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Floral visitors in urban gardens and natural areas: Diversity and interaction networks in a neotropical urban landscape
Journal Pre-proof Floral visitors in urban gardens and natural areas: diversity and interaction networks in a neotropical urban landscape ´ Linda Mar´ın, Mariana Esther Mart´ınez-Sanchez, Philippe Sagot, Dar´ıo Navarrete, Helda Morales
PII:
S1439-1791(19)30282-8
DOI:
https://doi.org/10.1016/j.baae.2019.10.003
Reference:
BAAE 51211
To appear in:
Basic and Applied Ecology
Received Date:
23 February 2019
Accepted Date:
9 October 2019
Please cite this article as: { doi: https://doi.org/ This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.
Marín et al.
Floral visitors in a neotropical landscape
Title: Floral visitors in urban gardens and natural areas: diversity and interaction networks in a neotropical urban landscape.
Marín, Lindaa*, Mariana Esther Martínez-Sánchezb,c, Philippe Sagota, Darío Navarreted and
a
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Helda Moralesa
Grupo de Agroecología, El Colegio de la Frontera Sur, San Cristóbal de Las Casas,
Departamento de Ecología Funcional, Instituto de Ecología, Universidad Nacional
Autónoma de México, Ciudad de México, Mexico
Consejo Nacional de Ciencia y Tecnología, Ciudad de México, Mexico Laboratorio de Análisis de Información Geográfica y Estadística, El Colegio de la
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d
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Chiapas, Mexico.
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Frontera Sur, San Cristóbal de Las Casas, Chiapas, Mexico.
*Corresponding author. Tel:(52) 1 222 599 5938, email: [email protected] Present address: Universidades Benito Juárez García, Tlaxcala, Mexico
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Highlights
Floral visitor richness and abundance varied with season and management Seasonality had a strong effect on the floral visitor community Urban gardens functioned as an oasis for the floral visitor community Species composition between urban gardens and natural areas was complementary Interaction networks between flowers and their visitors were dynamic and complex across habitats
Abstract 1
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Floral visitors in a neotropical landscape
Because cities concentrate 50% of the world’s population, and are experiencing a reemergence of urban agriculture, we investigated the influences of urban agriculture and surrounding natural areas on floral visitors (bees, wasps, butterflies and flies) and plant species in San Cristóbal de Las Casas, Mexico. Throughout the frost, dry and rainy seasons of 2015, we sampled floral visitors in nine urban gardens and nine natural areas. We found 210 floral visitor species: 78%
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pollinators, 18% predators, and 4% florivores. Rarefaction curves showed that natural areas
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harbor significantly more floral visitor species (148) than home gardens (132). However,
the differences in species composition between habitats and seasons highlight the need to
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view natural areas and home gardens as complementary habitats with which floral visitors
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interact in varying ways, during successive seasons, to meet different needs. Furthermore, mean species richness of floral visitors was influenced mainly by seasonality, and increased
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as seasons progressed from the dry, frost season to the rainy season. Nonetheless, some taxa were influenced by both season and habitat type. Floral visitor abundance was
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influenced by both habitat type and season, with home gardens showing higher abundance across seasons. Moreover, interaction networks for each season were more asymmetric in natural areas than in home gardens. Urban cover in the surrounding landscape influenced in a quadratic way the species number of floral visitors, but not their abundance. Thus, our
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results are evidence that natural areas surrounding cities and urban agriculture contribute to floral visitor communities and their networks.
Keywords: Bees, urban agriculture, pollinators, species fluxes
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Introduction Half of the world’s people now live in cities and 60% are projected to do so by 2030 (Pickett et al., 2011). Worldwide, this concentration has changed environments within cities and around them. Hence, cities pose many challenges like urban heat, food provisioning, and encroachment of natural areas (Pickett et al., 2011; Wong, Paddon, & Jimenez, 2013).
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These challenges have spurred urban citizens to develop a wide array of alternatives for understanding, using, and protecting resources available within cities as well near them
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(Morales et al., 2015). Urban agriculture, the practice of agricultural activities in the cities, occupies a special place among those alternatives because it provides multiple benefits,
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including food production, relaxation, and rescue of cultural heritage. Urban agriculture
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takes place in a variety of forms ranging from small home gardens to median and large agricultural plots in public parks or private properties; however, a crucial characteristic is
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that all or at least most of the agricultural urban manifestations are immersed in a cement matrix, hence that urban agriculture may become a hotspot for biodiversity (Lin, Philpott,
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& Jha, 2015; Philpott et al., 2014), specially of pollinators in temperate cities (Baldock et al., 2015), as it provides resources not available elsewhere. Nonetheless, gaining a satisfactory understanding of the ecology of urban agriculture and its management is still a huge challenge in many parts of the world. For
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example, urban growers ask how they might manage their agricultural home gardens in ways that insect floral visitors are attracted to their plots and thus increase their agricultural production. Indeed, insect floral visitors are an insufficiently studied key group that includes pollinators (bees, flies and butterflies) and predators (e. g. predatory wasps, flies
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and true bugs) that through their functions can influence the agricultural output in urban and rural agroecosystems (Lowenstein, Matteson, & Minor, 2015; Morales et al., 2018).
Moreover, these floral visitor species through their interactions with flowers form ecological networks. These networks have a full range of generalists that interact with specialists, thus ensuring the network´s stability over time. Furthermore, the topology of the
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networks as well as their indices exemplify the complexity of ecosystems and thus can be
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used to study community robustness, biodiversity conservation and management
(Bascompte & Jordano, 2007). In addition, evolutionary, ecological and management
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variables influence the topology of these networks. For example, within a given area, the
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floral visitors, plants, and the interactions among them may change spatially in response to habitat (Tylianakis, Tscharntke, & Lewis, 2007), and temporally in response to seasonal
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environmental conditions (Gotlieb, Hollender, & Mandelik, 2011). The potential for such variables to have cascading effects throughout an entire ecosystem is strong motivation for
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characterizing and understanding floral visitors and plants as part of a system (Gagic et al., 2012; Marrero, Torretta, & Medan, 2014; Tylianakis et al., 2007). In addition, networks, ecological functions, and biodiversity in the cities may be affected by landscape context (Holzschuh, Dudenhoffer, & Tscharntke, 2012; Philpott &
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Bichier, 2017; Tscharntke et al., 2012). Certainly, in urban landscapes the amount of urbanization (the cement matrix) around urban gardens is an important variable for floral visitors (Ahrne, Bengtsson, & Elmqvist, 2009; Fortel et al., 2014; Glaum, Simao, Vaidya, Fitch, & Iulinao, 2017) and their networks (Geslin, Gauzens, Thebault, & Dajoz, 2013) since it critically influences the movement of the organisms.
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Owing to accelerated urban sprawl and lack of planning many tropical countries from the Global South face multiple challenges (Inostroza, Baur, & Csaplovics, 2013) including biodiversity loss. Biodiversity loss due to urbanization and urban sprawl is quite threatening because the simplification risk that ecological networks already established may face (Burkle, Marlin, & Knight, 2013). Furthermore, considering that most of the biodiversity recorded in the world still is found in the tropical regions, addressing
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biodiversity status and ecological interaction networks in these regions is quite relevant for
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urban agriculture, and biodiversity conservation. In Mexico, a country from the Global
South, urban sprawl is accelerating throughout the country, including the traditionally less-
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populated southern states (Mendoza-Gonzalez, Martinez, Lithgow, Perez-Maqueo, &
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Simonin, 2012). The population of one of those states, Chiapas, has increased significantly during the last 30 years. The population of one of its cities, San Cristóbal de Las Casas,
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more than doubled between 1990 and 2010: from 75,000 to 158,000 (INEGI, 1990, 2013). During the same period, local people and immigrants developed a vigorous urban
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agriculture (Morales et al., 2015).
In this study we aim to elucidate the interactions that exist between urban agriculture (represented by agricultural home gardens located in the city) and natural areas
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in San Cristóbal de Las Casas (hereinafter San Cristóbal). More specifically, we ask (1) What is the contribution of natural areas and agricultural home gardens (hereinafter home gardens) to the accumulated species richness of floral visitors? (2) What is the influence of seasonality and habitat type upon the mean species richness and abundance of the floral visitors in natural areas and home gardens? (3) What is the influence of seasonality and habitat type upon the interaction networks established between flowers and their insect 5
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visitors? and (4) What is the influence of the surrounding landscape on species number and abundance of floral visitors in home gardens and natural areas?
Materials and methods Study area
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Our study area was the city of San Cristóbal and the natural areas that surround it (Fig. 1). The city, whose population is approximately 160,000, is located at 2120 m.a.s.l. in
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a small valley within an endorheic basin in the rugged altiplane region of Chiapas (Fig. 1)
(Figueroa-Jáuregui, Ibáñez-Castillo, Arteaga-Ramírez, Arellano-Monterrosas, & Vázquez-
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Peña, 2011). Its climate has two clearly-defined, markedly different seasons: a rainy season
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from June to October, and a dry season from November to May. During the latter, a threemonth “frost season” from November to the end of February is clearly identified. Although
(INEGI, 2003).
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the frosts are only occasional, the year’s lowest temperatures occur during this period
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The dry season is characterized by an absence of heavy rains (on average 30 mm of pluvial precipitation per month). In contrast, heavy rains (on average 200 mm of pluvial precipitation per month) are common during the rainy season (INEGI, 2003). The natural vegetation in and around San Cristóbal consists of pine-oak forest
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remnants, woodlots, wetlands, shrublands and prairies (most of them visited by sheep). We located nine home gardens and nine natural sites within the study area, for a total of 18 sites. Minimum distance between sites was 500 m. The nine home gardens that we sampled were distributed over the city (Fig. 1). These gardens had a combination of edible, ornamental and medicinal plants and did not receive any pesticide applications. All natural
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areas that we sampled were open prairies surrounded by natural vegetation. One of the natural sites was an open prairie surrounded by a mountainous wetland, while the other eight consisted of open prairies surrounded by pine oak forest or pine forest. We decided to sample prairies instead of forest fragments because there are virtually no flowers in the forest fragments and the wetland during the six-month dry season. In each of the 18 sites, we sampled floral visitors and plants on three occasions: during the frost season (February
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2015), dry season (April 2015), and rainy season (September-October 2015).
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Characterization of home gardens and natural areas
The nine home gardens that we studied ranged in size from 0.007 ha up to 0.3 ha,
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whereas the sizes of the nine natural sites ranged from approximately 0.07 ha to
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approximately 3 ha. During the frost season (February 2015), we characterized the sites at local scale by establishing a 20 m 20 m plot in each site (Marín et al., 2016). Within each
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plot we counted tree abundance and tree species, and estimated the percentage of ground cover. In each plot, we identified tree species by sight, when we could not identify a species
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positively in the field, we collected samples of it for later identification at the Herbarium of El Colegio de La Frontera Sur Unidad San Cristóbal de Las Casas, Chiapas (hereinafter “ECOSUR”). For ground cover estimation we defined, within each 20 m 20 m plot, four 1 m 1 m plots in which we measured the percentage of the ground that was occupied by
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bare soil, herbaceous plants, grass, leaf litter, and straw/mulch. In addition, we characterized the landscape within a 250 m radius of each site, using
a Geographic Information system (GIS) based on a 2011 digital image of San Cristóbal de Las Casas (IKONOS) and updated with Google Earth high resolution images from 2015. We identified the land cover types present in each circle based on classification from the
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Instituto Nacional de Geografía y Estadística (INEGI) and on fieldwork corroboration. Thus, we recorded seven land covers: pine oak forest and woodlots, shrublands, wetlands, prairies, agriculture (orchards, homegardens and large crop plots), barren ground (quarries and bare ground), and developed areas (buildings and streets). Then we used these seven land cover types identified in the 18 circles to form four categories: agricultural (home gardens, orchard and large crop plots), natural (pineoak forests and woodlots, wetlands,
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prairies), urban (developed areas), and barren ground (quarries and bare ground).
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Sampling of floral visitors
Because some of the home gardens we sampled were quite small, we did our
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sampling in plots that measured 2 m 2 m (Hennig & Ghazoul, 2012). We established two
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such plots in each of the 18 sites, we delineated plots where flowers were present (Ahrne et al., 2009). During the frost season (February 2015), dry season (April 2015), and rainy
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season (September-October 2015), we sampled all insects that visited each 2 m 2 m plot within a 40 minute interval, and recorded the plant species on which we observed or
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captured them. Thus, each of the 18 sites was sampled once per season, for a total of 80 minutes in each of the three seasons.
We collected most of the floral visitors, except Apis mellifera and those insects that we were able to identify by sight. The floral visitors, which we could not identify by sight,
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were taken to the laboratory, where we identified them to species or morphospecies level by consulting specialists and using selected literature. For beetles we consulted Morón, Ratcliffe, and Deloya (1997). For bees we followed Michener, McGlinley, and Danforth (1994). Certain genera, such as Lasioglossum and Hylaeus bees, were identified to morphospecies level. For butterflies we consulted Glassberg (2007), whereas for flies we
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followed Brown et al. (2009). Syrphids and bibionids were identified to species level, while most of the other families of flies were identified to morphospecies level, by matching females with their respective males. For wasps we consulted Fernández and Sharkey (2006). We deposited voucher specimens at ECOSUR’s bee collection (ECOAB) and entomological collection (ECO-SC-E).
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Having identified all of the floral visitors that came to the 2 m 2 m plots, we had a record of how many individuals of each species arrived during 80 minutes of observation
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for each site and each season. We also had a record of the number of interactions of each floral visitor species with each flowering plant species. Simultaneously with sampling of
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floral visitors, we recorded the plant species present in each 2 m 2 m plot in each season.
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We collected leaf samples of plants that we could not identify, for identification at
Data analysis
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ECOSUR’s Herbarium.
Contrasts between habitat characteristics of home gardens and natural areas
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In order to characterize home gardens and natural areas we tested differences for each variable (local or landscape scale) by using t-tests. When the variables were not normal, even after transformation, we used the Wilcoxon test. In order to determine the significance of between habitat and between seasons differences in plant species richness
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and species richness of flowering plants we used two way ANOVA and subsequent Tukey tests ( = 0.05); when plant data were not normally distributed, we normalized them using the square root transformation, then back transformed the results to obtain the mean values reported here (Gotelli & Ellison, 2012).
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Floral visitors richness, composition and fluxes To provide a proxy for floral visitor functions performed in both habitats (i.e., home gardens and natural areas) and acknowledging that one organism can play several roles in food webs (e.g. a ladybeetle consumes aphids but also eats pollen), we categorized each floral visitor species as pollinator, predator, or florivore, based upon literature reviews, quick visual inspection of insects under the stereoscope (for pollen presence) and field
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observations. Through field observations on the flowers we were able to identify predators
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(e. g. heteropterans eating flies), pollinators (insects with swift movements at flowers), and florivores (insects consuming floral parts). So even if we may have found pollen in
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pollinators and florivores, field observations allowed us to discern between them.
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In regard to floral visitor richness, we evaluated the accumulated floral visitor richness in both habitats by constructing rarefaction curves with EstimateS (Colwell, 2005). To
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analyze the change in species composition between habitats, we used Non-Metric Multidimensional Scaling (NMDS). To assess the significance of the difference in species
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composition between natural areas and home gardens we used Analysis of Similarities (ANOSIM), which provides an R-value. R-values close to 1 mean that habitats are greatly dissimilar in especies composition whereas values close to 0 mean that habitats are very similar (Hammer, Harper, & Ryan, 2001).
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To detect habitat and seasonal changes in floral visitors, we assigned each visitor to
one of three categories, according to the habitat or habitats in which it had been recorded during each season: home garden, natural area, or both. Then, we determined which floral visitors could be found in more than one season, and determined whether or not they remained in the same habitat across seasons. For visualizing habitat and seasonal changes
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in floral visitors (species fluxes) we used Venn Diagrams and RAWgraphs (DensityDesignResearchLab, 2019). Contrasts involving floral visitors To determine the significance of between habitat and between season differences in species richness of floral visitors per site, species richness of floral visitors taxa per site, and in abundance at both total floral visitors and by taxa, we used two way ANOVA and
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subsequent Tukey tests ( = 0.05) when data were normally distributed. When the data
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were not normally distributed, we normalized them using the square root transformation, then back transformed the results to obtain the mean values reported here (Gotelli &
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Ellison, 2012). When data did not meet the normality assumptions even after
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transformation, we used Wilcoxon tests for each season. Interaction networks across habitats and seasons
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We constructed bipartite networks (adjacency matrices) for each habitat and season, using the recorded interactions between floral visitor species and plant species. Thus for each
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season we pooled the flower insect interactions that took place in each of the nine natural areas and constructed one network for each season. We did the same for the home gardens, and obtained six interaction networks. The weight of the interactions in those networks corresponded to the number of times the interaction was observed. We looked for
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differences in the interaction networks across habitats and seasons by comparing uncorrelated indices that describe network structure [number of floral visitor and species, number of plant species, number of links, generality of floral visitors, and H2] (Blüthgen, Menzel, & Blüthgen, 2006). We carried out all analyses, plus the associated adjacency matrices, using R software packages car, vegan and bipartite (R Core Team, 2016). For
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visualizing the adjacency matrices, we used the package matplotlib with Python software (Hunter, 2007). Landscape context To identify how landscape context might affect floral visitor species richness and abundance across seasons, we first explored the data by plotting floral visitor species number against the four categories of land cover types: natural, agricultural, barren ground,
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and urban (Appendix A: Fig.1). We did the same to explore the relationship between floral
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visitor abundance and landscape context (Appendix A: Fig. 2). Simultaneously, we evaluated correlations between urban cover category and the other three variables
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(Appendix A: Table 1). Upon these explorations, we selected “urban cover category” as
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explanatory variable in individual linear models for each season. Because some scatter plots (Appendix A: Figs. 1 and 2) suggested a quadratic relationship between floral species
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richness and urban cover, we raised urban cover variable to the square and tested it as explanatory variable. When necessary (because of non normality of distributions), we
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normalized the response variables as described above.
Results
Characteristics of home garden and natural area sites Home gardens had higher percentages of bare soil and herbaceous cover than
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natural areas, but natural areas had a higher percentage of ground covered by leaf litter. Other variables, such as tree species richness, tree abundance, and ground cover by rocks and mulch did not differ significantly between the two habitats (Table 1). At the landscape context scale, we found that both natural cover and urban cover showed a wide range of values, whereas agricultural cover and barren ground showed a
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more restricted range and similar values (Table 1). We found that the home gardens and natural areas differed strongly in their amounts of agricultural, natural and urban land cover types (Table 1). Indeed, the average urban cover of home garden sites was 52.7%, versus 12.3% in natural-area sites, whereas agricultural cover of home garden sites was 6.7%, versus 3% in natural area sites.
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Plant species richness
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Mean plant species richness differed significantly between home gardens (16.37 ± 1.6) and natural areas (8.40 ± 0.98) (F1, 48 = 33.27, p < 0.0001). In addition, we found a
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season effect (F2, 48 = 6.03, p = 0.005), and a clear difference in plant species richness
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between the frost and the rainy seasons (Fig. 2A, Appendix A: Tables 2 and 3). Likewise, species richness of flowering plants differed significantly between home gardens (8.09 ±
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0.63) and natural areas (3.41 ± 0.46) (F1, 48 = 49.94, p < 0.001) and increased across seasons (F2, 48 = 7.19, p = 0.002; Fig. 2B, Appendix A: Tables 2 and 3). In addition, an
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interaction effect between habitat type and season was found, as the species richness values for flowering plants in both habitats converged in the rainy season (F2, 48 = 5.02, p = 0.01).
Floral visitors
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A total of 1301 floral visitor individuals representing 210 species or morphospecies
were recorded from a total of 99 plant species at the 18 sampling sites. Among the floral visitors, we found 74 species of flies (35% of the total species), 57 species of bees (27%), 33 of butterflies (16%), 25 species of wasps (12%), 14 of beetles (6.6%), and seven of bugs (3%). These 210 species were distributed in three guilds: pollinators (164 species, 78%), predators (38 species, 18%), and florivores (8 species, 4%). These floral insects visited 32 13
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plant families distributed in both habitat types with Asteraceae (36% of the visits), Brassicae (18% of the visits) and Fabaceae (9% of the visits) being the most visited.
Accumulated species richness of floral visitors Of the 210 species and morphospecies of floral visitors, 148 were recorded in natural areas, and 132 in home gardens (Fig. 3A). The rarefaction curves do not become
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fully asymptotic, but by the 150 individual mark clearly more species are accumulated in
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the natural areas than in the home gardens. We found a strong difference between species composition of floral visitors in natural areas versus home gardens (Fig. 3B, R value =
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0.59).
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Analysis of the recorded floral visitor species between habitats and seasons revealed a large number of singletons (species that just appeared once) and also suggested that the
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flux of species between specific habitats and seasons was restricted. Of the 210 species of floral visitors, 78 species (37%) were restricted to the natural areas, whereas 62 species
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(29.5%) were restricted to home gardens and 70 species (33%) were presented in both habitats (Fig. 4A). Furthermore of the 210 species of floral visitors, 21 species (10%) appeared in all three seasons (Fig. 4B), while 139 species (66%) appeared in only one season. The number of floral visitor species varied seasonally (Appendix A: Fig. 3). Of the
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78 species present during the frost season, 38 were recorded in the dry season. Of the 106 species recorded during the dry season, 43 were recorded in the rainy season, and of the 118 species recorded during the rainy season, 32 had been recorded in the frost season. Mean species richness of floral visitors We found no differences (F1, 48 =0.34, p= 0.85) between the floral visitor species richness in home gardens and in natural areas. The floral visitor species richness (mean ± SE) in home 14
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gardens was 10.07 ± 1.099 versus 10.31 ± 1.011 in natural areas. However, we found a significant effect of season (F2, 48 = 7.82, p = 0.001, Appendix A: Table 4), with mean species richness of floral visitors tending to increase from the frost to the rainy season (Fig. 5A, Appendix A: Tables 4 and 5). When examining the mean species richness for taxa we found that bees and butterflies showed strong, opposed patterns (Fig. 5B and C). Bee species richness did not
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show a habitat effect across all seasons (F1, 48 = 2.33, p = 0.13): bee species richness in
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home gardens was 4.04 ± 0.45, versus 3.28 ± 0.53 in natural areas. However, the seasonal influence upon bee species richness was clear (F2,48 = 23.65, p < 0.0001). The interaction
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between habitat and season was also significant, with home gardens showing higher bee
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species richness during the frost season (F2, 48 = 4.002, p = 0.025, Fig. 5B, Appendix A: Table 4). In contrast, species richness of butterflies across all seasons was greater in natural
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Appendix A: Table 6).
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areas (2.22 ± 0.38) than in home gardens (0.74 ± 0.18) (W =526, p = 0.004, Fig. 5C,
Floral visitor abundance
We found an effect of habitat and season upon the abundances of floral visitors, plus an interaction between habitat and season. Floral visitor abundance (mean ± SE) for
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home gardens was (26.60 ± 2.84), versus (18.078 ± 2.00) for natural areas (F1, 48 = 9.18, p = 0.004), with floral visitor abundance increasing from the frost to the rainy season (F2, 48 = 12.61, p < 0.0001, Fig. 5D, Appendix A: Tables 4 and 5). When we examined abundance by taxonomic group, we found a general trend of floral visitor abundance increasing from the frost season to the rainy season, with some groups showing a marked preference for one or the other of the two habitats (Appendix A: 15
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Tables 4 and 5). Bee abundance was influenced by habitat and season. Overall bee abundance was greater in home gardens (13.09 ± 2.11) than in natural areas (7.02 ± 1.46) (F1, 48 = 14.22, p = 0.0004). It tended to increase as the seasons progressed from frost to rainy (F2, 48 = 39.16, p < 0.001, Fig. 5E). Although the habitat effect disappeared after taking out the Apis mellifera abundance, the season effect remained, with bee abundance again increasing from the frost to the rainy season (F2, 48 = 26.01, p < 0.0001). For fly
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abundance, we found an interaction effect of habitat and season. Fly abundance was 5.08 ±
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1.086 in home gardens, and 2.61 ± 0.68 in natural areas (F1, 48 = 4.75, p = 0.003). A clear season effect was found, with fly abundance being higher during the dry season (F2, 48 =
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7.14, p = 0.002). Butterfly abundance was significantly higher in natural areas (3.37 ± 0.69)
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than in home gardens (1.04 ± 0.28, W = 512, p < 0.0001). This pattern was unmistakable throughout the three seasons, and was especially clear during the frost and rainy seasons
Network analysis
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(Fig. 5F, Appendix A: Table 6).
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The plants and floral visitors that we found in home gardens and natural areas formed a complex network of 210 floral visitor species and 99 flowering plant species, displaying 609 interactions and 1301 observations. In home gardens, the overall floral visitor network across the three seasons comprised 62 plant species and 132 floral visitor
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species (39 bee species, 10 wasp species, 5 bug species, 7 beetle species, 12 butterfly species, and 59 fly species), with 314 interactions and 774 observations. In natural areas, the overall network was arranged by 45 plant species and 149 floral visitor species (44 bee species, 20 wasp species, 3 bug species, 11 beetle species, 30 butterfly species, and 41 fly species), with 305 interactions and 527 observations. Of the 609 interactions, 421 were observed only once. We found that interactions with Apis mellifera, the honey bee, 16
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predominated: this insect interacted with 52 plant species, and accounted for 34% of the observations. The network formed across seasons was highly dynamic. Only 1.06% of the interactions occurred in both of the habitats (rather than in just one of them), even though 33% of the insects and 8% of plants were found in both habitats. The interactions also changed between seasons. Only 5.66% of interactions were observed in more than one
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season, in contrast with the 34% of insects and 27% of plants that were observed in more
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than one season (Fig. 6). Network indices pointed to a higher degree of specialization and vulnerability in natural areas than in home gardens (Table 2, Fig. 6). Flower visitor
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generality (the average number of plant species per floral visitor species) was greater in
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home gardens. Furthermore, the values of the H2 index, an indicator of the specialization degree at the network level that takes into account the different abundances of plants and
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pollinators (Blüthgen et al., 2006) were higher in natural areas during the frost season
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(H2=0.51), indicating that during this season natural areas had more specialists.
Landscape context
We found that apart from season, landscape context influenced floral visitor species number. In particular, the percentage of urban cover raised to the square influenced the
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square root of the total number of floral visitor species number in a quadratic way (pvalue=0.024, Table 3); whereas urban cover did not influence the abundance of the floral visitors in any season (p value ≥0.4).
Discussion
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Our work sheds light on the important effects of habitat type and seasonality upon species richness, species abundance, and network structure for floral visitors and their flowering plants in tropical regions. At the same time, it has implications for urban agriculture, landscape management and biodiversity conservation. Home gardens and natural areas differed in their characteristics at both the local and landscape levels. At the local level the most conspicuous differences were in ground cover,
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with home gardens having a larger fraction of herbaceous cover, and natural areas having a
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greater fraction of leaf litter cover. In contrast, home gardens and natural areas did not differ in the average number of tree species and tree abundance. Differences in ground
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cover may be explained by (1) the regular watering of home gardens, which favors and
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enhances herbaceous and floral cover (Gotlieb et al. 2011) and (2) the potentially greater provision of leaf litter by trees around natural areas. The lack of differences in tree species
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and abundance between natural areas and home gardens seems to derive from the fact that natural areas were not strictly forested areas, but prairies surrounded by forests and
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wetlands, and that most gardens had a variety of trees and shrubs for multiple purposes (Morales et al. 2015). Differences at the landscape context level seem to reflect contrast in land use between natural areas and more anthropogenic areas (Forman 1995). We found that natural areas harbored higher accumulated species richness of floral
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visitors than home gardens; however, more sampling is required to better assess the floral visitor species number that compose this community of beneficial insects in each habitat. Nonetheless, the inter habitat differences found in species composition as well as the suggested species fluxes (Fig. 4 and Appendix A: Fig. 3) highlight the need to view natural areas and home gardens as complementary habitats that together hold a floral visitor community composed of at least 210 species. Habitat complementarity is a key element for 18
Marín et al.
Floral visitors in a neotropical landscape
achieving biodiversity conservation and agroecological management (Colwell & Coddington, 1994; Mandelik, Winfree, Neeson, & Kremen, 2012; Marín et al., 2016; Tscharntke et al., 2012).
Furthermore, floral visitor species richness tended to be affected less by habitat type than by season, thus highlighting the importance of seasonality for floral visitors in a
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neotropical urban landscape. Nonetheless, the importance of habitat for some taxa was
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quite real. By examining the species densities of the main taxonomic groups of floral
visitors, we found that butterflies and bees were strongly influenced by both habitat and
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season. Bee species richness was greater in home gardens during the frost season, thus
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suggesting that bees were very good at exploiting the more abundant urban floral resources during the frost season (see Hall et al., 2016). On the contrary, species densities of
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butterflies tended to be higher in natural areas throughout the year, suggesting that butterflies depend strongly upon natural habitats. This dependence might be due to host
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plant fidelity, a phenomenon widely recognized in butterflies (DeVries, 1987). Moreover, we found that the influence of habitat and season on abundance of visitors showed a more striking pattern, with more individuals being recorded in home gardens than in natural areas over the frost and dry seasons. Overall, these results about floral visitor species richness
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and abundance highlight home gardens as hotspots in this neotropical city just as recently has been found at larger scale in temperate regions (Baldock et al., 2019; Hall et al., 2016). Home gardens may act as biodiversity hotspots by providing plenty floral resources to floral visitors (see sEbeling et al. 2018). Indeed, in this study we found that across seasons home gardens tended to show higher species richness of plants and flowering plants than
19
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Floral visitors in a neotropical landscape
natural areas; thus suggesting that the influence of habitat type and seasonality cascades through plant diversity to floral visitors. Network structure changed qualitatively across habitats and seasons, indicating that interactions between plant species and their floral visitors are highly dynamic and dependent upon environmental and habitat factors (Fig. 6) (Bascompte & Jordano 2007). Furthermore, the basic network indices (Table 2) show that overall networks in natural
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areas were more specialized and potentially less robust, whereas home gardens networks
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showed the opposite pattern (Marrero et al., 2014). Thus we posit that the networks in the
natural areas studied here are more vulnerable to habitat loss and climate change (Burkle et
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al., 2013; Geslin et al., 2013; Gotlieb et al., 2011; Tylianakis et al., 2007).
In this study, we explored in a basic way the influence that the immediate landscape
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context surrounding each of the 18 sites had on the total number of floral visitor species as well on their abundance. While, we did not find an influence of urban cover on the
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abundance of floral visitors in any season it is important to highlight that we found that increasing urbanization cover affected the square root of the species number of floral visitors in a quadratic way (Table 3). The quadratic behavior of species number in relation to urban cover is a pattern that has been previously reported (Fortel et al., 2014) and
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therefore, is noteworthy to highlight that adding more green in the context of a cement matrix requires a variety of sources (medium-sized agricultural plots, home gardens, agroforests, vacant lands, woodlots, and parks) (Gardiner, Burkman, & Prajzner, 2013; Glaum et al., 2017) that offer habitat and other resources to the floral visitors and thus potentially enhance their functions (Lin et al., 2015; Holzschuh et al., 2012). Overall, our
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Floral visitors in a neotropical landscape
results emphasize the need to establish conservation and management plans for San Cristóbal and its natural areas and home gardens.
Conclusions At local and landscape scale, natural areas and home gardens are both required for maintaining floral visitor diversity as well as ecological interaction networks in this
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neotropical city. Patterns in floral visitor species richness, abundance and their interaction networks with plants are greatly influenced by seasonality. Home gardens function as a
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refuge for floral visitors. Urban cover influenced floral visitor species number. Thus, our work points out to the need of considering agricultural home gardens and natural areas
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habitat types for maintaining biodiversity, its functions and network structure in neotropical
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urban landscapes. Otherwise, San Cristóbal and other cities face the possible simplification
provide. Conflict of interest
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of their biodiversity, ecological networks, and consequent loss of the functions they
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We declare we have no conflict of interest
Acknowledgments
We would like to thank Jorge Mérida, Benigno Gómez, Dr. Brailovsky and Miguel
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Martínez-Icó for identifying insects and plants. Initial talks with Rémy Vandame were key inputs for this research. Mariana Robles Calderón, Olivia Bracconier, Nathan Einbinder, Alejandro Roblero, Ruve Culej, and Amparo Hernández helped us with fieldwork and logistics and Jim Smith did an editorial review of a previous draft. We are greatly grateful to the two anonymous reviewers and to the editors that provided insightful comments on
21
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previous versions of this paper. We received funding through a CONACYT postdoctoral fellowship granted to Linda Marín, as well through funds from the Urban Agroecology Program (El Colegio de la Frontera Sur) granted to Helda Morales. Appendix A. Supplementary material associated with this article can be found, in the online
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version, at XXX.
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Tylianakis, J. M., Tscharntke, T., & Lewis, O. T. (2007). Habitat modification alters the structure of tropical host-parasitoid food webs. Nature, 445(7124), 202-205. doi: 10.1038/nature05429 Wong, K. V., Paddon, A., & Jimenez, A. (2013). Review of world urban heat islands: Many linked to increased mortality. Journal of Energy Resources TechnologyTransactions of the Asme, 135(2). doi: 10.1115/1.4023176
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Figure legends’
Fig. 1. Study area in San Cristóbal and surroundings, showing locations of the nine urban gardens sites (blue symbols) and nine natural area sites (green symbols) studied in the work
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reported here.
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Fig 2. Mean species richness for (A) all plant species and (B) flowering species in natural
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areas (green circles) and home gardens (blue circles) in San Cristóbal.
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Fig. 3. Species rarefaction curves (A) and NMDS plot for species composition (B) in
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natural areas (green circles) and home gardens (blue circles) in San Cristóbal. These figures
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were elaborated with the species records for the three seasons.
Fig. 4. Venn diagrams for floral visitor species shared between habitats (A) and seasons (B).
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Figure 5. Mean species richness and abundance of floral visitors in natural areas (green
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circles) and home gardens (blue circles) in San Cristóbal. Key to symbols: (A) mean total floral visitor species richness; (B) bee species richness; (C) butterfly species richness; (D)
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total floral visitors abundance; (E) bee abundance; (F) butterfly abundance.
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Figure 6. Adjacency plots for floral visitor species and flowering plant species in home gardens and natural areas across frost, dry, and rainy seasons. In each adjacency plot, the pink horizontal histogram corresponds to floral visitor abundance, whereas the green vertical histogram corresponds to plant abundance. The intensity of the interactions
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between floral visitors and plants is indicated by the saturation of the color of the squares found between both histograms. White squares = 0 interactions, brown squares = the highest value of interaction intensity for that plot.
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Table 1. Local and landscape scale habitat characterizations for home gardens and natural areas in San Cristóbal. Variable
Range
Home Gardens
Natural Areas
Test
pvalue
(t) or (W) Local scale Tree richness Tree abundance
6.11 ± 2.08 20.00 ± 5.56
6.44 ± 0.88 28.77 ± 8.47
0 - 30
30.03 ± 6.21
8.58 ± 3.83
Percent of herbaceous plants 0 - 58 Percent of leaf litter 0 - 69
33.81 ± 5.30 5.88 ± 4.00
17.39 ± 4.90 26.35 ± 7.77
Percent of grass Percent of mulch-straw Rocks
19.83 ± 7.07 4.61 ± 1.21 2.25 ± 1.50
37.19 ± 8.13 6.89 ± 4.89 2.64 ± 1.20
Percent of urban cover
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(t)
0.89 0.57 0.01
(t) 0.037 0.017 (t) 0.127 (W) 0.36 0.48
0 - 39.6
6.74 ± 4.25
2.91 ± 2.91
8. 00 (W) 0.003
0 - 39.3
4.93 ± 1.47 35.63 ± 7.18
6.62 ± 4.13 78.15 ± 4.93
35.00 (W) 0.66
52.70 ± 10.62
12.32 ± 3.49
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Landscape scale Percent of agricultural cover Percent of barren ground cover Percent of natural cover
0 - 83 0 - 45 0 - 14
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Percent of bare soil
0.15 47.50 (W) 11.00 (W) -2.27 67.50 (W) 1.61 30.00 48.50 (W)
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0 - 18 0 - 92
6.5 - 97.3 2.7 - 93.3
4.88
<0.00 1 9. 00 (W) 0.004
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t= t of Student, W= Wilcoxon test
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(t)
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Table 2. Network indices for networks found in home gardens and natural areas in San Cristóbal. Entries are values of the respective indices.
Frost Dry Rainy Season Season Season Home Natural Home Natural Home Natural Home Natural Gardens Areas Gardens Areas Gardens Areas Gardens Areas 67
68
75
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67
24 117 232 1.98 6.1
11 94 159 1.69 2.76
40 143 335 2.34 0.09
32 160 276 1.73 6.28
8.25
20.18
6.61
7.94
4.73 0.42
2.26 0.42
5.54 0.47
5.19 0.37
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Number of floral visitor 132 149 42 49 species Number of plant species 62 45 24 10 Number of interactions 314 305 84 62 Number of observations 774 527 207 92 Mean interaction weight 2.46 1.73 2.46 1.48 Mean number of floral 15.93 7.72 8.63 1.99 visitor links Mean number of plant 12.01 15.2 6.09 14.17 links Generality floral visitors 9.73 6.03 6.09 1.66 H2 0.37 0.32 0.38 0.51 Overall= The network formed by including the three seasons.
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Table 3. Influence of urban cover on floral visitor species number during the rainy season
Square root of floral visitor species ~ season + (urban cover)2 Estimate Standard Error 0.185 0.242 0.242 0.000
18.871 -2.850 1.263 -2.283
p-value
<0.001 0.006 0.212 0.0240
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3.484 0.690 0.306 -0.001
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Intercept Season (Frost) Season (Rainy) (Urban cover)^2
t-value
p-value
Intercept Season (Frost) Season (Rainy) (Urban cover)^2
<0.001 0.120 0.004 -0.390
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0.305 0.400 0.400 0.000
15.160 -1.570 3.000 -0.850
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4.620 0.628 1.197 0.000
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Square root of floral visitors abundance ~ season + (urban cover)2 Estimate Standard t-value Error
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PII:
S1439-1791(19)30282-8
DOI:
https://doi.org/10.1016/j.baae.2019.10.003
Reference:
BAAE 51211
To appear in:
Basic and Applied Ecology
Received Date:
23 February 2019
Accepted Date:
9 October 2019
Please cite this article as: { doi: https://doi.org/ This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.
Marín et al.
Floral visitors in a neotropical landscape
Title: Floral visitors in urban gardens and natural areas: diversity and interaction networks in a neotropical urban landscape.
Marín, Lindaa*, Mariana Esther Martínez-Sánchezb,c, Philippe Sagota, Darío Navarreted and
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Helda Moralesa
Grupo de Agroecología, El Colegio de la Frontera Sur, San Cristóbal de Las Casas,
Departamento de Ecología Funcional, Instituto de Ecología, Universidad Nacional
Autónoma de México, Ciudad de México, Mexico
Consejo Nacional de Ciencia y Tecnología, Ciudad de México, Mexico Laboratorio de Análisis de Información Geográfica y Estadística, El Colegio de la
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Chiapas, Mexico.
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Frontera Sur, San Cristóbal de Las Casas, Chiapas, Mexico.
*Corresponding author. Tel:(52) 1 222 599 5938, email: [email protected] Present address: Universidades Benito Juárez García, Tlaxcala, Mexico
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Highlights
Floral visitor richness and abundance varied with season and management Seasonality had a strong effect on the floral visitor community Urban gardens functioned as an oasis for the floral visitor community Species composition between urban gardens and natural areas was complementary Interaction networks between flowers and their visitors were dynamic and complex across habitats
Abstract 1
Marín et al.
Floral visitors in a neotropical landscape
Because cities concentrate 50% of the world’s population, and are experiencing a reemergence of urban agriculture, we investigated the influences of urban agriculture and surrounding natural areas on floral visitors (bees, wasps, butterflies and flies) and plant species in San Cristóbal de Las Casas, Mexico. Throughout the frost, dry and rainy seasons of 2015, we sampled floral visitors in nine urban gardens and nine natural areas. We found 210 floral visitor species: 78%
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pollinators, 18% predators, and 4% florivores. Rarefaction curves showed that natural areas
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harbor significantly more floral visitor species (148) than home gardens (132). However,
the differences in species composition between habitats and seasons highlight the need to
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view natural areas and home gardens as complementary habitats with which floral visitors
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interact in varying ways, during successive seasons, to meet different needs. Furthermore, mean species richness of floral visitors was influenced mainly by seasonality, and increased
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as seasons progressed from the dry, frost season to the rainy season. Nonetheless, some taxa were influenced by both season and habitat type. Floral visitor abundance was
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influenced by both habitat type and season, with home gardens showing higher abundance across seasons. Moreover, interaction networks for each season were more asymmetric in natural areas than in home gardens. Urban cover in the surrounding landscape influenced in a quadratic way the species number of floral visitors, but not their abundance. Thus, our
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results are evidence that natural areas surrounding cities and urban agriculture contribute to floral visitor communities and their networks.
Keywords: Bees, urban agriculture, pollinators, species fluxes
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Floral visitors in a neotropical landscape
Introduction Half of the world’s people now live in cities and 60% are projected to do so by 2030 (Pickett et al., 2011). Worldwide, this concentration has changed environments within cities and around them. Hence, cities pose many challenges like urban heat, food provisioning, and encroachment of natural areas (Pickett et al., 2011; Wong, Paddon, & Jimenez, 2013).
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These challenges have spurred urban citizens to develop a wide array of alternatives for understanding, using, and protecting resources available within cities as well near them
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(Morales et al., 2015). Urban agriculture, the practice of agricultural activities in the cities, occupies a special place among those alternatives because it provides multiple benefits,
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including food production, relaxation, and rescue of cultural heritage. Urban agriculture
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takes place in a variety of forms ranging from small home gardens to median and large agricultural plots in public parks or private properties; however, a crucial characteristic is
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that all or at least most of the agricultural urban manifestations are immersed in a cement matrix, hence that urban agriculture may become a hotspot for biodiversity (Lin, Philpott,
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& Jha, 2015; Philpott et al., 2014), specially of pollinators in temperate cities (Baldock et al., 2015), as it provides resources not available elsewhere. Nonetheless, gaining a satisfactory understanding of the ecology of urban agriculture and its management is still a huge challenge in many parts of the world. For
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example, urban growers ask how they might manage their agricultural home gardens in ways that insect floral visitors are attracted to their plots and thus increase their agricultural production. Indeed, insect floral visitors are an insufficiently studied key group that includes pollinators (bees, flies and butterflies) and predators (e. g. predatory wasps, flies
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and true bugs) that through their functions can influence the agricultural output in urban and rural agroecosystems (Lowenstein, Matteson, & Minor, 2015; Morales et al., 2018).
Moreover, these floral visitor species through their interactions with flowers form ecological networks. These networks have a full range of generalists that interact with specialists, thus ensuring the network´s stability over time. Furthermore, the topology of the
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networks as well as their indices exemplify the complexity of ecosystems and thus can be
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used to study community robustness, biodiversity conservation and management
(Bascompte & Jordano, 2007). In addition, evolutionary, ecological and management
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variables influence the topology of these networks. For example, within a given area, the
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floral visitors, plants, and the interactions among them may change spatially in response to habitat (Tylianakis, Tscharntke, & Lewis, 2007), and temporally in response to seasonal
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environmental conditions (Gotlieb, Hollender, & Mandelik, 2011). The potential for such variables to have cascading effects throughout an entire ecosystem is strong motivation for
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characterizing and understanding floral visitors and plants as part of a system (Gagic et al., 2012; Marrero, Torretta, & Medan, 2014; Tylianakis et al., 2007). In addition, networks, ecological functions, and biodiversity in the cities may be affected by landscape context (Holzschuh, Dudenhoffer, & Tscharntke, 2012; Philpott &
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Bichier, 2017; Tscharntke et al., 2012). Certainly, in urban landscapes the amount of urbanization (the cement matrix) around urban gardens is an important variable for floral visitors (Ahrne, Bengtsson, & Elmqvist, 2009; Fortel et al., 2014; Glaum, Simao, Vaidya, Fitch, & Iulinao, 2017) and their networks (Geslin, Gauzens, Thebault, & Dajoz, 2013) since it critically influences the movement of the organisms.
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Floral visitors in a neotropical landscape
Owing to accelerated urban sprawl and lack of planning many tropical countries from the Global South face multiple challenges (Inostroza, Baur, & Csaplovics, 2013) including biodiversity loss. Biodiversity loss due to urbanization and urban sprawl is quite threatening because the simplification risk that ecological networks already established may face (Burkle, Marlin, & Knight, 2013). Furthermore, considering that most of the biodiversity recorded in the world still is found in the tropical regions, addressing
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biodiversity status and ecological interaction networks in these regions is quite relevant for
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urban agriculture, and biodiversity conservation. In Mexico, a country from the Global
South, urban sprawl is accelerating throughout the country, including the traditionally less-
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populated southern states (Mendoza-Gonzalez, Martinez, Lithgow, Perez-Maqueo, &
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Simonin, 2012). The population of one of those states, Chiapas, has increased significantly during the last 30 years. The population of one of its cities, San Cristóbal de Las Casas,
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more than doubled between 1990 and 2010: from 75,000 to 158,000 (INEGI, 1990, 2013). During the same period, local people and immigrants developed a vigorous urban
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agriculture (Morales et al., 2015).
In this study we aim to elucidate the interactions that exist between urban agriculture (represented by agricultural home gardens located in the city) and natural areas
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in San Cristóbal de Las Casas (hereinafter San Cristóbal). More specifically, we ask (1) What is the contribution of natural areas and agricultural home gardens (hereinafter home gardens) to the accumulated species richness of floral visitors? (2) What is the influence of seasonality and habitat type upon the mean species richness and abundance of the floral visitors in natural areas and home gardens? (3) What is the influence of seasonality and habitat type upon the interaction networks established between flowers and their insect 5
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Floral visitors in a neotropical landscape
visitors? and (4) What is the influence of the surrounding landscape on species number and abundance of floral visitors in home gardens and natural areas?
Materials and methods Study area
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Our study area was the city of San Cristóbal and the natural areas that surround it (Fig. 1). The city, whose population is approximately 160,000, is located at 2120 m.a.s.l. in
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a small valley within an endorheic basin in the rugged altiplane region of Chiapas (Fig. 1)
(Figueroa-Jáuregui, Ibáñez-Castillo, Arteaga-Ramírez, Arellano-Monterrosas, & Vázquez-
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Peña, 2011). Its climate has two clearly-defined, markedly different seasons: a rainy season
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from June to October, and a dry season from November to May. During the latter, a threemonth “frost season” from November to the end of February is clearly identified. Although
(INEGI, 2003).
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the frosts are only occasional, the year’s lowest temperatures occur during this period
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The dry season is characterized by an absence of heavy rains (on average 30 mm of pluvial precipitation per month). In contrast, heavy rains (on average 200 mm of pluvial precipitation per month) are common during the rainy season (INEGI, 2003). The natural vegetation in and around San Cristóbal consists of pine-oak forest
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remnants, woodlots, wetlands, shrublands and prairies (most of them visited by sheep). We located nine home gardens and nine natural sites within the study area, for a total of 18 sites. Minimum distance between sites was 500 m. The nine home gardens that we sampled were distributed over the city (Fig. 1). These gardens had a combination of edible, ornamental and medicinal plants and did not receive any pesticide applications. All natural
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areas that we sampled were open prairies surrounded by natural vegetation. One of the natural sites was an open prairie surrounded by a mountainous wetland, while the other eight consisted of open prairies surrounded by pine oak forest or pine forest. We decided to sample prairies instead of forest fragments because there are virtually no flowers in the forest fragments and the wetland during the six-month dry season. In each of the 18 sites, we sampled floral visitors and plants on three occasions: during the frost season (February
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2015), dry season (April 2015), and rainy season (September-October 2015).
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Characterization of home gardens and natural areas
The nine home gardens that we studied ranged in size from 0.007 ha up to 0.3 ha,
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whereas the sizes of the nine natural sites ranged from approximately 0.07 ha to
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approximately 3 ha. During the frost season (February 2015), we characterized the sites at local scale by establishing a 20 m 20 m plot in each site (Marín et al., 2016). Within each
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plot we counted tree abundance and tree species, and estimated the percentage of ground cover. In each plot, we identified tree species by sight, when we could not identify a species
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positively in the field, we collected samples of it for later identification at the Herbarium of El Colegio de La Frontera Sur Unidad San Cristóbal de Las Casas, Chiapas (hereinafter “ECOSUR”). For ground cover estimation we defined, within each 20 m 20 m plot, four 1 m 1 m plots in which we measured the percentage of the ground that was occupied by
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bare soil, herbaceous plants, grass, leaf litter, and straw/mulch. In addition, we characterized the landscape within a 250 m radius of each site, using
a Geographic Information system (GIS) based on a 2011 digital image of San Cristóbal de Las Casas (IKONOS) and updated with Google Earth high resolution images from 2015. We identified the land cover types present in each circle based on classification from the
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Instituto Nacional de Geografía y Estadística (INEGI) and on fieldwork corroboration. Thus, we recorded seven land covers: pine oak forest and woodlots, shrublands, wetlands, prairies, agriculture (orchards, homegardens and large crop plots), barren ground (quarries and bare ground), and developed areas (buildings and streets). Then we used these seven land cover types identified in the 18 circles to form four categories: agricultural (home gardens, orchard and large crop plots), natural (pineoak forests and woodlots, wetlands,
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prairies), urban (developed areas), and barren ground (quarries and bare ground).
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Sampling of floral visitors
Because some of the home gardens we sampled were quite small, we did our
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sampling in plots that measured 2 m 2 m (Hennig & Ghazoul, 2012). We established two
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such plots in each of the 18 sites, we delineated plots where flowers were present (Ahrne et al., 2009). During the frost season (February 2015), dry season (April 2015), and rainy
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season (September-October 2015), we sampled all insects that visited each 2 m 2 m plot within a 40 minute interval, and recorded the plant species on which we observed or
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captured them. Thus, each of the 18 sites was sampled once per season, for a total of 80 minutes in each of the three seasons.
We collected most of the floral visitors, except Apis mellifera and those insects that we were able to identify by sight. The floral visitors, which we could not identify by sight,
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were taken to the laboratory, where we identified them to species or morphospecies level by consulting specialists and using selected literature. For beetles we consulted Morón, Ratcliffe, and Deloya (1997). For bees we followed Michener, McGlinley, and Danforth (1994). Certain genera, such as Lasioglossum and Hylaeus bees, were identified to morphospecies level. For butterflies we consulted Glassberg (2007), whereas for flies we
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followed Brown et al. (2009). Syrphids and bibionids were identified to species level, while most of the other families of flies were identified to morphospecies level, by matching females with their respective males. For wasps we consulted Fernández and Sharkey (2006). We deposited voucher specimens at ECOSUR’s bee collection (ECOAB) and entomological collection (ECO-SC-E).
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Having identified all of the floral visitors that came to the 2 m 2 m plots, we had a record of how many individuals of each species arrived during 80 minutes of observation
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for each site and each season. We also had a record of the number of interactions of each floral visitor species with each flowering plant species. Simultaneously with sampling of
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floral visitors, we recorded the plant species present in each 2 m 2 m plot in each season.
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We collected leaf samples of plants that we could not identify, for identification at
Data analysis
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ECOSUR’s Herbarium.
Contrasts between habitat characteristics of home gardens and natural areas
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In order to characterize home gardens and natural areas we tested differences for each variable (local or landscape scale) by using t-tests. When the variables were not normal, even after transformation, we used the Wilcoxon test. In order to determine the significance of between habitat and between seasons differences in plant species richness
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and species richness of flowering plants we used two way ANOVA and subsequent Tukey tests ( = 0.05); when plant data were not normally distributed, we normalized them using the square root transformation, then back transformed the results to obtain the mean values reported here (Gotelli & Ellison, 2012).
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Floral visitors richness, composition and fluxes To provide a proxy for floral visitor functions performed in both habitats (i.e., home gardens and natural areas) and acknowledging that one organism can play several roles in food webs (e.g. a ladybeetle consumes aphids but also eats pollen), we categorized each floral visitor species as pollinator, predator, or florivore, based upon literature reviews, quick visual inspection of insects under the stereoscope (for pollen presence) and field
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observations. Through field observations on the flowers we were able to identify predators
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(e. g. heteropterans eating flies), pollinators (insects with swift movements at flowers), and florivores (insects consuming floral parts). So even if we may have found pollen in
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pollinators and florivores, field observations allowed us to discern between them.
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In regard to floral visitor richness, we evaluated the accumulated floral visitor richness in both habitats by constructing rarefaction curves with EstimateS (Colwell, 2005). To
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analyze the change in species composition between habitats, we used Non-Metric Multidimensional Scaling (NMDS). To assess the significance of the difference in species
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composition between natural areas and home gardens we used Analysis of Similarities (ANOSIM), which provides an R-value. R-values close to 1 mean that habitats are greatly dissimilar in especies composition whereas values close to 0 mean that habitats are very similar (Hammer, Harper, & Ryan, 2001).
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To detect habitat and seasonal changes in floral visitors, we assigned each visitor to
one of three categories, according to the habitat or habitats in which it had been recorded during each season: home garden, natural area, or both. Then, we determined which floral visitors could be found in more than one season, and determined whether or not they remained in the same habitat across seasons. For visualizing habitat and seasonal changes
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in floral visitors (species fluxes) we used Venn Diagrams and RAWgraphs (DensityDesignResearchLab, 2019). Contrasts involving floral visitors To determine the significance of between habitat and between season differences in species richness of floral visitors per site, species richness of floral visitors taxa per site, and in abundance at both total floral visitors and by taxa, we used two way ANOVA and
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subsequent Tukey tests ( = 0.05) when data were normally distributed. When the data
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were not normally distributed, we normalized them using the square root transformation, then back transformed the results to obtain the mean values reported here (Gotelli &
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Ellison, 2012). When data did not meet the normality assumptions even after
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transformation, we used Wilcoxon tests for each season. Interaction networks across habitats and seasons
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We constructed bipartite networks (adjacency matrices) for each habitat and season, using the recorded interactions between floral visitor species and plant species. Thus for each
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season we pooled the flower insect interactions that took place in each of the nine natural areas and constructed one network for each season. We did the same for the home gardens, and obtained six interaction networks. The weight of the interactions in those networks corresponded to the number of times the interaction was observed. We looked for
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differences in the interaction networks across habitats and seasons by comparing uncorrelated indices that describe network structure [number of floral visitor and species, number of plant species, number of links, generality of floral visitors, and H2] (Blüthgen, Menzel, & Blüthgen, 2006). We carried out all analyses, plus the associated adjacency matrices, using R software packages car, vegan and bipartite (R Core Team, 2016). For
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Floral visitors in a neotropical landscape
visualizing the adjacency matrices, we used the package matplotlib with Python software (Hunter, 2007). Landscape context To identify how landscape context might affect floral visitor species richness and abundance across seasons, we first explored the data by plotting floral visitor species number against the four categories of land cover types: natural, agricultural, barren ground,
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and urban (Appendix A: Fig.1). We did the same to explore the relationship between floral
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visitor abundance and landscape context (Appendix A: Fig. 2). Simultaneously, we evaluated correlations between urban cover category and the other three variables
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(Appendix A: Table 1). Upon these explorations, we selected “urban cover category” as
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explanatory variable in individual linear models for each season. Because some scatter plots (Appendix A: Figs. 1 and 2) suggested a quadratic relationship between floral species
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richness and urban cover, we raised urban cover variable to the square and tested it as explanatory variable. When necessary (because of non normality of distributions), we
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normalized the response variables as described above.
Results
Characteristics of home garden and natural area sites Home gardens had higher percentages of bare soil and herbaceous cover than
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natural areas, but natural areas had a higher percentage of ground covered by leaf litter. Other variables, such as tree species richness, tree abundance, and ground cover by rocks and mulch did not differ significantly between the two habitats (Table 1). At the landscape context scale, we found that both natural cover and urban cover showed a wide range of values, whereas agricultural cover and barren ground showed a
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more restricted range and similar values (Table 1). We found that the home gardens and natural areas differed strongly in their amounts of agricultural, natural and urban land cover types (Table 1). Indeed, the average urban cover of home garden sites was 52.7%, versus 12.3% in natural-area sites, whereas agricultural cover of home garden sites was 6.7%, versus 3% in natural area sites.
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Plant species richness
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Mean plant species richness differed significantly between home gardens (16.37 ± 1.6) and natural areas (8.40 ± 0.98) (F1, 48 = 33.27, p < 0.0001). In addition, we found a
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season effect (F2, 48 = 6.03, p = 0.005), and a clear difference in plant species richness
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between the frost and the rainy seasons (Fig. 2A, Appendix A: Tables 2 and 3). Likewise, species richness of flowering plants differed significantly between home gardens (8.09 ±
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0.63) and natural areas (3.41 ± 0.46) (F1, 48 = 49.94, p < 0.001) and increased across seasons (F2, 48 = 7.19, p = 0.002; Fig. 2B, Appendix A: Tables 2 and 3). In addition, an
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interaction effect between habitat type and season was found, as the species richness values for flowering plants in both habitats converged in the rainy season (F2, 48 = 5.02, p = 0.01).
Floral visitors
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A total of 1301 floral visitor individuals representing 210 species or morphospecies
were recorded from a total of 99 plant species at the 18 sampling sites. Among the floral visitors, we found 74 species of flies (35% of the total species), 57 species of bees (27%), 33 of butterflies (16%), 25 species of wasps (12%), 14 of beetles (6.6%), and seven of bugs (3%). These 210 species were distributed in three guilds: pollinators (164 species, 78%), predators (38 species, 18%), and florivores (8 species, 4%). These floral insects visited 32 13
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plant families distributed in both habitat types with Asteraceae (36% of the visits), Brassicae (18% of the visits) and Fabaceae (9% of the visits) being the most visited.
Accumulated species richness of floral visitors Of the 210 species and morphospecies of floral visitors, 148 were recorded in natural areas, and 132 in home gardens (Fig. 3A). The rarefaction curves do not become
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fully asymptotic, but by the 150 individual mark clearly more species are accumulated in
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the natural areas than in the home gardens. We found a strong difference between species composition of floral visitors in natural areas versus home gardens (Fig. 3B, R value =
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0.59).
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Analysis of the recorded floral visitor species between habitats and seasons revealed a large number of singletons (species that just appeared once) and also suggested that the
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flux of species between specific habitats and seasons was restricted. Of the 210 species of floral visitors, 78 species (37%) were restricted to the natural areas, whereas 62 species
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(29.5%) were restricted to home gardens and 70 species (33%) were presented in both habitats (Fig. 4A). Furthermore of the 210 species of floral visitors, 21 species (10%) appeared in all three seasons (Fig. 4B), while 139 species (66%) appeared in only one season. The number of floral visitor species varied seasonally (Appendix A: Fig. 3). Of the
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78 species present during the frost season, 38 were recorded in the dry season. Of the 106 species recorded during the dry season, 43 were recorded in the rainy season, and of the 118 species recorded during the rainy season, 32 had been recorded in the frost season. Mean species richness of floral visitors We found no differences (F1, 48 =0.34, p= 0.85) between the floral visitor species richness in home gardens and in natural areas. The floral visitor species richness (mean ± SE) in home 14
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gardens was 10.07 ± 1.099 versus 10.31 ± 1.011 in natural areas. However, we found a significant effect of season (F2, 48 = 7.82, p = 0.001, Appendix A: Table 4), with mean species richness of floral visitors tending to increase from the frost to the rainy season (Fig. 5A, Appendix A: Tables 4 and 5). When examining the mean species richness for taxa we found that bees and butterflies showed strong, opposed patterns (Fig. 5B and C). Bee species richness did not
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show a habitat effect across all seasons (F1, 48 = 2.33, p = 0.13): bee species richness in
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home gardens was 4.04 ± 0.45, versus 3.28 ± 0.53 in natural areas. However, the seasonal influence upon bee species richness was clear (F2,48 = 23.65, p < 0.0001). The interaction
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between habitat and season was also significant, with home gardens showing higher bee
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species richness during the frost season (F2, 48 = 4.002, p = 0.025, Fig. 5B, Appendix A: Table 4). In contrast, species richness of butterflies across all seasons was greater in natural
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Appendix A: Table 6).
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areas (2.22 ± 0.38) than in home gardens (0.74 ± 0.18) (W =526, p = 0.004, Fig. 5C,
Floral visitor abundance
We found an effect of habitat and season upon the abundances of floral visitors, plus an interaction between habitat and season. Floral visitor abundance (mean ± SE) for
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home gardens was (26.60 ± 2.84), versus (18.078 ± 2.00) for natural areas (F1, 48 = 9.18, p = 0.004), with floral visitor abundance increasing from the frost to the rainy season (F2, 48 = 12.61, p < 0.0001, Fig. 5D, Appendix A: Tables 4 and 5). When we examined abundance by taxonomic group, we found a general trend of floral visitor abundance increasing from the frost season to the rainy season, with some groups showing a marked preference for one or the other of the two habitats (Appendix A: 15
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Tables 4 and 5). Bee abundance was influenced by habitat and season. Overall bee abundance was greater in home gardens (13.09 ± 2.11) than in natural areas (7.02 ± 1.46) (F1, 48 = 14.22, p = 0.0004). It tended to increase as the seasons progressed from frost to rainy (F2, 48 = 39.16, p < 0.001, Fig. 5E). Although the habitat effect disappeared after taking out the Apis mellifera abundance, the season effect remained, with bee abundance again increasing from the frost to the rainy season (F2, 48 = 26.01, p < 0.0001). For fly
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abundance, we found an interaction effect of habitat and season. Fly abundance was 5.08 ±
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1.086 in home gardens, and 2.61 ± 0.68 in natural areas (F1, 48 = 4.75, p = 0.003). A clear season effect was found, with fly abundance being higher during the dry season (F2, 48 =
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7.14, p = 0.002). Butterfly abundance was significantly higher in natural areas (3.37 ± 0.69)
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than in home gardens (1.04 ± 0.28, W = 512, p < 0.0001). This pattern was unmistakable throughout the three seasons, and was especially clear during the frost and rainy seasons
Network analysis
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(Fig. 5F, Appendix A: Table 6).
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The plants and floral visitors that we found in home gardens and natural areas formed a complex network of 210 floral visitor species and 99 flowering plant species, displaying 609 interactions and 1301 observations. In home gardens, the overall floral visitor network across the three seasons comprised 62 plant species and 132 floral visitor
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species (39 bee species, 10 wasp species, 5 bug species, 7 beetle species, 12 butterfly species, and 59 fly species), with 314 interactions and 774 observations. In natural areas, the overall network was arranged by 45 plant species and 149 floral visitor species (44 bee species, 20 wasp species, 3 bug species, 11 beetle species, 30 butterfly species, and 41 fly species), with 305 interactions and 527 observations. Of the 609 interactions, 421 were observed only once. We found that interactions with Apis mellifera, the honey bee, 16
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predominated: this insect interacted with 52 plant species, and accounted for 34% of the observations. The network formed across seasons was highly dynamic. Only 1.06% of the interactions occurred in both of the habitats (rather than in just one of them), even though 33% of the insects and 8% of plants were found in both habitats. The interactions also changed between seasons. Only 5.66% of interactions were observed in more than one
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season, in contrast with the 34% of insects and 27% of plants that were observed in more
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than one season (Fig. 6). Network indices pointed to a higher degree of specialization and vulnerability in natural areas than in home gardens (Table 2, Fig. 6). Flower visitor
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generality (the average number of plant species per floral visitor species) was greater in
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home gardens. Furthermore, the values of the H2 index, an indicator of the specialization degree at the network level that takes into account the different abundances of plants and
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pollinators (Blüthgen et al., 2006) were higher in natural areas during the frost season
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(H2=0.51), indicating that during this season natural areas had more specialists.
Landscape context
We found that apart from season, landscape context influenced floral visitor species number. In particular, the percentage of urban cover raised to the square influenced the
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square root of the total number of floral visitor species number in a quadratic way (pvalue=0.024, Table 3); whereas urban cover did not influence the abundance of the floral visitors in any season (p value ≥0.4).
Discussion
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Our work sheds light on the important effects of habitat type and seasonality upon species richness, species abundance, and network structure for floral visitors and their flowering plants in tropical regions. At the same time, it has implications for urban agriculture, landscape management and biodiversity conservation. Home gardens and natural areas differed in their characteristics at both the local and landscape levels. At the local level the most conspicuous differences were in ground cover,
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with home gardens having a larger fraction of herbaceous cover, and natural areas having a
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greater fraction of leaf litter cover. In contrast, home gardens and natural areas did not differ in the average number of tree species and tree abundance. Differences in ground
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cover may be explained by (1) the regular watering of home gardens, which favors and
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enhances herbaceous and floral cover (Gotlieb et al. 2011) and (2) the potentially greater provision of leaf litter by trees around natural areas. The lack of differences in tree species
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and abundance between natural areas and home gardens seems to derive from the fact that natural areas were not strictly forested areas, but prairies surrounded by forests and
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wetlands, and that most gardens had a variety of trees and shrubs for multiple purposes (Morales et al. 2015). Differences at the landscape context level seem to reflect contrast in land use between natural areas and more anthropogenic areas (Forman 1995). We found that natural areas harbored higher accumulated species richness of floral
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visitors than home gardens; however, more sampling is required to better assess the floral visitor species number that compose this community of beneficial insects in each habitat. Nonetheless, the inter habitat differences found in species composition as well as the suggested species fluxes (Fig. 4 and Appendix A: Fig. 3) highlight the need to view natural areas and home gardens as complementary habitats that together hold a floral visitor community composed of at least 210 species. Habitat complementarity is a key element for 18
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achieving biodiversity conservation and agroecological management (Colwell & Coddington, 1994; Mandelik, Winfree, Neeson, & Kremen, 2012; Marín et al., 2016; Tscharntke et al., 2012).
Furthermore, floral visitor species richness tended to be affected less by habitat type than by season, thus highlighting the importance of seasonality for floral visitors in a
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neotropical urban landscape. Nonetheless, the importance of habitat for some taxa was
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quite real. By examining the species densities of the main taxonomic groups of floral
visitors, we found that butterflies and bees were strongly influenced by both habitat and
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season. Bee species richness was greater in home gardens during the frost season, thus
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suggesting that bees were very good at exploiting the more abundant urban floral resources during the frost season (see Hall et al., 2016). On the contrary, species densities of
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butterflies tended to be higher in natural areas throughout the year, suggesting that butterflies depend strongly upon natural habitats. This dependence might be due to host
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plant fidelity, a phenomenon widely recognized in butterflies (DeVries, 1987). Moreover, we found that the influence of habitat and season on abundance of visitors showed a more striking pattern, with more individuals being recorded in home gardens than in natural areas over the frost and dry seasons. Overall, these results about floral visitor species richness
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and abundance highlight home gardens as hotspots in this neotropical city just as recently has been found at larger scale in temperate regions (Baldock et al., 2019; Hall et al., 2016). Home gardens may act as biodiversity hotspots by providing plenty floral resources to floral visitors (see sEbeling et al. 2018). Indeed, in this study we found that across seasons home gardens tended to show higher species richness of plants and flowering plants than
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natural areas; thus suggesting that the influence of habitat type and seasonality cascades through plant diversity to floral visitors. Network structure changed qualitatively across habitats and seasons, indicating that interactions between plant species and their floral visitors are highly dynamic and dependent upon environmental and habitat factors (Fig. 6) (Bascompte & Jordano 2007). Furthermore, the basic network indices (Table 2) show that overall networks in natural
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areas were more specialized and potentially less robust, whereas home gardens networks
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showed the opposite pattern (Marrero et al., 2014). Thus we posit that the networks in the
natural areas studied here are more vulnerable to habitat loss and climate change (Burkle et
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al., 2013; Geslin et al., 2013; Gotlieb et al., 2011; Tylianakis et al., 2007).
In this study, we explored in a basic way the influence that the immediate landscape
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context surrounding each of the 18 sites had on the total number of floral visitor species as well on their abundance. While, we did not find an influence of urban cover on the
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abundance of floral visitors in any season it is important to highlight that we found that increasing urbanization cover affected the square root of the species number of floral visitors in a quadratic way (Table 3). The quadratic behavior of species number in relation to urban cover is a pattern that has been previously reported (Fortel et al., 2014) and
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therefore, is noteworthy to highlight that adding more green in the context of a cement matrix requires a variety of sources (medium-sized agricultural plots, home gardens, agroforests, vacant lands, woodlots, and parks) (Gardiner, Burkman, & Prajzner, 2013; Glaum et al., 2017) that offer habitat and other resources to the floral visitors and thus potentially enhance their functions (Lin et al., 2015; Holzschuh et al., 2012). Overall, our
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results emphasize the need to establish conservation and management plans for San Cristóbal and its natural areas and home gardens.
Conclusions At local and landscape scale, natural areas and home gardens are both required for maintaining floral visitor diversity as well as ecological interaction networks in this
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neotropical city. Patterns in floral visitor species richness, abundance and their interaction networks with plants are greatly influenced by seasonality. Home gardens function as a
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refuge for floral visitors. Urban cover influenced floral visitor species number. Thus, our work points out to the need of considering agricultural home gardens and natural areas
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habitat types for maintaining biodiversity, its functions and network structure in neotropical
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urban landscapes. Otherwise, San Cristóbal and other cities face the possible simplification
provide. Conflict of interest
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of their biodiversity, ecological networks, and consequent loss of the functions they
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We declare we have no conflict of interest
Acknowledgments
We would like to thank Jorge Mérida, Benigno Gómez, Dr. Brailovsky and Miguel
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Martínez-Icó for identifying insects and plants. Initial talks with Rémy Vandame were key inputs for this research. Mariana Robles Calderón, Olivia Bracconier, Nathan Einbinder, Alejandro Roblero, Ruve Culej, and Amparo Hernández helped us with fieldwork and logistics and Jim Smith did an editorial review of a previous draft. We are greatly grateful to the two anonymous reviewers and to the editors that provided insightful comments on
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previous versions of this paper. We received funding through a CONACYT postdoctoral fellowship granted to Linda Marín, as well through funds from the Urban Agroecology Program (El Colegio de la Frontera Sur) granted to Helda Morales. Appendix A. Supplementary material associated with this article can be found, in the online
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version, at XXX.
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Tylianakis, J. M., Tscharntke, T., & Lewis, O. T. (2007). Habitat modification alters the structure of tropical host-parasitoid food webs. Nature, 445(7124), 202-205. doi: 10.1038/nature05429 Wong, K. V., Paddon, A., & Jimenez, A. (2013). Review of world urban heat islands: Many linked to increased mortality. Journal of Energy Resources TechnologyTransactions of the Asme, 135(2). doi: 10.1115/1.4023176
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Figure legends’
Fig. 1. Study area in San Cristóbal and surroundings, showing locations of the nine urban gardens sites (blue symbols) and nine natural area sites (green symbols) studied in the work
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Fig 2. Mean species richness for (A) all plant species and (B) flowering species in natural
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areas (green circles) and home gardens (blue circles) in San Cristóbal.
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Fig. 3. Species rarefaction curves (A) and NMDS plot for species composition (B) in
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natural areas (green circles) and home gardens (blue circles) in San Cristóbal. These figures
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were elaborated with the species records for the three seasons.
Fig. 4. Venn diagrams for floral visitor species shared between habitats (A) and seasons (B).
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Figure 5. Mean species richness and abundance of floral visitors in natural areas (green
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circles) and home gardens (blue circles) in San Cristóbal. Key to symbols: (A) mean total floral visitor species richness; (B) bee species richness; (C) butterfly species richness; (D)
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total floral visitors abundance; (E) bee abundance; (F) butterfly abundance.
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Figure 6. Adjacency plots for floral visitor species and flowering plant species in home gardens and natural areas across frost, dry, and rainy seasons. In each adjacency plot, the pink horizontal histogram corresponds to floral visitor abundance, whereas the green vertical histogram corresponds to plant abundance. The intensity of the interactions
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between floral visitors and plants is indicated by the saturation of the color of the squares found between both histograms. White squares = 0 interactions, brown squares = the highest value of interaction intensity for that plot.
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Table 1. Local and landscape scale habitat characterizations for home gardens and natural areas in San Cristóbal. Variable
Range
Home Gardens
Natural Areas
Test
pvalue
(t) or (W) Local scale Tree richness Tree abundance
6.11 ± 2.08 20.00 ± 5.56
6.44 ± 0.88 28.77 ± 8.47
0 - 30
30.03 ± 6.21
8.58 ± 3.83
Percent of herbaceous plants 0 - 58 Percent of leaf litter 0 - 69
33.81 ± 5.30 5.88 ± 4.00
17.39 ± 4.90 26.35 ± 7.77
Percent of grass Percent of mulch-straw Rocks
19.83 ± 7.07 4.61 ± 1.21 2.25 ± 1.50
37.19 ± 8.13 6.89 ± 4.89 2.64 ± 1.20
Percent of urban cover
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(t)
0.89 0.57 0.01
(t) 0.037 0.017 (t) 0.127 (W) 0.36 0.48
0 - 39.6
6.74 ± 4.25
2.91 ± 2.91
8. 00 (W) 0.003
0 - 39.3
4.93 ± 1.47 35.63 ± 7.18
6.62 ± 4.13 78.15 ± 4.93
35.00 (W) 0.66
52.70 ± 10.62
12.32 ± 3.49
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Landscape scale Percent of agricultural cover Percent of barren ground cover Percent of natural cover
0 - 83 0 - 45 0 - 14
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Percent of bare soil
0.15 47.50 (W) 11.00 (W) -2.27 67.50 (W) 1.61 30.00 48.50 (W)
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0 - 18 0 - 92
6.5 - 97.3 2.7 - 93.3
4.88
<0.00 1 9. 00 (W) 0.004
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t= t of Student, W= Wilcoxon test
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(t)
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Table 2. Network indices for networks found in home gardens and natural areas in San Cristóbal. Entries are values of the respective indices.
Frost Dry Rainy Season Season Season Home Natural Home Natural Home Natural Home Natural Gardens Areas Gardens Areas Gardens Areas Gardens Areas 67
68
75
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67
24 117 232 1.98 6.1
11 94 159 1.69 2.76
40 143 335 2.34 0.09
32 160 276 1.73 6.28
8.25
20.18
6.61
7.94
4.73 0.42
2.26 0.42
5.54 0.47
5.19 0.37
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Number of floral visitor 132 149 42 49 species Number of plant species 62 45 24 10 Number of interactions 314 305 84 62 Number of observations 774 527 207 92 Mean interaction weight 2.46 1.73 2.46 1.48 Mean number of floral 15.93 7.72 8.63 1.99 visitor links Mean number of plant 12.01 15.2 6.09 14.17 links Generality floral visitors 9.73 6.03 6.09 1.66 H2 0.37 0.32 0.38 0.51 Overall= The network formed by including the three seasons.
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Table 3. Influence of urban cover on floral visitor species number during the rainy season
Square root of floral visitor species ~ season + (urban cover)2 Estimate Standard Error 0.185 0.242 0.242 0.000
18.871 -2.850 1.263 -2.283
p-value
<0.001 0.006 0.212 0.0240
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3.484 0.690 0.306 -0.001
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Intercept Season (Frost) Season (Rainy) (Urban cover)^2
t-value
p-value
Intercept Season (Frost) Season (Rainy) (Urban cover)^2
<0.001 0.120 0.004 -0.390
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0.305 0.400 0.400 0.000
15.160 -1.570 3.000 -0.850
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4.620 0.628 1.197 0.000
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Square root of floral visitors abundance ~ season + (urban cover)2 Estimate Standard t-value Error
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