BIOTROPICA 48(2): 181–187 2016
10.1111/btp.12276
Does Fire Trigger Seed Germination in the Neotropical Savannas? Experimental Tests with Six Cerrado Species ^nia Santos Fichino1, Julia R. G. Dombroski1, Va ^nia R. Pivello1, and Alessandra Fidelis2,3 Beta 1
~ o Paulo, Rua do Mata ~o, Travessa 14, 321, Sa ~ o Paulo, 05508-900, Brazil Departamento de Ecologia, USP – Universidade de Sa
2
^nica, UNESP – Univ. Estadual Paulista, Av. 24-A, 1515, Rio Claro, 13506-900, Brazil Departamento de Bota
ABSTRACT The Cerrado (Brazilian savanna) is a biodiversity hotspot with a history of fire that goes back as far as 10 million years. Fire has influenced the evolution of several aspects of the vegetation, including reproduction and life cycles. This study tested how fire by-products such as heat and smoke affect the germination of six species common to two Cerrado open physiognomies: wet grasslands and the campo sujo (grassland with scattered shrubs and dwarf trees). We subjected seeds collected in northern Brazil to heat shock and smoke treatments, both separately and combined, using different temperatures, exposure times, and smoke concentrations in aqueous solutions. High temperatures and smoke did not break seed dormancy nor stimulate germination of the Cerrado study species. However, seeds were not killed by high temperatures, indicating that they are fire-tolerant. Our findings differed from those of other fire-prone ecosystems (mostly of Mediterranean vegetation), where fire stimulates germination. Moreover, we provide important information regarding germination strategies of non-woody Cerrado plants, showing the importance of considering the tolerance of seeds to high temperatures when evaluating fire-related traits in fire-prone ecosystems. Abstract in Portuguese is available with online material. Key words: campo sujo; fire-prone ecosystems; heat shock; smoke; tropical savanna; wet grassland.
SEEDS
DIFFER IN THEIR CAPACITY TO WITHSTAND HARSH ENVIRON-
MENTAL PRESSURES.
In pyrogenic ecosystems, the response of seeds to heat and smoke from fire directly impacts plant population dynamics (Keeley et al. 2011, 2012). A number of studies, mostly in Mediterranean environments, demonstrate that heat and smoke from fire can affect seed survival and germination in flammable environments (e.g., Brown 1993, Whelan 1995, Paula & Pausas 2008, Moreira et al. 2010, Keeley et al. 2012). While smoke can trigger germination in permeable seeds, exposure to high temperatures can induce maturation in water-permeable seeds or end dormancy in water-impermeable ones by breaking the seed coat layer (Baskin & Baskin 2000, 2001). Vegetation gaps created by fire may increase post-fire germination by exposing seeds to diurnal temperature fluctuations and breaking physical dormancy (Moreno-Casasola et al. 1994, Santana et al. 2013). Thus, the germination response to fire can distinguish obligate pyrogenic dormant species (dependent on fire to germinate) from facultative pyrogenic dormant ones (gap dependent) (Ooi et al. 2014). Most studies of seeds from fire-prone ecosystems report fire-related cues to germination such as dormancy breaking and stimulation by smoke (Merrit et al. 2007, Thompson & Ooi 2010), without evaluating the fire-tolerance of seeds as a standalone trait. However, species show different seed tolerances to high temperatures and exposure times (Gashaw & Michelsen 2002), which are related to two regeneration strategies: seeding or Received 16 September 2014; revision accepted 3 July 2015. 3
Corresponding author; e-mail: afi
[email protected]
ª 2016 The Association for Tropical Biology and Conservation
resprouting (Paula & Pausas 2008). In frequently burned environments, the seeds of seeder species are resistant to high temperatures, or are even stimulated by fire, compared with resprouter species (Paula & Pausas 2008). Fire has been an important ecological and evolutionary factor in Cerrado (Brazilian savanna) for up to 10 million years (Simon et al. 2009). The Cerrado is a biodiversity hotspot (Myers et al. 2000) that comprises a mosaic of vegetation types from grasslands to woodlands determined by soil properties, water availability, topography, and fire (Coutinho 1982, Klink & Machado 2005). Seeds of Cerrado species may show adaptations to fire, such as resistance to high temperatures. Seeds of Heteropterys pteropetala (Malpighiaceae), a typical Cerrado shrub, can resist temperatures up to 100°C for 5 min (Schmidt et al. 2005). Syngonanthus nitens, a typical forb in wet grasslands in Cerrado, has seeds that resist up to 150°C (Fichino et al. 2012). Some other typical Cerrado trees have seeds resistant to temperatures between 80°C and 140°C (Rizzini 1976, Ribeiro & Borghetti 2014), whereas the seeds of forest species from the same families die under such temperatures (Ribeiro et al. 2013, Ribeiro & Borghetti 2014). As most studies of the Cerrado vegetation involve trees (but see Fichino et al. 2012, Le Stradic et al. 2015), the role of fire in breaking seed dormancy and stimulating germination is still unclear for herbaceous plants, and very little information is available despite the Cerrado herbaceous flora being much richer compared to the woody species (Filgueiras 2002). The effects of high temperatures and smoke from fire on germination of Cerrado seeds may have a direct link to species recruitment, plant population, and community dynamics. Accord181
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Fichino, Dombroski, Pivello, and Fidelis
ingly, the use of prescribed fires to maintain taxonomic and genetic diversity requires an understanding of fire effects on vegetation. This study aimed to evaluate the effects of temperature and smoke on the germination of six species commonly found in Cerrado physiognomies where fire frequency is high (2–5 yr). We hypothesized that the seeds of the six selected species would be affected by fire: that smoke solutions would enhance germination of seeds with permeable coats, and high temperatures would break the dormancy of species with impermeable seeds, as shown for other fire-prone ecosystems (e.g., the Mediterranean Basin, Moreira et al. 2010). We also expected seeds would be fire-resistant and able to germinate even after exposure to temperatures >100°C.
MATERIALS AND METHODS We collected seeds from two Cerrado natural reserves: the Jalap~ao State Park and the Jalap~ao Environmental Protected Area (10–12°S, 45–47°W, Tocantins, Northern Brazil). The average annual rainfall in the region is 1700 mm, of which 90 percent occurs in the rainy season (October to April), and the mean temperature is approximately 27°C (SEPLAN 2003). The main vegetation type in both areas is campo sujo (>50% of the area, Pereira Junior et al. 2014), which is an open savanna characterized by a continuous herbaceous layer with scattered shrubs and dwarf trees (up to 2 m high). Within this vegetation, there are isolated patches of wet grasslands, a physiognomy composed mostly of graminoid species and some forbs (mainly of the families Poaceae, Cyperaceae, Xyridaceae, and Eriocaulaceae). Wet grasslands are seasonally flooded and frequently burned. In Jalap~ao, humans burn (surface fires) these wet grasslands every 2 yr during the dry season (mostly in September, when the accumulation of dead biomass is high, Fidelis et al. 2013) to stimulate the production of the flowering stalks of Syngonanthus nitens (Eriocaulaceae), a nontimber species used for crafts (Schmidt et al. 2007). People also set fires in both the wet grasslands and the campo sujo to stimulate grass regrowth for cattle. According to Pereira Junior et al. (2014), the areas of the campo sujo have the lowest fire return interval ( 0.05). By contrast, smoke significantly decreased germination of Hyptis velutina (1:10, P = 0.005) and Xyris hymenachne (1:1, P = 0.02).
TABLE 2. Seed coat permeability (I = impermeable; P = permeable) and germination (%, mean 1SE) of the studied species at different concentrations of SLS (1:1 and 1:10). Letters after percentages indicate significant differences within species between the treatments (P ≤ 0.05).
Species
Seed coat permeability
Control 11
SLS 1:1 2 1.2
SLS 1:10 32
Abolboda poarchon
I
Chamaecrista sp.
I
20 11.2
Hyptis crenata
P
18 3.7
Hyptis velutina
P
16 2.9 a
Vellozia glauca
P
74 6.2
70 4.7
63 2.5
Xyris hymenachne
P
96 1.9 ab
81 6.2 b
99 1 a
14.7 6.1
16 6.9
31 6.6
25 7.8
8 2.5 a
11b
184
Fichino, Dombroski, Pivello, and Fidelis
A
B
C
D
E
F
FIGURE 1. Germination (%) of seeds from Cerrado (campo sujo and wet grassland) species after exposure to temperatures of 60°C, 100°C, 150°C and 200°C and the environmental temperature (control) for 1, 3, and 5 min. (A) Vellozia glauca (Velloziaceae, campo sujo); (B) Xyris hymenachne (Xyridaceae, wet grassland); (C) Hyptis velutina (Lamiaceae, wet grassland); (D) Hyptis crenata (Lamiaceae, wet grassland/campo sujo); (E) Abolboda poarchon (Xyridaceae, wet grassland); and (F) Chamaecrista sp. (Fabaceae, wet grassland). Different letters indicate a significant effect of the treatments (P ≤ 0.05). N.S. indicates no significant differences, and the P-values refer to significant differences only among the groups.
HEAT SHOCK TREATMENT (HS).—Four species showed low germination rates (65 percent (Vellozia glauca: 67 4.9%, and Xyris hymenachne: 76.5 0.9%, Fig. 1). Contrary to our expectations, germination was not enhanced by exposure to high temperatures, but instead was
inhibited (due to the mortality of seeds) by temperatures between 100°C and 200°C independently of the exposure duration (P < 0.05, Fig. 1). In addition, no interaction was observed between exposure duration and temperature for any species (P > 0.05). Species with higher germination percentages (Vellozia glauca, Xyris hymenachne, and Hyptis crenata) showed drastic
Germination Not Triggered by Fire
185
TABLE 3. Germination percentages (%, mean 1SE) of the studied species after being soaked in SLS (1:1) and exposed to different temperatures (60°C, 100°C, 150°C, and 200°C) for 3 min. The control seeds were soaked in distilled water and not exposed to high temperatures. Letters after rates indicate significant differences within species between the treatments (P ≤ 0.05). Species Abolboda poarchon Chamaecrista sp. Hyptis crenata
Control 5.3 2.5 22 4.9 a 33.4 6 a
SLS + 60°C
SLS + 100°C
6.7 3
2.7 1.6
24 6.8 a 16 4.5 ab
12 8 ab 18.7 4.9 ab
SLS + 150°C
SLS + 200°C
00
00
00b 10.7 4.5 b
Hyptis velutina
9.4 3.4
18.7 7.4
18.7 6.1
6.7 2.1
Vellozia glauca
92 7.4 a
74.7 6.5 a
82.7 17.2 a
6.7 5.2 b
decreases when exposed to temperatures ≥150°C (Fig. 1A, B, and D; P ≤ 0.05). Germination of species with low germination percentages decreased upon exposure to high temperatures for only 1 min (Hyptis velutina and Alboboda poarchon, Fig. 1C, E, P ≤ 0.05). Chamaecrista sp. also showed low germination (control = 13.3 6.3) and seeds exhibited lower germination when exposed to 100°C for 3 and 5 min (P = 0.02 and P = 0.03, respectively, Fig. 1F). However, this was the only species that showed a tendency of increasing germination when exposed to 60°C for 3 and 5 min. HEAT SHOCK + SMOKE-LIQUID SOLUTION (HS + SLS) TREATMENT.— In this treatment, the seeds followed the same trend as in HS, i.e., a general decrease in germination percentages with higher temperatures (Table 3). No significant response was observed for Abolboda poarchon (P = 0.08) or Hyptis velutina (P = 0.06), similar to the results found for HS. All other species showed very low germination at 200°C, and some species (A. poarchon, Chamaecrista sp., and Hyptis crenata) did not germinate at all.
DISCUSSION The seeds of species from fire-prone ecosystems exhibit different strategies during and after a fire: either resisting high temperatures with no changes in germination, or being stimulated to germinate (Paula & Pausas 2008). Most studies with Mediterranean species found higher germination percentages after the seeds were exposed to high temperatures or to smoke (see Moreira et al. 2010). However, we did not find similar germination responses for our study species: seeds were neither stimulated nor was their dormancy broken, but they were resistant to the exposure to high temperatures. The two species with impermeable seed coats (Abolboda poarchon and Chamaecrista sp.) showed very low germination percentages and did not have their dormancy broken by high temperatures (although such a tendency was observed for Chamaecrista sp.). Le Stradic et al. (2015) recently reported that the dominant herbaceous species of the campos rupestres (a grassland in the highlands of the Cerrado region) are fire-resistant, but found no evidence that germination is triggered by fire, although post-fire-fruiting species had relatively faster and more synchronous germination, indicating an advantage for these species in post-fire environments.
00b 00c 1.3 1.3 14.7 14 b
Tolerance to high temperatures provides persistence at the population level in flammable ecosystems: seeds that are not killed during fires find favorable conditions for germination in post-fire environments (Paula & Pausas 2008). Fires in the Cerrado are usually fast, with temperatures just below the soil surface remaining
