Alien bird species decrease the diversity of bird communities
across human-disturbed landscapes
Introduced alien species have direct and indirect effects on native
communities, leading to lower taxonomic diversity and negative impacts
on ecosystem functioning. Moreover, other aspects of diversity could be
negatively affected, through alteration of functional and phylogenetic
diversity of a community. This is particularly evident in habitats where
human disturbance may favour alien species, posing an additional
stressor on native communities. Following the community resistance
hypothesis (higher diversity, higher resistance to invasion), we
hypothesized: i) higher taxonomic, functional and phylogenetic diversity
(TD, FD and PD respectively) in non-invaded bird communities (i.e. no
alien bird species); and, ii) lower alien species impact on all
diversity metrics in less human-disturbed areas. We surveyed bird
communities in a modified Mediterranean landscape subject to varying
levels of human disturbance. We tested whether TD, FD and PD indices
were significantly different between non-invaded and invaded bird
communities, and assessed the effect of landscape composition and
configuration on these indices. We found that non-invaded communities
retained higher TD and FD than invaded communities. Alien birds occupied
novel parts of the functional space in invaded communities, but that
they did not fully compensate for the taxonomic and functional diversity
loss caused by the absence of native species. These results were
consistent across different habitats, suggesting weak environmental
filtering of communities. Generally, both communities were negatively
affected by more human-disturbed areas (e.g. agriculture and urban
areas) and enhanced by forest areas and by landscape heterogeneity. Our
results suggest that the occurrence of alien birds negatively affects TD
and FD (but not PD) of bird community assemblages, but that this impact
is stronger in human-modified landscapes. Therefore, since the
conservation of biodiversity in anthropogenic habitats is a worldwide
challenge, researchers should prioritize efforts to assess the effects
of alien species on communities inhabiting those habitats.
Keywords: biological invasion; bird assemblage; diversity
metrics; human-altered landscape; non-native species; community
resistance;
Introduction
Biological invasions are well-established as one of the greatest threats
to ecosystems worldwide due to their negative impacts on native species,
communities and ecosystem functioning (Pyšek et al., 2020; Vilà &
Hulme, 2017). The introduction of alien species has direct and indirect
effects on native biodiversity, potentially disrupting the recipient
community structure (White et al., 2006) through alterations of
functional and phylogenetic diversity (FD and PD, respectively;
Ricciardi et al., 2013). This can occur through expansion or contraction
of native functional and phylogenetic space, affecting ecosystem
functioning and biodiversity maintenance (Finerty et al., 2016; Gerhold
et al., 2011). Studying FD and PD in synergy could lead to a more
comprehensive approach to understanding impacts of alien species on
communities (Cadotte, 2013; Galland et al., 2019), since FD is
associated with ecosystem functioning (Matuoka et al., 2020; Saavedra et
al., 2014), and PD can express differences between species that are not
captured by FD (Whitfeld et al., 2014).
Community resistance (i.e.
the capacity of a community to withstand disturbance; Lake, 2013) to
invasion has been hypothesised to be affected in two distinct and
opposite ways. Taxonomically, functionally and phylogenetically diverse
communities may be more resistant to alien establishment due to higher
competition and greater effectiveness in using the resources available
(Hejda & de Bello, 2013; Lososová et al., 2015). On the other hand,
more diverse communities may have high resource availability that could
be also exploited by alien species, inferring a lower resistance to
invasion (Andrikou-Charitidou & Kallimanis, 2021; Klingbeil & Willig,
2016). Another important ecological property of a community lies in the
concept of ecological resilience, which measures the ability of a given
system to absorb changes in order to maintain the same identity (Folke
et al. 2010). Since resistance is inversely correlated with the degree
of change following a disturbance event (Justus, 2007), a resilient
ecological system should better resist disturbance events such as
invasions, climate or land use changes (Haegeman et al., 2016).
Functional evenness (a component of FD) has been used as a proxy for the
resilience of communities (Lee & Martin, 2017; Morelli et al., 2020;
but see Kosman et al., 2019) and can be a useful measure to assess
species resource use in a given space (Mouchet et al., 2010). High
functional evenness represents efficient use of resources by species in
the community (Lee & Martin, 2017), and low functional evenness implies
under-exploitation of available resources, leading to higher
susceptibility of communities to disturbance (e.g. biological invasions;
Shea & Chesson, 2002).
Disturbed areas (e.g.
human-modified landscapes such as urban and agricultural areas) are well
known to favour alien species establishment in several taxa (Cardador &
Blackburn, 2020; Hulme, 2009; Pyšek et al., 2010). Alien birds, for
example, are better than native bird species at exploiting the
ecological opportunities that arise in human-modified landscapes (the
‘opportunism hypothesis’; Sol et al., 2012). Anthropized areas are thus
highly diversified repositories of alien bird species (e.g. Bonter et
al., 2010; Chiron et al., 2009) and land-use changes caused by the
expansion of urban areas and human-managed landscapes worldwide will
likely increase the spread of generalist, opportunistic non-native
species at the expense of native species (McKinney, 2006). Moreover,
bird communities in disturbed areas are at risk of biotic homogenization
processes acting on the three diversity dimensions (taxonomical,
functional and phylogenetic; Liang et al., 2019), leading to a
generalized decrease in diversity. Since, at a local scale, several
studies have reported how high levels of FD and PD lead to higher
resistance to invasion (Gerhold et al., 2011; Lososová et al., 2015),
the decrease in these diversity dimensions in communities inhabiting
disturbed areas could hamper their resistance, making them more
susceptible to invasion.
Recent studies on above
three diversity dimensions in bird communities have focused on the
association between native and alien bird diversity at a regional scale,
finding a positive association between the two (Andrikou-Charitidou &
Kallimanis, 2021; McKinney & Kark, 2017). Nonetheless, it is at the
local community scale that impacts on biodiversity and ecosystem
functioning take place (Loiola et al., 2018). At this scale, the impact
could be predicted by two contrasting scenarios (Loiola et al., 2018):
alien species establish in a portion of functional and phylogenetic
space formerly occupied by native species (increasing the similarity
between species in invaded communities); or alien species
fill the niche-gap in a community
(limiting similarity), expanding the functional and phylogenetic space
of invaded communities, leading to higher FD and PD compared to
non-invaded communities.
To assess which of these two mechanisms could impact native communities,
a set of tests comparing the three diversity dimensions between
non-invaded and invaded communities is needed (Loiola et al., 2018;
Thuiller et al., 2010): i) non-invaded vs invaded communities (i.e.
assessing the overall effect of invasion); ii) non-invaded vs invaded
communities excluding alien species (assessing if invaded communities
are more prone to invasion than non-invaded communities or if alien
species replace native species’ functional and phylogenetic space in
invaded communities); iii) invaded vs invaded communities excluding
alien species (i.e. assessing the difference in the functional and
phylogenetic space between alien and native species of the same
community).
In this study,we applied this approach to assess the impact of alien
birds on bird community diversity by characterising TD, FD, and PD in a
highly human-modified landscape in southern Portugal with several alien
birds that are currently establishing new populations or expanding
existing ones. To do this we ran the three tests on the three diversity
dimensions, accounting for the effect of landscape. It is hypothesised
that higher resilience and lower alien species impact (higher FD and PD)
is more prevalent in non-invaded bird communities inhabiting less
human-disturbed areas. The novelty of our study lies in the
understanding of the degree of impact of alien bird species on the
diversity of bird communities, and how this interacts with human
modification of the landscape, in order to better assess the
vulnerability of native communities to alien bird species invasion.