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Fire cues and germination of invasive and native grasses in the Cerrado

ABSTRACT

Fire-related cues may enhance seed recruitment in flammable ecosystems and differences in fire-germination responses of invasive vs. native species can drive the invasion process. We evaluated the effects of heat shock and smoke water solution treatment on seed germination of invasive (Melinis minutiflora, Urochloa decumbens, U. brizantha) and native grasses (Axonopus pressus, Aristida setifolia, Gymnopogon foliosus) of the Cerrado. The effect of fire temperature was tested by exposing seeds to heat shock treatments of 60, 100, and 200 °C for one minute, comparing them to untreated seeds. The effect of smoke was tested by soaking seeds for 24-h in an aqueous smoke comparing them to seeds soaked in distilled water. Differences among treatments were evaluated by ANOVA and randomization tests. None of the tested species had germination stimulated by the temperature or smoke. Both species of Urochloa experienced decreased viability with increasing temperature, while seeds of native species and M. minutiflora tolerated heat shock up to 200 °C. The invasive grasses usually germinated faster than the native grasses. Germination time is therefore a crucial trait driving the invasion process, irrespective of fire-related cues. Other seed traits (e.g. dormancy) and higher resprouting capacity may help invasive species to persist in frequently burned savannas.

Keywords:
African grasses; Cerrado grasses; fire temperature; Melinis minutiflora; smoke solution; Urochloa brizantha; Urochloa decumbens

Introduction

Successful germination and seedling establishment are important regeneration traits that lead to effective processes of biological invasion (Pyšek & Richardson 2007Pyšek P, Richardson DM. 2007. Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W. (ed.) Biological invasions . Berlin, Springer . p. 97-126.; Gioria & Pyšek 2017Gioria M, Pyšek P. 2017. Early bird catches the worm: germination as a critical step in plant invasion. Biological Invasions 19: 1055-1080. ). In disturbed ecosystems, potentially invasive species are often more adapted to disturbance regimes when compared to the native ones (Facon et al. 2006Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P. 2006. A general eco-evolutionary framework for understanding bioinvasions. Trends in Ecology and Evolution 21: 130-135. ). Fire is a principal disturbance in many ecosystems, and its effects depend on its origin (natural, by a lightning strike, or accidental, by human actions), season and intensity (Whelan 1995Whelan RJ. 1995. The ecology of fire. Cambridge, Cambridge University Press . ), as well as on the particular adaptations of the community species (Huston 2004Huston MA. 2004. Management strategies for plant invasions: manipulating productivity, disturbance, and competition. Diversity and Distributions 10: 167-178. ; Lockwood et al. 2007Lockwood JL, Hoopes MF, MarChetti MP. 2007. Invasion ecology. Oxford, Blackwell.).

At a community level, fire could affect plants by altering species richness, composition and structure (Whelan 1995Whelan RJ. 1995. The ecology of fire. Cambridge, Cambridge University Press . ; Fidelis et al. 2012Fidelis A, Blanco CC, Muller SC, Pillar VD, Pfadenhauer J. 2012. Short term changes caused by fire and mowing in BrazilianCamposgrasslands with different long‐term fire histories. Journal of Vegetation Science 23: 552-562.). At the individual level, some species (such as grasses) could have a rapid regrowth, increased productivity, flowering and seed production after fire (Whelan 1995Whelan RJ. 1995. The ecology of fire. Cambridge, Cambridge University Press . ). Fire also could affect the survival, viability and germination of seeds (Moreira et al. 2010Moreira B, Tormo J, Estrelles E, Pausas JG. 2010. Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Annals of Botany 105: 627-635.; Clarke & French 2005Clarke S, French K. 2005. Germination response to heat and smoke of 22 Poaceae species from grassy woodlands. Australian Journal of Botany 53: 445-454.).

Seed exposure to fire-related germination cues may enhance recruitment of both invasive and native species (Adkins & Peters 2001Adkins SW, Peters NCB. 2001. Smoke derived from burnt vegetation stimulates germination of arable weeds. Seed Science Research 11: 213-222. ; Figueroa et al. 2009Figueroa JA, Cavieres LA, Gómez-González S, Montenegro M, Jaksic FM. 2009. Do heat and smoke increase emergence of exotic and native plants in the matorral of central Chile? Acta Oecologica 35: 335-340. ; Arán et al. 2013Arán D, García-Duro J, Reyes O, Casal M. 2013. Fire and invasive species: Modifications in the germination potential of Acacia melanoxylon, Conyza canadensis and Eucalyptus globulus. Forest Ecology and Management 302: 7-13.). Heat shock and plant-derived smoke solutions, for instance, can stimulate germination of many grass species in fire-prone ecosystems (Clarke & French 2005Clarke S, French K. 2005. Germination response to heat and smoke of 22 Poaceae species from grassy woodlands. Australian Journal of Botany 53: 445-454.). On the other hand, little effect of heat shock and exposure to smoke solution in germination has been reported for herbaceous species from Brazilian grasslands and savannas (Overbeck et al. 2006Overbeck GE, Müller SC, Pillar VD, Pfadenhauer J. 2006. No heat-stimulated germination found in herbaceous species from burned subtropical grassland. Plant Ecology 184: 237-247. ; Stradic et al. 2015Stradic S, Silveira FAO, Buisson E, Cazalles K, Carvalho V, Fernandes GW. 2015. Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Austral Ecology 40: 537-546. ; Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ; Ramos et al. 2016Ramos DM, Liaffa ABS, Diniz P, et al. 2016. Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical Savanna grasses. International Journal of Wildland Fire 25: 1273-1280. ; Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.).

However, seeds of many Cerrado (Ribeiro et al. 2013Ribeiro LC, Pedrosa M, Borghetti F. 2013. Heat shock effects on seed germination of five Brazilian savanna species. Plant Biology 15: 152-157.; Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ) and Chaco species (Jaureguiberry & Díaz 2015Jaureguiberry P, Díaz S. 2015. Post-burning regeneration of the Chaco seasonally dry forest: germination response of dominant species to experimental heat shock. Oecologia 177: 689-699. ) may tolerate exposure to temperatures up to 100 °C. Therefore, seed survival to fire has been suggested as a critical trait for post-fire regeneration (Pausas et al. 2004Pausas JG, Bradstock RA, Keith DA, Keeley JE. 2004. Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85: 1085-1100. ; Paula & Pausas 2008Paula S, Pausas JG. 2008. Burning seeds: germinative response to heat treatments in relation to resprouting ability. Journal of Ecology 96: 543-552.; Ramos et al. 2016Ramos DM, Liaffa ABS, Diniz P, et al. 2016. Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical Savanna grasses. International Journal of Wildland Fire 25: 1273-1280. ). Species that have fire-tolerant seeds and are able to promptly germinate after fire may have a competitive advantage in post-fire environments (Ramula et al. 2015Ramula S, Jauni M, Ooi VT. 2015. Propagule pressure governs establishment of an invasive herb. Acta Oecologica 68: 18-23. ). Hence, in Brazil, seed tolerance to high temperatures, rather than fire-stimulated germination, appears to promote species’ survival in fire-prone environments (Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ; Fidelis et al. 2016Fidelis A, Daibes LF, Martins AR. 2016. To resist or to germinate? The effect of fire on legume seeds in Brazilian subtropical grasslands. Acta Botanica Brasilica 30: 147-151.) and may foster biological invasion after fire events (Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.).

Fire has been present in the Cerrado for millions of years, and has received some academic and scientific attention (Simon et al. 2009Simon MF, Grether R, Queiroz LP, Skema C, Pennigngton T, Hughes CE. 2009. Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences of the United States of America 106: 20359-20364.). Nevertheless, few studies have investigated the direct effects of fire on germination of Cerrado grass species (but see Ramos et al. 2016Ramos DM, Liaffa ABS, Diniz P, et al. 2016. Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical Savanna grasses. International Journal of Wildland Fire 25: 1273-1280. ; Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.). In addition to the native species, C4 African grasses (such as Urochloa spp., previously Brachiaria) were introduced in Brazil for cattle forage (Pivello et al. 1999Pivello VR, Carvalho V, Lopes P. 1999a. Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) biological reserve. Biotropica 31: 71-82.a; bPivello VR, Shida CN, Meirelles ST. 1999b. Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodiversity and Conservation 8: 1281-1294.; Durigan et al. 2007Durigan G, Siqueira MF, Franco GADC. 2007. Threats to the Cerrado remnants of the state of São Paulo, Brazil. Scientia Agricola 64: 355-363.; Ziller & Dechoum 2013Ziller SR, Dechoum MS. 2013. Plantas e vertebrados exóticos invasores em unidades de conservação no Brasil. Biodiversidade Brasileira 3: 4-31. ). Such African grasses have spread from the pastures and became a threaten to Cerrado native herbs by reducing their biomass and diversity (Pivello et al. 1999Pivello VR, Carvalho V, Lopes P. 1999a. Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) biological reserve. Biotropica 31: 71-82.a; bPivello VR, Shida CN, Meirelles ST. 1999b. Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodiversity and Conservation 8: 1281-1294.; Damasceno et al. 2018Damasceno G, Souza L, Pivello VR, Gorgone-Barbosa EG, Giroldo PZ, Fidelis A. 2018. Impact of invasive grasses on Cerrado under natural regeneration. Biological Invasions 20: 3621-3629.).

Invasive grasses can also change fire behaviour by enhancing flame height and temperature, thus increasing the mortality of native species (Mistry & Berardi 2005Mistry J, Berardi A. 2005. Assessing fire potential in a Brazilian savanna nature reserve. Biotropica 37: 439-451.; Gorgone-Barbosa et al. 2015Gorgone-Barbosa E, Pivello VR, Bautista S, Zupo T, Rissi MN, Fidelis A. 2015. How can an invasive grass affect fire behavior in a tropical savanna? A community and individual plant level approach. Biological Invasions 17: 423-431). Improved understanding of the direct effects of fire on seed germination and on seedling recruitment may provide useful insight to control these species in protected areas (Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.). Therefore, understanding fire effects at early stages of plant development is fundamental to elucidating biological invasion processes (Pyšek & Richardson 2007Pyšek P, Richardson DM. 2007. Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W. (ed.) Biological invasions . Berlin, Springer . p. 97-126.). Studies of post-fire regeneration strategies of invasive and native species are also crucial for planning of conservation and management programs (Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.). Such programs may include prescribed fire management in order to identify mechanisms of post-fire competitive advantage of the invasives, and thus avoid their proliferation in burned areas.

Because Cerrado is subjected to frequent fires, we initially expected seeds of native and invasive grasses to respond to fire-related cues (high temperature and smoke water solution, a proxy for smoke) by tolerating or benefitting from fire. Given that several African grasses outcompete Cerrado grasses and become invasive (Pivello et al. 1999Pivello VR, Carvalho V, Lopes P. 1999a. Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) biological reserve. Biotropica 31: 71-82.a; bPivello VR, Shida CN, Meirelles ST. 1999b. Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodiversity and Conservation 8: 1281-1294.) we hypothesized higher seed survival/germination of such African grasses under fire events compared to native Cerrado grasses. Therefore, in this study we aimed to evaluate the effects of heat shock and smoke (fire-related cues) on seed viability, germination percentage, and mean germination time (MGT) of three invasive (Melinis minutiflora, Urochloa decumbens and Urochloa brizantha), and three native (Axonopus pressus, Aristida setifolia and Gymnopogon foliosus) grass species frequently found in open Cerrado. Specifically, we assessed (1) the effect of heat shock (60, 100 and 200 °C) and (2) the effect of smoke water solution on seed germination.

Materials and methods

Focal species

We tested germination of six grasses that commonly co-occur in the Cerrado: three native species: Axonopus pressus (Nees ex Steud.) Parodi, Aristida setifolia Kunth and Gymnopogon foliosus (Willd.) Nees, and three of the most aggressive invasives: Melinis minutiflora P. Beauv, Urochloa decumbens (Stapf) R.D. Webster and Urochloa brizantha (Stapf) Webster (Pivello et al. 1999Pivello VR, Carvalho V, Lopes P. 1999a. Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian Savanna) biological reserve. Biotropica 31: 71-82.a; bPivello VR, Shida CN, Meirelles ST. 1999b. Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodiversity and Conservation 8: 1281-1294.). Urochloa species are perennial grasses that copiously resprout after fire, but their seeds might also germinate under temperatures up to 50 °C (Gorgone-Barbosa et al. 2016Gorgone-Barbosa E, Pivello VR, Baeza JM, Fidelis A. 2016. Disturbance as a factor in breaking dormancy and enhacing invasiveness of African grasses in a Neotropical Savanna. Acta Botanica Brasilica 30: 131-137.). Melinis minutiflora, although able to resprout, apparently regenerates primarily through seeds (Lorenzi 2008Lorenzi H. 2008. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas. 4th. edn. Nova Odessa, Plantarum. p.523. ). Among the native species, A. pressus and A. setifolia can resprout after fire, while G. foliosus is an annual grass. Germination percentages of A. setifolia and G. foliosus are usually higher than 50 % (Carmona et al. 1998Carmona R, Martins CR, Fávero AP. 1998. Fatores que afetam a germinação de sementes de gramíneas nativas do cerrado. Revista Brasileira de Sementes 20: 16-22.; 1999Carmona R, Martins CR, Fávero AP. 1999. Características de sementes de gramíneas nativas do Cerrado. Pesquisa Agropecuária Brasileira 34: 1066-1074. ; Kolb et al. 2016Kolb RM, Pilon N, Durigan G. 2016. Factors influencing seed germination in Cerrado grasses. Acta Botanica Brasilica 30: 87-92. ), while A. pressus shows a high proportion of empty seeds (E Gorgone-Barbosa unpubl. res.), and thus low germination percentage (Kolb et al. 2016Kolb RM, Pilon N, Durigan G. 2016. Factors influencing seed germination in Cerrado grasses. Acta Botanica Brasilica 30: 87-92. ).

Seed collection

Since the three invasive species are widely commercialized, we used commercial seeds obtained from certified producers. The selected native species were collected in patches of campo sujo, which is an open Cerrado physiognomy dominated by grasses and forbs with scattered shrubs and dwarf trees (Coutinho 1978Coutinho LM. 1978. Aspectos ecológicos do fogo no Cerrado. I. A temperatura do solo durante as queimadas. Revista Brasileira de Botânica 1: 93-96.). Axonopus pressus and G. foliosus were collected in Itirapina Ecological Station (22°15’S 47°49’W; Southeastern Brazil), and A. setifolia was collected in a private property (close to the Jalapão State Park) in the Tocantins state (10°22’S 46°40’W; Northern Brazil).

Seeds of each species were collected from at least 20 individuals and stored at room temperature for less than three months until the beginning of the experiments. Heat shock experiments were conducted first, and smoke solution effects tested with a difference of around two months later. Prior to the experiments, the seeds were visually screened to avoid malformed and/or empty seeds, which were discarded. Detachable parts of the propagules (usually the glumes and palea) were also carefully removed, avoiding any mechanical damage to the seed.

Germination experiments

To test seed responses to fire cues, we subjected them to heat shocks and smoke solutions, under laboratory conditions. We subjected seeds to dry heat shocks of 60 °C, 100 °C and 200 °C for one minute in a pre-heated electric oven. These treatments were chosen based on field-recorded fire temperatures (Coutinho 1978Coutinho LM. 1978. Aspectos ecológicos do fogo no Cerrado. I. A temperatura do solo durante as queimadas. Revista Brasileira de Botânica 1: 93-96.; Miranda et al. 1993Miranda AC, Miranda HS, Dias IFO, Dias BFS. 1993. Soil and air temperatures during prescribed Cerrado fires in Central Brazil. Journal of Tropical Ecology 9: 313-320.; Daibes et al. 2018Daibes LF, Gorgone-Barbosa EG, Silveira FAO, Fidelis A. 2018. Gaps critical for the survival of exposed seeds during Cerrado fires. Australian Journal of Botany 66: 116-123. ). Belowground temperatures reach up to 60 °C in the soil seed bank and increase with aboveground fuel load (Daibes et al. 2017Daibes LF, Zupo TM, Silveira FAO, Fidelis A. 2017. A field perspective on effects of fire and temperature fluctuation on Cerrado legume seeds. Seed Science Research 27: 74-83. ). When exposed at the soil surface, seeds face temperatures >100 °C, mostly being killed by temperatures >200 °C (Daibes et al. 2018Daibes LF, Gorgone-Barbosa EG, Silveira FAO, Fidelis A. 2018. Gaps critical for the survival of exposed seeds during Cerrado fires. Australian Journal of Botany 66: 116-123. ). Moreover, Cerrado fires are fast and rapidly consume the herbaceous biomass, therefore the heat pulse rarely reaches more than a few minutes (Miranda et al. 1993Miranda AC, Miranda HS, Dias IFO, Dias BFS. 1993. Soil and air temperatures during prescribed Cerrado fires in Central Brazil. Journal of Tropical Ecology 9: 313-320.; 2002Miranda HS, Bustamante MMC, Miranda AC. 2002. The fire factor. In: Oliveira OS, Marquis RJ. (eds.) Cerrados of Brazil. New York, Columbian Univerisity Press. p. 51-69.).

For the heat shock treatments, we used five replicates of 20 seeds per treatment for each of the six species. We placed each replicate separately into the oven to avoid pseudo-replication (Morrison & Morris 2000Morrison DA, Morris EC. 2000. Pseudoreplication in experimental designs for the manipulation of seed germination treatments. Austral Ecology 25: 292-296.). Seeds of the different study species were exposed to the treatments all together at the same time, but separately for each replicate. Control seeds were not exposed to heat shock (untreated seeds).

We used smoke water as a proxy for smoke to examine smoke effects. We prepared aqueous smoke solutions following the methodology adapted by Moreira et al. (2010Moreira B, Tormo J, Estrelles E, Pausas JG. 2010. Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Annals of Botany 105: 627-635.) and Fichino et al. (2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ). We heated 5 g of dry aboveground biomass - composed mostly of native grasses from an open Cerrado savanna - in an oven for 30 min at 200 °C. Immediately after removing the biomass from the oven, we added 50 ml of distilled water into the material and, after 10 minutes, we filtered the solution in filter paper (Whatman n°1). We prepared one solution for each replicate to avoid pseudo-replication. Subsequently, seeds were soaked in the aqueous smoke solution for 24 hours. Control seeds were soaked in distilled water for the same period.

After both experiments, seeds were placed in Petri dishes (60 mm diameter) with moistened filter paper (distilled water) and placed in germination chambers at a constant temperature of 27 ºC and light cycle of 12 h (according to Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ). Seeds were observed every two days for 30 days. We counted and removed germinated seeds that showed primary root protrusion (Bewley et al. 2013Bewley J, Bradford K, Hilhorst H, Nonogaki H .2013. Seeds: Physiology of development, germination and dormancy. 3rd. edn. New York, Springer New York.). By the end of germination experiments, we tested non-germinated seeds of the control and heat shock experiments for viability, using a 1 % tetrazolium salt solution (pH 7) (Hilhorst 2011Hilhorst HWM. 2011. Standardizing Seed Dormancy Research. In: Kermode AR. (ed.) Seed dormancy: methods and protocols. Springer. p. 43-52. ).

Data analysis

We calculated the percentage of germination and the mean germination time (MGT), according to Ranal & Santana (2006Ranal MA, Santana DG. 2006. How and why to measure the germination process? Revista Brasileira de Botânica 29: 1-11. ). Besides germination, seed survival could also be affected in the heat shock treatments, and therefore we calculated the total seed viability as the germination percentage + the seeds stained as viable by the tetrazolium tests. Separately for each species, we performed one-way analysis of variance (ANOVA) with permutation tests (10,000 iterations, Euclidean distance between sampling units) to verify the effect of treatments (heat shocks and smoke solution) on seed viability, germination percentage, and MGT. Because germination times are crucial to determine the early steps of invasion process (Gioria & Pyšek 2017Gioria M, Pyšek P. 2017. Early bird catches the worm: germination as a critical step in plant invasion. Biological Invasions 19: 1055-1080. ; Gioria et al. 2018Gioria M, Pyšek P, Osborne BA. 2018. Timing is everything: does early and late germination favor invasions by herbaceous alien plants? Journal of Plant Ecology 11: 4-16.), we also verified differences in the MGT among species, independently of the treatment. In all analyses, we used permutation tests since there are no assumptions regarding normal data distribution. All statistical analyses were performed using the software MULTIV (Pillar 2006Pillar V. 2006. MULTIV: Multivariate exploratory analysis, randomization testing and bootstrap resampling. User's guide. Vol. 2.4. Porto Alegre, Departamento de Ecologia. http://ecoqua.ecologia.ufrgs.br. 30 Dec. 2019.
http://ecoqua.ecologia.ufrgs.br...
).

Results

The invasive M. minutiflora showed germination percentages around 60 %, regardless of the heat shock treatment (Tab. 1), and average MGT of 5.1 days (Tab. 2). Additionally, M. minutiflora seed viability was not affected by any of the heat shocks (Tab. 3). Seed germination of U. decumbens varied from 25 to 42 %, but showed no significant difference among temperatures (Tab. 1), while MGT was < 4.3 days in all heat shock treatments (Tab. 2). Seed viability of U. decumbens was significantly reduced at 100 and 200 °C (Tab. 3). Seeds of U. brizantha showed germination percentages around 60 %, but it was reduced to <20 % when seeds were subjected to 200 °C (Tab. 1). Average MGT was of 4.7 days and it was not affected by heat shock treatments (Tab. 2). Viability of U. brizantha also showed values ca. 15 % higher than seed germination in the control and showed an abrupt reduction in the hottest treatment (Tab. 3).

Table 1
Germination ( %, mean ± SE) of invasive species (Melinis minutiflora, Urochloa brizantha and Urochloa decumbens) and native species (Aristida setifolia, Axonopus pressus and Gymnopogon foliosus) seeds submitted to dry heat shocks of one minute at 60 ºC, 100 ºC and 200 ºC, and the control (not exposed to high temperatures). Different letters mean significant differences among treatments of (P ≤ 0.05) according to one-way ANOVA with permutation tests.

Table 2
Mean germination time (MGT, days, mean ± SE) of invasive and native species seeds submitted to dry heat shock treatments of one minute at 60 ºC, 100 ºC and 200 ºC, and the control (not exposed to high temperatures). P values of temperature comparisons (P ≤ 0.05) according to one-way ANOVA with permutation tests.

Table 3
Viability ( %, mean ± SE) of invasive species (Melinis minutiflora, Urochloa brizantha and Urochloa decumbens) and native species (Aristida setifolia, Axonopus pressus and Gymnopogon foliosus) seeds submitted to dry heat shocks of one minute at 60 ºC, 100 ºC and 200 ºC, and the control (not exposed to high temperatures). Different letters mean significant differences among treatments (P ≤ 0.05) according to one-way ANOVA with permutation tests.

Heat shock did not affect germination of native grasses. Aristida setifolia seeds showed high germination percentages (from 63 to 75 %) and viability higher than 70 %, both not affected by any of the temperatures (Tabs. 1 and 3 respectively). MGT of A. setifolia varied from six to nine days, with no difference among treatments (Tab. 2). On the other hand, low germination percentages and viability (≤ 20 %, Tabs. 1, 3) were observed in A. pressus in all treatments, showing a slow MGT (14.3 days on average, Tab. 2). Gymonopogon foliosus had germination percentages always higher than 60 % and seed viability of nearly 100 % in all treatments (Tabs. 1 and 3, respectively). In contrast to the other two native species, G. foliosus seeds germinated very fast - on average 2.5 days - with no difference among treatments (Tab. 2).

Neither germination percentage nor MGT of invasive and native species were affected by the smoke solution treatment. Despite the variation, values were not statistically different (Tab. 4). Native species germination percentages were ca. 60 % for G. foliosus and A. setifolia (from 54 to 64 %) and lower for A. pressus (from 26 to 32 %) when subjected to smoke solution, indicating no treatment effect (Tab. 4).

Table 4
Germination percentage and mean germination time (MGT, days, mean ± SE) of invasive and native species submitted to aqueous smoke solutions and the control (distilled water); P values of germination and temperature comparisons (P≤0.05) according to one-way ANOVA with permutation tests.

When comparing MGT among the six species independently of treatment (combining heat shock and smoke), we observed that seeds of invasive species germinate approximately twice as fast as the native ones (P <0.0001), except for the native G. foliosus, which had the lowest MGT value (2.5 days, P <0.001 - Tab. 5).

Table 5
Mean germination time (days, mean ± SE) of invasive and native species seeds independently of the treatment. Different letters mean significant differences among species (P ≤ 0.05) according to one-way ANOVA with permutation tests.

Discussion

Fire cues did not trigger germination of the study species, regardless of whether they were invasive or native grasses. On the contrary, heat shock decreased germination and/or viability of the invasive Urochloa spp. Such results contrast with other invasive species elsewhere (Arán et al. 2013Arán D, García-Duro J, Reyes O, Casal M. 2013. Fire and invasive species: Modifications in the germination potential of Acacia melanoxylon, Conyza canadensis and Eucalyptus globulus. Forest Ecology and Management 302: 7-13.; Cóbar-Carranza et al. 2015Cóbar-Carranza AJ, García RA, Pauchard A, Peña E. 2015. Efecto de la alta temperatura en la germinación y supervivencia de semillas de la especie invasora Pinus contorta y dos especies nativas del sur de Chile. Bosque (Valdivia) 36: 53-60. ), and therefore fire-related cues apparently do not directly facilitate the invasion of these African grasses in the Cerrado savannas. Seeds of the invasive Melinis minutiflora and the native species were not affected by high temperatures, corroborating similar results described for native and invasive grasses in the Cerrado, under temperatures from 50 to 150°C (Paredes et al. 2018Paredes MVF, Cunha ALN, Musso C, Aires SS, Sato MN, Miranda HS. 2018. Germination responses of native and invasive Cerrado grasses to simulated fire temperature. Plant Ecology & Diversity 11: 193-203.).

Because seeds of the native grasses retained their viability similar to controls under the hottest treatment (200 °C), their tolerance to high temperatures can be considered as an important trait for persisting under Cerrado fires (Ramos et al. 2016Ramos DM, Liaffa ABS, Diniz P, et al. 2016. Seed tolerance to heating is better predicted by seed dormancy than by habitat type in Neotropical Savanna grasses. International Journal of Wildland Fire 25: 1273-1280. ). Hence, fire survival may provide propagule supply for the species regeneration in frequently burned environments (Overbeck et al. 2006Overbeck GE, Müller SC, Pillar VD, Pfadenhauer J. 2006. No heat-stimulated germination found in herbaceous species from burned subtropical grassland. Plant Ecology 184: 237-247. ; Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ). However, fire temperatures just below the soil surface increase only a few degrees during Cerrado typical fires (Miranda et al. 1993Miranda AC, Miranda HS, Dias IFO, Dias BFS. 1993. Soil and air temperatures during prescribed Cerrado fires in Central Brazil. Journal of Tropical Ecology 9: 313-320.; Daibes et al. 2017Daibes LF, Zupo TM, Silveira FAO, Fidelis A. 2017. A field perspective on effects of fire and temperature fluctuation on Cerrado legume seeds. Seed Science Research 27: 74-83. ). Therefore, most propagules of either invasive or native species would survive during fires when incorporated to the soil seed banks.

Persistence of buried propagules in the soil seed banks would thus allow the recolonization of the recently burned environment. Hence, recruitment from seed occurs with the onset of the well-marked rainy season in Cerrado (Andrade & Miranda 2014Andrade LAZ, Miranda HS. 2014. The dynamics of the soil seed bank after a fire event in a woody savanna in central Brazil. Plant Ecology 215: 1199-1209.; Ramos et al. 2017Ramos DM, Diniz P, Ooi MKJ, Borghetti F, Valls JFM. 2017. Avoiding the dry season: dispersal time and syndrome mediate seed dormancy in grasses in Neotropical savanna and wet grasslands. Journal of Vegetation Science 28: 798-807. ). Once seeds survived fire heat shock, indirect effects of disturbance could thus benefit their germination in the post-fire environment. Such effects include enhanced temperature fluctuations, which may break physiological dormancy of invasive grasses (Musso et al. 2015Musso C, Miranda HS, Aires SS, Bastos AC, Soares AMVM, Loureiro S. 2015. Simulated post-fire temperatures affects germination of native grasses in cerrado (Brazilian savanna). Plant Ecology & Diversity 8: 219-227. ; Gorgone-Barbosa et al. 2016Gorgone-Barbosa E, Pivello VR, Baeza JM, Fidelis A. 2016. Disturbance as a factor in breaking dormancy and enhacing invasiveness of African grasses in a Neotropical Savanna. Acta Botanica Brasilica 30: 131-137.). Other factors related to biomass removal could be related to reduced competition and/or favourable microsites, but competitive interactions between invasive and native species are still poorly understood and difficult to measure in the field (Zouhar et al. 2008Zouhar K, Smith JK, Sutherland S. 2008. Effects of fire on nonnative invasive plants and invasibility of wildland ecosystems. In: Zouhar K, Smith JK, Sutherland S, Brooks ML. (eds.) Wildland fire in ecosystems: fire and nonnative invasive plants. Ogden, USDA. p 7-31).

Our results showed no effect of smoke water on germination, similar to the lack of smoke-mediated germination which has been reported for Cerrado species in the literature (Stradic et al. 2015Stradic S, Silveira FAO, Buisson E, Cazalles K, Carvalho V, Fernandes GW. 2015. Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Austral Ecology 40: 537-546. ; Fichino et al. 2016Fichino S, Dombroski JRG, Pivello VR, Fidelis A. 2016. Does fire trigger seed germination in the neotropical savannas? Experimental tests with six Cerrado species. Biotropica 2: 1-7. ). This absence of a positive response strongly contrasts to germination of Australian grasses, which show smoke-stimulated germination (Clarke & French 2005Clarke S, French K. 2005. Germination response to heat and smoke of 22 Poaceae species from grassy woodlands. Australian Journal of Botany 53: 445-454.). However, smoke has recently been suggested to enhance root growth of Cerrado seedlings (Ramos et al. 2019Ramos DM, Valls JFM, Borghetti F, Ooi M. 2019. Fire cues trigger germination and stimulate seedling growth in grass species from Brazilian savannas. American Journal of Botany 106: 1190-1201.). Moreover, the effect of smoke solution depends on concentration and environmental interactions, as reported for Mediterranean ecosystems (Crosti et al. 2006Crosti R, Ladd PG, Dixon KW, Piotto B. 2006. Post- fire germination: the effect of smoke on seeds of selected species from the central Mediterranean Basin. Forest Ecology and Management 221: 306-312. ; Moreira & Pausas 2018Moreira B, Pausas JG. 2018. Shedding light through the smoke on the germination of Mediterranean Basin flora. South African Journal of Botany 115: 244-250.). Because germination of grasses can be light-dependent (Carmona et al. 1998Carmona R, Martins CR, Fávero AP. 1998. Fatores que afetam a germinação de sementes de gramíneas nativas do cerrado. Revista Brasileira de Sementes 20: 16-22.; Baskin & Baskin, 1998Baskin CC, Baskin JM. 1998. Ecology of seed dormancy and germination in grasses. In: Bradshaw A, Cheplick E. (eds.) Population biology of grasses. Cambridge, Cambridge University Press. p. 30-83.), further studies should also consider the role of smoke on stimulating germination under dark conditions (see Gardner et al. 2001Gardner MJ, Dalling KJ, Light ME, Jägger AK, Staden J. 2001. Does smoke substitute for red light in the germination of light-sensitive lettuce seeds by affecting gibberellin metabolism? South African Journal of Botany 67: 636-640). Such an approach could help to explain the post-fire germination of propagules buried in soil seed banks.

Irrespective of fire-related cues, a shorter germination time has been demonstrated to enhance species’ invasiveness (Pyšek & Richardson 2007Pyšek P, Richardson DM. 2007. Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W. (ed.) Biological invasions . Berlin, Springer . p. 97-126.; Gioria & Pyšek 2017Gioria M, Pyšek P. 2017. Early bird catches the worm: germination as a critical step in plant invasion. Biological Invasions 19: 1055-1080. ). In accordance with that, our results showed that MGT was usually lower for the invasive species compared to the native ones. In disturbed environments, seeds shall at first place survive fires and then find conditions for germination to occur, thus the timing of germination is actually one aspect of a more complex process. Therefore, invasive species could show a competitive advantage for quickly recolonizing the post-fire environment (Jauni et al. 2015Jauni M, Gripenberg S, Ramula S. 2015. Non-native plant species benefit from disturbance: A meta-analysis. Oikos 124: 122-129.; Gioria et al. 2018). The exception was G. foliosus, a native species that showed the lowest MGT of all studied species. Being an annual species, its population persistence after fire relies only on regeneration from seeds (Pausas & Keeley 2014Pausas JG, Keeley JE. 2014. Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytologist 204: 55-65.) and, therefore, germination time becomes critical for this species’ survival.

Hence, germination of both M. minutiflora and G. foliosus may be favoured in the post-fire environment, given their seed tolerance to high temperatures and rapid germination. However, several other regeneration traits, such as high seed production, have been recognized to increase invasiveness (Pyšek & Richardson 2007Pyšek P, Richardson DM. 2007. Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W. (ed.) Biological invasions . Berlin, Springer . p. 97-126.). Melinis minutiflora produces more than 70,000 seeds/m2 (Martins et al. 2009Martins CR, Hay JV, Carmona R. 2009. Invasion potencial of two cultivars of Melinis minutiflora in Brasilizan Cerrado - seed characteristics ans seedling establishment. Revista Árvore 33: 713-722. ) with high viability and persistence in the soil seed bank - for more than three years (Carmona & Martins 2010Carmona R, Martins CR. 2010. Dormência e armazenabilidade de sementes de capim-gordura. Revista Brasileira de Sementes 32: 71-79. ). These traits may promote a rapid post-fire establishment, increase competitiveness over the natives and facilitate the invasion (Lake & Leishman 2004Lake JC, Leishman MR. 2004. Invasion success of exotic plants in natural ecosystems: The role of disturbance, plant attributes and freedom from herbivores. Biological Conservation 117: 215-226. ; Tierney & Cushman 2006Tierney TA, Cushman JH. 2006. Temporal changes in native and exotic vegetation and soil characteristics following disturbances by feral pigs in a California grassland. Biological Invasions 8: 1073-1089. ).

Resprouting ability is also a post-fire regeneration strategy (Pausas et al. 2004Pausas JG, Bradstock RA, Keith DA, Keeley JE. 2004. Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85: 1085-1100. ). Therefore, many species from fire-prone environments may persist by forming a bud bank (Fidelis et al. 2014Fidelis A, Appezzato-da-Gloria B, Pillar VD, Pfadenhauer J. 2014. Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands? Flora 209: 110-116), rather than post-fire recruitment from the seeds (Paula & Pausas 2008Paula S, Pausas JG. 2008. Burning seeds: germinative response to heat treatments in relation to resprouting ability. Journal of Ecology 96: 543-552.). This could be the case of Urochloa spp., considering that - despite the reduced germination and viability percentages under the highest temperatures - U. brizantha has shown a remarkable capacity for post-fire resprouting (Gorgone-Barbosa 2016Gorgone-Barbosa E. 2016. A relação entre fogo e uma gramínea invasora no Cerrado: O fogo pode ser utilizado como uma estratégia de controle? PhD Thesis, Universidade Estadual Paulista, São Paulo. ). Hence, once seeds have colonized (and established in) a certain area, resprouting seems to be a major strategy to warrant Urochloa persistence after fire. This ability is so effective that may provide advantage to Urochloa species even over M. minutiflora in the invaded habitats where they co-occur (Pivello et al. 1999Pivello VR, Shida CN, Meirelles ST. 1999b. Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodiversity and Conservation 8: 1281-1294.a).

In summary, seeds of native grasses are tolerant to Cerrado fires, as well as seeds of the invasive M. minutiflora. On the other hand, U. brizantha and U. decumbens seeds are sensitive to hotter temperatures (100 and 200 °C) and rely mostly on resprouting to persist in the burned savannas, although a proportion of seeds would probably tolerate fire temperatures if incorporated into the soil seed bank. In general, invasive species showed the ability to germinate faster than most natives, which helps to explain their invasiveness in the Cerrado. Smoke solution showed no effect either on invasive or native species, but further research is needed to explore this topic. The information obtained in this research is fundamental to elucidate post-fire invasion process in the Cerrado and may guide management strategies for controlling invasive species.

Acknowledgements

We thank Fundação Grupo Boticário de Proteção à Natureza (0153_2011_PR and 0106_2011_PR), CNPq-Conselho Nacional de Desenvolvimento Científico e Tecnológico (476334/2011-0 and 455183/2014-7) and FAPESP-Fundação de Amparo à Pesquisa do Estado de São Paulo (2015/06743-0) for financial support. VRP and AF received grants from CNPq (305253/2015-8 and 306170/2015-9, respectively).

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Publication Dates

  • Publication in this collection
    20 Mar 2020
  • Date of issue
    Jan-Mar 2020

History

  • Received
    11 Oct 2019
  • Accepted
    02 Nov 2019
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