Variability and trends of black truffle production in Spain (1970-2017): Linkages to climate, host growth, and human factors
Introduction
The highly-appreciated black truffle (Tuber melanosporum Vittad.) is an ectomycorrhizal fungus that lives in obligate symbiosis with the roots of several tree species. It is endemic to southern Europe, where it preferentially associates with Mediterranean oaks such as the evergreen Quercus ilex L or the deciduous Quercus faginea Lam. (Garcia-Barreda et al., 2012; Ricard et al., 2003). The fruiting body grows below ground for several months, with fruiting induction typically happening in late spring (Montant et al., 1983). During summer and early autumn, the fruiting body undergoes a series of sequential morphogenetic stages to develop its complex structure as its weight rapidly increases (Montant et al., 1983; Zarivi et al., 2015). At the end of this development and swelling stage, the fruiting body has practically achieved its final size. Then, during the maturation stage, typically in late autumn, the spores acquire their characteristic pigmentation and the gleba darkens (Garcia-Barreda et al., 2020; Zarivi et al., 2015). Throughout late autumn and all winter, the fruiting bodies are progressively harvested as they develop the aroma that allows dogs to locate them (the so-called ripening).
Climatic factors have a major influence on the outcome of the fruiting body formation process. The close relationship between summer rainfall and annual truffle production has for long been known to truffle harvesters and experts (Rebière, 1981; Ricard et al., 2003), with researchers confirming its importance (Büntgen et al., 2012a; Le Tacon et al., 1982, 2014). However, there is much less information and more controversy on the role of other climatic factors throughout the rest of the fruiting body lifespan (Bardet and Fresquet, 1995; Büntgen et al., 2019; Le Tacon et al., 2014; Montant and Kulifaj, 1990; Ricard et al., 2003). The physiological status of the host tree is also likely to influence annual truffle production, since the fruiting body depends on carbon allocated by the host tree to its fine roots (Le Tacon et al., 2013). Büntgen et al. (2012a) found a close relationship between tree-ring width of host trees and truffle production, pioneering the use of tree radial growth data to investigate the influence of climate on truffle production. A better knowledge of climate-growth-truffle relationships would help improve our knowledge on truffle ecology and adapt the cultivation practices to specific environmental conditions and to the different stages of the fruiting body formation.
Socio-economic and technological factors have also been claimed to affect trends in truffle production (Baragatti et al., 2019). Harvesters and experts agree that wild Spanish production of black truffle suffered a sharp decline during the 1970s and the 1980s (Reyna, 2012). Overexploitation due to high market price, and natural habitat deterioration due to forest encroachment and the increase in tree cover (linked to rural depopulation and land use change) are generally considered as major causes, although climate warming has also been claimed as an important factor (Büntgen et al., 2012a; Garcia-Barreda et al., 2018; Garcia-Barreda and Reyna, 2013). The high market price of black truffle and the decline of wild harvests were the spur for its cultivation in Spain, a key technological advance which began in 1968, although in the late 1990s only around 10% of the national production was harvested in plantations (Garcia-Barreda et al., 2018). Nowadays the share of black truffles produced in plantations is estimated to be 80-90%, with Spain accounting for 43% of the European production from 2013 to 2017 according to the records of the European Group for Truffle and Trufficulture.
The relationship of truffle fruiting with climatic conditions, host tree growth and other environmental or human factors should be contemplated in the context of the current regional climatic trends and their expected evolution based on climate change models (Vicente-Serrano et al., 2017a). Climatic trends associated with global warming have been linked to alterations in the production and phenology of epigeous fungi (Büntgen et al., 2012b; Kauserud et al., 2012). Assessing the impact of climate warming on truffle production and examining which biological mechanisms are involved is essential to foresee risks and plan for future needs of the truffle sector. A particularly intriguing challenge is to link climatic conditions and tree growth to truffle fruiting phenology. For epigeous fungi, Kauserud et al. (2012) found that the climatic trends associated with global warming were related to changes in the length and dates of the fruiting period, although the response was highly species-specific. In the case of black truffle, with a much longer fruiting season (typically spanning from November to March), no data on the first and last day of fruiting is available, although some hints exist that climatic or soil environmental conditions influence how truffle production is distributed throughout the fruiting season (Garcia-Barreda et al., 2020; Montant and Kulifaj, 1990).
The main objectives of this study are: (i) to investigate which climatic variables are important for explaining the variability in the annual black truffle production of Spain, (ii) to analyse whether climatic conditions and/or host plant growth are sufficient to explain the temporal variation in Spanish black truffle production since 1970, and (iii) to evaluate the effect of climatic conditions and host plant growth on how black truffle production is distributed throughout the fruiting season. We hypothesised that: (i) climatic conditions throughout the lifespan of the fruiting body, and not only in summer, influence black truffle production, (ii) socio-economic and technological factors need to be accounted for explaining the temporal evolution of black truffle production, and (iii) warm conditions promote earlier fruiting of black truffle. Finally, we discuss the likely effects of expected regional climate trends on Spanish black truffle production, based on trends for the 1970-2017 period and those pointed out by climate change models, as well as the implications of our results on the management of truffle plantations.
Section snippets
Statistical sources for truffle harvests
Data on the annual black truffle production in Spain from the fruiting season November 1970–March 1971 (hereafter called season 1970) to the season November 2017–March 2018 (i.e. season 2017) was obtained from the Spanish Federation of Associations of Truffle Growers (FETT) (Fig. S1, Supplementary Material). This record proved to be the most consistent among the Spanish statistical sources, being useful for climate change studies (Büntgen et al., 2012a; Garcia-Barreda et al., 2018).
Black
Annual truffle production
After controlling for the time trend (F = 9.5, P < 0.001), the following climatic variables were included as significant predictors in the GAM analysing the annual production of black truffle: July–August precipitation (F = 9.1, P < 0.001), mean maximum temperature of March–April (F = 3.1, P = 0.003), mean maximum temperature of July–August (F = 4.7, P < 0.001), mean maximum temperature of September–October (F = 1.7, P = 0.025), and mean maximum temperature of January–March (F = 3.5, P = 0.004).
Climatic conditions favouring truffle production
The GAM showed that the variability in annual black truffle production in Spain is largely related to variability in the climatic conditions. The climatic variables explaining the highest share of model deviance were those related to the development and swelling stage. July–August precipitation was the climatic variable with the closest relationship to truffle production, in agreement with Büntgen et al. (2012a) and Le Tacon et al. (2014). Wet summers were associated to high truffle harvests.
Conclusions
This study showed that annual production of black truffle in Spain in the 1970-2017 period was subject to a complex pattern of multiple factors. Its interannual variability was largely explained by climatic factors. Wet-cool summers enhanced truffle production, although nuanced by the non-linear relationships suggested by the GAM. The relationship between climatic factors and truffle records does not support the hypothesis that climatic variation explains the major time trend of black truffle
Declarations of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the collaboration agreement for the operation of CIET (funded by Diputación de Huesca, with the participation of CITA, Comarca de la Ribagorza and Ayuntamiento de Graus). R.S.N. is funded by a “Juan de la Cierva” postdoctoral grant FJCI-2017-31595.
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