Next Article in Journal
Afforestation of Land Abandoned by Farmers Poses Threat to Forest Sustainability Due to Heterobasidion spp.
Next Article in Special Issue
Assessment of Metal Elements and Biochemical Constituents of Wild Turkey Tail (Trametes versicolor) Mushrooms Collected from the Shivalik Foothills of the Himalayas, India
Previous Article in Journal
Application of MaxEnt Model in Biomass Estimation: An Example of Spruce Forest in the Tianshan Mountains of the Central-Western Part of Xinjiang, China
Previous Article in Special Issue
Bioaccumulation and Health Risk Assessment of Nickel Uptake by Five Wild Edible Saprotrophic Mushroom Species Collected from Croatia
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 14
Issue 5
10.3390/f14050952
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Updating Ecology and Distribution of Wild Truffles in Morocco

by
Fatima Henkrar
1,*,
Chaimae Meyad
1,2,
Marwa Oikrim
1,2,
Nezha Bouhaddou
3 and
Lahsen Khabar
2,*
1
Plant Biotechnology and Physiology Laboratory, Faculty of Sciences, Mohammed V University-Rabat, Rabat 10000, Morocco
2
Botany and Valorization of Plant and Fungal Resources Laboratory, Faculty of Sciences, Mohammed V University-Rabat, Rabat 10000, Morocco
3
Physiology and Pathophysiology Laboratory, Faculty of Sciences, Mohammed V University-Rabat, Rabat 10000, Morocco
*
Authors to whom correspondence should be addressed.
Forests 2023, 14(5), 952; https://doi.org/10.3390/f14050952
Submission received: 14 March 2023 / Revised: 28 April 2023 / Accepted: 3 May 2023 / Published: 5 May 2023
(This article belongs to the Special Issue Truffle Hunting and Mushrooms Ecology in Forest Ecosystems)
Browse Figures
Review Reports Versions Notes

Abstract

:
The distribution and abundance of the various truffle species are influenced by the climate, soil, and vegetation conditions. The setting of these characteristics is necessary for the potential species’ cultivation. Here, we describe the ecological characteristics of Moroccan truffles and desert truffles and their associations with host plants. We also determine the climate and soil parameters relating to the geographic distribution and fructification of truffles and desert truffles. In contrast to truffles, which are found in sub-humid environments, desert truffles are found in semi-arid and arid regions of Morocco. The dissemination of desert truffles in the Mamora forest and oriental regions of Morocco is typically linked to the presence of Helianthemum sp., whereas the existence of truffles (Tuber spp.) in the Middle Atlas depends on the subsistence of Quercus ilex and Q. faginea. The truffles’ and desert truffles’ fructification depends mainly on the precipitation frequency. Terfezia arenaria and Tuber oligospermum, the two major desert truffles of Mamora forest, require an annual rainfall of 435 mm on average in slightly acidic soil. While the oriental and Highland desert truffles, namely Terfezia boudieri, T. claveryi, and Tirmania spp., require an annual precipitation average of 123 to 267 mm and a high CaCO3 content. Otherwise, there is Tuber aestivum, localized in humid regions with a rainfall rate of more than 650 mm, and found under calcareous soil rich in organic matter with the presence of potential host plants, such as oaks, cedars, and pines. Our findings open up the possibility of successful cultivation of truffles and desert truffles having an economic interest through understanding their ecological requirements in Morocco.

1. Introduction

Morocco benefits from a privileged geographic location between Africa and Europe, being in the northwest of the African continent [1]. This geographical position provides Morocco with remarkable bioclimatic diversity, ranging from humid in the Rif, the Middle, and High Atlas (altitudes exceeding 1500–2000 m), to arid in South Morocco, through to sub-humid and semi-arid in the plains and foothills [1].
Hence, Morocco includes a variety of truffle and desert truffle species that require different edapho-climatic and ecological conditions. The truffles in Morocco that refer to the Tuber genus are harvested in humid or sub-humid areas, while the desert truffles colonize arid, semi-arid, and desert areas. The desert truffles belonging to Terfezia, Tirmania, Picoa, and Delastria prefer arid and semi-arid regions, either in sandy or loam soils, acid or calcareous soils, and arenaceous or light soils [2,3,4,5,6]. These various species are distinct from each other by their area of harvest, size, color, and host plant. Their main natural distribution is in the Mamora forest localized in the northwest, the plains of the Highlands in the east, and the Sahara in the south and southeast of Morocco [2,3]. The desert truffles in Morocco can establish symbioses with annual or perennial plants, especially those belonging to the Cistaceae family (Helianthemum, Cistus), while truffle species associate with woody plants [2,7,8,9].
These hypogeal fungi grow only from November to April, while others grow between March and May. The volume, as well as the quality, of the harvest varies according to rainfall and weather conditions [2,4]. Therefore, the truffles’ distribution and abundance depend highly on the rainy seasons, amount of precipitation, climatic conditions, humidity, and types of soil [10,11]. The environmental parameters for the species could be different or sometimes similar based on the altitude, geographical location, the period of measurement and the season [12]. The main goal of the present study is to describe the natural habitat of Moroccan truffles and desert truffles and to identify the climate and soil characteristics of the collection sites that determine their geographic distribution and fructification.

2. Materials and Methods

2.1. The Study Area

The study area covered eight sites in Morocco, located in three natural habitats for truffles and desert truffles in Morocco (Figure 1). The first region was located in the Mamora forest to the east of Rabat city, which covers about 130,000 hectares. The second region was in the eastern regions of Morocco that starts at Ain Beni-Mathar, and extends to Tendrara, Bouarfa, and Figuig. The attitude of this area varied from 1000 to 2000 m. The third region was situated in the Middle Atlas, covering Azrou, Ifrane and Immozer-Kandar. The attitude of this area ranged from 1100 to 1600 m (Table 1). The choice of the collection sites was made through the investigation of truffle collectors and the presence of the host plants.

2.2. Ecological Study of the Environment

For each sampling station, the execution of the surveys was conducted from 2014 to 2021, depending on the presence of the truffle species. The carpophore collection in the Mamora forest was established with the guidance of women collectors experienced in harvesting desert truffles in this area. Similarly, the selection of the studied area in eastern Morocco and carpophore harvest were performed with the assistance of Bedouin seasonal collectors living there, while the detection of Tuber spp. in the Middle Atlas was based on the presence of the host trees and the assistance of a trained dog. Three plots of about 100 m2 were established for plant species determination and carpophore collection at each site, regardless of rainfall and environmental variations. Rainfall data (annual averages, minimums, and maximums) and temperature data (annual averages, minimums, and maximums) were harvested from the NASA Langley Research Center POWER Project website, called POWER Data Access Viewer (https://power.larc.nasa.gov/data-access-viewer/ (accessed on 1 October 2022)) by inserting the Geographic Coordinates (Latitude/Longitude) of the selected sites as the input to relate the absolute location of each site. The harvested data were used as a basis for studying truffle ecology. Soil samples from the three major areas where truffles grow extensively were analyzed to determine the optimal soil physicochemical properties for truffle and desert truffle growth. The soil samples consisted of 10 samples taken from a depth of about 0–30 cm from an area of 100 m2. The soil samples were air-dried, homogenized, sieved (2 mm sieve-mesh), and conserved in the fridge. The soil sample analysis was performed in the laboratory of soil analysis at ARRAS, INRA Clermont-Ferrand, France. The plant species were recorded to describe the vegetation composition using visual estimation methods of Braun-Blanquet cover-abundance scales [12]. Periodic outings (6 times a year) were carried out to the sites to determine the various species including trees, shrubs, and herbaceous plants. Fungus identification was performed through macroscopic and microscopic attributes [13,14,15]. The distinction between Tuber gennadii and Tuber asa was established following Agnello and Kounas [16] description.

2.3. Statistical Analysis

A climograph (bar and line graph) of the monthly average precipitation and temperature from 1995 to 2021 was obtained using packages dplyr and ggplot2 in R Studio [17]. The principal component analysis was performed using FactoMineR and factoextra packages [18]. A one-way ANOVA was performed on the means of the soil properties to compare between the three bio-climatic truffle-growing areas [19]. The Tukey HSD test was used to accomplish the pairwise comparisons among means. The multcompLetters4() function from the multcompView package was used to indicate significant differences [20].

3. Results and Discussion

The natural habitat of truffles and desert truffles has always been the basis of truffle research. In Morocco, the wild truffles have very different ecological requirements, such as climatic conditions, host species, and levels of soil pH. These differences lead to a variations in the geographical distribution of these hypogeal fungi around the country. In this report, we studied the ecology of three naturally grown truffle areas in Morocco.

3.1. Floristic Composition

The truffle species and their potential host plants found in the collection sites of Morocco are shown in Table 2. In parallel, Figure 2 displayed the geographic distribution of the truffle and desert truffle species in those sites. In Mamora forest, the wild truffle fields were easily recognized due to the denuded aspect of the soil. Terfezia arenaria and Tuber oligospermum were the most frequently crossed during the survey in Mamora. The typical tree species of this forest were cork oak (Quercus suber), Pinus pinaster var. atlantica and Pinus mamorensis. Quercus suber was an endemic non-host tree of Mamora, as well as the newly reforested Eucalyptus camaldulensis tree. Pinus pinaster was the host plant of truffles, notably Delastria rosea and Tuber oligospermum. Pinus Pinaster var. atlantica was one of the species used for reforestation in this forest [21]. The presence of Tuber oligospermum depends highly on the existence of Pinus trees. Our results confirm the findings by Marjanović et al. [22], who proved as well that Tuber oligospermum is harvested under a non-native tree species for the area (Pinus halepensis Mill.), indicating that Pinus tree species are the principal host plants of Tuber oligospermum. Additionally, Cistus spp. represented the intermediate shrubby host plants of truffles in Mamora forest (Figure 3a), especially Cistus monspenliensis and Cistus salviifolius. Louro et al. [23] reported that the Terfezia–Cistus partnership exhibited a high percentage of mycorrhization and declared that the Cistus is a potential host plant for Terfezia species. The herbaceous stratum in Mamora forest was characterized mostly by the dominance of Tuberaria guttata and by bulbous plants (ex: Urginea maritima, Asphodelus microcarpus, and A. aestivus). Tuberaria guttata (Figure 3b) is the main host plant of Terfezia arenaria, T. leptoderma, and Tuber gennadii. In Algeria, Terfezia arenaria was identified in the Madagh forest, Stidia forest, and Kharouba forest, located in the northwest of Algeria where it is associated with the same host plant in the presence of similar conditions to the Mamora forest [24]. The most common method of harvesting in Mamora forest is by the “mark” produced by the fungi (Figure 3c) and the women depended on this criteria to detect the location of mature truffles (Figure 3d).
In the eastern highlands and southeastern Morocco, the vegetation is dominated by Alfa plants (Stipa tenacissima). This species occupies uniformly the west of the highlands, starting from Mlilla to Errachidia, where the Alfa grass finds its optimum bio-climatic conditions. In addition, Stipa tenacissima exists in the mountain hills of the region, especially in the east of Debdou, the western of Beni-Snassen Mountains, and the undulating reliefs that extend to El-Ayoun, Jerada, and the Moroccan–Algerian border. In the south, the Alfa gives way to distinctly Saharan species, such as Aristida obtusa, Fredolia woody steppe, and Haloxylon scoparium, a clear steppe more or less buried in sandy formations. Nevertheless, Stipa tenacissima is still present in some very advanced sectors between Figuig and Boudnib. The most frequent desert truffles species found in this area was Tirmania pinoyi, Terfezia boudieri, and T. claveryi, while Picoa juniperi was a very rare species found mainly in Tendrara. Those species established mycorrhization with Helianthemum spp., particularly Helianthemum lippii (Figure 3e), H. ledifolium, and H. apenninum, which confirms the results of Bermaki et al. [25]. Terfezia, Picoa and Tirmania were endemic to arid and semi-arid areas of the Mediterranean region [26], where they were associated with Helianthemum species. Morte et al. [5] added that the disposition of desert truffles depends on the presence of Helianthemum spp., since the desert truffles form mycorrhizal associations with these host plants. Therefore, the endurance of desert truffles is ensured by the presence and persistence of Helianthemum spp. in this region.
In the Middle Atlas, the natural habitat of black truffles (Tuber spp.) is divided into three main types. The sub-humid region in Immouzer-Kandar was dominated by Quercus ilex, Hyphaene thebaica, Juniperus oxycedrus, Arbutus unedo, and Cistus villosus. Meanwhile, in the humid forest of Ifrane, a mixture of Quercus ilex, Q. faginea, Q. suber, Cedrus atlantica, Daphne laureola, and Crataegus oxyacantha were identified. Plus, the Jaaba forest was highlighted by the presence of Chamaerops humilis alongside Quercus ilex. Otherwise, the Azrou region was dominated by Pinus pinaster (Figure 3f). The common Tuber species found in this region were Tuber aestivum, T. rufum, T. brumale, and T. excavatum. This finding was also reported by Stobbe et al. [27], who revealed that T. rufum developed in the same habitat as T. excavatum and T. aestivum. Tuber spp. of the Middle Atlas were detected particularly under Q. ilex (Figure 3g) and Q. faginea (Figure 3h). Garcia-Montero et al. [28] found that Tuber aestivum can establish mycorrhizal associations with various host plants, over 20 species, other than Quercus spp. [28]. Among them, the Pinus tree can be a potential host plant for Tuber aestivum production. Furthermore, Garcia-Montero et al. [28] reported that Pinus produces better carpophores of Tuber aestivum in natural conditions compared to Q. ilex and Q. faginea.

3.2. Climatic Data

The annual average of precipitation and temperature, the relative humidity and the bio-climatic classification of the eight sites are summarized in Table 3. The Mamora forest was characterized by a humid and temperate climate with hot and dry summers (Mediterranean climate). The average temperature in Mamora was about 25 °C in the warmest month and 15 °C in the coldest month (Figure 4), and the average annual precipitation is 435.73 mm. Terfezia arenaria in Mamora forest requires a maximum rainfall of 240 mm on average before March, while other Terfezia spp. require a rainfall amount of less than 200 mm for a good harvest (100 tons/year) [3]. A decrease in rainfall with a slight rise in temperature during the ripening period (March–May) is also necessary [3]. Adequate temperature values during this period are 14 to 18 °C [3]. The temperature is not the major determining factor: the fruiting of Mamora truffles depends mainly on well-distributed precipitation during the growth period (Figure 5). Bradai et al. [29] demonstrated that the abundance of Terfezia arenaria was positively related to the autumnal precipitations occurring from October to December that represent the germination season of this truffle along with the host-partner Helianthemum. They added that the abundance of this species was negatively correlated with minimal temperatures and precipitation from January to March. The precipitation frequency between October and March is essential for the Terfezia spp., as well as for the host plants, Helianthemum spp. Bradai et al. [29] affirmed that 180 mm of well-distributed precipitation from October to March increased the density of the host plant and increased their mycorrhization with desert truffles.
The oriental regions (Ain Beni-Mathar, Tendrara, Bouarfa, and Figuig) were characterized by an arid and Saharan–Mediterranean climate with an irregular rainfall rate ranging from 267 mm/year in Ain Beni-Mathar to 123 mm/year in Figuig (Table 3). The number of rainy days could be 30 to 40 per year [3]. The highest temperatures were around 37 °C and the lowest were around −4 °C. Terfezia claveryi was an abundant species in Ain Beni-Mathar, Tendrara and Bouarfa, in the presence of sufficient and regular precipitation in winter. Furthermore, Tirmania spp. were typical truffles of this region. Those sub-Saharan species could spread until Figuig and the south of Morocco. Otherwise, Terfezia boudieri was present in Ain Beni-Mathar and Bouarfa, where there was satisfactory and well-distributed precipitation during the fruiting period. Bermaki et al. [25] reported that Tirmania spp., Terfezia claveryi, and Terfezia boudieri were abundant in Figuig province. Tirmania spp. dominated Bni Guil, while Terfezia spp. occupied the Abou Lakhal region, and Picoa juniperi was identified only in Jebel Maiz. Bradai et al. [29] revealed that Tirmania nivea was the dominant species in the hyper-arid conditions of Algeria. In addition, they found that this species was highly productive, while Terfezia claveryi was more disrupted by the scarcity of the autumnal and annual precipitations. These results confirm the sensitivity of Terfezia claveryi and Terfezia boudieri to the climatic conditions and particularly to the lack of precipitation, restricting their presence in few regions compared to Tirmania spp., which could resist and disseminate in the hyper-arid areas. An optimal desert truffle production necessitates at least 100 mm of rainfall (Figure 5). Tadja [30] reported that a good production of wild truffles needs a rainfall amount ranging from 40 to 60 mm between October and November [30], followed by 26 mm of rainfall in March [31]. Nevertheless, no production will be obtained if the precipitation does not exceed 51 mm [29].
The climatic condition of the Middle Atlas (Imouzzer-Kander, Ifrane, and Azrou) according to the Köppen classification is Csb, with a humid and temperate climate and a dry summer (Mediterranean climate). The average temperature of the warmest month was 20 °C, while that of the coldest month was 5 °C (Figure 4). The average annual precipitation in this area reached 659 mm. It reached 40 mm in May and exceeded 70 mm in November, December, and January. Tuber aestivum, as one of the wild Tuber species found in this region, preferred a high rainfall rate in the winter (90 to 100 mm in December and January) and a moderate rainfall in summer (12 mm in August). Despite this, T. aestivum productivity is typically low and rises proportionally to increases in precipitation levels (Figure 5). The mean annual precipitation in several studied environments of Tuber aestivum was 825 mm, with generally more precipitation in summer (between May and August). In addition, the mean temperatures fluctuated from −0.7 °C in January to 17.4 °C in July with a yearly average of 8.25 °C [27]. Fischer et al. [32] mentioned that the Tuber spp. prefer areas that do not demonstrate severe or extreme temperatures. The temperature of the winter is particularly crucial because it influences the truffle maturation and production. Excessively low temperatures (−10 °C) for more than five days are harmful for truffle repining. Based on these outcomes, the studied sites of the Middle Atlas are suitable for the cultivation of Tuber aestivum due to the presence of an optimum climatic requirement for the species. Our findings confirm the conclusion of Khabar [4], who reported that the massive Debdou, the High Atlas and the Rif mountains of central Morocco are potentially adequate for Tuber spp. cultivation due to their humid and subhumid climates and generally calcareous soils.

3.3. Soil Analysis

The physicochemical properties of the soil in the natural habitats of wild desert truffles and Tuber spp. are summarized in Table 4. A notable variation was found between the three areas, indicating that the soil attributes and their proportions can differ from one geographical location to another. The soils of Mamora were slightly acidic (pH = 5.93) with a high proportion of sand (86%), which indicate a low water retention, with high permeability and better aeration. Nevertheless, the amounts of available nutrients and organic matter were low. This event could be explained by the low inputs of organic matter into the soil and the fast mineralization of organic components, since the availability of phosphorus in soil is low (58.77 mg kg−1). Bonifacio et al. [33] reported that the soils have low productivity when their phosphorus contents oscillate from 32 to 273 mg kg−1. Nevertheless, the phosphorus-deficient soil boosts the desert truffles’ mycorrhization in soils.
In the Ifrane soil where Tuber spp. grow, the clay and loam contents were around 32 and 45%, respectively, with a reasonable percentage of sand (22%). The pH was 7.86 (alkaline soil), while the organic matter was relatively abundant, well decomposed, and stabilized (C/N = 12). The calcium carbonate (CaCO3) content was often high. The abundance of exchangeable calcium was 20 times more than Mamora soil. This abundance was linked to the richness of the soil in carbonates. Rainwater saturated with carbon dioxide could increase the solubility of CaCO3 and convert calcium to an exchangeable form [33]. Similarly, in Bouarfa (oriental region), the pH was alkaline (pH = 8.74) and the calcium carbonate content was significant, which explains the high concentration of exchangeable CaO in the soil (Table 4). It was reported that the genus Tirmania was more extensive in soils with high CaCO3 and silt percentages than T. claveryi and P. juniperi [26], which explains the abundance of Tirmania in this region. However, due to the desert environment and the scarcity of the plant community, very little organic matter was registered, which explains the low availability of phosphorus in the soil. Principal component analysis results (Figure 6) between the physicochemical characteristics of the soil and the production of truffles explained 99.7% of the total variation (PC1: 28.3% and PC2: 71.4%). The high organic matter, Mgo, Mg, carbon percentage, and nitrogen percentage were correlated with T. aestivum, T. rufum, T. brumale, and T. excavatum production. Additionally, the CaCO3 and pH levels were correlated with T. nivea, T. pinoyi, T. boudieri, and T. claveryi production. Otherwise, there was no association between the Mamora truffles and any physicochemical element, showing that the optimal conditions for T. arenaria, T. oligospermum, and T. leptoderma are are low pH, low CaCO3, and low organic matter. The pH and carbonate abundance in the soil controls the presence of truffle species and fruit-body richness in situ. Terfezia arenaria, T. leptoderma, and Tuber oligospermum are acidophilic species [5,34]. These species grow mainly in Mamora forest, where the soil is acidic, whereas T. claveryi and T. boudieri thrive in alkaline environments such as Spain [5] and were the most abundant species in eastern regions of Morocco as well.

4. Conclusions

The environmental conditions of the Mamora forest, oriental regions, and Middle Atlas are very favorable for the presence of truffles or desert truffles. The reforestation of Mamora forest with Pinus pinaster will improve the yield of Tuber oligospermum, which does not exceed 30 tons per year since it is well appreciated by the citizens and the tourists. In oriental regions, a well-distributed precipitation promotes the production of Terfezia claveryi, T. boudieri and Tirmania spp. from 400 to 1000 tons per year, while in the Middle Atlas regions, the annual production and commercialization of Tuber aestivum are still unknown due to the difficulty of harvesting in the wild. The Middle Atlas presents positive indicators for establishing future plantations using Tuber aestivum mycorrhized seedlings. Thus, following the example of Tuber melanosporum, which is not a native species of Morocco and was not identified during the survey, it would be actually and successfully cultivated in a plantation of 2.5 ha in Debdou and Imouzzer-Kandar, localized in the Middle Atlas, with an annual production of 30 kg using mycorrhized seedlings with T. melanosporum originating from France.

Author Contributions

Conceptualization, L.K. and F.H.; methodology, L.K.; software, F.H.; validation, L.K., F.H. and N.B.; investigation, L.K., F.H. and N.B.; data curation, L.K.; writing—original draft preparation, F.H.; writing—review and editing, L.K.; visualization, C.M. and M.O.; supervision, L.K.; project administration, L.K.; review and editing, N.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

All data generated or analyzed during this study are included in this published article.

Acknowledgments

The authors thank the laboratory of soil analysis ARRAS, INRA Clermont-Ferrand, France for the technical support.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hssaisoune, M.; Bouchaou, L.; Sifeddine, A.; Bouimetarhan, I.; Chehbouni, A. Moroccan Groundwater Resources and Evolution with Global Climate Changes. Geosciences 2020, 10, 81. [Google Scholar] [CrossRef]
  2. Khabar, L. Mediterranean Basin: North Africa. In Desert Truffles: Phylogeny, Physiology, Distribution and Domestication; Kagan-Zur, V., Roth-Bejerano, N., Sitrit, Y., Morte, A., Eds.; Soil Biology; Springer: Berlin/Heidelberg, Germany, 2014; pp. 143–158. [Google Scholar]
  3. Khabar, L. Les Terfess et les Truffes du Maroc: Biodiversité et Valorisation; Éditions Universitaires Européennes: Saarbrücken, Germany, 2016; pp. 149–181. [Google Scholar]
  4. Khabar, L. Contribution to the Study of the Ecology of Tuber aestivum in Morocco: Phytosociological and Geological Aspects. Österr. Z. Für Pilzkd. 2010, 19, 261–264. [Google Scholar]
  5. Morte, A.; Zamora, M.; Gutiérrez, A.; Honrubia, M. Desert Truffle Cultivation in Semiarid Mediterranean Areas. In Mycorrhizas—Functional Processes and Ecological Impact; Azcón-Aguilar, C., Barea, J.M., Gianinazzi, S., Gianinazzi-Pearson, V., Eds.; Springer: Berlin/Heidelberg, Germany, 2009; pp. 221–233. [Google Scholar]
  6. Zambonelli, A.; Donnini, D.; Rana, G.L.; Fascetti, S.; Benucci, G.M.N.; Iotti, M.; Morte, A.; Khabar, L.; Bawadekji, A.; Piattoni, F.; et al. Hypogeous Fungi in Mediterranean Maquis, Arid and Semi-Arid Forests. Plant Biosyst. Int. J. Deal. Asp. Plant Biol. 2014, 148, 392–401. [Google Scholar] [CrossRef]
  7. Khabar, L. Etudes Pluridisciplinaires Des Truffes Du Maroc et Perspectives Pour l’amélioration de Production Des “Terfess” de La Forêt de La Mamora. Thèse de doctorat d’Etat Es-Sciences, Faculté des Sciences, Rabat, Morocco, 2002; p. 137. [Google Scholar]
  8. Fortas, Z. Diversité Des Espèces de Terfez (Truffes de Sables) Des Zones Arides Algériennes. International Conference EcoSys-09, University of Ouargla, Algeria. 2009. Available online: https://www.researchgate.net/publication/310459600_Diversite_des_especes_de_terfez_truffes_de_sables_des_zones_arides_algerienne (accessed on 14 March 2023).
  9. Henkrar, F.; Meyad, C.; Sabaa, S.; Khabar, L. Desert Truffles and Truffles in Morocco: Biodiversity of Promising Fungi to Combat Desertification. Environ. Sci. Proc. 2022, 16, 35. [Google Scholar] [CrossRef]
  10. Akyüz, M.; Kirbağ, S.; Gürhan, Y.; Bίrcan, B. Evaluation of Soil Characteristics and Environmental Parameters of Arid-Semi Arid Desert Truffles from Eastern Turkey. Hacet. J. Biol. Chem. 2017, 45, 395–402. [Google Scholar] [CrossRef]
  11. Shavit, E. The History of Desert Truffle Use. In Desert Truffles: Phylogeny, Physiology, Distribution and Domestication; Kagan-Zur, V., Roth-Bejerano, N., Sitrit, Y., Morte, A., Eds.; Soil Biology; Springer: Berlin/Heidelberg, Germany, 2014; pp. 217–241. [Google Scholar]
  12. Westhoff, V.; Van der Maarel, E. The Braun-Blanquet approach. In Classification of Plant Communities; Whittaker, R.H., Ed.; Springer: Hague, The Netherlands, 1973; pp. 617–726. [Google Scholar]
  13. Malençon Les Truffles Européennes. Rev. Mycol. 1938, 3, 1–92.
  14. Longato, S.; Bonfante, P. Molecular identification of mycorrhizal fungi by direct amplification of microsatellite regions. Mycol. Res. 1997, 101, 425–432. [Google Scholar] [CrossRef]
  15. Lanfranco, L.; Wyss, P.; Marzachí, C.; Bonfante, P. DNA Probes for Identification of the Ectomycorrhizal Fungus Tuber Magnatum Pico. FEMS Microbiol. Lett. 1993, 114, 245–251. [Google Scholar] [CrossRef]
  16. Agnello, C.; Kounas, V. Tuber Asa and T. Gennadii. A Close Morphological Study of Two Species Often Confused in The Past With A Brief Historical Bibliographic Summary. Ascomycete.org 2011, 3, 65–74. [Google Scholar]
  17. Tyner, S.; Briatte, F.; Hofmann, H. Network Visualization with Ggplot2. R J. 2017, 9, 27. [Google Scholar] [CrossRef]
  18. Le, S.; Josse, J.; Husson, F. FactoMineR: An R Package for Multivariate Analysis. J. Stat. Softw. 2008, 25, 1–18. [Google Scholar] [CrossRef]
  19. Assaad, H.I.; Zhou, L.; Carroll, R.J.; Wu, G. Rapid Publication-Ready MS-Word Tables for One-Way ANOVA. SpringerPlus 2014, 3, 474. [Google Scholar] [CrossRef] [PubMed]
  20. Graves, S.; Piepho, H.-P.; Selzer, L.; Dorai-Raj, S. MultcompView: Visualizations of Paired Comparisons, R package version 0.1-8. 2019. Available online: https://CRAN.R-project.org/package=multcompView (accessed on 12 December 2022).
  21. Zine El Abidine, A.; Bouderrah, M.; Lamhamedi, M.S.; Mounir, F.; Jean, V.H.-M.S.; Ponette, Q. Choix des essences de reboisement pour la forêt de la Maâmora (Maroc) sur la base de la tolérance des plants juvéniles à la sécheresse. Physio-Géo. Géographie Phys. Environ. 2020, 15, 133–160. [Google Scholar] [CrossRef]
  22. Marjanović, Z.S.; Grebenc, T.; Marković, M.; Glisić, A.; Milenković, M. Ecological Specificities and Molecular Diversity of Truffles (Genus Tuber) Originating from Mid-West of the Balkan Peninsula. Sydowia 2010, 62, 67–87. [Google Scholar]
  23. Louro, R.; Natário, B.; Santos-Silva, C. Morphological Characterization of the In Vitro Mycorrhizae Formed between Four Terfezia Species (Pezizaceae) with Cistus Salviifolius and Cistus Ladanifer—Towards Desert Truffles Production in Acid Soils. J. Fungi 2021, 7, 35. [Google Scholar] [CrossRef]
  24. Fortas, Z.; Dib-Bellahouel, S.; Chevalier, G. Ecology and Distribution of Desert Truffles in Algeria. Res. Sq. 2021, 1–32. [Google Scholar] [CrossRef]
  25. Bermaki, F.Z.; Khabar, L.; Ezzanega, A. Bioecology of Desert Truffles in the Province of Figuig in Eastern Morocco. Rev. Mex. Micol. 2017, 46, 29–36. Available online: http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0187-31802017000200029&lng=es (accessed on 3 April 2023). [CrossRef]
  26. Jamali, S.; Banihashemi, Z. Hosts and Distribution of Desert Truffles in Iran, Based on Morphological and Molecular Criteria. J. Agric. Sci. Technol. 2012, 14, 1379–1396. [Google Scholar]
  27. Stobbe, U.; Büntgen, U.; Sproll, L.; Tegel, W.; Egli, S.; Fink, S. Spatial Distribution and Ecological Variation of Re-Discovered German Truffle Habitats. Fungal Ecol. 2012, 5, 591–599. [Google Scholar] [CrossRef]
  28. Garcia-Montero, L.G.; Moreno, D.; Monleon, V.J.; Arredondo-Ruiz, F. Natural Production of Tuber Aestivum in Central Spain: Pinus Spp. versus Quercus Spp. Brûlés. For. Syst. 2014, 23, 394–399. [Google Scholar] [CrossRef]
  29. Bradai, L.; Bissati, S.; Chenchouni, H.; Amrani, K. Effects of Climate on the Productivity of Desert Truffles beneath Hyper-Arid Conditions. Int. J. Biometeorol. 2015, 59, 907–915. [Google Scholar] [CrossRef] [PubMed]
  30. Tadja, A. Etude Écologique de Deux Espècesde Terfezia Du Sud-Ouest Algérien. Essai de Leur Mycorhization Sur Trois Espèces Céréalières. Thèse Magister, Ecole Nationale Supérieure Agronomique Hassen Badi, El Harrach Alger, Algeria, 1996. Available online: http://catalogue.ensa.dz/cgi-bin/koha/opac-detail.pl?biblionumber=2284/ (accessed on 29 January 2023).
  31. Aïbeche, C. Caractéristiques Écologiques et Mycologiques d’une Espèce de Terfez de Littoral Ouest Algérie, Essai de Mycorhization Controlée Avec Sa Plante-Hote Naturelle Helianthemum Guttatum. Faculty of Sciences, Oran university, Oran, Algeria. 2008. Available online: https://dspace.univ-oran1.dz/items/357229d0-1044-4f7b-99ac-04511155e075 (accessed on 14 March 2023).
  32. Fischer, C.; Oliach, D.; Lledos, J.A.B.; Colinas, C. Best Practices for Cultivation of Truffles.; Forest Sciences Centre of Catalonia, Solsona, Spain; Yaşama Dair Vakıf: Antalaya, Turkey, 2017; p. 68. [Google Scholar]
  33. Bonifacio, E.; Scalenghe, R.; Barberis, E.; Zanini, E. Phosphorus Status in Some Natural Desert Truffle Stands. Commun. Soil Sci. Plant Anal. 1998, 29, 87–96. [Google Scholar] [CrossRef]
  34. Alvarado, P.; Moreno, G.; Manjón, J.L. Comparison between Tuber Gennadii and T. Oligospermum Lineages Reveals the Existence of the New Species T. Cistophilum (Tuberaceae, Pezizales). Mycologia 2012, 104, 894–910. [Google Scholar] [CrossRef] [PubMed]
Forests 14 00952 g001 550
Figure 1. The location of eight potential sites where the natural truffles and desert truffles grow in Morocco.
Figure 1. The location of eight potential sites where the natural truffles and desert truffles grow in Morocco.
Forests 14 00952 g001
Forests 14 00952 g002 550
Figure 2. Geographic distribution of truffle and desert truffle species in studied sites in Morocco.
Figure 2. Geographic distribution of truffle and desert truffle species in studied sites in Morocco.
Forests 14 00952 g002
Forests 14 00952 g003 550
Figure 3. Host plant of truffles in Morocco. (a) Cistus salvifolius flowers in Mamora forest; (b) Tuberaria guttata in Mamora forest; (c) soil fissures indicate the presence of truffles under the host plant; (d) women look for truffles in Mamora forest; (e) Helianthemum lippii in the desert of Bouarfa; (f) Pinus pinaster tree in Azrou; (g) Quercus ilex in Jaaba forest of Ifrane; (h) Quercus faginea in Jaaba forest of Ifrane.
Figure 3. Host plant of truffles in Morocco. (a) Cistus salvifolius flowers in Mamora forest; (b) Tuberaria guttata in Mamora forest; (c) soil fissures indicate the presence of truffles under the host plant; (d) women look for truffles in Mamora forest; (e) Helianthemum lippii in the desert of Bouarfa; (f) Pinus pinaster tree in Azrou; (g) Quercus ilex in Jaaba forest of Ifrane; (h) Quercus faginea in Jaaba forest of Ifrane.
Forests 14 00952 g003
Forests 14 00952 g004 550
Figure 4. The average monthly temperature and precipitation of the studied sited in Morocco from 1995 to 2021.
Figure 4. The average monthly temperature and precipitation of the studied sited in Morocco from 1995 to 2021.
Forests 14 00952 g004
Forests 14 00952 g005 550
Figure 5. Graphs from 2014 to 2021 illustrating the variation in desert truffle and truffle yields (kg/100 m2) in relation to the variance in precipitation (mm).
Figure 5. Graphs from 2014 to 2021 illustrating the variation in desert truffle and truffle yields (kg/100 m2) in relation to the variance in precipitation (mm).
Forests 14 00952 g005
Forests 14 00952 g006 550
Figure 6. Principal component analysis (PCA) linking Moroccan truffle production to the physico-chemical characteristics of the soil. pH: pH, Clay: Clay %, Loam: Loam %, Sand: Sand %, OM: Organic matter %, C: Carbon %, N: Nitrogen %, C.N: C/N, CaCo3: CaCO3 (g−1 kg−1), P2O5: P2O5 availability (mg kg−1), CaO: CaO (mg kg−1), MgO: MgO (mg kg−1), K2O: K2O (mg kg−1), Ca: Exchangeable Ca (mg kg−1), Mg: Exchangeable Mg (mg kg−1), K: Exchangeable K (mg kg−1).
Figure 6. Principal component analysis (PCA) linking Moroccan truffle production to the physico-chemical characteristics of the soil. pH: pH, Clay: Clay %, Loam: Loam %, Sand: Sand %, OM: Organic matter %, C: Carbon %, N: Nitrogen %, C.N: C/N, CaCo3: CaCO3 (g−1 kg−1), P2O5: P2O5 availability (mg kg−1), CaO: CaO (mg kg−1), MgO: MgO (mg kg−1), K2O: K2O (mg kg−1), Ca: Exchangeable Ca (mg kg−1), Mg: Exchangeable Mg (mg kg−1), K: Exchangeable K (mg kg−1).
Forests 14 00952 g006
Table
Table 1. Altitude, GPS details, and Köppen–Geiger climate classification of the three wild truffle areas of Morocco.
Table 1. Altitude, GPS details, and Köppen–Geiger climate classification of the three wild truffle areas of Morocco.
RegionSiteAltitude (m)GPS LocalizationClimate Classification of
Köppen–Geiger
RabatMamora Forest28034°15′52″ N, 6°39′27″ WCsa (Temperate)
Eastern MoroccoAin Beni-Mathar92134°0′30.38″ N, 2°1′55.98″ WBSk (Arid—Steppe)
Tendrara145133°2′60″ N, 2°0′0″ WBSk (Arid—Steppe)
Bouarfa117432°31′51″ N, 1°57′47″ WBWk (Arid—Desert cold)
Figuig90032°7′29.00″ N, 1°13′33.89″ WBWh (Arid—Desert hot)
Middle AtlasAzrou125033°26′29.21″ N, 5°13′29.27″ WCsb (Temperate)
Ifrane166533°30′22.49″ N, 5°9′2.80″ WCsb (Temperate)
Immouzer-Kandar145033°43′48.00″ N, 5°0′36.00″ WCsb (Temperate)
Table
Table 2. Truffle and desert truffle species identified and quantity harvested in the three investigated areas of Morocco, together with their potential host plants and maturity period.
Table 2. Truffle and desert truffle species identified and quantity harvested in the three investigated areas of Morocco, together with their potential host plants and maturity period.
SiteTruffle Species (According to Macro and Microscopic Morphology)Average Amount of Carpophores from 2014 to 2021 (kg/100 m2) Potential Host PlantMaturity Period
MamoraTerfezia arenaria9.50 ± 1.11Tuberaria guttataMarch to May
Terfezia leptoderma1.63 ± 0.37Pinus pinaster var. atlantica
Tuberaria guttata		3rd week of February until May
Delasria rosea1.25 ± 0.39Pinus pinaster var. atlanticaNovember to December
Tuber gennadi0.71 ± 0.19Tuberaria guttataEnd of February to April
Tuber oligospermum1.32 ± 0.54Pinus pinaster var. atlanticaDecember until April
Eastern MoroccoTerfezia claveryi10.79 ± 2.57Helianthemum lippii
Helianthemum scoparium
Helianthemum apenninum
Helianthemum ledifolium		March to May
Terfezia boudieri10.04 ± 3.44March to May
Picoa juniperi2.97 ± 0.88End of February
Tirmania pinoyi48.17 ± 12.04mi-December until end of March
Tirmania nivea51.83 ± 9.92mi-December until end of March
Middle AtlasTuber aestivum1.00 ± 0.30Quercus ilex
Quercus faginea		April until the end of May
Tuber excavatum0.02 ± 0.01
Tuber brumale0.06 ± 0.02
Tuber rufum0.03 ± 0.01
Table
Table 3. Climatic data of the three natural habitats of truffles and desert truffles analyzed in this study.
Table 3. Climatic data of the three natural habitats of truffles and desert truffles analyzed in this study.
RegionSiteRelative Humidity (%)T Min (°C) T Max (°C)Annual Average Temperature (°C)Annual Average Precipitation (mm)
RabatMamora74.167.3337.3118.85435.73
Eastern MoroccoAin Beni-Mathar55.18−4.1640.5016.07266.89
Tendrara49.15−4.8539.1715.65160.74
Bouarfa45.50−4.4940.1316.78226.85
Figuig38.39−3.0842.7419.43123.54
Middle AtlasAzrou
Ifrane
Immouzer-Kander		59.37−5.2238.1814.38658.87
Table
Table 4. Soil characteristics from the greatest truffle growing areas (Mamora, Ifrane, and Bouarfa).
Table 4. Soil characteristics from the greatest truffle growing areas (Mamora, Ifrane, and Bouarfa).
ComponentMamoraIfraneBouarfa
pH5.933 ± 0.152 c7.866 ± 0.351 b8.740 ± 0.180 a
Clay %10.276 ± 0.116 b32.466 ± 1.234 a26.0 ± 1.732 a
Loam %3.810 ± 1.223 c45.100 ± 2.306 a15.333 ± 5.033 b
Sand %86.013 ± 1.062 a22.433 ± 1.365 c58.667 ± 3.512 b
Organic matter %1.110 ± 0.223 b8.303 ± 4.481 a0.943 ± 0.159 b
Carbon %0.643 ± 0.132 b4.603 ± 2.689 a0.686 ± 0.127 b
Nitrogen %0.082 ± 0.027 b0.382 ± 0.225 a0.0717 ± 0.017 b
C/N8.080 ± 1.355 b12.067 ± 0.208 a9.653 ± 0.498 b
CaCO3 g kg−10.109 ± 0.003 c380.0 ± 14.731 b1044.1 ± 55.761 a
P2O5 availability mg kg−158.766 ± 10.813 a80.333 ± 1.527 a15.587 ± 4.783 b
CaO mg kg−1569.0 ± 12.124 c12,377.0 ± 1011.660 a10,700.0 ± 317.350 b
MgO mg kg−175.313 ± 32.796 c1480.0 ± 16.643 a302.056 ± 60.776 b
K2O mg kg−126.586 ± 2.707 b578.333 ± 11.504 a505.853 ± 132.010 a
Exchangeable Ca mg kg−1317.280 ± 62.548 c8760.0 ± 209.702 a7680.0 ± 478.434 b
Exchangeable Mg mg kg−145.370 ± 19.757 c891.0 ± 10.583 a181.837 ± 36.586 b
Exchangeable K mg kg−122.156 ± 2.257 b479.0 ± 16.522 a419.857 ± 109.567 a
Data shown as mean ± standard deviation (n = 3). Different superscript letters in the same raw data indicate a statistically significant difference between sites (p < 0.05).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Henkrar, F.; Meyad, C.; Oikrim, M.; Bouhaddou, N.; Khabar, L. Updating Ecology and Distribution of Wild Truffles in Morocco. Forests 2023, 14, 952. https://doi.org/10.3390/f14050952

AMA Style

Henkrar F, Meyad C, Oikrim M, Bouhaddou N, Khabar L. Updating Ecology and Distribution of Wild Truffles in Morocco. Forests. 2023; 14(5):952. https://doi.org/10.3390/f14050952

Chicago/Turabian Style

Henkrar, Fatima, Chaimae Meyad, Marwa Oikrim, Nezha Bouhaddou, and Lahsen Khabar. 2023. "Updating Ecology and Distribution of Wild Truffles in Morocco" Forests 14, no. 5: 952. https://doi.org/10.3390/f14050952

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop