Ecological determinants of interactions as key when planning pollinator-friendly urban greening: A plant-hummingbird network example

https://doi.org/10.1016/j.ufug.2021.127298Get rights and content

Highlights

  • Urban greening may benefit pollinator conservation.

  • What determines plant-pollinator interactions in urban areas is not well understood.

  • Phenological overlap was the main mechanism determining interactions.

  • Simulations indicated that native plants are important for network robustness.

  • We show how simulations of species removal can be used for urban conservation.

Abstract

Urban green spaces may function as habitats for pollinators. However, it is poorly understood how distinct ecological drivers determine the interactions between pollinator and plants in urban communities, and how pollinator-friendly plants may be selected based on these determinants. Here, we describe an urban hummingbird-plant interaction network in Brazil and evaluate the ecological determinants of pairwise interactions (abundance, morphology, and phenology). Moreover, we used a modeling framework to simulate species removal from networks while allowing for rewiring of interactions, to contrast the importance of native and exotic plants for the network robustness. The studied network showed low specialization and modularity, with one short-billed hummingbird species, Glittering-throated Emerald (Chionomesa fimbriata), dominating the recorded interactions. Phenological overlap was the main determinant of pairwise interaction frequency between hummingbirds and plants. Because morphological matching did not impose strong constraints in the network, simulation models including rewiring based on morphology conferred high robustness after species removal. Furthermore, as exotic plants were only a minor component in the studied network, their removal did not greatly affect network robustness. Our findings demonstrate the importance of considering phenology when planning urban greening for conservation of pollinators. Additionally, we illustrate an analytical procedure that can be applied to quantitatively assess the importance of distinct species/groups for urban interaction networks.

Introduction

Urbanization drastically modifies the environment, increasingly contributing to loss of habitats and to biotic homogenization (Fournier et al., 2020; McKinney, 2006). In this context, urban green spaces that consist of either natural remnants or artificial environments become important refuges for animals and plants, supporting various ecological relationships including mutualistic ones, such as pollination (Aronson et al., 2017; Rodrigues and Araujo, 2011; Salazar-Rivera et al., 2020). Biotic pollination is a major ecosystem service performed by different groups of animals, including nectarivorous birds such as hummingbirds that play an important role as pollinators of many New World plants (Dalsgaard et al., 2021, Michel et al., 2020; Rodríguez-Flores et al., 2019). However, how such bird-plant interactions are structured and maintained in urban environments is poorly understood (Maruyama et al., 2019).

In recent years, several studies have been conducted with the intention of understanding ecological processes that regulate interactions between species, using ecological networks. This approach allows the mapping of interactions and the inclusion of interaction patterns between species as an additional layer to describe biodiversity (Bascompte et al., 2006; Delmas et al., 2019). Furthermore, it allows the identification of ecological predictors related to the structure of communities, raising important information for the maintenance of species and interactions (Bascompte et al., 2003; Weinstein and Graham, 2017). However, these studies are mostly focused on understanding processes in natural and semi-natural areas, not usually considering sites under human intervention (e.g., Peralta et al., 2020; Vizentin-Bugoni et al., 2014; but see Ramírez‐Burbano et al., 2021). To determine the ecological drivers of interaction network structure in urban environments could help us better understand how biotic communities persist and can be promoted despite urbanization.

Interactions in local communities are determined by ecological drivers including neutrality and niche mediated mechanisms (Pérez-García et al., 2016; Vázquez et al., 2009a, 2009b; Vizentin-Bugoni et al., 2018). Neutral theory posit that abundant species are more likely to find and interact with the most abundant partners, so that more abundant species are likely to interact with each other, while rare species also tend to interact with abundant partners in the network (Vázquez et al., 2009a, 2007). On the other hand, interactions can also be determined by niche mechanisms, which consist of restrictions associated with the traits of the species involved (Vizentin-Bugoni et al., 2014). These include, for instance, when short-billed pollinators cannot access nectar from plants with deep corollas (Maglianesi et al., 2015) or when an interaction does not happen due to spatio-temporal mismatches (Gonzalez and Loiselle, 2016; Maruyama et al., 2014). In hummingbird-plant networks, morphological matching is often described as the major driver of interactions, followed by phenological overlap, while neutrality is less important (Maruyama et al., 2014; Sonne et al., 2020; Vizentin-Bugoni et al., 2014). Moreover, such drivers may also influence the role that species assume within the network (Albrecht et al., 2014; Maruyama et al., 2016), as well as affecting network macrostructures (Sonne et al., 2020), that may ultimately influence the stability of communities (Bascompte and Jordano, 2007; Thébault and Fontaine, 2010).

Considering community stability, the network approach enables the use of simulations to assess how a given community would be affected in the face of species extinction, i.e. its robustness (Memmott et al., 2004). Simulations can help with the identification of key species for community stability and propose measures that minimize negative impacts of disturbance (Memmott et al., 2004; Pocock et al., 2012). Recent advances in this framework includes more realistic simulations which include interaction rewiring after species extirpation from the community, following the neutral- and niche-based drivers to determine the “new” interactions (Vizentin-Bugoni et al., 2020). In the context of plant-animal interactions in urban areas, one key question that remains is the role of native and exotic plant species in supporting fauna (Berthon et al., 2021; Maruyama et al., 2019; Nascimento et al., 2020). Exotic plants are common across the cityscape (Aronson et al., 2014), can be highly attractive and have a role in supporting native pollinators (Chittka and Schürkens, 2001; Staab et al., 2020). Therefore, determining the importance of exotic species to the stability of urban interactions networks could be useful to guide possible actions to manage the urban biodiversity.

Here, we aim to: i) describe the structure of an interaction network between hummingbirds and plants in a tropical urban environment; ii) identify the main mechanisms that determine the frequency of interactions among species, specifically evaluating the importance of neutral and niche-based mechanisms; iii) understand how different species and groups of plants, native or exotic, contribute to the stability of the interaction network.

Section snippets

Study area

We conducted data sampling at the Municipality of Cáceres, Center-South of the state of Mato Grosso (MT), Midwest region of Brazil (16 ° 3′2.63″S and 57°41′5.87″W) (Fig. S1 - Supplementary materials). The predominant ecosystem of the region is the Pantanal wetland, with local vegetation classified as Seasonal Semi-Deciduous Alluvial Forest (Veloso et al., 1991). The climate is classified as Equatorial with dry winter (Aw), with annual precipitation around 1500 mm and average monthly temperature

Results

In total, 5 species of hummingbirds were recorded visiting flowers of 14 plant species (11 natives; Fig. 1). The most abundant hummingbird species was Chionomesa fimbriata (Gmelin, 1788) Glittering-throated Emerald, followed by Anthracothorax nigricollis (Vieillot, 1817) Black-throated Mango. Bill length varied among species, from 17.0 mm in Chionomesa fimbriata to 30.8 mm in Phaethornis pretrei (Lesson & Delattre, 1839) Planalto Hermit, which was recorded only infrequently. Chionomesa fimbriata

Discussion

The hummingbird-plant network evaluated here showed generalized interactions, with low specialization and modularity. A short-billed hummingbird, Chionomesa fimbriata, was the most dominant species in terms of abundance, occurrence during the study period and number of interactions. Interestingly, when considering plants, the mistletoe Psittacanthus cordatus was the species with most interactions, despite not being abundant but presenting an extended flowering. Phenological overlap, a mechanism

Conclusion

Our findings suggest that special attention to phenology of plants is needed when managing urban floral resources for pollinators, since the availability of flowers throughout the seasons is clearly important (e.g., Memmott et al., 2010) as well as promotion of native plants. Generalist species assume core positions in the network, performing an important role for the stability of the system. However, the absence of specialized hummingbirds, which may not be able to overcome the environmental

CRediT authorship contribution statement

Breno Dias Vitorino: Conceptualization, Formal analysis, Investigation, Data curation, Writing - original draft. Angélica Vilas Boas da Frota: Conceptualization, Investigation, Writing - review & editing. Pietro Kiyoshi Maruyama: Conceptualization, Methodology, Validation, Writing - review & editing, Supervision.

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgments

This study was partially financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES)- Finace Code 001, and the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT)through scholarships to AVBF and BDV (CAPES 007/2018). PKM was partially supported by the “Pró-Reitoria de Pesquisa da Universidade Federal de Minas Gerais (Edital 09/2019)” during the writing of this manuscript. We thank Jeferson Vizentin-Bugoni for initial input on sampling design, Camila

References (71)

  • M.F.J. Aronson et al.

    A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers

    Proc. R. Soc. B Biol. Sci.

    (2014)
  • M.F.J. Aronson et al.

    Biodiversity in the city: key challenges for urban green space management

    Front. Ecol. Environ.

    (2017)
  • I. Bartomeus et al.

    Contrasting effects of invasive plants in plant-pollinator networks

    Oecologia

    (2008)
  • J. Bascompte et al.

    Plant-animal mutualistic networks: the architecture of biodiversity

    Annu. Rev. Ecol. Evol. Syst.

    (2007)
  • J. Bascompte et al.

    The nested assembly of plant-animal mutualistic networks

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • J. Bascompte et al.

    Asymmetric coevolutionary networks facilitate biodiversity maintenance

    Science

    (2006)
  • S.J. Beckett

    Improved community detection in weighted bipartite networks

    R. Soc. Open Sci.

    (2016)
  • P. Biella et al.

    Experimental loss of generalist plants reveals alterations in plant-pollinator interactions and a constrained flexibility of foraging

    Sci. Rep.

    (2019)
  • Nico Blüthgen et al.

    Measuring specialization in species interaction networks

    BMC Ecol.

    (2006)
  • N.P. Chacoff et al.

    Evaluating sampling completeness in a desert plant-pollinator network

    J. Anim. Ecol.

    (2012)
  • A. Chao

    Nonparametric estimation of the number of classes in a population

    Scand. Stat. Theory Appl.

    (1984)
  • L. Chittka et al.

    Successful invasion of a floral market

    Nature

    (2001)
  • A. Coetzee et al.

    Urban nectarivorous bird communities in Cape Town, South Africa, are structured by ecological generalisation and resource distribution

    J. Avian Biol.

    (2018)
  • B. Dalsgaard et al.

    The influence of biogeographical and evolutionary histories on morphological trait‐matching and resource specialization in mutualistic hummingbird‐plant networks

    Funct. Ecol.

    (2021)
  • E. Delmas et al.

    Analysing ecological networks of species interactions

    Biol. Rev.

    (2019)
  • C.F. Dormann et al.

    Visualising bipartite networks and calculating some (ecological) indices

    R Package Version 2.15

    (2020)
  • S. Duguay et al.

    Effects of surrounding urbanization on non-native flora in small forest patches

    Landsc. Ecol.

    (2007)
  • F.L.R. Filardi

    Brazilian flora 2020: innovation and collaboration to meet target 1 of the global strategy for plant conservation (GSPC)

    Rodriguesia

    (2018)
  • A. Fisogni et al.

    Urbanization drives an early spring for plants but not for pollinators

    Oikos

    (2020)
  • B. Fournier et al.

    The origin of urban communities: from the regional species pool to community assemblages in city

    J. Biogeogr.

    (2020)
  • O. Gonzalez et al.

    Species interactions in an Andean bird–flowering plant network: phenology is more important than abundance or morphology

    PeerJ

    (2016)
  • N.J. Gotelli et al.

    Null Versus Neutral Models: What’s The Difference?

    Ecography (Cop.).

    (2006)
  • A.S. Hadley et al.

    Forest fragmentation and loss reduce richness, availability, and specialization in tropical hummingbird communities

    Biotropica

    (2018)
  • IBGE 2020 Instituto Brasileiro de Geografia e Estatística. https://cidades.ibge.gov.br/ Accessd 10 nov...
  • D.G. Justino et al.

    Floral resource availability and hummingbird territorial behaviour on a Neotropical savanna shrub

    J. Ornithol.

    (2012)
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      When the structure of hummingbird-plant networks was contrasted across different greenspaces, we found that more urbanized sites showed a trend to be more generalized (low specialization and modularity) than less urbanized sites as natural protected areas. Moreover, all networks were modular, but not nested, which is consistent with previous studies in urban areas in Brazil (Maruyama et al., 2019; Vitorino et al., 2021) and other natural areas in the Neotropics (Araujo et al., 2018; Izquierdo-Palma et al., 2021). Modularity is a ubiquitous feature of hummingbird-plant networks across the Americas in which hummingbird assemblages are composed of functionally distinct species forming strongly interacting subgroups with plants according to morphological and phenological matching (Araujo et al., 2018; Izquierdo-Palma et al., 2021; Martín González et al., 2018; Maruyama et al., 2014).

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