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.