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Introduction

Seed removal is a crucial process for recruiting new individuals in plant communities ([27]). It involves the relocation of seeds from one site to another by animal dispersers and accumulators. This process integrates both seed predation and secondary dispersal ([32]), contributing to the colonization of new sites, facilitating ecological succession ([19]), and enhancing genetic flow ([38]). However, seeds are susceptible to biotic and abiotic factors, such as predation and fire ([41]). Notably, fire influences recruitment rates and the establishment of various species, thereby shaping the composition of the plant communities ([34]).

Fires rapidly eliminate plant cover, including propagules, and negatively affect the abundance of seed-dispersal fauna ([6]). Additionally, fires cause habitat fragmentation, which may increase local extinction rates of both plants and animals ([2]). Although fires often have detrimental effects on ecosystems, their impact varies depending on fire severity ([26]). High-severity fires cause drastic changes in large mammal abundance and plant cover, create clearings and edge areas, and reduce the availability of shelter and forage for animals ([10]). Conversely, moderate-severity fires have a lesser impact on soil nutrients (N, P, K, and Mg), temperature, pH, and moisture, facilitating the reestablishing of herbaceous cover ([11]). The abundance of fauna, short and medium-term post-fire changes in resource availability, and vegetation structural characteristics are all influenced by fire severity and the time elapsed since the fire occurrence ([22]).

The primary seed removers in temperate forests are birds, rodents, and invertebrates ([32]). In the temperate zones of central Veracruz, small rodents such as Peromyscus spp. and Reithrodontomys spp., and birds such as Junco phaeonotus (Wagler, 1831), Tardas migratorius, Carpodacus mexicanus (P. L. Statius Müller, 1776), play a significant role in seed removal, accounting for up to 90% of the seeds that fall to the ground ([14]). In Mexico, wildfires are the third leading cause of biodiversity loss at the national level ([7]). Given the global increase in fire frequency and intensity and the ecological importance of this temperate forest ecosystem, it is imperative to evaluate wildfire effects not only on species diversity but also on ecosystem processes like seed removal. This process integrates seed predation and secondary seed dispersal, and is vital for seedling establishment and recruitment, which are critical phases in the natural post-fire regeneration of temperate forests ([21]).

Understanding seed removal patterns after fire is crucial both ecologically and for forest management, given the pivotal role seeds play in forest regeneration and ecosystem resilience. Fires, especially under changing climate conditions, can disrupt natural seed dispersal and predation dynamics, which are fundamental for recovering plant populations and maintaining biodiversity ([17]). In this context, this study aimed to evaluate seed removal under different wildfire severities in a Mexican temperate forest. It is hypothesized that: (i) seed removal will be higher with moderate fire severity compared to both unburnt forest and high-severity fire areas, due to vegetation recovery that supports the presence of granivores ([5]); (ii) vertebrates (birds and rodents) will exhibit higher seed removal rates because vegetation recovery provides protection against predators and allows granivores to expand their spatial range in search of food ([12]); (iii) the time elapsed since fire occurrence will affect seed removal by granivores ([22]).

Materials and methods

Site description

The study was conducted in the reserve San Juan del Monte reserve, a protected area dedicated to recreational and environmental education (Fig. 1a). The reserve covers 609.62 hectares on the northern slope of the Cofre de Perote volcano in Las Vigas de Ramírez, Veracruz, Mexico (19° 37′ 53.4″ N, 97° 07′ 00.1″ W; altitude 2700 m a.s.l. -[39]).

Fig. 1 - (A) Reserve for recreation and environmental education in San Juan del Monte, Veracruz, Mexico. (B) Spatial distribution of fire severity in the San Juan de Monte Reserve, Veracruz, Mexico. Surveyed sites: (a) unburnt forest (green square) without any damage from the wildfire; (b) moderate severity (light blue circle) the fire was limited to the lower layer (grasses, herbs and small shrubs), with trees showing green-yellow crown fractions; and (c) high severity (blue diamond) the tree, shrub and herb layers were burned with a layer of white ash.

Results

From the total of 11.160 seeds used in this study, 55% were removed. Of these, 53% were removed in the control treatment, with 40% of these removals occurring in areas of moderate severity. The results showed significant effects of time since the fire, treatment type (control/exclusion), fire severity, and their interactions: time since fire × fire severity, time since fire × treatment, and fire severity × treatment, all effects were statistically significant (p).

Tab. 3 -Summary of the effects of time since fire, treatment (exclusion/control), fire severity (unburnt forest, moderate and high severity), and their two-way interactions on artificial seed removal. (df): degrees of freedom.

Effects χ2 df p-value
Time since fire (TSF) 42.2 6

Time and severity of the fire

Seed removal rates varied significantly over time. The highest rates of seed removal occurred in September and December 2019 and September 2020, while the lowest rate was observed in December 2020 (Pa). Moderate fire severity consistently showed the highest seed removal rates, particularly in September 2019 and June 2020 (X2 =115, df =8, Pb). By December 2020, seed removal rates in unburned forest were significantly higher compared to those in high-severity areas (Fig. 2b).

Fig. 2 - Post-fire seed removal in March 2019 in the San Juan del Monte reserve, Las Vigas, Veracruz, Mexico. (A): Seed removal between 3 and 21 months after fire. (B): Seed removal between 3 and 21 months after fire in unburnt forest (green), moderate (yellow), and high severity (red). Different letters indicate significant differences (p [ less than ] 0.05).

In the overall analysis, areas with moderate fire severity exhibited significantly higher seed removal rates compared to the areas of high severity. However, seed removal rates in unburned forest areas were intermediate and did not significantly differ from those in moderate and high-severity areas (P > 0.05 - Fig. 3).

Fig. 3 - Post-fire seed removal rate in forest with different fire severity. Different letters indicate significant differences (p [ less than ] 0.05).

Treatments and severity of the fire

The exclusion treatment reduced the seed removal rate by 46% compared to the control (χ2 = 99, df = 1, pa). This effect was observed in areas of moderate and high severity, but not in the unburnt forest (χ2 = 43, df = 2, pb).

Fig. 4 - (A) Vertebrate exclusion experimental treatment. (B) Experimental vertebrate exclusion treatment, control (open circle) and exclusion (solid circle), in unburnt forest, moderate and high severity. Different letters indicate significant differences (p [ less than ] 0.05).

Time with treatments

The interaction between the control/exclusion treatment and time since the fire showed significant differences only in June 2020, when the control treatment exhibited a higher seed removal rate than the exclusion treatment (χ2 = 122, df = 6, p).

Fig. 5 - Seed removal after the March 2019 fire in the San Juan del Monte reserve, Las Vigas, Veracruz, Mexico. Experimental vertebrate exclusion treatment between 3 and 21 months post-fire. Different letters indicate significant differences (p [ less than ] 0.05).

Years and severity of the fire

The mixed-effects model revealed significant differences between years (χ2 = 12, df = 1, p). Seed removal rates were higher in June and December 2019 compared to March-December 2020. However, no significant differences were found between unburned forest, moderate severity and high severity areas (p > 0.05).

Fig. 6 - Seed removal following the March 2019 fire in the San Juan del Monte reserve, Las Vigas, Veracruz, Mexico in 2019 and 2020. Different letters indicate significant differences (p [ less than ] 0.05).

Discussion

This study evaluated the effects of fire severity on seed removal activity and the potential removal of natural seeds through a vertebrate and invertebrate exclusion experiment. Results reveal that moderate fire severity significantly influenced seed removal patterns 21 months after the San Juan de Monte reserve wildfires. Differences in vegetation structure, fire severity, and the time since the fire all affected seed removal rates and the organisms involved. Vertebrates were particularly critical in seed removal in the moderate-severity areas during the first year after the wildfire.

Wildfires modify vegetation structure, which in turn impacts granivorous-mediated seed removal ([36]). Less affected areas may act as refugees for regeneration, influenced by variations in temperature, humidity, and disperser activity. This aligns with prediction (i) of this study, as rapid vegetation recovery in moderate-severity areas, dominated by P. aquilinum (fern) and Muhlenbergia macroura L. (grass), Arbutus xalapensis (Kunth), and Baccharis conferta (Kunth) Hitchc. (shrub)- created micro-habitats with specific conditions (temperature, light, and moisture) favorable to granivores like Reithrodontomys sp., Dendroica occidentalis (J. K. Townsend, 1837), Wilsonia pusilla (A. Wilson, 1811), and Turdus grayi (Bonaparte, 1838), among others ([13], [31]).

Greater seed removal in areas affected by moderate fire severity can significantly influence the initial regeneration and successional trajectories of the forest. This process favors less-consumed species, enhances biodiversity, and accelerates the return to a mature forest state ([10]). While low-severity fires generally do not cause substantial changes to flora and fauna, enabling complete seed removal. Moderate fire severity negatively impacts large mammals, soil temperature, and pH levels. However, it also increases the availability of key nutrients (e.g., phosphorus, potassium, and magnesium) while preserving seed trees and supporting small mammals. These conditions allow for seed removal, seedling recruitment, and the continuation of forest regeneration and successional processes. On the other hand, high-severity fires severely disrupt seed trees, seed banks, organic matter, soil moisture, depth, and nutrient availability, thereby impairing seed availability, seed removal, and seedling establishment ([11]).

These findings are consistent with other studies conducted in temperate forests, which indicate that vertebrates, particularly birds and rodents, are the primary agents of seed removal ([5], [12]). Granivorous rodents display foraging patterns closely linked to vegetation compositions ([5], [12]). For example, Peromyscus melanotis and Mus musculusLinnaeus exhibit foraging behaviors influenced by vegetation composition, moving between fragments based on disturbance levels and resource availability ([13], [15]). Dense vegetation, such as that found in moderate-severity areas, provides cover that reduces predation risk, while open areas (e.g., high-severity sites) expose granivores to predators like eagles, owls, and snakes ([3])

Granivorous birds also contribute significantly to seed removal, with their mobility and use of vegetation as perch sites enhancing their foraging efficiency ([40]). For example, the ability to fly enables birds to move rapidly between different forage zones and cover greater distances by utilizing foliage profiles that serve as perch sites ([15]). In this study, moderate-severity sites were characterized by trees with green-yellow canopies and herbaceous vegetation. In contrast, high-severity sites were destroyed and characterized by completely charred trees, shrubs, and herbaceous vegetation. Additionally, Flores-Peredo ([13]) reported in the same study area that granivorous birds, such as Junco phaeonotus (Wagler, 1831), Tardas migratorius, Carpodacus mexicanus (P. L. Statius Müller, 1776), Spizella passerine (Bechstein, 1798), and Poocetes gramineus, play a fundamental role in seed removal and dispersal, primarily during the day. This observation could explain the higher seed removal values found in moderate-severity areas.

The time elapsed since the fire began influenced seed removal, supporting prediction (iii). Overall, the seed removal rate was higher in 2019 (September). Post-fire fire changes in plant coverage lead to decreased food resources and altered activity patterns as birds must forage at a greater distance from their nests ([33]). Conversely, when serotine cones open and release seeds due to the fire effect, the presence and abundance of granivorous birds are favored. In contrast, the nectarivorous, insectivorous, and frugivorous birds decrease ([25]). It was further observed that the recovery and restructuring of the plant community mediates the recovery of granivorous communities and their levels of seed removal. Factors such as understory plant density, herbaceous coverage, and number of mammals synergistically influenced resource availability within the ecosystem; these dynamics contribute to the lower seed removal observed in 2020 ([37]).

Seed removal is a critical ecological process influencing plant regeneration and ecosystem resilience. However, this process is increasingly vulnerable to the combined pressures of climate change and shifting fire regimes ([35]). These global phenomena alter the interactions between plants and animals, mediating seed dispersal and predation, with profound implications for forest dynamics, biodiversity, and ecosystem recovery. The interplay between climate change, fire regimes, and seed removal is a complex and pressing issue. These forces disrupt the delicate balance of ecosystems, modifying habitats and altering the behavior, distribution, and abundance of species involved in seed removal. Such disruptions hinder forest regeneration and threaten biodiversity ([17]). Addressing these challenges requires innovative research and conservation strategies to prevent forest resilience and the vital ecological processes that forests support.

Conclusions

Our results demonstrated higher seed removal by vertebrates (birds and rodents) in areas affected by moderate fire severity. These findings highlight the significant role of moderate fire severity in shaping granivorous communities and influencing seed removal patterns in the temperate forest of Veracruz, Mexico. Artificial seeds proved a valuable methodological approach, particularly in scenarios where fruiting seasons are disrupted due to the severity and intensity of fires, or where there is limited knowledge of local fruiting plant species. While the absence of natural seeds somewhat constrains this method, it offers a broader understanding of ecosystem functioning patterns by minimizing seed preference and size biases. This approach provides critical insights into the ecological processes that drive forest recovery and resilience in the face of environmental disturbances.

Author Contributions

DACZ: Conceptualization, Data curation, Formal analysis, Writing - original draft. JCI, JFAM, JDCZ: Supervision, Writing - review and editing. JLAV, LABG, SAS, JFDN: Supervision, Writing - review and editing. DACZ: Funding acquisition, Project administration. DACZ: Writing - review and editing.

Funding

This work was supported by the Veracruz Council for Scientific Research and Technological Development (COVEICYDET-8.8 2SO 2020) and a CONAHCYT grant awarded to DACZ (609138).

Data Availability Statement

The data presented in this study are available upon request. Due to privacy concerns, they are not publicly available.

Acknowledgements

We thank Ismael Guzman for their invaluable assistance in field campaigns and sorting samples. Diana Ramírez provided us with remote sensing maps of the affected area. A special thanks to SEDEMA-Xalapa for the logistic support and lodging facilities in the SJM Protected Area.

Declaration of Interest

The authors declare that they have no known competing financial interests or personal relationships that could influence the work reported in this paper.

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© 2025. This work is licensed under https://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.

Abstract

Wildfires are critical to the ecological dynamics of communities in temperate forests. However, their frequency and severity have increased significantly in recent decades due to human activities, negatively affecting flora, fauna, and ecosystem processes. Among the primary interactions for the natural regeneration of forests is seed removal, which promotes secondary seed dispersal and predation. This study evaluated artificial seed removal under different wildfire severities in a pine forest on the eastern edge of the Trans-Mexican Volcanic Belt. An experiment of differential exclusion of vertebrates and invertebrates was carried out, considering two treatments: totally exposed seeds and seeds with exclusion of vertebrates in the unburnt forest, moderate and high severity fire. Our results showed a higher seed removal by vertebrates (birds and rodents) in the wildfire moderate severity treatment and in the time elapsed since wildfire occurrence; however, excluding vertebrates decreased the seed removal rate after the fire. Therefore, moderate-severity sites are an important factor in the communities of granivores that influence seed removal patterns in the temperate forest of Veracruz, Mexico. The findings underscore the importance of considering fire severity gradients in forest management strategies, particularly in fire-adapted ecosystems. As climate change alters fire regimes worldwide, understanding how different fire severities affect ecological interactions such as granivory is essential for promoting forest resilience and biodiversity.

Details

Title
Moderate wildfire severity favors seed removal by granivores in a Mexican pine forest
Author
Cadena-Zamudio, Daniel A  VIAFID ORCID Logo  ; Cadena-Iñiguez, Jorge  VIAFID ORCID Logo  ; Aguirre-Medina, Juan F  VIAFID ORCID Logo  ; Cadena-Zamudio, Jorge D  VIAFID ORCID Logo  ; Arispe-Vázquez, José L  VIAFID ORCID Logo  ; Barrera-Guzmán, Luis A  VIAFID ORCID Logo  ; Ayvar-Serna, Sergio  VIAFID ORCID Logo  ; Díaz-Nájera, José F  VIAFID ORCID Logo 
Pages
121-127
Section
Research Articles
Publication year
2025
Publication date
2025
Publisher
The Italian Society of Silviculture and Forest Ecology (SISEF)
ISSN
19717458
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.3832/ifor4741-018
ProQuest document ID
3215003650
Copyright
© 2025. This work is licensed under https://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.