Discussion
Our results confirmed all our hypothesis and showed that although black
wheatears exhibit only minor sexual size dimorphism there was dietary
differentiation between both sexes, by (i) males having an overall
higher diet diversity and (ii) females preying more often on some ant
species than males. This is the first time such intra-specific
differences are either studied or found in birds using metabarcoding
techniques. As expected, the differences found in the diet composition
and estimated richness were smaller or not significant using higher
taxonomic ranks, suggesting that if lower taxonomic resolution
methodologies had been used, these differences would not have been
detected. This methodology could be particularly relevant for birds as
passerines and near passerines, that feed on hyper diverse taxonomic
groups that are often difficult to identify, as insects and other
arthropods, and in which diets are often evaluated to the order or
family level through conventional techniques (Araújo, Lopes, da Silva,
& Ramos, 2016; Catry et al., 2019; Hodar, 1995).
The morphometric differences between sexes observed in our study were
related to the thicker bill and longer wings and tail of males. In
previous studies conducted in Alicante (Pérez-Granados & Seoane, 2018)
and Hoya de Guadix (Møller, Lindén, Soler, Soler, & Moreno, 1995),
Spain, males were described not only as having longer wings (wing length
and 3rd primary) and tail, but also as being heavier
and with a longer tarsus than females. This indicates that sexual size
dimorphism on this species may differ across its distribution. The fact
that our males showed longer wings and tail, but similar body mass and
tarsus, a proxy for body size (Freeman & Jackson, 1990; Pérez-Granados
& Seoane, 2018; Rising & Somers, 1989), suggests a higher flight
capability of males compared to females. It has been suggested that the
larger wings and tail of male black wheatear’s could be related to their
stone-carrying behaviour (Pérez-Granados & Seoane, 2018; Soler, Soler,
Møller, Moreno, & Lindén, 1996) that is mainly done by males (Aznar &
Ibáñez-Agulleiro, 2016; Moreno, Soler, Møller, & Linden, 1994). Males
also move more often in their territories than females, especially for
territory defence, not only against conspecifics, but also against other
birds of different sizes (Møller, 1992; Prodon, 1985). Regarding the
thicker bill of males, it could also be an adaptation to the
stone-carrying behaviour and higher aggressivity.
The dietary composition of black wheatear observed in our study was
largely similar to that documented elsewhere. In particular, the large
dietary spectrum of arthropod groups and the ability to hunt relatively
large prey such as reptiles was already reported from natural habitats
of Spain, where the most frequent prey were also ants (Hodar, 1995;
Richardson, 1965). The highest difference found between previous dietary
studies of this species and our work, is the high frequency of berries
detected in our study. To some extent this could be due to the different
methods used for the identification of the droppings remains (da Silva
et al., 2019a). However, it is more likely related to differences in
habitat, since the Portuguese population occurs mainly in traditional
agricultural habitats (vineyards and olive groves) where Solanum
nigrum is a very widespread and abundant herb, providing a high number
of ripe fruits, while the studied Spanish populations were located in
shrub steppe areas, presumably with a lower availability of
berry-bearing plant species during the wheatear’s breeding season
(Hodar, 1995).
The differences in diet composition observed in our study are likely
more related to sexual behavioural differences during the breeding
season than to the morphometric differences observed. Although males
have a more robust bill than females, its length and width is similar,
which in principle allows both sexes to capture and swallow similar prey
items. In some birds it has been reported that females tend to forage
closer to their offspring than males (Sunde, Bølstad, & Møller, 2003).
This behaviour could lead females to prey more often on abundant and
predictable prey like ants, even if these are smaller and less
nutritious (Dean & Milton, 2018). On the other hand, the higher
mobility of males within territories could explain the lower frequency
of some less nutritious prey (e.g., ants), and the wider range of other
prey, likely less predictable and abundant.
As far as we could find, this is the first example of a monomorphic (or
minor dimorphic) passerine species exhibiting dietary differences
between sexes, during the breeding season.
Usually, the more sexually dimorphic a bird species is a higher resource
differentiation is expected (Fonteneau et al., 2009; Lewis et al., 2005;
Phillips et al., 2011; Selander, 1966). Nevertheless, on some
monomorphic seabirds species, different foraging areas have been
described between sexes, especially in the beginning of the breeding
period (Cleasby et al., 2015; Hedd et al., 2014; Pinet, Jaquemet,
Phillips, & Le Corre, 2012). On two New Guinean whistlers, passerine
species with little sexual dimorphism, vertical segregation was also
found between sexes and attributed to male territory defence and
intersexual food resource differentiation (Freeman, 2014). Nonetheless,
it is not clear how spatial segregation translates into dietary
segregation, and there seems to be little evidence of dietary
segregation in monomorphic species (Catry et al., 2019; Phillips et al.,
2011), despite some exceptions (Cleasby et al., 2015). Regardless of the
main cause for the dietary differentiation found in our study, it shows
a sexual dietary differentiation during the breeding period, which may
help lowering intraspecific competition, which can be especially
important in the (semi-)arid landscapes where black wheatears occur.
Overall, our study shows how even minor dimorphic bird species can have
subtle differences in diet during their breeding season. The differences
found were most likely related to sexual differences in behaviour rather
than morphology, which means that this pattern might be far more common
than what is currently recognized in birds. Moreover, this pattern was
only possible to detect thanks to the high taxonomic resolution offered
by metabarcoding, as analyses at higher taxonomic ranks were not able to
identify such differences. At a time when metabarcoding is starting to
be used to re-visit and assess the diet of many species, as well as to
study other species interactions like pollination, it becomes
increasingly important to understand the impact of taxonomic resolution
in ecological studies (Renaud, Baudry, & Bessa‐Gomes, 2020). Finally,
this study is an example of how the development of new techniques, such
as metabarcoding, can help ecological studies go a bit further and gain
better insights into fine ecological patterns that could otherwise go
unnoticed.