Next Article in Journal
Hydrogen Peroxide Imbibition Following Cold Stratification Promotes Seed Germination Rate and Uniformity in Peach cv. GF305
Previous Article in Journal
Potassium Nitrate Treatment Is Associated with Modulation of Seed Water Uptake, Antioxidative Metabolism and Phytohormone Levels of Pea Seedlings
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Seeds
Volume 1
Issue 1
10.3390/seeds1010003
seeds-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Biotic and Abiotic Interactions Shape Seed Germination of a Fire-Prone Species

by
Marcilio Fagundes
1,
Henrique Tadeu dos Santos
1,
Pablo Cuevas-Reyes
2 and
Tatiana Cornelissen
3,*
1
Programa de Pós-Graduação em Biodiversidade e Uso dos Recursos Naturais, Universidade Estadual de Montes Claros, Montes Claros 39401-089, MG, Brazil
2
Laboratorio de Ecología de Interacciones Bióticas, Universidad Michoacana de San Nicolás de Hidalgo, Morelia C.P. 58030, Michoacán, Mexico
3
Centro de Síntese Ecológica e Conservação, Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Belo Horizonte 30150-260, MG, Brazil
*
Author to whom correspondence should be addressed.
Seeds 2022, 1(1), 16-27; https://doi.org/10.3390/seeds1010003
Submission received: 2 November 2021 / Revised: 26 November 2021 / Accepted: 7 December 2021 / Published: 9 December 2021
Browse Figures
Versions Notes

Abstract

:
Both biotic and abiotic environmental filters drive the occurrence, distribution, and persistence of plant species. Amongst drivers that influence the distribution of plants in harsh environments, seed predation and temperature are particularly important in habitats that are prone to fire. In this study, we highlight the combined effects of predation and high temperature simulating fire to understand its effects on the germination percentage and germination speed of the fire prone species Copaifera oblongifolia. Groups of seeds attacked by the beetles Rhinochenus brevicollis and Apion sp., seeds manipulated by the ant Atta laevigata, and seeds left intact were put to germinate in controlled environments. To evaluate the effects of abiotic filters, seeds with intact elaiosomes and seeds with elaiosomes removed by the ant Atta laevigata were exposed to temperatures of 27, 60, 100, and 200 °C. The results showed that only 2.8% of the seeds attacked by R. brevicollis germinated. Seeds attacked by Apion sp. germinated faster, followed by seeds with their elaiosomes removed and seeds with intact elaiosomes. Seeds attacked by Apion sp. had the lowest germination percentage. The temperature of 200 °C killed seed embryos, whereas seeds exposed to 100 °C took longer to germinate than seeds exposed to other temperatures. Our results reveal that fire intensity and seed damage are important drivers of seed germination of C. oblongifolia.

1. Introduction

Biotic and abiotic environmental filters are able to regulate the recruitment of different plant species and shape the organization of natural communities [1,2,3,4]. However, some seed traits allow these environmental filters to be overcome, giving them a high capacity to colonize and be established in specific habitats [5,6]. Identifying the mechanisms that regulate seedling recruitment in different habitats is key to understanding the patterns of distribution and abundance of plant species and establish strategies for the conservation and management of terrestrial ecosystems [7]. This is particularly important in an anthropized world characterized by global and accelerated changes in abiotic factors such as temperature and fire regimes, with serious impacts on plant and animal communities [8].
One of the main biotic filters that determine the seedling recruitment success of many plant species in natural communities is seed consumption by different organisms [9,10,11,12,13]. The relationship between herbivores and seeds can range from negative [14,15,16] to neutral [13,17] to positive [18,19]. Some insects lay their eggs directly on fruits and the development of immature individuals take place inside the seeds [20]. These insects, which feed on the endosperm and embryo (often causing their death), act as true predators [12,21]. In other cases, insects partially consume the seeds without causing direct damage to the embryo, producing cracks in the tegument that can facilitate the imbibition and accelerate seed germination [13,19]. On the other hand, endosperm consumption can affect the availability of resources for the seed embryo and negatively affect germination and seedling establishment [22,23]. Finally, some organisms can also feed on the external seed structures without causing apparent damage to the embryo [24,25,26].
In fact, many plant species produce seeds with an appendage (elaiosome) rich in nutrients such as lipids, carbohydrates, proteins, and vitamins [27,28] that are attractive food resources for many animal species, including ants, birds, and small primates [12,24]. For example, it has been reported that the dispersion of seeds and fruits in more than 3000 plant species belonging to 80 families of plants is made by ants [29]. In this mutualistic relationship, the elaiosomes are key structures as ants collect seeds to use elaiosomes as a food resource [24,28]. Additionally, the dispersion of these propagules to distant habitats from the parental plants can promote predation-free spaces, favoring the recruitment of new seedlings [25,27,30,31]. Furthermore, some studies suggest that the manipulation of seeds by ants during elaiosome removal can cause cracks in the seed coat, which facilitate imbibition and accelerate germination [32,33,34]. Thus, myrmecochory (i.e., seed dispersal by ants) can positively affect seed germination, seedling survival, and plant community dynamics [35,36].
Many plant species of fire-prone ecosystems produce seeds that are adapted to resist high temperatures as a result of occasional fires [37,38,39,40]. Previous studies suggest that high temperatures can break seed dormancy, favoring the germination of fire-adapted species [37,41,42,43,44]. However, seed responses to different temperatures can vary within and between plant species [42,44,45]. For example, in Mimosa leiocephala, seed germination was positively related with the increase of temperature, whereas germination rates and seed viability of Mimosa pteridifolia and Harpalyce sp. were negatively associated to high temperatures [44]. Because the intensity and frequency of fires depends on the levels of drought and temperature in a particular habitat [46], it is possible to expect important consequences for the plant communities prone or adapted to fire. Therefore, understanding the effects of fire on expected future climate change scenarios is crucial to assess how species will respond to altered climatic conditions, as well as changes in the availability of mutualistic and antagonistic interacting species.
The Cerrado is the second largest biome in Brazil and represents one of the world’s biodiversity hotspots [47]. This biome harbors about 13,400 plant species whose phenology is related to local climatic seasonality and soil quality [39,48,49]. The vegetation of the Cerrado has its own characteristics, which probably arose in response to local stressors, such as fire and herbivory [39,50]. As such, many plants in the Brazilian Cerrado produce seeds with adaptations to resist high temperatures resulting from wild fires [40] or seeds with nourishing appendages that favor dispersal and recruitment [51,52]. Furthermore, leaf cutting ants belonging to Atta and Acromyrmex genera are the principal defoliating agents of Cerrado vegetation [53]. These ant species can also collect and transport seeds of myrmecocoric plants to their nests, impacting seed germination of many Cerrado plants [54,55] and influencing ecosystem services.
Copaifera oblongifolia Mart. ex Hayne (Fabaceae: Caesalpinioideae) is a shrub species that occurs in the central region of the Brazilian Cerrado. The seeds of C. oblongifolia have a hard coat and are partially covered by a fleshy, lipid-rich elaiosome [56]. The shrubs occur in dense patches and often invade pastures and cultivated areas, becoming dominant and negatively affecting the productivity of agricultural systems [57]. Therefore, characterizing the role of local environmental filters in the variation of seed germination success of this plant species is essential to understand its population dynamics and its invasiveness potential. In this study, we evaluated the effects of both biotic and abiotic environmental filters on seed germination of C. oblongifolia. The specific questions addressed were: (i) is seed germination of C. oblongifolia affected by the variation of the different insect damage levels? and (ii) how does seed germination of C. oblongifolia respond to thermal variation?

2. Materials and Methods

2.1. Study System

Copaifera oblongifolia popularly known in Brazil as pau d’olinho, is a shrub growing up to 2.5 m [56]. It is endemic to the Cerrado areas of central Brazil, occurring in open areas and disturbed environments such as abandoned pastures, roadsides, and edges of Cerrado fragments. Flowering occurs from February to May and fruits ripen from August to October. When the fruit is opened, an ellipsoid, black, and shiny seed, partially covered by a yellow–orange fat-rich elaiosome, is exposed. This propagule represents a food resource for birds, small marmosets, and different groups of insects [57,58].
Among insects, Rhinochenus brevicollis Chevrolat (Curculionidae: Cryptorhynchinae) represents the main insect predator of C. oblongifolia seeds. Females lay their eggs directly on the fruit in initial stages of seed formation and the larvae develop inside the seeds, feeding on the cotyledons and often causing damage to the embryo [12]. Different species of Apion (Brentidae: Apioninae) also attack the seeds of C. oblongifolia. This group of insects feeds upon the outermost parts of the seeds, such as the seed coat and the surface of the cotyledons [59,60]. Ants of the genus Atta also collect these seeds and use their elaiosomes to cultivate fungi inside their nests [61]. This ant species removes seeds from plants and transports them to the nest. Once the elaiosome is removed, the ants discard the seeds without elaiosomes onto the loose soil around the anthill [62].

2.2. Obtaining Seeds

Seeds were collected from a population of C. oblongifolia located in an abandoned pasture (−17.215, −44.414 UTM) in a rural area of the municipality of Jequitaí, northern Minas Gerais State, Brazil. This region has a semi-arid climate with well-defined dry and rainy seasons. The average annual temperature is 23 °C, and precipitation is around 1000 mm/year [63]. The region is located in a transition zone between the Cerrado and Caatinga biomes, evidencing a mosaic of phytophysiognomies such as campo rupestre, cerrado sensu stricto, semi-deciduous seasonal forests, and riparian forests [64].
Prior to the dispersion of fruits (August 2018), 40 reproductive-stage individuals of C. oblongifolia were identified and tagged in the field. These individuals were periodically monitored to ensure the seed collection only from the open fruits or in the process of opening. We collected at least 30 fruits with seeds for each plant sampled for the two germination experiments. All fruits collected were taken to the laboratory and stored individually in test tubes for a period of 30 days for the emergence of adult insects, which allowed the identification of predators and the type of damage caused to the seeds. The seeds were subsequently grouped into three classes of damage: (i) healthy seeds (intact seeds with no evidence of damage), (ii) seeds attacked by R. brevicollis, and (iii) seeds attacked by Apion sp. We evaluated a total of 70 seeds predated by R. brevicollis, 70 seeds attacked by Apion sp., and 350 intact seeds. In addition to collecting fruits from the plants, six nests of Atta laevigata Smith. (Hymenoptera: Formicidae) were identified in the study area to collect seeds manipulated by individuals of this ant species. We collected 350 non-elaiosome seeds (about 60 seeds per A. laevigata nest) located on the soil mounds of the six A. laevigata nests to be used in two germination bioassays.

2.3. Bioassay 1: Effects of Predation on Seed Germination

To evaluate the effects of different levels of seed predation by different insects (Figure 1) on the germination of C. oblongifolia seeds, 70 seeds from each of the four treatments (seeds without predation with intact elaiosome; seeds manipulated by A. laevigata without elaiosome; seeds attacked by Apion sp.; and seeds attacked by R. brevicollis) were placed to germinate in individual cells of four Styrofoam trays (one tray per treatment). This experimental design assumes that each seed represents a statistically independent experimental unit and allows comparing germination percentages among treatments using the binomial distribution [6,65]. Approximately 3.0 g of sterile vermiculite was used as the germination substrate in each tray cell. The four trays were placed to germinate in a germination chamber with controlled photoperiod, temperature, and light intensity (12 h/light at 28 °C and 12 h/dark at 28 °C, 47.5 µmol.m.−2s−1 irradiation). The humidity of the germination substrate was kept constant by the daily addition of 3 mL of distilled water to each germination cell. Seeds were monitored daily to determine germination percentage and the time required for germination. Seeds were considered germinated when they presented primary root protrusion.
Generalized linear models (GLM) were used, followed by analysis of variance (ANOVA) to assess whether germination percentage varied among predation treatments. In this model, seed treatments were used as the explanatory variable, and seed germination (0 or 1) was used as the response variable, with a binomial distribution (corrected for quasibinomial). Survival analysis with the Weibull distribution was used to test whether mean germination time differed among seed treatments [66]. In this analysis, seed treatments were used as the explanatory variable and seed germination time as the response variable. Residual analyses were performed to check the suitability of all models. After ANOVA tests, differences among treatments were assessed using contrast analysis, grouping levels that were similar and separating levels that were statistically different. These analyses were performed using R software version 3.5.0 [67].

2.4. Bioassay 2: Effects of Heating and Manipulation by Atta Laevigata on Seed Germination

To evaluate the interactions between abiotic and biotic factors on seed germination, an initial batch of 560 seeds of C. oblongifolia was divided into two groups. The first group consisted of 280 intact seeds (elaiosome present) collected directly from the plants. The second group consisted of 280 seeds manipulated by Atta laevigata (elaiosome removed) that were collected near the loose soil of A. laevigata nests. Each group of seeds was evenly divided into four subgroups of 70 seeds and subjected to four different heat treatments: (27, 60, 100, and 200 °C) using a heating oven (QUIMIS Q314M) to simulate the effects of seed exposure to different intensities of fire [68]. Thus, the oven was preheated to the desired temperature (27, 60, 100, or 200 °C) and immediately turned off, and 70 seeds from each treatment (seeds manipulated by ants and seeds with elaiosome) were placed inside. The oven door remained open until room temperature was reached, at which point the seeds were removed from the oven. This procedure was repeated for the four heating treatments. After fire simulation, each seed of the eight treatments were placed in individual cells of eight Styrofoam trays and placed to germinate in a B.O.D., as described in the previous bioassay.
GLMs, followed by ANOVA tests were used to assess whether germination percentage varied between heating and seed manipulation treatments. In this model, heating, seed manipulation by ants, and the interaction between them were used as explanatory variables and seed germination (0 or 1) as the response variable, with the binomial distribution (corrected for quasibinomial). The effects of different temperatures and of seed manipulation by A. laevigata on seed germination time were evaluated by survival analysis using the Weibull distribution [66]. In this analysis, treatments (heating and seed manipulation by ants) were used as the explanatory variables, and seed germination time was considered as the response variable. Residual analyses were performed to check the suitability of all models. Contrast analyses were used to group levels that were similar and separate levels that were statistically different when ANOVA indicated significant differences among treatments. These analyses were performed using R software version 3.5.0 [67].

3. Results

3.1. Bioassay 1

Our results showed that the percentage of seed germination of C. oblongifolia seeds significantly varied among the different treatments of predation (Table 1). Contrast analysis showed that germination percentage did not vary between non-manipulated seeds (with elaiosome) and seeds manipulated by ants. However, seeds attacked by Apion sp. had a lower germination percentage than intact seeds or seeds manipulated by ants. Only two seeds attacked by R. brevicollis germinated (Figure 2).
The time required for germination of C. oblongifolia seeds varied among the different predation treatments (Table 1). Particularly, contrast analysis indicated that seed germination time varied among the three treatments analyzed, with seeds attacked by Apion sp., ants and unmanipulated seeds requiring, respectively, 11.2 ± 0.5, 16.9 ± 0.8, and 22.3 ± 0.9 days for germination of 50% of seeds (Figure 3). Finally, it is important to emphasize that only two seeds (2.8%) attacked by R. brevicollis germinated, and this treatment was not included in the survival analyses.

3.2. Bioassay 2

Initially, it should be emphasized that no seed of the 200 °C treatment germinated, and this treatment was excluded from statistical analysis. The seed germination percentage of C. oblongifolia did not vary as a function of temperature (i.e., temperatures of 27, 60, and 100 °C), seed manipulation by ants, and their interaction (Table 2, Figure 4).
The time required for the germination of C. oblongifolia seeds varied statistically among treatments involving manipulation by ants, temperature, and their interaction (Table 2). Contrast analysis showed that seeds subjected to the 100 °C treatment had a slower germination speed than the seeds subjected to the 27 and 60 °C treatments. Seeds manipulated by ants required less time to germinate than non-manipulated seeds. However, a statistically significant interaction showed that the effect of seed manipulation by ants was evident only at the temperature of 27 °C, when seed manipulation reduced germination time by 5.3 days compared to non-manipulated seeds (Figure 5).

4. Discussion

The results of the bioassay of insect damage to seeds showed that seed predation by R. brevicollis drastically reduced the probability of germination of C. oblongifolia seeds. Females of these beetles lay their eggs inside the newly formed seeds where the immature insects complete their development, feeding on reserves and the embryo [12]. Seed predation by this beetle can reach 30% for seeds produced by C. langsdorffii [10]. If this same pattern occurs with C. oblongifolia, R. brevicollis can be responsible for the death of a high proportion of seeds produced by C. oblongifolia under natural conditions.
Seeds attacked by Apion sp. had a significant and strong reduction in germination compared to seeds of the control group. These beetles are external predators that feed on only part of the seeds, and, in many cases, do not cause death to the embryo. Despite the negative effect on germination percentage, seeds attacked by Apion sp. exhibited higher germination speed than seeds of the control treatment. This difference is probably related to cracks that these beetles causes in the seed pods, which increase imbibition speed [13]. Rapid germination is an efficient strategy for colonizing less competitive habitats, such as those in the early stages of succession [69]. In this scenario, seeds attacked by Apion sp. that still retain their elaiosomes could be expected to be dispersed by other animals and obtain some germination success away from the mother plants.
Our results showed that seeds manipulated by ants had a higher germination speed than non-manipulated seeds with elaiosomes intact. When ants transport seeds and remove the elaiosome, they cause wear to the integument, which promotes greater water absorption and accelerates germination [33,70]. Increased water absorption capacity is especially important under natural conditions because it allows a better use of a resource that is often scarce in seasonal environments such as the Brazilian Cerrado. Decreased germination time can also limit the amount of time seeds are in contact with pathogenic microorganisms in the soil, thereby increasing their germination probability. Therefore, seed transport and manipulation by ants may positively affect the dispersal and colonization of new habitats by C. oblongifolia. However, the directional dispersion performed by A. laevigata (i.e., from the plant towards the ant hill) could help to explain the clustered distribution of C. oblongifolia often observed in the field.
The germination percentage for seeds manipulated by the ant A. laevigata did not differ from that for non-manipulated seeds (with elaiosomes). Previous studies have shown that seed manipulation by ants can positively [35,36,71] or negatively [55] affect the probability of seed germination. Different mechanisms have been suggested to explain this variation. For instance, ants can release antibiotic substances during seed manipulation that protect the seeds against microorganism infection, thereby increasing the germination percentage [71]. On the other hand, removal of the elaiosomes by ants can expose the seed micropyle, which represents a window for microorganisms to enter the interior of the seed and cause its death [55,72]. Our experiment was conducted under aseptic conditions, and no fungal growth was observed in the seeds. Thus, variation in germination related to the action of microorganisms between treatments did not interfere with the germination results of C. oblongifolia. Furthermore, it is also important to emphasize that although some studies suggest elaiosomes can produce substances that inhibit seed germination, our results do not support the evidence that these structures can act as a germination inhibitor of C. oblongifolia seeds.
The results of the heating bioassay showed that seeds of C. oblongifolia did not resist high temperatures, as no seed submitted to the highest temperature of 200 °C germinated. Generally, fire in the Cerrado is characterized by high frequency (occurring every 3–4 years), superficial occurrence, and low intensity, with rapid consumption of the dry biomass of the subshrub stratum [68,73]. Soil surface temperatures during fires in the Cerrado range from 74 to 768 °C [74], but temperatures of the soil layers immediately below the surface do not exceed 80 °C [68]. Thus, considering that the germinability of C. oblongifolia did not vary among temperatures from 27 to 100 °C, and that this species is restricted to the Cerrado, it is reasonable to consider that seeds of C. oblongifolia have resistance to moderate temperatures. These results also indicate that fire does not directly stimulate the germination of these seeds. However, it has been observed that gases released during fires, such as ethylene and ammonia, can stimulate the germination of species of fire-prone ecosystems [41,75,76,77]. Thus, further studies testing this hypothesis of the indirect effects of fire on the germination of C. oblongifolia are still needed.
Moderately high temperatures (100 °C) slowed the germination rate. Seeds exposed to this temperature are likely to have a reduction in moisture content. Reduced moisture inhibits the production of gibberellin [78], which is important in the process of breaking seed dormancy [79,80]. Furthermore, we observed that, despite heating, seeds manipulated by ants had a higher germination speed. Thus, seeds manipulated by ants, even when subjected to fire, must absorb water more quickly and have a higher germination speed. Elaiosomes are lipid-rich appendices that partially involve the seed aril [55] and, therefore, could act as a thermal insulator, protecting the embryo from thermal oscillations. However, seeds manipulated and not manipulated by ants differed in the time for germination only at the temperature of 27 °C. These results, associated to fact that germination percentage was not affected by moderate temperatures, suggest that the elaiosome did not protect seeds of C. oblongifolia against thermal fluctuations. Thus, the resistance of the C. oblongifolia seeds to fire would be mainly associated with the hardness of the seed tegument.
Finally, our results show evidence that ants do not influence seed germinability, whereas beetle damage has serious negative consequence on seed germination of C. oblongifolia. We also highlight that C. oblongifolia seeds have a high tolerance to moderate temperatures typical of Cerrado environment. Leaf cutting ants and low intensity fire are two important biotic and abiotic filters capable of driving community organization in Cerrado areas, and we suggest that C. oblongifolia seed is adapted to overcome these environmental filters. Thus, these seed traits should be considered in future management strategies of this plant species in Cerrado areas.

Author Contributions

M.F. and P.C.-R. designed the study; H.T.d.S. collected data and performed experiments; and all authors contributed equally to data analysis, manuscript preparation, and editing. T.C. is the corresponding author. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially supported by FAPEMIG (APQ01375/21), CNPq (grant 313007/2020-9) and CAPES (financial code 001).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data and R coding are available upon request to the corresponding author.

Acknowledgments

The authors thank an anonymous reviewer that provided constructive feedback regarding experiments and analyses, which improved manuscript quality. We also acknowledge support from the Graduate Programs of Ecology PPG-BURN and ECMVS-UFMG.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Myers, J.A.; Harms, K.E. Seed arrival, ecological filters, and plant species richness: A meta-analysis. Ecol. Lett. 2009, 12, 1250–1260. [Google Scholar] [CrossRef]
  2. Vellend, M. Conceptual Synthesis in Community Ecology. Q. Rev. Biol. 2010, 85, 183–206. [Google Scholar] [CrossRef] [Green Version]
  3. Grman, E.; Bassett, T.; Zirbel, C.R.; Brudvig, L.A. Dispersal and establishment filters influence the assembly of restored prairie plant communities. Restor. Ecol. 2015, 23, 892–899. [Google Scholar] [CrossRef]
  4. Harms, K.E.; Gagnon, P.R.; Passmore, H.A.; Myers, J.A.; Platt, W.J. Groundcover community assembly in high-diversity pine savannas: Seed arrival and fire-generated environmental filtering. Ecosphere 2017, 8, e01716. [Google Scholar] [CrossRef]
  5. Keddy, P.A. Assembly and response rules: Two goals for predictive community ecology. J. Veg. Sci. 1992, 3, 157–164. [Google Scholar] [CrossRef] [Green Version]
  6. Souza, M.L.; Fagundes, M. Seed Size as Key Factor in Germination and Seedling Development of Copaifera langsdorffii (Fabaceae). Am. J. Plant Sci. 2014, 5, 2566–2573. [Google Scholar] [CrossRef] [Green Version]
  7. Zida, D.; Sanou, L.; Diawara, S.; Savadogo, P.; Thiombiano, A. Herbaceous seeds dominates the soil seed bank after long-term prescribed fire, grazing and selective tree cutting in savanna-woodlands of West Africa. Acta Oecologica 2020, 108, 103607. [Google Scholar] [CrossRef]
  8. Wagner, D.L.; Grames, E.M.; Forister, M.L.; Berenbaum, M.R.; Stopak, D. Insect decline in the Anthropocene: Death by a thousand cuts. Proc. Natl. Acad. Sci. USA 2021, 118, e2023989118. [Google Scholar] [CrossRef] [PubMed]
  9. Ramírez, N.; Traveset, A. Predispersal seed-predation by insects in the Venezuelan Central Plain: Overall patterns and traits that influence its biology and taxonomic groups. Perspect. Plant Ecol. Evol. Syst. 2010, 12, 193–209. [Google Scholar] [CrossRef]
  10. Fagundes, M.; Maia, M.L.; Queiroz, A.; Fernandes, G.W.; Costa, F.V. Seed predation of Copaifera langsdorffii Desf. (Fabaceae: Caesalpinioideae) by Rhinochenus brevicollis Chevrolat (Coleoptera: Curculionidae) in a brazilian Cerrado fragment. Ecol. Austral 2013, 23, 218–221. [Google Scholar] [CrossRef]
  11. Xu, Y.; Shen, Z.; Li, D.; Guo, Q. Pre-Dispersal Seed Predation in a Species-Rich Forest Community: Patterns and the Interplay with Determinants. PLoS ONE 2015, 10, e0143040. [Google Scholar] [CrossRef]
  12. Souza, M.L.; Fagundes, M. Seed predation of Copaifera langsdorffii (Fabaceae): A tropical tree with supra-annual fruiting. Plant Species Biol. 2016, 32, 66–73. [Google Scholar] [CrossRef]
  13. Han, Y.J.; Baskin, J.M.; Tan, D.Y.; Baskin, C.C.; Wu, M.Y. Effects of predispersal insect seed predation on the early life history stages of a rare cold sand-desert legume. Sci. Rep. 2018, 8, 3240. [Google Scholar] [CrossRef] [PubMed]
  14. Fukumoto, H.; Kajimura, H. Effects of insect predation on hypocotyl survival and germination success of mature Quercus variabilis acorns. J. For. Res. 2000, 5, 31–34. [Google Scholar] [CrossRef]
  15. Blubaugh, C.K.; Kaplan, I. Invertebrate Seed Predators Reduce Weed Emergence Following Seed Rain. Weed Sci. 2016, 64, 80–86. [Google Scholar] [CrossRef]
  16. De Sousa-Lopes, B.; Alves-Da-Silva, N.; Ribeiro-Costa, C.S.; Del-Claro, K. Temporal distribution, seed damage and notes on the natural history of Acanthoscelides quadridentatus and Acanthoscelides winderi (Coleoptera: Chrysomelidae: Bruchinae) on their host plant, Mimosa setosa var. paludosa (Fabaceae: Mimosoideae), in the Brazilian Cerrado. J. Nat. Hist. 2019, 53, 611–623. [Google Scholar] [CrossRef]
  17. Vallejo-Marín, M.; Dominguez, C.; Dirzo, R. Simulated seed predation reveals a variety of germination responses of neotropical rain forest species. Am. J. Bot. 2006, 93, 369–376. [Google Scholar] [CrossRef]
  18. Karban, R.; Lowenberg, G. Feeding by seed bugs and weevils enhances germination of wild Gossypium species. Oecologia 1992, 92, 196–200. [Google Scholar] [CrossRef]
  19. Silva, A.V.; Rossi, M.N. When a seed-feeding beetle is a predator and also increases the speed of seed germination: An intriguing interaction with an invasive plant. Evol. Ecol. 2019, 33, 211–232. [Google Scholar] [CrossRef]
  20. Pereira, A.C.F.; Fonseca, F.; Mota, G.R.; Fernandes, A.K.C.; Fagundes, M.; Reis-Júnior, R.; Faria, M.L. Ecological Interactions Shape the Dynamics of Seed Predation in Acrocomia aculeata (Arecaceae). PLoS ONE 2014, 9, e98026. [Google Scholar] [CrossRef]
  21. Janzen, D.H. Herbivores and the Number of Tree Species in Tropical Forests. Am. Nat. 1970, 104, 501–528. [Google Scholar] [CrossRef]
  22. Branco, M.; Branco, C.; Merouani, H.; Almeida, M.H. Germination success, survival and seedling vigour of Quercus suber acorns in relation to insect damage. For. Ecol. Manag. 2002, 166, 159–164. [Google Scholar] [CrossRef]
  23. Perea, R.; Fernandes, G.W.; Dirzo, R. Embryo size as a tolerance trait against seed predation: Contribution of embryo-damaged seeds to plant regeneration. Perspect. Plant Ecol. Evol. Syst. 2018, 31, 7–16. [Google Scholar] [CrossRef]
  24. Barroso, A.; Amor, F.; Cerda, X.; Boulay, R.R. Dispersal of non-myrmecochorous plants by a “keystone disperser” ant in a Mediterranean habitat reveals asymmetric interdependence. Insectes Sociaux 2012, 60, 75–86. [Google Scholar] [CrossRef] [Green Version]
  25. Camargo, P.H.S.A.; Martins, M.M.; Feitosa, R.M.; Christianini, A.V. Bird and ant synergy increases the seed dispersal effectiveness of an ornithochoric shrub. Oecologia 2016, 181, 507–518. [Google Scholar] [CrossRef] [PubMed]
  26. Camargo, P.H.; Rodrigues, S.B.; Piratelli, A.J.; Oliveira, P.S.; Christianini, A.V. Interhabitat variation in diplochory: Seed dispersal effectiveness by birds and ants differs between tropical forest and savanna. Perspect. Plant Ecol. Evol. Syst. 2019, 38, 48–57. [Google Scholar] [CrossRef]
  27. Van der Pijl, L. Ecological dispersal classes, established on the basis of the dispersing agents. In Principles of Dispersalin Higher Plants, 3rd ed.; Springer: Berlin/Heidelberg, Germany, 1982; pp. 22–90. [Google Scholar]
  28. Boesewinkel, F.D.; Bouman, F. The seed: Structure. In Embryology of Angiosperms; Johri, B.M., Ed.; Springer: Berlin/Heidelberg, Germany, 1984; pp. 567–610. [Google Scholar]
  29. Penn, H.J.; Crist, T.O. From dispersal to predation: A global synthesis of ant-seed interactions. Ecol. Evol. 2018, 8, 9122–9138. [Google Scholar] [CrossRef]
  30. Janzen, D.H. Seed predation by animals. Annu. Rev. Ecol. Syst. 1971, 2, 465–492. [Google Scholar] [CrossRef]
  31. Fernandes, T.V.; Paolucci, L.N.; Solar, R.R.C.; Neves, F.S.; Campos, R.I. Ant removal distance, but not seed manipulation and deposition site increases the establishment of a myrmecochorous plant. Oecologia 2019, 192, 133–142. [Google Scholar] [CrossRef]
  32. Culver, D.C.; Beattie, A.J. Myrmecochory in Viola: Dynamics of Seed-Ant Interactions in Some West Virginia Species. J. Ecol. 1978, 66, 53. [Google Scholar] [CrossRef]
  33. Zettler, J.A.; Spira, T.P.; Alen, C.R. Ant–seed mutualisms: Can red imported fire ants sour the relationship? Biol. Conserv. 2011, 101, 249–253. [Google Scholar] [CrossRef]
  34. Dayrell, R.L.C.; Gonçalves-Alvim, S.; Negreiros, D.; Fernandes, G.W.; Silveira, F. Environmental control of seed dormancy and germination of Mimosa calodendron (Fabaceae): Implications for ecological restoration of a highly threatened environment. Braz. J. Bot. 2015, 38, 395–399. [Google Scholar] [CrossRef]
  35. Leal, I.R.; Wirth, R.; Tabarelli, M. Seed Dispersal by Ants in the Semi-arid Caatinga of North-east Brazil. Ann. Bot. 2007, 99, 885–894. [Google Scholar] [CrossRef] [Green Version]
  36. Prior, K.M.; Saxena, K.; Frederickson, M. Seed handling behaviours of native and invasive seed-dispersing ants differentially influence seedling emergence in an introduced plant. Ecol. Èntomol. 2013, 39, 66–74. [Google Scholar] [CrossRef]
  37. Baskin, C.C. Breaking physical dormancy in seeds: Focusing on the lens. New Phytol. 2003, 158, 229–232. [Google Scholar] [CrossRef]
  38. Ribeiro, L.C.; Borghetti, F. Comparative effects of desiccation, heat shock and high temperatures on seed germination of savanna and forest tree species. Austral Ecol. 2013, 39, 267–278. [Google Scholar] [CrossRef]
  39. Fichino, B.S.; Dombroski, J.R.G.; Pivello, V.; Fidelis, A. Does Fire Trigger Seed Germination in the Neotropical Savannas? Experimental Tests with Six Cerrado Species. Biotropica 2016, 48, 181–187. [Google Scholar] [CrossRef]
  40. Wiggers, M.S.; Hiers, J.K.; Barnett, A.; Boyd, R.S.; Kirkman, L.K. Seed heat tolerance and germination of six legume species native to a fire-prone longleaf pine forest. Plant Vecol. 2016, 218, 151–171. [Google Scholar] [CrossRef]
  41. Moreira, B.; Tormo, J.; Estrelles, E.; Pausas, J.G. Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Ann. Bot. 2010, 105, 627–635. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Ribeiro, L.C.; Pedrosa, M.; Borghetti, F. Heat shock effects on seed germination of five Brazilian savanna species. Plant Biol. 2012, 15, 152–157. [Google Scholar] [CrossRef]
  43. Ooi, M.K.J.; Denham, A.J.; Santana, V.M.; Auld, T.D. Temperature thresholds of physically dormant seeds and plant functional response to fire: Variation among species and relative impact of climate change. Ecol. Evol. 2014, 4, 656–671. [Google Scholar] [CrossRef] [PubMed]
  44. Zirondi, H.L.; Silveira, F.; Fidelis, A. Fire effects on seed germination: Heat shock and smoke on permeable vs impermeable seed coats. Flora 2019, 253, 98–106. [Google Scholar] [CrossRef]
  45. Fidelis, A.; Daibes, L.F.; Martins, A.R. To resist or to germinate? The effect of fire on legume seeds in Brazilian subtropical grasslands. Acta Bot. Bras. 2016, 30, 147–151. [Google Scholar] [CrossRef] [Green Version]
  46. Junior, C.H.L.S.; Pessôa, A.C.M.; Carvalho, N.S.; Reis, J.B.C.; Anderson, L.O.; Aragão, L.E.O.C. The Brazilian Amazon deforestation rate in 2020 is the greatest of the decade. Nat. Ecol. Evol. 2020, 5, 144–145. [Google Scholar] [CrossRef] [PubMed]
  47. Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; Da Fonseca, G.A.; Kent, J. Biodiversity hotspots for conservation priorities. Nature 2000, 403, 853–858. [Google Scholar] [CrossRef] [PubMed]
  48. Van Schaik, C.P.; Terborgh, J.W.; Wright, S.J. The phenology of tropical forests: Adaptive significance and consequences for primary consumers. Annu. Rev. Ecol. Syst. 1993, 24, 353–377. [Google Scholar] [CrossRef]
  49. Souza, M.L.; Solar, R.R.; Fagundes, M. Reproductive strategy of Copaifer alangsdorffii (Fabaceae): More seeds or better seeds? Rev. Biol. Trop. 2015, 63, 1161–1167. [Google Scholar]
  50. Simon, M.; Pennington, 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]
  51. Christianini, A.V.; Mayhé-Nunes, A.J.; Oliveira, P.S. The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna. J. Trop. Ecol. 2007, 23, 343–351. [Google Scholar] [CrossRef] [Green Version]
  52. Christianini, A.V.; Mayhé-Nunes, A.J.; Oliveira, P.S. Exploitation of fallen diaspores by ants: Are there ant–plant partner choices? Biotropica 2012, 44, 360–367. [Google Scholar] [CrossRef]
  53. Costa, A.N.; Vasconcelos, H.L.; Vieira-Neto, E.H.; Bruna, E.M. Do herbivores exert top-down effects in Neotropical savannas? Estimates of biomass consumption by leaf-cutter ants. J. Veg. Sci. 2008, 19, 849–854. [Google Scholar] [CrossRef]
  54. Costa, A.N.; Vasconcelos, H.L.; Bruna, E.M. Biotic drivers of seedling establishment in Neotropical savannas: Selective granivory and seedling herbivory by leaf-cutter ants as an ecological filter. J. Ecol. 2016, 105, 132–141. [Google Scholar] [CrossRef]
  55. Fernandes, T.V.; Paolucci, L.N.; Carmo, F.M.S.; Sperber, C.F.; Campos, R.I. Seed manipulation by ants: Disentangling the effects of ant behaviours on seed germination. Ecol. Èntomol. 2018, 43, 712–718. [Google Scholar] [CrossRef]
  56. Veloso, A.; Silva, P.S.; Siqueira, W.K.; Duarte, K.L.; Gomes, I.L.V.; Santos, H.T.; Fagundes, M. Intraspecific variation in seed size and light intensity affect seed germination and initial seedling growth of a tropical shrub. Acta Bot. Bras. 2017, 31, 736–741. [Google Scholar] [CrossRef] [Green Version]
  57. Fagundes, M.; Cuevas-Reyes, P.; Araujo, W.S.; Faria, M.L.; Valerio, H.M.; Pimenta, M.A. Influence of light availability and seed mass on germinability and initial growth of two congeneric species of Fabaceae. Acta Bot. Mex. 2020, 127, e1638. [Google Scholar]
  58. Fagundes, M.; Barbosa, E.M.; Oliveira, J.B.B.S.; Brito, B.G.S.; Freitas, K.T.; Freitas, K.F.; Reis-Junior, R. Galling inducing insects associated with a tropical shrub: The role of resource concentration and species interactions. Ecol. Austral 2019, 29, 12–19. [Google Scholar] [CrossRef]
  59. Ramírez, N. Historia de vida de Copaifera pubiflora Benth. (Fabaceae, Caesalpinioideae) em los Altos Llanos Centrales Venezolanos. Trib. Del Investig. 1994, 1, 69–75. [Google Scholar]
  60. De Lima, R.M.; Santos, S.B.D.O.; Vaz, S.; Gomes, A.L.S.; De Sousa, W.O. Description of the larva and pupa of Apion brevicorne Gerstaecker, 1854 (Coleoptera: Brentidae: Apioninae) with biological information. Papéis Avulsos De Zool. 2020, 60, e202060. [Google Scholar] [CrossRef] [Green Version]
  61. Leal, I.; Oliveira, P.S. Interactions between Fungus-Growing Ants (Attini), Fruits and Seeds in Cerrado Vegetation in Southeast Brazil1. Biotropica 1998, 30, 170–178. [Google Scholar] [CrossRef]
  62. Giladi, I. Choosing benefits or partners: A review of the evidence for the evolution of myrmecochory. Oikos 2006, 112, 481–492. [Google Scholar] [CrossRef] [Green Version]
  63. INMET, Instituto Nacional de Meteorologia. Available online: http://www.inmet.gov.br/ (accessed on 10 September 2021).
  64. Kuchenbecker, J.; Fagundes, M. Diversity of insects associated with two common plants in the Brazilian Cerrado: Responses of two guilds of herbivores to bottom-up and top-down forces. Eur. J. Èntomol. 2018, 115, 354–363. [Google Scholar] [CrossRef] [Green Version]
  65. Warton, D.I.; Hui, F.K.C. The arcsine is asinine: The analysis of proportions in ecology. Ecology 2011, 92, 3–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Weibull, W. Wide applicability. J. Appl. Mech. 1951, 103, 293–297. [Google Scholar] [CrossRef]
  67. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2013. [Google Scholar]
  68. Zupo, T.; Baeza, M.J.; Fidelis, A. The effect of simulated heat-shock and daily temperature fluctuations on seed germination of four species from fire-prone ecosystems. Acta Bot. Bras. 2016, 30, 514–519. [Google Scholar] [CrossRef] [Green Version]
  69. Bohn, K.; Pavlick, R.; Reu, B.; Kleidon, A. The Strengths of r- and K-Selection Shape Diversity-Disturbance Relationships. PLoS ONE 2014, 9, e95659. [Google Scholar] [CrossRef] [Green Version]
  70. Imbert, E. Dispersal by ants in Centaurea corymbosa (Asteraceae): What is the elaiosome for? Plant Species Biol. 2006, 21, 109–117. [Google Scholar] [CrossRef]
  71. Ohkawara, K.; Akino, T. Seed cleaning behavior by tropical ants and its anti-fungal effect. J. Ethol. 2004, 23, 93–98. [Google Scholar] [CrossRef]
  72. Kulik, M.M.; Yaklich, R.W. Soybean Seed Coat Structures: Relationship to Weathering Resistance and Infection by the Fungus Phomopsis phaseoli. Crop. Sci. 1991, 31, 108–113. [Google Scholar] [CrossRef]
  73. Miranda, H.S.; Sato, M.N.; Neto, W.N.; Aires, F.S. Fires in the Cerrado, the Brazilian savanna. In Tropical Fire Ecology: Climate Change, Land Use and Ecosystem Dynamics; Cochrane, A.M., Ed.; Springer: Berlin/Heidelberg, Germany, 2009; pp. 427–450. [Google Scholar]
  74. Pivello, V.R.; Oliveras, I.; Miranda, H.S.; Haridasan, M.; Sato, M.N.; Meirelles, S.T. Effect of fires on soil nutrient availability in an open savanna in Central Brazil. Plant Soil 2010, 337, 111–123. [Google Scholar] [CrossRef]
  75. Corbineau, F.; Xia, Q.; Bailly, C.; El-Maarouf-Bouteau, H. Ethylene, a key factor in the regulation of seed dormancy. Front. Plant Sci. 2014, 5, 539. [Google Scholar] [CrossRef] [Green Version]
  76. Kępczyński, J. Induction of agricultural weed seed germination by smoke and smoke-derived karrikin (KAR 1), with a particular reference to Avena fatua L. Acta Physiol. Plant. 2018, 40, 87. [Google Scholar] [CrossRef] [Green Version]
  77. Shayanfar, A.; Ghaderi-Far, F.; Behmaram, R.; Soltani, A.; Sadeghipour, H.R. Impacts of fire cues on germination of Brassica napus L. seeds with high and low secondary dormancy. Plant Biol. 2020, 22, 647–654. [Google Scholar] [CrossRef] [PubMed]
  78. Nambara, E.; Okamoto, M.; Tatematsu, K.; Yano, R.; Seo, M.; Kamiya, Y. Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 2010, 20, 55–67. [Google Scholar] [CrossRef]
  79. Kang, J.; Yim, S.; Choi, H.; Kim, A.; Lee, K.P.; Lopez-Molina, L. Abscisic acid transporters cooperate to control seed germination. Nat. Commun. 2015, 6, 8113. [Google Scholar] [CrossRef] [Green Version]
  80. Penfield, S. Seed dormancy and germination. Curr. Biol. 2017, 27, 874–878. [Google Scholar] [CrossRef] [Green Version]
Seeds 01 00003 g001 550
Figure 1. Images of seeds of C. oblongifolia showing different predation treatments: (A) unmanipulated seeds with elaiosome intact, (B) seeds with elaiosome removed by Atta laevigata, (C) seeds damaged by Apion sp., and (D) seeds preyed upon by Rhinochenus brevicollis.
Figure 1. Images of seeds of C. oblongifolia showing different predation treatments: (A) unmanipulated seeds with elaiosome intact, (B) seeds with elaiosome removed by Atta laevigata, (C) seeds damaged by Apion sp., and (D) seeds preyed upon by Rhinochenus brevicollis.
Seeds 01 00003 g001
Seeds 01 00003 g002 550
Figure 2. Variation in the percentage of seed germination for C. oblongifolia seeds in relation to different types of predation. Seeds preyed upon by Rhinochenus brevicollis had the lowest germination percentage followed by seeds attacked by Apion sp., non-manipulated seeds, and seeds with elaiosomes removed by Atta laevigata.
Figure 2. Variation in the percentage of seed germination for C. oblongifolia seeds in relation to different types of predation. Seeds preyed upon by Rhinochenus brevicollis had the lowest germination percentage followed by seeds attacked by Apion sp., non-manipulated seeds, and seeds with elaiosomes removed by Atta laevigata.
Seeds 01 00003 g002
Seeds 01 00003 g003 550
Figure 3. Variation in the probability of germination for C. oblongifolia seeds in relation to germination percentage for seeds in each treatment. The intersection of vertical lines with the horizontal line indicates the probability of 50% germination for seeds of each treatment (in days).
Figure 3. Variation in the probability of germination for C. oblongifolia seeds in relation to germination percentage for seeds in each treatment. The intersection of vertical lines with the horizontal line indicates the probability of 50% germination for seeds of each treatment (in days).
Seeds 01 00003 g003
Seeds 01 00003 g004 550
Figure 4. Germination percentage for C. oblongifolia seeds in relation to temperature and manipulation by Atta laevigata.
Figure 4. Germination percentage for C. oblongifolia seeds in relation to temperature and manipulation by Atta laevigata.
Seeds 01 00003 g004
Seeds 01 00003 g005 550
Figure 5. Variation in germination time for C. oblongifolia seeds as a function of manipulation by Atta laevigata and temperature. The intersection of vertical lines with the horizontal line indicates the probability of 50% germination for seeds of each treatment (in days).
Figure 5. Variation in germination time for C. oblongifolia seeds as a function of manipulation by Atta laevigata and temperature. The intersection of vertical lines with the horizontal line indicates the probability of 50% germination for seeds of each treatment (in days).
Seeds 01 00003 g005
Table
Table 1. Generalized linear models used to evaluate the effects of different type of predators on germination time and percentage for C. oblongifolia seeds. (d.f. = degrees of freedom, Dev = deviance). Values in bold indicate statistically significant values at alfa = 5%.
Table 1. Generalized linear models used to evaluate the effects of different type of predators on germination time and percentage for C. oblongifolia seeds. (d.f. = degrees of freedom, Dev = deviance). Values in bold indicate statistically significant values at alfa = 5%.
Response VariableExplanatory VariableError DistributionD.f.Residual
Deviance		Residual DfDevFp
Time for germinationPredation treatmentsWeibull2---13128.278---<0.001
Germination percentagePredation treatmentsQuasibinomial2249.5720724.16911.912<0.001
Table
Table 2. Generalized linear models used to evaluate the effects of predation (seeds that had elaiosome removed by ant manipulation or seeds with an intact elaiosome) and temperature treatments on germination time and percentage for C. oblongifolia seeds. (d.f. = degrees of freedom, Dev = deviance).
Table 2. Generalized linear models used to evaluate the effects of predation (seeds that had elaiosome removed by ant manipulation or seeds with an intact elaiosome) and temperature treatments on germination time and percentage for C. oblongifolia seeds. (d.f. = degrees of freedom, Dev = deviance).
Response VariableExplanatory VariableError DistributionD.f.Residual DevianceResid. DfDevFp
Time for germinationElaiosomeWeibull2---2934.135---<0.001
Temperature1---29424.372---0.0419
Elaiosome * temperature2---2916.987---0.0303
Germination percentageElaiosomeQuasibinomial1506.124180.046210.04560.8311
Temperature2503.174162.951421.45460.2347
Elaiosome * temperature2501.994141.175160.57920.5608
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Fagundes, M.; dos Santos, H.T.; Cuevas-Reyes, P.; Cornelissen, T. Biotic and Abiotic Interactions Shape Seed Germination of a Fire-Prone Species. Seeds 2022, 1, 16-27. https://doi.org/10.3390/seeds1010003

AMA Style

Fagundes M, dos Santos HT, Cuevas-Reyes P, Cornelissen T. Biotic and Abiotic Interactions Shape Seed Germination of a Fire-Prone Species. Seeds. 2022; 1(1):16-27. https://doi.org/10.3390/seeds1010003

Chicago/Turabian Style

Fagundes, Marcilio, Henrique Tadeu dos Santos, Pablo Cuevas-Reyes, and Tatiana Cornelissen. 2022. "Biotic and Abiotic Interactions Shape Seed Germination of a Fire-Prone Species" Seeds 1, no. 1: 16-27. https://doi.org/10.3390/seeds1010003

APA Style

Fagundes, M., dos Santos, H. T., Cuevas-Reyes, P., & Cornelissen, T. (2022). Biotic and Abiotic Interactions Shape Seed Germination of a Fire-Prone Species. Seeds, 1(1), 16-27. https://doi.org/10.3390/seeds1010003

Article Metrics

Back to TopTop