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Macronutrient selection of free-ranging urban Australian white ibis (Threskiornis moluccus)

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Macronutrient selection of free-ranging urban Australian white ibis (Threskiornis moluccus)

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Anthropogenic habitats often provide urban wildlife the opportunity to feed on a range of nutritionally diverse foods, which may ultimately lead to human-wildlife conflict. The Australian white ibis (Threskiornis moluccus) provides an exemplar model for examining the nutritional priorities and constraints of a native vertebrate that is successfully transitioning to an urban specialist. Here, we used field-based feeding trials to investigate the macronutrient preferences of free-ranging ibis in Sydney, Australia. Feeding trials (n = 61) offering three experimental feeds showed that ibis selected significantly more high-carbohydrate (HC) than high-protein (HP) and high-lipid (HL) foods (95% CIHP-HC = −1.115 to −0.709; CIHL-HC = −1.874 to −1.468), and significantly more HP than HL (CIHL-HP = −0.962 to −0.556). The average proportion of macronutrient-derived energy selected by ibis was 25% protein (P; ± 1.1 SE): 23% lipid (L; ± 1.1): 52% carbohydrate (C; ± 1.8). Nutritional geometry suggested that mixtures selected at experimental feeders were substantially higher in C and lower in P than are natural prey (e.g. insects, crustaceans), which were composed primarily of P and L. Compositional log-ratio-based linear models of factors affecting macronutrient proportions selected by ibis showed that: 1) ln(P/C) increased with amount of recent rainfall; and 2) ln(L/C) also increased with rain and had a non-linear relationship with number of birds feeding. Our results suggest that ibis forage for macronutrients rather than energy “per se”, and that their urban foraging is influenced by competition and the environment.
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Behavioral
Ecology
Original Article
Macronutrient selection of free-ranging urban
Australian white ibis (Threskiornis moluccus)
Sean C.P.Coogan,a,b Gabriel E.Machovsky-Capuska,a,b Alistair M.Senior,b,c
John M.Martin,d Richard E.Major,e and DavidRaubenheimera,b
aSchool of Life and Environmental Sciences, University of Sydney, Sydney, Australia, bCharles Perkins
Centre, University of Sydney, Sydney, Australia, cSchool of Mathematics and Statistics, University of
Sydney, Sydney, Australia, dRoyal Botanic Gardens and Domain Trust, Sydney, Australia, and eAustralian
Museum Research Institute, Australian Museum, Sydney, NSW, Australia
Received 24 November 2016; revised 11 March 2017; editorial decision 23 March 2017; accepted 29 March 2017.
Anthropogenic habitats often provide urban wildlife the opportunity to feed on a range of nutritionally diverse foods, which may ulti-
mately lead to human-wildlife conflict. The Australian white ibis (Threskiornis moluccus) provides an exemplar model for examining the
nutritional priorities and constraints of a native vertebrate that is successfully transitioning to an urban specialist. Here, we used field-
based feeding trials to investigate the macronutrient preferences of free-ranging ibis in Sydney, Australia. Feeding trials (n=61) offer-
ing three experimental feeds showed that ibis selected significantly more high-carbohydrate (HC) than high-protein (HP) and high-lipid
(HL) foods (95% CIHP-HC=−1.115 to −0.709; CIHL-HC=−1.874 to −1.468), and significantly more HP than HL (CIHL-HP=−0.962 to −0.556). The
average proportion of macronutrient-derived energy selected by ibis was 25% protein (P; ± 1.1 SE): 23% lipid (L; ± 1.1): 52% carbohy-
drate (C; ± 1.8). Nutritional geometry suggested that mixtures selected at experimental feeders were substantially higher in C and lower
in P than are natural prey (e.g. insects, crustaceans), which were composed primarily of P and L.Compositional log-ratio-based linear
models of factors affecting macronutrient proportions selected by ibis showed that: 1)ln(P/C) increased with amount of recent rainfall;
and 2)ln(L/C) also increased with rain and had a non-linear relationship with number of birds feeding. Our results suggest that ibis for-
age for macronutrients rather than energy “per se”, and that their urban foraging is influenced by competition and the environment.
Key words: carbohydrate, foraging, macronutrient selection, nutritional ecology, urban ecology, urban exploiter.
INTRODUCTION
Urbanization has been identified as a major threat to global biodi-
versity, and its eects are expected to increase considerably owing
to the projected growth of the human population and urban areas
(Secr. Conv. Biol. Div. 2012; Seto etal. 2012; Aronson etal. 2014;
U. N.Dept. Econ. Soc. A. Pop. Div. 2015). Anthropogenic pres-
sures can present several challenges to wildlife inhabiting urban
areas (McKinney 2002; Kalnay and Cai 2003; Lowry etal. 2013).
They can also present opportunities, as evidenced by the many
non-human species that successfully inhabit anthropogenic envi-
ronments (McKinney 2002; McDonnell and Hahs 2015). For
example, wildlife occupying urban habitats may capitalize on
altered distributions, availabilities, and abundances of food relative
to “natural” habitats (Chace and Walsh 2006; Gordon etal. 2016).
The year-round availability of concentrated anthropogenic food
resources may ultimately aect aspects of the biology of urban
wildlife, potentially leading to changes in traits such as migratory
behaviour and reproduction (Beckmann and Berger 2003; Martin
etal. 2011; Gilbert etal. 2016). Furthermore, urban food resources
may lead to incidences of human-wildlife conflict (Murray et al.
2015; Coogan and Raubenheimer 2016).
The Australian white ibis (hereafter “ibis”, Threskiornis moluccus)
is a native Australian wading bird whose distribution has recently
shifted from natural wetlands towards urban habitats (Martin
et al. 2010; Smith et al. 2013). The species therefore provides an
exemplar model for examining the nutritional priorities and con-
straints of a native vertebrate that is successfully transitioning to
an urban specialist. Traditionally, the ibis was found in large popu-
lations throughout inland wetlands in eastern Australia, and was
rarely found in urban areas (Carrick 1962; Cowling and Lowe
198l; Kingsford and Johnson 1998). Urban populations of ibis in
eastern Australia, however, have increased dramatically since the
1970s, likely in response to increased agricultural water extraction
from inland rivers, drought, habitat loss, and crucially their ability
to utilize urban food resources (Martin etal. 2007, 2010, 2012). In
Address correspondence to S.C.P. Coogan, The University of Sydney,
Charles Perkins Centre, D17, Level 4 East, NSW, 2006, E-mail: sean.
coogan@sydney.edu.au
Behavioral Ecology (2017), 00(00), 1–9. doi:10.1093/beheco/arx060
Behavioral Ecology
fact, urban ibis can be considered pests and are involved in inci-
dences of human-wildlife conflict due to their habit of scavenging
anthropogenic foods from a variety of sources, including garbage
dumps, rubbish bins, and picnic tables (Ross 2004; Epstein et al.
2006; Martin etal. 2007, 2010).
Relatively few studies have investigated the natural diet of ibis,
although those which have, documented them as carnivores con-
suming a wide range of insect and small invertebrate and ver-
tebrate prey (Carrick 1959; Vestjens 1973; Barker and Vestjens
1990; Smith and Munro 2008). Interestingly, ibis in urban parks
have been shown to alternate foraging patterns depending on
previous rainfall. On days following rainfall, ibis were associ-
ated with parks with higher relative abundance of earthworms
(Oligochaeta), which they also consumed at a greater rate than
during dry periods (Chard 2015). Conversely, during dry peri-
ods ibis were associated with parks having higher availability of
anthropogenic foods (Chard 2015).
Despite foraging being cited as a main driver of ibis-human
conflicts, and the ability of ibis to forage on anthropogenic foods
being suggested as a key to their success in urban areas (Ross 2004;
Martin et al. 2007, 2010, 2011; Murray and Shaw 2009; Smith
2009), no studies have yet investigated the nutritional preferences
of the species. In other species, the ratios and amounts of protein,
lipid, and carbohydrate (and other nutrients) in foods have been
demonstrated to be key drivers of foraging behaviour and fitness,
independent of energy intake “per se” (reviewed in Simpson and
Raubenheimer 2012; Nie etal. 2014; Raubenheimer et al. 2015).
Nutrient-specific foraging behaviour is likely to play a role in the
food choice of even obligate carnivores, which might face relatively
less variation in food composition than herbivores or omnivores
(Jensen etal. 2012; Kohl etal. 2015). The nutritional compositions
of foods found in anthropogenic habitats may be fundamentally
dierent than foods from the “native” range. Compared to non-
urban areas, carbohydrate and lipid are likely relatively more avail-
able than protein in an urban setting (Coogan and Raubenheimer
2016). Additionally, the macronutrient preferences of a species
may play a prominent role in food-related human-wildlife conflict
(Coogan and Raubenheimer 2016). Understanding the macronu-
trient-specific foraging behaviour of urban ibis may thus provide
valuable insight into their successful urban colonization and food-
related conflict.
Here, we combine field-based experimental feeding trials, state-
space nutritional models (nutritional geometry), and compositional
data analysis to investigate the macronutrient preferences and
nutritional ecology of free-ranging ibis in an urban setting. We
test the prediction that ibis compose diets with non-random pro-
portions of macronutrients by addressing three questions. First,
do ibis select isoenergetic (i.e. equal energy density) foods experi-
mentally manipulated to contain predominantly one macronutri-
ent, high-protein (HP), high-lipid (HL), or high-carbohydrate (HC),
in unequal proportions (i.e. non-randomly)? Second, if ibis select
macronutrient proportions non-randomly, do they select primarily
HP and HL foods typical of a carnivorous diet (Kohl etal. 2015).
Third, is the selection of macronutrient ratios influenced by envi-
ronmental factors, such as the degree of intraspecific competition
and the amount of recent rainfall?
MATERIALS AND METHODS
This study was approved by the University of Sydney Animal
Ethics Committee (2015/927).
Experimentaldiets
We oered ibis three pelleted feeds (HP, HL, and HC) as
described in Machovsky-Capuska et al. (2016a), with a slightly
modified formulation to improve the structural integrity of pellets
(Supplementary Table S1). The three dierent feeds were isoener-
getic (3.1 kcal/g) to remove the confound of ibis potentially select-
ing higher-energy-density pellets, composed of primarily naturally
derived rather than semi-synthetic ingredients, and balanced in
micro- and macro-minerals. Indigestible powdered cellulose was
used as a filler to keep the energy content of foods constant. On a
wet-weight basis, HP pellets contained 48.0% crude protein (CP),
8.0% crude fat (CF), and 5.0% starch. HL pellets contained 2.0%
CP, 36.4% CF, and 0.1% starch. HC pellets contained 10.3% CP,
3.5% CF, and 58.2% starch.
Feeding stations and food consumption
Ibis in urban habitats are often associated with discrete anthropo-
genic features such as parks, landfills, and ponds or wetlands, and
show high site fidelity (Murray and Shaw 2009; Martin etal. 2011,
2012). The macronutrient selection study was conducted at Hyde
Park (~33°5219S, 151°1237E) and the Royal Botanic Gardens
(~33°5146S, 151°1255E; RBG), Sydney, New South Wales,
Australia. These areas were selected because they contain a rela-
tively large and consistent population of ibis as determined from
long term population surveys (Martin etal. 2010). The study was
conducted from April to June 2016, which was within the typical
non-breeding season (January to June) as defined by Martin et al.
(2010). All feeding trials were held in the morning (i.e. between sun-
rise and 12:00 PM). Typically two feeding trials were performed
per morning, one in each park. Care was taken to ensure no birds
were fed more than once per day. We performed feeding trials dur-
ing rain-free periods to avoid feeds getting wet and to standardize
our sampling design.
Experimental foods were supplied in a dish intended to emulate
those used by visitors to the parks to store foods, for example, for
lunches and picnicking. This approach was taken because a pilot
study (undertaken during January to March 2016)revealed that ibis
were generally wary of unfamiliar or opaque dishes (e.g. those used
in Machovsky-Capuska etal. 2016a), and/or would not recognize
the feeding stations as sources of food, which may be consistent
with previous observations of urban birds being bold yet neophobic
(Audet etal. 2016). We used a 1.1L semi-transparent plastic food
storage container (18×11×6cm), with two semi-transparent plas-
tic dividers inserted in the dish to create three equal sized compart-
ments (Figure1). Each compartment was filled with 50g of one of
the three experimental foods (150g total). The type of food in the
middle position of the dish was alternated each experimental day
to account for positional eects. To prevent ibis from tipping the
dish over, we attached dulled clear-plastic disposable picnic knives
to the bottom of the dish (oriented across the width of the dish)
using clear packing tape to act as stabilizers.
After locating ibis (individuals or groups) in the park, we pre-
sented the food dish to the bird(s) and placed it on the ground to
allow them to feed. If birds initiated feeding, sessions were limited
to a maximum of 20 min to prevent large groups of birds from
potentially consuming all the foods. Often during feeding ses-
sions, additional ibis recruited to the feeding dish. Ibis typically
fed one at a time at the feeding dish, during which time they had
full access to all foods. Typically, one dominant individual in the
group would monopolize and defend the dish. Once a dominant
Page 2 of 9
Coogan etal. • Macronutrient selection of urbanibis
bird was finished feeding it would typically leave and another bird
would take its place, and so on. We recorded the total number of
birds observed feeding from the dish, including ibis that quickly
and seemingly indiscriminately rushed in to feed from the dish in
the presence of the dominant feeder. Ibis fed on individual pellets
one at a time, which could be observed by a distinctive backwards
motion of their head which propelled the pellet from the tip of its
bill to its throat.
Feeding sessions were excluded from the analysis if: 1)there were
major interruptions that resulted in truncated feeding sessions (e.g.
competition from other birds or disturbance by people); 2)other
bird species fed from the dish; or 3)dishes were upturned, despite
our precautions. Behavioural observations of ibis feeding at the
dish were within 5 m (birds were already habituated to human pres-
ence), typically around 10 m (following Murray and Shaw 2009).
After a feeding session, remaining pellets were collected and stored
in separate plastic bags before being weighed later that day.
Nutritional composition of naturalprey
To estimate the nutritional composition of the natural ibis diet, we
identified natural food items potentially consumed by ibis via lit-
erature search (Carrick 1959; Vestjens 1973; Barker and Vestjens
1990; Smith and Munro 2008; Chard 2015), and estimated their
nutritional compositions via the literature (Tacon et al. 1983; Jones
et al. 1996; Bernard et al. 1997; Dierenfeld et al. 2002; Finke
2002; Ahmed 2008; Xiaoming etal. 2010) and the USDA nutrient
database (US Department of Agriculture, Agricultural Research
Service, Nutrient Data Laboratory 2015) (Supplementary Table
S2). We excluded anthropogenic foods, either scavenged or deliber-
ately provisioned, from this analysis.
Data analysis
Mass of food consumed
We assessed the dierence in the mass of food consumed in grams
from each dish compartment using linear mixed models (LMMs)
implemented with the “lmer” function in the R package lme4
(Bates et al. 2014) following Machovsky-Capuska et al. (2016a).
All analyses were performed in R version 3.0.3 (R Core Team
2014). We set the response variable as the log-transformed (+0.5;
Yamamura 1999) mass in grams of food consumed after each feed-
ing trial. The predictor variable was a 3-level categorical variable
representing one of the three experimental foods oered (HP, HL,
and HC) per session. Significance was inferred if 95% CIs did
not span zero. LMMs included a random factor for each feeding
session, to account for any between-session variance that may be
driven positional eects arising from how foods were presented.
Nutritional geometry of proportional
macronutrientintake
We used right-angled mixture triangles (RMT) to visualize the mac-
ronutrient ratio of foods selected by ibis groups at feeding stations
(full details of RMT methodology can be found in Raubenheimer
2011), where macronutrients were plotted on a percent metabo-
lizable energy basis and expressed as a proportion of total mac-
ronutrient-derived metabolizable energy. To do this, we applied
metabolizable energy conversion factors of 4 kcal/g for protein and
carbohydrate, and 9 kcal/g for lipid, to food compositions to esti-
mate metabolizable energy supplied by each macronutrient (Merrill
and Watt 1973). The metabolizable energy supplied by individual
macronutrients in each food was then plotted as a percentage of
the sum of total macronutrient energy. For simplicity, we express
the percent metabolizable energy of each macronutrient as: P (pro-
tein), L (lipid), and C (carbohydrate). HP pellets contained 67.6%
P, 25.4% L, and 7.0% C. HL pellets contained 2.4% P, 97.5% L,
and 0.1% C.HC pellets contained 13.5% P, 10.3% L, and 76.2%
C. Macronutrient composition estimates for natural foods were
plotted in the RMT using the same metabolizable energy conver-
sions to visualize the macronutrient space of their carnivorous diet.
Linear models of environmental factors affecting
proportional macronutrient selection
To determine whether rainfall and intraspecific competition
aected the proportions of P, L and C selected by ibis during feed-
ing sessions, we used linear models (LMs) implemented in the R
package compositions using an additive log-ratio (“alr”) approach
to analyzing closed compositions in a logistic geometry (“acomp”;
van den Boogaart and Tolosana-Delgado 2008; van den Boogaart
et al. 2014). The macronutrient C was treated as the denomina-
tor of the log-ratio, where two separate models were created with
either P or L in the numerator (“ln(P/C)” and “ln(L/C),” respec-
tively). We evaluated whether there was a relationship between the
total number of birds (“n_birds”) observed feeding from the food
dish during a feeding session and the proportion of macronutri-
ents selected. We included a quadratic term “n_birds^2” to evalu-
ate support for a non-linear relationship. We also explored whether
(a) (b)
Figure1
Representation of an experimental session showing: (a) a feeding station with an ibis feeding from one of three dish compartments each containing dierent
experimental pellets (HP, HL, or HC); and (b) a large group of ibis congregated around the feeding dish.
Page 3 of 9
Behavioral Ecology
total rain (mm) over the previous two days (“Rain2d”) influenced
macronutrient choice. Rainfall data was obtained from the Bureau
of Meteorology website (www.bom.gov.au) for the RBG weather
station.
We performed a sensitivity analysis for Rain2d using data from
the nearby Observatory Hill station and obtained nearly identi-
cal results (Supplementary Table S3). We also evaluated whether
confounding factors, “Site” (a two-level categorical predictor; Hyde
Park vs. RBG), and “Middle_food” (three-level categorical predic-
tor denoting the contents of the middle compartment of the feed-
ing dish) aected the composition of foods consumed, but detected
no significant eects (results not shown).
RESULTS
Mass of food consumed
On average, significantly more HC pellets were consumed dur-
ing a feeding session (n = 61 sessions) than HP or HL pellets
(LMM est.HP-HC, CI= −0.912, −1.115 to −0.709; LMM est.HL-HC,
CI = −1.671, −1.874 to −1.468; Figure 2). Likewise, significantly
more HP pellets were consumed than HL pellets (LMM est.HL-HP,
CI = −0.759, −0.962 to −0.556). Back-transformation indicated
that the average mass of HC (11.1 g) consumed per session was
almost 3 times that of HP (4.1g), and nearly 7 times greater than
HL (1.7g). The mean and mode number of birds feeding per ses-
sion was 5.3 (± 0.6 SE) and 4, respectively.
Analysis of proportional macronutrient
energyintake
Right-angled mixture triangle
On a metabolizable energy basis, the ratio of macronutrients
selected by ibis during individual feeding trials (n=61) was usually
higher in C than P or L (Figure 3). Across all feeding events, the
arithmetic mean proportion of macronutrient energy selected dur-
ing feeding trials was 25% P (± 1.1 SE): 23% L (± 1.1): 52% C (±
1.8), which is higher in C and lower in L than would be expected
based on random feeding (26% P: 47% L: 27%C).
The macronutrient ratios of natural foods of ibis determined
from the literature were typical of those consumed by carnivores,
being moderate to high in P, low to moderate in L, and low or
devoid of C (Figure 3). Insects were a modest source of C, while
crustaceans and vertebrate prey contained little or negligible C.We
observed ibis to feed on earthworms several times (this was not
quantified), particularly on mornings following heavy rain, which
supports data from the literature (the eect of rain is statistically
explored in the next section); these prey are high in P and moderate
to low in L and C, although earthworms were among the natural
foods highest inC.
Linear models of factors affecting proportional
macronutrient selection
There was an increase in selection of P after rainfall, with ln(P/C)
showing a small but statistically significant increase with Rain2d
(LM est.ln(P/C) = 0.006; Table 1; Figure 4). There was no signifi-
cant eect of the number of birds foraging at the dish on ln(P/C).
Selection of L relative to C also increased slightly after rainfall, with
ln(L/C) showing a small but significant relationship with Rain2d
(LM est.ln(L/C) = 0.005). There was also a significant quadratic
relationship with the number of birds feeding and ln(L/C), where
ln(L/C) increased with n_birds (LM est.ln(L/C) = 0.182) followed by
a decrease with n_birds^2 (LM est.ln(L/C) = −0.008; Table 1; Figure
4). The quadratic relationship showed that ln(L/C) increased with
group size up to around 10 birds, after which it appeared to level
o (Figure 4).
DISCUSSION
Our study yielded several insights in to the nutritional ecology of
ibis in urban settings, demonstrating that ibis typically selected HC
pellets over HP and HL, and HP over HL. These results support
the hypothesis that ibis do not forage primarily for energy “per se”,
but distinguish between dierent macronutrient combinations. Ibis
selection from feeders was typically high in C, which is in contrast
to the typical macronutrient composition of their natural foods.
Competition for a locally concentrated food resource in the form of
our experimental food dish showed that ibis selected higher propor-
tions of L as group size increased, although only up to a point. Ibis
also displayed a behavioral response to rainfall, where they tended
to show an increased preference for P and L relative to C after peri-
ods ofrain.
The compositions of natural foods of ibis were relatively high in
P and L, and low or absent in C, which is consistent with a typical
carnivorous diet (Kohl etal. 2015). The diets of carnivores, how-
ever, have been considered to follow a gradient of omnivory based
on the increasing utilization of C (Remonti etal. 2015). For exam-
ple, on one end of the continuum omnivorous carnivores such as
grizzly bears (Ursus arctos) heavily consume C-rich foods (e.g. fruits)
when seasonally available (Coogan etal. 2014), while at the other
extreme obligate carnivores such as wolves and feral cats consume
very little C (~1–2%; Plantinga etal. 2011; Bosch etal. 2014). Our
analysis of the natural diet of ibis suggests that they typically con-
sume low to moderate levels of C (e.g. up to ~20% in earthworms)
in natural habitats. However, selection from our feeders indicated
that ibis have a high preference for C intake (76% C in HC pel-
lets). The carnivorous European badger (Meles meles; Remonti etal.
2011) showed a similar, although less extreme flexibility in C intake,
consuming approximately a five-fold amount of C when in crop
lands depauperate in prey (Remonti etal. 2011).
3.0
2.5
2.0
1.5
Consumption (log grams+0.5)
1.0
0.5
0.0
HC HL HP
Figure2
The log mean (+ 0.5) grams of food consumed by ibis per feeding trial
(n=61). Error bars are ± 1 SE.
Page 4 of 9
Coogan etal. • Macronutrient selection of urbanibis
Our study suggests that ibis display a high degree of food-com-
position generalism (“sensu” Machovsky-Capuska et al. 2016b),
being able to potentially feed on a range of natural foods, as well
as our experimental foods, which taken together vary widely in
macronutrient composition. In terms of the macronutrient com-
position on which ibis are able to subsist (i.e. their “fundamental
macronutrient niche”, “sensu” Machovsky-Capuska etal. 2016b),
ibis may be macronutrient generalists able to tolerate a wide range
of macronutrient intakes, or conversely they may be macronutri-
ent specialists that consume very dierent foods to arrive at a con-
sistent macronutrient intake (Machovsky-Capuska et al. 2016b).
For example, the pine marten (Martes martes) and European badger
consumed a wide variety and combination of foods between geo-
graphically distinct populations, yet each species maintained similar
macronutrient intake ratios across populations despite dietary dif-
ferences (Remonti etal. 2011, 2015). Such a situation is indicative
100
High-protein food
High-lipid food
High-carbohydrate food
Feeder selection
Mean feeder selection (+/– SE)
Random feeding (null hypothesis)
Natural foods
Earthworms
95
90
85
80
75
65
55
45
35
25
15
5
0
0510 15
[90] [80] [70] [60] [50] [40] [30] [20] [10]
20 25 30 35 40 45 50 55
Protein (% energy)
Lipid (% energy)
[Carbohydrate (% energy)]
60 65 70 75 80 85 90 95
100
70
60
50
40
30
20
10
Figure3
Right-angled mixture triangle (RMT) showing the macronutrient mixtures (green circles) and mixture space (green polygon) selected by ibis when oered
a dish containing three individually compartmentalized experimental foods. The grey-shaded polygon connecting the three experimental foods, HP (black
triangle), HF (black circle), and HC (hollow square), represents the experimental mixture space within which feeder meal compositions were constrained to
lie. Blue circles represent the macronutrient balance of a variety of “natural” foods of ibis identified from the literature. Earthworms are distinguished, as
they were documented to be an important food in our study area and were observed to be fed upon by ibis during field work. Note that there are overlapping
data points for HC-only food selection which occurred during n=5 sessions (dark green circle). The arithmetic mean diet across all feeding trials is shown by
the black circle with bi-variate ±SE bars (for protein and lipid). The black square represents the macronutrient composition under the null hypothesis that ibis
selected the three foods in equal proportions or randomly.
Table1
Compositional linear model parameter estimates and SE predicting the log-ratio macronutrient proportions, ln(C/P) and ln(L/C),
selected by ibis during feeding sessions (n=61) as a quadratic function of the total number of birds observed eating food from the
experimental dish (n_birds + n_birds^2) and the total rain (mm) in the previous 2days (Rain2d)
Model parameters Estimate SE 95% CI lower 95% CI upper Adj. R2
ln(P/C) 0.15
(Intercept) −1.068 0.170 −1.408 −0.728
Rain2d 0.006 0.002 0.003 0.010
n_birds 0.067 0.055 −0.044 0.178
I(n_birds^2) −0.003 0.003 −0.010 0.004
ln(L/C) 0.19
(Intercept) −1.507 0.182 −1.872 −1.143
Rain2d 0.005 0.002 0.001 0.008
n_birds 0.182 0.059 0.063 0.301
I(n_birds^2) −0.008 0.004 −0.016 0.001
Also given are 95% confidence intervals (CI), and adjusted R-squared (Adj. R2) of model fit. Non-intercept 95% CIs that do not include zero are shown in bold.
Page 5 of 9
Behavioral Ecology
of evolved homeostatic regulatory mechanisms for optimizing mac-
ronutrient intake dictating the patterns of foraging in these spe-
cies (Raubenheimer etal. 2016). A widespread investigation of the
nutritional preferences of ibis across geographically distinct popula-
tions (e.g. urban vs. rural) would yield insights into the fundamental
nutritional niche of the species.
A C-deprived diet reduced aggression and activity in Argentine
ants (Linepithema humile), suggesting that C-rich diets might enhance
competitive behaviour (Grover et al. 2007), and interestingly
Australian ecosystems may be rich in carbohydrates due to nutri-
ent poor soils (Low 2014). In our study, the non-linear relationship
between the number of birds feeding and the proportion of L,
relative to C, may suggest that food choice is influenced by group
competition in ibis. One potential mechanism behind this, is that
as group size increases feeding becomes more indiscriminate across
all individuals (scramble competition); however, it is more likely
in our study that more of the less preferred food (HL) was con-
sumed as the number of subordinate animals indiscriminately feed-
ing increased with group size (contest competition). The trend of
increasing L appeared to stabilize, however, when approximately
10 or more birds had fed from the dish, suggesting that the pro-
portion of L selected was converging towards the mean at larger
group sizes. This could indicate that the maximum number of
indiscriminate feeders able to feed at the dish had been reached
by this point, and that variance in lipid intake was being averaged
away as more birds fed from the dish. A future line of inquiry,
therefore, might be whether intraspecific competition for food
resources is a driver of dietary imbalance in animals that feed in
large groups such as ibis, and how such competition contributes to
evolutionarily adaptive responses to dietary imbalance (i.e. “rules of
compromise”; Raubenheimer and Simpson 1993). Theory predicts
that high-intensity intra-group competition for nutrients can result
in organisms altering their nutritional strategy (Senior etal. 2015).
Given the observed relationship between group size and macronu-
trient choice, ibis may be a good model system for future research
on the influence of conspecific competition on nutritional strategy.
Urban habitats can be highly unstable and do not completely
buer anthropogenic commensal species from seasonal variability
(Hulme-Beaman et al. 2016). Ibis appeared to select a wide range
of macronutrient ratios during feeding sessions following periods
of zero to little rainfall. After periods of rainfall, however, ibis dis-
played a slight preference for increased P and L consumption that
increased linearly with rainfall, which is more typical of the mac-
ronutrient composition of the natural foods (e.g. earthworms) that
are likely more abundant post-rainfall (Chard 2015). This is in
contrast to the prediction that ibis would select more C from our
0.5–0.5
In(P/C)
–1.5
050 100 150 200
Previous 2 day rainfall (mm)
–1.0 0.0
(a)
0.0–1.0
In(L/C)
–2.0
050 100 150 200
–1.5 –0.50
0.5–0.5
In(P/C)
–1.5
51015
Number of birds feeding
–1.0 0.0
(b)
0.0–1.0
In(L/C)
–2.0
51
01
5
–1.5 –0.50
Figure4
Results of compositional log-ratio based linear models of macronutrient proportions, ln(P/C) and ln(L/C), selected by ibis as a function of the predictor
variables: (a) the total rain (mm) in the previous 2days; and (b) the total number of birds observed feeding on experimental foods during a session. Blue lines
are fitted values based on linear models, and the red lines show the mean ln(P/C) and ln(L/C) selected by ibis.
Page 6 of 9
Coogan etal. • Macronutrient selection of urbanibis
dish to redress a macronutrient imbalance after feeding on P- and
L-rich prey post-rainfall. One biological explanation is that ibis
are tuning their macronutrient preferences in keeping with envi-
ronmental resource availability post-rainfall to take advantage of
abundant resources. Such foraging behavior may be selected for in
highly-generalist feeders which encounter and opportunistically con-
sume a wide range of foods with diverse macronutrient composi-
tions, and which are able to tolerate a wide range of macronutrient
imbalance (Raubenheimer and Simpson 1999; Simpson etal. 2002;
Raubenheimer and Simpson 2003). Generalists with a wide diet
breadth have an elevated probability of subsequently encountering
foods with complementary nutritional properties, and taking advan-
tage of abundant yet nutritionally imbalanced resources may result
in higher fitness. Alternatively, the physiological requirements of ibis
may shift to higher P and L following periods of rainfall for some
yet to be determined reason. Another possibility is that the observed
relationship is being driven by outliers in the data following the peri-
ods of extreme rainfall. More research is thus required to elucidate
the relationship between ibis macronutrient preferences and rainfall.
One explanation for the ibis’ preference for HC foods in experi-
mental sessions compared to their natural diet, may be in part due
to the relatively low proportion and availability of C in their natural
foods. Under natural conditions, the ibis appetite systems may have
evolved to preferentially consume C when present given its relative
rarity in the nutritional environment to which they are adapted. For
example, humans are believed to have adaptively evolved behav-
ioral and physiological regulatory systems that find foods high in
C and L appetizing (Raubenheimer et al. 2014), because such
foods may have been rare in the ancestral environment (Speth and
Spielmann 1983; Cordain et al. 2000). In urban environments,
however, high-C food items are likely to be relatively more avail-
able than high-P and high-L foods (Coogan and Raubenheimer
2016). A species preference for high-C foods may therefore play a
role in human-wildlife conflict associated with anthropogenic food
resources. For instance, the grizzly bear is well known for incidences
of food-related conflict with humans and also has a preference for
high-C foods, especially when high-L foods are limiting (Coogan
and Raubenheimer 2016). An alternative explanation for our
results may thus be that ibis have an increased preference for C in
the urban environment, which may be due to a variety of factors
we did not have the opportunity to investigate (e.g. rapid local adap-
tation or phenotypic plasticity). The preference for C displayed by
relatively habituated urban ibis in our study may not be representa-
tive of the wild population. However, given the large population of
ibis in urban centres (8900 ibis in Sydney alone in 2008; Martin et
al. 2010), the preference for C may reflect the behaviour of a rela-
tively large proportion of the population. Ibis preference for high-C
therefore presents several lines of inquiry. Repeating studies such as
this across the ibis’ range and ecological contexts may yield insights
into the dynamics and evolution of nutritional preferences and the
factors involved in pre-adaptation and local-adaptation to urban
environments (McDonnell and Hahs 2015) and urban commensal-
ism (Hulme-Beaman et al. 2016).
CONCLUSIONS AND FUTURE RESEARCH
We have identified that urban ibis show a strong preference for C,
providing novel insights into the nutritional ecology of this suc-
cessful urban wildlife species. The influence of environmental (i.e.
across dierent contexts) and climate variables on the foraging
behavior of ibis will provide insights into how urban habitats have
influenced the nutritional preferences of this species, and more gen-
erally. Furthermore, we believe studies on urban nutritional ecology
can lead to a more holistic understanding of the general processes
underlying urban ecology and human-wildlife conflict, which can
in turn be applied in management strategies. A future priority is to
integrate data of free-ranging urban wildlife with controlled experi-
mental studies (e.g. in free-ranging enclosures). This combined
approach will allow us to better understand the nutritional dimen-
sions of foraging behaviour in complex and competitive nutritional
environments. We believe that ibis represent a potentially valuable
model system for the examining nutritional characteristics of a
highly successful urban wildlife generalist.
SUPPLEMENTARY MATERIAL
Supplementary data are available at Behavioral Ecology online.
FUNDING
S.C.P.C. was supported by the Natural Sciences and Engineering
Research Council (NSERC) of Canada, and an Australian
International Postgraduate Research Scholarship (IPRS) and
Australian Postgraduate Award (APA). GEMC is supported by the
Loxton research fellowship from the Faculty of Veterinary Science,
The University of Sydney.
ACKNOWLEDGMENTS
We thank Tamara King and Richard Burman for assistance in the field. We
thank Dr. Sonia Liu for assistance with experimental feeds.
Data accessibility: Analyses reported in this article can be reproduced using
data provided by Coogan etal. (2017).
Handling editor: Marc Thery
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Page 9 of 9
... graminoids, forbs, and browse), we used mean macronutrient content of dominant species within the study area for each functional forage group. While using macronutrient estimates from the literature may be a crude approach to estimating macronutrient content of food items, such an approach is useful when making dietary comparisons between groups of animals and is an informative method for studying comparative nutritional ecology (Remonti et al. 2016, Coogan et al. 2017. We then converted macronutrient content of individual foods to metabolisable energy values using appropriate conversion factors: 9 kcal g −1 for lipids; 4 kcal g −1 for proteins; and 4 kcal g −1 for carbohydrates (Merrill & Watt 1973). ...
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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.
... In this study we focused on behavioural flexibility and which type of food was consumed, and not on their exact nutritional composition. However the majority of the anthropogenic food items we observed (bread, muffin, and crisps) are generally considered to be carbohydrate rich foods, in keeping with the suggestion that carbohydrates are the most common macronutrient available in human food waste (Coogan et al. 2018), and some species may even shift their dietary preference towards high carbohydrate food resources in urban environments (Coogan et al. 2017). The quality of food items consumed could influence short-term physiological responses as well as long-term evolutionary adaptations: an issue which has still received little attention (but see review in Coogan et al. 2018), however we were unable to assess these effects within the scope of this study. ...
... The time spent foraging by Red-winged Starlings at the UCT was seemingly not dependent on human presence and their associated foods on campus, as they did not respond with increasing foraging effort on days of anthropogenic food shortage. Future research should be aimed at the physiological effects of a predominantly anthropogenic diet as anthropogenic food might be of lower quality (e.g., Andersson et al. 2015;Toledo et al. 2016) or different nutrient composition (Machovsky-Capuska et al. 2015;Peneaux et al. 2017;Coogan et al. 2017) and a high consumption could be costly in terms of bird health (Shochat et al. 2010;Lowry et al. 2012). Exploring how other urban bird species cope with these short-term food fluctuations would improve our understanding of whether the strategy seen here is generalized to other species and may help to understand whether these behaviours are integral to allow species to exploit urban habitats. ...
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Within highly urban systems, anthropogenic activity often fluctuates cyclically, e.g. between weekdays and weekends. Thus, urban species may regularly experience significant changes in human activity and anthropogenic food abundance over very short time scales. Knowledge of how urban birds cope with such fluctuations may improve our understanding of how some species exploit and thrive in urbanised habitats. In this study, we explore the consequences of highly fluctuating anthropogenic food for Red-winged Starlings Onychognathus morio at the University of Cape Town campus, South Africa. Here, high numbers of students (and therefore anthropogenic food resources) are present during weekdays in term time (high human presence “HHP” days). However, students are largely absent and food outlets closed during weekends and vacation periods (“LHP” days). Using focal observations and morning and evening weights of habituated colour-ringed starlings during the non-breeding season, we investigated how diet, behaviour and daily mass gain differed between HHP and LHP days. We hypothesised that anthropogenic food supply is beneficial to this city-dwelling species. We predicted that on HHP days starlings would consume overall more food and a greater proportion of anthropogenic food items, resulting in less time spent foraging and greater daily mass gain compared to LHP days. We found that on HHP days, starlings consumed more anthropogenic food, however overall food intake, and time budgets were similar to LHP days. Additionally, there was an indication that mass gain was greater on HHP days. Thus, starlings appear to cope with potential food shortage on LHP days by including more natural items in their diet.
... Since the nutrient balance and energy maximisation models were designed to be tested at the individual level, the main challenge was to obtain this information for free-living birds that can only be tracked for a short time before losing sight of them (which explains the scarcity of previous studies on dietregulation hypotheses in wild small-sized frugivores). Therefore, our results must be interpreted as the central tendency in the diet of the individuals of a population, whose realised macronutrient niche breadth tends to be greater than that of an individual bird and can smooth out extreme values observed at the individual level (Coogan et al., 2017). ...
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According to diet‐regulation hypotheses, animals select food to regulate the intake of macronutrients or maximise energy feeding efficiency. Specifically, the nutrient balance model proposes that foraging is primarily a process of balancing multiple nutrients to achieve a nutritional intake target, while the energy maximisation model proposes that foraging aims to maximise energy. Here, we evaluate the adjustment of fruit diets (the fruit‐derived component of the diets) to nutritional and energy intake targets, characterizing the nutrient balance and energy maximisation strategies across fruit‐eating bird species with different fruit‐handling behaviours ("gulpers", which swallow whole fruits, and "mashers", which process the fruit in the beak) in subtropical Andean forests. Food‐handling behaviour determines the food intake rate and, consequently, influences animal efficiency to obtain nutrients and energy. We used extensive field data from the diet of fruit‐eating birds to test how species adjust their food intake. We used nutritional geometry to explore macronutrient balance and the effectiveness framework to explore energy‐acquisition effectiveness. Observed diets showed a good fit with predictions of a diet balanced in macronutrient proportions. With few exceptions, diets clustered near an optimal macronutrient mixture and did not differ from each other in terms of maximising energy intake. Moreover, when comparing our results with a random diet based on local fruit availability, birds tended to fit better to the nutritional target, and less to the energy target, than expected from a random diet. Fruit‐handling behaviour did not affect the ability of bird species to reach a nutritional target but it affected species energy acquisition, which was lower in mashers than in gulpers. This study explores for the first time different diet‐regulation strategies in wild fruit‐eating birds, and supports the argument that the diet reflects a specific regulation of macronutrients. Understanding why birds select fruits is a complex question requiring multiple considerations. The nutrient balance model explains the relevance of nutrient composition in the fruit selection by fruit‐eating birds, although it is still necessary to determine its relative importance with respect to other dietary drivers.
... Birds which have been the focus of the majority of urban ecology studies often have access to a multitude of food sources due to human activities including supplementary foods (Galbraith et al., 2015), refuse thrown away by humans in cities which provide easy source of food (Nyari et al., 2006;Burgin and Saunders, 2007). High diversity and availability of food in urban habitats compared to natural ones may be a primary reason why some urban birds thrive (Coogan et al., 2017). ...
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Although the most direct impact of cities on biodiversity is the change in land cover associated with urban growth, large number of species have been recorded to live, and even thrive, within urban centers. The present study was conducted from August 2018 to March 2019 and aimed to investigate the seasonal diversity and habitat association of birds in Bahir Dar city. Semi-forest, wetland, waste dumping site and residential area were habitats identified based on topographic map and ground truthing survey. A total of 100 point count stations within 10 plots of the semi-forest habitat and 550 line transects within 55 blocks of open habitats were used to collect data. Diversity indices, chi-square and ANOVA were employed for data analyses. A total of 186 bird species belonging to 21 orders and 59 families were recorded. The highest diversity of bird species was observed in the residential area during the wet season (H' = 3.78) and the lowest was in waste dumping site during the dry season (H' = 2.11). Test of association between season and habitat types as a function of birds' abundance also confirmed the presence of strong association between season and birds abundance. Availability of food, water and nesting sites were the main players to determine the diversity and abundance of birds within Bahir Dar city. The study area supports large number of bird species that confirms the area's potential for bird watching tourism. Therefore, there must be a collaborative work with the city administration for protecting the urban ecosystem to conserve the biodiversity therein.
... Although anthropogenic food sources (e.g. human discards, pet foods, bird feeders) are suggested to be more abundant and predictable in cities, their nutritional composition often differs from that of natural foods (Coogan et al., 2017(Coogan et al., , 2018Pierotti and Annett, 1987). It has been suggested that abundant urban food sources can be inadequate in terms of allowing individuals to meet their nutritional and physiological needs (Heiss et al., 2009;Liker et al., 2008;Pierotti and Annett, 2001;Pollock et al., 2017;Schoech and Bowman, 2001). ...
Article
Theory suggests that overcrowding and increased competition in urban environments might be detrimental to individual condition in avian populations. Unfavourable conditions could be compounded by changes in dietary niche with additional consequences for individual quality of urban birds. We analysed the isotopic signatures, signal coloration, body condition, parasitic loads (feather mites and coccidia), and immune responsiveness of 191 adult common (Indian) mynas (Acridotheres tristis) captured in 19 localities with differing levels of urbanization. The isotopic signature of myna feathers differed across low and high urbanized habitats, with a reduced isotopic niche breadth found in highly urbanized birds. This suggests that birds in high urban environments may occupy a smaller foraging niche to the one of less urbanized birds. In addition, higher degrees of urbanization were associated with a decrease in carotenoid-based coloration, higher ectoparasite loads and higher immune responsiveness. This pattern of results suggests that the health status of mynas from more urbanized environments was poorer than mynas from less modified habitats. Our findings are consistent with the theory that large proportions of individual birds that would otherwise die under natural conditions survive due to prevailing top-down and bottom-up ecological processes in cities. Detrimental urban ecological conditions and search for more favourable, less crowded habitats offers the first reasonable explanation for why an ecological invader like the common myna continues to spread within its global invasive range.
... Urban land cover was the strongest driver of microbial community composition and is itself associated with many biotic and abiotic factors. Urban ibis in Australia also consume provisioned bread in parks and select for high-carbohydrate rather than high-protein foods [46]. The relative importance of macronutrients is an important predictor of microbiome composition across species [47] and so may be at least partially driving the shifts we observed in phylum relative abundance. ...
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Microbial communities in the gastrointestinal tract influence many aspects of host health, including metabolism and susceptibility to pathogen colonization. These relationships and the environmental and individual factors that drive them are relatively unexplored for free-living wildlife. We quantified the relationships between urban habitat use, diet, and age with microbiome composition and diversity for 82 American white ibises (Eudocimus albus) captured along an urban gradient in south Florida and tested whether gut microbial diversity was associated with Salmonella enterica prevalence. Shifts in community composition were significantly associated with urban land cover and, to a lesser extent, diets higher in provisioned food. The diversity of genera was negatively associated with community composition associated with urban land cover, positively associated with age class, and negatively associated with Salmonella shedding. Our results suggest that shifts in both habitat use and diet for urban birds significantly alter gut microbial composition and diversity in ways that may influence health and pathogen susceptibility as species adapt to urban habitats.
... The proportions-based nutritional geometry enables direct interpretation of the interactions among nutrients and pollutants as foods consumed (Raubenheimer, 2011). This approach has contributed to our knowledge of the nutritional decisions of animals in response to anthropogenic pressures in the form of environmental fluctuations (Rothman et al., 2015;Machovsky-Capuska et al., 2018) and urbanization (Coogan et al., 2017(Coogan et al., , 2018Machovsky-Capuska et al., 2015). Recently proportions-based nutritional geometry has allowed researchers to move beyond food-level dimensions to the dietary niche adding a nutrient-level component in a Multidimensional Nutritional Niche Framework (MNNF, Machovsky-Capuska et al., 2016). ...
Article
Little attention has been drawn toward the effects of marine debris ingestion in relation to nutrient acquisition and fitness consequences. We tested whether anthropogenic debris ingestion influence the nutritional niches of endangered green turtles (Chelonia mydas) in estuarine and reef habitats on the Brazilian coast. Our results showed that estuarine turtles consumed diets with lower proportional wet mass composition of protein (P) and water (W) than their reef conspecifics. The amounts of debris, mostly plastics, retrieved from the digestive tracts of estuarine turtles were higher compared with those individuals from reefs. The realized nutritional niche from estuarine turtles was subject to the debris density in the environment, lack of benthic food resources available and the surface foraging behavior, likely preventing them from reaching their nutritional goals and resulting in lower fitness. The study provides critical information for the management and conservation of ecologically threatened individuals, populations, and their natural habitats. To access pdf: https://authors.elsevier.com/a/1aX9t,ashxl5A
... Therefore, most existing studies of nutritional balancing in the field deal with vertebrates, e.g. birds whose feeding behavior can be readily observed (Tait et al. 2014;Machovsky-Capuska et al. 2016bc; Coogan et al. 2017), or herbivorous or omnivorous mammals (Felton et al. 2009; Rothman et al. ...
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Habitats vary in food resources with carnivores often being prey limited, but it is unclear whether habitats facilitate a nutritionally balanced diet. Two paradigms in nutritional ecology, ecological stoichiometry and nutritional geometry, predict that carnivores are limited mainly by protein or lipid, respectively. Using the carabid beetle Anchomenus dorsalis and 10 other predatory beetles from agricultural fields, we developed and tested two simple procedures for quantifying macronutrient‐specific habitat conditions without requiring information about the natural prey. Both procedures assume that predators forage for nutrients rather than specific prey. Our results show that 10 of 11 species were food limited. Five species were lipid limited and one species was protein limited in the field. Co‐existing predator species showed considerable segregation of fundamental macronutritional niches. A linear relationship between specific nutrient limitation and the target lipid:protein (L:P) intake ratio indicates that species with high L:P target are more protein limited while species with low L:P target are more lipid limited. The study illustrates how species within a natural assemblage vary in nutritional niche and in specific nutrient limitation. This article is protected by copyright. All rights reserved.
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The nutritional characteristics of food resources play an important role in the foraging behavior of animals and can provide information valuable to their conservation and management. We examined the nutritional ecology of wild water buffalo (Bubalus arnee ; hereafter “buffalo”) in the Koshi Tappu Wildlife Reserve of Nepal during autumn using a multidimensional nutritional niche framework. We identified 54 plant species as being foraged by buffalo. We found that buffalo consumed graminoids and forbs 2–3 times more frequently than browse items. Proximate analyses of the 16 most frequently foraged plants indicated that buffalo diets were highest in carbohydrate (40.41% ± 1.82%) followed by crude protein (10.52% ± 0.93%) and crude fat (1.68% ± 0.23%). The estimated macronutrient balance (i.e., realized nutrient niche) of the buffalo diet (20.5% protein: 72.8% carbohydrate: 6.7% lipid) was not significantly different than the average balance of all analyzed food items based on 95% confidence regions. Our study suggests that buffalo are likely macronutrient specialists, yet may be generalists in the sense that they feed on a wide range of food items to achieve a nutrient balance similar to that available in forage items. However, the four most frequently consumed items tended to be higher in protein energy than less frequently consumed foods, suggesting some preference for higher protein forage relative to relatively abundant carbohydrates. Although limited in scope, our study provides important information on the nutritional ecology of buffalo, which may be useful for the conservation and management of this endangered species.
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Foraging decisions tend to drive individuals toward maximising energetic gains within a patchy environment. This study aims to determine the extent to which rainfall, and associated changes in food availability, can explain foraging decisions within a patchy urbanised landscape, using the Australian white ibis as a model species. Ibis density, food consumption rates and food abundance (both natural and anthropogenic) were recorded during dry and wet weather within urban parks in Sydney, Australia. Rainfall influenced ibis density in these urban parks. Of the four parks assessed, the site with the highest level of anthropogenic food and the lowest abundance of natural food (earthworms), irrespective of weather, was observed to have three times the density of ibis. Rainfall significantly increased the rate of earthworm consumption as well as their relative availability in all sites. Overall, these density and consumption measures indicate that anthropogenic derived foods, mainly from direct feeding by people, explain the apparent distribution of ibis across urban parks. However, there was evidence of prey-switching when the availability of natural foods increased following rainfall, perhaps reflecting selection of particular nutrients.
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Anthropogenic environments can offer rich sources of energy to urban wildlife, but little is known about how they impact on nutritional balance and food selection. Common mynas (Sturnus tristis) provide a powerful model system for testing the nutritional constraints and priorities of an invasive species that has successfully adapted to urban environments. Here, we use behavioral observations, field-based feeding trials, videography, and the right-angled mixture triangle model (RMT) to examine the macronutrient preferences of these invasive birds. Our behavioral observations showed that mynas consumed insects (40.6%), worms (33.2%), human discards (17.6%), and plants (8.6%). Our feeding trials using nutritionally defined foods showed that mynas had a clear preference for food dishes containing only high-protein (HP) pellets over high-lipid (HL) or high-carbohydrate (HC) pellets. In addition, mixed feeders were also presented in 2 combinations: 1) contained equal proportions of HP and HC pellets and 2) equal proportions of HP and HL pellets. HP pellets were selectively consumed from both mixed feeders, this involving an increase in feeding time. Overall, the RMT showed that mynas consumed a higher proportion of protein from the feeders than in their natural diet. Furthermore, the majority of our observations of birds feeding at the dishes containing HP foods ended in intraspecific aggression, suggesting that protein is a contestable resource. These results suggest that mynas at our urban study site are deficient in protein relative to fats and carbohydrates.
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Commensalism within anthropogenic environments has not been extensively discussed, despite its impact on humans, and there is no formal framework for assessing this ecological relationship in its varied forms. Here, we examine commensalism in anthropogenic environments in detail, considering both ecological and evolutionary drivers. The many assumptions about commensalism and the nature of anthropogenic environments are discussed and we highlight dependency as a key attribute of anthropogenic commensals (anthrodependent taxa). We primarily focus on mammalian species in the anthropogenic-commensal niche, but the traits described and selective pressures presented are likely fundamental to many species engaged in intense commensal relationships with humans. Furthermore, we demonstrate that this largely understudied interaction represents an important opportunity to investigate evolutionary processes in rapidly changing environments.
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Background The migratory patterns of animals are changing in response to global environmental change with many species forming resident populations in areas where they were once migratory. The white stork (Ciconia ciconia) was wholly migratory in Europe but recently guaranteed, year-round food from landfill sites has facilitated the establishment of resident populations in Iberia. In this study 17 resident white storks were fitted with GPS/GSM data loggers (including accelerometer) and tracked for 9.1 ± 3.7 months to quantify the extent and consistency of landfill attendance by individuals during the non-breeding and breeding seasons and to assess the influence of landfill use on daily distances travelled, percentage of GPS fixes spent foraging and non-landfill foraging ranges. Results Resident white storks used landfill more during non-breeding (20.1 % ± 2.3 of foraging GPS fixes) than during breeding (14.9 % ± 2.2). Landfill attendance declined with increasing distance between nest and landfill in both seasons. During non-breeding a large percentage of GPS fixes occurred on the nest throughout the day (27 % ± 3.0 of fixes) in the majority of tagged storks. This study provides first confirmation of year-round nest use by resident white storks. The percentage of GPS fixes on the nest was not influenced by the distance between nest and the landfill site. Storks travelled up to 48.2 km to visit landfills during non-breeding and a maximum of 28.1 km during breeding, notably further than previous estimates. Storks nesting close to landfill sites used landfill more and had smaller foraging ranges in non-landfill habitat indicating higher reliance on landfill. The majority of non-landfill foraging occurred around the nest and long distance trips were made specifically to visit landfill. Conclusions The continuous availability of food resources on landfill has facilitated year-round nest use in white storks and is influencing their home ranges and movement behaviour. White storks rely on landfill sites for foraging especially during the non-breeding season when other food resources are scarcer and this artificial food supplementation probably facilitated the establishment of resident populations. The closure of landfills, as required by EU Landfill Directives, will likely cause dramatic impacts on white stork populations.
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Considerable progress has been made in understanding both evolutionary and mechanistic aspects of biological aging, although the two areas remain poorly integrated. We suggest that a greater emphasis on ecology can help to remedy this, by focusing on the interface between biological mechanisms and the environments in which they evolved by natural selection. Among the most salient aspects of the environment relevant to aging is nutrition, and yet in the bulk of aging research nutrition is coarsely represented as dietary restriction or caloric restriction, without consideration for how specific components of diet, beyond "energy" (the undifferentiated mix of macronutrients), are driving the observed effects. More recently, it has become clear that specific nutrients (notably amino acids) and interactions among nutrients (i.e., nutritional balance) play important roles in the biology of aging. We show how a method developed in nutritional ecology, called the Geometric Framework for nutrition, can help to understand the nutritional interactions of animals with their environments, by explicitly distinguishing the roles of calories, individual nutrients and nutrient balance. Central to these models are the active regulatory responses that animals use to mediate between variation in the nutritional environment and fitness-related consequences such as lifespan and reproduction. These homeostatic responses provide a guide for researchers that can help to link the biological mechanisms with evolutionary processes in the context of a multi-dimensional nutritional environment.
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The dietary generalist-specialist distinction plays a pivotal role in theoretical and applied ecology, conservation, invasion biology, and evolution and yet the concept remains poorly characterised. Diets, which are commonly used to define niche breadth, are almost exclusively considered in terms of foods, with little regard for the mixtures of nutrients and other compounds they contain. We use nutritional geometry (NG) to integrate nutrition with food-level approaches to the dietary niche and illustrate the application of our framework in the important context of invasion biology. We use an example that involves a model with four hypothetical nonexclusive scenarios. We additionally show how this approach can provide fresh theoretical insight into the ways nutrition and food choices impact trait evolution and trophic interactions.