The overlooked margins: how cities impact diversity of plants and terrestrial invertebrates along urban streams

Regarding the woody plants, species observed in the study area match other Portuguese riparian ecosystems (Aguiar and Ferreira 2005) and some of the species registered in other Mediterranean streams (Stella et al. 2013). However, there is only about 16–29% overlap between the reference lists of Central Portugal for riparian species (Aguiar et al. 2019; Ranta et al. 2021) and the full list of plant taxa identified in this study. This indicates that most taxa listed were not observed, and most taxa observed here were not listed. This is relevant considering that a large inventory of freshwater plants was made for the assessment of the ecological condition of rivers in the region. This disparity is also partially explained by the high number of non-native plant species found in our streams (29 taxa).

In addition, the presence of nine invasive species as significant elements of the urban flora associated to these streams is also relevant, as these species can have considerable impact on the ecosystems (Rahel 2002; Havel et al. 2015; Alonso et al. 2019). The ability of rivers and streams to function as corridors for circulation and dispersion of plants aids in invasive species’ spread across these ecosystems. The fact that the water flows through cities exposes it to species introduced by humans, and fluctuations in water level create new spaces for colonization (Richardson et al. 2007). This aligns with what was observed in the sites closest to residential areas, where some plant species introduced by humans became part of the riparian vegetation, such as Eriobotrya japonica, Ipomoea indica, Rosa spp. and Solanum spp. An invasive Oxalis pes-caprae was observed at most sites except three, contributing to homogeneization of the flora across the study area. The species, originating in South Africa and currently present across Portugal, spreads easily due to the vast swaths it creates eventually becoming one of the dominant species (invasoras.pt). On the other hand, fruit-eating birds aid in the spread of Phytolacca americana, suggesting that, as other authors have pointed out, the bird fauna may be contributing to this species’ invasion of urban streams (Stella et al. 2013). Acacia dealbata was also registered in the riparian corridors and is particularly relevant due to how successfuly it has spread. Introduced in Portugal as an ornamental plant (Lorenzo et al. 2010), it is notably problematic as an invasive species, partly due to how efficiently it attracts pollinators (Correia et al. 2014). The proliferation of this species, that is functionally different from native ones, affects the chemical cycles of an ecosystem and ultimately changes trophic chains (Ferreira et al. 2021). Finally, the reed Arundo donax was also registered in most sites and is known to spread partly through fragments that float down streams, making this another invasion closely associated with lotic ecosystems and dependent on the streams to persist (Lambert et al. 2010). The poor management of streams in urban areas, with frequent cuts that leave fragments of the reeds inside water, facilitates this process.

Indeed, a factor that can influence the diversity of riparian plant species and the number of non-native and invasive species is the management of the urban streams (Jones and Leather 2013; Jakobsson et al. 2018; Perry et al. 2020). In site 1 (Exploratório), the cutting of tree branches populated by a damaging pest eliminated a species but contributed to the health of these trees, while in site 5 (Hospital), the drastic pruning observed rendered the plants unable to support invertebrates or nesting birds (Jones and Leather 2013). Because less intense human intervention on riparian vegetation has been shown to result in increased biodiversity, this human intervention on riparian vegetation must be carefully considered (Robinson and Lundholm 2012; Watson et al. 2020).

In terms of life forms in the study area, most of the sites were dominated by herbaceous species (hemicryptophytes) along with annual plants that die after they reproduce, surviving unfavourable conditions like winter or drought in the form of seeds (therophytes). This can be explained by the type of climate of the region - Mediterranean, with dry and hot summers (Sotomayor 1988). Therophytes have also been associated with highly disturbed and urbanized sites (Muzafar et al. 2019), which is the case of sites 2 and 1 (Vale das Flores and Exploratório, respectively). Nevertheless, they were the most represented group in site 9 (Fornos), one of the least urbanized. Our results warrant deeper studies that consider in depth the abundance of each species and life form and can potentially bring a valuable perspective to further analyses of the effects of urbanization (Bloch-Petersen et al. 2006).

Finally, the water physio-chemical quality of the streams was correlated to the total richness and plant taxa richness. This confirms that water characteristics in streams can impact both aquatic and terrestrial biodiversity (Schindler et al. 2016; Serra et al. 2019a). According to research, urbanization-related changes in soil chemistry can have an impact on weed density and taxonomic in riparian zones, as well as the ability of the riparian fauna to provide ecosystem services (Hogan and Walbridge 2007; Grella et al. 2018). The distribution of riparian plant species can be affected by a multitude of factors from the nutrients in the water and the speed of currents to the type of soil and how it retains humidity (Aguiar et al. 2019). Indirect effects of changes in water chemistry on terrestrial taxa can also include, for example, alterations to the aquatic invertebrates-based diets of land animals (Kelly et al. 2019). Additionally, urbanization leads to changes in water and soil chemistry over time, making riparian biodiversity a product of both past and present-day conditions (Harding et al. 1998; Preston et al. 2003). As such, the taxa observed may be influenced by the history of changes within the land use and water chemistry parameters that were not analyzed.

Within terrestrial invertebrates the most common, besides the unidentified Acari species, were the leafhopper Cicadella viridis and the snail Cepea nemoralis, that are known as ubiquitous and abundant taxa in urban, peri-urban and pristine habitats (Ożgo 2011; Wang et al. 2019). The butterfly Pararge aegeria, known to easily adapt to urbanization (Kaiser et al. 2016) was observed in all sites except the least urbanized ones, which could indicate a preference for more disturbed sites or a reason for lower abundance in more pristine ones (Máthé and Batáry 2015). On the other hand, some taxa like the beetle Chrysomela populi were observed in our study only at the least urbanized sites thus being a potential indicator of ecological integrity of ecosystems (Gerlach et al. 2013). This beetle and the honeybee (Apis mellifera) were the main species responsible for similarities in terrestrial invertebrate assemblages of the least urbanized sites, also suggesting a vulnerability of A. mellifera, an extremely important generalist pollinator, to the effects of urbanization (Hung et al. 2018; Burdine and McCluney 2019).

Among arthropods, the diversity of spiders found in our sites (N = 10) was lower than the number of spider species previously suggested in the city of Coimbra (Branco et al. 2019 registering 317 in the province as a whole), which may be explained by different sampling methods. Linyphia hortensis and Araneus diadematus, found in sites 1 and 2, respectively, are common in urban areas, albeit with altered habits within cities (Nagy et al. 2018; Dahirel et al. 2019). Pisaura mirabilis, one of the species observed in site 1 (Exploratório), is a generalist species, non-sensitive to moderately sensitive to disturbances (Tajthi et al. 2017; Nagy et al. 2018). Zygiella x-notata on the other hand, seen in site 2 (Vale das Flores), the most urbanized site, is very tolerant to disturbances (Kralj-Fišer et al. 2017), which is in agreement with the local conditions. Indeed, the conditions within cities can bring a multitude of factors that can affect species distribution such as prey availability, city infrastructure increasing or decreasing spaces for spinning webs or building burrows, and the presence of artificial light (Dahirel et al. 2019; Kolenda et al. 2021). In the specific case of streams, flow regulation and water pollution can lead to a decrease in substrate availability for web-spinning spiders and severe changes to their feeding habits, as the aquatic insects that are more tolerant to pollution constitute low quality food for these spiders (Sanchez-Ruiz et al. 2017). Observations in this study point to the presence of complex spider assemblages in the study area that are affected by urbanization in both direct and undirect ways that suggest paths for further investigation.

Overall, we found many terrestrial invertebrate species (N = 62) considered underrepresented. This would require further indepth studies for this group, including more standardized and quantitative sampling efforts. However, it again indicates that there are very different terrestrial conditions associated to the margins of streams within a city. This is not unexpected, considering the wide variety of conditions and uses of the margins of streams that we observed as consequence of the urbanization process: from roads, sidewalks, cycle paths and buildings immediately constructed in the margins of some streams, to agricultural fields, urban orchards or grass lawns, banks occupied by invasive reeds such as the Arundo donax (and other herbaceous plants), or even strips of integrous and complex riparian vegetation. This variety of conditions leads to a wide diversity of habitats and different soil compositions, thus constraining the terrestrial invertebrates and other fauna.

Regarding the invasive terrestrial invertebrate species, only one was detected, i.e. Vespa velutina. This species is native to China and its presence is considered a danger to humans (Choi 2021). It was first detected in mainland Portugal in 2011 and has since expanded rapidly with no signs of halting, posing a threat to native bees. River valleys may function as corridors for this expansion (Carvalho et al. 2020; Laurino et al. 2020; Paixão et al. 2021).

Other invertebrate species registered in three sites have the potential to act as pests: Lauritrioza alacris infesting Laurus nobilis trees in sites 1 and 7 (Exploratório and S. Romão, respectively), and Trioza erytreae infesting a Citrus x sinensis tree in site 6 (Casa do Sal), both known hosts for these species (gd.eppo.int). While L. alacris is native to the Mediterranean region (Mifsud 2020), T. erytreae originates from northeast Africa and has been present in Portugal since at least 2015, posing a threat to citrus due to its ability to be a vector for the bacteria Liberibacter spp., which causes a serious disease in these plants (Cocuzza et al. 2017). Another notable case of parasitic associations between species was the occurrence of Cynips tozae galls in a Quercus robur tree in site 8 (Covões). The hemipteran Eurydema ornata (Linnaeus, 1758) was observed in site 3 (Coimbra-B) and it is known to associate with plants of the Brassicaceae family (gd.eppo.int), which are present in this site, but this association was not observed.

Instances of pollination by insects were recorded as well, albeit decreasing along the urbanization gradient. Matching the literature, the generalist pollinator Apis mellifera (Hung et al. 2018) was observed on the widest variety of plant taxa, and the plant of known generalist character Torilis arvensis (Gibson et al. 2006) presented the widest variety of pollinators. Generalist plants are important for ecosystem-wide plant-pollinator interactions as they lure in a variety of pollinator insects that counter the effects of urbanization and habitat fragmentation (Ashworth et al. 2004; Biella et al. 2019; Wenzel et al. 2020). The observations made in the study area suggest potential for further studies in this field.

Our study reveals the impacts of urbanization on the terrestrial realm of lotic ecosystems that has been vastly overlooked despite their importance for biodiversity conservation and as providers of numerous ecosystem services to the population of cities. From the management perspective, our study highlights the need to rethink city planning to consider all the requirements of stream ecosystems, including the different biological terrestrial elements and the links among them, as changes to one part ultimately impact the whole, as shown by others (Faeth et al. 2011; Feio et al. 2017; Rivaes et al. 2021). Monitoring and control measures should be undertaken to preserve the native biodiversity of urban streams and assure that they are not a vehicle for the dissemination of invasive species. The management of riparian corridors should be the least interventive possible to preserve the integrity of the ecosystems and thus the habitats for different biological groups of species. Measures towards the transference of relevant and practical information on the adequate management of these streams to the city decision makers are thus essential. It is also important to raise awareness of populations to prevent the emergence of new invasions.

Our study also indicates that beside impervious surfaces, urban parks, although usually considered natural areas within cities, may not preserve the regional pool of biodiversity due to a high degree of human intervention, for example, grass lawns, sidewalks, paved accesses, children’s playgrounds, or sports infrastructures and extensive pruning of vegetation. On the other hand, well-preserved urban nature should also promote the interconnectivity between fragmented natural areas, increasing global biodiversity and consequently the performance of ecosystem services (Shwartz et al. 2014).