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The nutritional nexus: Linking niche, habitat variability and prey composition in a generalist marine predator



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.
| J Anim Ecol. 2018;87:1286–1298.
© 2018 The Aut hors. Journa l of Anima l Ecolog y
© 2018 British Ecological Society
Received: 23 Januar y 2018 
  Accepted: 13 May 2018
DOI : 10.1111/136 5-265 6.12856
The nutritional nexus: Linking niche, habitat variability and prey
composition in a generalist marine predator
Gabriel E. Machovsky-Capuska1,2 | Mark G. R. Miller3| Fabiola R. O. Silva2|
Christophe Amiot4| Karen A. Stockin4| Alistair M. Senior1,5 | Rob Schuckard6|
David Melville6| David Raubenheimer1,2
1Charles Perkins Centre, The Universit y of Sydney, Sydney, NSW, Australia; 2School of Life and Environmental Sciences, The University of Sydney, Sydney,
NSW, Austr alia; 3College of Science and Engineering and Centre for Tropical Environment al and Sustainability Science, James Cook University, Cairns, QLD,
Australia; 4Institute of Natural and Mathematical Sciences, Massey University, Auckland, New Zealand; 5School of Mathematic s and Statistics, The University
of Sydney, Sydney, NSW, Australia and 6Ornithological Society of New Zealand, Nelson, New Zealand
Gabriel E. Machovsky- Capuska, Charles
Perkins Centre, The Universit y of Sydney,
Sydney, NSW, Australia.
Funding information
Faculty of Veterinar y Science DVC compact
fund (The University of Sydney); Massey
University Animal Ethics committee, Grant /
Award Number: 13/65; New Zealand
Depar tment of Conser vation, Grant/Award
Number: 35189-FAU; Loxton research
fellowship from the Sydney School of
Veterinary Science, The University of Sydney
Handling Editor: Blaine Griffen
1. Our understanding of the niche concept will remain limited while the quantity and
range of different food types eaten remain a dominant proxy for niche breadth, as
this does not account for the broad ecological context that governs diet. Linking
nutrition, physiology and behaviour is critical to predict the extent to which a spe-
cies adjusts its nutritional niche breadth at the levels of prey (“prey composition
niche,” defined as the range of prey compositions eaten) and diet (“realized nutri-
tional niche” is the range of diets composed through feeding on the prey).
2. Here, we studied adult chick-rearing Australasian gannets Morus serrator to pro-
pose an integrative approach using sea surface temperature anomalies (SSTa),
geographic location and bathymetry over different years, to explore their rela-
tionship with the nutritional composition of prey and diets (i.e. prey composition
and nutritional niche breadth), habitat use and foraging behaviour.
3. We found that gannets feed on prey that varied widely in their nutritional compo-
sition (have a broad prey composition niche), and composed diets from these prey
that likewise varied in composition (have a broad realized nutritional niche), sug-
gesting 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 (0–150 m).
5. During warm water events (strong positive SSTa), gannets expanded their forag-
ing 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
Journal of Animal Ecology
The niche concept is a powerful tool in ecological and evolutionary
theory. However, niche definitions can be vague, and there are often
difficulties in measuring and characterizing niches (Kearney, 2006;
Newsome, Martinez del Rio, Bearhop, & Phillips, 2007; Pulliam,
2000). Niche breadth, in particular, has been frequently linked to
dietary generalism and is often characterized in terms of food types
ingested and/or their energy content (Futuyma & Moreno, 1988).
Thus, it is widely believed that generalists consume a wide variety of
foods and have a wide niche, whereas specialists consume a narrow
range of foods and have a narrow niche (Ducatez, Clavel, & Lefebvre,
2015). However, the nutritional implications of niche breadth are
seldom considered in the application of niche theory. This is an im-
portant omission, because nutrients provide the mechanistic link
between an animal’s foraging choices and fitness, and are therefore
indispensable for understanding the distributions of animal popula-
tions (Raubenheimer, Simpson, & Tait, 2012).
Nutritional ecology provides a flexible context for understanding
the intricate interactions between organisms and their nutritional
environment (Parker, Barboza, & Gillingham, 2009; Raubenheimer,
Simpson, & Mayntz, 2009). A conceptual and analytical framework
from nutritional ecology called nutritional geometry (NG) has en-
abled scientists to gain a new ecological perspective of nutrition by
simplifying the complexities of modelling foods (hereafter prey) in
relation to foraging behaviour, physiology and geographic processes
(Raubenheimer, 2011; Raubenheimer & Simpson, 1993). Of late, NG
was used to develop a multidimensional nutritional niche framework
(MNNF) to unify food choices and diet composition into a multilevel
classification of dietary generalism (Machovsky- Capuska, Senior,
Simpson, & Raubenheimer, 2016). This novel approach allows the
characterization of niche breadth via the macronutrient composition
of diets that can sustain a population (i.e. their realized nutritional
niche) and the range of prey compositions (“prey composition niche”)
and physical and ecological attributes of prey that a population can
exploit (i.e. their food exploitation niche).
It has been suggested that nutritional niche breadth is shaped
by several nonexclusive factors. First, in order to meet potentially
changing nutritional requirements, foragers must adjust their for-
aging behaviour to select combinations of prey available to provide
the target mix of nutrients (Machovsky- Capuska, Senior, Benn et al.,
2016). Second, the location and quality of foods are likely to influ-
ence prey consumption and foraging decisions (Machovsk y- Capuska
et al., 2014; Spitz et al., 2012). Third, interactions between bathyme-
try, physical and biological processes promote nutrient- rich environ-
ments with high prey quality (Hunt, Russell, Coyle, & Weingartner,
1998). Fourth, environmental fluctuations influence the habitat in
which a population can forage and subsist (Carroll, Everett, Harcourt,
Slip, & Jonsen, 2016; Costa, 2007), for example variation in sea sur-
face temperature (Montevecchi & Myers, 1997; Perry, Low, Ellis, &
Reynolds, 2005). Former dietary niche characterizations have been
hampered by inadequate consideration of these complex factors.
The MNNF approach, however, attempts to place diet in the context
of these variables, thus contributing to a better understanding of the
constraints and opportunities that influence diet breadth in animals.
Marine apex predators are long- lived species that forage in
complex three- dimensional environments and therefore represent
an ideal group to better understand dietary generalism in the wild
(Denuncio et al., 2017; Machovsky- Capuska, Priddel et al., 2016;
Malinowski & Herzing, 2015; Österblom, Olsson, Blenckner, &
Furness, 2008; Spitz et al., 2011, 2012). Understanding the foraging
goals of marine predators is pivotal in predicting how they will re-
spond to environmental changes in prey availability and composition
(Tait, Raubenheimer, Stockin, Merriman, & Machovsky- Capuska,
2014). Although habitat use is a central aspect of foraging, marine
ecologists often study foraging behaviour in isolation, without ad-
dressing the multiple variables and scales that shape their environ-
ments (Austin, Bowen, McMillan, & Iverson, 2006). Gannets Morus
spp., in particular, have been extensively studied with respect to
both their foraging behaviour and food preferences. Based on the
diversity of prey they consume, gannet dietary patterns have often
been described as generalist, opportunistic or flexible feeders
(Bunce & Norman, 2000; Lewis, Sherratt, Hamer, Harris, & Wanless,
2003; Machovsky- Capuska et al., 2014; Montevecchi, 2007; Ropert-
Coudert et al., 20 09; Wanless, Harris, Lewis, Frederiksen, & Murray,
2008). Although a few studies have highlighted the importance of
prey quality in different gannet populations (Bunce, 2001; Grémillet
et al., 2008; Tait et al., 2014), the extent to which gannets are dietary
generalists or specialists in terms of the foods that they exploit and
diets that they compose from th ose foods remains to be esta bl ished.
6. Our findings are consistent with previous suggestions that dietary generalism
evolves in heterogeneous environments, and provide a framework for understand-
ing the nutritional goals in wild marine predators and how these goals drive eco-
logical interactions and are, in turn, ultimately shaped by environmental
bio-logging, multidimensional nutritional niche framework, multivariate ellipse-based Bayesian
approach, niche theory, nutritional landscapes, seabirds
Journal of Animal Ecology
Here, we combine niche theory and nutritional geometry, with
data from Global Positioning System (GPS) data loggers, dietary
analysis, macronutrient composition of prey and diets with a mul-
tivariate ellipse- based Bayesian approach to characterize the prey
composition niche and realized nutritional niche of Australasian gan-
nets M. serrator (hereafter gannets). In particular, we addressed the
following questions: (a) To what extent does the nutritional compo-
sition of prey and of diets vary spatially and temporally?; (b) Do gan-
nets adjust their foraging behaviour in regard to the macronutrient
composition of prey?; and (c) Do environmental factors (in this case
Sea Surface Temperature anomalies (SSTa) and bathymetry) influ-
ence nutritional composition of prey, foraging behaviour and habitat
2.1 | Study area
Fieldwork was conducted on Farewell Spit (FS, New Zealand,
40°33′S, 173°01′E), during the 2- to 5- week- old chick- rearing pe-
riod in December and January 2011–2012, 2013–2014, 2014–2015
and 2015–2016. FS is a beach colony located at sea level with a
population of gannets estimated at 3,900 breeding pairs (Schuckard,
Melville, Cook, & Machovsky- Capuska, 2012).
2.2 | Nutritional composition of prey and diets and
niche breadth
Adult gannets, captured using a blunt- tip shepherd’s crook, were
banded with an individually numbered metal ring on their leg and a
unique mark on their chest using nontoxic Sharpie markers ©. These
techniques enabled us to capture and track unique individuals. Birds
were handled for <10 min and released at the edge of the colony.
This study was conducted under Sydney Animal Ethics Committee
(N00/7- 2013/3/6016), Massey University Animal Ethics Committee
(13/65) and the New Zealand Department of Conservation
( 3 5 1 8 9 - F A U ) .
Regurgitations were collected from different individuals over
four breeding seasons (2011–2012 n = 24, 2013–2014 n = 35,
2014–2015 n = 51 and 2015–2016 n = 64). As gannets are known
for transpor ting recently captured undigested prey in their proven-
triculus, we collected regurgitations as soon as they returned from
foraging to the colony (Machovsky- Capuska, Dwyer, Alley, Stockin,
& Raubenheimer, 2011) reducing the loss of prey macronutrient and
water content (Montevecchi & Piatt, 1987). Samples were collected
from spontaneous regurgitations or after a 30- s throat massage
during handling and stored in individual polythene bags at −20°C
within 5 hr of collection.
Samples were defrosted, individual prey items were weighed to
0.1 g and the total length measured to 0.1 mm prior to taxonomic
identification using published guides (Paulin, Roberts, & McMillan,
1989). Following Duffy and Jackson (1986), we calculated (a) the
mass contribution of each prey item to the total diet as a mass
percentage (M %); (b) the percentage of the total number of prey
item contributed by individuals of a particular species as a numerical
abundance percentage (N %); and (c) the percentage of gannets that
had a particular species in their diet as a frequency of occurrence
percentage (F %).
We followed the methodology established by Tait et al. (2014)
and only selected prey for proximate composition analyses with the
following characteristics: (a) undigested prey samples; and (b) from
the most representative prey items that contributed >1% (wet mass)
to the diets of gannets. Given that carbohydrate content is a min-
imal nutritional component of most marine prey (Craig, Kenley, &
Talling, 1978) and fresh water is only available to seabirds from food
moisture (Montevecchi & Piatt, 1987), the proximate composition
analysis and our comparisons are based on three essential nutrients:
protein (P), lipid (L) and moisture (hereafter water—W). All samples
were oven- dried at 60°C, ground to powder with a laboratory mill
and then weighed before laboratory analysis. Protein (estimated as
Nitrogen × 6.25) was determined using the Kjeldahl procedure (see
AOAC, 2005 for more details). The method of Mojonnier was used to
measure total lipid (hereafter lipid, AOAC, 2005). W was estimated
by drying the samples in a convection oven at 125°C and combin-
ing the water loss with the initial loss from the overnight dry- down
(AOAC, 2002). Ash was determined by ignition in a furnace at 550°C
(AOAC, 2005).
Under the MNNF (Machovsky- Capuska, Senior, Simpson et al.,
2016), we linked a well- established proportion- based approach
(right- angled mixture triangle—RMT) that enables the modelling of
nutritional niches (Raubenheimer, 2011) with a multivariate ellipse-
based Bayesian approach that generates standard ellipse areas(SEA)
to measure isotopic niche breadth from proportions (Jackson, Inger,
Parnell, & Bearhop, 2011). Following Syväranta, Lensu, Marjomäki,
Oksanen, and Jones (2013), to account for small sample sizes, we
used corrected versions of SEA (SEAc). Hence, this integrative ap-
proach was use d to measure realized nutri tional niche and prey com-
position niche breadths (SEAc).
2.3 | Foraging behaviour
Global Positioning System (GPS) data loggers were deployed on
different individual adult chick- rearing gannets during three breed-
ing seasons (2011/2012 n = 11, 2014/2015 n = 17 and 2015/2016
n = 11). Departing birds were captured immediately after adopting
the sky- pointing posture for data logger deployments, as described
in Machovsky- Capuska et al. (2014). Canmore GT- 730FL- S (Taiwan)
GPS loggers embedded in a Loksak® waterproof bag (Loksak, USA)
weighing 45 g were attached with Temflex 1610 tape to the four
central tail feathers. Following Machovsk y- Capuska et al. (2014),
loggers were programmed to record data related to position (lati-
tude, longitude and altitude), speed and time at 1- s intervals. Marked
birds were recaptured upon arrival at the colony after one foraging
trip, and loggers and tape strips were retrieved.
Gannet GPS data were speed- filtered following McConnell,
Chambers, and Fedak (1992) (removal of points >75 km/hr), and
Journal of Animal Ecology
standardized to a 2- s interval between points (minimum interval
observed in data; season 20112012), prior to analysis. Individual
foraging trips were extracted using BirdLife International’s “ma-
rine IBA R package (Lascelles et al., 2016). Previous studies have
shown that gannet dive durations are primarily between 3 and 8 s
(Machovsky- Capuska, Vaughn, Würsig, Katzir, & Raubenheimer,
2011; Machovsky- Capuska et al., 2012); in this study, dive loca-
tions were inferred from interruptions of between 3 and 8 s in
GPS signals from our high- resolution loggers since interruptions
exceeding >10 s are likely to be related to loss of satellite signal
reception (Machovsky- Capuska, Vaughn et al., 2011; Machovsky-
Capuska et al., 2014; Moseley et al., 2012; Pichegru et al., 2007).
Using the GPS data, we calculated a range of movement parame-
ters for each foraging trip including maximum distance away from
the colony (MDC), total foraging path (TFP) and foraging trip du-
ration (FTD). To investigate foraging behaviour, we applied hid-
den Markov models (HMM) to the GPS data. We constructed a
single HMM for each year of GPS tracking, including an identifier
for each trip, using the package “moveHMM” (Michelot, Langrock,
& Patterson, 2016). For each consecutive GPS point, the step
length and turning angle were calculated, producing three distri-
butions consistent with resting (slow sinuous movement), foraging
(medium speed sinuous movement) and transiting (fast directed
movement) behaviours observed in HMM studies of Sulids (Boyd,
Punt, Weimerskirch, & Bertrand, 2014; Oppel et al., 2015). The
fitted HMMs were then used to classify each GPS point as either
foraging, resti ng or transiting, and fro m this, we calculate d the for-
aging time (FT) and transiting time (TT) of each trip (Miller, Silva,
Machovsky- Capuska, & Congdon, 2018). For each gannet, we de-
fined the general use foraging area by estimating the 95% utiliza-
tion distribution (UD 95) and the prey capture area by obtaining
the 50% utilization distribution (UD 50) from kernel analysis of
their dive locatio ns (Worton, 1987). Kernels were constructed and
linked with bathymetry in the package “adeha bitat hR” (Calenge,
2006) with a grid size of 0.5 km and a smoothing parameter (h) of
5 km, identified as the most appropriate area- restricted search
scale (Lascelles et al., 2016).
2.4 | Sea surface temperature and bathymetry
Satellite- derived sea surface temperature (SST, MODIS- Aqua) at a
resolution of 0.01° × 0.01° was obtained from Giovanni data portal
( Monthly SST was acquired
within 4 km of FS colony from December 2006 to December 2016.
We obtained the mean SST during December–January of each sea-
son (2011–2012: 18.1 ± 0.3; 2013–2014: 17.9 ± 0.6; 2014–2015:
18.7 ± 0.0; and 2015–2016: 19.2 ± 1.3) compared with the 10 years
December- January SST mean (18.3 ± 1.0°C) to establish potential
warmer or colder anomalies (SSTa) in the gannet’s foraging area.
We also accessed bathymetry measurements from the New Zealand
250- m gridded bathymetric dataset using the National Institute of
Water and Atmospheric Research (NIWA) website (https://www.
2.5 | Nutritional landscapes
For each of the tracked gannets that regurgitated upon logger re-
trieval (2011–2012, n = 3; 2014–2015, n = 8; 2015–2016, n = 10),
we established nutritional landscapes” (hereafter nutriscapes), link-
ing the nutritional content of prey (wet mass protein- to- lipid ratio—
P:L) to the most likely geographic area of capture and bathymetry.
First, considering gannets’ overall high success in prey capture (72%,
Machovsky- Capuska, Dwyer et al., 2011; Machovsky- Capuska et al.,
2012), we linked each individual’s area of capture from dive loca-
tions (UD 50, estimated above) with the average wet mass P:L ratio
of prey items caught during foraging trips. Second, we then mapped
all UD 50s from each sampling year together to identify main nutris-
capes and their nutritional composition. If UD 50s from one or more
gannets overlapped, we assigned the mean nutritional value to that
nutriscape (see Supporting Information for codes).
2.6 | Data analysis
All analyses were performed in the statistical software environment
program R version 3.2.4 (R Core Team 2016). Linear and generalized
linear models (LMs and GLMs) were implemented using the “lm” and
glmfunctions, and linear mixed models (LMMs) were performed
with lme4 package (Bates, Mächler, Bolker, & Walker, 2015). Data
analysed using LMs were initially tested using Levene’s test for ho-
moscedasticity and Shapiro–Wilk’s test for normality.
Interannual differences were evaluated by fitting a 4- level cat-
egorical predictor denoting the season in which observations were
made in LM/GLM. Evaluating differences in the total number of prey
items brought to the colony between seasons, we used a quasi-
Poisson (log- link) GLM where the response was the count of each
prey species regurgitated by an individual. Variations in weight and
length between seasons of prey species were evaluated using LMs.
Weight and length of prey were log- transformed and fitted against
the categorical predictor for season.
Following Machovsky- Capuska, Senior, Benn et al. (2016), linear
mixed models (LMMs) were used to evaluate the between- species
variation (quantified as standard deviation—SD) in the proximate
composition of prey. The LMM was implemented with the “lmer”
function in the package “lme4” (Bates et al., 2015) and fitted the logit
transformation of the wet mass proportions of P, L and W, and log
ratio of the proportion of protein to lipid (lnPL) from each individual
prey item, with species ID as a random effect. The statistical sig-
nificance of between- species variance was assessed using a likeli-
hood ratio test with the “rand” function in the package lm eRtest
(Kuznetsova, Brockhoff, & Christensen, 2015).
To explore whether the nutritional composition (log wet mass
proportion of P, L and lnPL and W) of diets fluctuated over sea-
sons, we fitted a LMs with the nutritional composition of interest
(as per above) from each diet sample as the response. Seasonal dif-
ferences in SEAc were estimated via Bayesian interference (SEAb)
using Markov chain Monte Carlo simulation with 2 x 104 iterations
with 95% credible inter vals (CI) among groups (Jackson et al., 2011).
Journal of Animal Ecology
Following Pelletier, Chiaradia, Kato, and Ropert- Coudert (2014), this
method enables direct interpretations of the differences in SEAb
that we tested using LM.
Seasonal differences in habitat use and foraging behaviour pa-
rameters were evaluated by fitting an LM with a 3- level categorical
predictor for each season. Following Bonett and Wright (2000), we
performed Pearson correlations to explore possible seasonal rela-
tionships between niche breadths (SEAc) with habitat use (UD50
and UD95) and foraging behaviour (TFP and FTD).
Bathymetry differences between seasons were tested using LM.
To assess the influence of SSTa on foraging behaviour, habitat use
parameters and nutritional composition of prey (as described pre-
viously), LMs were used. Here, each outcome was fitted against the
SSTa of the time at which the observation was made (binary predic-
tor; colder or warmer than the 10 years mean). MDC, FTD, total dive
duration were log (natural)- transformed to ensure the data were
normally distributed.
Nutritional niche breadths were calculated using sibeR pack-
age (Stable Isotope Bayesian Ellipses) in R version 3.2.4. We report
parametric data as mean ± standard error (M ± SE) unless otherwise
stated. For among- season differences in outcomes, we present over-
all effects from LMs/GLMs.
3.1 | Nutritional composition of prey, diets and
niche breadth
A total of 172 regurgitations were collected over four breeding sea-
sons (Table 1). A total of 1,341 prey items were identified from these
samples, including eight species of fish kahawai Arripis trutta; bar-
racouta Thyrsites atun; garfish Hyporhamphus ihi; yellow eye mullet
Aldrichetta forsteri; yellowtail jack mackerel Trach uru s spp.; pilchard
Sardinops neopilchardus; saury Scomberesox saurus and anchov y
Engraulis australis, and arrow squid Nototodarus spp. From the total
number of regurgitations, 84.9% contained only one species of prey,
13.4% contained two species and 1.7% contained three species.
Prey items had a mean weight of 22.4 ± 1.1 g and a mean length of
13.4 ± 0.2 cm.
Of all the prey species, garfish had the highest wet mass P:L
ratio (21.4:1.0), whereas barracouta had the lowest P:L ratio (1.5:1.0,
Figure 1). The nutrient composition of the different prey species
consumed by gannets showed differences in the wet mass propor-
tions of P (estimated between- prey species SD = 0.12, χ2 = 22.7,
df = 8, p < 0.0001), L (estimated between- prey species SD = 0.64,
χ2 = 10.5, df = 8, p < 0.001), lnPL (estimated between- prey species
SD = 0.74, χ2 = 11.5, df = 8, p < 0.0001) and W (estimated between-
prey species SD = 0.03, χ2 = 53.8, df = 8, p < 0.0001). The SEAc: 9.19
combin ed with the wide range of P:L wet mass ratios in the prey co n-
sumed over four breeding seasons (from 1.5:1.0 to 21.4:1.0) provide
an estimate of breadth of the prey composition niche (Figure 1). The
realized nutritional niche breadth was also estimated by combining
SEAc: 4.65 and the P:L wet mass ratios from the diets of gannets
(from 1.5:1.0 to 15.2:1.0; Figure 1).
The number of prey items per foraging trip was significantly
different between years (GLM, F3,13 37 = 15.41, p < 0.0001), with
the greatest number observed in 2015–2016 (see Supporting
Information Table S1). The weight and length of prey items con-
sumed by gannets differed significantly between seasons (LM
weight, F3 ,1337 = 45.08, p < 0.05 and LM length, F3,1337 = 55.27,
p < 0.05), with the lightest and smallest consumed in 2015–2016
(see Supporting Information Table S1). The greater number of
prey eaten in 2015–2016 did not, however, compensate for their
smaller size, as meal sizes were significantly lighter in 2015–2016
than in other years (LM, F3,168 = 54.33, p < 0.05, see Supporting
Information Table S1). Interannual differences of the nutritional
TABLE1 Diet composition of adult chick- rearing Australasian gannets estimated from 172 dietary samples collected over four
different breeding seasons at Farewell Spit colony (New Zealand). The sample size is given after each season in brackets. M % = wet mass,
N % = numerical abundance, F % = frequency of occurrence
Season 2011–2012 Season 2013–2014 Season 2014–2015 Season 2015–2016
(n = 24) (n = 35) (n = 50) (n = 63)
M % N % F % M % N % F % M % N % F % M % N % F %
Pilchard 53.57 8 6.15 6 6.67 22.56 8.53 20.0 0 35.09 10.40 2 9.69
Anchovy 0.57 3.08 8.33 1.89 1.71 5.71 22.89 43.94 42 .00 40.67 71.71 6 7.19
Squid 12.36 3.85 16 .67 0.70 3.41 5.71 8.45 4.04 10.00 6.27 1 .94 10.94
Garfish 0. 37 1.54 4.17 4 8. 24 83 .96 60.00 46.4 0 37.37 46.00 5.90 4.99 4.69
Yellowtail jack
19.9 7 3.08 12.50 21 .94 1.71 14 .2 9 10.4 8 1 .52 6.00 — — —
Kahawai 6. 23 1.54 8.33 3. 65 0.34 2.86 — — — — —
Barracouta 6.93 0.77 4.17 — — — — — — —
Yellow Eye
— — — 1.02 0.34 2.86 11.77 13.13 10.00 — — —
Saury — — — — — — — — — 12.07 10.96 9.38
Journal of Animal Ecology
composition of diets were significant for the wet mass propor-
tion of P (LM, F3,168 = 20.63, p < 0.0001), L (LM, F3,168 = 23.14,
p < 0.0001), W (LM, F3,168 = 5.35, p < 0.001) and lnPL (LM,
F3,168 = 27.71, p < 0.0001). Differences between years were also
observed in the breadth dimensions of the prey composition
niches (LM, F3 ,15996 = 29230, p < 0.0001) and the realized nutri-
tional niches (LM, F3,15996 = 50710, p < 0.0001; Figure 2, also see
Supporting Information Table S2).
3.2 | Foraging behaviour
A total number of 39 foraging trips were collected from birds car-
rying GPS data loggers (Table 2). The foraging habitat ranged from
1,100.89 to 1,374.24 km2 for UD95 and from 222.54 to 273.05 km2
for UD50 (Table 2), with no difference detected between breeding
seasons (UD50, LM, F2,36 = 0.95, p = 0.33 and UD95, LM, F2,36 = 2.04,
p = 0.16; Table 2).
The mean MDC that gannets travelled away from the colony
was 56.1 ± 4.5 km (Table 2). Gannets showed the longest FTD
in 2015–2016 (LM, F2,36 = 4.60, p < 0.05) and spent almost 25%
more time foraging (LM, F2, 36 = 6.16, p < 0.01) in deeper areas than
during other study years (LM, F2,36 = 5.82, p < 0.01). Total dive du-
ration showed that longest dives were recorded in 2011–2012 (LM,
F2,36 = 3.42, p < 0.05). No significant differences between seasons
were observed in the MDC (LM, F2,36 = 1.31, p = 0.28) and in the
TFP (LM, F2,36 = 0.42, p = 0.66; Table 2). Although nonsignificant,
negative seasonal trends were found between realized nutritional
niche breadths with foraging behaviour and habitat use parameters
(SEAc and UD50, Pearson r = −1.00, p < 0.05, n = 6; SEAc and UD95,
Pearson r = −0.81, p = 0.40, n = 6; SEAc and TFP, Pearson r = −0.98,
p = 0.13, n = 6 and SEAc and FTD, Pearson r = −0.93, p = 0.24, n = 6).
3.3 | Sea surface temperature anomalies
Strong negative indices (colder water than average) were re-
corded in 2013–2014 (December–January: −0.5°C) and 2011
2012 (December–January: −0.3°C), whereas strong positive
values (warm water than average) were recorded in 2014–2015
(December–January: +0.4°C) and 2015–2016 (December–January:
Foraging behaviour and habitat used were influenced by SSTa.
During warmer water periods (positive SSTa), gannets increased
their foraging habitat UD95 (km2), maximum distance to the col-
ony (km), foraging trip duration (hr), foraging path length (km),
transiting and foraging times (hr) and bathymetry depth prefer-
ence (m), whereas during colder water periods (negative SSTa),
FIGURE1 Right- angled mixture triangle (RMT) showing
foraging choices of chick- rearing adult Australasian gannets
at Farewell Spit colony. Nutritional composition of prey (grey
hollow circles) and diets (black solid symbols). Each prey and
diet represents a proportional mixture of protein (P), lipid (L) and
water (W). To geometrically define prey and diets in an RMT, % P
is plotted against % L. Considering that the three components in
the mixture sum to 100%, plotting % P (first axis) and % L (second
axis) will automatically reflect the value of % W in the third axis
(Raubenheimer, 2011). The prey composition niche (all the prey
consumed by gannets, Machovsky-Capuska, Senior, Simpson et al.
2016) breadth is measured as the area of standard ellipse (SEAc:
9.19, grey solid ellipse). The realized nutritional niche breadth of
gannets (all individual diets from the four breeding seasons studied
(2011–2012: triangle, 2013–2014: square, 2014–2015: diamond
and 2015–2016: circle)) is measured as the area of standard ellipse
(SEAc: 4.65, black dotted ellipse)
FIGURE2 Interannual differences in the nutritional niche breadth
of Australasian gannets. The box plot shows the credible interval
(CI) range for the estimated ellipse area (SEAb) for prey composition
niches and realized nutritional niches (diets) across seasons.
Boxed areas represent the 50%, 75% and 95% credible intervals
for the estimated ellipse areas. Black dots and the black crosses
represent the mode of SEAb and the maximum likelihood estimates
SEAc, respectively. All boxed areas denote significant difference
(p < 0.0001) [Colour figure can be viewed at]
Journal of Animal Ecology
gannets showed a significant increase in total dive duration (s;
Table 3). SSTa also influenced the nutritional composition of prey
and diets consumed by gannets. During colder water periods (neg-
ative SSTa), prey species and gannet diets revealed higher wet
mass pr opo r tio ns of P an d L and lower lnPL th an in wa rme r peri ods
(positive SSTa, Table 4).
3.4 | Nutritional landscapes
The nutriscapes varied in the nutritional composition of prey, geo-
graphic location and bathymetry over the seasons studied. The wet
mass P:L ranged from 7.26 to 13.0 in 2011–2012, 6.06 to 15.28 in
2014–2015 and 6.50 to 11.52 in 2015–2016. Gannets dived pre-
dominantly in shallow waters (0–50 m) during 2011–2012, moving
to deeper areas (50–100 m) in 2014–2015 and in 2015–2016 (50–
150 m; Figure 3).
There were no differences between tracked birds with and with-
out regurgitations in MDC (LM, F1,37 = 1.66, p = 0.20), FTD (LM,
F1,37 = 1.57, p = 0.48) and bathymetry (LM, F1,37 = 1.40, p = 0.24),
suggesting that the nutriscapes proposed for each breeding season
are representative for the wider tracked population. However, as a
consequence of lower sample size of tracked birds that regurgitated,
the UD50 of nutriscapes did not fully overlap with the UD50 of the
wider tracked population (Figure 3).
A mechanistic understanding of the species’ niche, including physi-
ology and especially behaviour, is critical to predict how they will
adjust to novel circumstances such as environmental fluctuations
(Kearney, 2006). A useful and robust measure of dietary niche shape
and breadth should contemplate the following factors: (a) the range
of prey consumed; (b) the evenness of prey components in the diet
over time; (c) foraging behaviour and geographic location (Bearhop,
Adams, Waldron, Fuller, & MacLeod, 2004); (d) nutritional composi-
tion of prey and diets; and (e) the influence of environmental fluctua-
tions (e.g. SSTa; Machovsky- Capuska, Senior, Simpson et al., 2016).
Therefore, our study yielded several novel insights into the nutri-
tional niche of gannets at different scales. First, we characterized
the prey composition and the realized nutritional niches and provide
evidence of their seasonal fluctuations in shape and breadth (Criteria
a, b and d above). Second, we demonstrated the importance of link-
ing foraging behaviour and the influence of environmental condi-
tions (SSTa) with nutritional niche theory (Criteria c and e).
4.1 | Measuring nutritional niches
The ecological niche concept has been fundamental to ecology since
its development fifty years ago (Chase & Leibold, 2003). Although
considerable effort has gone into defining, measuring and quanti-
fying the ecological niche, the concept remains poorly character-
ized (Feinsinger, Spears, & Poole, 1981; Kearney, 2006; Kearney,
Simpson, Raubenheimer, & Helmuth, 2010). While nutritional niches
have often been described using carbon and nitrogen either in the
form of isotope ratios (Newsome et al., 2007) or concentrations in
food items (González, Dezérald, Marquet, Romero, & Srivastava,
2017), the biological and physiological assumption that these con-
centrations are surrogate of lipids, proteins and carbohydrates may
often be incorrect (Raubenheimer et al., 2009; Wilder & Eubanks,
A growing body of evidence suggests that vertebrate predators
consume prey that varies in their nutritional and energetic composi-
tions (Lenky, Eisert, Oftedal, & Metcalf, 2012; Machovsky- Capuska,
Coogan, Simpson, & Raubenheimer, 2016; Machovsky- Capuska,
Priddel et al., 2016; Malinowski & Herzing, 2015; Mayntz et al.,
Parameter 2011–2012 2014–2015 2015–2016
Foraging habitat
Sample size (N)11 17 11
UD95 Individuals
1,100.89 ± 247.06 1,367.41 ± 432.46 1,374.24 ± 473.39
UD50 Individuals
222.54 ± 83.36 238.99 ± 65.48 273.05 ± 131.00
Bathymetry (m) 44.86 ± 65.15 74.78 ± 28.84 90.65 ± 25.94
Foraging trip characteristics
Max. distance to
colony (km)
44.93 ± 9.27 60.52 ± 7.48 57.24 ± 5.79
Total foraging path
227.91 ± 64.72 262.64 ± 35.21 289.55 ± 27.55
Foraging trip duration
14.71 ± 3.71 14.88 ± 2.34 26.36 ± 2.97
Transiting time (hr) 2.27 ± 1.75 1.82 ± 1.94 3.34 ± 2.82
Foraging time (hr) 2.97 ± 2.45 3.09 ± 3.45 4.21 ± 3.48
Total dive duration (s) 6.26 ± 0.87 3.66 ± 0.46 5.25 ± 0.63
TABLE2 Foraging habitat and trip
characteristics of adult chick- rearing
Australasian gannets at Farewell Spit
colony over three different breeding
seasons. Data presented as
mean ± standard error (M ± SE)
Journal of Animal Ecology
2009). Here, we demonstrated that there is an appreciable variation
in the proportional wet mass contribution of P, L, W and PL ratio
in the prey species consumed by gannets, which is consistent with
previous findings on gannet prey species (Machovsky- Capuska,
Senior, Benn et al., 2016; Tait et al., 2014). These results further
support previous suggestions on the importance of nutrient content
rather than just energetic value of prey alone (Machovsky- Capuska,
Coogan et al., 2016). As expected, the differences in the nutritional
values of prey were then translated into seasonal fluctuation in the
breadth (SEAc) of both the prey composition niche and realized nu-
tritional niche.
As a best practice to characterize and measure prey composition
and realized nutritional niches, we suggest the use of SEAc combined
with nutritional ratios. However, as is generally true of measuring
niches in wild populations (Chase & Leibold, 2003; Raubehneimer
et al., 2015), careful consideration needs to go into sampling design,
including how diet is measured, and the sampling effort required to
make reliable estimates of diet breadth. There is no simple answer to
these questions; each needs to be addressed in relation to the details
of particular study systems and research aims.
In our study, we were able to measure diet by soliciting regurgi-
tations from parent birds when they returned to the nest from for-
aging. A peculiarity of this method is that regurgitations can combine
foods that would contribute to the diet of the parents with those
that would be provisioned to chicks (Ropert- Coudert et al., 2004).
There is no easy way of distinguishing these, and consequently, the
use of regurgitations can be problematic in studies that aim to as-
sess the dietary composition of reproducing adults or of their chicks.
The use of regurgitations does not, however, compromise studies
that aim to enumerate dietary niches. This is because the niche con-
cept refers to the resources required to maintain the population, in-
cluding all stages of the life cycle (Pulliam, 2000). Indeed, sampling
Parameter SS Ta− SS Ta+ LM p
Protein 20.88 ± 0.25 19.79 ± 0.32 F = 15.66 <0.001
Lipid 2.68 ± 0.29 2.03 ± 0.16 F = 4.39 <0.01
Water 72.16 ± 0.42 73.68 ± 0.37 F = 3.1 2 <0.05
LnPL 2.22 ± 0.13 2.47 ± 0.16 F = 8.82 <0.001
Protein 21.71 ± 0.17 20.06 ± 0.13 F = 3.62 <0.01
Lipid 2.89 ± 0.21 2.25 ± 0.06 F = 20.3 0 <0.0001
Water 73.64 ± 0.30 75.70 ± 0.11 F = 0.34 0.56
LnPL 2.11 ± 0.07 2.36 ± 0.11 F = 20.20 <0.0001
TABLE4 Linear models (LM) testing
the interactions between sea surface
temperature anomaly (SSTa) on the
nutritional composition of prey and diets
(wet mass proportions of P, L, W and lnPL)
of adult chick- rearing Australasian
gannets. SSTa−: colder water periods and
SSTa+: warmer water periods. Data
presented as mean ± standard error
(M ± SE). Significant differences marked in
Parameter SS Ta− SS Ta+ LM p
Foraging habitat
UD95 Individuals
1,110.89 ± 100.86 1,367.41 ± 101.93 F = 3.72 <0.05
UD50 Individuals
222.53 ± 34.03 241.48 ± 17.89 F = 0 .71 0.40
Bathymetry (m) 52.23 ± 17.31 88.72 ± 3.29 F = 4.64 <0.01
Foraging trip characteristics
Max. distance to
colony (km)
58.26 ± 8.32 74.91 ± 5.52 F = 6.71 <0.01
Total foraging path
251.41 ± 22.98 295.09 ± 22.47 F = 4.38 <0.01
Foraging trip
duration (hr)
13.51 ± 3.46 21.34 ± 1.79 F = 5.74 <0.01
Transiting time (hr) 2.59 ± 0.67 4.09 ± 0.40 F = 5.26 <0.01
Foraging time (hr) 3.37 ± 0.96 5.71 ± 0.62 F = 5.61 <0.01
Total dive duration
4.75 ± 0.49 2.67 ± 0.07 F = 55.34 <0.0001
TABLE3 Linear models (LM) testing
the interactions between sea surface
temperature anomaly (SSTa) on foraging
habitat and foraging behaviour. SSTa−:
colder water periods and SSTa+: warmer
water periods. Data presented as
mean ± standard error (M ± SE). Significant
differences marked in bold
Journal of Animal Ecology
regurgitations that might have consisted of both adult and chick
foods was a benefit in our study, because this approach efficiently
encompasses the diets of both stages of the life cycle.
The question of sampling effort is particularly relevant to
demonstrating that a species is a dietary specialist. To establish di-
etary specialism, it would need to be demonstrated that the range
of foods eaten is not an artefact of local or otherwise insufficient
sampling, but rather a true reflection of the species’ biology. This
could be done either by ensuring that sampling effort is adequate
to establish an accurate measure of diet or by demonstrating that
the animals feed selectively from a broad range of prey options. In
contrast, if the data suggest that a population has a broad dietary
range, it is extremely unlikely that additional sampling or measuring
food availability will suggest that the animal is in fact a dietary spe-
cialist, although additional sampling might of course further expand
the documented dietary range.
We are confident that the sampling regime in our study has pro-
vided a reliable and unique representation of the prey composition
(wet mass P:L from 1.5:1.0 to 21.4:1.0 and SEAc: 9.19) and real-
ized nutritional niches (wet mass P:L from 1.5:1.0 to 15.2:1.0 and
SEAc: 4.65) of gannets from the study population. First, our data on
prey and diet compositions over four seasons are consistent with
a previous study of five- year diet in gannets at Farewell Spit col-
ony (Schuckard et al., 2012). Second, the range of macronutrients
that we recorded in prey and diets consumed by gannets comprises
most of the spectrum of marine fish wet mass concentrations of lipid
(0.2%–25.0%) and protein (17.0%–25.0%; Stansby, 1969; Santhanam,
2014), and it is thus unlikely that further sampling would have sig-
nificantly expanded this. The data therefore strongly suggest that
gannets are generalists at prey composition and macronutrient lev-
els, similar to Argentine ants Linepithema humile and wild boars Sus
scrofa (Machovsky- Capuska, Senior, Simpson et al., 2016; Senior,
Grueber, Machovsky- Capuska, Simpson, & Raubenheimer, 2016,
4.2 | Variables that shape the nutritional niche
It has been suggested that a decrease in food abundance will
cause individuals to increase their time spent foraging and shift
their diet, and pursue different resources influencing niche width
expansion in a population (Ceia et al., 2014; Svanbäck & Bolnick,
2007). If only the amount of prey and their energy value are the
main drivers of foraging (Stephens & Krebs, 1986), we would ex-
pect to have seen that gannets increased their foraging effort and
niche breadth (SEAc) under reduced prey availability. However,
our MNNF showed that in 2011–2012 gannets had the wides t prey
composition niche and realized nutritional niche while spending
the shortest amount of time foraging closer to the colony (MDC),
whereas in 2015–2016, they exhibited their narrowest prey com-
position and realized nutritional niche breadths while spending
more time searching for food (TFP) and foraging (hr). A likely expla-
nation is that both patterns are subject to nonexclusive effects of
prey availability and nutritional composition, although this remains
to be established.
Variation in prey distribution, densities and quality at sea is
driven by environmental factors, oceanographic processes and
bathymetric features (Garthe, Montevecchi, Chapdelaine, Rail, &
Hedd, 2007; Weimerskirch, Gault, & Cherel, 2005). SST anomalies
are known to drive spatial and temporal changes in the availability of
pelagic prey (Montevecchi & Myers, 1997; Perry et al., 2005). These
movements are often linked to primary production events (Becker,
Peery, & Beissinger, 2007) and also fish searching for suitable hab-
itats while adjusting their thermal tolerance to survive (Bates et al.,
2014). During warm water events (strong positive SSTa values), gan-
nets increased their foraging habitat (UD95, km2), foraging trip dura-
tion (hr) and total foraging path (km). This is consistent with previous
suggestions that warm water events reduce primary production
and negatively influence prey availability (Becker et al., 2007), im-
posing greater travel costs (time and distance) upon the forager and
FIGURE3 Foraging habitat and dive locations of adult chick- rearing Australasian gannets from Farewell Spit colony (New Zealand, green
diamond) during three chick- rearing seasons: (a) 2011–2012, (b) 2014–2015 and (c) 2015–2016. Kernel density utilization distributions (UD)
show habitat used (UD95: dotted lines) and prey capture areas (UD50: solid lines). Nutriscapes linking nutritional content of prey (wet mass
protein- to- lipid ratios—P:L) to the most likely geographic area of captured (coloured areas) and bathymetry. Isobaths expressed in metres (m)
Journal of Animal Ecology
likely influencing their offspring (Fritz, Said, & Weimerskirch, 2003;
Grémillet et al., 2004).
Although climate fluctuations are known to influence prey qual-
ity in marine (Österblom et al., 2008; Wanless, Harris, Redman, &
Speakman, 2005) and terrestrial environments (Raubenheimer,
Machovsky- Capuska, Chapman, & Rothman, 2015; Rothman et al.,
2015), the mechanisms behind these effects are probably complex
and remain unknown. In our study, strong warm water events neg-
atively influenced the nutritional composition of prey species (wet
mass proportions of P and L) and also diets consumed by gannets.
The likely explanation is that the gannets’ main prey are small an-
chovy, pilchard and gar fish that feed mostly on plankton (Schuckard
et al., 2012) and respond to regional plankton blooms under
nutrient- rich conditions (Hunt et al., 1998; Paul, Taylor, & Parkinson,
2001). However, warmer waters are often more stratified and char-
acterized by nutrient limitation and reduced plankton productivity
(Behrenfeld et al., 2006; Richardson & Schoeman, 2004). Thus, de-
clines in nutrient availability strongly influence population structure,
size, biomass and quality of prey species with subsequent implica-
tions on the trophic webs (Fuchs & Franks, 2010).
Foraging animals, in the laboratory and the wild, link their
movements to the distribution of their food sources (Masello, Kato,
Sommerfeld, Mattern, & Quillfeldt, 2017). Understanding the fac-
tors that make a place a foraging “hot- spot” is vital to unravel the
drivers of prey preferences in marine predators. We present un-
precedented evidence in the form of nutriscapes, linking the nu-
tritional composition with the geographic location of prey capture
areas (UD50) of foraging gannets. Over the three seasons studied,
the nutriscapes were patchily distributed, fluctuated from shallow to
deeper areas and had different nutritional composition; clearly, the
temporal extent of this dataset and the proposed approach brings
a novel opportunity to better understand whether the prey con-
sumed by wild predators could be supplementar y (similar P:L ratios
across prey) or complementary (different P:L ratios) with respect to
the diet. Thus, this approach could become the stepping stone for
research of foraging strategies in marine predators by investigating
habitat use and food patch selection and depletion in relation to prey
and diet composition and nutrition as previously seen in Guerezas
Colobus guereza (Johnson et al., 2017).
Bearing in mind that prey and geographic location were ob-
tained from foraging gannets arriving to colony, nutriscapes
should not be considered as a surrogate for qualitative or quan-
titative prey availability. From our point of view, in spite of the
small sample size presented herein, this novel approach provides
a unique opportunity to reconstruct foraging behaviours and hab-
itat use linked with geographic location, abiotic factors (e.g. salin-
ity, chlorophyll, sea surface temperature, bathymetry and others)
and temporal measures of resource acquisition quantified as spe-
cific nutrients. The use of bio- logging sensors including animal-
borne video and environmental data collection systems (AEVDs)
combined with NG has been proven to yield new insights into
marine wild predator nutritional ecology (Machovsky- Capuska,
Priddel et al., 2016) and could be vital to enhance the resolution
an d the expa nsio n on the use of nu t ris cap es. Thi s cuttin g- edge ap -
pro ach co uld contribute to either marine, fre shwater or terrestrial
environments, playing a fundamental role in assessing nutritional
decisions based on the nutritional composition of a wide range of
species in the wild. Nutriscapes can provide fresh insights into a
wide range of research fields including (a) predicting the distri-
bution and expansion of invasive species; (b) understanding the
dietary needs and the nutritional composition and availability of
habitats for endangered species; (c) exploring critical habitats for
species translocations; (d) understanding the location and nutri-
tional value of geographic areas prone to human–wildlife conflict
(e.g. fisheries); and (e) unravelling travelling routes for migratory
species based on nutrient composition and availability.
Dietary generalism has been suggested to evolve in hetero-
geneous environments, whereas specialism is a response to a ho-
mogeneous environment (Senior, Nakagawa, Lihoreau, Simpson,
& Raubenheimer, 2015). Overall, our study suggest s that gannets
(a) display a high degree of prey and diet composition generalism,
being able to prey upon species that vary in nutritional compo-
sition, and have a wide nutritional range in their diets; (b) across
seasons, nutritional landscapes varied in prey composition, over
space, time and bathymetry; and (c) during warm water events
(strong positive SSTa), gannets expanded their foraging habitat,
increased their foraging trip duration while consuming prey and
diets low in nutritional composition. Our results highlight the im-
portance of quantifying and characterizing the prey composition
and realized nutritional niches to test broader ecological ques-
tions to better understand the extent of dietary generalism in
the wild.
We thank M Ogle, W Cook, J and V Melville, P Jones, EC Benn,
K Barna, C Rowe, C Purvin, D Cooper and L Angel for their assistance
during fieldwork. Special thanks to PHW Leong and P Jones for sup-
port on the technical issues with the GPS data loggers, R Waern
for assistance with R software, and J. Hewitt and B. Würsig for
valuable comments that enhanced early versions of the manuscript.
I Tuck provided guidance on how to access SST data. Aspects of this
work were funded by Faculty of Veterinary Science DVC compact
fund (The University of Sydney). The Department of Conservation,
Golden Bay (New Zealand), kindly allowed the use of their house
at Farewell Spit and also assisted on the transport of the field gear.
GEM- C is supported by the Loxton research fellowship from the
Sydney School of Veterinary Science, The University of Sydney.
G.E.M.- C., F.R.O.S., R.S. and D.M. collected the data. G.E.M.- C.,
M.G.R.M., F.R.O.S., C.A., K.A.S., D.R. and A.M.S. analysed the data.
G.E. M.- C., F.R .O.S ., K. A .S., M.G.R.M., A.M. S. and D.R. wrote an d ed-
ited the manuscript. G.E.M.- C. designed the study. The authors do
not have any conflict of interest to declare.
Journal of Animal Ecology
Data used in this manuscript are available from Pangea® D at a R e p os it o r y : (Machovsky-
Capuska et al., 2018).
Gabriel E. Machovsky-Capuska ht tp://o r c i d .
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How to cite this article: Machovsky-Capuska GE, Miller MGR,
Silva FRO, et al. The nutritional nexus: Linking niche, habitat
variability and prey composition in a generalist marine
pred ator. J Anim Ecol. 2018;87:1286–1298.
... Several studies on seabirds (Machovsky-Capuska et al., 2018;Machovsky-Capuska and Raubenheimer, 2020), preda-tory fish , turtles (Machovsky-Capuska et al., 2020a;Santos et al., 2020), cetaceans (Denuncio et al., 2017;Machovsky-Capuska and Raubenheimer, 2020;Machovsky-Capuska et al., 2020b), pinnipeds (Machovsky-Capuska and Denuncio et al., 2021), and sharks (Machovsky-Capuska and Grainger et al., 2020), have increasingly applied the MNNF to (i) understand how marine predators adjust their foraging behaviour and nutritional goals to environmental fluctuations (Machovsky-Capuska et al., 2018); (ii) explore the nutritional consequences of consuming plastics and anthropogenic pollutants (Machovsky-Capuska et al., 2019, 2020aSantos et al., 2020Santos et al., , 2021Stockin et al., 2021a, b); and (iii) disentangle the dynamics that facilitates coexistence with other sympatric species (Denuncio et al., 2021), and examine how they are likely to interact with humans (Grainger et al., 2020). ...
... Several studies on seabirds (Machovsky-Capuska et al., 2018;Machovsky-Capuska and Raubenheimer, 2020), preda-tory fish , turtles (Machovsky-Capuska et al., 2020a;Santos et al., 2020), cetaceans (Denuncio et al., 2017;Machovsky-Capuska and Raubenheimer, 2020;Machovsky-Capuska et al., 2020b), pinnipeds (Machovsky-Capuska and Denuncio et al., 2021), and sharks (Machovsky-Capuska and Grainger et al., 2020), have increasingly applied the MNNF to (i) understand how marine predators adjust their foraging behaviour and nutritional goals to environmental fluctuations (Machovsky-Capuska et al., 2018); (ii) explore the nutritional consequences of consuming plastics and anthropogenic pollutants (Machovsky-Capuska et al., 2019, 2020aSantos et al., 2020Santos et al., , 2021Stockin et al., 2021a, b); and (iii) disentangle the dynamics that facilitates coexistence with other sympatric species (Denuncio et al., 2021), and examine how they are likely to interact with humans (Grainger et al., 2020). ...
... Following Machovsky-Capuska et al. (2016a), the variety of prey compositions eaten are known as prey composition niche, whereas the diets composed of consuming different prey are known as realized nutritional niches. To estimate the prey composition and realized nutritional niche breadths of dolphins and gannets from proportional data, we combined the MNNF with standard ellipse areas for small sample sizes (SEAc, Syväranta et al., 2013), following Machovsky-Capuska et al. (2018). ...
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.
... In accordance with this theory, seabirds can adjust their foraging strategies in response to extrinsic and intrinsic factors. They can thus switch their diet to prey that are more accessible (more abundant and/or closer to their nesting grounds), temporally available or more energetic/nutrient-rich (Quillfeldt 2002;Navarro et al. 2009;Machovsky-Capuska et al. 2018). They can also forage at more or less distant and/or large areas Ramos et al. 2018;Cerveira et al. 2020), and/or utilise different foraging habitats (Quillfeldt et al. 2005;Navarro et al. 2007;Cherel et al. 2014a;Geary et al. 2020). ...
... Finally, seabird foraging strategies can also differ between sexes (e.g. Forero et al. 2005;Bearhop et al. 2006;Miller et al. 2018;Zango et al. 2020). While this may reflect sexual habitat or dietary specialization or avoidance of competition in sexually dimorphic species, this may result from sexually differing reproductive roles, parental investment, nutritional requirements or from risk partitioning in monomorphic or dimorphic species (Phillips et al. 2011;. ...
Full-text available
Flexibility in foraging strategy is an important mechanism by which seabirds cope with spatiotemporal heterogeneity in food availability and the variable energetic constraints of their annual life cycle. Foraging strategy flexibility was investigated in the grey-faced petrel Pterodroma gouldi breeding on Ihumoana Island (36°53′S, 174°26′E) using stable isotope analyses. Intra- and inter-annual variations in stable isotope values, isotopic niches and diet inferred from isotope mixing models were studied by analysing δ15N and δ13C in adult wing feathers and blood, chick down and body feathers, and muscle from spontaneously regurgitated prey, collected during 2013 and 2014 breeding seasons. Grey-faced petrels exhibited variations in stable isotopes, isotopic niches and diet more markedly throughout their annual life cycle than between years. A trophic segregation occurred between adults and chicks presumably from adults feeding inshore and chicks being fed more oceanic prey of higher trophic level. Stable-isotope mixing models revealed that adult diet during the breeding season could consist mainly of ram’s horn squids Spirula spirula and chick diet of crustaceans, fish and other cephalopods being secondary prey throughout the breeding season. Adult male and female isotopic niches slightly differed. Finally, isotopic niche in adults during non-breeding was similar to that during breeding, suggesting non-breeding foraging areas located off the eastern Australian coast, around the limit between the Tasman and Coral seas. Our results demonstrated plasticity in the foraging strategy of grey-faced petrels in response to the changing nutritional demands of their annual cycle and to changes in oceanographic conditions likely driven by El Niño Southern Oscillation.
... However, to my knowledge, only one of these studies - Barger & Kitaysky (2012) -presented empirical evidence of seabird species contracting their spatial and dietary axes of their realized niches in response to low prey abundance. In contrast, other studies, which focus on a single seabird or marine mammal species, have found that in response to decreased prey availability, the species expanded their spatial and/or dietary axis of their realized niches by increasing the diversity of prey eaten or habitats foraged within (Elorriaga-Verplancken et al. 2016;Choy et al. 2017;Horswill et al. 2017;Machovsky-Capuska et al. 2018;Chiu-Werner et al. 2019). ...
... Already, there is much evidence that in response to climatically induced variability in resource availability, depending on the species and location of its colony, seabirds and seals can either switch their diet to temporally available prey (e.g. Chambellant et al. 2013;Reisinger et al. 2018b;Carpenter-Kling et al. 2019a;Mills et al. 2020), utilize different foraging habitats (Kowalczyk et al. 2015;Manugian et al. 2015;Machovsky-Capuska et al. 2018;Phillips et al. 2019) or attempt to follow the distribution of their preferred prey resources (Kappes et al. 2010;Pettex et al. 2012;Bost et al. 2015;Thorne et al. 2015). However, even if this behavioural plasticity is evident within a species, suitable foraging habitats can still become inaccessible or energetically costly to reach (e.g. ...
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Marine ecosystems are experiencing rapid changes due to climate change. The associated temporal and spatial changes in resource distribution impacts on the foraging behaviour of marine top predators. If these changes negatively affect the ability of marine predators to forage efficiently, there may be dire consequences for their populations. However, evidence of foraging plasticity during adverse conditions, or generalist foraging behaviour, can allow inference about the resilience of species to environmental change and provide essential knowledge towards effective and proactive conservation measures. I examined plasticity in the trophic ecology of 12 marine predator species breeding on Marion Island, southern Indian Ocean, over three years (2015 – 2018), a period characterized by pronounced environmental variability. Firstly, I correlated behavioural states inferred along the GPS tracks of incubating wandering, grey-headed, sooty and light-mantled albatrosses to environmental variables that are indicative of biologically productive oceanographic features. Secondly, I analysed δ13C and δ15N blood values in 12 marine predator species (the afore-mentioned albatrosses as well as king, gentoo, macaroni and eastern rockhopper penguins, northern and southern giant petrels and Antarctic and sub-Antarctic fur seals) over two seasons: summer and autumn. My results revealed that the foraging behaviour of all the species is, to some degree, either plastic (temporally variable isotopic niche) or general (large isotopic niche which remained similar over time), except for the king penguin (small isotopic niche which remained similar over time), a known foraging specialist. Furthermore, despite their dynamic foraging behaviour, resource partitioning among the predators was maintained over time. Due to the ease and relatively low cost of collecting tissues for stable isotope analysis it has the potential to be a powerful tool to monitor the trophic ecology of marine predators. I thus used my simultaneously collected dataset of GPS tracks with the stable isotope blood compositions to investigate some of the assumptions underlying the inferences made from marine predator δ13C and δ15N blood values. I reconstructed species- and guild- specific δ13C and δ15N isoscapes for eight seabird species. Following this, I coupled individual-based movement models of northern giant petrels with global marine isotope models to explore the sensitivity of tissue δ13C values to a range of extrinsic (environmental) and intrinsic (behavioural, physiological) drivers. My results demonstrate the strong influence of reference isoscapes on the inference of stable isotope compositions of marine predators. Furthermore, I show that caution should be used when using non-species-specific or temporally inaccurate isoscapes. I furthermore demonstrate that biological interactions, such as competition for food resources, either past or present, as well as spatio-temporal distribution of food patches strongly influence the foraging behaviour of marine predators. These findings highlight the importance of integrating biological interactions in species distribution models which are used to predict possible distributional shifts of marine predators in the context of global changes. My thesis further developed previously available methods and presents a novel approach to investigate sources of variance in the stable isotopic composition of animals’ tissues.
... Understanding a species diet composition is an integral component in learning about their life history. Species' diet corresponds directly to various aspects of their ecology, including habitat preference (Machovsky-Capuska et al., 2018;de Almeida-Rocha et al., 2020), predators (Ward-Fear et al., 2020) and pathogens (Valtonen et al., 2010). When comparing two species diet breadths, it is possible to distinguish if they are in competition and to what degree they overlap (Sutherland, 2011;Mollov et al., 2012). ...
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In this study we investigated the urbanised diets of Rhinella diptycha, Hemidactylus mabouia, and Tropidurus torquatus in Pilar, Paraguay. To retrieve stomach contents, we dissected the faecal matter of juvenile R. diptycha (n = 43), H. mabouia (n = 128) and T. torquatus (n = 50) and stomach flushed adult R. diptycha (n = 85). The three most abundant orders of prey by volume for each of the study species were R. diptycha: Coleoptera (41.14%), Formicidae (27.9%), Hemiptera (3.85%); H. mabouia: Orthoptera (29%), Coleoptera (11.66%), Hemiptera (6.31%), and T. torquatus: Coleoptera (38.36%), Formicidae (14.34%), Orthoptera (13.23%). We found dietary overlap between the invasive H. mabouia and native T. torquatus, suggesting the possibility of detrimental intraguild competition for the native species. Furthermore, we believe that these species adaptations to an urbanised lifestyle was the primary driver to their diet composition.
... The pre-moult distribution of African penguins departing from Dassen Island and Bird Island showed significant inter-annual variability. Plastic foraging distributions during the pre-and post-moult stages has [79][80][81][82][83][84] . The marine environment is highly dynamic with numerous biophysical factor determining the spatiotemporal distribution of prey 85 . ...
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The population of the Endangered African penguin Spheniscus demersus has decreased by > 65% in the last 20 years. A major driver of this decrease has been the reduced availability of their principal prey, sardine Sardinops sagax and anchovy Engraulis encrasicolus. To date, conservation efforts to improve prey availability have focused on spatial management strategies to reduce resource competition with purse-seine fisheries during the breeding season. However, penguins also undergo an annual catastrophic moult when they are unable to feed for several weeks. Before moulting they must accumulate sufficient energy stores to survive this critical life-history stage. Using GPS tracking data collected between 2012 and 2019, we identify important foraging areas for pre- and post-moult African penguins at three of their major colonies in South Africa: Dassen Island and Stony Point (Western Cape) and Bird Island (Eastern Cape). The foraging ranges of pre- and post-moult adult African penguins (c. 600 km from colony) was far greater than that previously observed for breeding penguins (c. 50 km from colony) and varied considerably between sites, years and pre- and post-moult stages. Despite their more extensive range during the non-breeding season, waters within 20 and 50 km of their breeding colonies were used intensively and represent important foraging areas to pre- and post-moult penguins. Furthermore, penguins in the Western Cape travelled significantly further than those in the Eastern Cape which is likely a reflection of the poor prey availability along the west coast of South Africa. Our findings identify important marine areas for pre- and post-moult African penguins and support for the expansion of fisheries-related spatio-temporal management strategies to help conserve African penguins outside the breeding season.
... Nutrients have the potential to influence communities and ecosystems by influencing the processes underpinning ecological interactions, such as foraging behaviour and physiology (Elser et al., 1998;Machovsky-Capuska, Coogan, Simpson, & Raubenheimer, 2016;Machovsky-Capuska et al., 2018;Potter, Stannard, Greenville, & Dickman, 2018). Certainly, the importance of nutrients for interactions has been demonstrated at various scales of organisation; for example, from the interactions between individual social insects up to the collective behaviour of superorganisms (Lihoreau et al., 2015(Lihoreau et al., , 2014(Lihoreau et al., , 2017. ...
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Nutrients are a critical driver of species interactions (e.g., plant-herbivore, predator-prey and host-parasite) but are not yet integrated into network ecology analyses. Ecological concepts like nutrient-specific foraging and nutrient-dependent functional responses could provide a mechanistic context for complex ecological interactions. These concepts in turn offer an opportunity to predict dynamic network processes such as interaction rewiring and extinction cascades. Here, we propose the concept of nutritional networks. By integrating nutritional data into ecological networks, we envisage significant advances to our understanding of ecological dynamics from individuals to ecosystem scales. We summarise the potential influence of nutrients on the structure and complexity of ecological networks, with specific reference to niche partitioning, predator-prey dynamics, spatiotemporal patterns and robustness. Using an empirical example of an inter-specific trophic network, we show that networks can be constructed with nutritional data to illuminate how nutrients may drive ecological interactions in natural systems. Throughout, we identify fundamental ecological hypotheses that can be explored in a nutritional network context and highlight methodological frameworks to facilitate their operationalisation.
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.
Description of animals’ trophic niches help us understand interactions between species in biological communities that are not easily observed. Analyses of macronutrient niches, i.e. the range of macronutrient (protein:lipid:carbohydrate) ratios selected by generalist feeders, may be a useful alternative approach to inter‐species comparisons of diets, especially within taxonomic assemblages of predators where species with similar nutritional requirements are likely to accept similar types of prey. Here we analysed the macronutritional niches of a woodland assemblage of seven harvestman species, all supposed to be predators with omnivorous tendencies. Five species (Mitopus morio, Leiobunum gracile, Oligolophus tridens, O. hanseni, Paroligolophus agrestis) were native and two species (Opilio canestrinii, Dicranopalpus ramosus) were recent invaders into the community. We compare the fundamental (FMN) and realized (RMN) macronutritional niche positions of the species using a ‘double‐test procedure’, which provides information on whether the species were food limited in their natural habitat, and whether they were limited by specific macronutrients. All seven species were food limited and six species were non‐protein limited in the field; of these, four species were carbohydrate limited, and in one species females were lipid limited and males carbohydrate limited. These findings add to the notion that predators are mainly non‐protein limited in the field. The FMN positions of the assemblage fell within 46‐50% protein, 29‐38% lipid, and 16‐22% carbohydrate. The amount of carbohydrate in the self‐selected diet combined with carbohydrate limitation confirms that the species are zoophytophagous. Two morphological clusters of species (large long‐legged vs. small short‐legged species) differed not only in microhabitat (upper vs. lower forest strata) but also in macronutrient selection, where large long‐legged species selected higher proportion of carbohydrate than small short‐legged species. Thus, morphologically similar species occupy the same habitat stratum and have similar macronutritional niches. We discuss the hypothesis that the invasive O. canestrinii might have an impact on native species as it allegedly had in urban environments previously. Two basic assumptions about interspecific resource competition were fulfilled, i.e. high overlap of nutritional requirements and limitation by food and macronutrients.
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.
Growing evidence that individuals of many generalist animals behave as resource specialists have attracted substantial research interest for its ecological and evolutionary implications. Variation in resource preferences is considered to be critical for developing a general theory of individual specialization. However, it remains to be shown whether diverging preferences can arise among individuals sharing a similar environment, and whether these preferences are sufficiently stable over time to be ecologically relevant. We addressed these issues by means of common garden experiments in feral pigeons (Columba livia), a species known to exhibit among-individual resource specialization in the wild. Food-choice experiments on wild-caught pigeons and their captive-bred cross-fostered descendants showed that short-term variation in food preferences can easily arise within a population, and that this variation may represent a substantial fraction of the population foraging niche. However, the experiments also showed that, rather than being limited by genetic or vertical cultural inheritance, food preferences exhibited high plasticity and tended to converge in the long-term. Although our results challenge the notion that variation in food preferences is a major driver of resource specialization, early differences in preferences could pave the way to specializations when combined with neophobic responses and/or positive feedbacks that reinforce niche conservation.
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Sexual segregation in the behaviour, morphology or physiology of breeding seabirds can be related to divergent parental roles, foraging niche partitioning or sex-specific nutritional requirements. Here, we combine GPS tracking, dietary and nutritional analysis to investigate sex-specific foraging of Brown Boobies breeding on Raine Island, Great Barrier Reef, Australia. We observed sex-specific segregation in: (1) foraging location: females undertook longer trips, foraging at more distant locations than males; (2) foraging time: male activity and foraging occurred throughout the day, while female activity and foraging increased from midday to an afternoon peak; and (3) prey type, females mostly consumed flying fish, whereas males consumed equal proportions of flying fish and squid. Brown Booby diets contained five tropical prey species that significantly differed in their nutritional composition (Protein, Lipid and Water, wet mass). Despite this variation we found no differences in the overall nutritional content of prey caught by each sex. The observed sex-specific differences in prey type, location and time of capture are likely driven by a combination of a division of labour, risk partitioning and competition. However, Brown Boobies breeding on Raine Island, and other populations, might flexibly partition foraging niches by sex in response to varying competitive and environmental pressures. In light of such potential foraging dynamism, our inconclusive exploration of nutritional segregation between sexes warrants further investigation in the species.
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The niche concept is essential to understanding how biotic and abiotic factors regulate the abundance and distribution of living entities, and how these organisms utilize, affect and compete for resources in the environment. However, it has been challenging to determine the number and types of important niche dimensions. By contrast, there is strong mechanistic theory and empirical evidence showing that the elemental composition of living organisms shapes ecological systems, from organismal physiology to food web structure. We propose an approach based on a multidimensional elemental view of the ecological niche. Visualizing the stoichiometric composition of individuals in multivariate space permits quantification of niche dimensions within and across species. This approach expands on previous elemental characterizations of plant niches, and adapts metrics of niche volume, overlap and nestedness previously used to quantify isotopic niches. We demonstrate the applicability of the multidimensional stoichiometric niche using data on carbon, nitrogen, and phosphorus of terrestrial and freshwater communities composed by multiple trophic groups. First, we calculated the stoichiometric niche volumes occupied by terrestrial and freshwater food webs, by trophic groups, by individual species, and by individuals within species, which together give a measure of the extent of stoichiometric diversity within and across levels of organization. Then we evaluated complementarity between these stoichiometric niches, through metrics of overlap and nestedness. Our case study showed that vertebrates, invertebrates, and primary producers do not overlap in their stoichiometric niches, and that large areas of stoichiometric space are unoccupied by organisms. Within invertebrates, niche differences emerged between freshwater and terrestrial food webs, and between herbivores and non-herbivores (detritivores and predators). These niche differences were accompanied by changes in the covariance structure of the three elements, suggesting fundamental shifts in organismal physiology and/or structure. We also demonstrate the sensitivity of results to sample size, and suggest that representative sampling is better than rarefaction in characterizing the stoichiometric niche occupied by food webs. Overall, our approach demonstrates that stoichiometric traits provide a common currency to estimate the dimensionality of stoichiometric niches, and help reduce and rationalize the number of axis required to characterize communities.
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Background: Foraging efficiency determines whether animals will be able to raise healthy broods, maintain their own condition, avoid predators and ultimately increase their fitness. Using accelerometers and GPS loggers, features of the habitat and the way animals deal with variable conditions can be translated into energetic costs of movement, which, in turn, can be translated to energy landscapes.We investigated energy landscapes in Gentoo Penguins Pygoscelis papua from two colonies at New Island, Falkland/Malvinas Islands. Results: In our study, the marine areas used by the penguins, parameters of dive depth and the proportion of pelagic and benthic dives varied both between years and colonies. As a consequence, the energy landscapes also varied between the years, and we discuss how this was related to differences in food availability, which were also reflected in differences in carbon and nitrogen stable isotope values and isotopic niche metrics. In the second year, the energy landscape was characterized by lower foraging costs per energy gain, and breeding success was also higher in this year. Additionally, an area around three South American Fur Seal Arctocephalus australis colonies was never used. Conclusions: These results confirm that energy landscapes vary in time and that the seabirds forage in areas of the energy landscapes that result in minimized energetic costs. Thus, our results support the view of energy landscapes and fear of predation as mechanisms underlying animal foraging behaviour. Furthermore, we show that energy landscapes are useful in linking energy gain and variable energy costs of foraging to breeding success.
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One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
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Carnivorous animals are assumed to consume prey to optimise energy intake. Recently, however, studies using Nutritional Geometry (NG) have demonstrated that specific blends of macronutrients (e.g. protein, fat and in some cases carbohydrates), rather than energy per se, drive the food selection and intake of some vertebrate and invertebrate predators in the laboratory. A vital next step is to examine the role of nutrients in the foraging decisions of predators in the wild, but extending NG studies of carnivores from the laboratory to the field presents several challenges. Biologging technology offers a solution for collecting relevant data which when combined with NG will yield new insights into wild predator nutritional ecology.
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We apply a recently established nutritional framework for defining dietary generalism to global populations of wild boar (Sus scrofa). Across its range, wild boar consume a diversity of foods that vary in nutritional composition. The macronutrient (carbohydrate, protein and fat) composition of the diets composed from those foods also varies substantially between countries, particularly in terms of proportion of energy from protein. These results suggest that as a species wild boar have a wide fundamental macronutrient niche, which likely contributes to the success of the species as an invader of novel environments.