into the foraging strategies of coastal seabirds. Anim
Behav 67:985–992
Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional
geometry: gorillas prioritize non-protein energy while consuming
surplus protein. Biol Lett 7:847–849
Rubio V, Sanchez F, Zamora S, Madrid J (2008) Endogenous modifi-
cation of macronutrient selection pattern in sea bass (Dicentrar-
chus labrax). Physiol Behav 95:32–35
Rubio VC, Navarro DB, Madrid JA, Sanchez-Vazquez FJ (2009)
Macronutrient self-selection in Solea senegalensis fed macronu-
trient diets and challenged with dietary protein dilutions. Aqua-
culture 291:95–100
Schuckard R, Melville DS, Cook W, Machovsky-Capuska GE (2012)
Diet of the Australasian gannet (Morus serrator) at Farewell Spit,
New Zealand. Notornis 59:66–70
Simpson SJ, Raubenheimer D (2012) The nature of nutrition: an inte-
grative framework from animal adaptation to human obesity.
Princeton University Press, Princeton
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University
Press, Princeton
Author's personal copy
2801Mar Biol (2014) 161:2791–2801
1 3
Votier SC, Bearhop S, MacCormick A, Ratcliffe N, Furness RW
(2003) Assessing the diet of great skuas, Catharacta skua, using
five different techniques. Polar Biol 26:20–26
Votier SC, Bearhop S, Witt MJ, Inger R, Thompson D, Newton J
(2010) Individual responses of seabirds to commercial fisheries
revealed using GPS tracking, stable isotopes and vessel monitor-
ing systems. J Appl Ecol 47:487–497
Wanless S, Harris MP, Redman P, Speakman JR (2005) Low energy
values of fish as a probable cause of a major seabird breeding
failure in the North Sea. Mar Ecol Prog Ser 294:1–8
Westoby M (1974) An analysis of diet selection by large generalist
herbivores. Am Nat 108:290–304
Westoby M (1978) What are biological bases of varied diets? Am Nat
Wilder SM, Eubanks MD (2010) Might nitrogen limitation promote
omnivory among carnivorous arthropods? Comment. Ecology
Wingham EJ (1985) Food and feeding range of the Australasian gan-
net Morus serrator (gray). Emu 85:231–239
Wingham E (1989) Energy requirements of Australasian gannets
Morus serrator (Gray) at a breeding colony. Emu 89:65–70
Work TM (2000) Avian necropsy manual for biologists in remote ref-
uges. US Geological Survey, National Wildlife Health Centre,
Hawaii Field Station, Honolulu
Author's personal copy
... Among these multiple sympatric predator-prey interactions, common dolphins (Delphinus delphis; hereafter dolphins) and Australasian gannets (Morus serrator; hereafter gannets) represent one of the most frequently observed associations during feeding events (Burgess, 2006;Stockin et al., 2008aStockin et al., , b, 2009ade la Brosse, 2010;Purvin, 2015) and can serve as a model to understand the behavioural, ecological, and evolutionary dimensions of such interactions. While the local diet of both predators is well characterized (Meynier et al., 2008a;Machovsky-Capuska et al., 2011a;Tait et al., 2014;Peters et al., 2020), a current lack of insight on their nutritional strategies with respect to foraging behaviours has prevented any detailed understanding of this conspecific relationship until now. ...
... For prey species that contributed >1% wet mass to the diets of both dolphins and gannets, we collected 30 individual samples from 7 species for subsequent proximate composition analyses. We further extracted proximate compositional data from Tait et al., (2014) for the remaining three species (Table 1). Carbohydrates are known to constitute a negligible content on squid and marine fish species (Craig et al., 1978), thus we measured the proximate composition of protein (P), lipid (L), water (W), and ash (A). ...
... For gannets, majority of nutritional dietary intake (91.5%, wet mass), occurred via the consumption of pilchard, yellow eye mullet, kahawai, and anchovy. These results are consistent with previous findings that suggest both predators' prey upon surface schooling anchovy, pilchard, and jack mackerel within the Hauraki Gulf (Tait et al., 2014;Peters et al., 2020). While vital to many marine predators coexisting in the area (Gostischa et al., 2021), the availability of prey across the Hauraki Gulf is subject to the East Auckland Current, shelf-upwelling patterns, and environmental oscillations that influence the nutrient production (Zeldis et al., 2004). ...
Full-text available
Prey detection and subsequent capture is considered a major hypothesis to explain feeding associations between common dolphins and Australasian gannets. However, a current lack of insight on nutritional strategies with respect to foraging behaviours of both species has until now, prevented any detailed understanding of this conspecific relationship. Here we combine stomach content analysis (SCA), nutritional composition of prey, a multidimensional nutritional niche framework (MNNF) and videography to provide a holistic dietary, nutritional, and behavioural assessment of the feeding association between dolphins and gannets in the Hauraki Gulf, New Zealand. Dolphins consumed ten prey species, including grey mullet (Mugil cephalus) as the most representative by wet mass (33.4%). Gannets preyed upon six species, with pilchards (Sardinops pilchardus) contributing most of the diet by wet mass (32.4%) to their diet. Both predators jointly preyed upon pilchard, jack mackerel (Trachurus spp.), arrow squid (genus Nototodarus), and anchovy (Engraulis australis). Accordingly, the MNNF revealed a moderate overlap in the prey composition niche (0.42) and realized nutritional niche (0.52) between dolphins and gannets. This suggests that both predators coexist in a similar nutritional space, while simultaneously reducing interspecific competition and maximizing the success of both encountering and exploiting patchily distributed prey. Behavioural analysis further indicated that dolphin and gannets feeding associations are likely to be mutually beneficial, with a carouselling foraging strategy and larger pod sizes of dolphins, influencing the diving altitude of gannets. Our approach provides a new, more holistic understanding of this iconic foraging relationship, which until now has been poorly understood.
... This nutritionally explicit framework is particularly relevant to marine apex predators known to forage in complex and fluctuating marine environments (Machovsky-Capuska et al., 2016a;Machovsky-Capuska and Raubenheimer, 2020). While the characterization of nutritional niche breadths of marine predators has shown to be critical to trophic interactions, marine pollution, aquaculture, captivity and rehabilitation, climate change, and conservation and management of endangered species (Machovsky-Capuska and , yet the field remains poorly characterized to few species of seabirds (Machovsky-Capuska et al., 2016c, 2016dMiller et al., 2018;Tait et al., 2014), sharks (Grainger et al., 2020;Machovsky-Capuska and Raubenheimer, 2020), turtles , cetaceans (Denuncio et al., 2017;Machovsky-Capuska et al., 2019) and pinnipeds . ...
... Following Tait et al. (2014), we collected prey samples from closest spatiotemporal range and size for proximate composition analysis of all the species that contributed >1% M to the diets of SASL and SAFS. Proximate composition of 11 prey species (50 individuals) were determined at the Instituto Nacional de Investigación y Desarrollo Pesquero (Table 1). ...
... el Niño y la Niña events, global warming) and life history traits (e.g. sex, growth and reproduction) (Lawson et al., 1998;Machovsky-Capuska et al., 2016c;Saadettin et al., 1998;Tait et al., 2014). An additional pelagic-demersal pattern in the nutritional composition of marine prey suggests a low lipid and energy content in demersal species in comparison to pelagic ones that are often higher in lipids and energy composition (Eder and Lewis, 2005;Machovsky-Capuska and Raubenheimer, 2020;Murray and Burt, 1969). ...
Niche segregation has been recognized as a valuable mechanism for sympatric species to reduce interspecific competition and facilitate coexistence. The differential use of habitats is one of the behavioural mechanisms that may shape coexistence among marine predators. In this study, we provide a dietary and nutritional assessment of two pinnipeds, the South American sea lion (SASL) and the South American fur seal (SAFS) and explore their sympatric coexistence within the Warm Temperate Southwestern Atlantic biogeographic province (WTSA province). Pelagic prey species within the WTSA province showed significantly higher proportional composition of lipids than demersal counterparts, evidencing a nutritional variability in a vertical dimension accessible to marine predators. By modelling the dietary niches of these pinnipeds through a nutritional lens, we showed high overlapping prey composition niche breadths suggesting that both species consumed prey with similar nutritional composition; however, distinct realized nutritional niches showed that diets are likely shaped by differences in foraging behaviours. The SAFS combined pelagic and demersal prey, whereas SASL mostly preyed upon demersal species. This paper provides crucial information on how nutritional variability in the water column likely drives the feeding strategies of both pinnipeds in the WTSA province. Given that this variation can influence the stability of the contrasting population trends shown by these two pinnipeds, nutritional dynamics must be taken into consideration when defining conservation strategies.
... Understanding trophic decisions in marine predators is necessary to predict their response to environmental and anthropogenic changes that alter prey availability and composition (Tait et al., 2014;Hays et al., 2016). Yet, these decisions vary substantially across species (e.g., Church et al., 2019) and sexes (e.g., Navarro et al., 2010). ...
... However, this variation also occurs in monomorphic species (Peck and Congdon, 2006). A number of factors contribute to sex differences in foraging, including differing nutritional requirements, parental care, sensitivity to offspring condition, and differences in foraging efficiency (Kato et al., 2000;Gray and Hamer, 2001;Lewis et al., 2002;Quillfeldt et al., 2004;Navarro et al., 2010;Stauss et al., 2012;Tait et al., 2014). When intersexual competition is present, competitive exclusion may arise and, in some groups, this is overcome by the differentiation of trophic niches between the sexes (Lewis et al., 2002;Peck and Congdon, 2006;Elliott et al., 2010). ...
... Gannets are only slightly sexually dimorphic, with females being marginally heavier than males (in our dataset, on average 170 g, or 5-6% of adult body weight), and previous studies have found no significant difference in length of the tarsus, bill, or wing of breeding gannets (Stauss et al., 2012;Malvat et al., 2020). Female gannets also make a greater contribution to chick provisioning (Montevecchi et al., 1984) than males, and are likely to have a calcium (and other nutrients) deficit from egg production, which may require them to target different food, particularly micronutrients compared to males (Tait et al., 2014). Data on discards in our study area shows that the demersal seine vessels, attended proportionately more by females, tend to discard low proportions of pelagic species, and significantly less discards overall than trawlers (Anon, 2011). ...
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Sex differences in diet and foraging behaviour are common in sexually dimorphic species, often driven by differences in the cost of locomotion or ability to exploit different ecological niches. However, sex-specific foraging strategies also occur in monomorphic or slightly dimorphic species where the drivers are poorly understood. Here, we study sex differences in foraging of northern gannets ( Morus bassanus ), where females are only slightly heavier than males. Using concurrently tracked gannets (298 full foraging trips from 81 individuals) and fishing vessels across 5 years, we quantify individual-based vessel-associated putative foraging, and relate this to discard consumption. We found a significant positive relationship between time spent in vessel-associated foraging and discard consumption for both sexes. However, while females showed greater proportions of vessel-associated foraging than males, discarded fish contributed less to the diet of females in all years. These results contrast with previous suggestions that female gannets interact with vessels less often than males, and are consistent with competitive exclusion of females from trawler-associated discards. Our findings give insight into sexual differences in foraging behaviour in the absence of dimorphism that are necessary to predict their response to environmental and anthropogenic changes.
... Certainly, knowledge of predator nutritional niche breadths and requirements could assist in understanding their responses to variations in prey availability and composition (Machovsky-Capuska et al., 2016d). Several studies on marine predators, including seabirds (Tait et al., 2014;Machovsky-Capuska et al., 2016b,c;Miller et al., 2017), cetaceans (Denuncio et al., 2017), fish, sharks and pinnipeds (Machovsky-Capuska and Raubenheimer, 2020) have now drawn from the MNNF to provide fresh insights into their nutritional ecology. Machovsky-Capuska et al. (2018) incorporated a standardised metric (standard ellipse area, SEA) and statistical framework utilising Bayesian multivariate ellipses (sensu Jackson et al., 2011) to quantify and compare nutritional niche breadths. ...
... Compositions of prey were expressed as wet mass percentages of protein (%P), lipid (%L) and water (%W), given that carbohydrate content is negligible in most marine prey (Craig et al., 1978). When possible, we extracted prey compositions from studies conducted in geographical proximity to the present study (Supplementary Table S7; Tait et al., 2014). If nutritional information was unavailable for a prey species, average values for closely related taxa (same genus or family) with similar ecological attributes were used (Supplementary Table S7; Eder and Lewis, 2005). ...
... While we acknowledge limitations in using literature prey data (e.g. potential spatiotemporal effects on prey proximate composition affecting comparisons; Tait et al., 2014), this has presented a valuable opportunity for integrating nutrition with existing knowledge of white sharks' diets and spurs interesting questions about the influence of prey compositions in broader white shark ecology. ...
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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.
... Nutritional ecology, defined as the study of how animals relate to their environment through nutritional interactions (Raubenheimer et al., 2009, has demonstrated the potential of generating new insights into feeding behaviour and its role in structuring populations, communities and ecosystems (Simpson et al., 2010;Tait et al., 2014). ...
Body nutrient profiles in ecological studies allow for relating the nutritional status of consumers and their effects on the movement and retention of elements in ecosystems, as well as reflecting feeding conditions and habitat quality. This study compared the detailed whole-body nutrient composition (macronutrients, minerals, fatty acids and amino acids) of two omnivorous natives Orestias killifish from Lake Titicaca (Orestias agassizii and Orestias luteus, Valenciennes), the largest lake in the Andes, as an indirect tool to understand differences in their feeding ecology. Although both species are usually described as omnivorous fish, both have amphipods (Hyalella spp) as their main food source. Our results showed that both killifish had a comparable macronutrient composition, and the mineral concentrations of Mg, P and Ca (reflecting bony structures) differed between them. Many of the saturated fatty acids were significantly lower in O. luteus, and O. agassizii had higher concentrations of cis-vaccenic acid (18:1n11 (cis)), supporting the idea of a higher algal contribution to the diet of this fish. The lower histidine and higher taurine concentrations in O. agassizii compared with O. luteus (independent of body size) may reflect its ubiquitous behaviour and plasticity. This study shows how whole-body nutrient analysis can identify differences in feeding ecology and feeding behaviour between related species.
... A key question at the frontier of nutritional ecology is: do carnivores exhibit SCIT 10,25,54,55 ? To our knowledge, our study is the first to test this hypothesis within the context of amino acids. ...
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In nutritional ecology the intake target is the diet that maximises consumer fitness. A key hypothesis of nutritional ecology is that natural selection has acted upon the behavioural and physiological traits of consumers to result in them Selectively Consuming prey to match the Intake Target (SCIT). SCIT has been documented in some herbivores and omnivores, which experience strong heterogeneity in the nutritional quality of available foods. Although carnivores experience a prey community with a much more homogeneous nutrient composition, SCIT by carnivores has nevertheless been deemed highly likely by some researchers. Here we test for SCIT for micronutrients (amino acids) in two freshwater carnivores: the river blackfish and the two-spined blackfish. Although both blackfishes exhibited non-random consumption of prey from the environment, this resulted in non-random consumption of amino acids in only one species, the river blackfish. Non-random consumption of amino acids by river blackfish was not SCIT, but instead an artefact of habitat-specific foraging. We present hypotheses to explain why wild populations of freshwater carnivores may not exhibit SCIT for amino acids. Our work highlights the need for careful, critical tests of the hypotheses and assumptions of nutritional ecology and its application to wild populations.
... This is consistent with observations of reduced Δ 15 N in (Table S2; see Data Sources section; also see Grainger et al., 2020). Compositions were extracted, where possible, from studies conducted in geographical proximity to the present study (Tait et al., 2014), and values for closely related taxa (same genus/family) were used if compositions were unavailable for particular prey species (Table S2; Eder & Lewis, 2005). Compositions of prey species were generally similar within source groupings (Table S2, Figure S3) and c-index nutrients (response) was also evaluated using a beta GLM to test whether similar levels of individual specialisation (i.e. ...
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Dietary specialisations are important determinants of ecological structure, particularly in species with high per‐capita trophic influence like marine apex predators. These species are, however, among the most challenging in which to establish spatiotemporally integrated diets. We introduce a novel integration of stable isotopes with a multidimensional nutritional niche framework that addresses the challenges of establishing spatiotemporally integrated nutritional niches in wild populations, and apply the framework to explore individual diet specialisation in a marine apex predator, the white shark Carcharodon carcharias . Sequential tooth files were sampled from juvenile white sharks to establish individual isotopic (δ‐space; δ ¹³ C, δ ¹⁵ N, δ ³⁴ S) niche specialisation. Bayesian mixing models were then used to reveal individual‐level prey (p‐space) specialisation, and further combined with nutritional geometry models to quantify the nutritional (N‐space) dimensions of individual specialisation, and their relationships to prey use. Isotopic and mixing model analyses indicated juvenile white sharks as individual specialists within a broader, generalist, population niche. Individual sharks differed in their consumption of several important mesopredator species, which suggested among‐individual variance in trophic roles in either pelagic or benthic food webs. However, variation in nutrient intakes was small and not consistently correlated with differences in prey use, suggesting white sharks as nutritional specialists and that individuals could use functionally and nutritionally different prey as complementary means to achieve a common nutritional goal. We identify how degrees of individual specialisation can differ between niche spaces (δ‐, p‐ or N‐space), the physiological and ecological implications of this, and argue that integrating nutrition can provide stronger, mechanistic links between diet specialisation and its intrinsic (fitness/performance) and extrinsic (ecological) outcomes. Our time‐integrated framework is adaptable for examining the nutritional consequences and drivers of food use variation at the individual, population or species level.
... The animals tend to adjust the macronutrient intake closer to their natural diet, especially by increasing protein consumption in the high-temperature treatment (Fig. 2.7). Such nutrientspecific diet selection is consistent with the ecology of marine organisms, which forage in nutritionally complex and fluctuating marine environments that vary spatially and temporally (Tait et al. 2014;Machovsky-Capuska et al. 2016a, 2018. ...
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.
... The macronutrient and fiber niches are composed of carbohydrates, lipids, and proteins, and lignin hemicellulose and cellulose, respectively Our investigation into the female Ronald Lake bison's seasonal macronutrient composition provides insight into herbivore nutrient availability and regulation. As herbivores, bison are restricted to a relatively narrow macronutrient niche when compared to omnivores (e.g., Senior et al., 2016) or carnivores (e.g., Tait et al., 2014). Our realized macronutrient and fiber niche measures are similar to other herbivores whose niches have been quantified, such as blue sheep (Aryal et al., 2015) and wild water buffalo (Shrestha et al., 2020). ...
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Diet is one of the most common traits used to organize species of animals into niches. For ruminant herbivores, the breadth and uniqueness of their dietary niche are placed on a spectrum from browsers that consume woody (i.e., browse) and herbaceous (i.e., forbs) plants, to grazers with graminoid-rich diets. However, seasonal changes in plant availability and quality can lead to switching of their dietary niche, even within species. In this study, we examined whether a population of wood bison (Bison bison athabascae) in northeast Alberta, Canada, seasonally switched their foraging behavior , and if so, whether this was associated with changes in nutrient acquisition. We hypothesized that bison should switch foraging behaviors from grazing in the winter when standing, dead graminoids are the only foliar plants readily available to browsing during spring and summer as nutritious and digestible foliar parts of browse and forbs become available. If bison are switching foraging strategy to maximize protein consumption, then there should be a corresponding shift in the nutritional niche. Alternatively, if bison are eating different plants, but consuming similar amounts of nutrients, then bison are switching their dietary niche to maintain a particular nutrient composition. We found wood bison were grazers in the winter and spring, but switch to a browsing during summer. However, only winter nutrient consumption of consumed plants differed significantly among seasons. Between spring and summer, bison maintained a specific nutritional composition in their diet despite compositional differences in the consumed plants. Our evidence suggests that bison are selecting plants to maintain a target macronutrient composition. We posit that herbivore's can and will switch their dietary niche to maintain a target nutrient composition.
... However, other tropical seabird species did show sexual segregation in foraging behavior (see Table 1 and Mancini et al. 2013). Possibly, the inconsistency in finding sexual segregation in foraging in Sulids is an effect of the distribution of their prey resources according to the geography Tait et al. 2014;Castillo-Guerrero et al. 2016), and time of the study (Hamer et al. 2007;Harding et al. 2007;Garthe et al. 2011). ...
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Sexual segregation in foraging occurs in some species and populations of boobies (Sulidae), but it is not a general pattern. Sexual segregation in foraging may occur to avoid competition for food, and this competition may intensify during specific stages of breeding. We examined sexual segregation in foraging in relation to breeding stage in masked boobies Sula dactylatra at Rapa Nui by tracking simultaneously incubating and chick-rearing birds using GPS recorders (n = 18) and collected a total of 11 regurgitate samples. Stable isotope analyses (δ¹³C and δ¹⁵N) of whole blood samples were carried out in 20 birds. There were no differences in foraging trip parameters or diet between females and males. Both sexes traveled farther and for longer while incubating than while rearing chicks. Isotopic niches (δ¹³C and δ¹⁵N) overlapped to some degree among all groups at all times, but the lowest overlap between sexes occurred during incubation. While preying on ephemerally distributed flying fish, vertical or horizontal competition avoidance may be almost impossible, and thus females and males share their foraging grounds. Since birds were tracked simultaneously, shorter foraging trips of chick-rearing birds must be an effect of the constraints of provisioning the chick. Differences observed in δ¹⁵N and δ¹³C values between sexes may be caused by subtle differences in their foraging behaviors, or by differences in physiology linked to breeding. Our findings suggest that local oceanography and its inherent food distribution are determinants for sexual segregation in foraging patterns in masked boobies and possibly also other booby species. Significance statement In some animals, females and males forage on different areas or prey on different species to avoid competition for food resources. In boobies (Sula sp.), some studies show evidence of sexual segregation in foraging and others do not. Here, we tested if sexual segregation in foraging occurred in masked boobies on the Pacific island of Rapa Nui by studying simultaneously incubating and chick-rearing birds. We found no evidence of sexual segregation on foraging behavior or diet. We discuss that the difference between this and other studies in boobies may be an effect of the local prey availability. When the prey community is more diverse and heterogeneously distributed, each sex may access different resources and thus sexual foraging segregation will occur. In contrast, in areas like Rapa Nui where prey resources are distributed ephemerally, sexual segregation in foraging will not be useful and is thus less likely to occur.
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The diet of the Australasian gannet (Morus serrator) at Farewell Spit, New Zealand, was studied by the analysis of 70 regurgitations collected from the 1995 to 2001 breeding seasons. Surface schooling pilchard (Sardinops neopilchardus) was the main prey, followed by anchovy (Engraulis australis). The composition of the diet was similar in most seasons examined except in 1996 in which anchovy was the main prey item. Such a change in diet could be linked with a pilchard mass mortality in New Zealand in August 1995. The estimated annual prey consumption by birds at the Farewell Spit gannetry was 852 tonnes. Although annual catches of pilchard and anchovy by commercial fsheries in the area are still relatively small, an increase may interfere with prey availability, and in turn, increase competition between marine predators and infuence the breeding success. Our analyses of diet are consistent with previous studies showing that Australasian gannets as fexible foragers and they highlight their importance as bioindicators of fsh stocks in New Zealand.
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We describe the energetics of postnatal growth and development of wild and captive Northern Gannet chicks. For 14 chicks 0-9 weeks old, a 24-week immature, and a breeding female, we determined water, lipid, and nonlipid content. During the 13-week nestling period, mass increased over 40-fold. Accumulation of lipid caused the energy density of chicks to increase steadily through 9 weeks. Lipid eventually accounted for about 60% of energy in tissues. Two captive chicks grew at rates comparable to wild young and consumed, on average, about 24 kg of fish containing 190,000 kJ during the nestling period. The energy density of chick guano was 13.3 ± 0.8 kJ/g. Estimated metabolizable energy (ME) rose rapidly from 952 kJ during week 1 to 19,318 kJ during week 6, after which ME fluctuated between about 9,000 and 16,400 kJ/week. During week 1, the growth increment (GI) was 801 kJ; GI increased sharply to 9,667 kJ during week 4 and peaked at 12,711 kJ in week 7. Net growth efficiency was 49% to 8 weeks of age and 33% to fledging at 13 weeks. The food requirement of the gannet population of Newfoundland is estimated.
Foraging deficiencies and supplementary feeding play critical roles in kakapo (Strigops habroptilus) breeding biology and conservation. We present a framework for the analysis of complex nutritional data (called the geometric framework - GF) which may contribute further understanding of the relationships between natural foods, supplementary feeding and kakapo reproduction. We outline the basic concepts of the approach, and illustrate its application using data for the protein, lipid and calcium content of a natural food (green fruits of rimu Dacrydium cupressinum) and a supplementary feed ("muesli"). We provide some pointers for the broader application of GF to the problem of kakapo supplementary feeding, and close with a brief review of a literature which suggests that calcium might be a key limiting factor in kakapo reproduction. We hypothesise that supplementary foods with low macronutrient:calcium ratios are likely to be most effective in supporting increased reproduction.
Nutrition has long been considered more the domain of medicine and agriculture than of the biological sciences, yet it touches and shapes all aspects of the natural world. The need for nutrients determines whether wild animals thrive, how populations evolve and decline, and how ecological communities are structured.The Nature of Nutritionis the first book to address nutrition's enormously complex role in biology, both at the level of individual organisms and in their broader ecological interactions. Stephen Simpson and David Raubenheimer provide a comprehensive theoretical approach to the analysis of nutrition--the Geometric Framework. They show how it can help us to understand the links between nutrition and the biology of individual animals, including the physiological mechanisms that determine the nutritional interactions of the animal with its environment, and the consequences of these interactions in terms of health, immune responses, and lifespan. Simpson and Raubenheimer explain how these effects translate into the collective behavior of groups and societies, and in turn influence food webs and the structure of ecosystems. Then they demonstrate how the Geometric Framework can be used to tackle issues in applied nutrition, such as the problem of optimizing diets for livestock and endangered species, and how it can also help to address the epidemic of human obesity and metabolic disease.