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Hummingbird-plant networks in rupestrian fields and riparian forests in altitudinal areas of the Serra da Canastra National Park, Minas Gerais, Brazil

Redes de beija-flor-planta em campos rupestres e florestas ripárias em áreas de altitude do Parque Nacional da Serra da Canastra, Minas Gerais, Brasil

Abstract:

Hummingbirds are specialized in consumption of nectar and play an important role in Neotropical plant communities acting as pollinator organisms. Despite the importance of this mutualistic interaction, studies about hummingbird-plant relationships remain scarce regarding the Cerrado domain (Brazilian savanna). In this study, we aimed to describe the interaction network between hummingbirds and plants in rupestrian fields and riparian forests located in altitudinal areas of the Serra da Canastra National Park. We established two transects in each phytophysiognomy, that were sampled monthly for four days, from November 2018 to October 2019. Flowering plants in each transect were observed each survey, and all the visiting hummingbirds were recorded. Networks were constructed using the R bipartite package, considering each phytophysiognomy type, and grouping data of both environments. From these three network arrangements, we extracted complementary metrics at the community level (modularity, nestedness, and network specialization index), and at the species level (species specialization index and species strength in the network). We recorded 647 interactions between 10 hummingbird species and 23 flowering plant species. The hummingbird Colibri serrirostris was responsible for most of observed bird-plant interactions and the plant Qualea cordata was the most visited. The general network was significantly modular, comprising four modules, and showed considerable high specialization and low nestedness. The interaction network in the rupestrian field showed a higher specialization, nestedness, and modularity index when compared to riparian forests, while the metrics of this ecosystem did not differ from those of the general network. However, the metrics at hummingbird species level did not differ significantly between phytophysiognomies. This study corroborated some findings about hummingbird-plant networks in other areas of the Cerrado domain, but also pointed idiosyncrasies in networks of the investigated phytophysiognomies, especially the rupestrian fields.

Keywords:
Cerrado; gallery forest; nectivory; pollination; rocky grassland

Resumo:

Beija-flores são especializados no consumo de néctar e desempenham um papel importante em comunidades de plantas Neotropicais, agindo como organismos polinizadores. Apesar da importância dessa relação mutualística, estudos sobre a relação de plantas e beija-flores ainda são escassos no Cerrado. Neste estudo, objetivamos descrever a rede de interações entre beija-flores e plantas em campos rupestres e matas ripárias localizadas em áreas de altitude do Parque Nacional da Serra da Canastra. Estabelecemos dois transectos em cada fitofisionomia, os quais foram amostrados mensalmente durante quatro dias, de novembro de 2018 a outubro de 2019. Plantas em floração em cada transecto foram observadas em cada amostragem, e todos os beija-flores visitantes foram registrados. As redes de interação foram construídas utilizando o pacote bipartite do R, considerando cada fitofisionomia e agrupando os dados de ambos os ambientes. Destes três arranjos de rede, extraímos métricas complementares no nível de comunidade (modularidade, aninhamento e índice de especialização de rede) e no nível de espécies (índice de especialização da espécie e força da espécie na rede). Registramos 647 interações entre 10 espécies de beija-flores e 23 espécies de plantas. O beija-flor Colibri serrirostris foi o responsável pela maior parte das interações ave-planta observadas e a planta Qualea cordata foi a mais visitada. A rede geral foi significativamente modular com quatro módulos e apresentou considerável especialização e baixo aninhamento. A rede de interações no campo rupestre apresentou maior especialização, aninhamento e índice de modularidade quando comparada à mata ripária, enquanto as métricas deste ecossistema não foram diferentes da rede geral. Entretanto, as métricas no nível de espécies de beija-flores não apresentaram diferenças significativas entre as fitofisionomias. Este estudo corrobora alguns resultados de redes de beija-flores-plantas em outras áreas do domínio do Cerrado, mas também aponta idiossincrasias nas redes das fitofisionomias investigadas, especialmente os campos rupestres.

Palavras-chave:
Campo rupestre; cerrado; mata de galeria; nectivoria; polinização

Introduction

Interactions between plants and animals are present in all terrestrial ecosystems, and biotic pollination is estimated to occur in 94% of tropical plants (Ollerton et al. 2011OLLERTON, J., WINFREE, R., & TARRANT, S. 2011. How many flowering plants are pollinated by animals? Oikos. 120(3):321-326.). These mutualistic interactions create complex networks and the comprehension of patterns and processes that structure them can be used to predict the dynamics and stability of biological communities (Bascompte 2009BASCOMPTE, J. 2009. Disentangling the web of life. Science, 325(5939):416-419., Thompson et al. 2012THOMPSON, R.M., BROSE, U., DUNNE, J.A., HALL JR, R.O., HLADYZ, S., KITCHING, R.L MARTINEZ, N.D., RANTALA, H., ROMANUK, T.N., STOUFFER, D.B. & TYLIANAKIS, J.M. 2012. Food webs: reconciling the structure and function of biodiversity. Trends Ecol Evol, 27(12):689-697., Schleuning et al. 2015SCHLEUNING, M., FRÜND, J. & GARCÍA, D, 2015. Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait‐based concepts to plant-animal interactions. Ecography, 38(4):380-392., Bartomeus et al. 2016BARTOMEUS, I., GRAVEL, D., TYLIANAKIS, J.M., AIZEN, M.A., DICKIE, I.A. & BERNARD‐VERDIER, M., 2016. A common framework for identifying linkage rules across different types of interactions. Funct Ecol, 30(12):1894-1903.; Tinoco et al. 2017TINOCO, B.A., GRAHAM, C.H., AGUILAR, J.M. & SCHLEUNING, M. 2017. Effects of hummingbird morphology on specialization in pollination networks vary with resource availability. Oikos, 126(1):52-60.). Recently, an increasing number of studies have been elucidated pollination relationships patterns and its architecture in the light of the network approach (e.g., Vizentin-Bugoni et al. 2014VIZENTIN-BUGONI, J., MARUYAMA, P.K., & SAZIMA, M. 2014. Processes entangling interactions in commu- nities: forbidden links are more important than abundance in a hummingbird-plant network. P Roy Soc B-Biol Sci, 281(1780):20132397., Souza et al. 2018SOUZA, C.S., MARUYAMA, P.K., AOKI, C., SIGRIST, M.R., RAIZER, J., GROSS, C.L. & ARAUJO, A.C. 2018. Temporal variation in plant-pollinator networks from seasonal tropical environments: higher specialization when resources are scarce. J Ecol, 106(6):2409-2420., Maruyama et al. 2019MARUYAMA, P.K., BONIZÁRIO, C., MARCON, A.P., D’ANGELO, G., SILVA, M.M., NETO, E.N.S., OLIVEIRA, P.E., SAZIMA, I., SAZIMA, M., VIZENTIN-BUGONI, J. ANJOS, L., RUI, A.M. & MARÇAL-JÚNIOR, O.M. 2019. Plant-hummingbird interaction networks in urban areas: Generalization and the importance of trees with specialized flowers as a nectar resource for pollinator conservation. Biol Conserv, 230:187-194.). However, networks remain under investigated in the tropics with a particular gap in central Neotropical savanna areas (Vizentin-Bugoni et al. 2018VIZENTIN-BUGONI, J., MARUYAMA, P.K., SOUZA, C.S., OLLERTON, J., RECH, A.R. & SAZIMA, M., 2018. Plant-pollinator networks in the tropics: a review. In Ecological Networks in the Tropics (W. Dáttilo & V. Rico-Gray, eds), Springer International Publishing, Cham, p.73-91.), especially in attitudinal environments and open vegetation.

The Cerrado is the second largest morphoclimatic and phytogeographic domain of Brazil and the most biodiverse savanna of the world (Ratter et al. 1997RATTER, J.A., RIBEIRO, J.F. & BRIDGEWATER, S. 1997. The Brazilian cerrado vegetation and threats to its biodiversity. Ann Bot, 80(3):223-230., Ribeiro & Walter 1998RIBEIRO, J.F. & WALTER, B.M.T. 1998. Fitofisionomias do bioma Cerrado. In: Cerrado: ambiente e flora. (S.M. Sano & S.P. Almeida, eds). EMBRAPA-CPAC, Planaltina, p.89-166.). It harbors diverse types of phytophysiognomies, that encompasses grasslands, savanic and forest formations, considered within the Cerrado sensu lato classification, and other singular ecosystems such as rupestrian environments and riparian forests (see Ribeiro & Walter 1998RIBEIRO, J.F. & WALTER, B.M.T. 1998. Fitofisionomias do bioma Cerrado. In: Cerrado: ambiente e flora. (S.M. Sano & S.P. Almeida, eds). EMBRAPA-CPAC, Planaltina, p.89-166.). The rupestrian fields, regionally called campos rupestres, are a montane vegetation complex that occurs over rock outcrops (Alves et al. 2014ALVES, R., SILVA, N., OLIVEIRA, J., &MEDEIROS, D. 2014. Circumscribing campo rupestre-megadiverse brazilian rocky montane savanas. Braz J Biol, 74(2):355-362., Silveira et al. 2016SILVEIRA, F.A., NEGREIROS, D., BARBOSA, N.P., BUISSON, E., CARMO, F. F., CARSTENSEN, D.W., CONCEIÇÃO, A.A., CORNELISSEN, T.G., ECHTERNACHT, L., FERNANDES, G.W., GARCIA, Q.S., GUERRA, T.J., JACOBI, C.M., LEMOS-FILHO, J.P., LE STRADIC, S., MORELLATO, L.P.C., NEVES, F.S., OLIVEIRA, R.S., SCHAEFER, C.E., VIANA, P.L. & LAMBERS, H. 2016. Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil, 403(1-2):129-152.). It is predominantly dominated by herbaceous and shrubby vegetation that have xeromorfic features (Alves et al. 2014ALVES, R., SILVA, N., OLIVEIRA, J., &MEDEIROS, D. 2014. Circumscribing campo rupestre-megadiverse brazilian rocky montane savanas. Braz J Biol, 74(2):355-362., Conceição et al. 2016CONCEIÇÃO, A.A., RAPINI, A., CARMO, F.F., BRITO, J.C., SILVA, G.A., NEVES, S.P.S. & JACOBI, C.M. 2016. Rupestrian Grassland Vegetation, Diversity, and Origin. In Ecology and Conservation of Mountaintop Grasslands in Brazil (G.W. Fernandes, ed). Springer International Publishing, Cham, p.105-127., Morellato & Silveira 2018MORELLATO, L.P.C. & SILVEIRA, F.A.O. 2018. Plant life in campo rupestre: New lessons from an ancient biodiversity hotspot. Flora, 238:1-10). The riparian forests occur alongside waterbodies and, unlike the adjacent grassland vegetation, are little affected by water restriction (Ribeiro & Walter 1998RIBEIRO, J.F. & WALTER, B.M.T. 1998. Fitofisionomias do bioma Cerrado. In: Cerrado: ambiente e flora. (S.M. Sano & S.P. Almeida, eds). EMBRAPA-CPAC, Planaltina, p.89-166., Coelho et al. 2007). This feature may have implications for the dynamics of interactions between animals and plants since the phenology of plant species is often associated with the water regime (Conceição et al. 2007CONCEIÇÃO, A.A., FUNCH, L.S. & PIRANI, J.R. 2007. Reproductive phenology, pollination and seed dispersal syndromes on sandstone outcrop vegetation in the “Chapada Diamantina”, northeastern Brazil: population and community analyses. Braz J Bot, 30(3):475-485.). Additionally, animals can move between different habitats according to the availability of resources, preferences for habitats and behavioral characteristics (Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747., 2019MARUYAMA, P.K., BONIZÁRIO, C., MARCON, A.P., D’ANGELO, G., SILVA, M.M., NETO, E.N.S., OLIVEIRA, P.E., SAZIMA, I., SAZIMA, M., VIZENTIN-BUGONI, J. ANJOS, L., RUI, A.M. & MARÇAL-JÚNIOR, O.M. 2019. Plant-hummingbird interaction networks in urban areas: Generalization and the importance of trees with specialized flowers as a nectar resource for pollinator conservation. Biol Conserv, 230:187-194., Rodrigues & Rodrigues 2015RODRIGUES, L.C. & RODRIGUES, M. 2015. Floral resources and habitat affect the composition of hummingbirds at the local scale in tropical mountaintops. Braz J Biol, 75(1):39-48.). Therefore, differences between phytophysiognomies may play an important role in structuring the plant-pollinator interaction networks, which is particularly evident among hummingbirds (e.g., Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747., 2019MARUYAMA, P.K., BONIZÁRIO, C., MARCON, A.P., D’ANGELO, G., SILVA, M.M., NETO, E.N.S., OLIVEIRA, P.E., SAZIMA, I., SAZIMA, M., VIZENTIN-BUGONI, J. ANJOS, L., RUI, A.M. & MARÇAL-JÚNIOR, O.M. 2019. Plant-hummingbird interaction networks in urban areas: Generalization and the importance of trees with specialized flowers as a nectar resource for pollinator conservation. Biol Conserv, 230:187-194., Rodrigues & Rodrigues 2015RODRIGUES, L.C. & RODRIGUES, M. 2015. Floral resources and habitat affect the composition of hummingbirds at the local scale in tropical mountaintops. Braz J Biol, 75(1):39-48.).

Hummingbirds are highly specialized in nectar consumption and act as important pollinator agents in the Neotropics, in such an extent that many plant species have evolved adaptations to attract then (Jordano 1987JORDANO, P. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat, 129(5):657-677., Cronk & Ojeda 2008CRONK Q. & OJEDA I. 2008. Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59:715-727.). Interactions between hummingbirds and plants provide good models to explore the structure of mutualistic networks, due to high dependence of hummingbirds on nectar, convenient sampling, and wide distribution of hummingbird species across nearly the entirety of the Americas (McGuire et al. 2014McGUIRE, J.A., WITT, C.C., REMSEN JR., J., CORL, A., RABOSKY, D.L., ALTSHULER, D.L. & DUDLEY, R. 2014. Molecular phylogenetics and the diversification of hummingbirds. Curr Biol, 24(8):910-916., Vizentin-Bugoni et al. 2018VIZENTIN-BUGONI, J., MARUYAMA, P.K., SOUZA, C.S., OLLERTON, J., RECH, A.R. & SAZIMA, M., 2018. Plant-pollinator networks in the tropics: a review. In Ecological Networks in the Tropics (W. Dáttilo & V. Rico-Gray, eds), Springer International Publishing, Cham, p.73-91.). In this sense, several studies have addressed structural patterns in hummingbird-plant networks, such as considerable specialization (e.g., Maglianesi et al. 2014MAGLIANESI, M.A., BLÜTHGEN, N., BÖHNING-GAESE, K., & SCHLEUNING, M. 2014. Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology, 95(12):3325-3334.), modular structure (e.g., Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747.) and usually low nestedness (e.g., Vizentin-Bugoni et al. 2014VIZENTIN-BUGONI, J., MARUYAMA, P.K., & SAZIMA, M. 2014. Processes entangling interactions in commu- nities: forbidden links are more important than abundance in a hummingbird-plant network. P Roy Soc B-Biol Sci, 281(1780):20132397.). In other words, hummingbird-plant networks are mainly characterized by: (1) few species have many partners and/or interactions, while most have just a few links (Bascompte et al. 2006BASCOMPTE, J., JORDANO, P., & OLESEN, J.M. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312(5772):431-433.); (2) modules of species that interact strongly with each other (Olesen et al. 2007OLESEN, J.M., BASCOMPTE, J., DUPONT, Y.L. & JORDANO, P. 2007. The modularity of pollination networks. P Natl Acad Sci Usa, 104(50):19891-19896.); and (3) species with few interactions do not always form subgroups with species with many interactions (Bascompte et al. 2003BASCOMPTE, J., JORDANO, P., MELIÁN, C.J. & OLESEN, J.M. 2003. The nested assembly of plant-animal mutualistic networks. P Natl Acad Sci Usa, 100(16):9383-9387.). Despite these general patterns, hummingbird-plant networks can show considerable variability through different habitats (e.g., Maruyama et al. 2019MARUYAMA, P.K., BONIZÁRIO, C., MARCON, A.P., D’ANGELO, G., SILVA, M.M., NETO, E.N.S., OLIVEIRA, P.E., SAZIMA, I., SAZIMA, M., VIZENTIN-BUGONI, J. ANJOS, L., RUI, A.M. & MARÇAL-JÚNIOR, O.M. 2019. Plant-hummingbird interaction networks in urban areas: Generalization and the importance of trees with specialized flowers as a nectar resource for pollinator conservation. Biol Conserv, 230:187-194.).

In altitudinal areas inside the Cerrado domain, the riparian forests and open vegetation in rupestrian fields can occur in mosaics at landscape levels (IBAMA 2005IBAMA 2005. Plano de manejo do Parque Nacional da Serra da Canastra. Brasília: Ministério do Meio Ambiente., Fieker et al. 2014FIEKER C.Z., REIS M.G. & BRUNO S.F. 2014. Guia de bolso: 100 aves do Parque Nacional da Serra da Canastra - MG. São Roque de Minas: ICMBio, 124 p.), creating an interesting situation in which hummingbirds can use floral resources from both ecosystem types. Thus, using the ecological network approach, we aimed to characterize the interactions between hummingbirds and their floral resources in the main plateau of the Serra da Canastra National Park (SCNP), a federal Conservation Unit in the state of Minas Gerais, Brazil, where, as far as we know, there are no surveys on mutualistic interactions between bird pollinators and the visited flower community. We investigated whether the interactions between hummingbirds and their floral resources differ between vegetation types, reflected in network topologies and specialization metrics.

Material and Methods

1. Study area

This study was conducted in the SCNP, in the plateau known as Chapadão da Canastra (20°13’51.52”S, 46°29’11.39”W; Cunha et al. 2019CUNHA, I. L. D., REIS, M. G., FIEKER, C. Z., & DIAS, M. M. 2019. Brasilia tapaculo (Scytalopus novacapitalis) seasonality and site occupancy in altitudinal riparian environments after non-natural burnings and feral pig invasion in Serra da Canastra National Park, Brazil. Braz J Biol, 81(2):278-284.) located in the southwestern portion of the Minas Gerais state, Brazil (IBAMA, 2005IBAMA 2005. Plano de manejo do Parque Nacional da Serra da Canastra. Brasília: Ministério do Meio Ambiente.). The geographical limits comprise an area of 71,525 ha at 1,250 to 1,450 m of elevation (Cunha et al. 2019CUNHA, I. L. D., REIS, M. G., FIEKER, C. Z., & DIAS, M. M. 2019. Brasilia tapaculo (Scytalopus novacapitalis) seasonality and site occupancy in altitudinal riparian environments after non-natural burnings and feral pig invasion in Serra da Canastra National Park, Brazil. Braz J Biol, 81(2):278-284.), harboring several phytophysiognomies of the Cerrado domain. The regional climate is characterized by a well-marked seasonality, with cold and dry winters (dry season) from April to September, and rainy summers (wet season) from October to March (IBAMA, 2005IBAMA 2005. Plano de manejo do Parque Nacional da Serra da Canastra. Brasília: Ministério do Meio Ambiente.). Our fieldwork was carried out in two phytophysiognomies: the rupestrian fields (campos rupestres), characterized by open vegetation (grassland and open savanna) in gravelly/sandy soil with clumps of rocky outcrops in altitudinal mountaintops, and the riparian forests, composed by riverine forests alongside streams and rivers, and small patches of forests in hydromorphic soils, commonly associated to water sources and connected with gallery forests.

2. Field methods

From November 2018 to October 2019, we made 11 expeditions to the SCNP with an interval of 30 to 35 days. Each data collection comprised four days of observations in four different sites. Two transects were established in riparian forest (each of approximately 100 m) and two in the rupestrian fields (each of approximately 200 m) (see Silva 2021SILVA, M.M. 2021. Beija-flores e seus recursos florais no Parque Nacional da Serra da Canastra. Dissertação de Mestrado, Universidade Federal de São Carlos, São Carlos. for detailed information). The differences in the transect length between the two phytophysiognomies is due to the difficulty in going through the fragments of riparian forests. Each site was sampled monthly during morning and afternoon, from 8 am to 12 pm and later from 3 pm to 6 pm (approximately seven hours per site per month), totalizing 308 hours of sampling effort. Observations of hummingbird-plant interactions normally start at sunrise (Machado & Rocca 2010MACHADO, C. G. & ROCCA, M. A. 2010. Protocolos para o estudo de polinização por aves. In: MATTER, S.V., STRAUBE, F.C., ACCORDI, I., PIACENTINI, V. & CÂNDIDO-JÚNIOR, J.F. (Eds.) Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Technical Books, Rio de Janeiro, p. 471-489.). However, we defined the observation time as mentioned above due to logistical difficulties to reach the study sites.

Flowering plants were observed for 30 minutes with direct visualization with the aid of binoculars (Nikon 8 x 42 mm). Whenever possible, more than one plant was observed simultaneously. For each plant species, we recorded the number of visits by hummingbirds, considering as one visit the foraging performed within an uninterrupted flight regardless of the number of flowers visited (Las-Casas et al. 2012LAS-CASAS, F.M. G., AZEVEDO-JÚNIOR, S.M., & DIAS-FILHO, M.M. 2012. The community of hummingbirds (Aves: Trochilidae) and the assemblage of flowers in a Caatinga vegetation. Braz J Biol, 72(1):51-58.). A new visit was counted when the bird perched and returned to the floral resource or when it left the site and returned to forage on flowers again. Only legitimate visits were considered, that is, when the bird accesses the floral resource through the opening of the corolla and meets the reproductive structures of the flower.

Identification of the hummingbirds were confirmed with the help of a specialized guide when necessary (Grantsau 1989GRANTSAU, R. 1989. Os beija-flores do Brasil: uma chave de identificação para todas as formas de beija-flores do Brasil com a descrição de quatro novas formas. Editora Expressão e Cultura, Rio de Janeiro.) and scientific nomenclature followed Piacentini et al. (2015)PIACENTINI, V.Q., ALEIXO, A., AGNE, C.E., MAURÍCIO, G.N., PACHECO, J.F., BRAVO, G.A., BRITO, G.R.R., NAKA, L.N., OLMOS, F., POSSO, S., SILVEIRA, L.F., BETINI, G.S., CARRANO, E., FRANZ, I., LEES, A.C., LIMA, L.M., PIOLI, D., SCHUNCK, F., AMARAL, F.R., BENCKE, G.A., COHN-HAFT, M., FIGUEIREDO, L.F.A., STRAUBE F.C. & CESARI, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia, 23(2): 91-298.. Samples from all plants visited were collected for identification to the highest possible taxonomic resolution and subsequently deposited at the herbarium of the Federal University of São Carlos (SPSC, acronym according to Thiers 2020THIERS, B. 2020 (continuously updated). Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium, New York. Available from: http://sweetgum.nybg.org/science/ih/
http://sweetgum.nybg.org/science/ih/...
).

3. Data analysis

To characterize and analyze hummingbird-plant network in the SCNP, we built interaction matrices weighted by the total number of visits observed between pairs of species. In these, three arrangements of interaction networks considering the entire period of study were considered: (1) general interaction network, in which all data collected in this study were grouped into a single matrix; (2) network of interactions in the rupestrian fields; (3) network of interactions in the riparian forests.

From these different network arrangements, we extracted three complementary metrics that describe different aspects of the network, namely: modularity, nestedness and network specialization index. The modularity in interaction networks allows the identification of subgroups (modules) of species that interact strongly with each other and with less intensity with species outside the module (Olesen et al. 2007OLESEN, J.M., BASCOMPTE, J., DUPONT, Y.L. & JORDANO, P. 2007. The modularity of pollination networks. P Natl Acad Sci Usa, 104(50):19891-19896.). Here, we compute modularity through DIRTLPAwb+ algorithm (Beckett 2016BECKETT, S.J. 2016. Improved community detection in weighted bipartite networks. Roy Soc Open Sci, 3(1):140536.). The modularity index ranges from 0 to 1, for the minimum modularity and maximum modularity, respectively. Nestedness was calculated using the weighted version of the metric NODF, the wNODF (Almeida-Neto & Ulrich 2011ALMEIDA-NETO, M. & ULRICH, W. 2011. A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Modell Softw, 26(2):173-178., Almeida-Neto et al. 2008ALMEIDA‐NETO, M., GUIMARAES, P., GUIMARAES JR, P.R., LOYOLA, R.D., & ULRICH, W. 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117(8), 1227-1239.). The wNODF index range is from 0 to 100, indicating, in this order, the minimum and maximum nestedness structure. The complementary specialization of the network was estimated using the metric H2’. This index is derived from Shannon entropy and describes the degree of specialization of a quantitative network (Blüthgen et al. 2006BLÜTHGEN, N., MENZEL, F., & BLÜTHGEN, N. 2006. Measuring specialization in species interaction networks. BMC Ecol, 6:9.). Its variation is from 0 to 1, indicating the lowest and highest specialization, respectively.

The metrics of the observed networks described above were compared with the averages of the estimated metrics of 1.000 random null models, using Z tests. We consider the significance level of 0.05, so if test values ranged between-1.96 and 1.96, it is accepted the null hypothesis of equality of metrics observed at the expense of those expected at random. The null models were generated using the vaznull method (Vázquez et al. 2007VÁZQUEZ, D.P., MELÍAN, C.J., WILLIAMS, N.M., BLÜTHGEN, N., KRASNOV, B.R. & POULIN, R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos, 116(7):1120-1127.). In this procedure, the observed network connectance is maintained and the totals of individual interactions are randomized. The analyzes were performed using the “bipartite” package (Dormann et al. 2008DORMANN, C.F., GRUBER, B. & FRÜND, J. 2008. Introducing the bipartite package: analysing ecological networks interaction, R News, 8:8-11.), with the metrics extracted by the function “networklevel” (Dormann et al. 2009DORMANN, C.F., FRÜND, J., BLÜTHGEN, N., & GRUBER, B. 2009. Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal, 2: 7-24.).

Regarding the species level network metrics, we consider only the metrics related to hummingbirds, as the plants may have other pollinators that were not identified here. The estimated metrics were: (1) species specialization by the d’ index and (2) species strength in the network. The first metric calculates how much a species deviates from a random sample of available interaction partners (Blüthgen et al. 2006BLÜTHGEN, N., MENZEL, F., & BLÜTHGEN, N. 2006. Measuring specialization in species interaction networks. BMC Ecol, 6:9.). Its variation occurs from 0 to 1, in a minimum and maximum specialization scale, respectively. The last one estimates the sum of the dependencies of each species (Bascompte et al. 2006BASCOMPTE, J., JORDANO, P., & OLESEN, J.M. 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312(5772):431-433.). We obtained these metrics also through the “bipartite” package, using the function “specieslevel” (Dormann 2011DORMANN, C.F. 2011. How to be a specialist? quantifying specialization in pollination networks. Network Biology, 1(1):1-20.). All analyzes were performed in the computational environment R Core Team (2020)R Core Team 2020. R: A language and environment for statistical computing..

Results

We recorded 647 interactions from 10 hummingbird species (Table 1) on 23 flowering plant species distributed in 14 plant families (Table 2). Seven species of hummingbirds visited 12 plant species in rupestrian fields and nine hummingbird species visited 13 species in riparian vegetation (see Figure 1). Only two plant species were recorded in both phytophysiognomies: Psittacanthus robustus and Hololepis pedunculata. Six bird species were observed interacting with plants in both vegetation types, while Calliphlox amethystina used nectar resources only in rupestrian fields, and Amazilia fimbriata, Anthracothorax nigricollis, and Heliomaster squammosus interacted with flowering plants only in riparian forests.

Table 1
Hummingbird assemblage (Aves: Trochilidae) recorded visiting plant species in riparian forests and rupestrian fields in the Serra da Canastra National Park, MG, southeastern Brazil, from Nov/2018 to Oct/2019. NI = number of interactions recorded; ss = species strength in the network; d’ = species specialization.
Table 2
Plants visited by hummingbirds in riparian forests and rupestrian fields of the Serra da Canastra National Park, MG, southern Brazil, from Nov/2018 to Oct/2019. ● Plants with ornithophilous syndrome; N.V = Number of visits. D = Degree of visits by hummingbirds.

Figure 1
Plant-hummingbird network in (A) rupestrian fields and (B) riparian forests of the Serra da Canastra National Park, from Nov/2018 to Oct/2019. Plant species are represented by black and hummingbirds by gray polygons.

Colibri serrirostris was responsible for most of observed bird-plant interactions (55.49%), followed by Eupetomena macroura (16.54%) and Chlorostilbon lucidus (15.76%). The high number of interactions observed for C. serrirostris was mainly attributed to visits to the entomophilous species Qualea cordata during massive flowering events, representing 22.27% of all observed interactions, which made this plant the most visited in the study area. The ornithophilous species Psittacanthus robustus, Hololepis pedunculata and Justicia monticola also received a high number of visits, however, from more species of hummingbirds (Figure 1 and Table 2).

The overall hummingbird-plant network was significantly modular (Qobs = 0.36, Qd = 0.24, z-score = 17.58, p-value < 0.0005), comprising four modules of interacting species (Figure 2). Of those, two modules were composed of a single interacting pair, Heliomaster squamosus grouped with Asteraceae sp.1 and Calliphlox amethystina with Lychnophora sp. The hummingbirds C. serrirostris and Amazilia lactea were arranged in a single module with 14 plant species. The module with the highest number of hummingbird species, namely, Amazilia fimbriata, Antrhacothorax nigricollis, Chlorostilbon lucidus, Eupetomena macroura, Thalurania furcata and the only hermit species in the community, Phaethornis pretrei, has been associated with eight plant species, as shown in Figure 2. The network also indicated a considerable specialization (H2obs = 0.44, H2d = 0.32, z-score = 17.12, p-value < 0.0005) and low nestedness (wNODFobs = 33.49, wNODFd =-17.08, z-score =-3.72, p-value < 0.0005).

Figure 2
Plant-pollinator community in the main plateau of the Serra da Canastra National Park with indication of interaction abundance (darker tones represent a greater number of records) and the four identified modules of interactions. Data collected from Nov/2018 to Oct/2019.

Regarding to the species level network, the highest values of species strength index were registered to C. serrirostris (s.s = 13.2649) and C. lucidus (s.s = 3.6593). The lowest values of species strength were attributed to the hummingbird species A. fimbriata (s.s = 0.0354) and A. nigricollis (s.s = 0.2857). On the other hand, C. lucidus obtained the lowest values of d’ index (d’ = 0.1729), indicating to be a generalized pollinator, while C. serrirostris was moderately generalized to specialized according to the metric (d’ = 0.6). The species that had d’ indexes above that observed for C. serrirostris were A. nigricollis, H. squamosus and C. amethystina (Table 1). These hummingbirds visited one or two plant species, while C. serrirostris obtained the highest degree from the community, interacting with 18 plant species, of which it was the exclusive visitor of five plants, including Barbacenia lymansmithii, an endemic species only recorded in grasslands and rupestrian fields of the SCNP (Mello-Silva & Menezes 1999MELLO-SILVA, R. & MENEZES, N.L. 1999. Barbacenia lymansmithii (Velloziaceae). Harvard Papers in Botany, p.271-274.).

When considering networks for the two sampled physiognomies, we observed some idiosyncrasies between the environments and in relation to the completeness network. The network of the rupestrian fields showed higher specialization (H2obs = 0.55, H2d = 0.4, z-score = 9.29, p-value < 0.0005) and low nestedness, but obtained the highest wNODF of comparisons (wNODFobs = 44.64, wNODFd =-8.01, z-score =-1.23, p-value > 0.05) and a higher modularity index (Qobs = 0.38, Qd = 0.26, z-score = 9.85, p-value < 0.0005). The estimated network metrics for riparian forest were similar to those observed for the overall community network, therefore, also considerably specialized (H2obs = 0.41, H2d = 0.32, z-score = 15.01, p-value < 0.0005), but with the lowest estimated nestedness of the analyzes (wNODFobs= 24.02, wNODFd =-32.39, z-score =-5.12, p-value < 0.0005) and the same observed modularity index of the general network (Qobs = 0.36, Qd = 0.23, z-score = 15.86, p-value < 0.0005). The hummingbird species level metrics separated by phytophysiognomies did not differ significantly from each other (dfd’ = 11.54, p-value = 0.53; W species strength = 23, p-value = 0.41).

Discussion

Studies on hummingbird-plant networks have revealed structural patterns characterized by heterogeneity in the distribution of interactions between species (Rodríguez-Flores et al. 2019RODRÍGUEZ-FLORES, C.I., ORNELAS, J.F., WETHINGTON, S. & ARIZMENDI, M.C. 2019. Are hummingbirds generalists or specialists? using network analysis to explore the mechanisms influencing their interaction with nectar resources. PloS one, 14(2):e0211855.), considerable specialization (Maglianesi et al. 2014MAGLIANESI, M.A., BLÜTHGEN, N., BÖHNING-GAESE, K., & SCHLEUNING, M. 2014. Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology, 95(12):3325-3334.), modular structure (Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747.), and low nestedness (Vizentin-Bugoni et al. 2014VIZENTIN-BUGONI, J., MARUYAMA, P.K., & SAZIMA, M. 2014. Processes entangling interactions in commu- nities: forbidden links are more important than abundance in a hummingbird-plant network. P Roy Soc B-Biol Sci, 281(1780):20132397.). These patterns were also detected in this study, considering the complete network and its arrangements for the two phytophysiognomic types sampled (rupestrian fields and riparian forests). However, when comparing the hummingbird-plant interactions network of the rupestrian field and riparian forest, the rupestrian field network was more specialized and nested than the riparian forest network. The structure of the hummingbird-plant interactions network can be influenced, among other factors, by the animals’ habitat preference for forest or open vegetation (Maruyama 2014, 2019). In this sense, the preference for open habitats of the hummingbird with the highest degree and number of interactions in SCNP seems to lead to differences in network topology between the two phytophysiognomies sampled in this study, as discussed below.

In view of the high topographic heterogeneity, a common feature in the rupestrian ecosystems (Alves et al. 2014ALVES, R., SILVA, N., OLIVEIRA, J., &MEDEIROS, D. 2014. Circumscribing campo rupestre-megadiverse brazilian rocky montane savanas. Braz J Biol, 74(2):355-362.), a high spatial turnover in interactions between pollinators and plants can be detected, which are more linked to variations in floristic composition than to differences in pollinator species between sites (see Carstensen et al. 2014CARSTENSEN, D. W., SABATINO, M., TRØJELSGAARD, K., & MORELLATO, L. P. C. 2014. Beta diversity of plant-pollinator networks and the spatial turnover of pairwise interactions. PLoS One 9(11): e112903.). Similarly, we observed noteworthy differences in the floristic composition, even between the same phytophysiognomy sampled in different areas, while the composition of hummingbird species was similar between the sampling sites. In fact, given the high mobility of hummingbirds and frequent generalized choice of floral resources (Stiles 1981STILES, F.G. 1981. Geographical aspects of bird-flower coevolution, with particular reference to Central America. Ann Mo Bot Gard, pages 323-351.; Wolf et al. 1976WOLF, L.L., STILES, F.G. & HAINSWORTH, F.R. 1976. Ecological organization of a tropical, highland hummingbird community. J Anim Ecol, 45(2):349-379.), it is expected a more homogeneous distribution of hummingbird species between different sites of the same region.Conversely, considering explicit variations in the vegetation landscape, such as forest patches immersed in open grasslands, the preference for habitat and/or the restriction on the occurrence of certain species before another hierarchically dominant species can emerge as a structuring pattern for interactions (Dupont et al. 2009DUPONT, Y.L., PADRÓN, B., OLESEN, J.M., & PETANIDOU, T. 2009. Spatio-temporal variation in the structure of pollination networks. Oikos, 118(8):1261-1269., Morales & Vázquez, 2008MORALES, J.M. & VÁSQUEZ, D. 2008. The effect of space in plant-animal mutualistic networks: insights from a simulation study. Oikos, 117(9):1362-1370.). In this sense, the network topologies were consistently different between environments, with the greatest specialization and nestedness in the rupestrian fields.

The formation of subgroups of species that interact more strongly with each other than with species outside the group, that is, the modular arrangement of interactions (Olesen et al. 2007OLESEN, J.M., BASCOMPTE, J., DUPONT, Y.L. & JORDANO, P. 2007. The modularity of pollination networks. P Natl Acad Sci Usa, 104(50):19891-19896.), supported the findings about the differences in network topologies between phytophysiognomies. The module with the highest number of hummingbird species was, above all, associated with the plant species observed in forest patches. Interestingly, this module also included the long-billed hummingbird, Phaethornis pretrei, the only recorded species of the hermit clade, which is capable of travelling long distances using the trapline foraging behavior (McGuire et al. 2014McGUIRE, J.A., WITT, C.C., REMSEN JR., J., CORL, A., RABOSKY, D.L., ALTSHULER, D.L. & DUDLEY, R. 2014. Molecular phylogenetics and the diversification of hummingbirds. Curr Biol, 24(8):910-916.). This result contrasts with other studies also developed in the Cerrado domain, in which P. pretrei has been separated from the other hummingbirds in a single module (Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747., Queiroz 2018QUEIROZ, S.N.P. 2018. Dinâmica temporal e funcional da rede de interações entre plantas e beija-flores no campo rupestre da Serra do Espinhaço, Minas Gerais. Dissertação de Mestrado, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina.), what can be expected given the frequent association of hermit hummingbirds with morphologically specialized flowers of the ornithophilous plants (Feinsinger & Colwell 1978FEINSINGER, P. & COLWELL, R.K. 1978. Community organization among neotropical nectar-feeding birds. Am Zool, 18(4):779-795., Maglianesi et al. 2014MAGLIANESI, M.A., BLÜTHGEN, N., BÖHNING-GAESE, K., & SCHLEUNING, M. 2014. Morphological traits determine specialization and resource use in plant-hummingbird networks in the neotropics. Ecology, 95(12):3325-3334., Maruyama et al. 2014MARUYAMA, P.K., VIZENTIN-BUGONI, J., OLIVEIRA, G.M., OLIVEIRA, P.E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica, 46(6):740-747.). However, this particularity reported here for the interactions between hummingbirds and plants in forest patches does not seem to be associated with greater generalization in the choice of P. pretrei, but the greater frequency of visitation to ornithophilous plant species by hummingbirds belonging to other clades.

While the module formed by the largest number of hummingbird species was mostly composed of plant species from forest patches, another module with only two hummingbird species, Colibri serrirostris and Amazilia lactea, was associated with more than half of the plant species registered in the entire community, mainly with flowering species observed in the rupestrian fields. Similarly, the arrangement of Colibri serrirostris and Amazilia lactea in the same module closely related to plant species in open landscapes of the Cerrado domain was detected in another study (Maruyama et al. 2013MARUYAMA, P.K., OLIVEIRA, G.M., FERREIRA, C., DALSGAARD, B. & OLIVEIRA, P.E. 2013. Pollination syndromes ignored: importance of non-ornithophilous flowers to neotropical savanna hummingbirds. Naturwissenschaften, 100(11):1061-1068.). The hummingbird C. serrirostris interacted not only with all plant species in the module, but with all plants recorded in the rupestrian fields. The high degree of visitation performed by this hummingbird indicated its connecting role in the network of rupestrian fields, which is in line with his preference for open vegetation types (Sick 2001SICK, H. 2001. Ornitologia brasileira. Nova Fronteira, Rio de Janeiro.). In the forest patches, the role as connector species, according to the degree distribution to the plant species visited, was played by Chlorostilbon lucidus.

As pointed out by the modular structure of the network, we found that the interaction network in the rupestrian fields is more specialized and, still, nested than the network in forest patches. These variations in the network topology are probably related to the preference of habitats of the main interacting hummingbird species in each phytophysiognomy. The greater abundance in the rupestrian fields of a hummingbird known to be territorialist (Jacobi & Antonini 2008JACOBI, C.M. & ANTONINI, Y. 2008. Pollinators and defence of Stachytarpheta glabra (verbenaceae) nectar resources by the hummingbird Colibri serrirostris (trochilidae) on ironstone outcrops in south-east Brazil. J Trop Ecol, 24(3):301-308., Justino et al. 2012JUSTINO, D.G., MARUYAMA, P.K. & OLIVEIRA, P.E. 2012. Floral resource availability and hummingbird territorial behaviour on a neotropical savanna shrub. J Ornithol, 153(1):189-197.) seems to be associated with the greater exclusivity of the interactions in these environments. In this context, C. serrirostris was the exclusive visitor of five plant species in the rupestrian field, including the species Barbacenia lymansmithii, endemic to the SCNP (Mello-Silva & Menezes 1999MELLO-SILVA, R. & MENEZES, N.L. 1999. Barbacenia lymansmithii (Velloziaceae). Harvard Papers in Botany, p.271-274.). In other study, carried out in rupestrian ecosystems, the main visitor was C. lucidus (Rodrigues & Rodrigues 2014RODRIGUES, L.C. & RODRIGUES, M. 2014. Flowers visited by hummingbirds in the open habitats of the southeastern Brazilian mountaintops: species composition and seasonality. Braz J Biol, 74(3):659-676.), but in this study, it showed the highest degree of visitation in forest patches. The larger body size and high abundance of C. serrirostris, coupled with its preference for open habitats, seems to lead C. lucidus to forage preferentially in forest environments in the SCNP.

Acknowledgments

We thank CAPES for the scholarship granted to M. Maianne and the Programa de Pós-Graduação em Ecologia e Recursos Naturais (PPG-ERN) of the Universidade Federal de São Carlos (UFSCar). We are grateful to the Serra da Canastra National Park staff for the assistance and ICMBio/SISBIO for the authorization to develop this research; to the Hympar Institute for provide vehicle and a technician (Sr. Airton S. Soares) to help during field work; to Yago Barros-Souza and Márcia Martins for the field support and help in plant identification. We would like to thank Biota Neotropica’s reviewers and Editors for their valuable comments and suggestions.

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Edited by

Associate Editor
Márcia Alexandra Rocca

Publication Dates

  • Publication in this collection
    08 June 2022
  • Date of issue
    2022

History

  • Received
    15 Sept 2021
  • Accepted
    18 Apr 2022
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