We set out to disentangle the manifold and interacting drivers of fruit production of large, long-lived tropical canopy trees. We used two B. excelsa populations as models given the critical importance of this single species to ecosystem processes, Amazonian livelihoods, and tropical biodiversity conservation. Our findings uncovered that over 10 years, one site (Cachoeira) consistently generated production levels that were threefold higher than that of the other site (Filipinas). Fruit production variation at Cachoeira was also relatively constant at both individual and population levels compared to Filipinas. Yet as anticipated in the tropics (versus temperate regions) where low climate variability minimizes resource variation18, neither population exhibited masting behavior as indicated by synchrony (S).
Given that we hypothesized that fruit production would show similar patterns over time, and common driving variables, we expected weather and weather cues to play important roles in fruit production. Because our research sites are only ~ 30 km apart, we assumed that each population and individual tree experienced approximately the same weather and climatic cues. Our climate model indicated that more wet days during the narrow 3-month dry season prior to flowering resulted in increased fruit production. Furthermore, the model also indicated that when drier atmospheric conditions (represented by VAP) were present and extended beyond the dry season into the flowering period, fruit production tended to be reduced. Still, models that used the simple “year” variable to explain fruit production variation (versus multiple specific, albeit remote climate variables) had better statistical fit. This leads us to question what overall weather conditions might have caused the extremely low and highly variable production levels of 2017; in Filipinas, more than half of the trees did not produce any fruits (Fig. 1). Local Brazil nut harvesters also characterized 2017 as an exceptional nadir in production – a sentiment echoed in popular media across the Amazon basin19.
The year 2015 was a “Very Strong” El Niño year, which followed immediately on a “Weak” one (2014)20. These years relate to our 2017 production because of > 15-month fruit maturation lag times. Such El Niño events yield sunny, dry conditions in our study region. Over the 10-year study, VAP for 2017 production was the lowest ranked (26.27 hPa), and 2016 was the second lowest (25.37 hPa) (SI Table S2), signaling back-to-back years of persistent low atmospheric moisture. While increases in solar radiation can boost forest productivity21,22, persistent dry conditions and higher accompanying temperatures induce tree stress23, and ultimately higher mortality24. As a canopy emergent, B. excelsa crowns are exposed to greater radiation levels and higher evaporative demand. Hence, they are predicted to be particularly sensitive to drought due to hydraulic stress25, potentially exacerbated by increased water column tension in such exceptionally tall trees23. Still, such large trees access stored groundwater via deep roots more than previously assumed26, and fluctuations in water supply can be moderated by internal storage in stems, roots and leaves27. It is unknown, however, the extent to which two successive El Niño years may have impacted groundwater recharge and storage, and aggravated overall tree stress. There is evidence that canopy trees are resilient to normal Amazonian dry seasons due to deep roots that access water stored from wet season precipitation3,28; yet they are more vulnerable to extended tropical droughts, as demonstrated by the higher rates of large tree, drought-related mortality29. Corlett23 suggested that this tall tree vulnerability can be attributed to the physiological challenges of transporting water from drying soil through lengthy water conduits to exposed leaves. B. excelsa demonstrates drought avoidance by losing leaves during the dry period, but only for a few days in our study region30, where deciduousness is unexceptional and average rainfall falls short of ~ 2000 mm expected for evergreen tropical forests31. Finally, drought inducement experiments have demonstrated that lower rainfall levels over time negatively affect tropical tree fruit production. Throughfall exclusion over a 4-year period had a cumulative negative effect on fruit production (− 12%) of a sub-canopy tropical Rubiaceae, but differences were only significant in 1 year32.
Delayed rainy season onset also may have influenced the extremely low 2017 fruit production. In our region, the rainy season typically begins in September, yet the key 6-month rainfall (DTF; June through November) period that influenced 2017 production was the lowest in our 10-year data set. Moreover, of the entire 117-year CRU data set, the 2017 DTF period was the 16th lowest on record (SI Table S2), indicating that rainy season onset was delayed beyond norms. Since 1979, there has been a delay in dry season end dates (or rainy season onset) and an increase in dry season length for southern Amazonia33. Grogan and Schulze34 reported that delayed rainy season onset had a negative effect on tropical canopy tree growth, but they did not track fecundity. Finally, negative correlations between fruit production and minimum temperatures during both DPF and DTF (dry season prior to, and through flowering, respectively), particularly in Cachoeira, are consistent with other tropical studies that have showed clear negative effects of high nighttime temperatures on tropical tree growth22. In sum, evidence suggests that dry, and perhaps warming, conditions may have produced cascading effects that compromised 2017 fruit production at both sites (Table S2). Still, Cachoeira responded better than Filipinas not only in 2017, but across all years, as indicated by highly significant site effects across models.
Given these results, we explored the role that site differences might play in fruit production. Previous studies have detected subtle differences in demographic structures at our sites, indicating the presence of smaller B. excelsa individuals in the Filipinas population, but without a clear attribution to ecological or socioeconomic factors9. While Cachoeira has a longer history of disturbance (i.e., low-intensity timber harvest), which could influence the dominance of B. excelsa, we lack evidence that this disturbance influences production. Despite close proximity, our sites are located in different watersheds, and are characterized by slightly different forest types and soil characteristics. Specifically, Cachoeira’s significantly higher levels of P and K (Table 1) are informative, as soil P has been positively linked to higher levels of B. excelsa production11,17. Costa35 showed that B. excelsa can be productive in acidic, less fertile soils, while suggesting that Ca is a key macronutrient for this species.
Site quality has been used extensively to explain and predict productivity across diverse forest types for decades36, and inclusion of more site variables (such as depth to water table) would likely yield improved explanations for Cachoeira’s comparatively superior production. Notwithstanding, individual tree differences, regardless of site, offer further fruit production insights. As with almost all trees, B. excelsa reproductive status and fruit production levels are explained by DBH12,16,37,38,39, with the most productive trees in the 100–150 cm DBH range11. Moreover, DBH for these trees is correlated with crown size17, which was a significant and positive explanatory variable for all our production models, although less so for large trees (≥ 100 cm DBH) in Cachoeira versus Filipinas (Table 2, Models 4a & b). Large crowns of individual trees imply greater photosynthetic capacity and sturdy physical structures that support carbohydrate and nutrient demands of the large B. excelsa fruits. Large-diameter trees with big crowns produce more fruits. Furthermore, these trees are tall; all exhibit dominant or co-dominant canopy positions, suggesting fairly unlimited access to light. Notably, while basal area growth was a significant predictor of fruit production in trees < 100 cm DBH, it was not in large trees (Table 2, Models 3a-b). This finding corroborates a previous analysis which suggested that once healthy B. excelsa individuals attain sizeable girth and maturity, they allocate resources more equitably to both fruit production and basal area increment17.
Sapwood area of individual trees also was implicated in fruit production variation in our models, but varied by site and year, and seemed specific to large trees (Table 2). While sapwood area did not explain fruit production in most years, in 2017, Cachoeira trees with large sapwood areas produced significantly more fruit than those with small areas (Models 3b and 4a, Fig. 6). Year 2017 production bore witness to two successive El Niño years and an abnormally delayed rainy season. Further evidence of the positive effect of sapwood on fruit production under dry conditions came from our climate model. Model 2 revealed that higher VAP levels (drier air) limited fruit production, but this was mitigated when trees had more sapwood area, particularly in Cachoeira (Fig. 4). Sapwood mitigation of drought was also evident in Filipinas in 2013. After 2017, this was the second driest 6-month June–November (DTF) in our data, and in Filipinas, trees with large sapwood areas produced significantly more fruits than those with small. In sum, the more sapwood, the more likely any individual tree could continue producing fruits even in the face of a drier atmosphere.
Sapwood plays a key role in tree-water relations, and it is unsurprising that sapwood area was positively correlated to B. excelsa fruit production (r = 0.37), regardless of year or site. When dry conditions were sustained over abnormally long periods, however, sapwood area seemed to be a key trait that differentiated fruit production. In their study of biomass growth of tropical canopy trees, van der Sande et al.40 reported that sapwood area strongly explained aboveground biomass growth. While sapwood assures water and nutrient transport from roots, for large trees, sapwood capacity to store water may be most important. Goldstein et al.41 reported that canopy trees with larger sapwood areas maintained maximum transpiration rates for a longer fraction of the day, noting that water stored in stem tissues can reach canopy leaves more quickly than soil water, which can take days to ascend to tropical tree crowns.
In both our study sites, favorable climate and site conditions have supported viable B. excelsa populations and related fruit production over generational timeframes. Our 10-year data, however, permitted linkage of annually disparate weather conditions with individual B. excelsa tree fruit production. Individual tree level research facilitates close-up examination of the biological unit that responds directly to weather and site interactions40, illuminating more nuanced understanding of how site-level resources are internally allocated to produce a seed crop in any given year. In both sites, persistent dry conditions (two consecutive low rainfall years) coupled with delayed rainy season onset seemed to have had cumulative negative effects on 2017 fruit production. Given that B. excelsa individuals can live for centuries, isolated low fruit production years are unlikely to result in long-term population declines, but they certainly affect short-term harvester incomes. For example, the weather anomaly that seemed key to low 2017 harvests was a concerning event that reverberated throughout Amazonia. Of potentially greater concern, however, is the extent to which long-term climatic changes might modify B. excelsa mortality. Using 14 years of data, Bertwell et al.6 found no evidence that isolated years of drought threatened population stability, but undoubtedly the possibility of tree mortality increases after multiple years of low rainfall42. That fruit production was also linked to soil characteristics opens a door for potential individual tree nutrient manipulation to enhance production. Our study also showed that sapwood area was positively correlated with fruit production, and that in dry years, larger sapwood areas seemed to guard against low fruit production of the largest and presumably most productive trees. Is it possible (and even advisable) to attempt to delay heartwood formation to produce more drought resistant individuals?
On a much larger scale, the importance of maintaining economically viable B. excelsa populations on the landscape cannot be overemphasized. Contemporary significance of Brazil nut fruit production to Amazonian economies and conservation of biodiversity and sociocultural values has been highlighted by analysis of estimated Brazil nut rents across the Brazilian Amazon43, though much of these Brazil nut-rich forests remain unharvested. Detailed examination of the Amazonian state of Rondônia, for example, reveals that ~ 7.5 million ha (~ 1/3 of the state) are demarcated for sustainable use (i.e., Indigenous Territories, Extractive Reserves)15, and if fully exploited, could yield more Brazil nuts than are currently harvested in all of Amazonia. With fairly steady increases in Brazil nut prices over the last decades, Indigenous Amazonians (who occupy 27% of the Brazilian Amazon44), increasingly are breaking into Brazil nut markets. While continued monitoring is necessary to ensure sustainable harvests and Brazil nut populations, spatially explicit models that uncover associations between B. excelsa distributions and human presence in the Amazon historically, and into the future16,45, are encouraging. Furthermore, recent projections suggest that B. excelsa and its Dasyprocta sp. disperser are resilient to climate change itself, although the co-occurrence of B. excelsa and its pollinators was projected to diminish by almost 80% by Year 209046. Significant contemporary threats to Brazil nut sustainability also undoubtedly include felling of reproductively mature trees6 and conversion of Brazil nut-rich forests to other uses47,48. Disentangling the drivers of fruit production contributes to better scientific understanding of climatic, site-specific and endogenous factors that control fruit and seed production of long-lived, canopy trees. The B. excelsa case also highlights factors that sustain this important species on the conservation landscape, while providing potential pathways to increase productivity of extant trees that economically support both local families and a thriving extractive industry.
Source: Ecology - nature.com
