CO2 and fire influence tropical ecosystem stability in response to climate change

7084

Interactions between climate, fire and CO2 are believed to play a crucial role in controlling the distributions of tropical woodlands and savannas, but our understanding of these processes is limited by the paucity of data from undisturbed tropical ecosystems. Here we use a 28,000-year integrated record of vegetation, climate and fire from West Africa to examine the role of these interactions on tropical ecosystem stability. We find that increased aridity between 28–15 kyr B.P. led to the widespread expansion of tropical grasslands, but that frequent fires and low CO2 played a crucial role in stabilizing these ecosystems, even as humidity changed. This resulted in an unstable ecosystem state, which transitioned abruptly from grassland to woodlands as gradual changes in CO2 and fire shifted the balance in favor of woody plants. Since then, high atmospheric CO2 has stabilized tropical forests by promoting woody plant growth, despite increased aridity. Our results indicate that the interactions between climate, CO2 and fire can make tropical ecosystems more resilient to change, but that these systems are dynamically unstable and potentially susceptible to abrupt shifts between woodland and grassland dominated states in the future.

Savanna-forest complexes occupy nearly 20% of the Earth’s land surface1, are responsible for 30% of the Earth’s terrestrial primary production and play an important role in global carbon budgets2. Anthropogenic climate change is anticipated to have a significant influence on the ecology and distribution of tropical ecosystems, though the magnitude, rate and direction of these changes are uncertain3. These uncertainties reflect the competing influences of moisture availability, CO2 and fire on tropical vegetation4,5,6. For example, although the dominant factor controlling the potential amount of woody cover in savanna ecosystems is precipitation, actual woody cover is controlled by landscape disturbance, much of which is attributable to fire7,8. The establishment of woody plants in fire-prone tropical grasslands depends on both the frequency of fires and growth rates by affecting whether plants can achieve sufficient stem diameters and heights to survive subsequent fires9,10. In ecosystems with frequent fires or slow growth rates, woody plants may be unable to escape this “fire trap” despite increases in moisture availability. Changes in CO2 may alter these relationships by changing the carbon available for woody plant growth9,10, and increased CO2 has been shown to increase growth rates, leading to increased survivability in the presence of fire9,11,12.

To better understand the stability of tropical forest-savanna systems, we use the sediment record from Lake Bosumtwi, Ghana, which is located in the lowland tropical forest, several hundred kilometers south of the modern-day savanna-forest boundary (Fig. 1). We reconstruct changes in vegetation and hydrology using the carbon and hydrogen isotope composition of sedimentary leaf wax n-alkanes (δ13Cwax, δDwax). Changes in δ13C are interpreted as reflecting changes in the relative proportions of plants using the C3 and C4 photosynthetic pathways13. C3 vegetation includes most woody plants and winter season grasses with average δ13C values that are as low as −36‰, whereas most summer or dry season C4 grasses have δ13C values of around −20‰14. We simultaneously reconstruct changes in precipitation using hydrogen isotope analysis of the same compounds (δDwax)15, which allows us to assess the relative phasing of vegetation and precipitation changes independent of any potential complications associated with organic matter transport pathways or residence time.

Figure 1Full size image
Modeled variations in vegetation cover computed as proportions of C3 and C4 plants replotted from41. White areas indicate deserts. Circle indicates the location of Lake Bosumtwi, Ghana (6°30′N, 1°25′W). Map produced using ESRI ArcGIS software [v.10.3.1], (http://www.esri.com/software/arcgis).

Changes in fire frequency are estimated from layer counts of distinct charcoal laminae within the annual sediment laminations (Fig. 2). Because the charcoal occurs as layers and is composed mostly of relatively intact fragments, we interpret the charcoal layers as reflecting the seasonal transport of charcoal to the lake from dry season fires with little or no time lag. We then use the frequency of charcoal layers as a proxy for annual fire frequency. Reconstructions of fire frequency are supported by fire reconstructions from concentrations of levoglucosan, a byproduct of cellulose combustion, and sediment particulate charcoal counts in pollen slides. Previous studies have shown that particulate charcoal16 and levoglucosan17 can provide reliable indicators of paleofire in some sedimentary archives and Lake Bosumtwi is an ideal location for preservation of the fire marker levoglucosan because of its permanent bottom water anoxia and well-preserved organic matter18. While all three approaches provide proxies of changes in fire regime, processes such as transport and deposition, fire intensity/temperature and fuel source will affect them differently, leading to differences in fire reconstructions19,20,21,22,23 (Fig. 3). However, the most significant changes are consistent between the fire proxy indicators, indicating that they do preserve consistent large scale variations in the fire regime (SOM).

Figure 2: Evidence for changes in fire frequency.

Figure 2

Photomicrographs showing changes in the frequency of charcoal laminations in transmitted light sediment thin section from (A) the late Holocene (~1500 yr BP) when discrete bands of charcoal are absent, (B) the deglacial transition (~14,600 yr BP) when charcoal frequency has started to decline, (C) the glacial (~18,200 yr BP) when charcoal bands occur almost annually. Varves are evident in the millimeter to sub-millimeter scale couplets of light and dark laminae. The charcoal appears as distinct black layers in the boundaries of some of the annual laminae.

Full size image

Figure 3

Figure 3

(A) Temporal variations in the climate-fire-CO2-vegetation system of tropical West Africa over the last 28,000 years BP reconstructed from Lake Bosumtwi. Atmospheric CO2 from the EPICA (triangles)42 and Taylor Dome ice cores43 (squares). Computed changes in Northern Hemisphere summer (JJA) insolation at 6.5°N44 (grey line). Reconstructed precipitation changes from the δD values of C31 n-alkanes (blue circles) from Lake Bosumtwi15. Reconstructed changes in fire from a 20-year moving average of the frequency of charcoal layers in thin sections (brown), concentrations of the cellulose combustion byproduct levoglucosan (ng/cm2/yr) orange circles) and particulate charcoal influx (particles/cm2/yr; pink diamonds). Relative proportion of C3 and C4 plants from the δ13C values of C31 n-alkanes. (B) Expanded view of the transition from dry, frequently burned, grassland dominated ecosystems to more humid, low fire and CO2 dominated forested ecosystems during the last deglaciation. The blue dashed line indicates the onset of humid conditions, the green dashed line indicates the midpoint of the abrupt deglacial vegetation shift.

Full size image

The Lake Bosumtwi record shows that the climate, fire and ecological regimes of tropical West Africa changed significantly over the past 28,000 years. During the early part of the record (Fig. 3A; 15,000–28,000 yr BP), δDwax values were positive, indicating more arid conditions, fire was more frequent and δ13Cwax values were higher (−17.3 to −20.6‰) indicating that the landscape was dominated by drought-tolerant C4 summer grasses with only minor contributions from C3 woody plants that burned almost annually. In comparison with the rest of the record, δ13Cwax values show little variability, despite significant variations in δDwax and fire at this time. After ca. 15,100 yr BP (Fig. 3B, blue dashed line), more depleted δDwax values indicate a gradual return to more humid conditions. These are accompanied by a decline in the frequency of fires, which disappear almost entirely for much of the most humid portion of the Holocene (i.e., 10,000–3,200 yr BP). However, in contrast to the gradual nature of these changes in precipitation and fire, the δ13Cwax record suggests that the vegetation response was abrupt, with a ~25% change in the proportion of C3 woody plants in <150 years. The rapid expansion of woody plants also occurs ca. 300 years after the onset of wetter conditions (at 14,800 yr BP), at the time when fire frequency had declined from nearly annual to one fire every five years (Fig. 3B, green dashed line). Over much of the remainder of the record, the landscape around Lake Bosumtwi was dominated by a variable mix of C3 and C4 plants suggestive of an open woodland or forest environment similar to today, though the data also suggest a trend towards an increasing proportion of C3 plants over the past 14,500 years. Coherent variations in δ13Cwax and δDwax, during this period indicate that the dominant control over changes in the relative proportions of C3/C4 plants was precipitation, as expected in the absence of fire disturbance. After ca. 3200 yr BP, δDwax values suggest that conditions became significantly more arid, and were accompanied by an increase in fire. Nevertheless, fire frequency during the late Holocene was much lower than during the late Pleistocene (27 to 15 ka), and the magnitude of the fire response recorded in the levoglucosan and particulate charcoal records differ, suggesting a distinctly different fire regime. Unlike the earlier part of the record, severe late Holocene aridity (∆δDwax = ~17‰) was associated with only minor changes in δ13Cwax, (∆δ13Cwax = ~2–3‰) indicating that woody plant-dominated ecosystems persisted despite these environmental changes.

The changing relationships between δ13Cwax and δDwax suggest that reconstructed vegetation changes over the past 28,000 years cannot be explained solely by precipitation but instead reflect the competing influences of climate, fire and atmospheric CO2, as suggested by modeling and modern ecosystem studies24,25. The invariant nature of the early portion of the δ13Cwax record, when compared with changes in δDwax, shows that these grasslands were insensitive to temporarily increased precipitation. The fire proxies also show that at this time, significant landscape-scale fires occurred at annual to interannual timescales. Our evidence for extensive grasslands across tropical Africa at this time with a high frequency of burning is supported by both vegetation synthesis and modeling studies26,27 and lower resolution fire reconstructions from marine sediment cores, which indicate that glacial conditions were accompanied by substantial export of fire-derived elemental carbon28. We hypothesize that these fires were sufficiently frequent and widespread to prevent woody plants from becoming established, as can occur in modern savannah ecosystems7,8. Prior to ~15,000 yr BP, this effect would have been exacerbated by low CO2 levels, which would have slowed the rate of woody plant germination, growth and recovery, making it difficult for C3 plants to recover from fire disturbance even as humidity increased4.

We propose that the high fire frequency early in the record is also the proximate cause of the abrupt and delayed expansion of C3 plants at 14,800 yr BP (Fig. 4). The rapid shift in vegetation occurred when precipitation was similar to earlier (>18,000 yr BP) and later (<3000 yr BP) periods when no systematic vegetation change happened, demonstrating that vegetation was not responding to changes in precipitation alone (Fig. 3). Instead, the abrupt vegetation change reflects a threshold response to the interactions between gradually declining fire frequency, increasing CO2 and increasing precipitation. The abruptness of this transition likely reflects a combination of the equilibration of C3 plant composition with available moisture and a feedback between woody plant expansion and a further reduction in the spread of subsequent grassland fires. Support for a threshold mechanism in controlling the vegetation response is also consistent with the ~300 year lag between the initial changes in δDwax and δ13Cwax, and the transition from a system where vegetation is unresponsive to changes in precipitation (>14,800 yr BP) to one where the dominant control on vegetation is precipitation (14,800–3,000 yr BP) (Fig. 3). Although other abrupt changes in vegetation occur in the record at ca. 11,500 yr BP and 5700 yr BP, these lack the characteristics indicative of a threshold vegetation response (Supplementary Information Fig. S4). For example, neither show clear evidence for a lag in the timing of the vegetation response to climate, nor is there evidence of changing sensitivity of the vegetation to environmental conditions. Both of these are evident in the shift at 14,800 yr BP.

Figure 4: Model of the impacts of climate, fire and atmospheric CO2 on the vegetation of tropical Africa.

Figure 4

Left: cartoon of changes in the climate-ecosystem balance as a function of time. Right: schematic of changes in each parameter indicating the size and direction of change between timesteps (arrows) and the relationships between the parameters (red: negative feedback, blue: positive feedback, circle: hypothesized driver of the relationship, dashed: the relationship between these two parameters is weakened by other feedback relationships.

Full size image

Following the initial expansion of C3 plants and for much of the remaining record, the frequency and intensity of fire remained low, CO2 was high and increasing, and vegetation responded on centennial to millennial timescales to changes in precipitation, with greater proportions of C3 plants accompanying wetter conditions (Fig. 3). However, this interval is also characterized by an overall trend towards greater C3 plant abundance and a decrease in the sensitivity of vegetation to changes in precipitation. We hypothesize that this reflects the influence of increasing CO2, which favors the growth of C3 plants relative to C4 grasses29. These effects would also have been enhanced by biogeophysical feedbacks; well-developed forests can act to suppress the growth and colonization of grasses by reducing ground light availability, maintaining higher sub-canopy humidity and keeping temperatures lower, all of which promote the growth of C3 plants and are capable of maintaining forest stability30, even as environmental conditions change.

Interactions between climate, fire and CO2 are believed to play a crucial role in controlling the distributions of tropical woodlands and savannas, but our understanding of these processes is limited by the paucity of data from undisturbed tropical ecosystems. Here we use a 28,000-year integrated record of vegetation, climate and fire from West Africa to examine the role of these interactions on tropical ecosystem stability. We find that increased aridity between 28–15 kyr B.P. led to the widespread expansion of tropical grasslands, but that frequent fires and low CO2 played a crucial role in stabilizing these ecosystems, even as humidity changed. This resulted in an unstable ecosystem state, which transitioned abruptly from grassland to woodlands as gradual changes in CO2 and fire shifted the balance in favor of woody plants. Since then, high atmospheric CO2 has stabilized tropical forests by promoting woody plant growth, despite increased aridity. Our results indicate that the interactions between climate, CO2 and fire can make tropical ecosystems more resilient to change, but that these systems are dynamically unstable and potentially susceptible to abrupt shifts between woodland and grassland dominated states in the future.

Savanna-forest complexes occupy nearly 20% of the Earth’s land surface1, are responsible for 30% of the Earth’s terrestrial primary production and play an important role in global carbon budgets2. Anthropogenic climate change is anticipated to have a significant influence on the ecology and distribution of tropical ecosystems, though the magnitude, rate and direction of these changes are uncertain3. These uncertainties reflect the competing influences of moisture availability, CO2 and fire on tropical vegetation4,5,6. For example, although the dominant factor controlling the potential amount of woody cover in savanna ecosystems is precipitation, actual woody cover is controlled by landscape disturbance, much of which is attributable to fire7,8. The establishment of woody plants in fire-prone tropical grasslands depends on both the frequency of fires and growth rates by affecting whether plants can achieve sufficient stem diameters and heights to survive subsequent fires9,10. In ecosystems with frequent fires or slow growth rates, woody plants may be unable to escape this “fire trap” despite increases in moisture availability. Changes in CO2 may alter these relationships by changing the carbon available for woody plant growth9,10, and increased CO2 has been shown to increase growth rates, leading to increased survivability in the presence of fire9,11,12.

To better understand the stability of tropical forest-savanna systems, we use the sediment record from Lake Bosumtwi, Ghana, which is located in the lowland tropical forest, several hundred kilometers south of the modern-day savanna-forest boundary (Fig. 1). We reconstruct changes in vegetation and hydrology using the carbon and hydrogen isotope composition of sedimentary leaf wax n-alkanes (δ13Cwax, δDwax). Changes in δ13C are interpreted as reflecting changes in the relative proportions of plants using the C3 and C4 photosynthetic pathways13. C3 vegetation includes most woody plants and winter season grasses with average δ13C values that are as low as −36‰, whereas most summer or dry season C4 grasses have δ13C values of around −20‰14. We simultaneously reconstruct changes in precipitation using hydrogen isotope analysis of the same compounds (δDwax)15, which allows us to assess the relative phasing of vegetation and precipitation changes independent of any potential complications associated with organic matter transport pathways or residence time.

Figure 1Full size image
Modeled variations in vegetation cover computed as proportions of C3 and C4 plants replotted from41. White areas indicate deserts. Circle indicates the location of Lake Bosumtwi, Ghana (6°30′N, 1°25′W). Map produced using ESRI ArcGIS software [v.10.3.1], (http://www.esri.com/software/arcgis).

Changes in fire frequency are estimated from layer counts of distinct charcoal laminae within the annual sediment laminations (Fig. 2). Because the charcoal occurs as layers and is composed mostly of relatively intact fragments, we interpret the charcoal layers as reflecting the seasonal transport of charcoal to the lake from dry season fires with little or no time lag. We then use the frequency of charcoal layers as a proxy for annual fire frequency. Reconstructions of fire frequency are supported by fire reconstructions from concentrations of levoglucosan, a byproduct of cellulose combustion, and sediment particulate charcoal counts in pollen slides. Previous studies have shown that particulate charcoal16 and levoglucosan17 can provide reliable indicators of paleofire in some sedimentary archives and Lake Bosumtwi is an ideal location for preservation of the fire marker levoglucosan because of its permanent bottom water anoxia and well-preserved organic matter18. While all three approaches provide proxies of changes in fire regime, processes such as transport and deposition, fire intensity/temperature and fuel source will affect them differently, leading to differences in fire reconstructions19,20,21,22,23 (Fig. 3). However, the most significant changes are consistent between the fire proxy indicators, indicating that they do preserve consistent large scale variations in the fire regime (SOM).

Figure 2: Evidence for changes in fire frequency.

Figure 2

Photomicrographs showing changes in the frequency of charcoal laminations in transmitted light sediment thin section from (A) the late Holocene (~1500 yr BP) when discrete bands of charcoal are absent, (B) the deglacial transition (~14,600 yr BP) when charcoal frequency has started to decline, (C) the glacial (~18,200 yr BP) when charcoal bands occur almost annually. Varves are evident in the millimeter to sub-millimeter scale couplets of light and dark laminae. The charcoal appears as distinct black layers in the boundaries of some of the annual laminae.

Full size image

Figure 3

Figure 3

(A) Temporal variations in the climate-fire-CO2-vegetation system of tropical West Africa over the last 28,000 years BP reconstructed from Lake Bosumtwi. Atmospheric CO2 from the EPICA (triangles)42 and Taylor Dome ice cores43 (squares). Computed changes in Northern Hemisphere summer (JJA) insolation at 6.5°N44 (grey line). Reconstructed precipitation changes from the δD values of C31 n-alkanes (blue circles) from Lake Bosumtwi15. Reconstructed changes in fire from a 20-year moving average of the frequency of charcoal layers in thin sections (brown), concentrations of the cellulose combustion byproduct levoglucosan (ng/cm2/yr) orange circles) and particulate charcoal influx (particles/cm2/yr; pink diamonds). Relative proportion of C3 and C4 plants from the δ13C values of C31 n-alkanes. (B) Expanded view of the transition from dry, frequently burned, grassland dominated ecosystems to more humid, low fire and CO2 dominated forested ecosystems during the last deglaciation. The blue dashed line indicates the onset of humid conditions, the green dashed line indicates the midpoint of the abrupt deglacial vegetation shift.

Full size image

The Lake Bosumtwi record shows that the climate, fire and ecological regimes of tropical West Africa changed significantly over the past 28,000 years. During the early part of the record (Fig. 3A; 15,000–28,000 yr BP), δDwax values were positive, indicating more arid conditions, fire was more frequent and δ13Cwax values were higher (−17.3 to −20.6‰) indicating that the landscape was dominated by drought-tolerant C4 summer grasses with only minor contributions from C3 woody plants that burned almost annually. In comparison with the rest of the record, δ13Cwax values show little variability, despite significant variations in δDwax and fire at this time. After ca. 15,100 yr BP (Fig. 3B, blue dashed line), more depleted δDwax values indicate a gradual return to more humid conditions. These are accompanied by a decline in the frequency of fires, which disappear almost entirely for much of the most humid portion of the Holocene (i.e., 10,000–3,200 yr BP). However, in contrast to the gradual nature of these changes in precipitation and fire, the δ13Cwax record suggests that the vegetation response was abrupt, with a ~25% change in the proportion of C3 woody plants in <150 years. The rapid expansion of woody plants also occurs ca. 300 years after the onset of wetter conditions (at 14,800 yr BP), at the time when fire frequency had declined from nearly annual to one fire every five years (Fig. 3B, green dashed line). Over much of the remainder of the record, the landscape around Lake Bosumtwi was dominated by a variable mix of C3 and C4 plants suggestive of an open woodland or forest environment similar to today, though the data also suggest a trend towards an increasing proportion of C3 plants over the past 14,500 years. Coherent variations in δ13Cwax and δDwax, during this period indicate that the dominant control over changes in the relative proportions of C3/C4 plants was precipitation, as expected in the absence of fire disturbance. After ca. 3200 yr BP, δDwax values suggest that conditions became significantly more arid, and were accompanied by an increase in fire. Nevertheless, fire frequency during the late Holocene was much lower than during the late Pleistocene (27 to 15 ka), and the magnitude of the fire response recorded in the levoglucosan and particulate charcoal records differ, suggesting a distinctly different fire regime. Unlike the earlier part of the record, severe late Holocene aridity (∆δDwax = ~17‰) was associated with only minor changes in δ13Cwax, (∆δ13Cwax = ~2–3‰) indicating that woody plant-dominated ecosystems persisted despite these environmental changes.

The changing relationships between δ13Cwax and δDwax suggest that reconstructed vegetation changes over the past 28,000 years cannot be explained solely by precipitation but instead reflect the competing influences of climate, fire and atmospheric CO2, as suggested by modeling and modern ecosystem studies24,25. The invariant nature of the early portion of the δ13Cwax record, when compared with changes in δDwax, shows that these grasslands were insensitive to temporarily increased precipitation. The fire proxies also show that at this time, significant landscape-scale fires occurred at annual to interannual timescales. Our evidence for extensive grasslands across tropical Africa at this time with a high frequency of burning is supported by both vegetation synthesis and modeling studies26,27 and lower resolution fire reconstructions from marine sediment cores, which indicate that glacial conditions were accompanied by substantial export of fire-derived elemental carbon28. We hypothesize that these fires were sufficiently frequent and widespread to prevent woody plants from becoming established, as can occur in modern savannah ecosystems7,8. Prior to ~15,000 yr BP, this effect would have been exacerbated by low CO2 levels, which would have slowed the rate of woody plant germination, growth and recovery, making it difficult for C3 plants to recover from fire disturbance even as humidity increased4.

We propose that the high fire frequency early in the record is also the proximate cause of the abrupt and delayed expansion of C3 plants at 14,800 yr BP (Fig. 4). The rapid shift in vegetation occurred when precipitation was similar to earlier (>18,000 yr BP) and later (<3000 yr BP) periods when no systematic vegetation change happened, demonstrating that vegetation was not responding to changes in precipitation alone (Fig. 3). Instead, the abrupt vegetation change reflects a threshold response to the interactions between gradually declining fire frequency, increasing CO2 and increasing precipitation. The abruptness of this transition likely reflects a combination of the equilibration of C3 plant composition with available moisture and a feedback between woody plant expansion and a further reduction in the spread of subsequent grassland fires. Support for a threshold mechanism in controlling the vegetation response is also consistent with the ~300 year lag between the initial changes in δDwax and δ13Cwax, and the transition from a system where vegetation is unresponsive to changes in precipitation (>14,800 yr BP) to one where the dominant control on vegetation is precipitation (14,800–3,000 yr BP) (Fig. 3). Although other abrupt changes in vegetation occur in the record at ca. 11,500 yr BP and 5700 yr BP, these lack the characteristics indicative of a threshold vegetation response (Supplementary Information Fig. S4). For example, neither show clear evidence for a lag in the timing of the vegetation response to climate, nor is there evidence of changing sensitivity of the vegetation to environmental conditions. Both of these are evident in the shift at 14,800 yr BP.

Figure 4: Model of the impacts of climate, fire and atmospheric CO2 on the vegetation of tropical Africa.

Figure 4

Left: cartoon of changes in the climate-ecosystem balance as a function of time. Right: schematic of changes in each parameter indicating the size and direction of change between timesteps (arrows) and the relationships between the parameters (red: negative feedback, blue: positive feedback, circle: hypothesized driver of the relationship, dashed: the relationship between these two parameters is weakened by other feedback relationships.

Full size image

Following the initial expansion of C3 plants and for much of the remaining record, the frequency and intensity of fire remained low, CO2 was high and increasing, and vegetation responded on centennial to millennial timescales to changes in precipitation, with greater proportions of C3 plants accompanying wetter conditions (Fig. 3). However, this interval is also characterized by an overall trend towards greater C3 plant abundance and a decrease in the sensitivity of vegetation to changes in precipitation. We hypothesize that this reflects the influence of increasing CO2, which favors the growth of C3 plants relative to C4 grasses29. These effects would also have been enhanced by biogeophysical feedbacks; well-developed forests can act to suppress the growth and colonization of grasses by reducing ground light availability, maintaining higher sub-canopy humidity and keeping temperatures lower, all of which promote the growth of C3 plants and are capable of maintaining forest stability30, even as environmental conditions change.