Next Article in Journal
Comparative Study on Production Performance of Different Oat (Avena sativa) Varieties and Soil Physicochemical Properties in Qaidam Basin
Previous Article in Journal
Xylem Sap Mycobiota in Grapevine Naturally Infected with Xylella fastidiosa: A Case Study: Interaction of Xylella fastidiosa with Sclerotinia sclerotiorum
Previous Article in Special Issue
Trait-Based Selection of Seeds Ingested and Dispersed by North American Waterfowl
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Effects of Frost and Fire on the Traits, Resources, and Floral Visitors of a Cerrado Plant, and Their Impact on the Plant–Visitor Interaction Network and Fruit Formation

by
Gabriela Fraga Porto
1,
José Henrique Pezzonia
1,
Ludimila Juliele Carvalho Leite
1,
Jordanny Luiza Sousa Santos
2 and
Kleber Del-Claro
2,*
1
Programa de Pós-Graduação em Entomologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto—FFCLRP, Universidade de São Paulo—USP, Ribeirão Preto 14040-901, Brazil
2
Instituto de Biologia, Universidade Federal de Uberlândia, Uberlândia 38400-902, Brazil
*
Author to whom correspondence should be addressed.
Plants 2025, 14(13), 1977; https://doi.org/10.3390/plants14131977 (registering DOI)
Submission received: 2 June 2025 / Revised: 24 June 2025 / Accepted: 25 June 2025 / Published: 28 June 2025

Abstract

The Cerrado, the world’s most diverse savanna, has several adaptations to fire. However, intense and frequent fires, especially after frosts, can severely impact this ecosystem. Despite this, few studies have evaluated the combined effects of frost followed by fire. We investigated how these disturbances affect plant traits, floral resources, floral visitor richness, and the structures of plant–pollinator interaction networks by using Byrsonima intermedia, a common Malpighiaceae shrub, as a model. We compared areas affected by frost alone and frost followed by fire and the same fire-affected area two years later. We examined pollen, oil volume, buds, and racemes and recorded floral visitors. Our main hypothesis was that fire-affected areas would exhibit higher floral visitor richness, more conspicuous plant traits, and greater fruit production than areas affected by frost only, which would show higher interaction generalization due to stronger negative impacts. The results confirmed that frost drastically reduced floral traits, visitor richness, and reproductive success. In contrast, fire facilitated faster recovery, triggering increased floral resource quantities, richer pollinator communities, more specialized interactions, and greater fruit production. Our findings highlight that fire, despite its impact, promotes faster ecosystem recovery compared to frost, reinforcing its ecological role in the Cerrado’s resilience.

1. Introduction

The Cerrado is an ecosystem strongly shaped by fire, which has historically determined its structure, composition, and functioning [1,2]. The species that comprise its biota have developed a set of adaptations that favor persistence in environments subject to recurrent fires. These adaptations include structural traits such as thick bark, protected buds, and underground reserve organs as well as life-cycle strategies like high resprouting capacity and synchronization of activity periods with the post-fire increase in resource availability [3,4,5].
Although fire plays a central ecological role in the Cerrado, extreme climatic events such as frost can also significantly impact this region’s biodiversity. Despite occurring sporadically, frost events cause high mortality for aboveground biomass, primarily affecting young individuals and cold-sensitive species [6,7]. When these events occur sequentially or coincide temporally, their effects may be intensified, leading to changes in vegetation regeneration, species functional traits, and the dynamics of ecological interactions [8].
Mutualistic interactions between plants and pollinators are fundamental to maintaining biodiversity, as they ensure plant reproduction and promote gene flow [9,10,11]. The formation and stability of these interactions depend on floral traits such as flower abundance, phenology, and the quantity of floral resources offered, in addition to environmental conditions like temperature and precipitation [12,13,14,15]. Changes in these factors can affect pollinator behavior, interaction frequency, and the organization of ecological networks [16,17,18,19].
In the Cerrado, there is evidence that fire directly influences flowering patterns, the availability of floral resources, and the composition of flower visitor communities [20,21]. These effects often favor generalist species, which are more flexible in terms of partner selection and therefore more resilient [22]. In contrast, specialist species tend to be more sensitive to environmental changes [23,24]. Consequently, ecological networks in fire-affected areas usually exhibit lower degrees of specialization, which, despite increasing the cohesion of interactions in the short term, may reduce stability in the face of new disturbances [25,26,27,28].
Despite our extensive knowledge of the effects of fire, little is known about how frost, either alone or in combination with fire, impacts vegetative traits, floral resource availability, and plant–pollinator interaction networks in the Cerrado. This knowledge gap becomes particularly relevant given the increasing frequency of extreme climatic events associated with global climate change [7,8,29,30].
In this context, we investigated the effects of frost and frost followed by fire on vegetative traits, floral resources, visitor richness and abundance, and the structure of interaction networks of Byrsonima intermedia A.Juss. (Figure 1), a key species in the Cerrado. We evaluated these parameters shortly after a severe frost event that affected a Cerrado reserve in July 2021. Two months later, the same area was impacted by a large wildfire that lasted three days and burned almost the entire reserve, leaving only a small area, less than 10%, unaffected by fire. Additionally, we reassessed plant traits, resources, and plant–pollinator interaction network structure and fruit formation two years after frost and fire to understand how these events influence interactions over time. This unique sequence of events provided an opportunity to simultaneously investigate the effects of frost and frost followed by fire on plant–floral visitor interaction networks.
Based on the high resilience of fire-adapted species [31,32], we hypothesized that the area affected by frost followed by fire would exhibit higher visitor abundance and richness, greater development of vegetative traits, higher availability of floral resources, and greater fruit production compared to the area affected only by frost. This expectation was based on the fact that fire, in addition to removing the dead biomass left by frost, promotes canopy opening, improves light conditions, and stimulates physiological processes such as resprouting and flowering, thus accelerating vegetation recovery [8,33]. In contrast, in the area affected exclusively by frost, we expected a more generalized interaction network due to the lower availability of floral resources and reduced visitor abundance and diversity, a pattern already observed in networks affected by environmental disturbances [28,34,35].

2. Materials and Methods

2.1. Study Site

The study was conducted in a Cerrado (Brazilian tropical savanna) area within the legal reserve area of the “Clube de Caça e Pesca Itororó (CCPIU)” in Uberlândia, State of Minas Gerais, Southeastern Brazil (18°59′569″ S–48°18′351″ W). According to the Köppen classification, the climate in the region is of the AW type, with two well-defined seasons: a rainy season occurring from October to April and a dry season from May to September [36]. There are different types of vegetation in the reserve, such as open grassland or savanna with sparse or no trees (Campo limpo); grassland with scattered shrubs and small trees (Campo sujo); a savanna characterized by a combination of grasslands, scrublands, and areas with scattered trees and shrubs (Cerrado); a dense, more wooded or forested area (Cerradão); and “Veredas”, that is, palm swamps or wetland surrounded by Cerrado vegetation [37]. We operated in an area of the Cerrado that suffered heavy frost in July 2021, an area of the Cerrado that suffered frost and was burned in early September 2021, and an area where B. intermedia flowering occurred in 2023.

2.2. Study System

The plant species chosen as a model for this study was Byrsonima intermedia A. Juss., commonly known as “murici-pequeno” (Figure 1). The choice of this species was motivated by its abundant occurrence in the reserve and its rapid recovery after fire. This shrub can reach heights of approximately 0.5 to 2.5 meters [38]. The floral morphology of this species is similar to that of Malpighiaceae in general: five sepals with oil-producing glands (elaiophores), ten stamens, and three carpels [39]. Its anthesis is diurnal, and the flowers last an average of 48 hours [40]. This species is self-incompatible and primarily pollinated by bees, offering floral resources such as oil and pollen [41,42].

2.3. Measuring Richness, Abundance, and Frequency of Floral Visitors

In order to assess whether disturbances affected the richness, abundance, and frequency of floral visitors and the structure of the plant–floral visitor interaction network of B. intermedia in 2021, we selected 30 shrubs in the area affected only by frost and in the area affected by frost and subsequent fire. The area affected only by frost was located approximately 500 m away from the area that experienced impacts from both frost and subsequent fire. The individuals were of similar sizes (~1 m to 1.5 m in height) and separated by at least 10 m. Later, in November 2023, two years after the disturbances, we again, and in the same manner, selected thirty individuals in the area affected by frost and subsequent fire to evaluate the effect of these disturbances on traits, resources, and the plant–pollinator network structure over time. In both years of study, the plants were inspected three times a week on sunny days during the flowering period. We made direct observations lasting 40 min for each plant, between 8 am and 5 pm, with a 10 min rest interval at the end of each series. The visitors were collected and taken for identification at the Laboratory of Behavioral Ecology and Interactions (LECI) at the Federal University of Uberlândia. All collected visitors were identified using taxonomic keys [43,44] and collections previously checked by taxonomists specialized in Brazilian bees.

2.4. Measuring Traits and Resources of B. Intermedia

To evaluate whether the disturbances affected the plants’ resource production, we previously bagged flower buds at the pre-anthesis stage to quantify the number of pollen grains and the volume of oil produced. To quantify the volume of floral oil, we used the 30 specimens of B. intermedia selected for the study in each area affected by frost (2021) and frost followed by fire (2021) and the area two years post-frost followed by fire (2023). However, to quantify the number of pollen grains, we randomly selected five individuals from each disturbed area (with one bud per individual). Subsequently, the buds were taken to the Laboratory of Behavioral Ecology and Interactions, and the pollen grains were carefully removed from the anthers using tweezers and placed onto a slide to allow for counting. We used acetic carmine as a stain, as indicated by Kearns and Inouye (1993) [45], and counting was performed using a manual counter under an Olympus CX40 optical microscope. To quantify the oil volume, we used microcapillaries with a capacity of 1 µL.
To evaluate whether the disturbances affected plant growth, we counted the total number of racemes and healthy buds produced by B. intermedia specimens weekly near the flowering period and considered the highest number of buds before flowering to be the total number of buds produced by each individual. We preferred to count buds instead of flowers because the buds of this plant are severely attacked by parasitic wasps.

2.5. Measuring Formed Fruits

To investigate whether fruit production was affected by disturbances both post-frost (2021) and post-frost and post-fire (2021) and two years post-frost and post-fire (2023), we randomly marked an inflorescence on each B. intermedia specimen (N = 30 per disturbance area) where observations of floral visitors were made and carried out hand pollination experiments. In treatment (1), a spontaneous self-pollination test was carried out, used to measure autogamy and the need for pollinators; and in treatment (2), an artificial self-pollination test was performed to determine self-compatibility. Finally, we also carried out a control experiment in which the flowers were not manipulated and remained free for natural pollination. In the first two treatments, the flower buds were bagged with voile fabric bags to avoid visitation by pollinating agents while allowing the entry of sunlight and the exchange of gases.

2.6. Plant–Pollinator Interaction Network

To investigate how disturbances affect the structure of plant–pollinator networks, making them more or less specialized, three quantitative interaction matrices were constructed for each area affected by frost (2021) and frost and fire (2021) and for the areas two years post-frost and post-fire (2023). A network-level metric (H2′) and two individual-level metrics were calculated using the ‘bipartite’ package in R, following recommendations on weighted interaction metric analysis from the package documentation [46,47] (Dormann et al., 2008, 2009). The network-level metrics were calculated using the ‘networklevel’ function, while the species-level indices were quantified using the ‘specieslevel’ function [46].
We measured the specialization of each area under the influence of disturbances in network level (H2′). This is a measure based on the deviation of a species’ realized number of interactions from what is expected based on the total number of interactions. The more selective the species, the greater the value of H2′ for the web, with 0 indicating no specialization and 1 indicating complete specialization [48,49]. To assess if an observed network structure is a result of randomness, 1000 null matrices were constructed using the Patefield method (the ‘r2dtable’ method in the nullmodel function of the bipartite package). The Patefield method generates relatively unconstrained null models controlling only for the network dimensions and the condition that marginal totals remain identical to the observed network [47,50].
The species-level metrics calculated were specialization (d’), which measures the deviation of the observed interaction frequencies of the focal species from an expected interaction frequency of a perfectly generalized species (with interactions evenly distributed among all partners), for which values range from 0 (extreme generalization) to 1 (specialization) [48], and degree, which is the number of links per species, i.e., the number of plant species with which each pollinator species interacts [51].

2.7. Data Analysis

To investigate whether the richness and abundance of floral visitors, the number of floral racemes and buds, the volume of oil, and the number of pollen grains differed between the areas under the influence of the different disturbances, we used Generalized Linear Models with negative Gaussian, Poisson, or binomial distributions (whenever superdispersion occurred). The response variables of this study were the richness and abundance of floral visitors and the traits and resources of a plant, and the explanatory variables were the disturbances (frost, frost and fire, and conditions two years after frost and fire). However, to evaluate whether the disturbances affected the fruit production of B. intermedia in each pollination treatment, we used a Generalized Linear Model (GLM) with a binomial distribution since the data related to incidences (absence/presence of fruits). The response variable was the number of fruits grown, and the explanatory variables were the disturbances. Finally, to compare the means of the metrics of individual networks (Specialization d’ and Degreee), we used an analysis-of-variance model (ANOVA). Assumptions of normality and homoscedasticity were examined using the “DHARMa” package [52], followed by post hoc tests with estimated marginal means using the “emmeans” package [53].

3. Results

3.1. Richness and Abundance of Floral Visitors

The richness of floral visitors varied significantly among disturbances (GLM: χ2 = 6.12, p = 0.04). The lowest richness occurred in the frost-only area (2021) (0.06 ± 0.18), and the highest occurred two years after frost and fire (2023) (0.47 ± 0.14) (Figure 2a). In contrast, visitor abundance did not differ significantly (GLM: χ2 = 3.77, p = 0.152), although there was an increasing trend over time. The lowest abundance was recorded after frost (2021) (0.31 ± 0.23), followed by frost and fire (2021) (0.80 ± 0.21), and the highest was recorded two years after frost and fire (2023) (0.90 ± 0.21) (Figure 2b).

3.2. Frequency of Floral Visitors

The composition of dominant floral visitors shifted across disturbances. After frost and fire (2021), Trigona spinipes (40%) and Tetragonisca angustula (28%) were most frequent. In the frost-only area (2021), Tetragonisca angustula dominated (45%), followed by Paratrigona lineata (17%). Two years later (2023), visitor composition diversified, with Paratrigona lineata and Centris aenea (17% each) and Epicharis bicolor (14%) being the most frequent. Several new species appeared in 2023, including Augochloropsis sp., Frieseomelitta flavicornis, Apis mellifera, and Pseudaugochlora graminea (Figure 3).

3.3. Traits and Resources of B. Intermedia

The vegetative traits and floral resources of B. intermedia differed among disturbances. The quantities of racemes (GLM: χ2 = 6.30, p = 0.036) and buds (GLM: χ2 = 8.51, p = 0.014) were lowest after frost (2021) and progressively increased after frost and fire (2021), increasing even further two years later (2023) (Figure 2c,e).
Floral oil volume also differed (GLM: χ2 = 9.08, p = 0.01), with the lowest value occurring after frost (2021) (0.07 ± 0.01) and the highest observed two years after frost and fire (2023) (0.15 ± 0.02) (Figure 2d). Pollen production exhibited the clearest pattern (GLM: χ2 = 135.63, p < 0.001), nearly doubling from 16,286 ± 946 in the frost-only area to 30,701 ± 946 two years after frost and fire (2023) (Figure 2f).

3.4. Fruit Production

Pollination tests confirmed that B. intermedia requires cross-pollination for fruit setting, as neither spontaneous nor manual self-pollination resulted in significant fruit development (GLM: χ2 = 0.22, p = 0.90; χ2 = 4.49, p = 0.11). The few fruits produced were likely a product of contamination during manipulation.
Under natural pollination conditions, fruit production differed significantly (GLM: χ2 = 9.86, p = 0.007) (Figure 4). The highest fruit-setting level was observed two years after frost and fire (2023) (3.3 ± 1.0), and this figure was followed by those for the frost-only area (2021) (1.0 ± 0.41) and the area affected by frost and fire (2021) (0.8 ± 0.3).

3.5. Plant–Visitor Interaction Network

The values of the specialization/generalization indices (H2′) at the network level were significantly higher compared to the null expectation under random association (p < 0.05) for the area affected by frost and fire (2021) (0.47; p = 0.002) and in the same area two years after frost and fire (2023) (0.42; p = 0.003). In the area affected only by frost (2021), the network was less specialized, although the observed value was not significant, suggesting that this result may be due to chance (0.24; p = 0.32; Figure 5).
Among the species-level network metrics, the average degree values were not significantly different among the disturbances (F = 0.81; DF = 2; p = 0.45). Similarly, the average specialization d’ values did not vary among the different disturbances (F = 2.49; DF = 2; p = 0.09), although a trend towards lower specialization was observed for areas affected by frost (2021) (Figure 6).

4. Discussion

The hypothesis that fire affects plant traits, resources, and plant–floral visitor interactions in the Cerrado less than frost was corroborated by our main results. The frost event of 2021 had a more negative impact on plant traits and resources, making the plant–floral visitor interaction network more generalized, resulting in lower reproductive success of B. intermedia. The floral traits and resources of the plants were less conspicuous in the frost-only area, and the richness of floral visitors was significantly lower. In addition, the plant–floral visitor ecological network of the area affected by frost only was the most generalized. This area had more frequent visits from generalist species and maintained a greater number of interactions with B. intermedia, which possibly contributed to the lower average number of fruits developed. On the other hand, plant traits, such as the number of racemes and buds, were higher in the areas affected by frost and fire. After the frost event and the subsequent fire, the resources in the area increased significantly two years later, and there was also a greater richness of floral visitors. The appearance of new species in the area two years after the disturbance contributed to a higher average for fruit formation.
This is the first study to investigate the effects of frost and frost followed by fire on traits, floral resources, and plant–visitor floral interactions for a Cerrado plant species. In this study, we observed that the richness of floral visitors decreased considerably after frosts, especially species considered specific pollinators, such as oil-collecting species (e.g., members of the genera Epicharis and Centris) [39,54]. Previous studies conducted in other locations also showed that low temperatures have a negative impact on pollinator richness and floral visitors [55,56,57] and lead to a deficiency in the development of pollen and ovules [58,59]. In our study, the area affected by frost had the fewest pollen grains produced per bud, especially when compared to the area evaluated two years after frost and fire. This indicates that the low temperature caused by frost possibly causes low pollen production by B. intermedia as well as lower quantities of floral oil, racemes, and buds. Nevertheless, the plants in the Cerrado present efficient fire adaptation, responding to this physical stimulus by resprouting and blossoming [60].
Previous studies have shown the direct effects of frost on leaves, flower buds, and plant growth [7,37,61,62]. However, few studies have been conducted in tropical savannas [63,64], and among these, none have focused on plant traits that directly affect interactions with animals. Evidence from other ecosystems suggests that frost can indeed impact floral traits relevant to pollination. For instance, Pardee et al. [65] reported a 40% decrease in the number of flowers developed by a plant species exposed to frost in Colorado, USA. Additionally, this species experienced 48% fewer pollinator visits and an 8.5% reduction in fruit setting. Similarly, in our study, the area affected by frost in the Cerrado produced the lowest average number of racemes and buds, indicating that frost can impair the growth and development of floral structures essential for attracting pollinators. This area also exhibited lower network-level specialization and a higher frequency of visits by generalist floral visitors, such as Tetragonisca angustula and Paratrigona lineata, a pattern comparable to that observed for B. intermedia in disturbed areas of the Cerrado [66,67].
Although generalist species are considered critical in disturbed environments, as they participate in most of the links established with plant species [23,68,69], there is limited understanding of the ecosystem services provided by generalist pollinators. Burns et al. [70] showed that the ability to attract many pollinator species (high generalization) in disturbed locations resulted in decreased seed-by-ovule ability (fitness), i.e., decreased plant reproductive capacity. Here, we found that the average number of fruits formed was lower in the area under the influence of frost alone compared to the area under the influence of frost followed by fire. This shows that frost has currently unknown indirect and direct effects on the reproductive capacity of Cerrado plants.
In contrast to the area under the influence of frost only, in the area under the influence of frost and subsequent fire, both in the first flowering period and two years after, there was a greater presence of specific pollinators as well as more conspicuous traits and resources. Studies have shown positive changes in resource availability and post-fire pollinator communities [4,71,72], which may result in changes in network specialization [73,74,75]. In this case, the specialization of the network in the area under the influence of frost followed by fire was similar in the first flowering and two years after the disturbance (0.47 and 0.42, respectively). This may be linked to the greater availability of resources and the greater attraction of specific pollinators, especially two years after the disturbances, when new species colonized the disturbed area. Despite this, we did not detect significant differences in the metrics at the species level evaluated, although the specialization of the species tended to decrease in the area under the influence of frost only, reinforcing the notion that the interactions were less specialized.
Although fire has played an important evolutionary role in the formation of the Cerrado [1,32], its high frequency, driven by anthropogenic factors, may negatively affect species and their interactions [76,77,78]. We found that two years after frost and fire, important bee species that had disappeared reemerged. This includes Paratetrapedia, a key genus of oil-collecting bees in the Americas [79], and Epicharis analis and E. flava, both associated with Malpighiaceae species [41]. These observations reinforce the importance of conducting long-term studies to understand the direct and indirect effects of anthropogenic disturbances and climatic extremes on ecological communities. Our results also have practical implications for fire management in the Cerrado. While high fire frequency can be detrimental [78,80], fire following frost may help restore floral traits and pollinator communities, mitigating some of the negative impacts of frost. This suggests that indiscriminate fire suppression could inadvertently hinder natural regenerative processes essential for maintaining plant–pollinator interactions in this fire-adapted ecosystem. Nevertheless, our study has limitations. The short temporal scale may not fully capture long-term dynamics, and focusing on a single plant species and few plots limits broader generalization. Expanding the temporal and spatial scales and including multiple species would be crucial to facilitate more effective conservation and management strategies under increasing climate variability.

5. Conclusions

Our study reveals the complex dynamics between floral traits, resources, and plant-visitor interactions in response to different environmental disturbances in the Cerrado. We observed that frost, in isolation, had a significant negative effect, reducing the conspicuity of floral traits and the richness of visitors, resulting in a more generalized ecological network and lower reproductive success of B. intermedia. In contrast, areas that suffered the combined effects of frost followed by fire showed a remarkable recovery of floral traits and resources, with an increase in visitor richness and specialization of interactions, which culminated in greater reproductive success. These findings corroborate the hypothesis that compared to frost, fire has a less negative impact on the traits, resources, and networks of floral visitors of Cerrado species. In addition, this study highlights the importance of conducting long-term research to understand the effects of environmental disturbances, especially those promoted by anthropogenic activities, on ecological communities. These results highlight the need for mitigation strategies aimed at preserving species and maintaining ecological interactions in the Cerrado.

Author Contributions

G.F.P.: conceptualization; methodology; investigation; validation; project administration; formal analysis; data curation; writing—original draft; writing—review and editing; visualization; software; and resources. J.H.P.: methodology; and data curation and review. L.J.C.L.: methodology; and data curation and review. J.L.S.S.: methodology; and data curation and review. K.D.-C.: funding acquisition; investigation; validation; supervision; writing—review and editing; and resources. All authors have read and agreed to the published version of the manuscript.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (403647/2021-5) and CAPES (C1).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank the Clube de Caça e Pesca Itororó de Uberlândia (CCPIU) for the logistical support, and the Laboratory of Behavioral Ecology and Interactions (LECI) at the Federal University of Uberlândia for assistance with species identification. We also thank all the colleagues who supported our field activities.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Simon, M.F.; Grether, R.; Queiroz, L.P.; Skema, C.; Pennington, R.T.; Hughes, C.E. Recent Assembly of the Cerrado, a Neotropical Plant Diversity Hotspot, by In Situ Evolution of Adaptations to Fire. Proc. Natl. Acad. Sci. USA 2009, 106, 20359–20364. [Google Scholar] [CrossRef] [PubMed]
  2. Pivello, V.R. The Use of Fire in the Cerrado and Amazonian Rainforests of Brazil: Past and Present. Fire Ecol. 2011, 7, 24–39. [Google Scholar] [CrossRef]
  3. February, E.C.; Coetsee, C.; Cook, G.D. Physiological Traits of Savanna Woody Species. In Savanna Woody Plants and Large Herbivores; Blackwell Publishing Ltd.: Oxford, UK, 2019; pp. 309–329. [Google Scholar] [CrossRef]
  4. Carbone, L.M.; Tavella, J.; Marquez, V.; Ashworth, L.; Pausas, J.G.; Aguilar, R. Fire effects on pollination and plant reproduction: A quantitative review. Ann. Bot. 2025, 135, 43–56. [Google Scholar] [CrossRef]
  5. Lazarina, M.; Sgardelis, S.P.; Tscheulin, T.; Kallimanis, A.S.; Petanidou, T. Bee Response to Fire in Mediterranean Ecosystems: The Role of Nesting and Foraging Traits. J. Anim. Ecol. 2016, 85, 537–547. [Google Scholar] [CrossRef]
  6. Antonio, A.C.; Scalon, M.C.M.; Rossatto, D.R. The Role of Bud Protection and Bark Density in Frost Resistance of Savanna Trees. Plant Biol. 2019, 22, 55–61. [Google Scholar] [CrossRef]
  7. Hoffmann, W.A.; Flake, S.W.; Abreu, R.C.; Pilon, N.A.; Rossatto, D.R.; Durigan, G. Rare frost events reinforce tropical savanna–forest boundaries. J. Ecol. 2019, 107, 468–477. [Google Scholar] [CrossRef]
  8. Porto, G.F.; Pezzonia, J.H.; Del-Claro, K. Extrafloral Nectary-Bearing Plants Recover Ant Association Benefits Faster and More Effectively after Frost-Fire Events Than after Frost Alone. Plants 2023, 12, 3592. [Google Scholar] [CrossRef]
  9. Ollerton, J. Pollinator Diversity: Distribution, Ecological Function, and Conservation. Annu. Rev. Ecol. Evol. Syst. 2017, 48, 353–376. [Google Scholar] [CrossRef]
  10. Bascompte, J.; Jordano, P. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. Annu. Rev. Ecol. Evol. Syst. 2007, 38, 567–593. [Google Scholar] [CrossRef]
  11. Torezan-Silingardi, H.M.; Silberbauer-Gottsberger, I.; Gottsberger, G. Pollination ecology: Natural history, perspectives and future directions. In Plant-Animal Interactions; Springer: Cham, Switzerland, 2021; pp. 119–174. [Google Scholar]
  12. Trunschke, J.; García-Meneses, P.M.; Sauquet, H.; Dellinger, A.S.; Chartier, M. The Evolutionary Ecology of Plant–Pollinator Interactions under Climate Change. New Phytol. 2024, 241, 1322–1337. [Google Scholar] [CrossRef]
  13. Caruso, C.M.; Eisen, K.; Martin, R.A.; Sletvold, N. A meta-analysis of the agents of selection on floral traits. Evolution 2018, 73, 4–14. [Google Scholar] [CrossRef]
  14. Thompson, J.N. The coevolving web of life. Am. Nat. 2009, 173, 125–140. [Google Scholar] [CrossRef] [PubMed]
  15. Morente-López, J.; Lara-Romero, C.; García, M.B.; Iriondo, J.M. Phenological Shifts Associated with Climate Change Influence Pollination Effectiveness in High-Mountain Plants. Perspect. Plant Ecol. Evol. Syst. 2018, 30, 62–72. [Google Scholar] [CrossRef]
  16. Suárez-Mariño, A.; Arceo-Gómez, G.; Albor, C.; Parra-Tabla, V. Co-flowering modularity and floral trait similarity help explain temporal changes in plant–pollinator network structure. Plant Ecol. 2022, 223, 1289–1304. [Google Scholar] [CrossRef]
  17. Lázaro, A.; Valido, A.; Tella, J.L.; Nogales, M. Flower Traits, Flower-Visiting Insects and Pollination Effectiveness in Shrubs from the Canary Islands. Perspect. Plant Ecol. Evol. Syst. 2019, 38, 20–28. [Google Scholar] [CrossRef]
  18. Peralta, G.; Frost, C.M.; Rand, T.A.; Didham, R.K.; Tylianakis, J.M. Complementarity and Specialisation Determine the Resilience of Pollination Networks to Species Extinctions. Ecol. Lett. 2017, 20, 1325–1333. [Google Scholar] [CrossRef]
  19. Carvalheiro, L.G.; Biesmeijer, J.C.; Benadi, G.; Fründ, J.; Stang, M.; Bartomeus, I.; Kaiser-Bunbury, C.N.; Baude, M.; Gomes, S.I.F.; Merckx, V.; et al. The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol. Lett. 2014, 17, 1389–1399. [Google Scholar] [CrossRef]
  20. Welti, E.A.R.; Joern, A. Fire and Grazing Modulate Pollinator Communities in Tallgrass Prairie. J. Appl. Ecol. 2018, 55, 1851–1861. [Google Scholar] [CrossRef]
  21. Teixido, A.L.; Souza, C.S.; Barônio, G.J.; Torezan, J.M.D.; Fidelis, A. Post-Fire Temporal Dynamics of Plant-Pollinator Communities in a Tropical Savanna. Oecologia 2024, 206, 199–210. [Google Scholar] [CrossRef]
  22. Pires, E.P.; Faria, L.D.B.; Monteiro, A.B.; Domingos, D.Q.; Mansanares, M.E.; Hermes, M.G. Insect Sociality Plays a Major Role in a Highly Complex Flower-Visiting Network in the Neotropical Savanna. Apidologie 2022, 53, 14. [Google Scholar] [CrossRef]
  23. Zografou, K.; Svensson, B.M.; Hovestadt, T.; Krauss, J.; Schweiger, O. Specialist Pollinators Are More Sensitive to Fire than Generalists Regardless of Dispersal Ability. J. Appl. Ecol. 2020, 57, 1203–1212. [Google Scholar] [CrossRef]
  24. Fidelis, A.; Zirondi, D.L. Does Fire Always Affect Plant Reproduction? A Long-Term Study in Brazilian Savannas. Acta Oecol. 2021, 112, 103794. [Google Scholar] [CrossRef]
  25. Bugmann, H.; Seidl, R.; Hartig, F.; Bohn, F.; Brůna, J.; Cailleret, M.; François, L.; Heinke, J.; Henrot, A.J.; Hickler, T.; et al. Tree mortality submodels drive simulated long-term forest dynamics: Assessing 15 models from the stand to global scale. Ecosphere 2019, 10, e02616. [Google Scholar] [CrossRef] [PubMed]
  26. Barônio, G.J.; Torezan, J.M.D.; Fidelis, A. Effects of Fire on Reproductive Phenology in Brazilian Savannas: What Do We Know and What Is Still Missing? Flora 2021, 283, 151921. [Google Scholar] [CrossRef]
  27. Aizen, M.A.; Sabatino, M.; Tylianakis, J.M. Specialization and Rarity Predict Vulnerability of Plant–Pollinator Networks to Species Extinctions. Proc. R. Soc. B Biol. Sci. 2012, 279, 2121–2130. [Google Scholar] [CrossRef]
  28. Peralta, G.; Stevani, E.L.; Chacoff, N.P.; Dorado, J.; Vázquez, D.P. Fire influences the structure of plant–bee networks. J. Anim. Ecol. 2017, 86, 1372–1379. [Google Scholar] [CrossRef] [PubMed]
  29. IPCC. Climate Change 2021: The Physical Science Basis. In Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK, 2021. [Google Scholar]
  30. Maxwell, S.L.; Butt, N.; Maron, M.; McAlpine, C.A.; Chapman, S.; Ullmann, A.; Segan, D.B.; Watson, J.E.M. Conservation Implications of Ecological Responses to Extreme Weather and Climate Events. Divers. Distrib. 2019, 25, 613–625. [Google Scholar] [CrossRef]
  31. Hardesty, J.; Myers, R.; Fulks, W. January. Fire, ecosystems, and people: A preliminary assessment of fire as a global conservation issue. Georg. Wright Forum 2005, 22, 78–87. [Google Scholar]
  32. Simon, M.F.; Pennington, R.T. Evidence for Adaptation to Fire Regimes in the Tropical Savannas of the Brazilian Cerrado. Int. J. Plant Sci. 2012, 173, 711–723. [Google Scholar] [CrossRef]
  33. Pilon, N.A.L.; Cava, M.G.B.; Hoffmann, W.A.; Abreu, R.C.R.; Fidelis, A.; Durigan, G. The Diversity of Post-Fire Regeneration Strategies in the Cerrado Ground Layer. J. Veg. Sci. 2018, 29, 781–792. [Google Scholar] [CrossRef]
  34. da Silva Goldas, C.; Podgaiski, L.R.; Veronese Corrêa da Silva, C.; Abreu Ferreira, P.M.; Vizentin-Bugoni, J.; de Souza Mendonça, M., Jr. Structural Resilience and High Interaction Dissimilarity of Plant–Pollinator Interaction Networks in Fire-Prone Grasslands. Oecologia 2022, 198, 179–192. [Google Scholar] [CrossRef] [PubMed]
  35. Maruyama, P.K.; Bosenbecker, C.; Cardoso, J.C.F.; Sonne, J.; Ballarin, C.S.; Souza, C.S.; Leguizamón, J.; Lopes, A.V.; Maglianesi, M.A.; Otárola, M.F.; et al. Urban Environments Increase Generalization of Hummingbird–Plant Networks across Climate Gradients. Proc. Natl. Acad. Sci. USA 2024, 121, e2322347121. [Google Scholar] [CrossRef] [PubMed]
  36. Velasque, M.; Del-Claro, K. Host plant phenology may determine the abundance of an ecosystem engineering herbivore in a tropical savanna. Ecol. Entomol. 2016, 41, 421–430. [Google Scholar] [CrossRef]
  37. Fagundes, R.; Lange, D.; Anjos, D.V.; de Lima, F.P.; Nahas, L.; Corro, E.J.; Silva, P.B.G.; Del-Claro, K.; Ribeiro, S.P.; Dáttilo, W. Limited effects of fire disturbances on the species diversity and structure of ant-plant interaction networks in Brazilian Cerrado. Acta Oecol. 2018, 93, 65–73. [Google Scholar] [CrossRef]
  38. Sannomia, M.; Cardoso, C.R.P.; Figueiredo, M.E.; Rodrigues, C.M.; Santos, L.C.S.; dos Santos, F.V.; Serpeloni, J.M.; Cólus, I.M.; Vilegas, W.; Varanda, E.A. Mutagenic evaluation and chemical investigation of Byrsonima intermedia A. Juss. leaf extracts. J. Ethnopharmacol. 2007, 112, 319–326. [Google Scholar] [CrossRef]
  39. Oliveira, M.I.B.; Polido, C.A.; Costa, L.C.; Fava, W.S. Sistema reprodutivo e polinização de Byrsonima intermedia A. Juss. (Malpighiaceae) em Mato Grosso do Sul, Brasil. Rev. Bras. Biociênc. 2007, 5, 756–758. [Google Scholar]
  40. Filho, L.C.R.; Lomônaco, C. Variações fenotípicas em subpopulações de Davilla elliptica A. St.-Hil. (Dilleniaceae) e Byrsonima intermedia A. Juss. (Malpighiaceae) em uma área de transição cerrado-vereda. Acta Bot. Bras. 2006, 20, 719–725. [Google Scholar] [CrossRef]
  41. Boas, J.C.V.; Fava, W.S.; Laroca, S.; Sigrist, M.R. Two sympatric Byrsonima species (Malpighiaceae) differ in phenological and reproductive patterns. Flora 2013, 208, 360–369. [Google Scholar] [CrossRef]
  42. Balestra, C.L.; Fachardo, A.L.S.; Soares, M.P.; Reys, P.; Silva, F.G. Reproductive biology and pollination of two species of Byrsonima Kunth in a Cerrado fragment in Central Brazil. Rev. Bioci. 2014, 20, 71–81. [Google Scholar]
  43. Silveira, F.A.; Melo, G.A.R.; Almeida, E.A.B. Abelhas Brasileiras: Sistemática e Identificação; Fundação Araucária: Belo Horizonte, Brazil, 2002. [Google Scholar]
  44. Oliveira, F.F.; Richers, B.T.T.; Silva, J.R.; Farias, R.C.; Matos, T.A.L. Guia Ilustrado das Abelhas Sem-Ferrão das Reservas Amanã e Mamirauá, Brasil (Hymenoptera, Apidae, Meliponini); IDSN: Manaus, Brazil, 2013. [Google Scholar]
  45. Kearns, C.A.; Inouye, D. Techniques for Pollination Biologists; University Press of Colorado: Niwot, CO, USA, 1993. [Google Scholar]
  46. Dormann, C.F.; Gruber, B.; Fründ, J. Introducing the bipartite package: Analysing ecological networks. R News 2008, 8, 8–11. [Google Scholar]
  47. Dormann, C.F.; Fründ, J.; Blüthgen, N.; Gruber, B. Indices, graphs and null models: Analyzing bipartite ecological networks. Open Ecol. J. 2009, 2, 7–24. [Google Scholar] [CrossRef]
  48. Blüthgen, N.; Menzel, F.; Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol. 2006, 6, 9. [Google Scholar] [CrossRef] [PubMed]
  49. Blüthgen, N.; Fründ, J.; Vázquez, D.P.; Menzel, F. What do interaction network metrics tell us about specialization and biological traits? Ecology 2008, 89, 3387–3399. [Google Scholar] [CrossRef] [PubMed]
  50. Patefield, W.M. Algorithm AS 159: An efficient method of generating random R × C tables with given row and column totals. J. R. Stat. Soc. C (Appl. Stat.) 1981, 30, 91–97. [Google Scholar] [CrossRef]
  51. Jordano, P.; Bascompte, J.; Olesen, J.M. Invariant properties in coevolutionary networks of plant–animal interactions. Ecol. Lett. 2003, 6, 69–81. [Google Scholar] [CrossRef]
  52. Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models (Version 0.4.1) [R Package]. Available online: https://cran.r-project.org/package=DHARMa (accessed on 24 June 2024).
  53. Lenth, R. Estimated Marginal Means, Aka Least-Squares Means (emmeans). Available online: https://cran.r-project.org/web/packages/emmeans/index.html (accessed on 24 June 2024).
  54. Teixeira, L.A.G.; Machado, I.C. Sistema de polinização e reprodução de Byrsonima sericea DC (Malpighiaceae). Acta Bot. Bras. 2000, 14, 347–357. [Google Scholar] [CrossRef]
  55. McCallum, K.P.; McDougall, F.O.; Seymour, R.S. A review of the energetics of pollination biology. J. Comp. Physiol. B 2013, 183, 867–876. [Google Scholar] [CrossRef] [PubMed]
  56. Classen, A.; Peters, M.K.; Kindeketa, W.J.; Appelhans, T.; Eardley, C.D.; Gikungu, M.W.; Hemp, A.; Nauss, T.; Steffan-Dewenter, I. Temperature versus resource constraints: Which factors determine bee diversity on Mount Kilimanjaro, Tanzania? Glob. Ecol. Biogeogr. 2015, 24, 642–652. [Google Scholar] [CrossRef]
  57. Li, D.; Belitz, M.; Campbell, L.; Guralnick, R. Extreme Weather Events Have Strong but Different Impacts on Plant and Insect Phenology. Nat. Clim. Change 2025, 15, 321–328. [Google Scholar] [CrossRef]
  58. Ohnishi, S.; Miyoshi, T.; Shirai, S. Low temperature stress at different flower developmental stages affects pollen development, pollination, and pod set in soybean. Environ. Exp. Bot. 2010, 69, 56–62. [Google Scholar] [CrossRef]
  59. Thakur, P.; Kumar, S.; Malik, J.A.; Berger, J.D.; Nayyar, H. Cold stress effects on reproductive development in grain crops: An overview. Environ. Exp. Bot. 2010, 67, 429–443. [Google Scholar] [CrossRef]
  60. Chiminazzo, M.A.; Bombo, A.B.; Charles-Dominique, T.; Fidelis, A. To protect or to hide: Why not both? An investigation of fire-related strategies in Cerrado woody species. Flora 2023, 306, 152350. [Google Scholar] [CrossRef]
  61. de Antonio, A.C.; Scalon, M.C.; Rossatto, D.R. Leaf Size and Thickness Are Related to Frost Damage in Ground Layer Species of Neotropical Savannas. Flora 2022, 292, 152208. [Google Scholar] [CrossRef]
  62. Pearce, R. Plant freezing and damage. Ann. Bot. 2001, 87, 417–424. [Google Scholar] [CrossRef]
  63. Muller, K.; O’Connor, T.G.; Henschel, J.R. Impact of a Severe Frost Event in 2014 on Woody Vegetation within the Nama-Karoo and Semi-Arid Savanna Biomes of South Africa. J. Arid Environ. 2016, 133, 112–121. [Google Scholar] [CrossRef]
  64. Whitecross, M.A.; Archibald, S.A.; Witkowski, E.T.F. Do Freeze Events Create a Demographic Bottleneck for Colophospermum mopane? S. Afr. J. Bot. 2012, 83, 9–18. [Google Scholar] [CrossRef]
  65. Pardee, G.L.; Inouye, D.W.; Irwin, R.E. Direct and indirect effects of episodic frost on plant growth and reproduction in subalpine wildflowers. Glob. Change Biol. 2018, 24, 848–857. [Google Scholar] [CrossRef]
  66. e Silva, S.C.O.; Souza, C.S.; de Araújo, W.S. Individual-based plant-visitor networks in Brazilian palm swamps under different dryness levels. Plant Ecol. 2024, 25, 543–554. [Google Scholar] [CrossRef]
  67. Roel, A.R.; Peruca, R.D.; Lima, F.V.O.; Cheung, K.C.; Neto, A.A.; Da Silva, L.V.; Soares, S. Diversity of Meliponini and Other Apiformes (Apidae sensu lato) in a Cerrado Fragment and Its Surroundings, Campo Grande, MS. Biota Neotropica 2019, 19, e20170333. [Google Scholar] [CrossRef]
  68. Giannini, T.C.; Garibaldi, L.A.; Acosta, A.L.; Silva, J.S.; Maia, K.P.; Saraiva, A.M.; Guimarães, P.R.; Kleinert, A.M.P.; Blenau, W. Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE 2015, 10, e0137198. [Google Scholar] [CrossRef]
  69. Bascompte, J.; Jordano, P.; Melián, C.J.; Olesen, J.M. The nested assembly of plant–animal mutualistic networks. Proc. Natl. Acad. Sci. USA 2003, 100, 9383–9387. [Google Scholar] [CrossRef] [PubMed]
  70. Burns, C.; Villalobos, S.; Vamosi, J.C. When less is more: Visitation by generalist pollinators can have neutral or negative effects on plant reproduction. Front. Ecol. Evol. 2022, 10, 1012809. [Google Scholar] [CrossRef]
  71. Tunes, P.; Alves, V.N.; Valentin-Silva, A.; Batalha, M.A.; Guimarães, E. Does fire affect the temporal pattern of trophic resource supply to pollinators and seed-dispersing frugivores in a Brazilian savanna community? Plant Ecol. 2017, 218, 345–357. [Google Scholar] [CrossRef]
  72. Potts, S.G.; Vulliamy, B.; Dafni, A.; Ne’eman, G.; Willmer, P.G. Linking bees and flowers: How do floral communities structure pollinator communities? Ecology 2003, 84, 2628–2642. [Google Scholar] [CrossRef]
  73. Barônio, G.J.; Souza, C.S.; Maruyama, P.K.; Raizer, J.; Sigrist, M.R.; Aoki, C. Natural fire does not affect the structure and beta diversity of plant–pollinator networks, but diminishes floral-visitor specialization in Cerrado. Flora 2021, 281, 151869. [Google Scholar] [CrossRef]
  74. Aguiar, L.M.S.; Diniz, U.M.; Bueno-Rocha, I.D.; Filomeno, L.R.A.; Aguiar-Machado, L.S.; Gomes, P.A.; Togni, P.H.B. Untangling Biodiversity Interactions: A Meta-Network on Pollination in Earth’s Most Diverse Tropical Savanna. Ecol. Evol. 2024, 14, e11094. [Google Scholar] [CrossRef]
  75. Brown, J.; York, A.; Christie, F.; McCarthy, M. Effects of Fire on Pollinators and Pollination. J. Appl. Ecol. 2016, 53, 313–322. [Google Scholar] [CrossRef]
  76. Carbone, M.; Aguilar, R. Fire frequency effects on soil and pollinators: What shapes sexual plant reproduction? Plant Ecol. 2017, 218, 1283–1297. [Google Scholar] [CrossRef]
  77. García, Y.; Castellanos, M.C.; Pausas, J.G. Fires can benefit plants by disrupting antagonistic interactions. Oecologia 2016, 182, 1165–1173. [Google Scholar] [CrossRef]
  78. Chiminazzo, M.A.; Charles-Dominique, T.; Andrade, R.S.; Bombo, A.B.; Fidelis, A. How Do Plants Survive in the Starving, Burning, and Hiding Vegetation Realms Generated by Novel Fire Regimes? Perspect. Plant Ecol. Evol. Syst. 2025, 68, 125885. [Google Scholar] [CrossRef]
  79. Aguiar, J.C.; Melo, G.A.R. Revision and phylogeny of the bee genus Paratetrapedia Moure, with description of a new genus from the Andean Cordillera (Hymenoptera, Apidae, Tapinotaspidini). Zool. J. Linn. Soc. 2011, 162, 351–442. [Google Scholar] [CrossRef]
  80. Jones, M.W.; Abatzoglou, J.T.; Veraverbeke, S.; Andela, N.; Lasslop, G.; Forkel, M.; Smith, A.J.P.; Burton, C.; Betts, R.A.; van der Werf, G.R.; et al. Global and Regional Trends and Drivers of Fire Under Climate Change. Rev. Geophys. 2022, 60, e2020RG000726. [Google Scholar] [CrossRef]
Figure 1. A typical shrub of Byrsonima intermedia (A), with flowers being visited by Centridini bees (Apidae): Epicharis bicolor (B) and Centris aenea (C).
Figure 1. A typical shrub of Byrsonima intermedia (A), with flowers being visited by Centridini bees (Apidae): Epicharis bicolor (B) and Centris aenea (C).
Plants 14 01977 g001
Figure 2. Effects of disturbances on B. intermedia two years after frost and fire (2023), after frost followed by fire (2021), and after frost only (2021). Variables analyzed: (a) floral visitor richness, (b) floral visitor abundance, (c) number of racemes, (d) oil volume, (e) number of floral buds, and (f) pollen quantity. Different letters indicate statistically significant differences between treatments. * p < 0.05; ** p < 0.01; *** p< 0.001.
Figure 2. Effects of disturbances on B. intermedia two years after frost and fire (2023), after frost followed by fire (2021), and after frost only (2021). Variables analyzed: (a) floral visitor richness, (b) floral visitor abundance, (c) number of racemes, (d) oil volume, (e) number of floral buds, and (f) pollen quantity. Different letters indicate statistically significant differences between treatments. * p < 0.05; ** p < 0.01; *** p< 0.001.
Plants 14 01977 g002
Figure 3. Frequency of floral visitors in B. intermediates two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021).
Figure 3. Frequency of floral visitors in B. intermediates two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021).
Plants 14 01977 g003
Figure 4. Difference in the number of fruits formed between pollination treatments (SSP—spontaneous self-pollination, SP—self-pollination, and NP—Natural pollination) two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021). The symbols *** and n.s. indicate significant and non-significant differences, respectively.
Figure 4. Difference in the number of fruits formed between pollination treatments (SSP—spontaneous self-pollination, SP—self-pollination, and NP—Natural pollination) two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021). The symbols *** and n.s. indicate significant and non-significant differences, respectively.
Plants 14 01977 g004
Figure 5. Interaction networks between individuals of Byrsonima intermedia and their floral visitors (a) after being subjected to frost only, (b) under the influence of frost and fire (2021), and (c) two years after frost and fire (2023). In the networks, the pink circles represent the floral visitors, and the gray squares signify the B. intermedia specimens.
Figure 5. Interaction networks between individuals of Byrsonima intermedia and their floral visitors (a) after being subjected to frost only, (b) under the influence of frost and fire (2021), and (c) two years after frost and fire (2023). In the networks, the pink circles represent the floral visitors, and the gray squares signify the B. intermedia specimens.
Plants 14 01977 g005
Figure 6. Average of the d’ specialization (a) and degree (b) values for floral visitors of Byrsonima intermedia two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021). The ANOVA did not show significant differences (p > 0.05). n.s. indicates non-significant differences.
Figure 6. Average of the d’ specialization (a) and degree (b) values for floral visitors of Byrsonima intermedia two years after frost and fire (2023), under the influence of frost and fire (2021), and under the influence of frost only (2021). The ANOVA did not show significant differences (p > 0.05). n.s. indicates non-significant differences.
Plants 14 01977 g006
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Porto, G.F.; Pezzonia, J.H.; Leite, L.J.C.; Sousa Santos, J.L.; Del-Claro, K. The Effects of Frost and Fire on the Traits, Resources, and Floral Visitors of a Cerrado Plant, and Their Impact on the Plant–Visitor Interaction Network and Fruit Formation. Plants 2025, 14, 1977. https://doi.org/10.3390/plants14131977

AMA Style

Porto GF, Pezzonia JH, Leite LJC, Sousa Santos JL, Del-Claro K. The Effects of Frost and Fire on the Traits, Resources, and Floral Visitors of a Cerrado Plant, and Their Impact on the Plant–Visitor Interaction Network and Fruit Formation. Plants. 2025; 14(13):1977. https://doi.org/10.3390/plants14131977

Chicago/Turabian Style

Porto, Gabriela Fraga, José Henrique Pezzonia, Ludimila Juliele Carvalho Leite, Jordanny Luiza Sousa Santos, and Kleber Del-Claro. 2025. "The Effects of Frost and Fire on the Traits, Resources, and Floral Visitors of a Cerrado Plant, and Their Impact on the Plant–Visitor Interaction Network and Fruit Formation" Plants 14, no. 13: 1977. https://doi.org/10.3390/plants14131977

APA Style

Porto, G. F., Pezzonia, J. H., Leite, L. J. C., Sousa Santos, J. L., & Del-Claro, K. (2025). The Effects of Frost and Fire on the Traits, Resources, and Floral Visitors of a Cerrado Plant, and Their Impact on the Plant–Visitor Interaction Network and Fruit Formation. Plants, 14(13), 1977. https://doi.org/10.3390/plants14131977

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Article metric data becomes available approximately 24 hours after publication online.
Back to TopTop