Abstract. Growing evidence that individuals of many generalist
animals behave as resource specialists has attracted research interest
for its ecological and evolutionary implications. Although variation in
resource preferences is critical for developing a general theory of
individual specialization, it remains to be shown whether diverging
preferences can arise among individuals sharing a similar environment
and whether these are stable enough to be ecologically relevant. We
addressed these issues by means of common garden experiments in feral
pigeons (Columba livia), a species known to exhibit resource
specialization in the wild. Food-choice experiments on wild-caught
pigeons and their captive-bred descendants showed that variation in food
preferences can easily arise within a population and that this variation
may represent a substantial fraction of the population niche. However, a
cross-fostering experiment revealed that the genetic and early
common-environment components of food preferences were low, reducing
their stability and eroding niche variation in the long-term.
Keyword: Niche variation; individual differences;
decision-making; learning the niche; behavioural plasticity;
heritability of behaviour; cross-fostering experiment.
Niche variation—in which individuals consistently use a subset of the
resources available for the population (Van Valen 1965)—is a
widespread phenomenon in vertebrate and invertebrate taxa (Bolnicket al. 2003). Although much of this variation can be explained by
either ontogenetic niche shifts or sexual dimorphism (Schoener 1986;
Price 1987), resource-use variation is observed even among individuals
of the same age and sex (Araújo et al. 2011). In Brünnich’s
guillemots (Uria lomvia ), for example, individuals show foraging
specializations in diving technique, which are then reflected in
differences in the type of fish and marine invertebrates they mostly
capture (Woo et al. 2008). This type of niche variation —known
as individual specialization— has attracted considerable interest for
its ecological and evolutionary implications (reviewed in Bolnicket al. , 2003, 2011; Dall et al. , 2012). Thus, individual
specialization has been related to a wide array of ecologically and
evolutionary relevant processes, including skill-pools, population
stability, species coexistence, extinction, niche evolution and
speciation (Giraldeau 1984; Sol et al. 2005; Tinker et al.2008; Bolnick et al. 2011). Surprisingly, however, how individual
variation in resource use is generated and maintained within populations
is still insufficiently understood (Araújo et al. 2011; Bolnicket al. 2011). As a consequence, the actual relevance of
individual resource specialization in ecology and evolution remains
unclear.
The existence of variation among individuals in resource preferences is
central for developing a general theory of individual specialization. As
pointed by Bolnick et al. (2003), if a population is found to be
composed of individuals that consistently prefer different subsets of
available foods, few would object to considering such individuals
specialists. However, why should individuals sharing a same environment
end up using only a subset of all available resources? Classic optimal
foraging theory predicts that organisms’ food choices should maximize
some currency linked to fitness, like energy intake (Pyke 1984;
Shettleworth 1985). It follows that if individuals behave optimally,
they should converge in the way they use the resources rather than
diverge.
Theoretical models suggest, however, that specialization may still occur
if preferences are state-dependent, that is, if the decisions of
individuals are modulated by their morphological, physiological and
psychological features (Houston & McNamara 1999). Araújo et al. ,
(2011) discussed two main ways how this can occur. One is when
phenotypic variation produces among-individual differences in the
ability to detect, capture, handle, or digest alternative prey. The
second is when individuals use different optimization criteria in
resource-choice, for example because they have different energetic
requirements (Schoener 1971). Both mechanisms may not only cause
individuals to prefer some resources over others, but they may make
preferences to be transmitted to offspring if the state-traits that have
driven them are themselves heritable. Thus, although preferences can be
extremely plastic, they can change more slowly if optimal choices are
connected to a slow-changing state variable (Luttbeg & Sih 2010).
Resource specialization may arise in yet another way, that is, through
learning (Tinker et al. 2009). Although behaviour, physiology and
morphology may set the limits to what an individual can eat, food
preferences within these boundaries may arise through positive feedbacks
(sensu Dingemanse & Wolf 2010), where early experiences in the use of
certain foods reinforce (if positive) initial choices (Dridi & Lehmann
2015). A variety of situations may make individuals to have distinct
early food experiences, including different perception of risk or
spatially and/or temporally variation in resource availability. There is
indeed growing evidence that learning is crucial for animals to develop
their own niche (Slagsvold & Wiebe 2007; Tinker et al. 2009).
Given that resource preferences will be environmentally induced rather
than constrained by the genetic architecture, however, it is not obvious
how learned preferences will be maintained within a population. One
would expect that as individuals are exposed to positive food
experiences, their preferences will continue to expand rather than
remain narrow. Yet, learning may still cause stable resource preferences
if adopting new foods is cognitively costly, for example because it
requires to learn a new foraging technique (Partridge & Green 1987;
Tinker et al. 2009). Learned preferences may also be maintained
if they are phase-sensitive, that is, if they occur at a young age and
after that individuals acquire an aversion to explore and incorporate
new foods (Greenberg & Mettke-hofmann 2001; Slagsvold & Wiebe 2007).
Despite the importance of resource preferences in constructing a general
theory of individual specialization, there has been little effort to
assess whether individuals within populations consistently vary in
resource preferences and to what extent this variation remains stable
over time (Araújo et al. 2011; Bolnick et al. 2011). One
reason of this neglect is that resource preferences are difficult to
quantify. A major confounding effect is resource availability (Moon &
Zeigler 1979; De Cáceres et al. 2011). Preference is the
likelihood that an individual selects a given item when offered
alternative choices on an equal basis (Johnson 1980). If a particular
food is relatively scarce or is monopolized by a superior competitor, it
may represent only a small proportion of the resources used even if the
animal has a high preference for that food. Preference also implies that
the likelihood of selecting a given item is higher than expected by
chance. This means that resource preferences need to be measured in
standardized replicated observations, which may also be challenging
(Araújo et al. 2011). On the other hand, although one can measure
individual differences in resource preferences, the challenge remains as
to how interpret the differences. Given that individuals may use
different optimization criteria to rank foods, interpreting preferences
requires to consider the energetic and nutritional contents of food
(Machovsky-Capuska et al. 2018). It also requires to consider the
multi-dimensional nature of foraging behaviour, which includes the
search, identification, handling, consumption and digestion of foods.
Perhaps the most tractable way to tackle the difficulties of assessing
and interpreting food preferences is the use of common garden
experiments. Despite concerns over the extent to which the mechanisms we
observe in these experiments tap into those actually used by animals in
the wild, food-choice experiments involving a variety of food types in
exactly the same amount remain the best way to estimate individual
preferences under different optimization criteria and reducing the
complexities associated with the multi-dimensional nature of foraging
behaviour (Pyke 1984). Combined with cross-fostering breeding
experiments —where the effects of rearing environment and genetic
influences may be disentangled (Slagsvold & Wiebe 2007)— food-choice
experiments offer the opportunity to investigate 1) whether individuals
exhibit consistent differences in resource preferences and 2) to what
extent these differences have a genetic basis or are
environmentally-induced. Here, we address these questions in the Feral
pigeon (Columba livia ), a granivorous bird that has been
instrumental in the study of decision-making theory (Inman et al.1987; Shettleworth 1987a) and that in the wild is known to exhibit
individual differences in food use (Giraldeau & Lefebvre 1985; Johnston
& Janiga 1995). Although previous experiments in pigeons have found
evidence for a unitary preference for certain seeds (Moon & Zeigler
1979; Inman et al. 1987; Shettleworth 1987a; Biedermann et
al. 2012), some authors have suggested that individuals might also vary
in their preferences (Moon & Zeigler 1979; Giraldeau & Lefebvre 1985).
To investigate whether resource specialization reflect variation in food
preferences, we conducted replicated food-choice assays in a common
garden framework using pigeons from two wild populations. In addition,
we conducted food-choice assays on their captive-bred descendants—half
of them cross-fostered among nests—to estimate the heritability,
vertical transmission and reactions norms of the preferences by means of
a quantitative genetics approach. Finally, we repeated the food-choice
assays one year later to assess the long-term stability of food
preferences. Following De Cacéres et al. (2011), the contribution of
niche specialization to the total niche width of the populations was
assessed based on a comprehensive framework that extends classic
information theory by incorporating the energetic and nutritional
resemblance between resources into the calculation of resource niche
metrics. Characterizing the niche exclusively in terms of quantity and
range of different resources would ignore that individuals may use
different optimization criteria to rank foods. Moreover, it would bias
estimation of niche breadth as the niche of individuals consuming the
same number of foods will be considered equivalent even when some
individuals are using more different types of foods (Colwell et
al. 1971; De Cáceres et al. 2011).