Multidimensional nutritional ecology and urban birds

Abstract

There is growing interest in the question of how urbanization affects the ecology of birds, across timescales from relatively short‐term physiological responses to long‐term evolutionary adaptation. The ability to gain the required nutrients in urban habitats is a key trait of successful urban birds. Foraging behavior, in itself, increasingly is recognized as a complex nutritional phenomenon, where the ratios, proportions, and amounts of macronutrients (protein, carbohydrate, and lipid) in foods, meals, and diets have been shown to exert a driving influence. Yet, despite the rising trend of urbanization, the importance of food quality and quantity in urban ecology, and the growing evidence demonstrating the pervasive and sometimes complex role of macronutrients in foraging behavior, the nutritional ecology of urban birds remains poorly understood. Here, we review the foraging behavior and role of macronutrients in the ecology of urban birds and demonstrate how incorporating a multidimensional approach to nutrition can provide new insights into their urban ecology. To that end, we demonstrate how a macronutrient‐based view can aid in understanding the relationships between natural, anthropogenic, and supplementary foods. We then provide an overview of multidimensional nutritional niche concepts that can be used to generate explanatory and predictive models for urban bird ecology. We conclude that multidimensional nutritional ecology provides an appropriate framework for understanding the roles that nutrition plays in the relationships between urban birds and their environments.

Full text

CONCEPTS & THEORY
Multidimensional nutritional ecology and urban birds
SEAN C. P. COOGAN ,
1,2,

DAVI D RAUBENHEIMER,
1
SIMON P. ZANTIS,
1
AND GABRIEL E. MACHOVSKY-CAPUSKA
1
1
School of Life and Environmental Sciences and the Charles Perkins Centre, University of Sydney, Sydney, NSW 2006 Australia
2
Department of Renewable Resources, University of Alberta, Edmonton, Alberta T6G 2H1 Canada
Citation: Coogan, S. C. P., D. Raubenheimer, S. P. Zantis, and G. E. Machovsky-Capuska. 2018. Multidimensional
nutritional ecology and urban birds. Ecosphere 9(4):e02177. 10.1002/ecs2.2177
Abstract. There is growing interest in the question of how urbanization affects the ecology of birds,
across timescales from relatively short-term physiological responses to long-term evolutionary adapta-
tion. The ability to gain the required nutrients in urban habitats is a key trait of successful urban
birds. Foraging behavior, in itself, increasingly is recognized as a complex nutritional phenomenon,
where the ratios, proportions, and amounts of macronutrients (protein, carbohydrate, and lipid) in
foods, meals, and diets have been shown to exert a driving influence. Yet, despite the rising trend of
urbanization, the importance of food quality and quantity in urban ecology, and the growing evidence
demonstrating the pervasive and sometimes complex role of macronutrients in foraging behavior, the
nutritional ecology of urban birds remains poorly understood. Here, we review the foraging behavior
and role of macronutrients in the ecology of urban birds and demonstrate how incorporating a multi-
dimensional approach to nutrition can provide new insights into their urban ecology. To that end, we
demonstrate how a macronutrient-based view can aid in understanding the relationships between nat-
ural, anthropogenic, and supplementary foods. We then provide an overview of multidimensional
nutritional niche concepts that can be used to generate explanatory and predictive models for urban
bird ecology. We conclude that multidimensional nutritional ecology provides an appropriate frame-
work for understanding the roles that nutrition plays in the relationships between urban birds and
their environments.
Key words: birds; foraging behavior; macronutrients; multidimensional nutritional niche; nutritional ecology;
supplementary food; urban ecology.
Received 13 June 2017; revised 8 February 2018; accepted 27 February 2018. Corresponding Editor: Paige Warren.
Copyright: ©2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution
License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
E-mail: sean.c.p.coogan@gmail.com
INTRODUCTION
Urbanization, broadly defined as the substitu-
tion of natural ecosystems with anthropogenic
features, has a variety of habitat-altering impacts
operating on different spatial and temporal
scales (McKinney 2002, Kalnay and Cai 2003,
Grimm et al. 2008, Lowry et al. 2013, McDonnell
and Hahs 2015). Urban habitat alterations can
present a wide range of challenges to wildlife
species adapted to pre-existing natural condi-
tions, yet can provide opportunities to species
that are preadapted or have high levels of adapt-
ability to urban conditions (McKinney 2002,
2006, McDonnell and Hahs 2015). These habitats
can thus result in novel ecosystems and associ-
ated species assemblages that have no natural or
historic analogue (Fox 2007, Hobbs and Cramer
2008, Seastadt et al. 2008). The suite of novel con-
ditions and intense selection pressures in urban
habitats provides the potential to study ecology
and evolution under unprecedented environ-
mental conditions (Diamond 1986, Hahs and
Evans 2015).
❖www.esajournals.org 1April 2018 ❖Volume 9(4) ❖Article e02177

Central to surviving in urban habitats is the
ability of wildlife to meet nutritional require-
ments in the face of altered or novel nutritional
environments. Birds (Aves), 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 supplemen-
tary foods (e.g., bird feeders; Galbraith et al.
2015), anthropogenic food waste (Smith and Car-
lile 1993), and vegetation changes (e.g., planted
native and non-native food-bearing trees; Burgin
and Saunders 2007).
The increased diversity and availability of
foods in urban habitats compared to natural ones
may be a primary reason that some urban birds
thrive (Clergeau et al. 1998, Coogan et al. 2017).
Species able to exploit urban food resources are
likely to experience considerable effects on their
biology, including body mass, song behavior,
migration, and population density and distribu-
tion, among others (Auman et al. 2008, Robb
et al. 2008, Saggese et al. 2011, Martin et al.
2012, Amrhein 2013). However, bird species dif-
fer in their ability to forage in urban habitats,
resulting in changes in bird community composi-
tion (McKinney 2006, Ducatez et al. 2015, Gal-
braith et al. 2015).
Foraging behavior in itself is a complex phe-
nomenon, involving the interplay of homeostatic
regulatory mechanisms that mediate the nutri-
tional preferences and requirements of animals
with their nutritional environment (Rauben-
heimer et al. 2012). Empirical and theoretical
studies from the field of nutritional ecology (i.e.,
the study of the nutritional interactions between
organisms and their environments) have demon-
strated the power of multidimensional nutri-
tional models in predicting and explaining
foraging behavior (Simpson and Raubenheimer
2012, Machovsky-Capuska et al. 2016a). The
multidimensional approach contrasts more tradi-
tional approaches which employ a single nutri-
tional currency, such as protein or energy
(Simpson et al. 2015, Coogan and Raubenheimer
2016).
In particular, nutritional ecology studies have
demonstrated that the amounts, concentrations,
and ratios of macronutrients (protein, carbohy-
drate, and lipid) in foods and diets can strongly
influence animal foraging behavior, including
homeostatically regulated intake in the face
of both optimal and imbalanced nutritional
environments (Raubenheimer and Simpson 1993,
Simpson and Raubenheimer 1993). This macronu-
trient-focused approach has been broadly applied
from individuals to populations (Simpson and
Raubenheimer 2012), and across a wide range of
nutritionally influenced research disciplines,
including wildlife ecology and conservation
(Raubenheimer and Simpson 2006, Rothman
et al. 2011, Raubenheimer et al. 2012, Coogan
et al. 2014, human–wildlife conflict (Coogan and
Raubenheimer 2016), biological invasions (Sword
et al. 2010, Machovsky-Capuska et al. 2016b,
Peneaux et al. 2017), and companion animal
nutrition (Raubenheimer et al. 2015a, Gosper
et al. 2016).
Despite the rising trend of urbanization, the
importance of urban food resources in urban
ecology, and the growing weight of evidence
demonstrating the influence of specific macronu-
trients in foraging, the nutritional ecology of
urban birds remains poorly understood. The pur-
pose of this paper is to (1) review some key
aspects of foraging behavior and macronutrition
in the ecology of urban birds thereby establishing
their importance; (2) demonstrate how incorpo-
rating a multidimensional approach to nutrition
can provide new insights into this line of
research; and (3) suggest future research priori-
ties and present our conclusions.
URBAN FORAGING AND MACRONUTRITION
Foraging behavior in urban environments
In order to meet their nutritional and foraging
goals, urban birds must deal with multiple chal-
lenges, including the nutritional characteristics of
available foods (e.g., natural vs anthropogenic;
Coogan et al. 2017), the ability to tolerate distur-
bance (Lowry et al. 2013), and the ability to deal
with strong intra- and inter-specific competition
(Shochat et al. 2004, Machovsky-Capuska et al.
2016c, Coogan et al. 2017). Birds foraging in
urban habitats may be bolder than rural con-
specifics (Evans et al. 2010), while at the same
time being more neophobic toward novel fea-
tures in the environment (Audet et al. 2015).
Anthropogenic foods can distort the diets of
urban species to various extents. Diet analysis of
Australian silver gulls (Larus novaehollandiae)
revealed that 85% of stomach contents contained
❖www.esajournals.org 2April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

exclusively human discards (Smith and Carlile
1993), supporting previous suggestions regard-
ing the tendency of gulls (Larus spp.) to exploit
anthropogenic foods (i.e., an urban exploiter;
Harris 1965). Approximately 38% of energy con-
sumed per hour by suburban Florida scrub jays
(Aphelocoma coerulescens) was composed of pea-
nuts and other miscellaneous anthropogenic
foods (Fleischer et al. 2003). Approximately 15%
of the diet provisioned to nestlings of both great
(Parus major) and blue tits (Parus caeruleus)ina
suburban habitat was composed of anthro-
pogenic foods (Cowie and Hinsley 1988). Like-
wise, Australian magpie (Cracticus tibicen) used
only minor quantities of available anthropogenic
foods both when foraging and provisioning
young (O’Leary and Jones 2006).
Birds tend to reduce their foraging home range
when provisioned with additional food (Boutin
1990, Moritzi et al. 2001). A comparison between
Florida scrub jays foraging in wild habitats (with
access to natural foods) with conspecifics forag-
ing in suburban areas (with access to anthro-
pogenic foods) showed that suburban birds had
more efficient foraging trips (spent less time for-
aging and handled more food per foraging hour)
than their wild counterparts (Fleischer et al.
2003). Black-tailed gulls (Larus crassirostris) con-
sumed natural and human-related foods, show-
ing shorter foraging trips (in range and distance
traveled) when exploiting urban feeding grounds
in comparison with their oceanic resources (Yoda
et al. 2012).
The availability of anthropogenic foods has
also influenced the migratory behavior of popu-
lations of European white storks (Ciconia ciconia)
and Australian white ibis (Threskiornis molucca),
which have switched from seasonal migration to
year-round residency in association with landfills
(Martin et al. 2012, Gilbert et al. 2016). There has
been a major shift in the diversity and abundance
of parrots in the Sydney region (Australia; AU)
over the last century, with supplementary feed-
ing and the planting of food-bearing native and
non-native vegetation likely being major drivers
(Burgin and Saunders 2007).
Anthropogenic food sources are often highly
predictable in space and time (Oro et al. 2013),
resulting in greater foraging efficiency (Fleis-
cher et al. 2003). However, urban habitats can
be highly variable and might not completely
shield urban wildlife from environmental fac-
tors (Hulme-Beaman et al. 2016). For instance,
the foraging behavior and macronutrient selec-
tion of urban Australian white ibis in Sydney
were found to be influenced by the amount of
recent rainfall (Chard et al. 2017, Coogan et al.
2017).
Reproduction
Both the amounts and proportions of mac-
ronutrients consumed have been shown to influ-
ence reproductive parameters in various model
organisms, including both invertebrates (e.g.,
Jensen et al. 2012) and vertebrates (e.g., Solon-
Biet et al. 2015)—importantly, reproductive mea-
sures were optimized on diets containing specific
amounts and proportions of macronutrients.
Likewise, reproduction in free-ranging herring
gulls (Larus argentatus) has been linked to the
nutritional characteristics of available food rather
than energy per se (Pierotti and Annett 1991).
Anthropogenic foods have also been shown to
affect avian reproductive performance. There
was a positive correlation between garbage in
the diet and fledging rate in the glaucous gull
(Larus hyperboreus; Weiser and Powell 2010).
Reproductive success in European white storks
decreased with distance from artificial feeding
sites by 8% per kilometer (Hilgartner et al. 2014).
Conversely, overwinter fat supplementation
impaired spring egg production in blue tits
(Plummer et al. 2013), and breeding success did
not significantly differ between white storks fed
supplementary food vs. those that were not
(Moritzi et al. 2001).
Research on the life history of seasonally
breeding birds suggests that the quantity of food
available to adults acts as a proximate cue in the
timing of reproduction (Davies and Deviche
2014). Studies aimed at understanding this rela-
tionship have generally shown that food supple-
mentation advances laying date and clutch
initiation date across a diverse range of birds
(Robb et al. 2008). Less research, however, has
explored the relationship between the nutritional
composition (i.e., quality) of supplemented food
and reproductive timing of free-ranging birds
(Davies and Deviche 2014). Those studies that
have investigated the role of macronutrients in
initiating egg production tended to focus on one
or two nutrients (i.e., protein and/or lipid), but
❖www.esajournals.org 3April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

not the balance of nutrients. Protein or amino
acid content has been suggested as a limiting fac-
tor in initiating egg production (Meijer and Drent
1999, Schoech and Bowman 2003), while protein
and lipid content of pre-breeding diet influenced
laying date, egg size and composition, and clutch
size in the Florida scrub jay (Reynolds et al.
2003). However, protein and/or fat supplementa-
tion did not advance the lay date of lesser black-
backed gulls (Larus fuscus; Bolton et al. 1992),
great tits (Nager et al. 1997), or blue tits (Ramsay
and Houston 1997). Captive mallards (Anas
platyrhynchos) likewise did not experience an
advance in laying date when fed an enriched
high-protein diet vs. wheat (Eldridge and Krapu
1988); however, mallards on the high-protein diet
experienced increased clutch size, egg mass, lay-
ing rate, nesting attempts, and total eggs laid, in
addition to differences in egg composition (i.e.,
increased yolk mass and percentage dry matter,
with a relatively constant percentage of lipids).
Studies investigating the effects of single-
nutrient manipulations are likely to overlook the
interactive effects of multiple nutrients (Simpson
et al. 2015). Therefore, these contrasting respo-
nses to dietary supplementation might be better
explained by adopting a multidimensional nutri-
tional perspective. Regardless of the source (i.e.,
natural vs. anthropogenic), the amounts and pro-
portions of nutrients in foods consumed by
urban birds have the potential to influence their
nutritional state (sensu Simpson and Rauben-
heimer 2012) toward, or further away from, what
is optimal for reproduction. Thus, experiments
that systematically vary the amounts and pro-
portions of multiple nutrients offered will pro-
vide valuable information on the nutritional
basis for optimum reproduction, and the conse-
quences of dietary imbalance (Raubenheimer
et al. 2016).
Diet and nutrition are also linked to other key
reproductive traits in birds. Mate selection is
often based on traits that indicate potential mate
quality that are energetically and nutritionally
costly to maintain, such as singing behavior and
plumage coloration (Zahavi 1975, Cotton et al.
2004). Plumage coloration in the form of melanin
production and carotenoids can be influenced by
dietary factors (Veiga and Puerta 1996, Klasing
1998, Roulin 2016). The effects of malnutrition on
bird coloration have been observed in house
finches (Carpodacus mexicanus; Hill 2000), house
sparrow (Passer domesticus), and the brown-
headed cowbird (Molothrus ater; McGraw et al.
2002).
Immunity and health
Animals may adjust food selection to support
immune components that best resist a given
infection, and perhaps support a healthy micro-
bial community (Ponton et al. 2011). Birds are
known to adjust food selection and eat soils to
self-medicate (Diamond 1999, Bravo et al. 2014).
Immune defense is important for brain function
and cognitive abilities in birds, such as feeding
innovation (Sol et al. 2002, 2005, Møller et al.
2005). Yet, feeding innovation comes at the cost
of increased exposure to pathogens (Vas et al.
2011, Soler et al. 2012). Given the positive rela-
tionships between brain size, feeding innovation,
and immune defense, feeding innovation may
have co-evolved with brain size, giving rise to a
relationship between immune defense and inno-
vation (Garamszegi et al. 2007). A study of bull-
finch (Loxigilla barbadensis) found that urban
birds were better at problem solving and had
enhanced immunocompetence compared to rural
conspecifics (Audet et al. 2015).
Anthropogenic foods may have adverse effects
on the health of urban birds if they contribute
toward imbalancing the diet thus leading to mal-
nutrition. For example, nutritional imbalance is
implicated as a primary cause of angel wing dis-
order (Kreeger and Waiser 1984, Zsivanovits
et al. 2006). Supplementary feeding in urban
ecosystems may also have indirect effects on bird
health, as wild bird feeding stations have been
suggested to facilitate the transmission of avian
disease (Robinson et al. 2010, Lawson et al.
2012).
MULTIDIMENSIONAL NUTRITIONAL ECOLOGY
AND URBAN BIRDS
Investigating the influence of macronutrition
on biological outcomes, such as those discussed
in the previous section, requires a visual format
that accommodates three-dimensional interac-
tions. Mixture triangles are one such format that
naturally lend themselves to plotting macronutri-
ent proportions within a simplex, with each
macronutrient represented on one of the
❖www.esajournals.org 4April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

triangle’s axes (i.e., sides). While conventional
ternary diagrams (i.e., equilateral mixture trian-
gles) have been around for some time, the more
recently developed right-angled mixture triangle
(RMT) has been increasingly used to examine
both empirical and theoretical aspects of nutri-
tional ecology (Raubenheimer 2011). Because the
RMT is a relatively recent development (~2011),
we provide a brief overview of its use before
applying it to demonstrate multidimensional
nutritional niche concepts relevant to urban
birds.
In Fig. 1A, we plot in an RMT the macronutri-
ent composition (protein, lipid, and carbohydrate
on the x-, y-, and z-axes, respectively) of a variety
of hypothetical foods as points representing the
percentage of energy contributed by each to total
macronutrient energy. The macronutrients in the
RMT are modeled as proportions of their sum;
thus, any value of the implicit axis, z, in the plot
Fig. 1. (A) Right-angled mixture triangle (RMT) illustrating three-component macronutrient mixtures
expressed as a percentage of total macronutrient-derived energy. Protein and lipid are plotted on the x- and y-
axes respectively, as in traditional x–yplots. Carbohydrate is modeled on the implicit z-axis, the values of which
can be read along the negatively sloped lines. The value of carbohydrate (z) is the same anywhere along a partic-
ular z-axis line, where the position of the point on this line is determined by the ratio of protein to lipid. For
example, two foods containing 50% carbohydrate have been plotted, each with different percentages of protein
and lipid. The value of carbohydrate on the z-axis also decreases inversely to the origin of the plot: Points at the
origin contain 100% carbohydrate energy, while points that lie on the hypotenuse contain 0% carbohydrate
energy. (B) Conceptual RMT illustrating how the percent energy balance of macronutrients in a variety of hypo-
thetical foods (squares), meals (triangles), and diets (circles) can be incorporated into a single model. A polygon
(i.e., triangle) connecting the three foods forms a mixture space in which the macronutrient proportions of meals
can be composed by consuming some amount of the three foods (triangles with black outline). Meals composed
of only two foods are constrained to lie somewhere on the line joining the respective foods. Meals outside of the
food mixture space (gray triangles) cannot be composed from the three foods alone. Similarly, diets composed of
meals are constrained to fall within the mixture space of the meals consumed. The diet represented by the black
circle could be composed of meals containing only the three foods. The diet represented by the gray circle repre-
sents a diet that could be composed from the broader array of meals that have incorporated other hypothetical
foods (not shown). The empty circle represents a diet that lies outside the bounds of the possible mixture space
for meals.
❖www.esajournals.org 5April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

is equal to 100 (x+y). Because of this, a par-
ticular value on the z-axis is represented by a
negatively sloped line, such that any point along
this line equates to the same proportion of carbo-
hydrate with co-varying proportions of protein
and lipid. Since any increase in the z-variable is
by definition offset by a decrease in the x- and/or
y-variables, the z-value increases as the diagonal
lines approach the x–yorigin. In Fig. 1B, we
show how the RMT can be used to model a hier-
archy of macronutrient compositions in the
foods, meals, and diets consumed by an animal
(Raubenheimer and Simpson 2016).
Characterizing the urban nutritional environment
An important step in understanding the nutri-
tional ecology of animals is to characterize their
relevant nutritional environment. A diversity of
foraging modes exists among bird species, each
with their own associated anatomical and physi-
ological adaptations (Klasing 1998). Given the
large range of feeding modes, the nutritional
composition of natural foods consumed by birds
varies widely, to which they have acquired a
suite of morphological, physiological, and meta-
bolic adaptations (Stevens and Hume 1995, Klas-
ing 1998, Baldwin et al. 2014). Similar types of
foods often have similar average macronutrient
compositions (Klasing 1998, Coogan et al. 2014),
despite sometimes considerable intra- and inter-
specific variance (Rothman et al. 2012, Tait et al.
2014). For this reason, specific food items are
often placed into broad food categories (e.g., soft
fruit, insects) in nutritional studies. To illustrate,
in Fig. 2A we plot the proportion of macronutri-
ents (% metabolizable energy) and region of
nutrient space occupied by a variety of common
food groups consumed by birds, using data from
Klasing (1998; Appendix S1).
Anthropogenic food subsidies are an impor-
tant feature of urban habitats (Oro et al. 2013).
Deliberate wild bird feeding has been suggested
to be the most popular and widespread form of
human–wildlife interaction globally (Jones 2011).
Approximately 64% of households in the United
Kingdom (UK) participated in the activity
(Davies et al. 2012), 43% in the United States
(Martinson and Flaspohler 2003), 47% in New
Zealand (NZ; Galbraith et al. 2015), and 36–48%
in suburban and rural AU (Ishigame and Baxter
2007). Anthropogenic food available to urban
species may also be unintentional, for example,
through human waste, refuse, or fishing discards
(Oro et al. 2013).
A few studies of supplementary bird feeding
have identified the types of foods offered in the
UK, the United States, NZ and AU. In the UK, it
was estimated that up to 60 million kg of food
(mainly peanuts and bird seed) is supplied to
wild birds annually (Glue 2006), whereas in 2002
over 450 million kg of seed was fed to wild birds
in the United States (as cited in Jones 2011). In
NZ, a survey encompassing six cities represent-
ing approximately 42% of the total population
estimated that 5.1 million loaves of bread, along
with 13.6 million pieces of fruit, 1.8 million kg of
seed, and 5.3 million L of sugar–water, was sup-
plied to wild birds per annum (Galbraith et al.
2015). An AU study found that 58% of respon-
dents surveyed provided bread, which was the
most common food reported, followed by mince
(32%), seed (22%), cheese (22%), and commercial
feed (20%), among others (Rollinson et al. 2003).
With such large quantities of food being intro-
duced to ecosystems on a year-round basis (Roll-
inson et al. 2003, Horn and Johansen 2013, Orros
and Fellowes 2015)—enough energy and nutri-
ents to hypothetically support 300 million chick-
adees annually in the United States (Robb et al.
2008)—it is not surprising that supplementary
feeding has been identified as one of the main
factors affecting the structure of urban bird com-
munities. Food supplementation research sug-
gests that the practice generally supports an
increase in invasive over native species. A NZ
study found that the abundance of invasive
house sparrow and spotted dove (Streptopelia chi-
nensis) increased with supplementary feeding,
while there was a negative effect on native gray
warbler (Gerygone igata; Galbraith et al. 2015).
Supplementary feeding has been suggested to
influence the distribution of birds, such as the
American goldfinch (Carduelis tristis) and north-
ern cardinal (Cardinalis cardinalis) which have
shifted northward in range in the United States
likely in keeping with supplementary feeding
practices (Robb et al. 2008).
As in the aforementioned studies, identifying
the types of foods consumed by urban birds is a
critical step in understanding their foraging
behavior. However, a multidimensional approach
to nutritional ecology goes beyond the level of
❖www.esajournals.org 6April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

identifying foods consumed, by also considering
the mixtures of nutrients that comprise those
foods and the diets that are assembled from those
foods. This nutritionally complex dimension
could add considerable predictive power to
foraging models of urban birds. Urban environ-
ments are likely to provide a wide range of
macronutrient combinations from available foods
(e.g., supplementary foods, food waste, planted
vegetation) and may be differentially available
among urban habitat types (e.g., residential areas,
commercial areas, landfills, parks).
In Fig. 2B, we plot the proportions of
macronutrient energy in a variety of the most
popular supplementary foods offered to wild
birds (Appendix S1: Table S1). The macronutrient
proportions of these supplementary feeds vary
widely, suggesting that urban birds have access
to a potentially wide range of macronutrient
mixtures from which to compose their diet. Such
complex environments are likely favorable to
generalists for which foods can easily be comple-
mented. Supplementary foods may also serve as
substitutes to natural foods for specialists (e.g.,
fruit, seeds, or sugar–water solutions) if they are
sufficiently similar in macronutrient composition
(Fig. 2A), provide the required micronutrients,
and are physically and ecologically suited to
being exploited by the birds. In this respect, diet-
ary specialists may also encounter favorable
nutritional environments in urban habitats.
The proportion of macronutrients available
from provisioned supplementary feeds may differ
from those typically found in scavenged anthro-
pogenic food waste. Carbohydrate is likely the
most common macronutrient available in human
food waste, and to a lesser extent lipids, due to
the relatively high frequency of these macronutri-
ents in anthropogenic foods and lower monetary
cost relative to protein (Brooks et al. 2010, Coogan
and Raubenheimer 2016). On the other hand, a
number of deliberately provisioned supplemen-
tary foods of urban birds are proportionally high
in protein (Fig. 2B). Mixtures of supplementary
food combined with anthropogenic food waste
thus have the potential to supply urban birds with
a wide variety of macronutrient options, includ-
ing novel combinations.
Multidimensional nutritional generalism
The dietary generalist–specialist distinction
likely plays a pivotal role in urban nutritional
ecology. Based on the ability to consume a wide
range of foods, dietary omnivores and general-
ists have been suggested to be better adapted to
urban environments (Chace and Walsh 2006,
Fig. 2. (A) Right-angled mixture triangle (RMT) depicting the typical proportions of macronutrient energy in a
variety of natural food categories consumed by birds. Data extracted from Klasing (1998). (B) RMT showing the
proportion of macronutrients in a variety of supplementary foods fed to wild birds.
❖www.esajournals.org 7April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

Ducatez et al. 2015). In general, studies of inva-
sive urban species have considered their ability
to consume a wide variety of foods (i.e., ecologi-
cal generalism) with a focus on the physical and
ecological characteristics of foods exploited.
Recently, however, researchers have high-
lighted the need to integrate nutrition with food-
level approaches in a multi-nutrient framework
to produce novel theoretical understandings of
dietary generalism (Machovsky-Capuska et al.
2016a, Fig. 3). Birds differ in their ability to con-
sume foods of various macronutrient composi-
tions, with those consuming widely dissimilar
foods being food composition generalists, or con-
versely being food composition specialists if
foods consumed are nutritionally similar.
Another dimension of generalism regards a
species’ability to exploit the physical properties
Fig. 3. A species’multidimensional nutritional niche and thus degree of generalism or specialism can be con-
sidered in terms of their ability to (1) consume foods differing in macronutrient compositions; (2) exploit foods
based on their physical properties; and (3) consume overall diets differing in macronutrient composition. The
conceptual right-angled mixture triangle (RMT) models highlight four scenarios for two different conspecific
populations (e.g., urban vs. rural birds; red and blue), showing their diets (stars), varying non-nutritional proper-
ties of foods (shapes), and associated macronutrient compositions (RMT coordinates): (A) The species is a food
composition generalist, food exploitation generalist, and macronutrient specialist; (B) the species is a food com-
position generalist, food exploitation specialist, macronutrient generalist; (C) the species is a food composition
specialist, food exploitation generalist, and macronutrient specialist; and (D) the species is a food composition
generalist, food exploitation generalist, and both a macronutrient specialist (protein) and macronutrient general-
ist (lipid and carbohydrate). Figure adapted from Machovsky-Capuska et al. (2016a).
❖www.esajournals.org 8April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

of foods (Machovsky-Capuska et al. 2016a,
Fig. 3). For example, nectarivores adapted to
feeding from flowers would generally be
expected to be food exploitation specialists, as
opposed to species that are able to exploit a wide
range of foods differing in their physical proper-
ties (i.e., food exploitation generalists) due to, for
example, characteristics associated with cogni-
tion, foraging behavior, and morphology.
A species’niche can also be thought of in
terms of the macronutrient composition of a
species’overall diet, where the fundamental
macronutrient niche of a species population is
defined as the range of dietary macronutrient
compositions that allow the population to persist
(Machovsky-Capuska et al. 2016a). The observed
diet of a species population can be considered
suggestive of the realized macronutrient niche of
that population, when the population is subject
to ecologically constraining factors such as intra-
and inter-specific competition and food or prey
availability. This approach can provide insight
into whether a particular species is a macronutri-
ent generalist (i.e., having a relatively large fun-
damental macronutrient niche) or macronutrient
specialist (i.e., having a narrow fundamental
macronutrient niche). This was investigated for
the omnivorous wild boar (Sus scrofa) and brown
bear (Ursus arctos), which were found to have
wide fundamental macronutrient niches that
likely contributed to their success in occupying a
range of diverse habitats (Senior et al. 2016,
Coogan et al. 2018). Brown bear populations
receiving anthropogenic subsidies in the afore-
mentioned study were found to have on average
higher proportions of carbohydrate, and lower
proportions of protein, in their diets than popula-
tions with natural diets.
Diet selection in different habitats
A fundamental issue to address in urban nutri-
tional ecology studies is to determine to what
extent the diets of species occupying urban habi-
tats differ from conspecifics inhabiting environ-
ments with little or no anthropogenic food
subsidies (e.g., rural or natural habitats; Gavett
and Wakeley 1986). The level of anthropogenic
food in bird diets can also be examined along a
gradient of use and availability, which likely dif-
fers among cities, rural areas, and natural areas.
Such dietary differences may have profound
implications for the fitness of individuals in
urban populations if their diet is imbalanced rel-
ative to nutritional requirements that evolved
under natural conditions.
A valid hypothesis, however, is that urban
birds consume a similar proportion of macronu-
trients as birds in natural habitats despite con-
suming different foods (i.e., food composition
generalist and macronutrient specialists), due to
shared regulatory systems governing nutrient
intake. Such active nutrient regulation has been
tested in the field, where geographically distinct
populations of mountain gorillas (Gorilla beringei
beringei) had similar nutrient intakes despite con-
suming different combinations of foods (Roth-
man et al. 2007, Raubenheimer et al. 2015b).
Similar findings were observed in pine martins
(Martes martes) across different regions of Eur-
ope, despite the consumption of a wide variety
of foods across seasons (Remonti et al. 2016). In
contrast, a study of Australasian gannets found
that birds from two different geographic popula-
tions in NZ composed diets differing in propor-
tional macronutrient compositions (Tait et al.
2014). The nutritional composition of gannet
prey was significantly different both within and
between prey species.
The multidimensional nutritional approach
outlined above can be used to understand and
predict the nutritional niche requirements and
foraging goals of birds transitioning from native
to urban habitats. Knowledge of a species’multi-
dimensional nutritional niche in its native range
can be used to predict how they might respond
to environmental changes in the quantity and
nutritional characteristics of available food in
urban environments (Raubenheimer et al. 2012).
To illustrate, we review four conceptual nonex-
clusive examples that birds might encounter in
their transition from native to urban habitats
(Machovsky-Capuska et al. 2016a, Fig. 4). In
Fig. 4A, the species is considered preadapted to
the urban nutritional environment when the
anthropogenic foods encountered have similar
nutritional and physical properties to those
encountered in its natural range. Fig. 4B depicts
a scenario in which both the natural and urban
habitat have physically similar foods that differ
in their macronutrient compositions. Fig. 4C
depicts a scenario in which urban foods are
physically different than those found in the bird’s
❖www.esajournals.org 9April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

Fig. 4. Right-angled mixture triangle models showing four hypothetical scenarios illustrating the nutritional
ecology of the native vs. urban habitats of birds during habitat transition. Foods (e.g., plant and animal species)
found in native habitats are shown in green, and urban foods are shown in orange. Food points differing in shape
(circle vs. triangle) indicate different physical properties of foods. (A) Native and urban habitats have physically
similar foods of similar macronutrient composition. (B) Native and urban habitats have foods with similar physi-
cal properties, but differ in their macronutrient composition. (C) Physical properties of foods differ between
native and urban habitats, but are similar in macronutrient composition. (D) Native and urban habitats have
physically different foods that also differ in macronutrient composition. Figure adapted from Machovsky-
Capuska et al. (2016a).
❖www.esajournals.org 10 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

native range, yet have similar macronutrient
compositions. Fig. 4D represents the most chal-
lenging scenario in which both the food composi-
tions and physical properties differ in urban
habitats.
The multidimensional nutritional niche of a
bird species can thus be used to predict how that
species responds to novel and complex urban
nutritional environments. Such an approach
would be useful in disentangling birds’nutri-
tional goals and realized macronutrient niches in
their native habitats and whether these are main-
tained during their transition, and final adapta-
tion, to urban environments.
FUTURE RESEARCH AND CONCLUSIONS
A particularly useful approach for understand-
ing the multidimensional nutritional ecology of
animals has been a state-space modeling
approach known as nutritional geometry, which
is an expansion of the geometric framework for
nutrition (Raubenheimer 2011, Simpson and
Raubenheimer 2012). Nutritional geometry has
been very useful in generating insight into the
relationships between foraging behavior and
macronutrients, including the biological effects
of consuming them in different amounts and
proportions (Jensen et al. 2012). For example,
such studies have demonstrated that low-protein
high-carbohydrate diets are associated with
increased lifespan in mice and several other
model species, while conversely several repro-
ductive measures were higher in mice fed hig-
her ratios of protein relative to carbohydrate
(Raubenheimer et al. 2016).
To date, three studies have applied nutritional
geometry to examine the nutritional ecology of
free-ranging urban birds. In the first, an urban
population of common mynas displayed a strong
preference for high-protein experimental food
over high-lipid and high-carbohydrate foods in
field-based feeding trials (Machovsky-Capuska
et al. 2016b). The myna’s preference for high-pro-
tein foods, combined with increased levels of
intra-specific aggression over the resource, led
the authors to conclude that protein was a limit-
ing macronutrient for that population. The sec-
ond study, performed on captured urban mynas
in outdoor aviaries, revealed intra-specific differ-
ences in foraging preferences, where those that
selected high-protein foods were more explora-
tory and more rapidly solved foraging tasks
than conspecifics that selected high-carbohydrate
foods (Peneaux et al. 2017). These findings
showed the ability of this species to evaluate the
nutritional content of foods, suggesting that this
mechanism might be important to their ecologi-
cal success as invaders. In contrast to the myna, a
third study showed that urban populations of
Australian white ibis generally preferred high-
carbohydrate experimental foods when offered
the choice from an experimental feeding dish
(Coogan et al. 2017). The preference for carbohy-
drate was in contrast to the natural diet of ibis
(i.e., relatively low in carbohydrate, and higher
in protein and lipid), yet more similar to the com-
position of some anthropogenic foods, such as
bread. An important area of future research is to
expand upon nutritional geometry studies of
urban birds to link the effects of macronutrient
intake to biological responses (e.g., reproduction,
lifespan, and immunity). Such an approach could
provide valuable insight toward understanding
the implications of free-ranging urban birds con-
suming anthropogenic foods.
For example, expanding our understanding of
the role of nutrition as a modulator of cognitive
abilities in birds would be a powerful approach
to better comprehending relevant successes or
failures of urban birds (Peneaux et al. 2017). Our
knowledge of the relationships between cogni-
tion and nutrition is mostly derived from studies
of rodents, non-human primates, and humans
(Wahl et al. 2016). Yet, intelligence and behav-
ioral flexibility, such as cognitive learning and
innovation, are important characteristics for suc-
cessful foraging in urban and novel habitats for
many birds (Sol et al. 2002, 2005, Lefebvre et al.
2004, Ducatez et al. 2015). Furthermore, nutri-
tional stress has been shown to impair cognitive
function in offspring (Kitaysky et al. 2003, Pravo-
sudov and Kitaysky 2006) and may also influ-
ence song development (Nowicki et al. 1998).
In general, the potential for multidimensional
nutritional ecology to increase our understand-
ing of the nutritional ecology of urban birds is
promising. The multidimensional macronutrient
perspective can be used to examine the nutri-
tional ecology of so-called urban adapters vs.
urban exploiters, each of which is suggested to
target different foods (McKinney 2006). Food
❖www.esajournals.org 11 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

might become more available for predatory spe-
cies with more abundant prey in urban habitats
(Chace and Walsh 2006, Robb et al. 2008); hence,
urban environments also provide the opportu-
nity to enhance our knowledge of the nutritional
ecology of predators using advances in biolog-
ging technology in combination with nutritional
geometry and other techniques (Machovsky-
Capuska et al. 2016c).
Importantly, multidimensional nutritional ecol-
ogy extends beyond macronutrients and can be
expanded to examine a wide range of function-
ally important nutritional parameters. Antioxi-
dants such as carotenoids and flavonoids, which
may be lower in some urban plants and insects
(Isaksson and Andersson 2007), could, for
instance, be modeled using nutritional geometry
with associated physiological responses, such as
potential inflammation and oxidative stress
(Isaksson 2015), modeled using interpolative
response surfaces. Furthermore, the physiologi-
cal mechanisms mediating nutrition and fitness
can be examined using such an approach (Solon-
Biet et al. 2015, Raubenheimer et al. 2016), for
example, the roles of endocrine factors (e.g., lep-
tin, glucocorticoids, and GnIH-neuropeptide Y;
Davies and Deviche 2014) in the timing of avian
reproduction.
Urban environments offer powerful systems
for increasing our understanding of ecology and
evolution due to the often extreme and uncom-
mon selection pressures (Diamond 1986, Hahs
and Evans 2015). However, a criticism of urban
ecology research to date has been the focus on
describing patterns along environmental gradi-
ents as opposed to investigating the mechanistic
and evolutionary processes that lie at the heart of
functional ecology (Hahs and Evans 2015). Mul-
tidimensional nutritional ecology provides a
powerful perspective when integrating mecha-
nistic and functional drivers of nutrition-related
patterns (Simpson and Raubenheimer 2012) and
a useful approach toward unraveling the nutri-
tionally complex ecology of urban birds.
ACKNOWLEDGMENTS
Sean C P Coogan was supported by an Australian
Postgraduate Award (APA) and International Post-
graduate Research Scholarship (IPRS), and the Natural
Sciences and Engineering Research Council (NSERC)
of Canada. GEMC is supported by the Loxton research
fellowship from the Sydney School of Veterinary
Science, The University of Sydney. DR acknowledges
support from the Australian Research Council (Link-
age Grant LP140100235).
LITERATURE CITED
Amrhein, V. 2013. Wild bird feeding (probably) affects
avian urban ecology. Pages 29–37 in D. Gil and H.
Brumm, editors. Avian urban ecology. Oxford
University Press, Oxford, UK.
Audet, J.-N., S. Ducatez, and L. Lefebvre. 2015. The
town bird and the country bird: Problem solving
and immunocompetence vary with urbanization.
Behavioral Ecology 27:637–644.
Auman, H. J., C. E. Meathrel, and A. Richardson. 2008.
Supersize me: Does anthropogenic food change the
body condition of Silver Gulls? A comparison
between urbanized and remote, non-urbanized
areas. Waterbirds 31:122–126.
Baldwin, M. W., Y. Toda, T. Nakagita, M. J. O’Connell,
K. C. Klasing, T. Misaka, S. V. Edwards, and S. D.
Liberles. 2014. Evolution of sweet taste perception
in hummingbirds by transformation of the ances-
tral umami receptor. Science 22:929–933.
Bolton, M., D. Houston, and P. Monaghan. 1992. Nutri-
tional constraints on egg formation in the lesser
black-backed gull: an experimental study. Journal
of Animal Ecology 61:521–532.
Boutin, S. 1990. Food supplementation experiments
with terrestrial vertebrates: patterns, problems and
the future. Canadian Journal of Zoology 68:203–
220.
Bravo, C., L. M. Bautista, M. Garc
ıa-Paris, G. Blanco,
and J. C. Alonso. 2014. Males of a strongly polygy-
nous species consume more poisonous food than
females. PLoS ONE 9:e111057.
Brooks, R. C., S. J. Simpson, and D. Raubenheimer.
2010. The price of protein: combining evolutionary
and economic analysis to understand excessive
energy consumption. Obesity Reviews 11:887–894.
Burgin, S., and T. Saunders. 2007. Parrots of the Syd-
ney region: population changes over 100 years.
Pages 185–194 in D. Lunney, P. Ebby, P. Hutchings,
and S. Burgin, editors. Pest or Guest: the zoology
of overabundance. Royal Zoological Society of
New South Wales, Mosman, New South Wales,
Australia.
Chace, J. F., and J. J. Walsh. 2006. Urban effects on
native avifauna: a review. Landscape and Urban
Planning 74:46–69.
Chard, M., J. Martin, K. French, and R. E. Major. 2017.
Rainfall events drive foraging choices by an urban
colonizer. Urban Ecosystems 20:1285–1290.
❖www.esajournals.org 12 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

Clergeau, P., J. P. L. Savard, G. Mennechez, and G.
Falardeau. 1998. Bird abundance and diversity
along an urban-rural gradient: a comparative
study between two cities on different continents.
Condor 100:413–425.
Coogan, S. C. P., G. E. Machovsky-Capuska, A. M.
Senior, J. M. Martin, R. E. Major, and D. Rauben-
heimer. 2017. Macronutrient selection of free-ran-
ging urban Australian white ibis (Threskiornis
moluccus). Behavioral Ecology 28:1021–1029.
Coogan, S. C. P., and D. Raubenheimer. 2016. Might
macronutrient requirements influence grizzly
bear–human conflict? Insights from nutritional
geometry. Ecosphere 7:e01204.
Coogan, S. C. P., D. Raubenheimer, G. B. Stenhouse, N.
C. Coops, and S. E. Nielsen. 2018. Functional
macronutritional generalism in a large omnivore,
the brown bear. Ecology and Evolution 8:2365–
2376.
Coogan, S. C. P., D. Raubenheimer, G. B. Stenhouse,
and S. E. Nielsen. 2014. Macronutrient optimiza-
tion and seasonal diet mixing in a large omnivore,
the grizzly bear: a geometric analysis. PLoS ONE 9:
e97968.
Cotton, S., K. Fowler, and A. Pomiankowski. 2004. Do
sexual ornaments demonstrate heightened condi-
tion-dependent expression as predicted by the
handicap hypothesis? Proceedings of the Royal
Society London B 271:771–783.
Cowie, R. J., and S. A. Hinsley. 1988. Feeding ecology
of Great Tits (Parus major) and Blue Tits (Parus caer-
uleus) breeding in suburban gardens. Journal of
Animal Ecology 57:611–626.
Davies, S., and P. Deviche. 2014. At the crossroads of
physiology and ecology: food supply and the tim-
ing of avian reproduction. Hormones and Behavior
66:41–55.
Davies, Z. G., R. A. Fuller, M. Dallimer, A. Loram, and
K. J. Gaston. 2012. Household factors influencing
participation in bird feeding activity: a national
scale analysis. PLoS ONE 7:e39692.
Diamond, J. M. 1986. Rapid evolution of urban birds.
Nature 324:107–108.
Diamond, J. M. 1999. Evolutionary biology: dirty eat-
ing for healthy living. Nature 400:120–121.
Ducatez, S., J. Clavel, and L. Lefebvre. 2015. Ecological
generalism and behavioural innovation in birds:
Technical intelligence or the simple incorporation
of new foods? Journal of Animal Ecology 85:79–89.
Eldridge, J. L., and G. L. Krapu. 1988. The influence of
diet quality on clutch size and laying pattern in
mallards. Auk 105:102–110.
Evans, J., K. Boudreau, and J. Hyman. 2010. Beha-
vioural syndromes in urban and rural populations
of song sparrows. Ethology 116:588–595.
Fleischer Jr, A. L., R. Bowman, and G. E. Woolfenden.
2003. Variation in foraging behavior, diet, and time
of breeding of Florida scrub-jays in suburban and
wildland habitats. Condor 105:515–527.
Fox, D. 2007. Back to the no-analog future? Science
316:823–824.
Galbraith, J. A., J. R. Beggs, D. N. Jones, and M. C.
Stanley. 2015. Supplementary feeding restructures
urban bird communities. Proceedings of the
National Academy of Sciences of the United States
of America 112:E2648–E2657.
Garamszegi, L. Z., J. Erritzøe, and A. P. Møller. 2007.
Feeding innovations and parasitism in birds. Bio-
logical Journal of the Linnean Society 90:441–455.
Gavett, A. P., and J. S. Wakeley. 1986. Blood con-
stituents and their relation to diet in urban and
rural house sparrows. Condor 88:279–284.
Gilbert, N. I., R. A. Correia, J. P. Silva, C. Pacheco, I.
Catry, P. W. Atkinson, J. A. Gill, and A. M. A.
Franco. 2016. Are white storks addicted to junk
food? Impacts of landfill use on the movement and
behaviour of resident white storks (Ciconia ciconia)
from a partially migratory population. Movement
Ecology 4:7.
Glue, D. 2006. Variety at winter bird tables. Bird Popu-
lations 7:212–215.
Gosper, E. C., D. Raubenheimer, G. E. Machovsky-
Capuska, and A. V. Chaves. 2016. Discrepancy
between the composition of some commercial cat
foods and their package labelling and suitability
for meeting nutritional requirements. Australian
Veterinary Journal 94:12–17.
Grimm, N. B., S. H. Faeth, N. E. Golubiewski, C. L.
Redman, J. Wu, X. Bai, and J. M. Briggs. 2008. Glo-
bal change and the ecology of cities. Science
319:756–760.
Hahs, A. L., and K. L. Evans. 2015. Expanding funda-
mental ecological knowledge by studying urban
ecosystems. Functional Ecology 29:863–867.
Harris, M. P. 1965. The food of some Larus gulls. Ibis
107:43–53.
Hilgartner, R., D. Stahl, and D. Zinner. 2014. Impact of
supplementary feeding on reproductive success of
white storks. PLoS ONE 9:e104276.
Hill, G. E. 2000. Energetic constraints on expression of
carotenoid-based plumage coloration. Journal of
Avian Biology 31:559–566.
Hobbs, R. J., and V. A. Cramer. 2008. Restoration ecol-
ogy: interventionist approaches for restoring and
maintaining ecosystem function in the face of rapid
environmental change. Annual Review of Environ-
ment and Resources 33:39–61.
Horn, D. J., and S. M. Johansen. 2013. A comparison of
bird-feeding practices in the United States and
Canada. Wildlife Society Bulletin 37:293–300.
❖www.esajournals.org 13 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

Hulme-Beaman, A., K. Dobney, T. Cucchi, and J. B.
Searle. 2016. An ecological and evolutionary frame-
work for commensalism in anthropogenic environ-
ments. Trends in Ecology & Evolution 31:633–645.
Isaksson, C. 2015. Urbanization, oxidative stress and
inflammation: a question of evolving, acclimatizing
or coping with urban environmental stress. Func-
tional Ecology 29:913–923.
Isaksson, C., and S. Andersson. 2007. Carotenoid diet
and nestling provisioning in urban and rural great
tits, Parus major. Journal of Avian Biology 38:564–
572.
Ishigame, G., and G. S. Baxter. 2007. Practice and atti-
tudes of suburban and rural dwellers to feeding
wild birds in Southeast Queensland, Australia.
Ornithological Science 6:11–19.
Jensen, K., D. Mayntz, S. Toft, F. J. Clissold, J. Hunt, D.
Raubenheimer, and S. J. Simpson. 2012. Optimal
foraging for specific nutrients in predatory beetles.
Proceedings of the Royal Society B 279:2212–2218.
Jones, D. 2011. An appetite for connection: why we
need to understand the effect and value of feeding
wild birds. Emu 111:i–vii.
Kalnay, E., and M. Cai. 2003. Impact of urbanization
and land-use change on climate. Nature 423:528–
531.
Kitaysky, A. S., E. V. Kitaiskaia, J. F. Piatt, and J. C.
Wingfield. 2003. Benefits and costs of increased
levels of corticosterone in seabird chicks. Hor-
mones and Behavior 43:140–149.
Klasing, K. C. 1998. Comparative avian nutrition. Cab
International, New York, New York, USA.
Kreeger, T. J., and M. M. Waiser. 1984. Car-
pometacarpal deformity in giant Canada geese
(Branta Canadensis maxima Delacour). Journal of
Wildlife Diseases 20:245–248.
Lawson, B., S. Lachish, K. M. Colvile, C. Durrant, K.
M. Peck, M. P. Toms, B. C. Sheldon, and A. A.
Cunningham. 2012. Emergence of a novel avian
pox disease in British tit species. PLoS ONE 7:
e40176.
Lefebvre, L., S. M. Reader, and D. Sol. 2004. Brains,
innovations and evolution in birds and primates.
Brain, Behavior and Evolution 63:233–246.
Lowry, H., A. Lill, and B. Wong. 2013. Behavioural
responses of wildlife to urban environments. Bio-
logical Reviews 88:537–549.
Machovsky-Capuska, G. E., A. M. Senior, S. J. Simp-
son, and D. Raubenheimer. 2016a. The multidimen-
sional nutritional niche. Trends in Ecology and
Evolution 31:355–365.
Machovsky-Capuska, G. E., A. M. Senior, S. P. Zantis,
K. Barna, A. J. Cowieson, S. Pandya, C. Pavard, M.
Shiels, and D. Raubenheimer. 2016b. Dietary pro-
tein selection in a free-ranging urban population of
common myna birds. Behavioral Ecology 27:219–
227.
Machovsky-Capuska, G. E., S. C. P. Coogan, S. J. Simp-
son, and D. Raubenheimer. 2016c. Motive for kill-
ing: What drives prey choice in wild predators?
Ethology 122:1–9.
Martin, J., K. French, and R. Major. 2012. Behavioural
adaptation of a bird from transient wetland spe-
cialist to an urban resident. PLoS ONE 7:e50006.
Martinson, T. J., and D. J. Flaspohler. 2003. Winter bird
feeding and localized predation on simulated bark-
dwelling arthropods. Wildlife Society Bulletin
31:510–516.
McDonnell, M. J., and A. K. Hahs. 2015. Adaptation
and adaptedness of organisms to urban environ-
ments. Annual Review of Ecology, Evolution and
Systematics 46:261–280.
McGraw, K. J., E. A. Mackillop, J. Dale, and M. E. Hau-
ber. 2002. Different colors reveal different informa-
tion: how nutritional stress affects the expression
of melanin-and structurally based ornamental plu-
mage. Journal of Experimental Biology 205:3747–
3755.
McKinney, M. L. 2002. Urbanization, biodiversity, and
conservation. BioScience 52:883–890.
McKinney, M. L. 2006. Urbanization as a major cause
of biotic homogenization. Biological Conservation
127:247–260.
Meijer, T., and R. Drent. 1999. Re-examination of the
capital and income dichotomy in breeding birds.
Ibis 141:399–414.
Møller, A. P., J. Erritzøe, and L. Z. Garamszegi. 2005.
Covariation between brain size and immunity in
birds: implications for brain size evolution. Journal
of Evolutionary Biology 18:223–237.
Moritzi, M., L. Maumary, D. Schmid, I. Steiner, L. Val-
lotton, R. Spaar, and O. Biber. 2001. Time budget,
habitat use and breeding success of White Storks
Ciconia ciconia under variable foraging conditions
during the breeding season in Switzerland. Ardea
89:457–470.
Nager, R. G., C. Ruegger, and A. J. van Noordwijk.
1997. Nutrient or energy limitation on egg forma-
tion: a feeding experiment in great tits. Journal of
Animal Ecology 66:495–507.
Nowicki, S., S. Peters, and J. Podos. 1998. Song learn-
ing, early nutrition and sexual selection in song-
birds. American Zoologist 38:179–190.
O’Leary, R. E., and D. N. Jones. 2006. The use of sup-
plementary foods by Australian magpies Gym-
norhina tibicen: implications for wildlife feeding in
suburban environments. Austral Ecology 31:208–
216.
Oro, D., M. Genovart, G. Tavecchia, M. S. Fowler, and
A. Martinez-Abrain. 2013. Ecological and
❖www.esajournals.org 14 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

evolutionary implications of food subsidies from
humans. Ecology Letters 16:1501–1514.
Orros, M. E., and M. D. E. Fellowes. 2015. Wild bird
feeding in an urban area: intensity, economics and
numbers of individuals supported. Acta Ornitho-
logica 50:43–58.
Peneaux, C., G. E. Machovsky-Capuska, D. Rauben-
heimer, F. Lermite, C. Rousseau, T. Ruhan, J. C.
Rodger, and A. S. Griffin. 2017. Tasting novel foods
and selecting nutrient content in a highly success-
ful ecological invader, the common myna. Journal
of Avian Biology 48:1432–1440.
Pierotti, R., and C. A. Annett. 1991. Diet choice in the
herring gull: constraints imposed by reproductive
and ecological factors. Ecology 72:319–328.
Plummer, K. E., S. Bearhop, D. I. Leech, D. E. Cham-
berlain, and J. D. Blount. 2013. Fat provisioning in
winter impairs egg production during the follow-
ing spring: a landscape-scale study of blue tits.
Journal of Animal Ecology 82:673–682.
Ponton, F., K. Wilson, S. C. Cotter, D. Raubenheimer,
and S. J. Simpson. 2011. Nutritional immunology: a
multi-dimensional approach. PLoS Pathogens 7:
e1002223.
Pravosudov, V. V., and A. S. Kitaysky. 2006. Effects of
nutritional restrictions during post-hatching devel-
opment on adrenocortical function in western
scrub-jays (Aphelocoma californica). General and
Comparative Endocrinology 145:25–31.
Ramsay, S. L., and D. C. Houston. 1997. Nutritional
constraints on egg production in the blue tit: a sup-
plemental feeding study. Journal of Animal Ecol-
ogy 66:649–657.
Raubenheimer, D. 2011. Toward a quantitative nutri-
tional ecology: the right-angled mixture triangle.
Ecological Monographs 81:407–427.
Raubenheimer, D., G. E. Machovsky-Capuska, A. K.
Gosby, and S. J. Simpson. 2015a. Nutritional ecol-
ogy of obesity: from humans to companion
animals. British Journal of Nutrition 113(Suppl):
S26–S39.
Raubenheimer, D., G. E. Machovsky-Capuska, C. A.
Chapman, and J. M. Rothman. 2015b. Geometry of
nutrition in field studies: an illustration using wild
primates. Oecologia 177:223–234.
Raubenheimer, D., and S. J. Simpson. 1993. The geom-
etry of compensatory feeding in the locust. Animal
Behaviour 45:953–964.
Raubenheimer, D., and S. J. Simpson. 2006. The chal-
lenge of supplementary feeding: Can geometric
analysis help save the kakapo? Notornis 53:100–
111.
Raubenheimer, D., and S. J. Simpson. 2016. Nutritional
ecology and human health. Annual Review of
Nutrition 36:603–626.
Raubenheimer, D., S. J. Simpson, D. G. Le Couteur, S.
M. Solon-Biet, and S. C. P. Coogan. 2016. Nutri-
tional ecology and the evolution of ageing. Experi-
mental Gerontology 86:50–61.
Raubenheimer, D., S. J. Simpson, and A. H. Tait. 2012.
Match and mismatch: conservation physiology,
nutritional ecology and the timescales of biological
adaptation. Philosophical Transactions of the Royal
Society B 367:1628–1646.
Remonti, L., A. Balestrieri, D. Raubenheimer, and N.
Saino. 2016. Functional implications of omnivory
for dietary nutrient balance. Oikos 125:1233–1240.
Reynolds, S. J., S. J. Schoech, and R. Bowman. 2003.
Nutritional quality of prebreeding diet influences
breeding performance of the Florida scrub-jay.
Oecologia 134:308–316.
Robb, G. N., R. A. McDonald, D. E. Chamberlain, and
S. Bearhop. 2008. Food for thought: supplementary
feeding as a driver of ecological change in avian
populations. Frontiers in Ecology and the Environ-
ment 6:476–484.
Robinson, R. A., et al. 2010. Emerging infectious dis-
ease leads to rapid population declines of common
British birds. PLoS ONE 5:e12215.
Rollinson, D. J., R. O’Leary, and D. N. Jones. 2003. The
practice of wildlife feeding in suburban Brisbane.
Corella 27:52–58.
Rothman, J. M., C. A. Chapman, and P. J. Van Soest.
2012. Methods in primate nutritional ecology: a
user’s guide. International Journal of Primatology
33:542–566.
Rothman, J. M., A. J. Plumptre, E. S. Dierenfeld, and A.
N. Pell. 2007. Nutritional composition of the diet of
the gorilla (Gorilla beringei): a comparison between
two montane habitats. Journal of Tropical Ecology
23:673–682.
Rothman, J. M., D. Raubenheimer, and C. A. Chap-
man. 2011. Nutritional geometry: Gorillas priori-
tize non-protein energy while consuming surplus
protein. Biology Letters 7:847–849.
Roulin, A. 2016. Condition-dependence, pleiotropy
and the handicap principle of sexual selection in
melanin-based colouration. Biological Reviews
91:328–348.
Saggese, K., F. Korner-Nievergelt, T. Slagsvold, and V.
Amrhein. 2011. Wild bird feeding delays start of
dawn singing in the great tit. Animal Behaviour
81:361–365.
Schoech, S. J., and R. Bowman. 2003. Does differential
access to protein influence differences in timing of
breeding of Florida scrub-jays (Aphelocoma coerules-
cens) in suburban and wildland habitats? Auk
120:1114–1127.
Seastadt, T. R., R. J. Hobbs, and K. N. Suding. 2008.
Management of novel ecosystems: Are novel
❖www.esajournals.org 15 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.

approaches required? Frontiers in Ecology and the
Environment 6:547–553.
Senior, A. M., C. E. Grueber, G. Machovsky-Capuska,
S. J. Simpson, and D. Raubenheimer. 2016. The
macronutritional consequences of food generalism
in an invasive mammal, the wild boar. Mammalian
Biology 81:523–526.
Shochat, E., S. B. Lerman, M. Katti, and D. B. Lewis.
2004. Linking optimal foraging behaviour to bird
community structure in an urban-desert landscape:
field experiments with artificial food patches.
American Naturalist 164:232–243.
Simpson, S. J., D. G. Le Couteur, and D. Rauben-
heimer. 2015. Putting the balance back in diet. Cell
161:18–23.
Simpson, S. J., and D. Raubenheimer. 1993. A multi-
level analysis of feeding behaviour: the geometry
of nutritional decisions. Philosophical Transactions
of the Royal Society B 342:381–402.
Simpson, S. J., and D. Raubenheimer. 2012. The nature
of nutrition: an integrative framework from animal
adaptation to human obesity. Princeton University
Press, Princeton, New Jersey, USA.
Smith, G. C., and N. Carlile. 1993. Food and feeding
ecology of breeding Silver Gulls (Larus novaehollan-
diae) in urban Australia. Colonial Waterbirds 16:9–
16.
Sol, D., R. P. Duncan, T. M. Blackburn, P. Cassey, and
L. Lefebvre. 2005. Big brains, enhanced cognition,
and response of birds to novel environments. Pro-
ceedings of the National Academy of Sciences of
the United States of America 102:5460–5465.
Sol, D., S. Timmermans, and L. Lefebvre. 2002. Beha-
vioural flexibility and invasion success in birds.
Animal Behaviour 63:495–502.
Soler, J. J., J. M. Peralta-S
anchez, M. Mart
ın-Vivaldi, A.
M. Mart
ın-Platero, E. Flensted-Jensen, and A. P.
Møller. 2012. Cognitive skills and bacterial load:
comparative evidence of costs of cognitive profi-
ciency in birds. Naturwissenschaften 99:111–122.
Solon-Biet, S. M., K. A. Walters, U. K. Simanainen, A.
C. McMahon, K. Ruohonen, J. W. O. Ballard, D.
Raubenheimer, D. J. Handelsman, D. G. Le
Couteur, and S. J. Simpson. 2015. Macronutrient
balance, reproductive function, and lifespan in
aging mice. Proceedings of the National Academy
of Sciences of the United States of America
112:3481–3486.
Stevens, C. E., and I. D. Hume. 1995. Comparative
physiology of the vertebrate digestive system.
Cambridge University Press, Cambridge, UK.
Sword, G. A., M. Lecoq, and S. J. Simpson. 2010. Phase
polyphenism and preventative locust manage-
ment. Journal of Insect Physiology 56:949–957.
Tait, A., D. Raubenheimer, K. A. Stockin, M. Merri-
man, and G. E. Machovsky-Capuska. 2014. Nutri-
tional geometry of gannets and the challenges in
field studies. Marine Biology 12:2791–2801.
Vas, Z., L. Lefebvre, K. P. Johnson, J. Reiczigel, and L.
R
ozsa. 2011. Clever birds are lousy: co-variation
between avian innovation and the taxonomic rich-
ness of their amblyceran lice. International Journal
for Parasitology 41:1295–1300.
Veiga, J. P., and M. Puerta. 1996. Nutritional con-
straints determine the expression of a sexual trait
in the house sparrow, Passer domesticus. Proceed-
ings of the Royal Society B 263:229–234.
Wahl, D., et al. 2016. Nutritional strategies to optimize
cognitive function in the ageing brain. Ageing
Research Reviews 31:80–92.
Weiser, E. L., and A. N. Powell. 2010. Does garbage in
the diet improve reproductive output of glaucous
gulls? Condor 112:530–538.
Yoda, K., N. Tomita, Y. Mizutani, A. Narita, and Y. Nii-
zuma. 2012. Spatio-temporal responses of black-
tailed gulls to natural and anthropogenic food
resources. Marine Ecology Progress Series 466:249–
259.
Zahavi, A. 1975. Mate selection—A selection for a
handicap. Journal of Theoretical Biology 53:205–
214.
Zsivanovits, P., D. J. Monks, and N. A. Forbes.
2006. Bilateral valgus deformity of the distal wings
(angel wing) in a northern goshawk (Accipiter gen-
tilis). Journal of Avian Medicine and Surgery
20:21–26.
SUPPORTING INFORMATION
Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ecs2.
2177/full
❖www.esajournals.org 16 April 2018 ❖Volume 9(4) ❖Article e02177
CONCEPTS & THEORY COOGAN ET AL.